Abstract

We developed and applied rapid scanning laser-emission microscopy (LEM) to detect abnormal changes in cell nuclei for early diagnosis of cancer and cancer precursors. Regulation of chromatins is essential for genetic development and normal cell functions, while abnormal nuclear changes may lead to many diseases, in particular, cancer. The capability to detect abnormal changes in “apparently normal” tissues at a stage earlier than tumor development is critical for cancer prevention. Here we report using LEM to analyze colonic tissues from mice at-risk for colon cancer (induced by a high-fat diet) by detecting pre-polyp nuclear abnormality. By imaging the lasing emissions from chromatins, we discovered that, despite the absence of observable lesions, polyps, or tumors under stereoscope, high-fat mice exhibited significantly lower lasing thresholds than low-fat mice. The low lasing threshold is, in fact, very similar to that of adenomas and is caused by abnormal cell proliferation and chromatin deregulation that can potentially lead to cancer. Our findings suggest that conventional detection methods, such as colonoscopy followed by histopathology, by itself, may be insufficient to reveal hidden or early tumors under development. We envision that this innovative work will provide new insights into LEM and support existing tools for early tumor detection in clinical diagnosis, and fundamental biological and biomedical research of chromatin changes at the biomolecular level of cancer development.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref] [PubMed]

2018 (4)

R. Li, S. A. Grimm, D. Mav, H. Gu, D. Djukovic, R. Shah, B. A. Merrick, D. Raftery, and P. A. Wade, “Transcriptome and DNA methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal cancer,” Cell Reports 22(3), 624–637 (2018).
[Crossref] [PubMed]

S. D. McClintock, J. A. Colacino, D. Attili, M. K. Dame, A. Richter, A. Reddy, V. Basrur, A. H. Rizvi, D. K. Turgeon, J. Varani, and M. N. Aslam, “Calcium-induced differentiation of human colon adenomas in colonoid culture: calcium alone versus calcium with additional trace elements,” Cancer Prev. Res. 11(7), 413–428 (2018).

Y.-C. Chen, Q. Chen, X. Wu, X. Tan, J. Wang, and X. Fan, “A robust tissue laser platform for analysis of formalin-fixed paraffin-embedded biopsies,” Lab Chip 18(7), 1057–1065 (2018).
[Crossref] [PubMed]

X. Wu, Q. Chen, P. Xu, Y.-C. Chen, B. Wu, R. M. Coleman, L. Tong, and X. Fan, “Nanowire lasers as intracellular probes,” Nanoscale 10(20), 9729–9735 (2018).
[Crossref] [PubMed]

2017 (6)

Y.-C. Chen, Q. Chen, T. Zhang, W. Wang, and X. Fan, “Versatile tissue lasers based on high-Q Fabry-Pérot microcavities,” Lab Chip 17(3), 538–548 (2017).
[Crossref] [PubMed]

Y.-C. Chen, X. Tan, Q. Sun, Q. Chen, W. Wang, and X. Fan, “Laser-emission imaging of nuclear biomarkers for high-contrast cancer screening and immunodiagnosis,” Nat. Biomed. Eng. 1(9), 724–735 (2017).
[Crossref] [PubMed]

Y.-A. Wen, X. Xing, J. W. Harris, Y. Y. Zaytseva, M. I. Mitov, D. L. Napier, H. L. Weiss, B. Mark Evers, and T. Gao, “Adipocytes activate mitochondrial fatty acid oxidation and autophagy to promote tumor growth in colon cancer,” Cell Death Dis. 8(2), e2593 (2017).
[Crossref] [PubMed]

R. L. Siegel, K. D. Miller, and A. Jemal, “Colorectal cancer mortality rates in adults aged 20 to 54 years in the United States, 1970-2014,” JAMA 318(6), 572–574 (2017).
[Crossref] [PubMed]

Y. Wang, Z. Duan, Z. Qiu, P. Zhang, J. Wu, D. Zhang, and T. Xiang, “Random lasing in human tissues embedded with organic dyes for cancer diagnosis,” Sci. Rep. 7(1), 8385 (2017).
[Crossref] [PubMed]

M. Humar, A. Dobravec, X. Zhao, and S. H. Yun, “Biomaterial microlasers implantable in the cornea, skin, and blood,” Optica 4(9), 1080–1085 (2017).
[Crossref] [PubMed]

2016 (7)

Y.-C. Chen, Q. Chen, and X. Fan, “Lasing in blood,” Optica 3(8), 809–815 (2016).
[Crossref] [PubMed]

S. Cho, M. Humar, N. Martino, and S. H. Yun, “Laser Particle Stimulated Emission Microscopy,” Phys. Rev. Lett. 117(19), 193902 (2016).
[Crossref] [PubMed]

D. Lieberman, “Colorectal Cancer Screening With Colonoscopy,” JAMA Intern. Med. 176(7), 903–904 (2016).
[Crossref] [PubMed]

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

A. C. Mirabella, B. M. Foster, and T. Bartke, “Chromatin deregulation in disease,” Chromosoma 125(1), 75–93 (2016).
[Crossref] [PubMed]

C. P. Dietrich, A. Steude, L. Tropf, M. Schubert, N. M. Kronenberg, K. Ostermann, S. Höfling, and M. C. Gather, “An exciton-polariton laser based on biologically produced fluorescent protein,” Sci. Adv. 2(8), e1600666 (2016).
[Crossref] [PubMed]

E. Ignesti, F. Tommasi, L. Fini, F. Martelli, N. Azzali, and S. Cavalieri, “A new class of optical sensors: a random laser based device,” Sci. Rep. 6(1), 35225 (2016).
[Crossref] [PubMed]

2015 (3)

M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. C. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15(8), 5647–5652 (2015).
[Crossref] [PubMed]

M. Humar and S. H. Yun, “Intracellular microlasers,” Nat. Photonics 9(9), 572–576 (2015).
[Crossref] [PubMed]

D. K. Rex, P. S. Schoenfeld, J. Cohen, I. M. Pike, D. G. Adler, M. B. Fennerty, J. G. Lieb, W. G. Park, M. K. Rizk, M. S. Sawhney, N. J. Shaheen, S. Wani, and D. S. Weinberg, “Quality indicators for colonoscopy,” Gastrointest. Endosc. 81(1), 31–53 (2015).
[Crossref] [PubMed]

2014 (4)

X. Fan and S.-H. Yun, “The potential of optofluidic biolasers,” Nat. Methods 11(2), 141–147 (2014).
[Crossref] [PubMed]

L. Cherkezyan, Y. Stypula-Cyrus, H. Subramanian, C. White, M. Dela Cruz, R. K. Wali, M. J. Goldberg, L. K. Bianchi, H. K. Roy, and V. Backman, “Nanoscale changes in chromatin organization represent the initial steps of tumorigenesis: a transmission electron microscopy study,” BMC Cancer 14(1), 189 (2014).
[Crossref] [PubMed]

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14(24), 4590–4595 (2014).
[Crossref] [PubMed]

X. Wu, M. K. Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5(1), 3779 (2014).
[Crossref] [PubMed]

2012 (1)

M. N. Aslam, I. Bergin, M. Naik, T. Paruchuri, A. Hampton, M. Rehman, M. K. Dame, H. Rush, and J. Varani, “A multimineral natural product from red marine algae reduces colon polyp formation in C57BL/6 mice,” Nutr. Cancer 64(7), 1020–1028 (2012).
[Crossref] [PubMed]

2011 (1)

M. De Robertis, E. Massi, M. L. Poeta, S. Carotti, S. Morini, L. Cecchetelli, E. Signori, and V. M. Fazio, “The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies,” J. Carcinog. 10(1), 9 (2011).
[Crossref] [PubMed]

2010 (1)

M. N. Aslam, T. Paruchuri, N. Bhagavathula, and J. Varani, “A mineral-rich red algae extract inhibits polyp formation and inflammation in the gastrointestinal tract of mice on a high-fat diet,” Integr. Cancer Ther. 9(1), 93–99 (2010).
[Crossref] [PubMed]

2009 (1)

L. Ellis, P. W. Atadja, and R. W. Johnstone, “Epigenetics in cancer: targeting chromatin modifications,” Mol. Cancer Ther. 8(6), 1409–1420 (2009).
[Crossref] [PubMed]

2008 (1)

K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
[Crossref] [PubMed]

2007 (1)

D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
[Crossref] [PubMed]

2005 (1)

N. Mandir, A. J. FitzGerald, and R. A. Goodlad, “Differences in the effects of age on intestinal proliferation, crypt fission and apoptosis on the small intestine and the colon of the rat,” Int. J. Exp. Pathol. 86(2), 125–130 (2005).
[Crossref] [PubMed]

2002 (1)

S. J. Winawer and A. G. Zauber, “The advanced adenoma as the primary target of screening,” Gastrointest. Endosc. Clin. N. Am. 12(1), 1–9 (2002).
[Crossref] [PubMed]

2001 (1)

H. L. Newmark, K. Yang, M. Lipkin, L. Kopelovich, Y. Liu, K. Fan, and H. Shinozaki, “A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice,” Carcinogenesis 22(11), 1871–1875 (2001).
[Crossref] [PubMed]

1997 (1)

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
[Crossref] [PubMed]

1988 (1)

C. Lindholm, P.-Å. Hofer, and H. Jonsson, “Karyometric findings and prognosis of stage I cutaneous malignant melanomas,” Acta Oncol. 27(3), 227–233 (1988).
[Crossref] [PubMed]

1987 (1)

S. J. Stryker, B. G. Wolff, C. E. Culp, S. D. Libbe, D. M. Ilstrup, and R. L. MacCarty, “Natural history of untreated colonic polyps,” Gastroenterology 93(5), 1009–1013 (1987).
[Crossref] [PubMed]

1975 (1)

T. Muto, H. J. R. Bussey, and B. C. Morson, “The evolution of cancer of the colon and rectum,” Cancer 36(6), 2251–2270 (1975).
[Crossref] [PubMed]

1963 (1)

S. Welin, J. Youker, and J. S. Spratt, “The rates and patterns of growth of 375 tumors of the large intestine and rectum observed serially by double contrast enema study (Malmoe technique),” Am. J. Roentgenol. Radium Ther. Nucl. Med. 90, 673–687 (1963).
[PubMed]

Abu-Remaileh, M.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Adler, D. G.

D. K. Rex, P. S. Schoenfeld, J. Cohen, I. M. Pike, D. G. Adler, M. B. Fennerty, J. G. Lieb, W. G. Park, M. K. Rizk, M. S. Sawhney, N. J. Shaheen, S. Wani, and D. S. Weinberg, “Quality indicators for colonoscopy,” Gastrointest. Endosc. 81(1), 31–53 (2015).
[Crossref] [PubMed]

Akkad, A.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Alberts, D. S.

D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
[Crossref] [PubMed]

Arias, E.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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S. D. McClintock, J. A. Colacino, D. Attili, M. K. Dame, A. Richter, A. Reddy, V. Basrur, A. H. Rizvi, D. K. Turgeon, J. Varani, and M. N. Aslam, “Calcium-induced differentiation of human colon adenomas in colonoid culture: calcium alone versus calcium with additional trace elements,” Cancer Prev. Res. 11(7), 413–428 (2018).

M. N. Aslam, I. Bergin, M. Naik, T. Paruchuri, A. Hampton, M. Rehman, M. K. Dame, H. Rush, and J. Varani, “A multimineral natural product from red marine algae reduces colon polyp formation in C57BL/6 mice,” Nutr. Cancer 64(7), 1020–1028 (2012).
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M. N. Aslam, T. Paruchuri, N. Bhagavathula, and J. Varani, “A mineral-rich red algae extract inhibits polyp formation and inflammation in the gastrointestinal tract of mice on a high-fat diet,” Integr. Cancer Ther. 9(1), 93–99 (2010).
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L. Ellis, P. W. Atadja, and R. W. Johnstone, “Epigenetics in cancer: targeting chromatin modifications,” Mol. Cancer Ther. 8(6), 1409–1420 (2009).
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S. D. McClintock, J. A. Colacino, D. Attili, M. K. Dame, A. Richter, A. Reddy, V. Basrur, A. H. Rizvi, D. K. Turgeon, J. Varani, and M. N. Aslam, “Calcium-induced differentiation of human colon adenomas in colonoid culture: calcium alone versus calcium with additional trace elements,” Cancer Prev. Res. 11(7), 413–428 (2018).

Augenlicht, L.

K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
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E. Ignesti, F. Tommasi, L. Fini, F. Martelli, N. Azzali, and S. Cavalieri, “A new class of optical sensors: a random laser based device,” Sci. Rep. 6(1), 35225 (2016).
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L. Cherkezyan, Y. Stypula-Cyrus, H. Subramanian, C. White, M. Dela Cruz, R. K. Wali, M. J. Goldberg, L. K. Bianchi, H. K. Roy, and V. Backman, “Nanoscale changes in chromatin organization represent the initial steps of tumorigenesis: a transmission electron microscopy study,” BMC Cancer 14(1), 189 (2014).
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K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
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D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
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D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
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S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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Bhagavathula, N.

M. N. Aslam, T. Paruchuri, N. Bhagavathula, and J. Varani, “A mineral-rich red algae extract inhibits polyp formation and inflammation in the gastrointestinal tract of mice on a high-fat diet,” Integr. Cancer Ther. 9(1), 93–99 (2010).
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L. Cherkezyan, Y. Stypula-Cyrus, H. Subramanian, C. White, M. Dela Cruz, R. K. Wali, M. J. Goldberg, L. K. Bianchi, H. K. Roy, and V. Backman, “Nanoscale changes in chromatin organization represent the initial steps of tumorigenesis: a transmission electron microscopy study,” BMC Cancer 14(1), 189 (2014).
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S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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Y.-C. Chen, Q. Chen, X. Wu, X. Tan, J. Wang, and X. Fan, “A robust tissue laser platform for analysis of formalin-fixed paraffin-embedded biopsies,” Lab Chip 18(7), 1057–1065 (2018).
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X. Wu, Q. Chen, P. Xu, Y.-C. Chen, B. Wu, R. M. Coleman, L. Tong, and X. Fan, “Nanowire lasers as intracellular probes,” Nanoscale 10(20), 9729–9735 (2018).
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Y.-C. Chen, X. Tan, Q. Sun, Q. Chen, W. Wang, and X. Fan, “Laser-emission imaging of nuclear biomarkers for high-contrast cancer screening and immunodiagnosis,” Nat. Biomed. Eng. 1(9), 724–735 (2017).
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Y.-C. Chen, Q. Chen, T. Zhang, W. Wang, and X. Fan, “Versatile tissue lasers based on high-Q Fabry-Pérot microcavities,” Lab Chip 17(3), 538–548 (2017).
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Y.-C. Chen, Q. Chen, and X. Fan, “Lasing in blood,” Optica 3(8), 809–815 (2016).
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Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14(24), 4590–4595 (2014).
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X. Wu, M. K. Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5(1), 3779 (2014).
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X. Wu, Q. Chen, P. Xu, Y.-C. Chen, B. Wu, R. M. Coleman, L. Tong, and X. Fan, “Nanowire lasers as intracellular probes,” Nanoscale 10(20), 9729–9735 (2018).
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Y.-C. Chen, Q. Chen, X. Wu, X. Tan, J. Wang, and X. Fan, “A robust tissue laser platform for analysis of formalin-fixed paraffin-embedded biopsies,” Lab Chip 18(7), 1057–1065 (2018).
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Y.-C. Chen, X. Tan, Q. Sun, Q. Chen, W. Wang, and X. Fan, “Laser-emission imaging of nuclear biomarkers for high-contrast cancer screening and immunodiagnosis,” Nat. Biomed. Eng. 1(9), 724–735 (2017).
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Y.-C. Chen, Q. Chen, T. Zhang, W. Wang, and X. Fan, “Versatile tissue lasers based on high-Q Fabry-Pérot microcavities,” Lab Chip 17(3), 538–548 (2017).
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Y.-C. Chen, Q. Chen, and X. Fan, “Lasing in blood,” Optica 3(8), 809–815 (2016).
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S. D. McClintock, J. A. Colacino, D. Attili, M. K. Dame, A. Richter, A. Reddy, V. Basrur, A. H. Rizvi, D. K. Turgeon, J. Varani, and M. N. Aslam, “Calcium-induced differentiation of human colon adenomas in colonoid culture: calcium alone versus calcium with additional trace elements,” Cancer Prev. Res. 11(7), 413–428 (2018).

Coleman, R. M.

X. Wu, Q. Chen, P. Xu, Y.-C. Chen, B. Wu, R. M. Coleman, L. Tong, and X. Fan, “Nanowire lasers as intracellular probes,” Nanoscale 10(20), 9729–9735 (2018).
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K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
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M. N. Aslam, I. Bergin, M. Naik, T. Paruchuri, A. Hampton, M. Rehman, M. K. Dame, H. Rush, and J. Varani, “A multimineral natural product from red marine algae reduces colon polyp formation in C57BL/6 mice,” Nutr. Cancer 64(7), 1020–1028 (2012).
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De Robertis, M.

M. De Robertis, E. Massi, M. L. Poeta, S. Carotti, S. Morini, L. Cecchetelli, E. Signori, and V. M. Fazio, “The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies,” J. Carcinog. 10(1), 9 (2011).
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L. Cherkezyan, Y. Stypula-Cyrus, H. Subramanian, C. White, M. Dela Cruz, R. K. Wali, M. J. Goldberg, L. K. Bianchi, H. K. Roy, and V. Backman, “Nanoscale changes in chromatin organization represent the initial steps of tumorigenesis: a transmission electron microscopy study,” BMC Cancer 14(1), 189 (2014).
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S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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Dogum, R.

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K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
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Einspahr, J. G.

D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
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L. Ellis, P. W. Atadja, and R. W. Johnstone, “Epigenetics in cancer: targeting chromatin modifications,” Mol. Cancer Ther. 8(6), 1409–1420 (2009).
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K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
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Y.-C. Chen, Q. Chen, X. Wu, X. Tan, J. Wang, and X. Fan, “A robust tissue laser platform for analysis of formalin-fixed paraffin-embedded biopsies,” Lab Chip 18(7), 1057–1065 (2018).
[Crossref] [PubMed]

X. Wu, Q. Chen, P. Xu, Y.-C. Chen, B. Wu, R. M. Coleman, L. Tong, and X. Fan, “Nanowire lasers as intracellular probes,” Nanoscale 10(20), 9729–9735 (2018).
[Crossref] [PubMed]

Y.-C. Chen, Q. Chen, T. Zhang, W. Wang, and X. Fan, “Versatile tissue lasers based on high-Q Fabry-Pérot microcavities,” Lab Chip 17(3), 538–548 (2017).
[Crossref] [PubMed]

Y.-C. Chen, X. Tan, Q. Sun, Q. Chen, W. Wang, and X. Fan, “Laser-emission imaging of nuclear biomarkers for high-contrast cancer screening and immunodiagnosis,” Nat. Biomed. Eng. 1(9), 724–735 (2017).
[Crossref] [PubMed]

Y.-C. Chen, Q. Chen, and X. Fan, “Lasing in blood,” Optica 3(8), 809–815 (2016).
[Crossref] [PubMed]

X. Wu, M. K. Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5(1), 3779 (2014).
[Crossref] [PubMed]

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14(24), 4590–4595 (2014).
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X. Fan and S.-H. Yun, “The potential of optofluidic biolasers,” Nat. Methods 11(2), 141–147 (2014).
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S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

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E. Ignesti, F. Tommasi, L. Fini, F. Martelli, N. Azzali, and S. Cavalieri, “A new class of optical sensors: a random laser based device,” Sci. Rep. 6(1), 35225 (2016).
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S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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Foster, B. M.

A. C. Mirabella, B. M. Foster, and T. Bartke, “Chromatin deregulation in disease,” Chromosoma 125(1), 75–93 (2016).
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Ganiats, T. G.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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Gao, T.

Y.-A. Wen, X. Xing, J. W. Harris, Y. Y. Zaytseva, M. I. Mitov, D. L. Napier, H. L. Weiss, B. Mark Evers, and T. Gao, “Adipocytes activate mitochondrial fatty acid oxidation and autophagy to promote tumor growth in colon cancer,” Cell Death Dis. 8(2), e2593 (2017).
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Gather, M. C.

C. P. Dietrich, A. Steude, L. Tropf, M. Schubert, N. M. Kronenberg, K. Ostermann, S. Höfling, and M. C. Gather, “An exciton-polariton laser based on biologically produced fluorescent protein,” Sci. Adv. 2(8), e1600666 (2016).
[Crossref] [PubMed]

M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. C. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15(8), 5647–5652 (2015).
[Crossref] [PubMed]

Giardiello, F. M.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
[Crossref] [PubMed]

Glick, S. N.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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Godlee, F.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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Goldberg, M. J.

L. Cherkezyan, Y. Stypula-Cyrus, H. Subramanian, C. White, M. Dela Cruz, R. K. Wali, M. J. Goldberg, L. K. Bianchi, H. K. Roy, and V. Backman, “Nanoscale changes in chromatin organization represent the initial steps of tumorigenesis: a transmission electron microscopy study,” BMC Cancer 14(1), 189 (2014).
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Goldschmid, S.

D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
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Goodlad, R. A.

N. Mandir, A. J. FitzGerald, and R. A. Goodlad, “Differences in the effects of age on intestinal proliferation, crypt fission and apoptosis on the small intestine and the colon of the rat,” Int. J. Exp. Pathol. 86(2), 125–130 (2005).
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Grimm, S. A.

R. Li, S. A. Grimm, D. Mav, H. Gu, D. Djukovic, R. Shah, B. A. Merrick, D. Raftery, and P. A. Wade, “Transcriptome and DNA methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal cancer,” Cell Reports 22(3), 624–637 (2018).
[Crossref] [PubMed]

Gu, H.

R. Li, S. A. Grimm, D. Mav, H. Gu, D. Djukovic, R. Shah, B. A. Merrick, D. Raftery, and P. A. Wade, “Transcriptome and DNA methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal cancer,” Cell Reports 22(3), 624–637 (2018).
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Guo, G.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Gupta, N.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Hamilton, P.

D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
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Hampton, A.

M. N. Aslam, I. Bergin, M. Naik, T. Paruchuri, A. Hampton, M. Rehman, M. K. Dame, H. Rush, and J. Varani, “A multimineral natural product from red marine algae reduces colon polyp formation in C57BL/6 mice,” Nutr. Cancer 64(7), 1020–1028 (2012).
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Harris, J. W.

Y.-A. Wen, X. Xing, J. W. Harris, Y. Y. Zaytseva, M. I. Mitov, D. L. Napier, H. L. Weiss, B. Mark Evers, and T. Gao, “Adipocytes activate mitochondrial fatty acid oxidation and autophagy to promote tumor growth in colon cancer,” Cell Death Dis. 8(2), e2593 (2017).
[Crossref] [PubMed]

Hess, L. M.

D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
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Hofer, P.-Å.

C. Lindholm, P.-Å. Hofer, and H. Jonsson, “Karyometric findings and prognosis of stage I cutaneous malignant melanomas,” Acta Oncol. 27(3), 227–233 (1988).
[Crossref] [PubMed]

Höfling, S.

C. P. Dietrich, A. Steude, L. Tropf, M. Schubert, N. M. Kronenberg, K. Ostermann, S. Höfling, and M. C. Gather, “An exciton-polariton laser based on biologically produced fluorescent protein,” Sci. Adv. 2(8), e1600666 (2016).
[Crossref] [PubMed]

Hong, S.-J.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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Humar, M.

M. Humar, A. Dobravec, X. Zhao, and S. H. Yun, “Biomaterial microlasers implantable in the cornea, skin, and blood,” Optica 4(9), 1080–1085 (2017).
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S. Cho, M. Humar, N. Martino, and S. H. Yun, “Laser Particle Stimulated Emission Microscopy,” Phys. Rev. Lett. 117(19), 193902 (2016).
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M. Humar and S. H. Yun, “Intracellular microlasers,” Nat. Photonics 9(9), 572–576 (2015).
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Ignesti, E.

E. Ignesti, F. Tommasi, L. Fini, F. Martelli, N. Azzali, and S. Cavalieri, “A new class of optical sensors: a random laser based device,” Sci. Rep. 6(1), 35225 (2016).
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Ilstrup, D. M.

S. J. Stryker, B. G. Wolff, C. E. Culp, S. D. Libbe, D. M. Ilstrup, and R. L. MacCarty, “Natural history of untreated colonic polyps,” Gastroenterology 93(5), 1009–1013 (1987).
[Crossref] [PubMed]

Ismail, A.

D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
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Jemal, A.

R. L. Siegel, K. D. Miller, and A. Jemal, “Colorectal cancer mortality rates in adults aged 20 to 54 years in the United States, 1970-2014,” JAMA 318(6), 572–574 (2017).
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Johnstone, R. W.

L. Ellis, P. W. Atadja, and R. W. Johnstone, “Epigenetics in cancer: targeting chromatin modifications,” Mol. Cancer Ther. 8(6), 1409–1420 (2009).
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Jonsson, H.

C. Lindholm, P.-Å. Hofer, and H. Jonsson, “Karyometric findings and prognosis of stage I cutaneous malignant melanomas,” Acta Oncol. 27(3), 227–233 (1988).
[Crossref] [PubMed]

Karl, M.

M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. C. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15(8), 5647–5652 (2015).
[Crossref] [PubMed]

Katz, Y.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Kedrin, D.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Kopelovich, L.

H. L. Newmark, K. Yang, M. Lipkin, L. Kopelovich, Y. Liu, K. Fan, and H. Shinozaki, “A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice,” Carcinogenesis 22(11), 1871–1875 (2001).
[Crossref] [PubMed]

Kronenberg, N. M.

C. P. Dietrich, A. Steude, L. Tropf, M. Schubert, N. M. Kronenberg, K. Ostermann, S. Höfling, and M. C. Gather, “An exciton-polariton laser based on biologically produced fluorescent protein,” Sci. Adv. 2(8), e1600666 (2016).
[Crossref] [PubMed]

M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. C. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15(8), 5647–5652 (2015).
[Crossref] [PubMed]

Krouse, R. S.

D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
[Crossref] [PubMed]

Kurihara, N.

K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
[Crossref] [PubMed]

Lamming, D. W.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Lance, P.

D. S. Alberts, J. G. Einspahr, R. S. Krouse, A. Prasad, J. Ranger-Moore, P. Hamilton, A. Ismail, P. Lance, S. Goldschmid, L. M. Hess, M. Yozwiak, H. G. Bartels, and P. H. Bartels, “Karyometry of the colonic mucosa,” Cancer Epidemiol. Biomarkers Prev. 16(12), 2704–2716 (2007).
[Crossref] [PubMed]

Lesser, M.

K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
[Crossref] [PubMed]

Li, R.

R. Li, S. A. Grimm, D. Mav, H. Gu, D. Djukovic, R. Shah, B. A. Merrick, D. Raftery, and P. A. Wade, “Transcriptome and DNA methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal cancer,” Cell Reports 22(3), 624–637 (2018).
[Crossref] [PubMed]

Libbe, S. D.

S. J. Stryker, B. G. Wolff, C. E. Culp, S. D. Libbe, D. M. Ilstrup, and R. L. MacCarty, “Natural history of untreated colonic polyps,” Gastroenterology 93(5), 1009–1013 (1987).
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Lieb, J. G.

D. K. Rex, P. S. Schoenfeld, J. Cohen, I. M. Pike, D. G. Adler, M. B. Fennerty, J. G. Lieb, W. G. Park, M. K. Rizk, M. S. Sawhney, N. J. Shaheen, S. Wani, and D. S. Weinberg, “Quality indicators for colonoscopy,” Gastrointest. Endosc. 81(1), 31–53 (2015).
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Lieberman, D.

D. Lieberman, “Colorectal Cancer Screening With Colonoscopy,” JAMA Intern. Med. 176(7), 903–904 (2016).
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Liehm, P.

M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. C. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15(8), 5647–5652 (2015).
[Crossref] [PubMed]

Lindholm, C.

C. Lindholm, P.-Å. Hofer, and H. Jonsson, “Karyometric findings and prognosis of stage I cutaneous malignant melanomas,” Acta Oncol. 27(3), 227–233 (1988).
[Crossref] [PubMed]

Lipkin, M.

K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
[Crossref] [PubMed]

H. L. Newmark, K. Yang, M. Lipkin, L. Kopelovich, Y. Liu, K. Fan, and H. Shinozaki, “A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice,” Carcinogenesis 22(11), 1871–1875 (2001).
[Crossref] [PubMed]

Liu, Y.

H. L. Newmark, K. Yang, M. Lipkin, L. Kopelovich, Y. Liu, K. Fan, and H. Shinozaki, “A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice,” Carcinogenesis 22(11), 1871–1875 (2001).
[Crossref] [PubMed]

Livote, E.

K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
[Crossref] [PubMed]

MacCarty, R. L.

S. J. Stryker, B. G. Wolff, C. E. Culp, S. D. Libbe, D. M. Ilstrup, and R. L. MacCarty, “Natural history of untreated colonic polyps,” Gastroenterology 93(5), 1009–1013 (1987).
[Crossref] [PubMed]

Mana, M. D.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Mandir, N.

N. Mandir, A. J. FitzGerald, and R. A. Goodlad, “Differences in the effects of age on intestinal proliferation, crypt fission and apoptosis on the small intestine and the colon of the rat,” Int. J. Exp. Pathol. 86(2), 125–130 (2005).
[Crossref] [PubMed]

Marciniak, D. A.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
[Crossref] [PubMed]

Mark Evers, B.

Y.-A. Wen, X. Xing, J. W. Harris, Y. Y. Zaytseva, M. I. Mitov, D. L. Napier, H. L. Weiss, B. Mark Evers, and T. Gao, “Adipocytes activate mitochondrial fatty acid oxidation and autophagy to promote tumor growth in colon cancer,” Cell Death Dis. 8(2), e2593 (2017).
[Crossref] [PubMed]

Martelli, F.

E. Ignesti, F. Tommasi, L. Fini, F. Martelli, N. Azzali, and S. Cavalieri, “A new class of optical sensors: a random laser based device,” Sci. Rep. 6(1), 35225 (2016).
[Crossref] [PubMed]

Martino, N.

S. Cho, M. Humar, N. Martino, and S. H. Yun, “Laser Particle Stimulated Emission Microscopy,” Phys. Rev. Lett. 117(19), 193902 (2016).
[Crossref] [PubMed]

Massi, E.

M. De Robertis, E. Massi, M. L. Poeta, S. Carotti, S. Morini, L. Cecchetelli, E. Signori, and V. M. Fazio, “The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies,” J. Carcinog. 10(1), 9 (2011).
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Mav, D.

R. Li, S. A. Grimm, D. Mav, H. Gu, D. Djukovic, R. Shah, B. A. Merrick, D. Raftery, and P. A. Wade, “Transcriptome and DNA methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal cancer,” Cell Reports 22(3), 624–637 (2018).
[Crossref] [PubMed]

Mayer, R. J.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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McClintock, S. D.

S. D. McClintock, J. A. Colacino, D. Attili, M. K. Dame, A. Richter, A. Reddy, V. Basrur, A. H. Rizvi, D. K. Turgeon, J. Varani, and M. N. Aslam, “Calcium-induced differentiation of human colon adenomas in colonoid culture: calcium alone versus calcium with additional trace elements,” Cancer Prev. Res. 11(7), 413–428 (2018).

Merrick, B. A.

R. Li, S. A. Grimm, D. Mav, H. Gu, D. Djukovic, R. Shah, B. A. Merrick, D. Raftery, and P. A. Wade, “Transcriptome and DNA methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal cancer,” Cell Reports 22(3), 624–637 (2018).
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Mihaylova, M. M.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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R. L. Siegel, K. D. Miller, and A. Jemal, “Colorectal cancer mortality rates in adults aged 20 to 54 years in the United States, 1970-2014,” JAMA 318(6), 572–574 (2017).
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Miller, L.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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Morini, S.

M. De Robertis, E. Massi, M. L. Poeta, S. Carotti, S. Morini, L. Cecchetelli, E. Signori, and V. M. Fazio, “The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies,” J. Carcinog. 10(1), 9 (2011).
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S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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M. N. Aslam, I. Bergin, M. Naik, T. Paruchuri, A. Hampton, M. Rehman, M. K. Dame, H. Rush, and J. Varani, “A multimineral natural product from red marine algae reduces colon polyp formation in C57BL/6 mice,” Nutr. Cancer 64(7), 1020–1028 (2012).
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Y.-A. Wen, X. Xing, J. W. Harris, Y. Y. Zaytseva, M. I. Mitov, D. L. Napier, H. L. Weiss, B. Mark Evers, and T. Gao, “Adipocytes activate mitochondrial fatty acid oxidation and autophagy to promote tumor growth in colon cancer,” Cell Death Dis. 8(2), e2593 (2017).
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K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
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H. L. Newmark, K. Yang, M. Lipkin, L. Kopelovich, Y. Liu, K. Fan, and H. Shinozaki, “A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice,” Carcinogenesis 22(11), 1871–1875 (2001).
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S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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X. Wu, M. K. Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5(1), 3779 (2014).
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S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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C. P. Dietrich, A. Steude, L. Tropf, M. Schubert, N. M. Kronenberg, K. Ostermann, S. Höfling, and M. C. Gather, “An exciton-polariton laser based on biologically produced fluorescent protein,” Sci. Adv. 2(8), e1600666 (2016).
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M. N. Aslam, I. Bergin, M. Naik, T. Paruchuri, A. Hampton, M. Rehman, M. K. Dame, H. Rush, and J. Varani, “A multimineral natural product from red marine algae reduces colon polyp formation in C57BL/6 mice,” Nutr. Cancer 64(7), 1020–1028 (2012).
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M. N. Aslam, T. Paruchuri, N. Bhagavathula, and J. Varani, “A mineral-rich red algae extract inhibits polyp formation and inflammation in the gastrointestinal tract of mice on a high-fat diet,” Integr. Cancer Ther. 9(1), 93–99 (2010).
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Pinello, L.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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Poeta, M. L.

M. De Robertis, E. Massi, M. L. Poeta, S. Carotti, S. Morini, L. Cecchetelli, E. Signori, and V. M. Fazio, “The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies,” J. Carcinog. 10(1), 9 (2011).
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M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. C. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15(8), 5647–5652 (2015).
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R. Li, S. A. Grimm, D. Mav, H. Gu, D. Djukovic, R. Shah, B. A. Merrick, D. Raftery, and P. A. Wade, “Transcriptome and DNA methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal cancer,” Cell Reports 22(3), 624–637 (2018).
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Reddy, K.

X. Wu, M. K. Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5(1), 3779 (2014).
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Rehman, M.

M. N. Aslam, I. Bergin, M. Naik, T. Paruchuri, A. Hampton, M. Rehman, M. K. Dame, H. Rush, and J. Varani, “A multimineral natural product from red marine algae reduces colon polyp formation in C57BL/6 mice,” Nutr. Cancer 64(7), 1020–1028 (2012).
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D. K. Rex, P. S. Schoenfeld, J. Cohen, I. M. Pike, D. G. Adler, M. B. Fennerty, J. G. Lieb, W. G. Park, M. K. Rizk, M. S. Sawhney, N. J. Shaheen, S. Wani, and D. S. Weinberg, “Quality indicators for colonoscopy,” Gastrointest. Endosc. 81(1), 31–53 (2015).
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Rigas, B.

K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
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Ritt, M.

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14(24), 4590–4595 (2014).
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D. K. Rex, P. S. Schoenfeld, J. Cohen, I. M. Pike, D. G. Adler, M. B. Fennerty, J. G. Lieb, W. G. Park, M. K. Rizk, M. S. Sawhney, N. J. Shaheen, S. Wani, and D. S. Weinberg, “Quality indicators for colonoscopy,” Gastrointest. Endosc. 81(1), 31–53 (2015).
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Roper, J.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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Rosen, L.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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Rush, H.

M. N. Aslam, I. Bergin, M. Naik, T. Paruchuri, A. Hampton, M. Rehman, M. K. Dame, H. Rush, and J. Varani, “A multimineral natural product from red marine algae reduces colon polyp formation in C57BL/6 mice,” Nutr. Cancer 64(7), 1020–1028 (2012).
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Saadatpour, A.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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Sabatini, D. M.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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Sawhney, M. S.

D. K. Rex, P. S. Schoenfeld, J. Cohen, I. M. Pike, D. G. Adler, M. B. Fennerty, J. G. Lieb, W. G. Park, M. K. Rizk, M. S. Sawhney, N. J. Shaheen, S. Wani, and D. S. Weinberg, “Quality indicators for colonoscopy,” Gastrointest. Endosc. 81(1), 31–53 (2015).
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Schoenfeld, P. S.

D. K. Rex, P. S. Schoenfeld, J. Cohen, I. M. Pike, D. G. Adler, M. B. Fennerty, J. G. Lieb, W. G. Park, M. K. Rizk, M. S. Sawhney, N. J. Shaheen, S. Wani, and D. S. Weinberg, “Quality indicators for colonoscopy,” Gastrointest. Endosc. 81(1), 31–53 (2015).
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Schubert, M.

C. P. Dietrich, A. Steude, L. Tropf, M. Schubert, N. M. Kronenberg, K. Ostermann, S. Höfling, and M. C. Gather, “An exciton-polariton laser based on biologically produced fluorescent protein,” Sci. Adv. 2(8), e1600666 (2016).
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M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. C. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15(8), 5647–5652 (2015).
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Selig, M.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Shah, R.

R. Li, S. A. Grimm, D. Mav, H. Gu, D. Djukovic, R. Shah, B. A. Merrick, D. Raftery, and P. A. Wade, “Transcriptome and DNA methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal cancer,” Cell Reports 22(3), 624–637 (2018).
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Shaheen, N. J.

D. K. Rex, P. S. Schoenfeld, J. Cohen, I. M. Pike, D. G. Adler, M. B. Fennerty, J. G. Lieb, W. G. Park, M. K. Rizk, M. S. Sawhney, N. J. Shaheen, S. Wani, and D. S. Weinberg, “Quality indicators for colonoscopy,” Gastrointest. Endosc. 81(1), 31–53 (2015).
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Shinagare, S.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
[Crossref] [PubMed]

Shinozaki, H.

H. L. Newmark, K. Yang, M. Lipkin, L. Kopelovich, Y. Liu, K. Fan, and H. Shinozaki, “A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice,” Carcinogenesis 22(11), 1871–1875 (2001).
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R. L. Siegel, K. D. Miller, and A. Jemal, “Colorectal cancer mortality rates in adults aged 20 to 54 years in the United States, 1970-2014,” JAMA 318(6), 572–574 (2017).
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Signori, E.

M. De Robertis, E. Massi, M. L. Poeta, S. Carotti, S. Morini, L. Cecchetelli, E. Signori, and V. M. Fazio, “The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies,” J. Carcinog. 10(1), 9 (2011).
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Sisk, J. E.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
[Crossref] [PubMed]

Sivaramakrishnan, S.

Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14(24), 4590–4595 (2014).
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Spratt, J. S.

S. Welin, J. Youker, and J. S. Spratt, “The rates and patterns of growth of 375 tumors of the large intestine and rectum observed serially by double contrast enema study (Malmoe technique),” Am. J. Roentgenol. Radium Ther. Nucl. Med. 90, 673–687 (1963).
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Steude, A.

C. P. Dietrich, A. Steude, L. Tropf, M. Schubert, N. M. Kronenberg, K. Ostermann, S. Höfling, and M. C. Gather, “An exciton-polariton laser based on biologically produced fluorescent protein,” Sci. Adv. 2(8), e1600666 (2016).
[Crossref] [PubMed]

M. Schubert, A. Steude, P. Liehm, N. M. Kronenberg, M. Karl, E. C. Campbell, S. J. Powis, and M. C. Gather, “Lasing within live cells containing intracellular optical micro-resonators for barcode-type cell tagging and tracking,” Nano Lett. 15(8), 5647–5652 (2015).
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Stolar, M. H.

S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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S. J. Stryker, B. G. Wolff, C. E. Culp, S. D. Libbe, D. M. Ilstrup, and R. L. MacCarty, “Natural history of untreated colonic polyps,” Gastroenterology 93(5), 1009–1013 (1987).
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L. Cherkezyan, Y. Stypula-Cyrus, H. Subramanian, C. White, M. Dela Cruz, R. K. Wali, M. J. Goldberg, L. K. Bianchi, H. K. Roy, and V. Backman, “Nanoscale changes in chromatin organization represent the initial steps of tumorigenesis: a transmission electron microscopy study,” BMC Cancer 14(1), 189 (2014).
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L. Cherkezyan, Y. Stypula-Cyrus, H. Subramanian, C. White, M. Dela Cruz, R. K. Wali, M. J. Goldberg, L. K. Bianchi, H. K. Roy, and V. Backman, “Nanoscale changes in chromatin organization represent the initial steps of tumorigenesis: a transmission electron microscopy study,” BMC Cancer 14(1), 189 (2014).
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Y.-C. Chen, X. Tan, Q. Sun, Q. Chen, W. Wang, and X. Fan, “Laser-emission imaging of nuclear biomarkers for high-contrast cancer screening and immunodiagnosis,” Nat. Biomed. Eng. 1(9), 724–735 (2017).
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Q. Chen, M. Ritt, S. Sivaramakrishnan, Y. Sun, and X. Fan, “Optofluidic lasers with a single molecular layer of gain,” Lab Chip 14(24), 4590–4595 (2014).
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X. Wu, M. K. Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5(1), 3779 (2014).
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Y.-C. Chen, Q. Chen, X. Wu, X. Tan, J. Wang, and X. Fan, “A robust tissue laser platform for analysis of formalin-fixed paraffin-embedded biopsies,” Lab Chip 18(7), 1057–1065 (2018).
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Y.-C. Chen, X. Tan, Q. Sun, Q. Chen, W. Wang, and X. Fan, “Laser-emission imaging of nuclear biomarkers for high-contrast cancer screening and immunodiagnosis,” Nat. Biomed. Eng. 1(9), 724–735 (2017).
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X. Wu, Q. Chen, P. Xu, Y.-C. Chen, B. Wu, R. M. Coleman, L. Tong, and X. Fan, “Nanowire lasers as intracellular probes,” Nanoscale 10(20), 9729–9735 (2018).
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Y.-C. Chen, Q. Chen, X. Wu, X. Tan, J. Wang, and X. Fan, “A robust tissue laser platform for analysis of formalin-fixed paraffin-embedded biopsies,” Lab Chip 18(7), 1057–1065 (2018).
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Y.-C. Chen, X. Tan, Q. Sun, Q. Chen, W. Wang, and X. Fan, “Laser-emission imaging of nuclear biomarkers for high-contrast cancer screening and immunodiagnosis,” Nat. Biomed. Eng. 1(9), 724–735 (2017).
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Y.-C. Chen, Q. Chen, T. Zhang, W. Wang, and X. Fan, “Versatile tissue lasers based on high-Q Fabry-Pérot microcavities,” Lab Chip 17(3), 538–548 (2017).
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Y. Wang, Z. Duan, Z. Qiu, P. Zhang, J. Wu, D. Zhang, and T. Xiang, “Random lasing in human tissues embedded with organic dyes for cancer diagnosis,” Sci. Rep. 7(1), 8385 (2017).
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S. J. Winawer and A. G. Zauber, “The advanced adenoma as the primary target of screening,” Gastrointest. Endosc. Clin. N. Am. 12(1), 1–9 (2002).
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S. J. Stryker, B. G. Wolff, C. E. Culp, S. D. Libbe, D. M. Ilstrup, and R. L. MacCarty, “Natural history of untreated colonic polyps,” Gastroenterology 93(5), 1009–1013 (1987).
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S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
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X. Wu, Q. Chen, P. Xu, Y.-C. Chen, B. Wu, R. M. Coleman, L. Tong, and X. Fan, “Nanowire lasers as intracellular probes,” Nanoscale 10(20), 9729–9735 (2018).
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Wu, J.

Y. Wang, Z. Duan, Z. Qiu, P. Zhang, J. Wu, D. Zhang, and T. Xiang, “Random lasing in human tissues embedded with organic dyes for cancer diagnosis,” Sci. Rep. 7(1), 8385 (2017).
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Wu, X.

Y.-C. Chen, Q. Chen, X. Wu, X. Tan, J. Wang, and X. Fan, “A robust tissue laser platform for analysis of formalin-fixed paraffin-embedded biopsies,” Lab Chip 18(7), 1057–1065 (2018).
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X. Wu, Q. Chen, P. Xu, Y.-C. Chen, B. Wu, R. M. Coleman, L. Tong, and X. Fan, “Nanowire lasers as intracellular probes,” Nanoscale 10(20), 9729–9735 (2018).
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X. Wu, M. K. Oo, K. Reddy, Q. Chen, Y. Sun, and X. Fan, “Optofluidic laser for dual-mode sensitive biomolecular detection with a large dynamic range,” Nat. Commun. 5(1), 3779 (2014).
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Y. Wang, Z. Duan, Z. Qiu, P. Zhang, J. Wu, D. Zhang, and T. Xiang, “Random lasing in human tissues embedded with organic dyes for cancer diagnosis,” Sci. Rep. 7(1), 8385 (2017).
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Xu, P.

X. Wu, Q. Chen, P. Xu, Y.-C. Chen, B. Wu, R. M. Coleman, L. Tong, and X. Fan, “Nanowire lasers as intracellular probes,” Nanoscale 10(20), 9729–9735 (2018).
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Yang, K.

K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
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H. L. Newmark, K. Yang, M. Lipkin, L. Kopelovich, Y. Liu, K. Fan, and H. Shinozaki, “A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice,” Carcinogenesis 22(11), 1871–1875 (2001).
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S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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Youker, J.

S. Welin, J. Youker, and J. S. Spratt, “The rates and patterns of growth of 375 tumors of the large intestine and rectum observed serially by double contrast enema study (Malmoe technique),” Am. J. Roentgenol. Radium Ther. Nucl. Med. 90, 673–687 (1963).
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Yuan, G. C.

S. Beyaz, M. D. Mana, J. Roper, D. Kedrin, A. Saadatpour, S.-J. Hong, K. E. Bauer-Rowe, M. E. Xifaras, A. Akkad, E. Arias, L. Pinello, Y. Katz, S. Shinagare, M. Abu-Remaileh, M. M. Mihaylova, D. W. Lamming, R. Dogum, G. Guo, G. W. Bell, M. Selig, G. P. Nielsen, N. Gupta, C. R. Ferrone, V. Deshpande, G. C. Yuan, S. H. Orkin, D. M. Sabatini, and Ö. H. Yilmaz, “High-fat diet enhances stemness and tumorigenicity of intestinal progenitors,” Nature 531(7592), 53–58 (2016).
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Yun, S. H.

M. Humar, A. Dobravec, X. Zhao, and S. H. Yun, “Biomaterial microlasers implantable in the cornea, skin, and blood,” Optica 4(9), 1080–1085 (2017).
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S. Cho, M. Humar, N. Martino, and S. H. Yun, “Laser Particle Stimulated Emission Microscopy,” Phys. Rev. Lett. 117(19), 193902 (2016).
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M. Humar and S. H. Yun, “Intracellular microlasers,” Nat. Photonics 9(9), 572–576 (2015).
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S. J. Winawer and A. G. Zauber, “The advanced adenoma as the primary target of screening,” Gastrointest. Endosc. Clin. N. Am. 12(1), 1–9 (2002).
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Y.-A. Wen, X. Xing, J. W. Harris, Y. Y. Zaytseva, M. I. Mitov, D. L. Napier, H. L. Weiss, B. Mark Evers, and T. Gao, “Adipocytes activate mitochondrial fatty acid oxidation and autophagy to promote tumor growth in colon cancer,” Cell Death Dis. 8(2), e2593 (2017).
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Y. Wang, Z. Duan, Z. Qiu, P. Zhang, J. Wu, D. Zhang, and T. Xiang, “Random lasing in human tissues embedded with organic dyes for cancer diagnosis,” Sci. Rep. 7(1), 8385 (2017).
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Y. Wang, Z. Duan, Z. Qiu, P. Zhang, J. Wu, D. Zhang, and T. Xiang, “Random lasing in human tissues embedded with organic dyes for cancer diagnosis,” Sci. Rep. 7(1), 8385 (2017).
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Zhang, T.

Y.-C. Chen, Q. Chen, T. Zhang, W. Wang, and X. Fan, “Versatile tissue lasers based on high-Q Fabry-Pérot microcavities,” Lab Chip 17(3), 538–548 (2017).
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Acta Oncol. (1)

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Am. J. Roentgenol. Radium Ther. Nucl. Med. (1)

S. Welin, J. Youker, and J. S. Spratt, “The rates and patterns of growth of 375 tumors of the large intestine and rectum observed serially by double contrast enema study (Malmoe technique),” Am. J. Roentgenol. Radium Ther. Nucl. Med. 90, 673–687 (1963).
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BMC Cancer (1)

L. Cherkezyan, Y. Stypula-Cyrus, H. Subramanian, C. White, M. Dela Cruz, R. K. Wali, M. J. Goldberg, L. K. Bianchi, H. K. Roy, and V. Backman, “Nanoscale changes in chromatin organization represent the initial steps of tumorigenesis: a transmission electron microscopy study,” BMC Cancer 14(1), 189 (2014).
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Cancer Prev. Res. (1)

S. D. McClintock, J. A. Colacino, D. Attili, M. K. Dame, A. Richter, A. Reddy, V. Basrur, A. H. Rizvi, D. K. Turgeon, J. Varani, and M. N. Aslam, “Calcium-induced differentiation of human colon adenomas in colonoid culture: calcium alone versus calcium with additional trace elements,” Cancer Prev. Res. 11(7), 413–428 (2018).

Cancer Res. (1)

K. Yang, N. Kurihara, K. Fan, H. Newmark, B. Rigas, L. Bancroft, G. Corner, E. Livote, M. Lesser, W. Edelmann, A. Velcich, M. Lipkin, and L. Augenlicht, “Dietary induction of colonic tumors in a mouse model of sporadic colon cancer,” Cancer Res. 68(19), 7803–7810 (2008).
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Carcinogenesis (1)

H. L. Newmark, K. Yang, M. Lipkin, L. Kopelovich, Y. Liu, K. Fan, and H. Shinozaki, “A Western-style diet induces benign and malignant neoplasms in the colon of normal C57Bl/6 mice,” Carcinogenesis 22(11), 1871–1875 (2001).
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Cell Death Dis. (1)

Y.-A. Wen, X. Xing, J. W. Harris, Y. Y. Zaytseva, M. I. Mitov, D. L. Napier, H. L. Weiss, B. Mark Evers, and T. Gao, “Adipocytes activate mitochondrial fatty acid oxidation and autophagy to promote tumor growth in colon cancer,” Cell Death Dis. 8(2), e2593 (2017).
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Cell Reports (1)

R. Li, S. A. Grimm, D. Mav, H. Gu, D. Djukovic, R. Shah, B. A. Merrick, D. Raftery, and P. A. Wade, “Transcriptome and DNA methylome analysis in a mouse model of diet-induced obesity predicts increased risk of colorectal cancer,” Cell Reports 22(3), 624–637 (2018).
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Gastroenterology (2)

S. J. Stryker, B. G. Wolff, C. E. Culp, S. D. Libbe, D. M. Ilstrup, and R. L. MacCarty, “Natural history of untreated colonic polyps,” Gastroenterology 93(5), 1009–1013 (1987).
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S. J. Winawer, R. H. Fletcher, L. Miller, F. Godlee, M. H. Stolar, C. D. Mulrow, S. H. Woolf, S. N. Glick, T. G. Ganiats, J. H. Bond, L. Rosen, J. G. Zapka, S. J. Olsen, F. M. Giardiello, J. E. Sisk, R. Van Antwerp, C. Brown-Davis, D. A. Marciniak, and R. J. Mayer, “Colorectal cancer screening: clinical guidelines and rationale,” Gastroenterology 112(2), 594–642 (1997).
[Crossref] [PubMed]

Gastrointest. Endosc. (1)

D. K. Rex, P. S. Schoenfeld, J. Cohen, I. M. Pike, D. G. Adler, M. B. Fennerty, J. G. Lieb, W. G. Park, M. K. Rizk, M. S. Sawhney, N. J. Shaheen, S. Wani, and D. S. Weinberg, “Quality indicators for colonoscopy,” Gastrointest. Endosc. 81(1), 31–53 (2015).
[Crossref] [PubMed]

Gastrointest. Endosc. Clin. N. Am. (1)

S. J. Winawer and A. G. Zauber, “The advanced adenoma as the primary target of screening,” Gastrointest. Endosc. Clin. N. Am. 12(1), 1–9 (2002).
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Int. J. Exp. Pathol. (1)

N. Mandir, A. J. FitzGerald, and R. A. Goodlad, “Differences in the effects of age on intestinal proliferation, crypt fission and apoptosis on the small intestine and the colon of the rat,” Int. J. Exp. Pathol. 86(2), 125–130 (2005).
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Integr. Cancer Ther. (1)

M. N. Aslam, T. Paruchuri, N. Bhagavathula, and J. Varani, “A mineral-rich red algae extract inhibits polyp formation and inflammation in the gastrointestinal tract of mice on a high-fat diet,” Integr. Cancer Ther. 9(1), 93–99 (2010).
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J. Carcinog. (1)

M. De Robertis, E. Massi, M. L. Poeta, S. Carotti, S. Morini, L. Cecchetelli, E. Signori, and V. M. Fazio, “The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies,” J. Carcinog. 10(1), 9 (2011).
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JAMA (1)

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JAMA Intern. Med. (1)

D. Lieberman, “Colorectal Cancer Screening With Colonoscopy,” JAMA Intern. Med. 176(7), 903–904 (2016).
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Lab Chip (3)

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Figures (11)

Fig. 1
Fig. 1 Conceptual illustrations of the experimental design and setup. a, Experimental animal model used in this work. We focused on the precursor of very early stage development of adenomas by using mouse colon tissues as a model system. Formalin fixed paraffin-embedded (FFPE) tissues from 50 mice were examined, including 10 1-month mice (5 males and 5 females), 40 15-month mice (20 males and 20 females with low-fat and high-fat dietary treatment). b, Conceptual illustration of a large-scale rapid scanning laser-emission microscopy (LEM) for studying cancer precursors, in which an FFPE tissue is sandwiched within a high-Q Fabry-Pérot (FP) cavity. Tissue thickness for all samples used in LEM was 10 μm. Excitation wavelength = 473 nm. Details can be found in Fig. 2. The left panel shows that no significant morphological difference is observed in the H&E images between a low-fat colon tissue and an “apparently normal” high-fat colon tissue. The right panel shows that significant differences can be seen in the LEM images (and other lasing characteristics) between the same two tissues in the left panel. For example, the high-fat tissue has a lower lasing threshold, and more lasing cells and stronger lasing emission under the same external excitation than the low-fat tissue. Those differences reflect the abnormal cell proliferation and chromatin deregulation (condensation) in the high-fat colon tissue, despite the absence of abnormal morphological changes in the H&E image.
Fig. 2
Fig. 2 (Left panel) Optical setup of the laser emission microscopy, in which the laser emission is collected from the FP cavity. (Middle panel) The FP cavity is formed by a bottom mirror on which a colon tissue section (10 μm in thickness) is placed and a top mirror on which SU-8 spacers (height: 15 µm) are microfabricated. The spacer height determines the FP cavity length. (Right panel) Illustration of the top mirror with spacers.
Fig. 3
Fig. 3 Lasing properties of 1-month mice. a, Examples of lasing spectra of a normal colon tissue from a 1-month old mouse (initial stage) stained with YOPRO (0.1 mM) under various pump energy densities. All curves are vertically shifted for clarity. b, Spectrally integrated laser output as a function of pump energy density extracted from the laser spectra of the normal colon tissue in a. The solid line is the linear fit above the lasing threshold, which was 11 μJ/mm2. Tissue thickness = 10 μm. Cavity length = 15 μm. Excitation wavelength = 473 nm. c, Statistics of the lasing threshold for cells in the normal colon tissues stained with YOPRO from five 1-month old male mice (labeled as M1-M5) and five 1-month old female mice (labeled as F1-F5). Exemplary H&E images of male and female mouse colon tissues are provided in the insets. d, Histogram of all male/female normal colon cell lasing thresholds (N = 100) extracted from c.
Fig. 4
Fig. 4 Comparison of laser emissions between low- and high-fat induced colon tissues. a, Example of lasing spectra of a normal colon tissue from a 15-month old low-fat male mouse stained with YOPRO under various pump energy densities. b, Example of lasing spectra of a normal colon tissue from a 15-month old female high-fat mouse stained with YOPRO under various pump energy densities. c, Spectrally integrated laser output as a function of pump energy density extracted from the laser spectra in a and b. The solid lines are the linear fit above the lasing threshold, which was 14 μJ/mm2 and 40 μJ/mm2 for the high-fat mouse and low-fat mouse, respectively. Tissue thickness = 10 μm. Cavity length = 15 μm. Excitation wavelength = 473 nm. d, Direct comparison of laser emission spectra of the same low-fat male (blue curve) and high-fat female (red curve) colon tissues used in c at fixed pump energy density of 30 µJ/mm2. e, Representative fluorescence microscopic images of colon cells from the same low-fat male (left column) and high-fat female (right column) colon tissues used in d. f, Representative laser emission images of colon cells from the same low-fat male (left column) and high-fat female (right column) mice used in e when pumped at 30 µJ/mm2. g, Laser emission images of the same sets of cells in f when the pump energy density increased to 70 µJ/mm2. All scale bars, 20 μm.
Fig. 5
Fig. 5 Assessment of the lasing threshold of low-fat and high-fat induced male mice. a, Statistics of the lasing threshold for cells in individual low-fat male colon tissues (10 mice) stained with YOPRO. b, Statistics of the lasing threshold for cells in individual high-fat male colon tissues (10 mice) stained with YOPRO. c, Histogram of all low-fat/high-fat cell lasing thresholds (N = 230) extracted from a and b. The inset is the corresponding Receiver Operating Characteristics (ROC) curve. The ROC curve is plotted by using the different excitations (in units of µJ/mm2) as the cut-off criterion. The area under the fitted curve is 0.71 and the sensitivity of 50% is obtained based on the cut-off criterion of 40 µJ/mm2. d, Statistic comparison of the lasing threshold for all 230 cells extracted from a and b. The p-value between the two groups is <10−3. The median is 54 and 40 µJ/mm2 for LF and HF, respectively. All tissues were 10 μm in thickness and were sandwiched in a 15 μm long cavity. [YOPRO] = 0.1 mM for all 20 mouse samples.
Fig. 6
Fig. 6 a, Comparison of Ki-67 proliferation biomarker expression among the low-fat male, high-fat male, low-fat female, and high-fat female groups. In each group 5 mice were randomly selected and used nuclear algorithm to analyze the Ki-67 expressions. The Ki-67 expressions were calculated based on the percentage of 2 + and 3 + positive Ki-67 cells in the colon tissue section. Details of the analyzing protocol can be found in the Experimental Section and Ref [28]. b, Exemplary IHC image of a high-fat female mouse with Ki-67 expression shown in dark brown color. c, Exemplary IHC image of a low-fat female mouse with Ki-67 expression shown in dark brown color. Scale bars, 100 µm.
Fig. 7
Fig. 7 Assessment of the lasing threshold of low-fat and high-fat induced female mouse. a, Statistics of the lasing threshold for cells in individual low-fat female colon tissues (10 mice) stained with YOPRO. b, Statistics of the lasing threshold for cells in individual high-fat female colon tissues (10 mice) stained with YOPRO. The black triangles above the 4 data sets indicate the 4 mice that had been identified with polyp growth in other parts of their colons (not in the parts used in the current study). c, Histogram of all low-fat/high-fat cell lasing thresholds (N = 204) extracted from a and b. The inset is the corresponding Receiver Operating Characteristics (ROC) curve. The ROC curve is plotted by using the different excitations (in units of µJ/mm2) as the cut-off criterion. The area under the fitted curve is 0.87 and the sensitivity of 99% is obtained based on the cut-off criterion of 45 µJ/mm2. d, Statistic comparison of the lasing threshold for all 204 cells extracted from a and b. The p-value between the two groups is <<10−3. The median is 41 and 24 µJ/mm2 for LF and HF, respectively. All tissues were 10 μm in thickness and were sandwiched in a 15 μm long cavity. [YOPRO] = 0.1 mM for all 20 mouse samples.
Fig. 8
Fig. 8 a, Histogram of all low-fat/high-fat cell lasing thresholds (N = 434) by combining the results for males and females in Figs. 5(c) and 7(c). The inset is the corresponding Receiver Operating Characteristics (ROC) curve. The ROC curve is plotted by using the different excitations (in units of µJ/mm2) as the cut-off criterion. The area under the fitted curve is 0.76 and the sensitivity of 70% is obtained based on the cut-off criterion of 40 µJ/mm2. b, Statistic comparison of the lasing threshold for all 434 cells extracted from Figs. 5(a), 5(b), 7(a), and 7(b) by grouping the mice based on low-fat and high-fat treatment regardless of the gender. The p-value between the two groups is <<10−3. All tissues were 10 μm in thickness and were sandwiched in a 15 μm long cavity. [YOPRO] = 0.1 mM for all 40 mouse samples.
Fig. 9
Fig. 9 Assessment of the lasing threshold of adenomas and adjacent tissues. a, Statistics of the lasing threshold for cells in individual colon adenoma tissues (5 3-month male mice on regular diet, denoted as Ad1 to Ad5) stained with YOPRO. The inset shows an exemplary H&E image of colon tissue. The blue dotted circle (2 mm in radius) indicates the area that has colon adenoma. b, Statistics of the lasing threshold for cells in the normal colon tissues adjacent to adenoma from the exactly same tissue section in a stained with YOPRO (Ad-N1 to Ad-N5 denote the adjacent normal tissues from Ad1 to Ad5 used in (a), respectively). The black arrows in the inset H&E image show the adjacent normal tissue used for measurements.
Fig. 10
Fig. 10 Laser-emission imaging of mice colon tissues. a, Representative low-fat male laser emission image (bottom) that is overlaid with the corresponding brightfield image (top). b, Representative high-fat male laser emission image (bottom) that is overlaid with the corresponding brightfield image (top). c, Representative low-fat female laser emission image (bottom) that is overlaid with the corresponding brightfield image (top). d, Representative high-fat laser emission image (bottom) that is overlaid with the corresponding brightfield image (top). e, IHC microscopic image of a high-fat female colon tissue labeled with Ki-67 biomarker (top image). The corresponding laser emission image (large scale scanning) overlaid with the corresponding brightfield image is shown in the bottom image. The tissues for the top image and the bottom image were sliced from the same FFPE block. The total area is 3 mm x 0.5 mm. All images were scanned and measured under a pump energy density of 45 µJ/mm2. All scale bars, 100 µm. The estimated number of lasing cells for images in a,b,c,d, and e are 4, 45, 16, 64, and 125, respectively. Note that the brightfield images appear to be red since they were taken through the mirror that blocks the green light.
Fig. 11
Fig. 11 a, (Left) Representative laser emission image of an adenoma tissue overlaid with the corresponding brightfield image. (Right) The laser emission image alone. b, (Left) Representative laser emission image of a normal tissue adjacent to adenoma overlaid with the corresponding brightfield image. (Right) The laser emission image alone. The LEM images were scanned and measured under a pump energy density of 45 µJ/mm2. Scale bars, 200 µm.

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