Abstract

Following prolonged administration, certain orally bioavailable but poorly soluble small molecule drugs are prone to precipitate out and form crystal-like drug inclusions (CLDIs) within the cells of living organisms. In this research, we present a quantitative multi-parameter imaging platform for measuring the fluorescence and polarization diattenuation signals of cells harboring intracellular CLDIs. To validate the imaging system, the FDA-approved drug clofazimine (CFZ) was used as a model compound. Our results demonstrated that a quantitative multi-parameter microscopy image analysis platform can be used to study drug sequestering macrophages, and to detect the formation of ordered molecular aggregates formed by poorly soluble small molecule drugs in animals.

© 2017 Optical Society of America

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References

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2016 (3)

C. A. Valades Cruz, H. A. Shaban, A. Kress, N. Bertaux, S. Monneret, M. Mavrakis, J. Savatier, and S. Brasselet, “Quantitative nanoscale imaging of orientational order in biological filaments by polarized superresolution microscopy,” Proc. Natl. Acad. Sci. U.S.A. 113(7), E820–E828 (2016).
[Crossref] [PubMed]

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular Order of Arterial Collagen Using Circular Polarization Second-Harmonic Generation Imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref] [PubMed]

G. S. Yoon, R. K. Keswani, S. Sud, P. M. Rzeczycki, M. D. Murashov, T. A. Koehn, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Clofazimine Biocrystal Accumulation in Macrophages Upregulates IL-1RA Production to Induce a Systemic Anti-Inflammatory State,” Antimicrob. Agents Chemother. 60(6), 3470–3479 (2016).
[Crossref]

2015 (6)

K. A. Min, W. G. Rajeswaran, R. Oldenbourg, G. Harris, R. K. Keswani, M. Chiang, P. Rzeczycki, A. Talattof, M. Hafeez, R. W. Horobin, S. D. Larsen, K. A. Stringer, and G. R. Rosania, “Massive Bioaccumulation and Self-Assembly of Phenazine Compounds in Live Cells,” Adv Sci (Weinh) 2(8), 1500025 (2015).
[Crossref] [PubMed]

R. K. Keswani, J. Baik, L. Yeomans, C. Hitzman, A. M. Johnson, A. S. Pawate, P. J. Kenis, N. Rodriguez-Hornedo, K. A. Stringer, and G. R. Rosania, “Chemical Analysis of Drug Biocrystals: A Role for Counterion Transport Pathways in Intracellular Drug Disposition,” Mol. Pharm. 12(7), 2528–2536 (2015).
[Crossref] [PubMed]

G. S. Yoon, S. Sud, R. K. Keswani, J. Baik, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Phagocytosed Clofazimine Biocrystals Can Modulate Innate Immune Signaling by Inhibiting TNFα and Boosting IL-1RA Secretion,” Mol. Pharm. 12(7), 2517–2527 (2015).
[Crossref] [PubMed]

B. C. Vidal, E. H. M. Dos Anjos, and M. L. S. Mello, “Optical anisotropy reveals molecular order in a mouse enthesis,” Cell Tissue Res. 362(1), 177–185 (2015).
[Crossref] [PubMed]

R. Keswani, G. Yoon, S. Sud, K. Stringer, and G. Rosania, “A Far-Red Fluorescent Probe For Flow Cytometric Xenobiotic-Sequestering Cell Functional Studies,” Cytometry A 87(9), 855–867 (2015).
[Crossref]

G. S. Yoon, S. Sud, R. K. Keswani, J. Baik, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Phagocytosed Clofazimine Biocrystals Can Modulate Innate Immune Signaling by Inhibiting TNFα and Boosting IL-1RA Secretion,” Mol. Pharm. 12(7), 2517–2527 (2015).
[Crossref] [PubMed]

2014 (2)

R. Logan, A. C. Kong, and J. P. Krise, “Time-Dependent Effects of Hydrophobic Amine-Containing Drugs on Lysosome Structure and Biogenesis in Cultured Human Fibroblasts,” J. Pharm. Sci. 103(10), 3287–3296 (2014).
[Crossref] [PubMed]

H. Z. Amin, S. Mori, N. Sasaki, and K. Hirata, “Diagnostic Approach to Cardiac Amyloidosis,” Kobe J. Med. Sci. 60(1), E5–E11 (2014).
[PubMed]

2013 (4)

M. Biegstraaten, G. E. Linthorst, I. N. van Schaik, and C. E. M. Hollak, “Fabry Disease: a Rare Cause of Neuropathic Pain,” Curr. Pain Headache Rep. 17(10), 365 (2013).
[Crossref] [PubMed]

J. Baik, K. A. Stringer, G. Mane, and G. R. Rosania, “Multiscale Distribution and Bioaccumulation Analysis of Clofazimine Reveals a Massive Immune System-Mediated Xenobiotic Sequestration Response,” Antimicrob. Agents Chemother. 57(3), 1218–1230 (2013).
[Crossref] [PubMed]

S. B. Mehta, M. Shribak, and R. Oldenbourg, “Polarized light imaging of birefringence and diattenuation at high resolution and high sensitivity,” J. Opt. 15(9), 094007 (2013).
[Crossref] [PubMed]

J. R. Molano and V. Molano, “Dementia with Lewy bodies,” Semin. Neurol. 33(4), 330–335 (2013).
[Crossref] [PubMed]

2012 (3)

J. Baik and G. R. Rosania, “Macrophages Sequester Clofazimine in an Intracellular Liquid Crystal-Like Supramolecular Organization,” PLoS One 7(10), e47494 (2012).
[Crossref] [PubMed]

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

R. S. Funk and J. P. Krise, “Cationic amphiphilic drugs cause a marked expansion of apparent lysosomal volume: implications for an intracellular distribution-based drug interaction,” Mol. Pharm. 9(5), 1384–1395 (2012).
[PubMed]

2011 (2)

J. Baik and G. R. Rosania, “Molecular imaging of intracellular drug-membrane aggregate formation,” Mol. Pharm. 8(5), 1742–1749 (2011).
[Crossref] [PubMed]

B. S. DeMay, X. Bai, L. Howard, P. Occhipinti, R. A. Meseroll, E. T. Spiliotis, R. Oldenbourg, and A. S. Gladfelter, “Septin filaments exhibit a dynamic, paired organization that is conserved from yeast to mammals,” J. Cell Biol. 193(6), 1065–1081 (2011).
[Crossref] [PubMed]

2008 (3)

S. B. Sparenga, “The Importance of Polarized Light Microscopy in the Analytical Setting,” Microsc. Microanal. 14(S2), 1032–1033 (2008).
[Crossref]

P. Libby, “Molecular and cellular mechanisms of the thrombotic complications of atherosclerosis,” J. Lipid Res. 50(Suppl), S352–S357 (2008).
[Crossref] [PubMed]

C. A. Naughton, “Drug-induced nephrotoxicity,” Am. Fam. Physician 78(6), 743–750 (2008).
[PubMed]

2007 (2)

J. A. Byrne, D. A. Pedersen, L. L. Clepper, M. Nelson, W. G. Sanger, S. Gokhale, D. P. Wolf, and S. M. Mitalipov, “Producing primate embryonic stem cells by somatic cell nuclear transfer,” Nature 450(7169), 497–502 (2007).
[Crossref] [PubMed]

W. Kaminsky, E. Gunn, R. Sours, and B. Kahr, “Simultaneous false-colour imaging of birefringence, extinction and transmittance at camera speed,” J. Microsc. 228(2), 153–164 (2007).
[Crossref] [PubMed]

2006 (1)

W. Kaminksy, L.-W. Jin, S. Powell, I. Maezawa, K. Claborn, C. Branham, and B. Kahr, “Polarimetric imaging of amyloid,” Micron 37(4), 324–338 (2006).
[Crossref] [PubMed]

2005 (1)

P. A. A. S. Navarro, L. Liu, J. R. Trimarchi, R. A. Ferriani, and D. L. Keefe, “Noninvasive imaging of spindle dynamics during mammalian oocyte activation,” Fertil. Steril. 83(4Suppl 1), 1197–1205 (2005).
[Crossref] [PubMed]

2004 (3)

M. D. Abramoff, P. J. Magalhaes, and S. J. Ram, “Image Processing With ImageJ,” Biophoton. Int. 11, 36–42 (2004).

C. J. Hewitt and G. Nebe-Von-Caron, “The application of multi-parameter flow cytometry to monitor individual microbial cell physiological state,” Adv. Biochem. Eng. Biotechnol. 89, 197–223 (2004).
[Crossref] [PubMed]

W. Kaminsky, K. Claborn, and B. Kahr, “Polarimetric imaging of crystals,” Chem. Soc. Rev. 33(8), 514–525 (2004).
[Crossref] [PubMed]

2003 (2)

S. L. Ciesla, J. Trahan, W. B. Wan, J. R. Beadle, K. A. Aldern, G. R. Painter, and K. Y. Hostetler, “Esterification of cidofovir with alkoxyalkanols increases oral bioavailability and diminishes drug accumulation in kidney,” Antiviral Res. 59(3), 163–171 (2003).
[Crossref] [PubMed]

F. Massoumian, R. Juskaitis, M. A. A. Neil, and T. Wilson, “Quantitative polarized light microscopy,” J. Microsc. 209(1), 13–22 (2003).
[Crossref] [PubMed]

2000 (1)

L. Liu, R. Oldenbourg, J. R. Trimarchi, and D. L. Keefe, “A reliable, noninvasive technique for spindle imaging and enucleation of mammalian oocytes,” Nat. Biotechnol. 18(2), 223–225 (2000).
[Crossref] [PubMed]

1998 (2)

R. Oldenbourg, E. D. Salmon, and P. T. Tran, “Birefringence of Single and Bundled Microtubules,” Biophys. J. 74(1), 645–654 (1998).
[Crossref] [PubMed]

S. R. Hawley, P. G. Bray, M. Mungthin, J. D. Atkinson, P. M. O’Neill, and S. A. Ward, “Relationship between antimalarial drug activity, accumulation, and inhibition of heme polymerization in Plasmodium falciparum in vitro,” Antimicrob. Agents Chemother. 42(3), 682–686 (1998).
[PubMed]

1996 (1)

S. R. Hawley, P. G. Bray, P. M. O’Neill, B. K. Park, and S. A. Ward, “The role of drug accumulation in 4-aminoquinoline antimalarial potency,” Biochem. Pharmacol. 52(5), 723–733 (1996).
[Crossref] [PubMed]

1985 (1)

W. Mickols, M. F. Maestre, I. Tinoco, and S. H. Embury, “Visualization of oriented hemoglobin S in individual erythrocytes by differential extinction of polarized light,” Proc. Natl. Acad. Sci. U.S.A. 82(19), 6527–6531 (1985).
[Crossref] [PubMed]

1981 (1)

L. D. Loose, J. B. Silkworth, T. Charbonneau, and F. Blumenstock, “Environmental chemical-induced macrophage dysfunction,” Environ. Health Perspect. 39, 79–91 (1981).
[Crossref] [PubMed]

Abramoff, M. D.

M. D. Abramoff, P. J. Magalhaes, and S. J. Ram, “Image Processing With ImageJ,” Biophoton. Int. 11, 36–42 (2004).

Aldern, K. A.

S. L. Ciesla, J. Trahan, W. B. Wan, J. R. Beadle, K. A. Aldern, G. R. Painter, and K. Y. Hostetler, “Esterification of cidofovir with alkoxyalkanols increases oral bioavailability and diminishes drug accumulation in kidney,” Antiviral Res. 59(3), 163–171 (2003).
[Crossref] [PubMed]

Amin, H. Z.

H. Z. Amin, S. Mori, N. Sasaki, and K. Hirata, “Diagnostic Approach to Cardiac Amyloidosis,” Kobe J. Med. Sci. 60(1), E5–E11 (2014).
[PubMed]

Atkinson, J. D.

S. R. Hawley, P. G. Bray, M. Mungthin, J. D. Atkinson, P. M. O’Neill, and S. A. Ward, “Relationship between antimalarial drug activity, accumulation, and inhibition of heme polymerization in Plasmodium falciparum in vitro,” Antimicrob. Agents Chemother. 42(3), 682–686 (1998).
[PubMed]

Bai, X.

B. S. DeMay, X. Bai, L. Howard, P. Occhipinti, R. A. Meseroll, E. T. Spiliotis, R. Oldenbourg, and A. S. Gladfelter, “Septin filaments exhibit a dynamic, paired organization that is conserved from yeast to mammals,” J. Cell Biol. 193(6), 1065–1081 (2011).
[Crossref] [PubMed]

Baik, J.

G. S. Yoon, S. Sud, R. K. Keswani, J. Baik, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Phagocytosed Clofazimine Biocrystals Can Modulate Innate Immune Signaling by Inhibiting TNFα and Boosting IL-1RA Secretion,” Mol. Pharm. 12(7), 2517–2527 (2015).
[Crossref] [PubMed]

R. K. Keswani, J. Baik, L. Yeomans, C. Hitzman, A. M. Johnson, A. S. Pawate, P. J. Kenis, N. Rodriguez-Hornedo, K. A. Stringer, and G. R. Rosania, “Chemical Analysis of Drug Biocrystals: A Role for Counterion Transport Pathways in Intracellular Drug Disposition,” Mol. Pharm. 12(7), 2528–2536 (2015).
[Crossref] [PubMed]

G. S. Yoon, S. Sud, R. K. Keswani, J. Baik, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Phagocytosed Clofazimine Biocrystals Can Modulate Innate Immune Signaling by Inhibiting TNFα and Boosting IL-1RA Secretion,” Mol. Pharm. 12(7), 2517–2527 (2015).
[Crossref] [PubMed]

J. Baik, K. A. Stringer, G. Mane, and G. R. Rosania, “Multiscale Distribution and Bioaccumulation Analysis of Clofazimine Reveals a Massive Immune System-Mediated Xenobiotic Sequestration Response,” Antimicrob. Agents Chemother. 57(3), 1218–1230 (2013).
[Crossref] [PubMed]

J. Baik and G. R. Rosania, “Macrophages Sequester Clofazimine in an Intracellular Liquid Crystal-Like Supramolecular Organization,” PLoS One 7(10), e47494 (2012).
[Crossref] [PubMed]

J. Baik and G. R. Rosania, “Molecular imaging of intracellular drug-membrane aggregate formation,” Mol. Pharm. 8(5), 1742–1749 (2011).
[Crossref] [PubMed]

Beadle, J. R.

S. L. Ciesla, J. Trahan, W. B. Wan, J. R. Beadle, K. A. Aldern, G. R. Painter, and K. Y. Hostetler, “Esterification of cidofovir with alkoxyalkanols increases oral bioavailability and diminishes drug accumulation in kidney,” Antiviral Res. 59(3), 163–171 (2003).
[Crossref] [PubMed]

Bertaux, N.

C. A. Valades Cruz, H. A. Shaban, A. Kress, N. Bertaux, S. Monneret, M. Mavrakis, J. Savatier, and S. Brasselet, “Quantitative nanoscale imaging of orientational order in biological filaments by polarized superresolution microscopy,” Proc. Natl. Acad. Sci. U.S.A. 113(7), E820–E828 (2016).
[Crossref] [PubMed]

Biegstraaten, M.

M. Biegstraaten, G. E. Linthorst, I. N. van Schaik, and C. E. M. Hollak, “Fabry Disease: a Rare Cause of Neuropathic Pain,” Curr. Pain Headache Rep. 17(10), 365 (2013).
[Crossref] [PubMed]

Blumenstock, F.

L. D. Loose, J. B. Silkworth, T. Charbonneau, and F. Blumenstock, “Environmental chemical-induced macrophage dysfunction,” Environ. Health Perspect. 39, 79–91 (1981).
[Crossref] [PubMed]

Branham, C.

W. Kaminksy, L.-W. Jin, S. Powell, I. Maezawa, K. Claborn, C. Branham, and B. Kahr, “Polarimetric imaging of amyloid,” Micron 37(4), 324–338 (2006).
[Crossref] [PubMed]

Brasselet, S.

C. A. Valades Cruz, H. A. Shaban, A. Kress, N. Bertaux, S. Monneret, M. Mavrakis, J. Savatier, and S. Brasselet, “Quantitative nanoscale imaging of orientational order in biological filaments by polarized superresolution microscopy,” Proc. Natl. Acad. Sci. U.S.A. 113(7), E820–E828 (2016).
[Crossref] [PubMed]

Bray, P. G.

S. R. Hawley, P. G. Bray, M. Mungthin, J. D. Atkinson, P. M. O’Neill, and S. A. Ward, “Relationship between antimalarial drug activity, accumulation, and inhibition of heme polymerization in Plasmodium falciparum in vitro,” Antimicrob. Agents Chemother. 42(3), 682–686 (1998).
[PubMed]

S. R. Hawley, P. G. Bray, P. M. O’Neill, B. K. Park, and S. A. Ward, “The role of drug accumulation in 4-aminoquinoline antimalarial potency,” Biochem. Pharmacol. 52(5), 723–733 (1996).
[Crossref] [PubMed]

Byrne, J. A.

J. A. Byrne, D. A. Pedersen, L. L. Clepper, M. Nelson, W. G. Sanger, S. Gokhale, D. P. Wolf, and S. M. Mitalipov, “Producing primate embryonic stem cells by somatic cell nuclear transfer,” Nature 450(7169), 497–502 (2007).
[Crossref] [PubMed]

Charbonneau, T.

L. D. Loose, J. B. Silkworth, T. Charbonneau, and F. Blumenstock, “Environmental chemical-induced macrophage dysfunction,” Environ. Health Perspect. 39, 79–91 (1981).
[Crossref] [PubMed]

Chiang, M.

K. A. Min, W. G. Rajeswaran, R. Oldenbourg, G. Harris, R. K. Keswani, M. Chiang, P. Rzeczycki, A. Talattof, M. Hafeez, R. W. Horobin, S. D. Larsen, K. A. Stringer, and G. R. Rosania, “Massive Bioaccumulation and Self-Assembly of Phenazine Compounds in Live Cells,” Adv Sci (Weinh) 2(8), 1500025 (2015).
[Crossref] [PubMed]

Ciesla, S. L.

S. L. Ciesla, J. Trahan, W. B. Wan, J. R. Beadle, K. A. Aldern, G. R. Painter, and K. Y. Hostetler, “Esterification of cidofovir with alkoxyalkanols increases oral bioavailability and diminishes drug accumulation in kidney,” Antiviral Res. 59(3), 163–171 (2003).
[Crossref] [PubMed]

Claborn, K.

W. Kaminksy, L.-W. Jin, S. Powell, I. Maezawa, K. Claborn, C. Branham, and B. Kahr, “Polarimetric imaging of amyloid,” Micron 37(4), 324–338 (2006).
[Crossref] [PubMed]

W. Kaminsky, K. Claborn, and B. Kahr, “Polarimetric imaging of crystals,” Chem. Soc. Rev. 33(8), 514–525 (2004).
[Crossref] [PubMed]

Clepper, L. L.

J. A. Byrne, D. A. Pedersen, L. L. Clepper, M. Nelson, W. G. Sanger, S. Gokhale, D. P. Wolf, and S. M. Mitalipov, “Producing primate embryonic stem cells by somatic cell nuclear transfer,” Nature 450(7169), 497–502 (2007).
[Crossref] [PubMed]

DeMay, B. S.

B. S. DeMay, X. Bai, L. Howard, P. Occhipinti, R. A. Meseroll, E. T. Spiliotis, R. Oldenbourg, and A. S. Gladfelter, “Septin filaments exhibit a dynamic, paired organization that is conserved from yeast to mammals,” J. Cell Biol. 193(6), 1065–1081 (2011).
[Crossref] [PubMed]

Dos Anjos, E. H. M.

B. C. Vidal, E. H. M. Dos Anjos, and M. L. S. Mello, “Optical anisotropy reveals molecular order in a mouse enthesis,” Cell Tissue Res. 362(1), 177–185 (2015).
[Crossref] [PubMed]

Eliceiri, K. W.

C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nat. Methods 9(7), 671–675 (2012).
[Crossref] [PubMed]

Embury, S. H.

W. Mickols, M. F. Maestre, I. Tinoco, and S. H. Embury, “Visualization of oriented hemoglobin S in individual erythrocytes by differential extinction of polarized light,” Proc. Natl. Acad. Sci. U.S.A. 82(19), 6527–6531 (1985).
[Crossref] [PubMed]

Ferriani, R. A.

P. A. A. S. Navarro, L. Liu, J. R. Trimarchi, R. A. Ferriani, and D. L. Keefe, “Noninvasive imaging of spindle dynamics during mammalian oocyte activation,” Fertil. Steril. 83(4Suppl 1), 1197–1205 (2005).
[Crossref] [PubMed]

Funk, R. S.

R. S. Funk and J. P. Krise, “Cationic amphiphilic drugs cause a marked expansion of apparent lysosomal volume: implications for an intracellular distribution-based drug interaction,” Mol. Pharm. 9(5), 1384–1395 (2012).
[PubMed]

Gladfelter, A. S.

B. S. DeMay, X. Bai, L. Howard, P. Occhipinti, R. A. Meseroll, E. T. Spiliotis, R. Oldenbourg, and A. S. Gladfelter, “Septin filaments exhibit a dynamic, paired organization that is conserved from yeast to mammals,” J. Cell Biol. 193(6), 1065–1081 (2011).
[Crossref] [PubMed]

Gokhale, S.

J. A. Byrne, D. A. Pedersen, L. L. Clepper, M. Nelson, W. G. Sanger, S. Gokhale, D. P. Wolf, and S. M. Mitalipov, “Producing primate embryonic stem cells by somatic cell nuclear transfer,” Nature 450(7169), 497–502 (2007).
[Crossref] [PubMed]

Gunn, E.

W. Kaminsky, E. Gunn, R. Sours, and B. Kahr, “Simultaneous false-colour imaging of birefringence, extinction and transmittance at camera speed,” J. Microsc. 228(2), 153–164 (2007).
[Crossref] [PubMed]

Hafeez, M.

K. A. Min, W. G. Rajeswaran, R. Oldenbourg, G. Harris, R. K. Keswani, M. Chiang, P. Rzeczycki, A. Talattof, M. Hafeez, R. W. Horobin, S. D. Larsen, K. A. Stringer, and G. R. Rosania, “Massive Bioaccumulation and Self-Assembly of Phenazine Compounds in Live Cells,” Adv Sci (Weinh) 2(8), 1500025 (2015).
[Crossref] [PubMed]

Harris, G.

K. A. Min, W. G. Rajeswaran, R. Oldenbourg, G. Harris, R. K. Keswani, M. Chiang, P. Rzeczycki, A. Talattof, M. Hafeez, R. W. Horobin, S. D. Larsen, K. A. Stringer, and G. R. Rosania, “Massive Bioaccumulation and Self-Assembly of Phenazine Compounds in Live Cells,” Adv Sci (Weinh) 2(8), 1500025 (2015).
[Crossref] [PubMed]

Hawley, S. R.

S. R. Hawley, P. G. Bray, M. Mungthin, J. D. Atkinson, P. M. O’Neill, and S. A. Ward, “Relationship between antimalarial drug activity, accumulation, and inhibition of heme polymerization in Plasmodium falciparum in vitro,” Antimicrob. Agents Chemother. 42(3), 682–686 (1998).
[PubMed]

S. R. Hawley, P. G. Bray, P. M. O’Neill, B. K. Park, and S. A. Ward, “The role of drug accumulation in 4-aminoquinoline antimalarial potency,” Biochem. Pharmacol. 52(5), 723–733 (1996).
[Crossref] [PubMed]

Hewitt, C. J.

C. J. Hewitt and G. Nebe-Von-Caron, “The application of multi-parameter flow cytometry to monitor individual microbial cell physiological state,” Adv. Biochem. Eng. Biotechnol. 89, 197–223 (2004).
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Hirata, K.

H. Z. Amin, S. Mori, N. Sasaki, and K. Hirata, “Diagnostic Approach to Cardiac Amyloidosis,” Kobe J. Med. Sci. 60(1), E5–E11 (2014).
[PubMed]

Hitzman, C.

R. K. Keswani, J. Baik, L. Yeomans, C. Hitzman, A. M. Johnson, A. S. Pawate, P. J. Kenis, N. Rodriguez-Hornedo, K. A. Stringer, and G. R. Rosania, “Chemical Analysis of Drug Biocrystals: A Role for Counterion Transport Pathways in Intracellular Drug Disposition,” Mol. Pharm. 12(7), 2528–2536 (2015).
[Crossref] [PubMed]

Hollak, C. E. M.

M. Biegstraaten, G. E. Linthorst, I. N. van Schaik, and C. E. M. Hollak, “Fabry Disease: a Rare Cause of Neuropathic Pain,” Curr. Pain Headache Rep. 17(10), 365 (2013).
[Crossref] [PubMed]

Horobin, R. W.

K. A. Min, W. G. Rajeswaran, R. Oldenbourg, G. Harris, R. K. Keswani, M. Chiang, P. Rzeczycki, A. Talattof, M. Hafeez, R. W. Horobin, S. D. Larsen, K. A. Stringer, and G. R. Rosania, “Massive Bioaccumulation and Self-Assembly of Phenazine Compounds in Live Cells,” Adv Sci (Weinh) 2(8), 1500025 (2015).
[Crossref] [PubMed]

Hostetler, K. Y.

S. L. Ciesla, J. Trahan, W. B. Wan, J. R. Beadle, K. A. Aldern, G. R. Painter, and K. Y. Hostetler, “Esterification of cidofovir with alkoxyalkanols increases oral bioavailability and diminishes drug accumulation in kidney,” Antiviral Res. 59(3), 163–171 (2003).
[Crossref] [PubMed]

Howard, L.

B. S. DeMay, X. Bai, L. Howard, P. Occhipinti, R. A. Meseroll, E. T. Spiliotis, R. Oldenbourg, and A. S. Gladfelter, “Septin filaments exhibit a dynamic, paired organization that is conserved from yeast to mammals,” J. Cell Biol. 193(6), 1065–1081 (2011).
[Crossref] [PubMed]

Jin, L.-W.

W. Kaminksy, L.-W. Jin, S. Powell, I. Maezawa, K. Claborn, C. Branham, and B. Kahr, “Polarimetric imaging of amyloid,” Micron 37(4), 324–338 (2006).
[Crossref] [PubMed]

Johnson, A. M.

R. K. Keswani, J. Baik, L. Yeomans, C. Hitzman, A. M. Johnson, A. S. Pawate, P. J. Kenis, N. Rodriguez-Hornedo, K. A. Stringer, and G. R. Rosania, “Chemical Analysis of Drug Biocrystals: A Role for Counterion Transport Pathways in Intracellular Drug Disposition,” Mol. Pharm. 12(7), 2528–2536 (2015).
[Crossref] [PubMed]

Juskaitis, R.

F. Massoumian, R. Juskaitis, M. A. A. Neil, and T. Wilson, “Quantitative polarized light microscopy,” J. Microsc. 209(1), 13–22 (2003).
[Crossref] [PubMed]

Kahr, B.

W. Kaminsky, E. Gunn, R. Sours, and B. Kahr, “Simultaneous false-colour imaging of birefringence, extinction and transmittance at camera speed,” J. Microsc. 228(2), 153–164 (2007).
[Crossref] [PubMed]

W. Kaminksy, L.-W. Jin, S. Powell, I. Maezawa, K. Claborn, C. Branham, and B. Kahr, “Polarimetric imaging of amyloid,” Micron 37(4), 324–338 (2006).
[Crossref] [PubMed]

W. Kaminsky, K. Claborn, and B. Kahr, “Polarimetric imaging of crystals,” Chem. Soc. Rev. 33(8), 514–525 (2004).
[Crossref] [PubMed]

Kaminksy, W.

W. Kaminksy, L.-W. Jin, S. Powell, I. Maezawa, K. Claborn, C. Branham, and B. Kahr, “Polarimetric imaging of amyloid,” Micron 37(4), 324–338 (2006).
[Crossref] [PubMed]

Kaminsky, W.

W. Kaminsky, E. Gunn, R. Sours, and B. Kahr, “Simultaneous false-colour imaging of birefringence, extinction and transmittance at camera speed,” J. Microsc. 228(2), 153–164 (2007).
[Crossref] [PubMed]

W. Kaminsky, K. Claborn, and B. Kahr, “Polarimetric imaging of crystals,” Chem. Soc. Rev. 33(8), 514–525 (2004).
[Crossref] [PubMed]

Keefe, D. L.

P. A. A. S. Navarro, L. Liu, J. R. Trimarchi, R. A. Ferriani, and D. L. Keefe, “Noninvasive imaging of spindle dynamics during mammalian oocyte activation,” Fertil. Steril. 83(4Suppl 1), 1197–1205 (2005).
[Crossref] [PubMed]

L. Liu, R. Oldenbourg, J. R. Trimarchi, and D. L. Keefe, “A reliable, noninvasive technique for spindle imaging and enucleation of mammalian oocytes,” Nat. Biotechnol. 18(2), 223–225 (2000).
[Crossref] [PubMed]

Kenis, P. J.

R. K. Keswani, J. Baik, L. Yeomans, C. Hitzman, A. M. Johnson, A. S. Pawate, P. J. Kenis, N. Rodriguez-Hornedo, K. A. Stringer, and G. R. Rosania, “Chemical Analysis of Drug Biocrystals: A Role for Counterion Transport Pathways in Intracellular Drug Disposition,” Mol. Pharm. 12(7), 2528–2536 (2015).
[Crossref] [PubMed]

Keswani, R.

R. Keswani, G. Yoon, S. Sud, K. Stringer, and G. Rosania, “A Far-Red Fluorescent Probe For Flow Cytometric Xenobiotic-Sequestering Cell Functional Studies,” Cytometry A 87(9), 855–867 (2015).
[Crossref]

Keswani, R. K.

G. S. Yoon, R. K. Keswani, S. Sud, P. M. Rzeczycki, M. D. Murashov, T. A. Koehn, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Clofazimine Biocrystal Accumulation in Macrophages Upregulates IL-1RA Production to Induce a Systemic Anti-Inflammatory State,” Antimicrob. Agents Chemother. 60(6), 3470–3479 (2016).
[Crossref]

G. S. Yoon, S. Sud, R. K. Keswani, J. Baik, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Phagocytosed Clofazimine Biocrystals Can Modulate Innate Immune Signaling by Inhibiting TNFα and Boosting IL-1RA Secretion,” Mol. Pharm. 12(7), 2517–2527 (2015).
[Crossref] [PubMed]

R. K. Keswani, J. Baik, L. Yeomans, C. Hitzman, A. M. Johnson, A. S. Pawate, P. J. Kenis, N. Rodriguez-Hornedo, K. A. Stringer, and G. R. Rosania, “Chemical Analysis of Drug Biocrystals: A Role for Counterion Transport Pathways in Intracellular Drug Disposition,” Mol. Pharm. 12(7), 2528–2536 (2015).
[Crossref] [PubMed]

K. A. Min, W. G. Rajeswaran, R. Oldenbourg, G. Harris, R. K. Keswani, M. Chiang, P. Rzeczycki, A. Talattof, M. Hafeez, R. W. Horobin, S. D. Larsen, K. A. Stringer, and G. R. Rosania, “Massive Bioaccumulation and Self-Assembly of Phenazine Compounds in Live Cells,” Adv Sci (Weinh) 2(8), 1500025 (2015).
[Crossref] [PubMed]

G. S. Yoon, S. Sud, R. K. Keswani, J. Baik, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Phagocytosed Clofazimine Biocrystals Can Modulate Innate Immune Signaling by Inhibiting TNFα and Boosting IL-1RA Secretion,” Mol. Pharm. 12(7), 2517–2527 (2015).
[Crossref] [PubMed]

Koehn, T. A.

G. S. Yoon, R. K. Keswani, S. Sud, P. M. Rzeczycki, M. D. Murashov, T. A. Koehn, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Clofazimine Biocrystal Accumulation in Macrophages Upregulates IL-1RA Production to Induce a Systemic Anti-Inflammatory State,” Antimicrob. Agents Chemother. 60(6), 3470–3479 (2016).
[Crossref]

Kong, A. C.

R. Logan, A. C. Kong, and J. P. Krise, “Time-Dependent Effects of Hydrophobic Amine-Containing Drugs on Lysosome Structure and Biogenesis in Cultured Human Fibroblasts,” J. Pharm. Sci. 103(10), 3287–3296 (2014).
[Crossref] [PubMed]

Kress, A.

C. A. Valades Cruz, H. A. Shaban, A. Kress, N. Bertaux, S. Monneret, M. Mavrakis, J. Savatier, and S. Brasselet, “Quantitative nanoscale imaging of orientational order in biological filaments by polarized superresolution microscopy,” Proc. Natl. Acad. Sci. U.S.A. 113(7), E820–E828 (2016).
[Crossref] [PubMed]

Krise, J. P.

R. Logan, A. C. Kong, and J. P. Krise, “Time-Dependent Effects of Hydrophobic Amine-Containing Drugs on Lysosome Structure and Biogenesis in Cultured Human Fibroblasts,” J. Pharm. Sci. 103(10), 3287–3296 (2014).
[Crossref] [PubMed]

R. S. Funk and J. P. Krise, “Cationic amphiphilic drugs cause a marked expansion of apparent lysosomal volume: implications for an intracellular distribution-based drug interaction,” Mol. Pharm. 9(5), 1384–1395 (2012).
[PubMed]

Larsen, S. D.

K. A. Min, W. G. Rajeswaran, R. Oldenbourg, G. Harris, R. K. Keswani, M. Chiang, P. Rzeczycki, A. Talattof, M. Hafeez, R. W. Horobin, S. D. Larsen, K. A. Stringer, and G. R. Rosania, “Massive Bioaccumulation and Self-Assembly of Phenazine Compounds in Live Cells,” Adv Sci (Weinh) 2(8), 1500025 (2015).
[Crossref] [PubMed]

Libby, P.

P. Libby, “Molecular and cellular mechanisms of the thrombotic complications of atherosclerosis,” J. Lipid Res. 50(Suppl), S352–S357 (2008).
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Lin, C. P.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular Order of Arterial Collagen Using Circular Polarization Second-Harmonic Generation Imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref] [PubMed]

Linthorst, G. E.

M. Biegstraaten, G. E. Linthorst, I. N. van Schaik, and C. E. M. Hollak, “Fabry Disease: a Rare Cause of Neuropathic Pain,” Curr. Pain Headache Rep. 17(10), 365 (2013).
[Crossref] [PubMed]

Liu, L.

P. A. A. S. Navarro, L. Liu, J. R. Trimarchi, R. A. Ferriani, and D. L. Keefe, “Noninvasive imaging of spindle dynamics during mammalian oocyte activation,” Fertil. Steril. 83(4Suppl 1), 1197–1205 (2005).
[Crossref] [PubMed]

L. Liu, R. Oldenbourg, J. R. Trimarchi, and D. L. Keefe, “A reliable, noninvasive technique for spindle imaging and enucleation of mammalian oocytes,” Nat. Biotechnol. 18(2), 223–225 (2000).
[Crossref] [PubMed]

Logan, R.

R. Logan, A. C. Kong, and J. P. Krise, “Time-Dependent Effects of Hydrophobic Amine-Containing Drugs on Lysosome Structure and Biogenesis in Cultured Human Fibroblasts,” J. Pharm. Sci. 103(10), 3287–3296 (2014).
[Crossref] [PubMed]

Loose, L. D.

L. D. Loose, J. B. Silkworth, T. Charbonneau, and F. Blumenstock, “Environmental chemical-induced macrophage dysfunction,” Environ. Health Perspect. 39, 79–91 (1981).
[Crossref] [PubMed]

Maestre, M. F.

W. Mickols, M. F. Maestre, I. Tinoco, and S. H. Embury, “Visualization of oriented hemoglobin S in individual erythrocytes by differential extinction of polarized light,” Proc. Natl. Acad. Sci. U.S.A. 82(19), 6527–6531 (1985).
[Crossref] [PubMed]

Maezawa, I.

W. Kaminksy, L.-W. Jin, S. Powell, I. Maezawa, K. Claborn, C. Branham, and B. Kahr, “Polarimetric imaging of amyloid,” Micron 37(4), 324–338 (2006).
[Crossref] [PubMed]

Magalhaes, P. J.

M. D. Abramoff, P. J. Magalhaes, and S. J. Ram, “Image Processing With ImageJ,” Biophoton. Int. 11, 36–42 (2004).

Mane, G.

J. Baik, K. A. Stringer, G. Mane, and G. R. Rosania, “Multiscale Distribution and Bioaccumulation Analysis of Clofazimine Reveals a Massive Immune System-Mediated Xenobiotic Sequestration Response,” Antimicrob. Agents Chemother. 57(3), 1218–1230 (2013).
[Crossref] [PubMed]

Massoumian, F.

F. Massoumian, R. Juskaitis, M. A. A. Neil, and T. Wilson, “Quantitative polarized light microscopy,” J. Microsc. 209(1), 13–22 (2003).
[Crossref] [PubMed]

Mattson, J. M.

R. Turcotte, J. M. Mattson, J. W. Wu, Y. Zhang, and C. P. Lin, “Molecular Order of Arterial Collagen Using Circular Polarization Second-Harmonic Generation Imaging,” Biophys. J. 110(3), 530–533 (2016).
[Crossref] [PubMed]

Mavrakis, M.

C. A. Valades Cruz, H. A. Shaban, A. Kress, N. Bertaux, S. Monneret, M. Mavrakis, J. Savatier, and S. Brasselet, “Quantitative nanoscale imaging of orientational order in biological filaments by polarized superresolution microscopy,” Proc. Natl. Acad. Sci. U.S.A. 113(7), E820–E828 (2016).
[Crossref] [PubMed]

Mehta, S. B.

S. B. Mehta, M. Shribak, and R. Oldenbourg, “Polarized light imaging of birefringence and diattenuation at high resolution and high sensitivity,” J. Opt. 15(9), 094007 (2013).
[Crossref] [PubMed]

Mello, M. L. S.

B. C. Vidal, E. H. M. Dos Anjos, and M. L. S. Mello, “Optical anisotropy reveals molecular order in a mouse enthesis,” Cell Tissue Res. 362(1), 177–185 (2015).
[Crossref] [PubMed]

Meseroll, R. A.

B. S. DeMay, X. Bai, L. Howard, P. Occhipinti, R. A. Meseroll, E. T. Spiliotis, R. Oldenbourg, and A. S. Gladfelter, “Septin filaments exhibit a dynamic, paired organization that is conserved from yeast to mammals,” J. Cell Biol. 193(6), 1065–1081 (2011).
[Crossref] [PubMed]

Mickols, W.

W. Mickols, M. F. Maestre, I. Tinoco, and S. H. Embury, “Visualization of oriented hemoglobin S in individual erythrocytes by differential extinction of polarized light,” Proc. Natl. Acad. Sci. U.S.A. 82(19), 6527–6531 (1985).
[Crossref] [PubMed]

Min, K. A.

K. A. Min, W. G. Rajeswaran, R. Oldenbourg, G. Harris, R. K. Keswani, M. Chiang, P. Rzeczycki, A. Talattof, M. Hafeez, R. W. Horobin, S. D. Larsen, K. A. Stringer, and G. R. Rosania, “Massive Bioaccumulation and Self-Assembly of Phenazine Compounds in Live Cells,” Adv Sci (Weinh) 2(8), 1500025 (2015).
[Crossref] [PubMed]

Mitalipov, S. M.

J. A. Byrne, D. A. Pedersen, L. L. Clepper, M. Nelson, W. G. Sanger, S. Gokhale, D. P. Wolf, and S. M. Mitalipov, “Producing primate embryonic stem cells by somatic cell nuclear transfer,” Nature 450(7169), 497–502 (2007).
[Crossref] [PubMed]

Molano, J. R.

J. R. Molano and V. Molano, “Dementia with Lewy bodies,” Semin. Neurol. 33(4), 330–335 (2013).
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Molano, V.

J. R. Molano and V. Molano, “Dementia with Lewy bodies,” Semin. Neurol. 33(4), 330–335 (2013).
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Monneret, S.

C. A. Valades Cruz, H. A. Shaban, A. Kress, N. Bertaux, S. Monneret, M. Mavrakis, J. Savatier, and S. Brasselet, “Quantitative nanoscale imaging of orientational order in biological filaments by polarized superresolution microscopy,” Proc. Natl. Acad. Sci. U.S.A. 113(7), E820–E828 (2016).
[Crossref] [PubMed]

Mori, S.

H. Z. Amin, S. Mori, N. Sasaki, and K. Hirata, “Diagnostic Approach to Cardiac Amyloidosis,” Kobe J. Med. Sci. 60(1), E5–E11 (2014).
[PubMed]

Mungthin, M.

S. R. Hawley, P. G. Bray, M. Mungthin, J. D. Atkinson, P. M. O’Neill, and S. A. Ward, “Relationship between antimalarial drug activity, accumulation, and inhibition of heme polymerization in Plasmodium falciparum in vitro,” Antimicrob. Agents Chemother. 42(3), 682–686 (1998).
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G. S. Yoon, S. Sud, R. K. Keswani, J. Baik, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Phagocytosed Clofazimine Biocrystals Can Modulate Innate Immune Signaling by Inhibiting TNFα and Boosting IL-1RA Secretion,” Mol. Pharm. 12(7), 2517–2527 (2015).
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R. Keswani, G. Yoon, S. Sud, K. Stringer, and G. Rosania, “A Far-Red Fluorescent Probe For Flow Cytometric Xenobiotic-Sequestering Cell Functional Studies,” Cytometry A 87(9), 855–867 (2015).
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G. S. Yoon, R. K. Keswani, S. Sud, P. M. Rzeczycki, M. D. Murashov, T. A. Koehn, T. J. Standiford, K. A. Stringer, and G. R. Rosania, “Clofazimine Biocrystal Accumulation in Macrophages Upregulates IL-1RA Production to Induce a Systemic Anti-Inflammatory State,” Antimicrob. Agents Chemother. 60(6), 3470–3479 (2016).
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Figures (6)

Fig. 1
Fig. 1 Schematic diagram of multi-parameter instrument used for live alveolar macrophage diattenuation imaging at 623nm or 546nm wavelengths and fluorescence microscopy. Adapted from Mehta et al. 2013 Journal of Optics [4].
Fig. 2
Fig. 2 Calibration of the LC-PolScope instrumentation and software. A slide comprised of four sheets of perfectly polarized glass, with each sheet polarized to light at either 0°, 45°, 90°, or 135° relative to the horizontal is used for calibration. (A) Brightfield image, (B) mean transmittance and (C) diattenuation image map of the calibration slide. (D) Colored schematic representing the angle of high transmittance, or the orientation of light which is most transmitted by the object. (E) Images generated from passing linearly polarized light at 0°, 45°, 90°, and 135°, from left to right, which are used to calculate the angle of high transmittance, diattenuation, and mean transmittance image maps.
Fig. 3
Fig. 3 Representative schematic of mask generation for data collection. The 0-degree polarization state image is selected (Panel A) and has the brightness and contrast adjusted (Panel B). Following this, the image undergoes a manual threshold in ImageJ, delineating between objects and background (Panel C). The image then undergoes the “Fill Holes” function, generating the mask for data analysis (Panel D)
Fig. 4
Fig. 4 Pol-Scope images of CLDIs isolated from the spleen of 8wk CFZ-treated mice. (A) Brightfield image displaying deep red color, rod-like shape of CLDIs. (B) Diattenuation, (C) mean transmittance and (D) Cy5 fluorescence of CLDIs with illuminating light at 623 nm. The high degree of diattenuation and Cy5 fluorescence of the CLDIs is readily visible. Scale bar is 50 μm.
Fig. 5
Fig. 5 Comparison of CFZ treated and control alveolar macrophages. Macrophages from mice following 8 weeks of treatment, displayed the characteristic CLDI formation. Brightfield (A, B), diattenuation (C, D), mean transmittance (E, F), and Cy5 fluorescence (G,H) images of isolated alveolar macrophages from treated and non-treated (control) mice. Both diattenuation and mean transmittance images were generated using illuminating light at 623nm. Note that the diattenuation and mean transmittance signal is entirely contained within the CLDIs. Scale bar is 15 μm.
Fig. 6
Fig. 6 Scatter plot displaying relationship between Cy5 fluorescence, optical density, and dichroism in control alveolar macrophage populations (A, D) and 8 week CFZ fed alveolar macrophage populations (B,C). Panels A and B show the same population of cells shown in panels D and C, but zoomed into the lower signal values. Treatment with CFZ results in a heterogeneous population of macrophages on basis of optical signals, while untreated cells remain homogenous.

Tables (1)

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Table 1 Average Signal Intensity of Macrophages

Equations (8)

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D λ ( c )= ( x,y )p( c ) D λ ( x,y )
T m,λ ( c )= ( x,y )p( c ) T m,λ ( x,y )
F Cy5 ( c )= ( x,y )p( c ) F Cy5 ( x,y )
O D λ ( c )= ( x,y )p( c ) log10( T m,λ ( x,y ) )
O D λ ( c )= ( x,y )p( c ) log10( T m,λ ( x,y ) ) ( x,y )p( c ) log10( T M,λ (BG))
D ¯ λ ( c )= ( x,y )p( c ) D λ ( x,y ) A
O ¯ D ¯ λ ( c )= ( x,y )p( c ) log10( T m,λ ( x,y ) ) ( x,y )p( c ) log10( T M,λ (BG)) A
F ¯ Cy5 ( c )= ( x,y )p( c ) F Cy5 ( x,y ) A

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