Abstract

In this short communication, we demonstrate for the first time, the use of far red fluorescent gene reporter, iRFP to longitudinally and non-invasively track the in vivo process of lymphatic metastases from an orthotopic site of mammary implantation through lymphatic vessels and to draining lymph nodes. Potentially useful to accelerate cancer drug discovery as an in vivo screening tool to monitor the pharmacological arrest of metastasis, we show that the custom as well as commercial small animal imaging devices have adequate performance to detect the gene reporter in stably expressing metastatic cancer cells.

© 2015 Optical Society of America

Full Article  |  PDF Article
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  1. M. Saxena and G. Christofori, “Rebuilding cancer metastasis in the mouse,” Mol. Oncol. 7(2), 283–296 (2013).
    [Crossref] [PubMed]
  2. U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
    [Crossref] [PubMed]
  3. G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, and V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
    [Crossref] [PubMed]
  4. M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
    [Crossref] [PubMed]
  5. B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
    [Crossref] [PubMed]
  6. B. Zhu, J. C. Rasmussen, and E. M. Sevick-Muraca, “A matter of collection and detection for intraoperative and noninvasive near-infrared fluorescence molecular imaging: to see or not to see?” Med. Phys. 41(2), 022105 (2014).
    [Crossref] [PubMed]
  7. B. Zhu and E. M. Sevick-Muraca, “A review of performance of near-infrared fluorescence imaging devices used in clinical studies,” Br. J. Radiol. 88(1045), 20140547 (2015).
    [Crossref] [PubMed]
  8. D. M. Shcherbakova, M. Baloban, and V. V. Verkhusha, “Near-infrared fluorescent proteins engineered from bacterial phytochromes,” Curr. Opin. Chem. Biol. 27, 52–63 (2015).
    [Crossref] [PubMed]
  9. E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
    [Crossref] [PubMed]
  10. N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
    [Crossref] [PubMed]
  11. G. D. Agollah, G. Wu, E. M. Sevick-Muraca, and S. Kwon, “In Vivo Lymphatic Imaging of a Human Inflammatory Breast Cancer Model,” J. Cancer 5(9), 774–783 (2014).
    [Crossref] [PubMed]

2015 (3)

B. Zhu and E. M. Sevick-Muraca, “A review of performance of near-infrared fluorescence imaging devices used in clinical studies,” Br. J. Radiol. 88(1045), 20140547 (2015).
[Crossref] [PubMed]

D. M. Shcherbakova, M. Baloban, and V. V. Verkhusha, “Near-infrared fluorescent proteins engineered from bacterial phytochromes,” Curr. Opin. Chem. Biol. 27, 52–63 (2015).
[Crossref] [PubMed]

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

2014 (3)

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

G. D. Agollah, G. Wu, E. M. Sevick-Muraca, and S. Kwon, “In Vivo Lymphatic Imaging of a Human Inflammatory Breast Cancer Model,” J. Cancer 5(9), 774–783 (2014).
[Crossref] [PubMed]

B. Zhu, J. C. Rasmussen, and E. M. Sevick-Muraca, “A matter of collection and detection for intraoperative and noninvasive near-infrared fluorescence molecular imaging: to see or not to see?” Med. Phys. 41(2), 022105 (2014).
[Crossref] [PubMed]

2013 (3)

M. Saxena and G. Christofori, “Rebuilding cancer metastasis in the mouse,” Mol. Oncol. 7(2), 283–296 (2013).
[Crossref] [PubMed]

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

2012 (1)

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

2011 (1)

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, and V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[Crossref] [PubMed]

Agollah, G. D.

G. D. Agollah, G. Wu, E. M. Sevick-Muraca, and S. Kwon, “In Vivo Lymphatic Imaging of a Human Inflammatory Breast Cancer Model,” J. Cancer 5(9), 774–783 (2014).
[Crossref] [PubMed]

Ale, A.

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

Álvarez-Velilla, R.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Azhdarinia, A.

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

Balaña-Fouce, R.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Baloban, M.

D. M. Shcherbakova, M. Baloban, and V. V. Verkhusha, “Near-infrared fluorescent proteins engineered from bacterial phytochromes,” Curr. Opin. Chem. Biol. 27, 52–63 (2015).
[Crossref] [PubMed]

Barry, S. T.

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Blakey, D. C.

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Burton, N. C.

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

Calvo-Álvarez, E.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Chan, W.

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

Christofori, G.

M. Saxena and G. Christofori, “Rebuilding cancer metastasis in the mouse,” Mol. Oncol. 7(2), 283–296 (2013).
[Crossref] [PubMed]

Deliolanis, N. C.

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

Escudero-Martínez, J. M.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Farokhzad, O. C.

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Filonov, G. S.

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, and V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[Crossref] [PubMed]

Fresno, M.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Gabizon, A.

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Ghosh, S. C.

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

Grodzinski, P.

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Hall, M. A.

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

Harvey, B. R.

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

Jain, R. K.

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Kim, K.

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, and V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[Crossref] [PubMed]

Kwon, S.

G. D. Agollah, G. Wu, E. M. Sevick-Muraca, and S. Kwon, “In Vivo Lymphatic Imaging of a Human Inflammatory Breast Cancer Model,” J. Cancer 5(9), 774–783 (2014).
[Crossref] [PubMed]

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

Lachance, P. A.

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

Maeda, H.

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Morscher, S.

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

Ntziachristos, V.

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

Pérez-Pertejo, Y.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Piatkevich, K. D.

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, and V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[Crossref] [PubMed]

Pinkston, K. L.

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

Prabhakar, U.

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Price, R. E.

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

Punzón, C.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Radrich, K.

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

Ranganathan, R.

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

Rasmussen, J. C.

B. Zhu, J. C. Rasmussen, and E. M. Sevick-Muraca, “A matter of collection and detection for intraoperative and noninvasive near-infrared fluorescence molecular imaging: to see or not to see?” Med. Phys. 41(2), 022105 (2014).
[Crossref] [PubMed]

Razansky, D.

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

Reguera, R. M.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Robinson, H.

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

Saxena, M.

M. Saxena and G. Christofori, “Rebuilding cancer metastasis in the mouse,” Mol. Oncol. 7(2), 283–296 (2013).
[Crossref] [PubMed]

Schaefer, K.

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

Sevick-Muraca, E. M.

B. Zhu and E. M. Sevick-Muraca, “A review of performance of near-infrared fluorescence imaging devices used in clinical studies,” Br. J. Radiol. 88(1045), 20140547 (2015).
[Crossref] [PubMed]

B. Zhu, J. C. Rasmussen, and E. M. Sevick-Muraca, “A matter of collection and detection for intraoperative and noninvasive near-infrared fluorescence molecular imaging: to see or not to see?” Med. Phys. 41(2), 022105 (2014).
[Crossref] [PubMed]

G. D. Agollah, G. Wu, E. M. Sevick-Muraca, and S. Kwon, “In Vivo Lymphatic Imaging of a Human Inflammatory Breast Cancer Model,” J. Cancer 5(9), 774–783 (2014).
[Crossref] [PubMed]

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

Shcherbakova, D. M.

D. M. Shcherbakova, M. Baloban, and V. V. Verkhusha, “Near-infrared fluorescent proteins engineered from bacterial phytochromes,” Curr. Opin. Chem. Biol. 27, 52–63 (2015).
[Crossref] [PubMed]

Stamatakis, K.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Tejería, A.

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Ting, L.-M.

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, and V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[Crossref] [PubMed]

Verkhusha, V. V.

D. M. Shcherbakova, M. Baloban, and V. V. Verkhusha, “Near-infrared fluorescent proteins engineered from bacterial phytochromes,” Curr. Opin. Chem. Biol. 27, 52–63 (2015).
[Crossref] [PubMed]

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, and V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[Crossref] [PubMed]

Wilganowski, N.

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

Wu, G.

G. D. Agollah, G. Wu, E. M. Sevick-Muraca, and S. Kwon, “In Vivo Lymphatic Imaging of a Human Inflammatory Breast Cancer Model,” J. Cancer 5(9), 774–783 (2014).
[Crossref] [PubMed]

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

Zamboni, W.

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Zhang, J.

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, and V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[Crossref] [PubMed]

Zhu, B.

B. Zhu and E. M. Sevick-Muraca, “A review of performance of near-infrared fluorescence imaging devices used in clinical studies,” Br. J. Radiol. 88(1045), 20140547 (2015).
[Crossref] [PubMed]

B. Zhu, J. C. Rasmussen, and E. M. Sevick-Muraca, “A matter of collection and detection for intraoperative and noninvasive near-infrared fluorescence molecular imaging: to see or not to see?” Med. Phys. 41(2), 022105 (2014).
[Crossref] [PubMed]

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

Br. J. Radiol. (1)

B. Zhu and E. M. Sevick-Muraca, “A review of performance of near-infrared fluorescence imaging devices used in clinical studies,” Br. J. Radiol. 88(1045), 20140547 (2015).
[Crossref] [PubMed]

Cancer Res. (1)

U. Prabhakar, H. Maeda, R. K. Jain, E. M. Sevick-Muraca, W. Zamboni, O. C. Farokhzad, S. T. Barry, A. Gabizon, P. Grodzinski, and D. C. Blakey, “Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology,” Cancer Res. 73(8), 2412–2417 (2013).
[Crossref] [PubMed]

Curr. Opin. Chem. Biol. (1)

D. M. Shcherbakova, M. Baloban, and V. V. Verkhusha, “Near-infrared fluorescent proteins engineered from bacterial phytochromes,” Curr. Opin. Chem. Biol. 27, 52–63 (2015).
[Crossref] [PubMed]

J. Cancer (1)

G. D. Agollah, G. Wu, E. M. Sevick-Muraca, and S. Kwon, “In Vivo Lymphatic Imaging of a Human Inflammatory Breast Cancer Model,” J. Cancer 5(9), 774–783 (2014).
[Crossref] [PubMed]

Med. Phys. (1)

B. Zhu, J. C. Rasmussen, and E. M. Sevick-Muraca, “A matter of collection and detection for intraoperative and noninvasive near-infrared fluorescence molecular imaging: to see or not to see?” Med. Phys. 41(2), 022105 (2014).
[Crossref] [PubMed]

Mol. Imaging Biol. (2)

N. C. Deliolanis, A. Ale, S. Morscher, N. C. Burton, K. Schaefer, K. Radrich, D. Razansky, and V. Ntziachristos, “Deep-tissue reporter-gene imaging with fluorescence and optoacoustic tomography: a performance overview,” Mol. Imaging Biol. 16(5), 652–660 (2014).
[Crossref] [PubMed]

B. Zhu, G. Wu, H. Robinson, N. Wilganowski, M. A. Hall, S. C. Ghosh, K. L. Pinkston, A. Azhdarinia, B. R. Harvey, and E. M. Sevick-Muraca, “Tumor margin detection using quantitative NIRF molecular imaging targeting EpCAM validated by far red gene reporter iRFP,” Mol. Imaging Biol. 15(5), 560–568 (2013).
[Crossref] [PubMed]

Mol. Oncol. (1)

M. Saxena and G. Christofori, “Rebuilding cancer metastasis in the mouse,” Mol. Oncol. 7(2), 283–296 (2013).
[Crossref] [PubMed]

Nat. Biotechnol. (1)

G. S. Filonov, K. D. Piatkevich, L.-M. Ting, J. Zhang, K. Kim, and V. V. Verkhusha, “Bright and stable near-infrared fluorescent protein for in vivo imaging,” Nat. Biotechnol. 29(8), 757–761 (2011).
[Crossref] [PubMed]

PLoS Negl. Trop. Dis. (1)

E. Calvo-Álvarez, K. Stamatakis, C. Punzón, R. Álvarez-Velilla, A. Tejería, J. M. Escudero-Martínez, Y. Pérez-Pertejo, M. Fresno, R. Balaña-Fouce, and R. M. Reguera, “Infrared Fluorescent Imaging as a Potent Tool for In Vitro, Ex Vivo and In Vivo Models of Visceral Leishmaniasis,” PLoS Negl. Trop. Dis. 9(3), e0003666 (2015).
[Crossref] [PubMed]

Prostate (1)

M. A. Hall, S. Kwon, H. Robinson, P. A. Lachance, A. Azhdarinia, R. Ranganathan, R. E. Price, W. Chan, and E. M. Sevick-Muraca, “Imaging prostate cancer lymph node metastases with a multimodality contrast agent,” Prostate 72(2), 129–146 (2012).
[Crossref] [PubMed]

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Figures (3)

Fig. 1
Fig. 1 Rows 1-4, iRFP fluorescence imaging (units in AU camera output) of animals 4 – 7 weeks after orthotopic implantation in right lower mammary gland showing primary tumor in ventral view (column 1, week 4 only); ventral view with primary tumor covered (column 2) showing lymphatic channels (arrows); lateral right view (Column 3, week 7 only) showing axillary lymph node (arrow); and left lateral view (column 4, week 7 only) showing faint lymphatic vessel (arrow). Images were collected using EMCCD camera system.
Fig. 2
Fig. 2 H&E staining showing the tumor cells (left, arrows) in the lymphovascular spaces and the residual lymphocytes and clusters of metastatic carcinoma (right, arrows) in the metastatic lymph node seven weeks after orthotopic implantation. All images were taken at 200X magnification and scale bars represent 50 μm.
Fig. 3
Fig. 3 Measured signal-to-noise ratio versus contrast measured on QDots 800 based fluorescent solid working standard using ICCD (open circles), EMCCD (filled triangles), and IVIS (open diamonds). Symbols denote a single measurement on the working standard.

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