Abstract

The development of prognostic indicators of breast cancer metastatic risk could reduce the number of patients receiving chemotherapy for tumors with low metastatic potential. Recent evidence points to a critical role for cell metabolism in driving breast cancer metastasis. Endogenous fluorescence intensity of nicotinamide adenine dinucleotide (NADH) and flavin adenine dinucleotide (FAD) can provide a label-free method for assessing cell metabolism. We report the optical redox ratio of FAD/(FAD + NADH) of four isogenic triple-negative breast cancer cell lines with varying metastatic potential. Under normoxic conditions, the redox ratio increases with increasing metastatic potential (168FARN>4T07>4T1), indicating a shift to more oxidative metabolism in cells capable of metastasis. Reoxygenation following acute hypoxia increased the redox ratio by 43 ± 9% and 33 ± 4% in the 4T1 and 4T07 cells, respectively; in contrast, the redox ratio decreased 14 ± 7% in the non-metastatic 67NR cell line. These results demonstrate that the optical redox ratio is sensitive to the metabolic adaptability of breast cancer cells with high metastatic potential and could potentially be used to measure dynamic functional changes that are indicative of invasive or metastatic potential.

© 2016 Optical Society of America

Full Article  |  PDF Article
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References

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2016 (4)

N. L. Henry, M. R. Somerfield, V. G. Abramson, K. H. Allison, C. K. Anders, D. T. Chingos, A. Hurria, T. H. Openshaw, and I. E. Krop, “Role of Patient and Disease Factors in Adjuvant Systemic Therapy Decision Making for Early-Stage, Operable Breast Cancer: American Society of Clinical Oncology Endorsement of Cancer Care Ontario Guideline Recommendations,” J. Clin. Oncol. 34(19), 2303–2311 (2016).
[Crossref] [PubMed]

J. Hou, H. J. Wright, N. Chan, R. Tran, O. V. Razorenova, E. O. Potma, and B. J. Tromberg, “Correlating two-photon excited fluorescence imaging of breast cancer cellular redox state with seahorse flux analysis of normalized cellular oxygen consumption,” J. Biomed. Opt. 21(6), 060503 (2016).
[Crossref] [PubMed]

A. J. Walsh, J. A. Castellanos, N. S. Nagathihalli, N. B. Merchant, and M. C. Skala, “Optical Imaging of Drug-Induced Metabolism Changes in Murine and Human Pancreatic Cancer Organoids Reveals Heterogeneous Drug Response,” Pancreas 45(6), 863–869 (2016).
[PubMed]

C. Lehuédé, F. Dupuy, R. Rabinovitch, R. G. Jones, and P. M. Siegel, “Metabolic Plasticity as a Determinant of Tumor Growth and Metastasis,” Cancer Res. 76(18), 5201–5208 (2016).
[Crossref] [PubMed]

2015 (3)

A. J. Walsh and M. C. Skala, “Optical metabolic imaging quantifies heterogeneous cell populations,” Biomed. Opt. Express 6(2), 559–573 (2015).
[Crossref] [PubMed]

R. V. Simões, I. S. Serganova, N. Kruchevsky, A. Leftin, A. A. Shestov, H. T. Thaler, G. Sukenick, J. W. Locasale, R. G. Blasberg, J. A. Koutcher, and E. Ackerstaff, “Metabolic plasticity of metastatic breast cancer cells: adaptation to changes in the microenvironment,” Neoplasia 17(8), 671–684 (2015).
[Crossref] [PubMed]

F. Dupuy, S. Tabariès, S. Andrzejewski, Z. Dong, J. Blagih, M. G. Annis, A. Omeroglu, D. Gao, S. Leung, E. Amir, M. Clemons, A. Aguilar-Mahecha, M. Basik, E. E. Vincent, J. St-Pierre, R. G. Jones, and P. M. Siegel, “PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer,” Cell Metab. 22(4), 577–589 (2015).
[Crossref] [PubMed]

2014 (6)

A. T. Shah, M. Demory Beckler, A. J. Walsh, W. P. Jones, P. R. Pohlmann, and M. C. Skala, “Optical Metabolic Imaging of Treatment Response in Human Head and Neck Squamous Cell Carcinoma,” PLoS One 9(3), e90746 (2014).
[Crossref] [PubMed]

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative Optical Imaging of Primary Tumor Organoid Metabolism Predicts Drug Response in Breast Cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

P. E. Porporato, V. L. Payen, J. Pérez-Escuredo, C. J. De Saedeleer, P. Danhier, T. Copetti, S. Dhup, M. Tardy, T. Vazeille, C. Bouzin, O. Feron, C. Michiels, B. Gallez, and P. Sonveaux, “A Mitochondrial Switch Promotes Tumor Metastasis,” Cell Reports 8(3), 754–766 (2014).
[Crossref] [PubMed]

V. S. LeBleu, J. T. O’Connell, K. N. Gonzalez Herrera, H. Wikman, K. Pantel, M. C. Haigis, F. M. de Carvalho, A. Damascena, L. T. Domingos Chinen, R. M. Rocha, J. M. Asara, and R. Kalluri, “PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis,” Nat. Cell Biol. 16(10), 992–1003 (2014).
[Crossref] [PubMed]

R. Boidot, S. Branders, T. Helleputte, L. I. Rubio, P. Dupont, and O. Feron, “A generic cycling hypoxia-derived prognostic gene signature: application to breast cancer profiling,” Oncotarget 5(16), 6947–6963 (2014).
[Crossref] [PubMed]

A. Varone, J. Xylas, K. P. Quinn, D. Pouli, G. Sridharan, M. E. McLaughlin-Drubin, C. Alonzo, K. Lee, K. Münger, and I. Georgakoudi, “Endogenous Two-Photon Fluorescence Imaging Elucidates Metabolic Changes Related to Enhanced Glycolysis and Glutamine Consumption in Precancerous Epithelial Tissues,” Cancer Res. 74(11), 3067–3075 (2014).
[Crossref] [PubMed]

2013 (2)

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical Metabolic Imaging Identifies Glycolytic Levels, Subtypes, and Early-Treatment Response in Breast Cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

K. P. Quinn, G. V. Sridharan, R. S. Hayden, D. L. Kaplan, K. Lee, and I. Georgakoudi, “Quantitative metabolic imaging using endogenous fluorescence to detect stem cell differentiation,” Sci. Rep. 3, 3432 (2013).
[Crossref] [PubMed]

2012 (4)

K. P. Quinn, E. Bellas, N. Fourligas, K. Lee, D. L. Kaplan, and I. Georgakoudi, “Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios,” Biomaterials 33(21), 5341–5348 (2012).
[Crossref] [PubMed]

R. Peto, C. Davies, J. Godwin, R. Gray, H. C. Pan, M. Clarke, D. Cutter, S. Darby, P. McGale, C. Taylor, Y. C. Wang, J. Bergh, A. Di Leo, K. Albain, S. Swain, M. Piccart, K. Pritchard, and Early Breast Cancer Trialists’ Collaborative Group (EBCTCG), “Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials,” Lancet 379(9814), 432–444 (2012).
[Crossref] [PubMed]

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

A. Walsh, R. S. Cook, B. Rexer, C. L. Arteaga, and M. C. Skala, “Optical imaging of metabolism in HER2 overexpressing breast cancer cells,” Biomed. Opt. Express 3(1), 75–85 (2012).
[Crossref] [PubMed]

2011 (2)

B. P. Dranka, G. A. Benavides, A. R. Diers, S. Giordano, B. R. Zelickson, C. Reily, L. Zou, J. C. Chatham, B. G. Hill, J. Zhang, A. Landar, and V. M. Darley-Usmar, “Assessing bioenergetic function in response to oxidative stress by metabolic profiling,” Free Radic. Biol. Med. 51(9), 1621–1635 (2011).
[Crossref] [PubMed]

Y. Dai, K. Bae, and D. W. Siemann, “Impact of hypoxia on the metastatic potential of human prostate cancer cells,” Int. J. Radiat. Oncol. Biol. Phys. 81(2), 521–528 (2011).
[Crossref] [PubMed]

2010 (4)

E. Louie, S. Nik, J. S. Chen, M. Schmidt, B. Song, C. Pacson, X. F. Chen, S. Park, J. Ju, and E. I. Chen, “Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation,” Breast Cancer Res. 12(6), R94 (2010).
[Crossref] [PubMed]

X. Lu, B. Bennet, E. Mu, J. Rabinowitz, and Y. Kang, “Metabolomic changes accompanying transformation and acquisition of metastatic potential in a syngeneic mouse mammary tumor model,” J. Biol. Chem. 285(13), 9317–9321 (2010).
[Crossref] [PubMed]

H. N. Xu, S. Nioka, J. D. Glickson, B. Chance, and L. Z. Li, “Quantitative mitochondrial redox imaging of breast cancer metastatic potential,” J. Biomed. Opt. 15, 036010 (2010).

J. H. Ostrander, C. M. McMahon, S. Lem, S. R. Millon, J. Q. Brown, V. L. Seewaldt, and N. Ramanujam, “Optical Redox Ratio Differentiates Breast Cancer Cell Lines Based on Estrogen Receptor Status,” Cancer Res. 70(11), 4759–4766 (2010).
[Crossref] [PubMed]

2009 (2)

C. Ruckenstuhl, S. Büttner, D. Carmona-Gutierrez, T. Eisenberg, G. Kroemer, S. J. Sigrist, K.-U. Fröhlich, and F. Madeo, “The Warburg Effect Suppresses Oxidative Stress Induced Apoptosis in a Yeast Model for Cancer,” PLoS One 4(2), e4592 (2009).
[Crossref] [PubMed]

L. Z. Li, R. Zhou, H. N. Xu, L. Moon, T. Zhong, E. J. Kim, H. Qiao, R. Reddy, D. Leeper, B. Chance, and J. D. Glickson, “Quantitative magnetic resonance and optical imaging biomarkers of melanoma metastatic potential,” Proc. Natl. Acad. Sci. U.S.A. 106(16), 6608–6613 (2009).
[Crossref] [PubMed]

2007 (2)

M. Cronin, C. Sangli, M.-L. Liu, M. Pho, D. Dutta, A. Nguyen, J. Jeong, J. Wu, K. C. Langone, and D. Watson, “Analytical Validation of the Oncotype DX Genomic Diagnostic Test for Recurrence Prognosis and Therapeutic Response Prediction in Node-Negative, Estrogen Receptor-Positive Breast Cancer,” Clin. Chem. 53(6), 1084–1091 (2007).
[Crossref] [PubMed]

M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

2006 (1)

J. Lanzen, R. D. Braun, B. Klitzman, D. Brizel, T. W. Secomb, and M. W. Dewhirst, “Direct demonstration of instabilities in oxygen concentrations within the extravascular compartment of an experimental tumor,” Cancer Res. 66(4), 2219–2223 (2006).
[Crossref] [PubMed]

2005 (1)

M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Res. 65(4), 1180–1186 (2005).
[Crossref] [PubMed]

2004 (2)

R. A. Cairns and R. P. Hill, “Acute hypoxia enhances spontaneous lymph node metastasis in an orthotopic murine model of human cervical carcinoma,” Cancer Res. 64(6), 2054–2061 (2004).
[Crossref] [PubMed]

J. Yang, S. A. Mani, J. L. Donaher, S. Ramaswamy, R. A. Itzykson, C. Come, P. Savagner, I. Gitelman, A. Richardson, and R. A. Weinberg, “Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis,” Cell 117(7), 927–939 (2004).
[Crossref] [PubMed]

2003 (1)

X. Lin, F. Zhang, C. M. Bradbury, A. Kaushal, L. Li, D. R. Spitz, R. L. Aft, and D. Gius, “2-Deoxy-D-glucose-induced cytotoxicity and radiosensitization in tumor cells is mediated via disruptions in thiol metabolism,” Cancer Res. 63(12), 3413–3417 (2003).
[PubMed]

2001 (3)

R. A. Cairns, T. Kalliomaki, and R. P. Hill, “Acute (cyclic) hypoxia enhances spontaneous metastasis of KHT murine tumors,” Cancer Res. 61(24), 8903–8908 (2001).
[PubMed]

R. Drezek, C. Brookner, I. Pavlova, I. Boiko, A. Malpica, R. Lotan, M. Follen, and R. Richards-Kortum, “Autofluorescence Microscopy of Fresh Cervical-Tissue Sections Reveals Alterations in Tissue Biochemistry with Dysplasia,” Photochem. Photobiol. 73(6), 636–641 (2001).
[Crossref] [PubMed]

N. Ramanujam, R. Richards-Kortum, S. Thomsen, A. Mahadevan-Jansen, M. Follen, and B. Chance, “Low temperature fluorescence imaging of freeze-trapped human cervical tissues,” Opt. Express 8(6), 335–343 (2001).
[Crossref] [PubMed]

2000 (1)

C. Groussard, I. Morel, M. Chevanne, M. Monnier, J. Cillard, and A. Delamarche, “Free radical scavenging and antioxidant effects of lactate ion: an in vitro study,” J. Appl. Physiol. 89(1), 169–175 (2000).
[PubMed]

1996 (1)

H. Kimura, R. D. Braun, E. T. Ong, R. Hsu, T. W. Secomb, D. Papahadjopoulos, K. Hong, and M. W. Dewhirst, “Fluctuations in red cell flux in tumor microvessels can lead to transient hypoxia and reoxygenation in tumor parenchyma,” Cancer Res. 56(23), 5522–5528 (1996).
[PubMed]

1995 (1)

G. L. Wang, B. H. Jiang, E. A. Rue, and G. L. Semenza, “Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension,” Proc. Natl. Acad. Sci. U.S.A. 92(12), 5510–5514 (1995).
[Crossref] [PubMed]

1992 (1)

C. J. Aslakson and F. R. Miller, “Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor,” Cancer Res. 52(6), 1399–1405 (1992).
[PubMed]

1987 (1)

D. J. Chaplin, P. L. Olive, and R. E. Durand, “Intermittent blood flow in a murine tumor: radiobiological effects,” Cancer Res. 47(2), 597–601 (1987).
[PubMed]

1985 (1)

W. S. Kunz and W. Kunz, “Contribution of different enzymes to flavoprotein fluorescence of isolated rat liver mitochondria,” Biochimica et Biophysica Acta (BBA)- General Subjects 841(3), 237–246 (1985).
[Crossref]

1979 (1)

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

1962 (1)

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

Abramson, V. G.

N. L. Henry, M. R. Somerfield, V. G. Abramson, K. H. Allison, C. K. Anders, D. T. Chingos, A. Hurria, T. H. Openshaw, and I. E. Krop, “Role of Patient and Disease Factors in Adjuvant Systemic Therapy Decision Making for Early-Stage, Operable Breast Cancer: American Society of Clinical Oncology Endorsement of Cancer Care Ontario Guideline Recommendations,” J. Clin. Oncol. 34(19), 2303–2311 (2016).
[Crossref] [PubMed]

Ackerstaff, E.

R. V. Simões, I. S. Serganova, N. Kruchevsky, A. Leftin, A. A. Shestov, H. T. Thaler, G. Sukenick, J. W. Locasale, R. G. Blasberg, J. A. Koutcher, and E. Ackerstaff, “Metabolic plasticity of metastatic breast cancer cells: adaptation to changes in the microenvironment,” Neoplasia 17(8), 671–684 (2015).
[Crossref] [PubMed]

Aft, R. L.

X. Lin, F. Zhang, C. M. Bradbury, A. Kaushal, L. Li, D. R. Spitz, R. L. Aft, and D. Gius, “2-Deoxy-D-glucose-induced cytotoxicity and radiosensitization in tumor cells is mediated via disruptions in thiol metabolism,” Cancer Res. 63(12), 3413–3417 (2003).
[PubMed]

Aguilar-Mahecha, A.

F. Dupuy, S. Tabariès, S. Andrzejewski, Z. Dong, J. Blagih, M. G. Annis, A. Omeroglu, D. Gao, S. Leung, E. Amir, M. Clemons, A. Aguilar-Mahecha, M. Basik, E. E. Vincent, J. St-Pierre, R. G. Jones, and P. M. Siegel, “PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer,” Cell Metab. 22(4), 577–589 (2015).
[Crossref] [PubMed]

Albain, K.

R. Peto, C. Davies, J. Godwin, R. Gray, H. C. Pan, M. Clarke, D. Cutter, S. Darby, P. McGale, C. Taylor, Y. C. Wang, J. Bergh, A. Di Leo, K. Albain, S. Swain, M. Piccart, K. Pritchard, and Early Breast Cancer Trialists’ Collaborative Group (EBCTCG), “Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials,” Lancet 379(9814), 432–444 (2012).
[Crossref] [PubMed]

Allison, K. H.

N. L. Henry, M. R. Somerfield, V. G. Abramson, K. H. Allison, C. K. Anders, D. T. Chingos, A. Hurria, T. H. Openshaw, and I. E. Krop, “Role of Patient and Disease Factors in Adjuvant Systemic Therapy Decision Making for Early-Stage, Operable Breast Cancer: American Society of Clinical Oncology Endorsement of Cancer Care Ontario Guideline Recommendations,” J. Clin. Oncol. 34(19), 2303–2311 (2016).
[Crossref] [PubMed]

Alonzo, C.

A. Varone, J. Xylas, K. P. Quinn, D. Pouli, G. Sridharan, M. E. McLaughlin-Drubin, C. Alonzo, K. Lee, K. Münger, and I. Georgakoudi, “Endogenous Two-Photon Fluorescence Imaging Elucidates Metabolic Changes Related to Enhanced Glycolysis and Glutamine Consumption in Precancerous Epithelial Tissues,” Cancer Res. 74(11), 3067–3075 (2014).
[Crossref] [PubMed]

Amir, E.

F. Dupuy, S. Tabariès, S. Andrzejewski, Z. Dong, J. Blagih, M. G. Annis, A. Omeroglu, D. Gao, S. Leung, E. Amir, M. Clemons, A. Aguilar-Mahecha, M. Basik, E. E. Vincent, J. St-Pierre, R. G. Jones, and P. M. Siegel, “PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer,” Cell Metab. 22(4), 577–589 (2015).
[Crossref] [PubMed]

Anders, C. K.

N. L. Henry, M. R. Somerfield, V. G. Abramson, K. H. Allison, C. K. Anders, D. T. Chingos, A. Hurria, T. H. Openshaw, and I. E. Krop, “Role of Patient and Disease Factors in Adjuvant Systemic Therapy Decision Making for Early-Stage, Operable Breast Cancer: American Society of Clinical Oncology Endorsement of Cancer Care Ontario Guideline Recommendations,” J. Clin. Oncol. 34(19), 2303–2311 (2016).
[Crossref] [PubMed]

Andrzejewski, S.

F. Dupuy, S. Tabariès, S. Andrzejewski, Z. Dong, J. Blagih, M. G. Annis, A. Omeroglu, D. Gao, S. Leung, E. Amir, M. Clemons, A. Aguilar-Mahecha, M. Basik, E. E. Vincent, J. St-Pierre, R. G. Jones, and P. M. Siegel, “PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer,” Cell Metab. 22(4), 577–589 (2015).
[Crossref] [PubMed]

Annis, M. G.

F. Dupuy, S. Tabariès, S. Andrzejewski, Z. Dong, J. Blagih, M. G. Annis, A. Omeroglu, D. Gao, S. Leung, E. Amir, M. Clemons, A. Aguilar-Mahecha, M. Basik, E. E. Vincent, J. St-Pierre, R. G. Jones, and P. M. Siegel, “PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer,” Cell Metab. 22(4), 577–589 (2015).
[Crossref] [PubMed]

Arteaga, C. L.

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative Optical Imaging of Primary Tumor Organoid Metabolism Predicts Drug Response in Breast Cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical Metabolic Imaging Identifies Glycolytic Levels, Subtypes, and Early-Treatment Response in Breast Cancer,” Cancer Res. 73(20), 6164–6174 (2013).
[Crossref] [PubMed]

A. Walsh, R. S. Cook, B. Rexer, C. L. Arteaga, and M. C. Skala, “Optical imaging of metabolism in HER2 overexpressing breast cancer cells,” Biomed. Opt. Express 3(1), 75–85 (2012).
[Crossref] [PubMed]

Asara, J. M.

V. S. LeBleu, J. T. O’Connell, K. N. Gonzalez Herrera, H. Wikman, K. Pantel, M. C. Haigis, F. M. de Carvalho, A. Damascena, L. T. Domingos Chinen, R. M. Rocha, J. M. Asara, and R. Kalluri, “PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis,” Nat. Cell Biol. 16(10), 992–1003 (2014).
[Crossref] [PubMed]

Aslakson, C. J.

C. J. Aslakson and F. R. Miller, “Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor,” Cancer Res. 52(6), 1399–1405 (1992).
[PubMed]

Audi, S.

R. Sepehr, K. Staniszewski, S. Maleki, E. R. Jacobs, S. Audi, and M. Ranji, “Optical imaging of tissue mitochondrial redox state in intact rat lungs in two models of pulmonary oxidative stress,” J. Biomed. Opt. 17(4), 046010 (2012).
[Crossref] [PubMed]

Aurisicchio, L.

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative Optical Imaging of Primary Tumor Organoid Metabolism Predicts Drug Response in Breast Cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

Bae, K.

Y. Dai, K. Bae, and D. W. Siemann, “Impact of hypoxia on the metastatic potential of human prostate cancer cells,” Int. J. Radiat. Oncol. Biol. Phys. 81(2), 521–528 (2011).
[Crossref] [PubMed]

Basik, M.

F. Dupuy, S. Tabariès, S. Andrzejewski, Z. Dong, J. Blagih, M. G. Annis, A. Omeroglu, D. Gao, S. Leung, E. Amir, M. Clemons, A. Aguilar-Mahecha, M. Basik, E. E. Vincent, J. St-Pierre, R. G. Jones, and P. M. Siegel, “PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer,” Cell Metab. 22(4), 577–589 (2015).
[Crossref] [PubMed]

Bellas, E.

K. P. Quinn, E. Bellas, N. Fourligas, K. Lee, D. L. Kaplan, and I. Georgakoudi, “Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios,” Biomaterials 33(21), 5341–5348 (2012).
[Crossref] [PubMed]

Benavides, G. A.

B. P. Dranka, G. A. Benavides, A. R. Diers, S. Giordano, B. R. Zelickson, C. Reily, L. Zou, J. C. Chatham, B. G. Hill, J. Zhang, A. Landar, and V. M. Darley-Usmar, “Assessing bioenergetic function in response to oxidative stress by metabolic profiling,” Free Radic. Biol. Med. 51(9), 1621–1635 (2011).
[Crossref] [PubMed]

Bennet, B.

X. Lu, B. Bennet, E. Mu, J. Rabinowitz, and Y. Kang, “Metabolomic changes accompanying transformation and acquisition of metastatic potential in a syngeneic mouse mammary tumor model,” J. Biol. Chem. 285(13), 9317–9321 (2010).
[Crossref] [PubMed]

Bergh, J.

R. Peto, C. Davies, J. Godwin, R. Gray, H. C. Pan, M. Clarke, D. Cutter, S. Darby, P. McGale, C. Taylor, Y. C. Wang, J. Bergh, A. Di Leo, K. Albain, S. Swain, M. Piccart, K. Pritchard, and Early Breast Cancer Trialists’ Collaborative Group (EBCTCG), “Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials,” Lancet 379(9814), 432–444 (2012).
[Crossref] [PubMed]

Blagih, J.

F. Dupuy, S. Tabariès, S. Andrzejewski, Z. Dong, J. Blagih, M. G. Annis, A. Omeroglu, D. Gao, S. Leung, E. Amir, M. Clemons, A. Aguilar-Mahecha, M. Basik, E. E. Vincent, J. St-Pierre, R. G. Jones, and P. M. Siegel, “PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer,” Cell Metab. 22(4), 577–589 (2015).
[Crossref] [PubMed]

Blasberg, R. G.

R. V. Simões, I. S. Serganova, N. Kruchevsky, A. Leftin, A. A. Shestov, H. T. Thaler, G. Sukenick, J. W. Locasale, R. G. Blasberg, J. A. Koutcher, and E. Ackerstaff, “Metabolic plasticity of metastatic breast cancer cells: adaptation to changes in the microenvironment,” Neoplasia 17(8), 671–684 (2015).
[Crossref] [PubMed]

Boidot, R.

R. Boidot, S. Branders, T. Helleputte, L. I. Rubio, P. Dupont, and O. Feron, “A generic cycling hypoxia-derived prognostic gene signature: application to breast cancer profiling,” Oncotarget 5(16), 6947–6963 (2014).
[Crossref] [PubMed]

Boiko, I.

R. Drezek, C. Brookner, I. Pavlova, I. Boiko, A. Malpica, R. Lotan, M. Follen, and R. Richards-Kortum, “Autofluorescence Microscopy of Fresh Cervical-Tissue Sections Reveals Alterations in Tissue Biochemistry with Dysplasia,” Photochem. Photobiol. 73(6), 636–641 (2001).
[Crossref] [PubMed]

Bouzin, C.

P. E. Porporato, V. L. Payen, J. Pérez-Escuredo, C. J. De Saedeleer, P. Danhier, T. Copetti, S. Dhup, M. Tardy, T. Vazeille, C. Bouzin, O. Feron, C. Michiels, B. Gallez, and P. Sonveaux, “A Mitochondrial Switch Promotes Tumor Metastasis,” Cell Reports 8(3), 754–766 (2014).
[Crossref] [PubMed]

Bradbury, C. M.

X. Lin, F. Zhang, C. M. Bradbury, A. Kaushal, L. Li, D. R. Spitz, R. L. Aft, and D. Gius, “2-Deoxy-D-glucose-induced cytotoxicity and radiosensitization in tumor cells is mediated via disruptions in thiol metabolism,” Cancer Res. 63(12), 3413–3417 (2003).
[PubMed]

Branders, S.

R. Boidot, S. Branders, T. Helleputte, L. I. Rubio, P. Dupont, and O. Feron, “A generic cycling hypoxia-derived prognostic gene signature: application to breast cancer profiling,” Oncotarget 5(16), 6947–6963 (2014).
[Crossref] [PubMed]

Braun, R. D.

J. Lanzen, R. D. Braun, B. Klitzman, D. Brizel, T. W. Secomb, and M. W. Dewhirst, “Direct demonstration of instabilities in oxygen concentrations within the extravascular compartment of an experimental tumor,” Cancer Res. 66(4), 2219–2223 (2006).
[Crossref] [PubMed]

H. Kimura, R. D. Braun, E. T. Ong, R. Hsu, T. W. Secomb, D. Papahadjopoulos, K. Hong, and M. W. Dewhirst, “Fluctuations in red cell flux in tumor microvessels can lead to transient hypoxia and reoxygenation in tumor parenchyma,” Cancer Res. 56(23), 5522–5528 (1996).
[PubMed]

Brizel, D.

J. Lanzen, R. D. Braun, B. Klitzman, D. Brizel, T. W. Secomb, and M. W. Dewhirst, “Direct demonstration of instabilities in oxygen concentrations within the extravascular compartment of an experimental tumor,” Cancer Res. 66(4), 2219–2223 (2006).
[Crossref] [PubMed]

Brookner, C.

R. Drezek, C. Brookner, I. Pavlova, I. Boiko, A. Malpica, R. Lotan, M. Follen, and R. Richards-Kortum, “Autofluorescence Microscopy of Fresh Cervical-Tissue Sections Reveals Alterations in Tissue Biochemistry with Dysplasia,” Photochem. Photobiol. 73(6), 636–641 (2001).
[Crossref] [PubMed]

Brown, J. Q.

J. H. Ostrander, C. M. McMahon, S. Lem, S. R. Millon, J. Q. Brown, V. L. Seewaldt, and N. Ramanujam, “Optical Redox Ratio Differentiates Breast Cancer Cell Lines Based on Estrogen Receptor Status,” Cancer Res. 70(11), 4759–4766 (2010).
[Crossref] [PubMed]

Büttner, S.

C. Ruckenstuhl, S. Büttner, D. Carmona-Gutierrez, T. Eisenberg, G. Kroemer, S. J. Sigrist, K.-U. Fröhlich, and F. Madeo, “The Warburg Effect Suppresses Oxidative Stress Induced Apoptosis in a Yeast Model for Cancer,” PLoS One 4(2), e4592 (2009).
[Crossref] [PubMed]

Cairns, R. A.

R. A. Cairns and R. P. Hill, “Acute hypoxia enhances spontaneous lymph node metastasis in an orthotopic murine model of human cervical carcinoma,” Cancer Res. 64(6), 2054–2061 (2004).
[Crossref] [PubMed]

R. A. Cairns, T. Kalliomaki, and R. P. Hill, “Acute (cyclic) hypoxia enhances spontaneous metastasis of KHT murine tumors,” Cancer Res. 61(24), 8903–8908 (2001).
[PubMed]

Carmona-Gutierrez, D.

C. Ruckenstuhl, S. Büttner, D. Carmona-Gutierrez, T. Eisenberg, G. Kroemer, S. J. Sigrist, K.-U. Fröhlich, and F. Madeo, “The Warburg Effect Suppresses Oxidative Stress Induced Apoptosis in a Yeast Model for Cancer,” PLoS One 4(2), e4592 (2009).
[Crossref] [PubMed]

Castellanos, J. A.

A. J. Walsh, J. A. Castellanos, N. S. Nagathihalli, N. B. Merchant, and M. C. Skala, “Optical Imaging of Drug-Induced Metabolism Changes in Murine and Human Pancreatic Cancer Organoids Reveals Heterogeneous Drug Response,” Pancreas 45(6), 863–869 (2016).
[PubMed]

Chan, N.

J. Hou, H. J. Wright, N. Chan, R. Tran, O. V. Razorenova, E. O. Potma, and B. J. Tromberg, “Correlating two-photon excited fluorescence imaging of breast cancer cellular redox state with seahorse flux analysis of normalized cellular oxygen consumption,” J. Biomed. Opt. 21(6), 060503 (2016).
[Crossref] [PubMed]

Chance, B.

H. N. Xu, S. Nioka, J. D. Glickson, B. Chance, and L. Z. Li, “Quantitative mitochondrial redox imaging of breast cancer metastatic potential,” J. Biomed. Opt. 15, 036010 (2010).

L. Z. Li, R. Zhou, H. N. Xu, L. Moon, T. Zhong, E. J. Kim, H. Qiao, R. Reddy, D. Leeper, B. Chance, and J. D. Glickson, “Quantitative magnetic resonance and optical imaging biomarkers of melanoma metastatic potential,” Proc. Natl. Acad. Sci. U.S.A. 106(16), 6608–6613 (2009).
[Crossref] [PubMed]

N. Ramanujam, R. Richards-Kortum, S. Thomsen, A. Mahadevan-Jansen, M. Follen, and B. Chance, “Low temperature fluorescence imaging of freeze-trapped human cervical tissues,” Opt. Express 8(6), 335–343 (2001).
[Crossref] [PubMed]

B. Chance, B. Schoener, R. Oshino, F. Itshak, and Y. Nakase, “Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals,” J. Biol. Chem. 254(11), 4764–4771 (1979).
[PubMed]

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

Chaplin, D. J.

D. J. Chaplin, P. L. Olive, and R. E. Durand, “Intermittent blood flow in a murine tumor: radiobiological effects,” Cancer Res. 47(2), 597–601 (1987).
[PubMed]

Chatham, J. C.

B. P. Dranka, G. A. Benavides, A. R. Diers, S. Giordano, B. R. Zelickson, C. Reily, L. Zou, J. C. Chatham, B. G. Hill, J. Zhang, A. Landar, and V. M. Darley-Usmar, “Assessing bioenergetic function in response to oxidative stress by metabolic profiling,” Free Radic. Biol. Med. 51(9), 1621–1635 (2011).
[Crossref] [PubMed]

Chen, E. I.

E. Louie, S. Nik, J. S. Chen, M. Schmidt, B. Song, C. Pacson, X. F. Chen, S. Park, J. Ju, and E. I. Chen, “Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation,” Breast Cancer Res. 12(6), R94 (2010).
[Crossref] [PubMed]

Chen, J. S.

E. Louie, S. Nik, J. S. Chen, M. Schmidt, B. Song, C. Pacson, X. F. Chen, S. Park, J. Ju, and E. I. Chen, “Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation,” Breast Cancer Res. 12(6), R94 (2010).
[Crossref] [PubMed]

Chen, X. F.

E. Louie, S. Nik, J. S. Chen, M. Schmidt, B. Song, C. Pacson, X. F. Chen, S. Park, J. Ju, and E. I. Chen, “Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation,” Breast Cancer Res. 12(6), R94 (2010).
[Crossref] [PubMed]

Chevanne, M.

C. Groussard, I. Morel, M. Chevanne, M. Monnier, J. Cillard, and A. Delamarche, “Free radical scavenging and antioxidant effects of lactate ion: an in vitro study,” J. Appl. Physiol. 89(1), 169–175 (2000).
[PubMed]

Chingos, D. T.

N. L. Henry, M. R. Somerfield, V. G. Abramson, K. H. Allison, C. K. Anders, D. T. Chingos, A. Hurria, T. H. Openshaw, and I. E. Krop, “Role of Patient and Disease Factors in Adjuvant Systemic Therapy Decision Making for Early-Stage, Operable Breast Cancer: American Society of Clinical Oncology Endorsement of Cancer Care Ontario Guideline Recommendations,” J. Clin. Oncol. 34(19), 2303–2311 (2016).
[Crossref] [PubMed]

Ciliberto, G.

A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative Optical Imaging of Primary Tumor Organoid Metabolism Predicts Drug Response in Breast Cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

Cillard, J.

C. Groussard, I. Morel, M. Chevanne, M. Monnier, J. Cillard, and A. Delamarche, “Free radical scavenging and antioxidant effects of lactate ion: an in vitro study,” J. Appl. Physiol. 89(1), 169–175 (2000).
[PubMed]

Clarke, M.

R. Peto, C. Davies, J. Godwin, R. Gray, H. C. Pan, M. Clarke, D. Cutter, S. Darby, P. McGale, C. Taylor, Y. C. Wang, J. Bergh, A. Di Leo, K. Albain, S. Swain, M. Piccart, K. Pritchard, and Early Breast Cancer Trialists’ Collaborative Group (EBCTCG), “Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials,” Lancet 379(9814), 432–444 (2012).
[Crossref] [PubMed]

Clemons, M.

F. Dupuy, S. Tabariès, S. Andrzejewski, Z. Dong, J. Blagih, M. G. Annis, A. Omeroglu, D. Gao, S. Leung, E. Amir, M. Clemons, A. Aguilar-Mahecha, M. Basik, E. E. Vincent, J. St-Pierre, R. G. Jones, and P. M. Siegel, “PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer,” Cell Metab. 22(4), 577–589 (2015).
[Crossref] [PubMed]

Cohen, P.

B. Chance, P. Cohen, F. Jobsis, and B. Schoener, “Intracellular oxidation-reduction states in vivo,” Science 137(3529), 499–508 (1962).
[Crossref] [PubMed]

Come, C.

J. Yang, S. A. Mani, J. L. Donaher, S. Ramaswamy, R. A. Itzykson, C. Come, P. Savagner, I. Gitelman, A. Richardson, and R. A. Weinberg, “Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis,” Cell 117(7), 927–939 (2004).
[Crossref] [PubMed]

Cook, R. S.

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V. S. LeBleu, J. T. O’Connell, K. N. Gonzalez Herrera, H. Wikman, K. Pantel, M. C. Haigis, F. M. de Carvalho, A. Damascena, L. T. Domingos Chinen, R. M. Rocha, J. M. Asara, and R. Kalluri, “PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis,” Nat. Cell Biol. 16(10), 992–1003 (2014).
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R. Boidot, S. Branders, T. Helleputte, L. I. Rubio, P. Dupont, and O. Feron, “A generic cycling hypoxia-derived prognostic gene signature: application to breast cancer profiling,” Oncotarget 5(16), 6947–6963 (2014).
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F. Dupuy, S. Tabariès, S. Andrzejewski, Z. Dong, J. Blagih, M. G. Annis, A. Omeroglu, D. Gao, S. Leung, E. Amir, M. Clemons, A. Aguilar-Mahecha, M. Basik, E. E. Vincent, J. St-Pierre, R. G. Jones, and P. M. Siegel, “PDK1-dependent metabolic reprogramming dictates metastatic potential in breast cancer,” Cell Metab. 22(4), 577–589 (2015).
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M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
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K. P. Quinn, E. Bellas, N. Fourligas, K. Lee, D. L. Kaplan, and I. Georgakoudi, “Characterization of metabolic changes associated with the functional development of 3D engineered tissues by non-invasive, dynamic measurement of individual cell redox ratios,” Biomaterials 33(21), 5341–5348 (2012).
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V. S. LeBleu, J. T. O’Connell, K. N. Gonzalez Herrera, H. Wikman, K. Pantel, M. C. Haigis, F. M. de Carvalho, A. Damascena, L. T. Domingos Chinen, R. M. Rocha, J. M. Asara, and R. Kalluri, “PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis,” Nat. Cell Biol. 16(10), 992–1003 (2014).
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K. P. Quinn, G. V. Sridharan, R. S. Hayden, D. L. Kaplan, K. Lee, and I. Georgakoudi, “Quantitative metabolic imaging using endogenous fluorescence to detect stem cell differentiation,” Sci. Rep. 3, 3432 (2013).
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R. Boidot, S. Branders, T. Helleputte, L. I. Rubio, P. Dupont, and O. Feron, “A generic cycling hypoxia-derived prognostic gene signature: application to breast cancer profiling,” Oncotarget 5(16), 6947–6963 (2014).
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B. P. Dranka, G. A. Benavides, A. R. Diers, S. Giordano, B. R. Zelickson, C. Reily, L. Zou, J. C. Chatham, B. G. Hill, J. Zhang, A. Landar, and V. M. Darley-Usmar, “Assessing bioenergetic function in response to oxidative stress by metabolic profiling,” Free Radic. Biol. Med. 51(9), 1621–1635 (2011).
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N. Ramanujam, R. Richards-Kortum, S. Thomsen, A. Mahadevan-Jansen, M. Follen, and B. Chance, “Low temperature fluorescence imaging of freeze-trapped human cervical tissues,” Opt. Express 8(6), 335–343 (2001).
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N. Ramanujam, R. Richards-Kortum, S. Thomsen, A. Mahadevan-Jansen, M. Follen, and B. Chance, “Low temperature fluorescence imaging of freeze-trapped human cervical tissues,” Opt. Express 8(6), 335–343 (2001).
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M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
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M. Cronin, C. Sangli, M.-L. Liu, M. Pho, D. Dutta, A. Nguyen, J. Jeong, J. Wu, K. C. Langone, and D. Watson, “Analytical Validation of the Oncotype DX Genomic Diagnostic Test for Recurrence Prognosis and Therapeutic Response Prediction in Node-Negative, Estrogen Receptor-Positive Breast Cancer,” Clin. Chem. 53(6), 1084–1091 (2007).
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J. H. Ostrander, C. M. McMahon, S. Lem, S. R. Millon, J. Q. Brown, V. L. Seewaldt, and N. Ramanujam, “Optical Redox Ratio Differentiates Breast Cancer Cell Lines Based on Estrogen Receptor Status,” Cancer Res. 70(11), 4759–4766 (2010).
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C. Lehuédé, F. Dupuy, R. Rabinovitch, R. G. Jones, and P. M. Siegel, “Metabolic Plasticity as a Determinant of Tumor Growth and Metastasis,” Cancer Res. 76(18), 5201–5208 (2016).
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Y. Dai, K. Bae, and D. W. Siemann, “Impact of hypoxia on the metastatic potential of human prostate cancer cells,” Int. J. Radiat. Oncol. Biol. Phys. 81(2), 521–528 (2011).
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A. J. Walsh, J. A. Castellanos, N. S. Nagathihalli, N. B. Merchant, and M. C. Skala, “Optical Imaging of Drug-Induced Metabolism Changes in Murine and Human Pancreatic Cancer Organoids Reveals Heterogeneous Drug Response,” Pancreas 45(6), 863–869 (2016).
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A. J. Walsh and M. C. Skala, “Optical metabolic imaging quantifies heterogeneous cell populations,” Biomed. Opt. Express 6(2), 559–573 (2015).
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A. J. Walsh, R. S. Cook, M. E. Sanders, L. Aurisicchio, G. Ciliberto, C. L. Arteaga, and M. C. Skala, “Quantitative Optical Imaging of Primary Tumor Organoid Metabolism Predicts Drug Response in Breast Cancer,” Cancer Res. 74(18), 5184–5194 (2014).
[Crossref] [PubMed]

A. T. Shah, M. Demory Beckler, A. J. Walsh, W. P. Jones, P. R. Pohlmann, and M. C. Skala, “Optical Metabolic Imaging of Treatment Response in Human Head and Neck Squamous Cell Carcinoma,” PLoS One 9(3), e90746 (2014).
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A. J. Walsh, R. S. Cook, H. C. Manning, D. J. Hicks, A. Lafontant, C. L. Arteaga, and M. C. Skala, “Optical Metabolic Imaging Identifies Glycolytic Levels, Subtypes, and Early-Treatment Response in Breast Cancer,” Cancer Res. 73(20), 6164–6174 (2013).
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A. Walsh, R. S. Cook, B. Rexer, C. L. Arteaga, and M. C. Skala, “Optical imaging of metabolism in HER2 overexpressing breast cancer cells,” Biomed. Opt. Express 3(1), 75–85 (2012).
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M. C. Skala, K. M. Riching, A. Gendron-Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, and N. Ramanujam, “In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia,” Proc. Natl. Acad. Sci. U.S.A. 104(49), 19494–19499 (2007).
[Crossref] [PubMed]

M. C. Skala, J. M. Squirrell, K. M. Vrotsos, J. C. Eickhoff, A. Gendron-Fitzpatrick, K. W. Eliceiri, and N. Ramanujam, “Multiphoton microscopy of endogenous fluorescence differentiates normal, precancerous, and cancerous squamous epithelial tissues,” Cancer Res. 65(4), 1180–1186 (2005).
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N. L. Henry, M. R. Somerfield, V. G. Abramson, K. H. Allison, C. K. Anders, D. T. Chingos, A. Hurria, T. H. Openshaw, and I. E. Krop, “Role of Patient and Disease Factors in Adjuvant Systemic Therapy Decision Making for Early-Stage, Operable Breast Cancer: American Society of Clinical Oncology Endorsement of Cancer Care Ontario Guideline Recommendations,” J. Clin. Oncol. 34(19), 2303–2311 (2016).
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E. Louie, S. Nik, J. S. Chen, M. Schmidt, B. Song, C. Pacson, X. F. Chen, S. Park, J. Ju, and E. I. Chen, “Identification of a stem-like cell population by exposing metastatic breast cancer cell lines to repetitive cycles of hypoxia and reoxygenation,” Breast Cancer Res. 12(6), R94 (2010).
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R. Peto, C. Davies, J. Godwin, R. Gray, H. C. Pan, M. Clarke, D. Cutter, S. Darby, P. McGale, C. Taylor, Y. C. Wang, J. Bergh, A. Di Leo, K. Albain, S. Swain, M. Piccart, K. Pritchard, and Early Breast Cancer Trialists’ Collaborative Group (EBCTCG), “Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials,” Lancet 379(9814), 432–444 (2012).
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Neoplasia (1)

R. V. Simões, I. S. Serganova, N. Kruchevsky, A. Leftin, A. A. Shestov, H. T. Thaler, G. Sukenick, J. W. Locasale, R. G. Blasberg, J. A. Koutcher, and E. Ackerstaff, “Metabolic plasticity of metastatic breast cancer cells: adaptation to changes in the microenvironment,” Neoplasia 17(8), 671–684 (2015).
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Opt. Express (1)

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A. J. Walsh, J. A. Castellanos, N. S. Nagathihalli, N. B. Merchant, and M. C. Skala, “Optical Imaging of Drug-Induced Metabolism Changes in Murine and Human Pancreatic Cancer Organoids Reveals Heterogeneous Drug Response,” Pancreas 45(6), 863–869 (2016).
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A. T. Shah, M. Demory Beckler, A. J. Walsh, W. P. Jones, P. R. Pohlmann, and M. C. Skala, “Optical Metabolic Imaging of Treatment Response in Human Head and Neck Squamous Cell Carcinoma,” PLoS One 9(3), e90746 (2014).
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Proc. Natl. Acad. Sci. U.S.A. (3)

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Science (1)

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Figures (4)

Fig. 1
Fig. 1

Optical redox ratio is sensitive to dynamic changes in oxygen consumption. A. Representative images of NADH, FAD and the calculated optical redox ratio (FAD/FAD + NADH) in response to the addition of mitochondrial inhibitors and uncouplers. All images were acquired from different fields of view within the same cell plate over several minutes after serial addition of each drug indicated above the figure panels. B. Quantification of the dynamic changes in the optical redox ratio in response to serial drug additions. Oligomycin, FCCP, and antimycin A/rotenone were injected at T = 30, 70, and 110 minutes, respectively. C. Normalized oxygen consumption rate measured using the Seahorse XFp analyzer. Oligomycin, FCCP, and antimycin A/rotenone were injected at T = 15, 35, and 55 minutes, respectively. The error bars are a standard deviation of the mean plate value.

Fig. 2
Fig. 2

Optical redox ratio of breast cancer cells of different metastatic potential is significantly different at normoxia and after exposure to acute hypoxia. A. Representative redox ratio images for 4T1, 4T07, 168FARN, and 67NR breast cancer cells. The redox ratio was measured at baseline normoxic conditions and 1 hour after exposure to acute hypoxia (60 minutes, 0.5% O2). B. Quantification of redox ratio images illustrates significant differences in the redox ratio between the different cell lines under normoxic conditions, and within each cell line after exposure to acute hypoxia (except 168FARN). Error bars represent standard deviation of the mean plate value. C. The normalized oxygen consumption rate (calculated as oxygen consumption rate/proton production rate) for all four cell lines and the direction of change after exposure to acute hypoxia are consistent with the optical redox ratio. Asterisks placed above bars indicate statistical significance. *** denotes p < 0.0001 and ** denotes p < 0.01.

Fig. 3
Fig. 3

Exposure to acute hypoxia leads to cell-line-dependent changes in redox ratio. Bar plots represent the difference in the mean values of normoxia and post-hypoxia reoxygenation groups. Error bars represent the standard deviation and were calculated as follows: ( s d 1 ) 2 +  ( s d 2 ) 2 , where sd1 and sd2 represent the normoxia and post-hypoxia groups within each cell line.

Fig. 4
Fig. 4

Effect of mitochondrial inhibitors and uncouplers on redox ratio. Initial addition of oligomycin inhibits ATP synthase, which decreases mitochondrial respiration, increases NADH that cannot be converted to NAD+ and hence decreases the redox ratio. FCCP is a mitochondrial uncoupler that causes protons to leak across the membrane, leading to a loss of proton gradient and hence the ability to generate ATP. Because the cell tries to restore the proton gradient, NADH is consumed, leading to increased redox ratio. Finally, Rotenone and Antimycin inhibit complexes I and III, leading to a shutdown of mitochondrial respiration and a decrease in the redox ratio.

Tables (1)

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Table 1 Invasion – metastasis cascade for Balb/c tumor-derived breast cancer cell lines

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