Journal of Innovative Optical Health Sciences, Volume. 18, Issue 1, 2450020(2025)
Correlating NAD(P)H lifetime shifts to tamoxifen resistance in breast cancer cells: A metabolic screening study with time-resolved flow cytometry
[2] [2] American Cancer Society, Atlanta, Georgia, USA.
[3] V. C. Jordan. Tamoxifen: A most unlikely pioneering medicine. Nat. Rev. Drug Discov., 2, 205-213(2003).
[4] V. M. Quirke. Tamoxifen from failed contraceptive pill to best-selling breast cancer medicine: A case-study in pharmaceutical innovation. Front. Pharmacol., 8, 620(2017).
[5] Y. M. Woo et al. Inhibition of aerobic glycolysis represses Akt/mTOR/HIF-1α axis and restores tamoxifen sensitivity in antiestrogen-resistant breast cancer cells. PLoS One, 10, e0132285(2015).
[6] E. A. Musgrove, R. L. Sutherland. Biological determinants of endocrine resistance in breast cancer. Nat. Rev. Cancer, 9, 631-643(2009).
[7] C. K. Osborne, R. Schiff. Mechanisms of endocrine resistance in breast cancer. Annu. Rev. Med., 62, 233-247(2011).
[8] J. Yao, K. Deng, J. Huang, R. Zeng, J. Zuo. Progress in the understanding of the mechanism of tamoxifen resistance in breast cancer. Front. Pharmacol., 11, 592912(2020).
[9] A. Vaziri-Gohar, Y. Zheng, K. D. Houston. IGF-1 receptor modulates FoxO1-mediated tamoxifen response in breast cancer cells. Mol. Cancer Res., 15, 489-497(2017).
[10] Y. Zheng, K. D. Houston. Glucose-dependent GPER1 expression modulates tamoxifen-induced IGFBP-1 accumulation. J. Mol. Endocrinol., 63, 103-112(2019).
[11] Y. Zheng, J. Y. Sowers, K. D. Houston. IGFBP-1 expression promotes tamoxifen resistance in breast cancer cells via Erk pathway activation. Front. Endocrinol. (Lausanne), 11, 233(2020).
[12] K. T. Pate et al. Wnt signaling directs a metabolic program of glycolysis and angiogenesis in colon cancer. EMBO J., 33, 1454-1473(2014).
[13] A. P. Drabovich, M. P. Pavlou, A. Dimitromanolakis, E. P. Diamandis. Quantitative analysis of energy metabolic pathways in MCF-7 breast cancer cells by selected reaction monitoring assay. Mol. Cell Proteom., 11, 422-434(2012).
[14] B. M. Sharaf et al. Untargeted metabolomics of breast cancer cells MCF-7 and SkBr3 treated with tamoxifen/trastuzumab. Cancer Genom. Proteom., 19, 79-93(2022).
[15] V. Rossi, M. Govoni, F. Farabegoli, G. Di Stefano. Lactate is a potential promoter of tamoxifen resistance in MCF7 cells. Biochim. Biophys. Acta Gen. Subj., 1866, 130185(2022).
[16] C. K. Das, A. Parekh, P. K. Parida, S. K. Bhutia, M. Mandal. Lactate dehydrogenase A regulates autophagy and tamoxifen resistance in breast cancer. Biochim. Biophys. Acta Mol. Cell Res., 1866, 1004-1018(2019).
[17] N. A. Daurio et al. AMPK activation and metabolic reprogramming by tamoxifen through estrogen receptor-independent mechanisms suggests new uses for this therapeutic modality in cancer treatment. Cancer Res., 76, 3295-3306(2016).
[18] V. Tomková, C. Sandoval-Acuña, N. Torrealba, J. Truksa. Mitochondrial fragmentation, elevated mitochondrial superoxide and respiratory supercomplexes disassembly is connected with the tamoxifen-resistant phenotype of breast cancer cells. Free Radic. Biol. Med., 143, 510-521(2019).
[19] P. I. Moreira, J. Custódio, A. Moreno, C. R. Oliveira, M. S. Santos. Tamoxifen and estradiol interact with the flavin mononucleotide site of complex I leading to mitochondrial failure. J. Biol. Chem., 281, 10143-10152(2006).
[20] Y. Unten et al. Comprehensive understanding of multiple actions of anticancer drug tamoxifen in isolated mitochondria. Biochim. Biophys. Acta Bioenerg., 1863, 148520(2022).
[21] A. Mishra, A. Srivastava, L. K. Sharma, A. K. Mishra, A. Shrivastava. Comparative metabolomics of MCF-7 and MCF-7/TAMR identifies potential metabolic pathways in tamoxifen resistant breast cancer cells. Am. J. Transl. Res., 16, 1337-1352(2024).
[22] P. M. Schaefer, S. Kalinina, A. Rueck, C. A. F. von Arnim, B. von Einem. NADH autofluorescence-A marker on its way to boost bioenergetic research. Cytometry A, 95, 34-46(2019).
[23] T. S. Blacker, M. R. Duchen, A. J. Bain. NAD(P)H binding configurations revealed by time-resolved fluorescence and two-photon absorption. Biophys. J., 122, 1240-1253(2023).
[24] D. K. Bird et al. Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH. Cancer Res., 65, 8766-8773(2005).
[25] C. Stringari, J. L. Nourse, L. A. Flanagan, E. Gratton. Phasor fluorescence lifetime microscopy of free and protein-bound NADH reveals neural stem cell differentiation potential. PLoS One, 7, e48014(2012).
[26] D. Voet, J. G. Voet. Biochemistry(2011).
[27] B. Chance, P. Cohen, F. Jobsis, B. Schoener. Intracellular oxidation-reduction states in vivo. Science, 137, 499-508(1962).
[28] J. V. Chacko, K. W. Eliceiri. Autofluorescence lifetime imaging of cellular metabolism: Sensitivity toward cell density, pH, intracellular, and intercellular heterogeneity. Cytometry A, 95, 56-69(2019).
[29] R. Cao, V. Pankayatselvan, J. P. Houston. Cytometric sorting based on the fluorescence lifetime of spectrally overlapping signals. Opt. Express, 21, 14816-14831(2013).
[30] W. Li, K. D. Houston, J. P. Houston. Shifts in the fluorescence lifetime of EGFP during bacterial phagocytosis measured by phase-sensitive flow cytometry. Sci. Rep., 7, 40341(2017).
[31] P. H. Lakner, M. G. Monaghan, Y. Möller, M. A. Olayioye, K. Schenke-Layland. Applying phasor approach analysis of multiphoton FLIM measurements to probe the metabolic activity of three-dimensional in vitro cell culture models. Sci. Rep., 7, 42730(2017).
[32] R. Leben, M. Köhler, H. Radbruch, A. E. Hauser, R. A. Niesner. Systematic enzyme mapping of cellular metabolism by phasor-analyzed label-free NAD(P)H fluorescence lifetime imaging. Int. J. Mol. Sci., 20, 5565(2019).
[33] J. P. Houston, M. A. Naivar, J. P. Freyer. Capture of fluorescence decay times by flow cytometry. Curr. Protoc. Cytom., 59, 1.25.1-1.25.21(2012).
[34] R. Cao, M. A. Naivar, M. Wilder, J. P. Houston. Expanding the potential of standard flow cytometry by extracting fluorescence lifetimes from cytometric pulse shifts. Cytometry A, 85, 999-1010(2014).
[35] W. Li, G. Vacca, M. Castillo, K. D. Houston, J. P. Houston. Fluorescence lifetime excitation cytometry by kinetic dithering. Electrophoresis, 35, 1846-1854(2014).
[36] P. Jenkins, M. A. Naivar, J. P. Houston. Toward the measurement of multiple fluorescence lifetimes in flow cytometry: Maximizing multi-harmonic content from cells and microspheres. J. Biophoton., 8, 908-917(2015).
[37] B. Sands et al. Measuring and sorting cell populations expressing isospectral fluorescent proteins with different fluorescence lifetimes. PLoS One, 9, e109940(2014).
[38] R. Cao et al. Phasor plotting with frequency-domain flow cytometry. Opt. Express, 24, 14596-14607(2016).
[39] J. L. Lubbeck, K. M. Dean, H. Ma, A. E. Palmer, R. Jimenez. Microfluidic flow cytometer for quantifying photobleaching of fluorescent proteins in cells. Anal. Chem. (Washington), 84, 3929-3937(2012).
[40] P. Manna, R. Jimenez. Time and frequency-domain measurement of ground-state recovery times in red fluorescent proteins. J. Phys. Chem. B, 119, 4944-4954(2015).
[41] K. M. Dean et al. Microfluidic flow cytometer for multiparameter screening of fluorophore photophysics. 2014 Conf. Lasers and Electro-Optics (CLEO) - Laser Science to Photonic Applications, 1-2(2014).
[42] D. Kage et al. Luminescence lifetime encoding in time-domain flow cytometry. Sci. Rep., 8, 16715(2018).
[43] J. Nedbal et al. Time-domain microfluidic fluorescence lifetime flow cytometry for high-throughput Förster resonance energy transfer screening. Cytometry A, 87, 104-118(2015).
[44] J. Sambrano, F. Rodriguez, J. Martin, J. P. Houston. Toward the development of an on-chip acoustic focusing fluorescence lifetime flow cytometer. Front. Phys., 9, 647985(2021).
[45] J. P. Houston, S. Valentino, A. Bitton. Fluorescence lifetime measurements and analyses: Protocols using flow cytometry and high-throughput microscopy. Methods Mol. Biol., 2779, 323-351(2024).
[46] A. Ulku et al. Wide-field time-gated SPAD imager for phasor-based FLIM applications. Methods Appl. Fluoresc., 8, 024002(2020).
[47] H. Mai et al. Development of a high-speed line-scanning fluorescence lifetime imaging microscope for biological imaging. Opt. Lett., 48, 2042-2045(2023).
[48] D. Xiao et al. Dynamic fluorescence lifetime sensing with CMOS single-photon avalanche diode arrays and deep learning processors. Biomed. Opt. Express, 12, 3450-3462(2021).
[49] V. Zickus et al. Fluorescence lifetime imaging with a megapixel SPAD camera and neural network lifetime estimation. Sci. Rep., 10, 20986(2020).
[50] S. Karpf et al. Spectro-temporal encoded multiphoton microscopy and fluorescence lifetime imaging at kilohertz frame-rates. Nat. Commun., 11, 2062(2020).
[51] N. Paillon, T. P. L. Ung, S. Dogniaux, C. Stringari, C. Hivroz. Label-free single-cell live imaging reveals fast metabolic switch in T lymphocytes. Mol. Biol. Cell, 35, ar11(2024).
[52] A. A. Gillette, R. A. DeStefanis, S. L. Pritzl, D. A. Deming, M. C. Skala. Inhibition of B-cell lymphoma 2 family proteins alters optical redox ratio, mitochondrial polarization, and cell energetics independent of cell state. J. Biomed. Opt., 27, 056505(2022).
[53] R. Datta, T. M. Heaster, J. T. Sharick, A. A. Gillette, M. C. Skala. Fluorescence lifetime imaging microscopy: fundamentals and advances in instrumentation, analysis, and applications. J. Biomed. Opt., 25, 1-43(2020).
[54] B. G. Pinsky, J. J. Ladasky, J. R. Lakowicz, K. Berndt, R. A. Hoffman. Phase-resolved fluorescence lifetime measurements for flow-cytometry. Cytometry, 14, 123-135(1993).
[55] F. Alturkistany, K. Nichani, K. D. Houston, J. P. Houston. Fluorescence lifetime shifts of NAD(P)H during apoptosis measured by time-resolved flow cytometry. Cytometry A, 95, 70-79(2019).
[56] J. P. Houston, M. A. Naivar, J. P. Freyer. Digital analysis and sorting of fluorescence lifetime by flow cytometry. Cytometry Part A, 77A, 861-872(2010).
[57] C. Giesecke et al. Determination of background, signal-to-noise, and dynamic range of a flow cytometer: A novel practical method for instrument characterization and standardization. Cytometry A, 91, 1104-1114(2017).
[58] K. Samimi et al. Autofluorescence lifetime flow cytometry with time-correlated single photon counting. Cytometry A, 105, 607-620(2024).
[59] O. I. Kolenc, K. P. Quinn. Evaluating cell metabolism through autofluorescence imaging of NAD(P)H and FAD. Antioxid. Redox Signal, 30, 875-889(2019).
[60] A. Hutschenreuther, G. Birkenmeier, M. Bigl, K. Krohn, C. Birkemeyer. Glycerophosphoglycerol, Beta-alanine, and pantothenic acid as metabolic companions of glycolytic activity and cell migration in breast cancer cell lines. Metabolites, 3, 1084-1101(2013).
[61] W. Telford. Deep ultraviolet 266 nm laser excitation for flow cytometry. Cytometry A, 105, 214-221(2024).
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Samantha Valentino, Karla Ortega-Sandoval, Kevin D. Houston, Jessica P. Houston. Correlating NAD(P)H lifetime shifts to tamoxifen resistance in breast cancer cells: A metabolic screening study with time-resolved flow cytometry[J]. Journal of Innovative Optical Health Sciences, 2025, 18(1): 2450020
Category: Research Articles
Received: Dec. 19, 2023
Accepted: Aug. 15, 2024
Published Online: Feb. 21, 2025
The Author Email: Houston Jessica P. (jph@nmsu.edu)