Abstract
Cellular redox states can regulate cell metabolism, growth, differentiation, motility, apoptosis, signaling pathways, and gene expressions etc. A growing body of literature suggest the importance of redox status for cancer progression. While most studies on redox state were done on cells and tissue lysates, it is important to understand the role of redox state in a tissue in vivo/ex vivo and image its heterogeneity. Redox scanning is a clinical-translatable method for imaging tissue mitochondrial redox potential with a submillimeter resolution. Redox scanning data in mouse models of human cancers demonstrate a correlation between mitochondrial redox state and tumor metastatic potential. I will discuss the significance of this correlation and possible directions for future research.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Adler V, Yin ZM, Tew KD, Ronai Z (1999) Role of redox potential and reactive oxygen species in stress signaling. Oncogene 18(45):6104–6111
Agarwal AK, Auchus RJ (2005) Minireview: cellular redox state regulates hydroxysteroid dehydrogenase activity and intracellular hormone potency. Endocrinology 146(6):2531–2538
Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, Thomas-Tikhonenko A, Thompson CB (2007) Autophagy inhibition enhances therapy-induced apoptosis in a Myc-induced model of lymphoma. J Clin Invest 117(2):326–336
Banerjee R (2008) Redox biochemistry. John Wiley & Sons, Hoboken
Barlow CH, Harden WR 3rd, Harken AH, Simson MB, Haselgrove JC, Chance B, O’Connor M, Austin G (1979) Fluorescence mapping of mitochrondrial redox changes in heart and brain. Crit Care Med 7(9):402–406
Becker DF, Zhu W, Moxley MA (2011) Flavin redox switching of protein functions. Antioxid Redox Signal 14(6):1079–1091
Blinova K, Levine RL, Boja ES, Griffiths GL, Shi ZD, Ruddy B, Balaban RS (2008) Mitochondrial NADH fluorescence is enhanced by Complex I binding. Biochemistry 47(36):9636–9645
Bohndiek SE, Kettunen MI, Hu D-e, Kennedy BWC, Boren J, Gallagher FA, Brindle KM (2011) Hyperpolarized [1-13C]-ascorbic and dehydroascorbic acid: vitamin C as a probe for imaging redox status in vivo. J Am Chem Soc 133(30):11795–11801
Brown JQ, Wilke LG, Geradts J, Kennedy SA, Palmer GM, Ramanujam N (2009) Quantitative optical spectroscopy: a robust tool for direct measurement of breast cancer vascular oxygenation and total hemoglobin content in vivo. Cancer Res 69(7):2919–2926
Cai K, Xu HN, Singh A, Haris M, Reddy R, Li LZ (2012). Characterizing prostate tumor mouse xenografts with CEST & MT MRI and redox scanning. Adv Exp Med Biol
Cairns RA, Harris IS, Mak TW (2011) Regulation of cancer cell metabolism. Nat Rev Cancer 11(2):85–95. doi:10.1038/nrc2981
Chance B (1966) Spectrophotometric and kinetic studies of flavoproteins in tissues, cell suspensions, mitochondria and their fragments. In: Slater EC (ed) Flavins and flavoproteins. Elsevier, Amsterdam, pp 498–510
Chance B, Baltscheffsky H (1958) Respiratory enzymes in oxidative phosphorylation. 7. Binding of intramitochondrial reduced pyridine nucleotide. J Biol Chem 233(3):736–739
Chance B, Cohen P, Jobsis F, Schoener B (1962) Intracellular oxidation-reduction states in vivo. Science 137:499–508
Chance B, Jobsis F (1959) Changes in fluorescence in a frog sartorius muscle following a twitch. Nature 184(4681):195–196
Chance B, Schoener B (1966) Fluorometric studies of flavin component of the respiratory chain. In: Slater EC (ed) Flavins and flavoproteins. Elsevier, Amsterdam, pp 510–519
Chance B, Schoener B, Oshino R, Itshak F, Nakase Y (1979) Oxidation-reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals. J Biol Chem 254(11):4764–4771
Chance B, Williams GR (1955a) A method for the localization of sites for oxidative phosphorylation. Nature 176(4475):250–254
Chance B, Williams GR (1955b) Respiratory enzymes in oxidative phosphorylation. III. The steady state. J Biol Chem 217(1):409–428
Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, Fleming MD, Schreiber SL, Cantley LC (2008) The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452(7184):230–233. doi:10.1038/nature06734
Chung Y, Jue T (1992) 1H NMR observation of redox potential in liver. Biochemistry 31(45):11159–11165
Cook JA, Gius D, Wink DA, Krishna MC, Russo A, Mitchell JB (2004) Oxidative stress, redox, and the tumor microenvironment. Semin Radiat Oncol 14(3):259–266
Dang CV (1999) c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol Cell Biol 19:1–11
Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, Tsien RY (2004) Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem 279(21):22284–22293
Dorward A, Sweet S, Moorehead R, Singh G (1997) Mitochondrial contributions to cancer cell physiology: redox balance, cell cycle, and drug resistance. J Bioenerg Biomembr 29(4):385–392
Drezek R, Brookner C, Pavlova I, Boiko I, Malpica A, Lotan R, Follen M, Richards-Kortum R (2001) Autofluorescence microscopy of fresh cervical-tissue sections reveals alterations in tissue biochemistry with dysplasia. Photochem Photobiol 73(6):636–641
Fidler IJ, Hart IR (1982) Biological diversity in metastatic neoplasms - origins and implications. Science 217(4564):998–1003
Fidler IJ, Kripke ML (1977) Metastasis results from preexisting variant cells within a malignant-tumor. Science 197(4306):893–895
Fisher AB, Furia L, Chance B (1976) Evaluation of redox state of isolated perfused rat lung. Am J Physiol 230(5):1198–1204
Gaustad JV, Benjaminsen IC, Graff BA, Brurberg KG, Ruud EBM, Rofstad EK (2005) Intratumor heterogeneity in blood perfusion in orthotopic human melanoma xenografts assessed by dynamic contrast-enhanced magnetic resonance imaging. J Magn Reson Imaging 21(6):792–800
Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, Stewart A, Tarpey P, Varela I, Phillimore B, Begum S, McDonald NQ, Butler A, Jones D, Raine K, Latimer C, Santos CR, Nohadani M, Eklund AC, Spencer-Dene B, Clark G, Pickering L, Stamp G, Gore M, Szallasi Z, Downward J, Futreal PA, Swanton C (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366(10):883–892
Gough NR (2009) Focus issue: the long and short of redox signaling. Sci Signal 2(90):eg12
Grek CL, Tew KD (2010) Redox metabolism and malignancy. Curr Opin Pharmacol 10(4):362–368
Gu Y, Qian Z, Chen J, Blessington D, Ramanujam N, Chance B (2002) High-resolution three-dimensional scanning optical image system for intrinsic and extrinsic contrast agents in tissue. Rev Sci Instrum 73(1):172–178
Gutscher M, Pauleau AL, Marty L, Brach T, Wabnitz GH, Samstag Y, Meyer AJ, Dick TP (2008) Real-time imaging of the intracellular glutathione redox potential. Nature Methods 5(6):553–559
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674
Haselgrove JC, Bashford CL, Barlow CH, Quistorff B, Chance B, Mayevsky A (1990) Time resolved 3-dimensional recording of redox ratio during spreading depression in gerbil brain. Brain Res 506(1):109–114
Hassinen I, Chance B (1968) Oxidation-reduction properties of the mitochondrial flavoprotein chain. Biochem Biophys Res Commun 31(6):895–900
Hsu PP, Sabatini DM (2008) Cancer cell metabolism: Warburg and beyond. Cell 134(5):703–707
Hung Yin P, Albeck John G, Tantama M, Yellen G (2011) Imaging cytosolic NADH-NAD+ redox state with a genetically encoded fluorescent biosensor. Cell Metabolism 14(4):545–554
Hyodo F, Matsumoto K, Matsumoto A, Mitchell JB, Krishna MC (2006) Probing the intracellular redox status of tumors with magnetic resonance imaging and redox-sensitive contrast agents. Cancer Res 66(20):9921–9928
Hyodo F, Murugesan R, Matsumoto K, Hyodo E, Subramanian S, Mitchell JB, Krishna MC (2008) Monitoring redox-sensitive paramagnetic contrast agent by EPRI, OMRI and MRI. J Magn Reson 190(1):105–112
Ido Y (2007) Pyridine nucleotide redox abnormalities in diabetes. Antioxid Redox Signal 9(7):931–942
Ishikawa K, Koshikawa N, Takenaga K, Nakada K, Hayashi JI (2008a) Reversible regulation of metastasis by ROS-generating mtDNA mutations. Mitochondrion 8(4):339–344
Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, Imanishi H, Nakada K, Honma Y, Hayashi J (2008b) ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320(5876):661–664
Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, Oshima M, Ikeda T, Asaba R, Yagi H, Masuko T, Shimizu T, Ishikawa T, Kai K, Takahashi E, Imamura Y, Baba Y, Ohmura M, Suematsu M, Baba H, Saya H (2011) CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc and thereby promotes tumor growth. Cancer Cell 19(3):387–400
Kaelin WG, Thompson CB (2010) Q&A: cancer: clues from cell metabolism. Nature 465(7298):562–564
Keshari KR, Kurhanewicz J, Bok R, Larson PEZ, Vigneron DB, Wilson DM (2011) Hyperpolarized (13)C dehydroascorbate as an endogenous redox sensor for in vivo metabolic imaging. Proc Natl Acad Sci U S A 108(46):18606–18611
King A, Selak MA, Gottlieb E (2006) Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 25(34):4675–4682
Kitai T, Tanaka A, Tokuka A, Ozawa K, Iwata S, Chance B (1992) Changes in the redox distribution of rat liver by ischemia. Anal Biochem 206(1):131–136
Koppenol WH, Bounds PL, Dang CV (2011) Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer 11(5):325–337. doi:10.1038/nrc3038
Lehninger AL, Nelson DL, Cox MM (1993) Principles of biochemistry, 2nd edn. Worth Publishers, New York
Lemasters JJ, Nieminen AL (2001) Mitochondria in pathogenesis. Kluwer Academic/Plenum Publishers, New York
Levitt JM, McLaughlin-Drubin ME, Munger K, Georgakoudi I (2011) Automated biochemical, morphological, and organizational assessment of precancerous changes from endogenous two-photon fluorescence images. PLoS One 6(9)
Li LZ, Xu HN, Ranji M, Nioka S, Chance B (2009a) Mitochondrial redox imaging for cancer diagnostic and therapeutic studies. Journal of Innovative Optical Health Sciences 2:325–341
Li LZ, Zhou R, Xu HN, Moon L, Zhong TX, Kim EJ, Qiao H, Reddy R, Leeper D, Chance B, Glickson JD (2009b) Quantitative magnetic resonance and optical imaging biomarkers of melanoma metastatic potential. Proc Natl Acad Sci U S A 106(16):6608–6613
Li LZJ, Zhou R, Zhong TX, Moon L, Kim EJ, Qiao H, Pickup S, Hendrix MJ, Leeper D, Chance B, Glickson JD (2007) Predicting melanoma metastatic potential by optical and magnetic resonance imaging. In: Maguire DJ, Bruley DF, Harrison DK (eds) Oxygen transport to tissue Xxviii (Vol. 599, Advances in Experimental Medicine and Biology). Springer, Berlin, pp 67–78
Lisanti MP, Martinez-Outschoorn UE, Lin Z, Pavlides S, Whitaker-Menezes D, Pestell RG, Howell A, Sotgia F (2011) Hydrogen peroxide fuels aging, inflammation, cancer metabolism and metastasis The seed and soil also needs “fertilizer”. Cell Cycle 10(15):2440–2449
Liu Q, Grant G, Li JJ, Zhang Y, Hu FY, Li SQ, Wilson C, Chen K, Bigner D, Tuan VD (2011) Compact point-detection fluorescence spectroscopy system for quantifying intrinsic fluorescence redox ratio in brain cancer diagnostics. J Biomed Opt 16(3)
Locasale Jason W, Cantley Lewis C (2011) Metabolic flux and the regulation of mammalian cell growth. Cell Metabolism 14(4):443–451
Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T, Thompson CB (2005) Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120(2):237–248
Ma X-H, Piao S, Wang D, McAfee QW, Nathanson KL, Lum JJ, *Li LZ, *Amaravadi RK (Equal contribution) (2011) Measurements of tumor cell autophagy predict invasiveness, resistance to chemotherapy, and survival in melanoma. Clin Canc Res 17(10):3478–3489
Mac Manus M, Hicks RJ (2008) The use of positron emission tomography (PET) in the staging/evaluation, treatment, and follow-up of patients with lung cancer: a critical review. Int J Radiat Oncol Biol Phys 72(5):1298–1306
Maccarrone M, Brune B (2009) Redox regulation in acute and chronic inflammation. Cell Death Differ 16(8):1184–1186
Masters BR, Falk S, Chance B (1981) In vivo flavoprotein redox measurements of rabbit corneal normoxic-anoxic transitions. Curr Eye Res 1(10):623–627
Matsumoto K, Hyodo F, Matsumoto A, Koretsky AP, Sowers AL, Mitchell JB, Krishna MC (2006) High-resolution mapping of tumor redox status by magnetic resonance imaging using nitroxides as redox-sensitive contrast agents. Clin Cancer Res 12(8):2455–2462
Mayevsky A (2009) Mitochondrial function and energy metabolism in cancer cells: past overview and future perspectives. Mitochondrion 9(3):165–179
Mayevsky A, Rogatsky GG (2007) Mitochondrial function in vivo evaluated by NADH fluorescence: from animal models to human studies. Am J Physiol Cell Physiol 292(2):C615–640
Mayevsky A, Zarchin N, Kaplan H, Haveri J, Haselgroove J, Chance B (1983) Brain metabolic responses to ischemia in the mongolian gerbil: in vivo and freeze trapped redox scanning. Brain Res 276(1):95–107
Modica-Napolitano JS, Kulawiec M, Singh KK (2007) Mitochondria and human cancer. Curr Mol Med 7(1):121–131
Mueller-Klieser W, Kroeger M, Walenta S, Rofstad EK (1991) Comparative imaging of structure and metabolites in tumors. Int J Radiat Biol 60(1–2):147–159
Mueller-Klieser W, Walenta S (1993) Geographical mapping of metabolites in biological tissue with quantitative bioluminescence and single photon imaging. Histochem J 25(6):407–420
Nichols MG, Barth EE, Nichols JA (2005) Reduction in DNA synthesis during two-photon microscopy of intrinsic reduced nicotinamide adenine dinucleotide fluorescence. Photochem Photobiol 81(2):259–269
Nkabyo YS, Ziegler TR, Gu LH, Watson WH, Jones DP (2002) Glutathione and thioredoxin redox during differentiation in human colon epithelial (Caco-2) cells. Am J Physiol Gastrointest Liver Physiol 283(6):G1352–G1359
Nowell PC (1976) Clonal evolution of tumor-cell populations. Science 194(4260):23–28
Olovnikov IA, Kravchenko JE, Chumakova PM (2009) Homeostatic functions of the p53 tumor suppressor: regulation of energy metabolism and antioxidant defense. Semin Canc Biol 19(1):32–41
Olschewski A, Hong ZG, Peterson DA, Nelson DP, Porter VA, Weir EK (2004) Opposite effects of redox status on membrane potential, cytosolic calcium, and tone in pulmonary arteries and ductus arteriosus. Am J Physiol Lung Cell Mol Physiol 286(1):L15–L22
Orrenius S, Gogvadze A, Zhivotovsky B (2007) Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol 47:143–183
Ozawa K, Chance B, Tanaka A, Iwata S, Kitai T, Ikai I (1992) Linear correlation between acetoacetate beta-hydroxybutyrate in arterial blood and oxidized flavoprotein reduced pyridine-nucleotide in freeze-trapped human liver-tissue. Biochimica Et Biophysica Acta 1138(4):350–352
Pani G, Galeotti T, Chiarugi P (2010) Metastasis: cancer cell’s escape from oxidative stress. Cancer Metastasis Rev 29:351–378
Pani G, Giannoni E, Galeotti T, Chiarugi P (2009) Redox-based escape mechanism from death: the cancer lesson. Antioxidants & Redox Signaling 11:2791–2806
Pedersen PL (2007) Warburg, me and hexokinase 2: multiple discoveries of key molecular events underlying one of cancers’ most common phenotypes, the “Warburg Effect”, i.e., elevated glycolysis in the presence of oxygen. J Bioenerg Biomembr 39(3):211–222
Pelicano H, Lu W, Zhou Y, Zhang W, Chen Z, Hu Y, Huang P (2009) Mitochondrial dysfunction and reactive oxygen species imbalance promote breast cancer cell motility through a CXCL14-mediated mechanism. Cancer Res 69(6):2375–2383
Puppi A, Dely M (1983) Tissue redox-state potential (E0) – As regulator of physiological processes. Acta Biologica Hungarica 34:323–350
Quistorff B, Haselgrove JC, Chance B (1985) High resolution readout of 3-D metabolic organ structure: an automated, low-temperature redox ratio-scanning instrument. Anal Biochem 148:389–400
Quon A, Gambhir SS (2005) FDG-PET and beyond: molecular breast cancer imaging. J Clin Oncol 23(8):1664–1673
Ramanujam N, Richards-Kortum R, Thomsen S, Mahadevan-Jansen A, Follen M, Chance B (2001) Low temperature fluorescence imaging of freeze-trapped human cervical tissues. Opt Express 8(6):335–343
Ramanujan VK, Zhang JH, Biener E, Herman B (2005) Multiphoton fluorescence lifetime contrast in deep tissue imaging: prospects in redox imaging and disease diagnosis. J Biomed Opt 10(5)
Ranji M, Nioka S, Xu N, Wu B, Li LZ, Jaggard DL, Chance B (2009) Fluorescent images of mitochondrial redox states in in situ mouse hypoxic ischemic intestines. Journal of International Optical Health Sciences 2:365–374
Rocheleau JV, Head WS, Piston DW (2004) Quantitative NAD(P)H/flavoprotein autofluorescence imaging reveals metabolic mechanisms of pancreatic islet pyruvate response. J Biol Chem 279(30):31780–31787
Sarsour EH, Kumar MG, Chaudhuri L, Kalen AL, Goswami PC (2009) Redox control of the cell cycle in health and disease. Antioxid Redox Signal 11:2985–3011
Sato B, Tanaka A, Mori S, Yanabu N, Kitai T, Tokuka A, Inomoto T, Iwata S, Yamaoka Y, Chance B (1995) Quantitative analysis of redox gradient within the rat liver acini by fluorescence images: effects of glucagon perfusion. Biochim Biophys Acta 1268(1):20–26
Sattlar UGA, Walenta S, Mueller-Klieser W (2007) A bioluminescence technique for quantitative and structure-associated imaging of pyruvate. Lab Investig 87(1):84–92
Sattler UGA, Walenta S, Mueller-Klieser W (2007) Lactate and redox status in malignant tumors. Anaesthesist 56(5):466–469
Scholz R, Thurman RG, Williamson JR, Chance B, Bucher T (1969) Flavin and pyridine nucleotide oxidation-reduction changes in perfused rat liver. I. Anoxia and subcellular localization of fluorescent flavoproteins. J Biol Chem 244(9):2317–2324
Schroeder T, Yuan H, Viglianti BL, Peltz C, Asopa S, Vujaskovic Z, Dewhirst MW (2005) Spatial heterogeneity and oxygen dependence of glucose consumption in R3230Ac and fibrosarcomas of the Fischer 344 rat. Cancer Res 65(12):5163–5171
Semenza GL (2010) HIF-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev 20(1):51–56
Senda T, Senda M, Kimura S, Ishida T (2009) Redox control of protein conformation in flavoproteins. Antioxid Redox Signal 11(7):1741–1766
Shah SP, Roth A, Goya R, Oloumi A, Ha G, Zhao Y, Turashvili G, Ding J, Tse K, Haffari G, Bashashati A, Prentice LM, Khattra J, Burleigh A, Yap D, Bernard V, McPherson A, Shumansky K, Crisan A, Giuliany R, Heravi-Moussavi A, Rosner J, Lai D, Birol I, Varhol R, Tam A, Dhalla N, Zeng T, Ma K, Chan SK, Griffith M, Moradian A, Cheng SWG, Morin GB, Watson P, Gelmon K, Chia S, Chin S-F, Curtis C, Rueda OM, Pharoah PD, Damaraju S, Mackey J, Hoon K, Harkins T, Tadigotla V, Sigaroudinia M, Gascard P, Tlsty T, Costello JF, Meyer IM, Eaves CJ, Wasserman WW, Jones S, Huntsman D, Hirst M, Caldas C, Marra MA, Aparicio S (2012) The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature, advance online publication. doi:10.1038/nature10933
Shiino A, Haida M, Beauvoit B, Chance B (1999) Three-dimensional redox image of the normal gerbil brain. Neuroscience 91(4):1581–1585
Skala MC, Riching KM, Gendron-Fitzpatrick A, Eickhoff J, Eliceiri KW, White JG, Ramanujam N (2007a) In vivo multiphoton microscopy of NADH and FAD redox states, fluorescence lifetimes, and cellular morphology in precancerous epithelia. [Research Support, N.I.H., Extramural Research Support, U.S. Gov’t, Non-P.H.S.]. Proc Natl Acad Sci U S A 104(49):19494–19499
Skala MC, Riching KM, Gendron-Fitzpatrick A, Eickhoff J, Eliceiri KW, White JG, Ramanujam N (2007b) 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
Tachtsidis I, Tisdall MM, Pritchard C, Leung TS, Ghosh A, Elwell CE, Smith M (2011) Analysis of the changes in the oxidation of brain tissue cytochrome-c-oxidase in traumatic brain injury patients during hypercapnoea a broadband NIRS study. In: LaManna JC, Puchowicz MA, Xu K, Harrison DK, Bruley DF (eds) Oxygen transport to tissue Xxxii (Vol. 701, Advances in Experimental Medicine and Biology). Springer, Berlin, pp 9–14
Taylor BL, Rebbapragada A, Johnson MS (2001) The FAD-PAS domain as a sensor for behavioral responses in escherichia coli. Antioxid Redox Signal 3(5):867–879
Thompson CB (2009) Metabolic enzymes as oncogenes or tumor suppressors. N Engl J Med 360(8):813–815
Tisdall MM, Tachtsidis I, Leung TS, Elwell CE, Smith M (2007) Near-infrared spectroscopic quantification of changes in the concentration of oxidized cytochrome c oxidase in the healthy human brain during hypoxemia. J Biomed Opt 12(2)
Veech RL (2006) The determination of the redox states and phosphorylation potential in living tissues and their relationship to metabolic control of disease phenotypes. Biochem Mol Biol Educ 34(3):168–179
Weir EK, Hong ZG, Porter VA, Reeve HL (2002) Redox signaling in oxygen sensing by vessels. Respir Physiol Neurobiol 132(1):121–130
Xu HN, Addis RC, Goings DF, Nioka S, Chance B, Gearhart JD, Li LZ (2011a) Imaging redox state heterogeneity within individual embryonic stem cell colonies. Journal of Innovative Optical Health Sciences 4:279–288
Xu HN, Nioka S, Chance B, Li LZ (2011b) Heterogeneity of mitochondrial redox state in premalignant pancreas in a PTEN null transgenic mouse model. Adv Exp Med Biol 701:207–213
Xu HN, Nioka S, Chance B, Zheng G, Li LZ (2011c) High-resolution simultaneous mapping of mitochondrial redox state and glucose uptake in human breast tumor xenografts. In: Advances in experimental medicine and biology (Vol. 737, Advances in Experimental Medicine and Biology). Springer, New York, pp 175–179
Xu HN, Nioka S, Glickson J, Chance B, Li LZ (2010) Quantitative mitochondrial redox imaging of breast cancer metastatic potential. J Biomed Opt 15:036010
Xu HN, Tchou J, Chance B, Li LZ (2012) Imaging the redox states of human breast cancer core biopsies. Adv Exp Med Biol
Xu HN, Wu B, Nioka S, Chance B, Li LZ (2009a) Calibration of CCD-based redox imaging for biological tissues. Paper presented at the Proceedings of SPIE - Medical Imaging 2009: Biomedical Applications in Molecular, Structural, and Functional Imaging, Lake Buena Vista, FL, USA
Xu HN, Wu B, Nioka S, Chance B, Li LZ (2009b) Quantitative redox scanning of tissue samples using a calibration procedure. Journal of Innovative Optical Health Sciences 2:375–385
Xu HN, Zhou R, Nioka S, Chance B, Glickson JD, Li LZ (2009c) Histological basis of MR/optical imaging of human melanoma mouse xenografts spanning a range of metastatic potentials. Adv Exp Med Biol 645:247–253
Ying WH (2008) NAD(+)/ NADH and NADP(+)/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid Redox Signal 10(2):179–206
Zhang Q, Wang SY, Nottke AC, Rocheleau JV, Piston DW, Goodman RH (2006) Redox sensor CtBP mediates hypoxia-induced tumor cell migration. Proc Natl Acad Sci U S A 103(24):9029–9033
Zhang Z, Blessington D, Li H, Busch TM, Glickson J, Luo Q, Chance B, Zheng G (2004a) Redox ratio of mitochondria as an indicator for the response of photodynamic therapy. J Biomed Opt 9(4):772–778
Zhang ZH, Li H, Liu Q, Zhou LL, Zhang M, Luo QM, Glickson J, Chance B, Zheng G (2004b) Metabolic imaging of tumors using intrinsic and extrinsic fluorescent markers. Biosens Bioelectron 20(3):643–650
Zhu C, Burnside ES, Sisney GA, Salkowski LR, Harter JM, Yu B, Ramanujam N (2009) Fluorescence spectroscopy: an adjunct diagnostic tool to image-guided core needle biopsy of the breast. IEEE Trans Biomed Eng 56(10):2518–2528
Ziegler M (2005) A vital link between energy and signal transduction. Regulatory functions of NAD(P). FEBS J 272(18):4561–4564
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Li, L.Z. Imaging mitochondrial redox potential and its possible link to tumor metastatic potential. J Bioenerg Biomembr 44, 645–653 (2012). https://doi.org/10.1007/s10863-012-9469-5
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10863-012-9469-5