In vivo imaging of cerebral energy metabolism with two-photon fluorescence lifetime microscopy of NADH

Biomedical Optics Express

Volumn 4, Issue 2, 2013, Pages 307-321

  Yaseen, Mohammad A ^a   Sakadžić, Sava ^a   Wu, Weicheng ^a   Becker, Wolfgang ^b   Kasischke, Karl A ^c   Boas, David A ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BECKER AND HICKL GMBH   (Germany)

^c UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENCE; PHOTONS;

AUTOFLUORESCENCE LIFETIME; CELLULAR ENERGY; ENERGY METABOLISM; FLUORESCENCE DECAYS; HIGH RESOLUTION; IN-VIVO; IN-VIVO IMAGING; INDIVIDUAL COMPONENTS; MINIMALLY INVASIVE; MOLECULAR PATHWAYS; NADH FLUORESCENCE; OXIDATIVE METABOLISM; PATHOPHYSIOLOGY; SPECIALIZED SOFTWARE; TIME-CORRELATED SINGLE PHOTON COUNTING; TRANSIENT BEHAVIOR; TWO PHOTON IMAGING; TWO-PHOTON FLUORESCENCE LIFETIME;

METABOLISM;

RATTUS;

EID: 84873276386     PISSN: None     EISSN: 21567085     Source Type: Journal    
DOI: 10.1364/BOE.4.000307     Document Type: Article

References (54)

1. L. Sokoloff, "The physiological and biochemical bases of functional brain imaging," Cogn Neurodyn 2(1), 1-5 (2008).
2. D. C. Wallace, "A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine," Annu. Rev. Genet. 39(1), 359-407 (2005).
3. M. Monsalve, S. Borniquel, I. Valle, and S. Lamas, "Mitochondrial dysfunction in human pathologies," Front. Biosci. 12(1), 1131-1153 (2007).
4. M. R. Duchen, "Mitochondria in health and disease: perspectives on a new mitochondrial biology," Mol. Aspects Med. 25(4), 365-451 (2004).
5. F. Hyder, "Dynamic imaging of brain function," in Dynamic Brain Imaging: Multi-Modal Methods and In vivo Applications, F. Hyder, ed. (Humana, Totowa, NJ, 2009), pp. 3-21.
6. B. Chance, P. Cohen, F. Jobsis, and B. Schoener, "Intracellular oxidation-reduction states in vivo: the microfluorometry of pyridine nucleotide gives a continuous measurement of the oxidation state," Science 137(3529), 499-508 (1962).
7. A. A. Heikal, "Intracellular coenzymes as natural biomarkers for metabolic activities and mitochondrial anomalies," Biomarkers Med. 4(2), 241-263 (2010).
8. B. Chance and B. Thorell, "Localization and kinetics of reduced pyridine nucleotide in living cells by microfluorometry," J. Biol. Chem. 234, 3044-3050 (1959).
9. K. Svoboda and R. Yasuda, "Principles of two-photon excitation microscopy and its applications to neuroscience," Neuron 50(6), 823-839 (2006).
10. G. H. Patterson, S. M. Knobel, P. Arkhammar, O. Thastrup, and D. W. Piston, "Separation of the glucosestimulated cytoplasmic and mitochondrial NAD(P)H responses in pancreatic islet β cells," Proc. Natl. Acad. Sci. U.S.A. 97(10), 5203-5207 (2000).
11. S. Huang, A. A. Heikal, and W. W. Webb, "Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein," Biophys. J. 82(5), 2811-2825 (2002).
12. W. R. Zipfel, R. M. Williams, R. Christie, A. Y. Nikitin, B. T. Hyman, and W. W. Webb, "Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation," Proc. Natl. Acad. Sci. U.S.A. 100(12), 7075-7080 (2003).
13. K. A. Kasischke, H. D. Vishwasrao, P. J. Fisher, W. R. Zipfel, and W. W. Webb, "Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis," Science 305(5680), 99-103 (2004).
14. W. Becker, Advanced Time-Correlated Single Photon Counting Techniques (Springer, Berlin, 2005).
15. M. Y. Berezin and S. Achilefu, "Fluorescence lifetime measurements and biological imaging," Chem. Rev. 110(5), 2641-2684 (2010).
16. J. R. Lakowicz, Principles of Fluorescence Spectroscopy (Springer, New York, 2006).
17. D. F. Eaton, "Recommended methods for fluorescence decay analysis," Pure Appl. Chem. 62(8), 1631-1648 (1990).
18. R. Niesner, B. Peker, P. Schlüsche, and K.-H. Gericke, "Noniterative biexponential fluorescence lifetime imaging in the investigation of cellular metabolism by means of NAD(P)H autofluorescence," ChemPhysChem 5(8), 1141-1149 (2004).
19. H. D. Vishwasrao, A. A. Heikal, K. A. Kasischke, and W. W. Webb, "Conformational dependence of intracellular NADH on metabolic state revealed by associated fluorescence anisotropy," J. Biol. Chem. 280(26), 25119-25126 (2005).
20. Q. Yu and A. A. Heikal, "Two-photon autofluorescence dynamics imaging reveals sensitivity of intracellular NADH concentration and conformation to cell physiology at the single-cell level," J. Photochem. Photobiol. B 95(1), 46-57 (2009).
21. T. H. Chia, A. Williamson, D. D. Spencer, and M. J. Levene, "Multiphoton fluorescence lifetime imaging of intrinsic fluorescence in human and rat brain tissue reveals spatially distinct NADH binding," Opt. Express 16(6), 4237-4249 (2008).
22. 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).
23. C. Stringari, A. Cinquin, O. Cinquin, M. A. Digman, P. J. Donovan, and E. Gratton, "Phasor approach to fluorescence lifetime microscopy distinguishes different metabolic states of germ cells in a live tissue," Proc. Natl. Acad. Sci. U.S.A. 108(33), 13582-13587 (2011).
24. S. Sakadžić, E. Roussakis, M. A. Yaseen, E. T. Mandeville, V. J. Srinivasan, K. Arai, S. Ruvinskaya, A. Devor, E. H. Lo, S. A. Vinogradov, and D. A. Boas, "Two-photon high-resolution measurement of partial pressure of oxygen in cerebral vasculature and tissue," Nat. Methods 7(9), 755-759 (2010).
25. M. A. Yaseen, V. J. Srinivasan, S. Sakadžić, H. Radhakrishnan, I. Gorczynska, W. Wu, J. G. Fujimoto, and D. A. Boas, "Microvascular oxygen tension and flow measurements in rodent cerebral cortex during baseline conditions and functional activation," J. Cereb. Blood Flow Metab. 31(4), 1051-1063 (2011).
26. L. K. Klaidman, A. C. Leung, and J. D. Adams, Jr., "High-performance liquid chromatography analysis of oxidized and reduced pyridine dinucleotides in specific brain regions," Anal. Biochem. 228(2), 312-317 (1995).
27. R. Guarneri and V. Bonavita, "Nicotinamide adenine dinucleotides in the developing rat brain," Brain Res. 2(2), 145-150 (1966).
28. Y. Avi-Dor, J. M. Olson, M. D. Doherty, and N. O. Kaplan, "Fluorescence of pyridine nucleotides in mitochondria," J. Biol. Chem. 237, 2377-2383 (1962).
29. V. V. Ghukasyan and F.-J. Kao, "Monitoring cellular metabolism with fluorescence lifetime of reduced nicotinamide adenine dinucleotide," J. Phys. Chem. C 113(27), 11532-11540 (2009).
30. E. Gratton, S. Breusegem, J. Sutin, Q. Ruan, and N. Barry, "Fluorescence lifetime imaging for the two-photon microscope: time-domain and frequency-domain methods," J. Biomed. Opt. 8(3), 381-390 (2003).
31. M. Van Den Zegel, N. Boens, D. Daems, and F. C. De Schryver, "Possibilities and limitations of the timecorrelated single photon counting technique: a comparative study of correction methods for the wavelength dependence of the instrument response function," Chem. Phys. 101(2), 311-335 (1986).
32. A. Habenicht, J. Hjelm, E. Mukhtar, F. Bergström, and L. B.-Å. Johansson, "Two-photon excitation and timeresolved fluorescence: I. The proper response function for analysing single-photon counting experiments," Chem. Phys. Lett. 354(5-6), 367-375 (2002).
33. K. Blinova, S. Carroll, S. Bose, A. V. Smirnov, J. J. Harvey, J. R. Knutson, and R. S. Balaban, "Distribution of mitochondrial NADH fluorescence lifetimes: steady-state kinetics of matrix NADH interactions," Biochemistry 44(7), 2585-2594 (2005).
34. E. Baraghis, A. Devor, Q. Fang, V. J. Srinivasan, W. Wu, F. Lesage, C. Ayata, K. A. Kasischke, D. A. Boas, and S. Sakadzić, "Two-photon microscopy of cortical NADH fluorescence intensity changes: correcting contamination from the hemodynamic response," J. Biomed. Opt. 16(10), 106003 (2011).
35. A. Nimmerjahn, F. Kirchhoff, J. N. D. Kerr, and F. Helmchen, "Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo," Nat. Methods 1(1), 31-37 (2004).
36. A. Gafni and L. Brand, "Fluorescence decay studies of reduced nicotinamide adenine dinucleotide in solution and bound to liver alcohol dehydrogenase," Biochemistry 15(15), 3165-3171 (1976).
37. M. Wakita, G. Nishimura, and M. Tamura, "Some characteristics of the fluorescence lifetime of reduced pyridine nucleotides in isolated mitochondria, isolated hepatocytes, and perfused rat liver in situ," J. Biochem. 118(6), 1151-1160 (1995).
38. T. G. Scott, R. D. Spencer, N. J. Leonard, and G. Weber, "Synthetic spectroscopic models related to coenzymes and base pairs. V. Emission properties of NADH. Studies of fluorescence lifetimes and quantum efficiencies of NADH, AcPyADH, [reduced acetylpyridineadenine dinucleotide] and simplified synthetic models," J. Am. Chem. Soc. 92(3), 687-695 (1970).
39. D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, and N. Ramanujam, "Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH," Cancer Res. 65(19), 8766-8773 (2005).
40. V. K. Ramanujan, J. A. Jo, G. Cantu, and B. A. Herman, "Spatially resolved fluorescence lifetime mapping of enzyme kinetics in living cells," J. Microsc. 230(3), 329-338 (2008).
41. D. Li, W. Zheng, and J. Y. Qu, "Time-resolved spectroscopic imaging reveals the fundamentals of cellular NADH fluorescence," Opt. Lett. 33(20), 2365-2367 (2008).
42. M. W. Conklin, P. P. Provenzano, K. W. Eliceiri, R. Sullivan, and P. J. Keely, "Fluorescence lifetime imaging of endogenous fluorophores in histopathology sections reveals differences between normal and tumor epithelium in carcinoma in situ of the breast," Cell Biochem. Biophys. 53(3), 145-157 (2009).
43. Y. Sun, J. Phipps, D. S. Elson, H. Stoy, S. Tinling, J. Meier, B. Poirier, F. S. Chuang, D. G. Farwell, and L. Marcu, "Fluorescence lifetime imaging microscopy: in vivo application to diagnosis of oral carcinoma," Opt. Lett. 34(13), 2081-2083 (2009).
44. C. A. Thorling, X. Liu, F. J. Burczynski, L. M. Fletcher, G. C. Gobe, and M. S. Roberts, "Multiphoton microscopy can visualize zonal damage and decreased cellular metabolic activity in hepatic ischemia-reperfusion injury in rats," J. Biomed. Opt. 16(11), 116011 (2011).
45. D. L. Nelson and M. M. Cox, Lehninger Principles of Biochemistry (W.H. Freeman, New York, 2008).
46. A. Devor, S. Sakadžić, P. A. Saisan, M. A. Yaseen, E. Roussakis, V. J. Srinivasan, S. A. Vinogradov, B. R. Rosen, R. B. Buxton, A. M. Dale, and D. A. Boas, "'Overshoot' of O2 is required to maintain baseline tissue oxygenation at locations distal to blood vessels," J. Neurosci. 31(38), 13676-13681 (2011).
47. 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).
48. N. D. Kirkpatrick, C. Zou, M. A. Brewer, W. R. Brands, R. A. Drezek, and U. Utzinger, "Endogenous fluorescence spectroscopy of cell suspensions for chemopreventive drug monitoring," Photochem. Photobiol. 81(1), 125-134 (2005).
49. T. A. Wang, Y. V. Yu, G. Govindaiah, X. Ye, L. Artinian, T. P. Coleman, J. V. Sweedler, C. L. Cox, and M. U. Gillette, "Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons," Science 337(6096), 839-842 (2012).
50. S. K. Shankar, "Biology of aging brain," Indian J. Pathol. Microbiol. 53(4), 595-604 (2010).
51. J. V. Rocheleau, W. S. Head, and D. W. Piston, "Quantitative NAD(P)H/flavoprotein autofluorescence imaging reveals metabolic mechanisms of pancreatic islet pyruvate response," J. Biol. Chem. 279(30), 31780-31787 (2004).
52. J. R. Lakowicz, ed., Principles of Fluorescence Spectroscopy (Springer, New York, 2006).
53. M. vandeVen, M. Ameloot, B. Valeur, and N. Boens, "Pitfalls and their remedies in time-resolved fluorescence spectroscopy and microscopy," J. Fluoresc. 15(3), 377-413 (2005).
54. M. Köllner and J. Wolfrum, "How many photons are necessary for fluorescence-lifetime measurements?" Chem. Phys. Lett. 200(1-2), 199-204 (1992).