Probing the impact of gamma-irradiation on the metabolic state of neural stem and precursor cells using dual-wavelength intrinsic signal two-photon excited fluorescence

Journal of Innovative Optical Health Sciences

Volumn 4, Issue 3, 2011, Pages 289-300

  Krasieva, Tatiana B ^a   Giedzinski, Erich ^b   Tran, Katherine ^b   Lan, Mary ^b   Limoli, Charles L ^b   Tromberg, Bruce J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

brain tumors; cellular metabolic index; flavoproteins; gamma radiation; Multiphoton microscopy; NAD(P)H

Indexed keywords

BRAIN TUMORS; CELLULAR METABOLIC INDEX; FLAVOPROTEINS; MULTI-PHOTON MICROSCOPY; NAD(P)H;

AMIDES; CELL PROLIFERATION; EXCITED STATES; FLUORESCENCE; IRRADIATION; METABOLISM; PHOTONS; RADIATION EFFECTS; THREE DIMENSIONAL;

STEM CELLS;

EID: 79960798368     PISSN: 17935458     EISSN: 17937205     Source Type: Journal    
DOI: 10.1142/S1793545811001629     Document Type: Article

References (59)

1. O. K. Abayomi,"Pathogenesis of irradiationinduced cognitive dysfunction," Acta. Oncol. 35(6), 659-663 (1996).
2. P. J. Tofilon, J. R. Fike,"The radioresponse of the central nervous system: A dynamic process," Radiat. Res. 153(4), 357-370 (2000). (Pubitemid 30185388)
3. C. A. Meyers, P. D. Brown,"Role and relevance of neurocognitive assessment in clinical trials of patients with CNS tumors," J. Clin. Oncol. 24(8), 1305-1309 (2006). (Pubitemid 46622034)
4. J. R. Fike, S. Rosi, C. L. Limoli,"Neural precursor cells and central nervous system radiation sensitivity," Semin. Radiat. Oncol. 19(2), 122-132 (2009).
5. C. D. Clelland, M. Choi, C. Romberg, G. D. Clemenson, Jr., A. Fragniere, P. Tyers, S. Jessberger, L. M. Saksida, R. A. Barker, F. H. Gage, T. J. Bussey,"A functional role for adult hippocampal neurogenesis in spatial pattern separation," Science 325 (5937), 210-213 (2009).
6. C. A. Meyers, F. Geara, P. F. Wong, W. H. Morrison,"Neurocognitive effects of therapeutic irradiation for base of skull tumors," Int. J. Radiat. Oncol. Biol. Phys. 46(1), 51-55 (2000). (Pubitemid 30021479)
7. T. D. Palmer, J. Takahashi, F. H. Gage,"The adult rat hippocampus contains primordial neural stem cells," Mol. Cell. Neurosci. 8(6), 389-404 (1997). (Pubitemid 127796477)
8. F. H. Gage,"Mammalian neural stem cells," Science 287(5457), 1433-1438 (2000). (Pubitemid 30127128)
9. E. Giedzinski, R. Rola, J. R. Fike, C. L. Limoli,"Efficient production of reactive oxygen species in neural precursor cells after exposure to 250 MeV protons," Radiat. Res. 164(4 Pt 2), 540-544 (2005). (Pubitemid 41368933)
10. C. Limoli, E. Giedzinski, R. Rola, S. Otsuka, T. Palmer, J. Fike,"Radiation response of neural precursor cells: Linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress," Radiat. Res. 161, 17-27 (2004). (Pubitemid 38018720)
11. C. L. Limoli, E. Giedzinski, J. Baure, R. Rola, J. R. Fike,"Altered growth and radiosensitivity in neural precursor cells subjected to oxidative stress," Int. J. Radiat. Biol. 82(9), 640-647 (2006). (Pubitemid 44581947)
12. C. L. Limoli, E. Giedzinski, J. Baure, R. Rola, J. R. Fike,"Redox changes induced in hippocampal precursor cells by heavy ion irradiation," Radiat. Environ. Biophys. 46(2), 167-172 (2007). (Pubitemid 46725997)
13. M. M. Acharya, M. L. Lan, V. H. Kan, N. H. Patel, E. Giedzinski, B. P. Tseng, C. L. Limoli,"Consequences of ionizing radiation-induced damage in human neural stem cells," Free Radic. Biol. Med. 49(2), 1846-1855 (2010).
14. J. R. Fike, R. Rola, C. L. Limoli,"Radiation response of neural precursor cells," Neurosurg. Clin. North Am. 18(1), 115 (2007).
15. A. Boveris,"Mitochondrial production of superoxide radical and hydrogen peroxide," Adv. Exp. Med. Biol. 78, 67-82 (1977).
16. A. Boveris, E. Cadenas,"Production of superoxide radicals and hydrogen peroxide in mitochondria," in Superoxide Dismutase, Vol. II, L. W. Oberley, ed., CRC Press, Boca Raton, FL, pp. 15-30.
17. D. Voet, J. G. Voet, C. W. Pratt,"Electron transport and oxidative phosphorylation, Chapter 17, in Fundamentals of Biochemistry, John Wiley & Sons, Inc, 492-525 (1999).
18. J. R. Collins-Underwood, W. Zhao, J. G. Sharpe, M. E. Robbins,"NADPH oxidase mediates radiation-induced oxidative stress in rat brain microvascular endothelial cells," Free Radic. Biol. Med. 45(6), 929-938 (2008).
19. Y. Wang, L. Liu, S. K. Pazhanisamy, H. Li, A. Meng, D. Zhou,"Total body irradiation causes residual bone marrow injury by induction of persistent oxidative stress in murine hematopoietic stem cells," Free Radic. Biol. Med. 48(2), 348-356 (2010).
20. B. Chance, H. Baltscheffsky,"Respiratory enzymes in oxidative phosphorylation," J. Biol. Chem. 233(3), 736-739 (1958).
21. B. Chance, P. Cohen, G. Jobsis, B. Schoener,"Intracellular oxidation-reduction states in vivo," Science 137, 499-508 (1962).
22. B. Chance, B. Schoener, R. Oshino, F. Itshak, Y. Nakase,"Oxidation- reduction ratio studies of mitochondria in freeze-trapped samples. NADH and flavoprotein fluorescence signals," J. Biol. Chem. 254(11), 11 (1979).
23. J. V. Rocheleau, H. W. Steven, D. W. Piston,"Quantitative NAD(P)H/flavoprotein auto-fluorescence imaging reveals metabolic mechanisms of pancreatic islet pyruvate response," J. Biol. Chem. 279(30), 31780-31787 (2004). (Pubitemid 39037850)
24. L. M. Tiede, S. M. Rocha-Sanchez, R. Hallworth, M. G. Nichols, K. Beisel,"Determination of hair cell metabolic state in isolated cochlear preparations by two-photon microscopy," J. Biomed. Opt. 12(2), 021004 (2007).
25. C. J. Zhuo Shuangmu, X. Jiang, X. Cheng, S. Xie,"Visualizing extracellular matrix and sensing fibroblasts metabolism in human dermis by nonlinear spectral imaging," Skin Res. Technol. 13(4), 406-411 (2007). (Pubitemid 47506404)
26. S. Zhuo, J. Chen, B. Yu, X. Jiang, T. Luo, Q. Liu, R. Chen, S. Xie,"Nonlinear optical microscopy of the bronchus," J. Biomed. Opt. 13(5), 7 (2008).
27. V. del Marisol, J. M. R. Cano, C. Y. Park, X. Gao, K. Mori, R. S.Chuck, P. L.Gehllach,"Demonstration by redox fluorometry that sulforaphane protects retinal pigment epithelial cells against oxidative stress," Invest. Ophthalmol. Visual Sci. 49(6), 2606-2612 (2008).
28. M. Ranji, M. Matsubara, B. G. Leshnower, R. H. Hinmon, D. L. Jaggard, B. Chance, R. C. Gorman, J. H. Gorman,"Quantifying acute myocardial injury using ratiometric fluorometry," IEEE Transact. Biomed. Eng. 56(5), 1556-1563 (2009).
29. Z. Zhang, D. Blessington, H. Li, T. M. Busch, J. Glickson, Q. Luo, B. Chance, G. Zheng,"Redox ratio of mitochondria as an indicator for the response of photodynamic therapy," J. Biomed. Opt. 9(4), 772-778 (2004).
30. L. Z. J. Li, Z. R. T. Zhong, L. Moon, E. J. Kim, H. Qiao, S. Pickup, M. J. Hendrix, D. Leeper, B. Chance, J. D. Glickson,"Predicting melanoma metastatic potential by optical and magnetic resonance imaging," in Oxygen Transport to Tissue XXVIII, D. J. Maguire, D. F. Bruely, D. K. Harrison, ed. pp. 67-78 (2007).
31. L. Z. Li, R. Zhou, H. N. Xu, L. Moon, T. Zhong, E. J. Kim, H. Qiao, R. Reddy, D. Leeper, B. Chance, J. D. Glicksona,"Quantitative magnetic resonance and optical imaging biomarkers of melanoma metastatic potential," PNAS 106(16), 6608-6613 (2009).
32. J. Smith, E. Ladi, M. Mayer-Prooschel, M. Noble,"Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell," PNAS 97(18), 10032-10037 (2000).
33. J. M. G. Reyes, S. Fermanian, F. Yang, S.-Y. Zhou, S. Herretes,D.B.Murphy, J. H. Elisseeff,R. S. Chuck,"Metabolic changes in mesenchymal stem cells in osteogenic medium measured by autofluorescence spectroscopy," Stem Cells 24, 1213-1217 (2006). (Pubitemid 44464689)
34. S. Huang, A. A. Heikal, W. W. Webb,"Two-photon fluorescence spectroscopy and microscopy of NAD (P)H and flavoprotein," Biophys. J. 82(5), 2811-2825 (2002). (Pubitemid 34441317)
35. R. Scholz,R.G.Thurman, J.R.Williamson, B.Chance, T. Bucher,"Flavin and pyridine nucleotide oxidationreduction changes in perfused rat liver. I. Anoxia and subcellular localization of fluorescent flavoproteins," J. Biol. Chem. 244(9), 2317-2324 (1969).
36. J. R. Koke, W. Wylie, M. Wills,"Sensitivity of flavoprotein fluorescence to oxidative state in single isolated heart cells," Cytobios. 32(127-128), 139-145 (1981). (Pubitemid 12122577)
37. A. Kindzelskii, H. R. Petty,"Fluorescence spectroscopic detection of mitochondrial flavoprotein redox oscillations and transient reduction of the NADPH oxidase-associated flavoprotein in leukocytes," Eur. Biophys. J. 33(4), 291-299 (2004). (Pubitemid 38915616)
38. D. Chorvat Jr., J. Kirchnerova, M. Cagalinec, J. Smolka, A. Mateasik, A. Chorvatova,"Spectral unmixing of flavin autofluorescence components in cardiacmyocytes," Biophys. J. 89(6), L55-L57 (2005). (Pubitemid 41725586)
39. G. H. Patterson, S. M. Knobel, P. Arkhammar, O. Thastrup, D. W. Piston,"Separation of the glucosestimulated cytoplasmic and mitochondrial NAD(P) H responses in pancreatic islet b cells," Proc. Natl. Acad. Sci. 97(10), 5 (2000).
40. A. Shiino, M. Matsuda, B. Chance,"Three-dimensional redox imaging of frozen-quenched brain and other organs," in Methods in Enzymology, Vol. 352, Elsevier, p. 8 (2002).
41. W. S. Kunz, W. Kunz,"Contribution of different enzymes to flavoprotein fluorescence of isolated rat liver mitochondria," Biochim. Biophys. Acta. 841 (3), 237-246 (1985). (Pubitemid 16217193)
42. V. Shneyvays, D. Leshem, Y. Shmist, T. Zinman, A. Shainberg,"Effects of menadione and its derivative on cultured cardiomyocytes with mitochondrial disorders," J. Mol. Cell. Cardiol. 39(1), 149-158 (2005). (Pubitemid 40836051)
43. J. K. Leach, G. Van Tuyle, P. S. Lin, R. Schmidt-Ullrich, R. B. Mikkelsen,"Ionizing radiationinduced, mitochondria-dependent generation of reactive oxygen/nitrogen," Cancer Res. 61(10), 3894-3901 (2001). (Pubitemid 32720947)
44. P. Venkatachalam, S. M. de Toledo, B. N. Pandey, L. A. Tephly, A. B. Carter, J. B. Little, D. R. Spitz, E. I. Azzam,"Regulation of normal cell cycle progression by flavin-containing oxidases," Oncogene 27(1), 20-31 (2008).
45. M. G. Vander Heiden, L. C. Cantley, C. B. Thompson,"Understanding the Warburg effect: The metabolic requirements of cell proliferation," Science 324(5930), 1029-1033 (2009).
46. N. C. Denko,"Hypoxia, HIF1 and glucose metabolism in the solid tumour," Nat. Rev. Cancer 8(9), 705-713 (2008).
47. D. R. Spitz, J. E. Sim, L. A. Ridnour, S. S. Galoforo, Y. J. Lee,"Glucose deprivation-induced oxidative stress in human tumor cells. A fundamental defect in metabolism? Ann. N. Y. Acad. Sci. 899, 349-362 (2000). (Pubitemid 30352799)
48. D. R. Spitz, E. I. Azzam, J. J. Li, D. Gius,"Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: A unifying concept in stress response biology," Cancer Metastasis Rev. 23(3-4), 311-322 (2004). (Pubitemid 38881814)
49. E. I. Azzam, S. M. de Toledo, J. B. Little,"Stress signaling from irradiated to non-irradiated cells," Curr. Cancer Drug Targets 4(1), 53-64 (2004). (Pubitemid 38332564)
50. S. M. de Toledo, N. Asaad, P. Venkatachalam, L. Li, R. W. Howell, D. R. Spitz, E. I. Azzam,"Adaptive responses to low-dose/low-dose-rate gamma rays in normal human fibroblasts: The role of growth architecture and oxidative metabolism," Radiat. Res. 166(6), 849-857 (2006). (Pubitemid 44888250)
51. K. Fishman, J. Baure, Y. Zou, T. T. Huang, M. Andres-Mach, R. Rola, T. Suarez, M. Acharya, C. L. Limoli, K. R. Lamborn, J. R. Fike, "Radiationinduced reductions in neurogenesis are ameliorated in mice deficient in CuZnSOD or MnSOD," Free Radic. Biol. Med. 47(10), 1459-1467 (2009).
52. R. Rola, Y. Zou, T. T. Huang, K. Fishman, J. Baure, S. Rosi, H. Milliken, C. L. Limoli, J. R. Fike,"Lack of extracellular superoxide dismutase (EC-SOD) in the microenvironment impacts radiation-induced changes in neurogenesis," Free Radic. Biol. Med. 42(8), 1133-1145 (2007); discussion 1131-112. (Pubitemid 46428514)
53. H. Matsui, Y. Murata, K.-I. Hirano, T. Sasaki, R. Shiba, H. Muto, T. Ono,"Hydrogen peroxidinduced cellular injury is associated with increase in endogenous fluorescence from rat gastric mucosal epithelial cell culture: A new method for detecting oxidative cellular onjury by fluorescence measurement," J. Gastroenterol. 33, 8 (1998).
54. S. W. Tuttle, A. Maity, P. R. Oprysko, A. V. Kachur, I. S. Ayene, J. E. Biaglow, C. J. Koch,"Detection of reactive oxygen species via endogenous oxidative pentose phosphate cycle activity in response to oxygen concentration: Implications for the mechanism of HIF-1alpha stabilization under moderate hypoxia," J. Biol. Chem. 282(51), 36790-36796 (2007).
55. S. Tuttle, T. Stamato, M. L. Perez, J. Biaglow,"Glucose-6-phosphate dehydrogenase and the oxidative pentose phosphate cycle protect cells against apoptosis induced by low doses of ionizing radiation," Radiat. Res. 153(6), 781-787 (2000). (Pubitemid 30349553)
56. J. K. Leach, S. M. Black, R. K. Schmidt-Ullrich, R. B. Mikkelsen,"Activation of constitutive nitricoxide synthase activity is an early signaling event induced by ionizing radiation," J. Biol. Chem. 277 (18), 15400-15406 (2002). (Pubitemid 34967802)
57. D. N. Criddle, S. Gillies, H. K. Baumgartner-Wilson, M. Jaffar, E. C. Chinje, S. Passmore, M. Chvanov, S. Barrow, O. V. Gerasimenko, A. V. Tepikin, R. Sutton, O. H. Petersen,"Menadione-induced reactive oxygen species generation via redox cycling promotes apoptosis of murine pancreatic acinar cells," J. Biol. Chem. 281(52), 40485-40492 (2006). (Pubitemid 46041851)
58. M. Ranji, S. Kanemoto, M. Matsubara, M. A. Grosso, J. H. Gorman, 3rd, R. C. Gorman, D. L. Jaggard, B. Chance,"Fluorescence spectroscopy and imaging of myocardial apoptosis," J. Biomed. Opt. 11(6), 064036 (2006).
59. S. Corda, C. Laplace, E. Vicaut, J. Duranteau,"Rapid reactive oxygen species production by mitochondria in endothelial cells exposed to tumor necrosis factor-alpha is mediated by ceramide," Am. J. Respir. Cell. Mol. Biol. 24(6), 762-768 (2001). (Pubitemid 32550600)