Radiation-induced reductions in neurogenesis are ameliorated in mice deficient in CuZnSOD or MnSOD

Free Radical Biology and Medicine

Volumn 47, Issue 10, 2009, Pages 1459-1467

  Fishman, Kelly ^a   Baure, Jennifer ^a   Zou, Yani ^b   Huang, Ting Ting ^b,c   Andres Mach, Marta ^a   Rola, Radoslaw ^a,d   Suarez, Tatiana ^e   Acharya, Munjal ^e   Limoli, Charles L ^e   Lamborn, Kathleen R ^a   Fike, John R ^a,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^d MEDICAL UNIVERSITY OF LUBLIN   (Poland)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain; Free radicals; Inflammation; Neurogenesis; Oxidative stress; Radiation; SOD

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; MANGANESE SUPEROXIDE DISMUTASE; XANTHINE; XANTHINE OXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CELL ACTIVATION; CELL FATE; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; HIPPOCAMPUS; IN VITRO STUDY; IONIZING RADIATION; ISOELECTRIC FOCUSING; MICROGLIA; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RADIATION DOSE; RADIATION EXPOSURE; WESTERN BLOTTING; WILD TYPE; X RAY;

ANIMALS; DOSE-RESPONSE RELATIONSHIP, RADIATION; HETEROZYGOTE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGENESIS; NEURONS; OXIDATIVE STRESS; RADIATION, IONIZING; SUPEROXIDE DISMUTASE;

MUS;

EID: 70350028714     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.08.016     Document Type: Article

References (85)

1. Tofilon P.J., and Fike J.R. The radioresponse of the central nervous system: a dynamic process. Radiat. Res. 153 (2000) 357-370
2. Sheline G.E., Wara W.M., and Smith V. Therapeutic irradiation and brain injury. Int. J. Radiat. Oncol. Biol. Phys. 6 (1980) 1215-1228
3. Butler J.M., Rapp S.R., and Shaw E.G. Managing the cognitive effects of brain tumor radiation therapy. Curr. Treat. Options Oncol. 7 (2006) 517-523
4. Meyers C.A., and Brown P.D. Role and relevance of neurocognitive assessment in clinical trials of patients with CNS tumors. J. Clin. Oncol. 24 (2006) 1305-1309
5. Abayomi O.K. Pathogenesis of irradiation-induced cognitive dysfunction. Acta Oncol. 35 (1996) 659-663
6. Crossen J.R., Garwood D., Glatstein E., and Neuwelt E.A. Neurobehavioral sequelae of cranial irradiation in adults: a review of radiation-induced encephalopathy. J. Clin. Oncol. 12 (1994) 627-642
7. Roman D.D., and Sperduto P.W. Neuropsychological effects of cranial radiation: current knowledge and future directions. Int. J. Radiat. Oncol. Biol. Phys. 31 (1995) 983-998
8. Surma-aho O., Niemela M., Vilkki J., Kouri M., Brander A., Salonen O., Paetau A., Kallio M., Pyykkonen J., and Jaaskelainen J. Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients. Neurology 56 (2001) 1285-1290
9. Madsen T.M., Kristjansen P.E., Bolwig T.G., and Wortwein G. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119 (2003) 635-642
10. Raber J., Fan Y., Matsumori Y., Liu Z., Weinstein P.R., Fike J.R., and Liu J. Irradiation attenuates neurogenesis and exacerbates ischemia-induced deficits. Ann. Neurol. 55 (2004) 381-389
11. Raber J., Rola R., LeFevour A., Morhardt D.R., Curley J., Mizumatsu S., VandenBerg S.R., and Fike J.R. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat. Res. 162 (2004) 39-47
12. Rola R., Raber J., Rizk A., Otsuka S., VandenBerg S.R., Morhardt D.R., and Fike J.R. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp. Neurol. 188 (2004) 316-330
13. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., and Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16 (2006) 296-304
14. Mizumatsu S., Monje M.L., Morhardt D.R., Rola R., Palmer T.D., and Fike J.R. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res. 63 (2003) 4021-4027
15. Monje M.L., and Palmer T. Radiation injury and neurogenesis. Curr. Opin. Neurol. 16 (2003) 129-134
16. Saxe M.D., Battaglia F., Wang J.W., Malleret G., David D.J., Monckton J.E., Garcia A.D., Sofroniew M.V., Kandel E.R., Santarelli L., Hen R., and Drew M.R. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. USA 103 (2006) 17501-17506
17. Snyder J.S., Hong N.S., McDonald R.J., and Wojtowicz J.M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 130 (2005) 843-852
18. Fan Y., Liu Z., Weinstein P.R., Fike J.R., and Liu J. Environmental enrichment enhances neurogenesis and improves functional outcome after cranial irradiation. Eur. J. Neurosci. 25 (2007) 38-46
19. Shi L., Adams M.M., Long A., Carter C.C., Bennett C., Sonntag W.E., Nicolle M.M., Robbins M., D'Agostino R., and Brunso-Bechtold J.K. Spatial learning and memory deficits after whole-brain irradiation are associated with changes in NMDA receptor subunits in the hippocampus. Radiat. Res. 166 (2006) 892-899
20. Villasana L., Acevedo S., Poage C., and Raber J. Sex- and APOE isoform-dependent effects of radiation on cognitive function. Radiat. Res. 166 (2006) 883-891
21. Rosi S., Andres-Mach M., Fishman K.M., Levy W., Ferguson R.A., and Fike J.R. Cranial irradiation alters the behaviorally induced immediate-early gene arc (activity-regulated cytoskeleton-associated protein). Cancer Res. 68 (2008) 9763-9770
22. Gage F.H. Mammalian neural stem cells. Science 287 (2000) 1433-1438
23. Ramirez-Amaya V., Marrone D.F., Gage F.H., Worley P.F., and Barnes C.A. Integration of new neurons into functional neural networks. J. Neurosci. 26 (2006) 12237-12241
24. Zhao C., Teng E.M., Summers Jr. R.G., Ming G.L., and Gage F.H. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci. 26 (2006) 3-11
25. Kempermann G. Why new neurons? Possible functions for adult hippocampal neurogenesis. J. Neurosci. 22 (2002) 635-638
26. van Praag H., Christie B.R., Sejnowski T.J., and Gage F.H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. USA 96 (1999) 13427-13431
27. Monje M.L., Mizumatsu S., Fike J.R., and Palmer T.D. Irradiation induces neural precursor-cell dysfunction. Nat. Med. 8 (2002) 955-962
28. Monje M.L., Vogel H., Masek M., Ligon K.L., Fisher P.G., and Palmer T.D. Impaired human hippocampal neurogenesis after treatment for central nervous system malignancies. Ann. Neurol. 62 (2007) 515-520
29. Fike J.R., Rola R., and Limoli C.L. Radiation response of neural precursor cells. Neurosurg. Clin. North Am. 18 (2007) 115-127
30. Monje M.L., Toda H., and Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302 (2003) 1760-1765
31. Rola R., Sarkissian V., Obenaus A., Nelson G.A., Otsuka S., Limoli C.L., and Fike J.R. High LET irradiation induced inflammation and persistent changes in markers of hippocampal neurogenesis. Radiat. Res. 164 (2005) 556-560
32. Rola R., Zou Z., Huang T.T., Fishman K., Baure J., Rosi S., Milliken H., Limoli C.L., and Fike J.R. Lack of EC-SOD in the microenvironment impacts radiation-induced changes in neurogenesis. Free Radic. Biol. Med. 42 (2007) 1133-1145
33. Smith J., Ladi E., Mayer-Proschel M., and Noble M. Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell. Proc. Natl. Acad. Sci. USA 97 (2000) 10032-10037
34. Peuchen S., Bolanos J.P., Heales S.J., Almeida A., Duchen M.R., and Clark J.B. Interrelationships between astrocyte function, oxidative stress and antioxidant status within the central nervous system. Prog. Neurobiol. 52 (1997) 261-281
35. Smith K.J., Kapoor R., and Felts P.A. Demyelination: the role of reactive oxygen and nitrogen species. Brain Pathol. 9 (1999) 69-92
36. Forster M.J., Dubey A., Dawson K.M., Stutts W.A., Lal H., and Sohal R.S. Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc. Natl. Acad. Sci. USA 93 (1996) 4765-4769
37. Juurlink B.H., and Paterson P.G. Review of oxidative stress in brain and spinal cord injury: suggestions for pharmacological and nutritional management strategies. J. Spinal Cord Med. 21 (1998) 309-334
38. Love S. Oxidative stress in brain ischemia. Brain Pathol. 9 (1999) 119-131
39. Lin M.T., and Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443 (2006) 787-795
40. Fike J.R., Rosi S., and Limoli C.L. Neural precursor cells and central nervous system radiation sensitivity. Semin. Radiat. Oncol. 19 (2009) 122-132
41. Limoli C.L., Giedzinski E., Rola R., Otsuka S., Palmer T.D., and Fike J.R. Radiation response of neural precursor cells: linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress. Radiat. Res. 161 (2004) 17-27
42. Limoli C.L., Rola R., Giedzinski E., Mantha S., Huang T.T., and Fike J.R. Cell density dependent regulation of neural precursor cell function. Proc. Natl. Acad. Sci. USA 101 (2004) 16052-16057
43. Lonergan P.E., Martin D.S., Horrobin D.F., and Lynch M.A. Neuroprotective effect of eicosapentaenoic acid in hippocampus of rats exposed to gamma-irradiation. J. Biol. Chem. 277 (2002) 20804-20811
44. Riley P.A. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int. J. Radiat. Biol. 65 (1994) 27-33
45. Huang T.T., Carlson E.J., Raineri I., Gillespie A.M., Kozy H., and Epstein C.J. The use of transgenic and mutant mice to study oxygen free radical metabolism. Ann. N. Y. Acad. Sci. 893 (1999) 95-112
46. Kishida K.T., and Klann E. Sources and targets of reactive oxygen species in synaptic plasticity and memory. Antioxid. Redox Signal. 9 (2007) 233-244
47. Slemmer J.E., Shacka J.J., Sweeney M.I., and Weber J.T. Antioxidants and free radical scavengers for the treatment of stroke, traumatic brain injury and aging. Curr. Med. Chem. 15 (2008) 404-414
48. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., and Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39 (2007) 44-84
49. Elchuri S., Oberley T.D., Qi W., Eisenstein R.S., Jackson Roberts L., Van Remmen H., Epstein C.J., and Huang T.T. CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24 (2005) 367-380
50. Van Remmen H., Ikeno Y., Hamilton M., Pahlavani M., Wolf N., Thorpe S.R., Alderson N.L., Baynes J.W., Epstein C.J., Huang T.T., Nelson J., Strong R., and Richardson A. Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol. Genomics 16 (2003) 29-37
51. Huang T.T., Raineri I., Eggerding F., and Epstein C.J. Transgenic and mutant mice for oxygen free radical studies. Methods Enzymol. 349 (2002) 191-213
52. Abercrombie M. Estimation of nuclear population from microtome sections. Anat. Rec. 94 (1946) 239-247
53. 2 scavenging and signaling. Antioxid. Redox Signal. 10 (2008) 1565-1576
54. Winterbourn C.C., and Hampton M.B. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45 (2008) 549-561
55. Hansen J.M., Zhang H., and Jones D.P. Differential oxidation of thioredoxin-1, thioredoxin-2, and glutathione by metal ions. Free Radic. Biol. Med. 40 (2006) 138-145
56. Muscoli C., Cuzzocrea S., Riley D.P., Zweier J.L., Thiemermann C., Wang Z.Q., and Salvemini D. On the selectivity of superoxide dismutase mimetics and its importance in pharmacological studies. Br. J. Pharmacol. 140 (2003) 445-460
57. Hu D., Cao P., Thiels E., Chu C.T., Wu G.Y., Oury T.D., and Klann E. Hippocampal long-term potentiation, memory, and longevity in mice that overexpress mitochondrial superoxide dismutase. Neurobiol. Learn. Mem. 87 (2007) 372-384
58. Levin E.D., Brady T.C., Hochrein E.C., Oury T.D., Jonsson L.M., Marklund S.L., and Crapo J.D. Molecular manipulations of extracellular superoxide dismutase: functional importance for learning. Behav. Genet. 28 (1998) 381-390
59. Kamsler A., Avital A., Greenberger V., and Segal M. Aged SOD overexpressing mice exhibit enhanced spatial memory while lacking hippocampal neurogenesis. Antioxid. Redox Signal. 9 (2007) 181-189
60. Serrano F., and Klann E. Reactive oxygen species and synaptic plasticity in the aging hippocampus. Ageing Res. Rev. 3 (2004) 431-443
61. Noble M., Mayer-Proschel M., and Proschel C. Redox regulation of precursor cell function: insights and paradoxes. Antioxid. Redox Signaling 7 (2005) 1456-1467
62. Gori T., and Forconi S. The role of reactive free radicals in ischemic preconditioning-clinical and evolutionary implications. Clin. Hemorheol. Microcirc. 33 (2005) 19-28
63. Yu B.P., and Chung H.Y. Adaptive mechanisms to oxidative stress during aging. Mech. Ageing Dev. 127 (2006) 436-443
64. Qutob S.S., Multani A.S., Pathak S., McNamee J.P., Bellier P.V., Liu Q.Y., and Ng C.E. Fractionated X-radiation treatment can elicit an inducible-like radioprotective response that is not dependent on the intrinsic cellular X-radiation resistance/sensitivity. Radiat. Res. 166 (2006) 590-599
65. Van Remmen H., Salvador C., Yang H., Huang T.T., Epstein C.J., and Richardson A. Characterization of the antioxidant status of the heterozygous manganese superoxide dismutase knockout mouse. Arch. Biochem. Biophys. 363 (1999) 91-97
66. Spitz D.R., Dewey W.C., and Li G.C. Hydrogen peroxide or heat shock induces resistance to hydrogen peroxide in Chinese hamster fibroblasts. J. Cell. Physiol. 131 (1987) 364-373
67. Sullivan S.J., Roberts R.J., and Spitz D.R. Replacement of media in cell culture alters oxygen toxicity: possible role of lipid aldehydes and glutathione transferase in oxygen toxicity. J. Cell. Physiol. 147 (1991) 427-433
68. Cao L., Jiao X., Zuzga D.S., Liu Y., Fong D.M., Young D., and During M.J. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet. 36 (2004) 827-835
69. Cardenas A., Moro M.A., Hurtado O., Leza J.C., and Lizasoain I. Dual role of nitric oxide in adult neurogenesis. Brain Res. Brain Res. Rev. 50 (2005) 1-6
70. Gibbs S.M. Regulation of neuronal proliferation and differentiation by nitric oxide. Mol. Neurobiol. 27 (2003) 107-120
71. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., and Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192 (2005) 348-356
72. Nedergaard M., Ransom B., and Goldman S.A. New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci. 26 (2003) 523-530
73. Barkho B.Z., Song H., Aimone J.B., Smrt R.D., Kuwabara T., Nakashima K., Gage F.H., and Zhao X. Identification of astrocyte-expressed factors that modulate neural stem/progenitor cell differentiation. Stem Cells Dev. 15 (2006) 407-421
74. Jordan J.D., Ma D.K., Ming G.L., and Song H. Cellular niches for endogenous neural stem cells in the adult brain. CNS Neurol. Disord. Drug Targets 6 (2007) 336-341
75. Harrison J.F., Hollensworth S.B., Spitz D.R., Copeland W.C., Wilson G.L., and LeDoux S.P. Oxidative stress-induced apoptosis in neurons correlates with mitochondrial DNA base excision repair pathway imbalance. Nucleic Acids Res. 33 (2005) 4660-4671
76. Hollensworth S.B., Shen C., Sim J.E., Spitz D.R., Wilson G.L., and LeDoux S.P. Glial cell type-specific responses to menadione-induced oxidative stress. Free Radic. Biol. Med. 28 (2000) 1161-1174
77. Xu L., Sapolsky R.M., and Giffard R.G. Differential sensitivity of murine astrocytes and neurons from different brain regions to injury. Exp. Neurol. 169 (2001) 416-424
78. Oberley L.W., Oberley T.D., and Buettner G.R. Cell differentiation, aging and cancer: the possible roles of superoxide and superoxide dismutases. Med. Hypotheses 6 (1980) 249-268
79. Baydas G., and Tuzcu M. Protective effects of melatonin against ethanol-induced reactive gliosis in hippocampus and cortex of young and aged rats. Exp. Neurol. 194 (2005) 175-181
80. Doetsch F. The glial identity of neural stem cells. Nat. Neurosci. 6 (2003) 1127-1134
81. Ekdahl C.T., Kokaia Z., and Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158 (2009) 1021-1029
82. Whitney N.P., Eidem T.M., Peng H., Huang Y., and Zheng J.C. Inflammation mediates varying effects in neurogenesis: relevance to the pathogenesis of brain injury and neurodegenerative disorders. J. Neurochem. 108 (2009) 1343-1359
83. Butovsky O., Ziv Y., Schwartz A., Landa G., Talpalar A.E., Pluchino S., Martino G., and Schwartz M. Microglia activated by IL-4 or IFN-γ differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol. Cell. Neurosci. 31 (2006) 149-160
84. Muller F.L., Song W., Liu Y., Chaudhuri A., Pieke-Dahl S., Strong R., Huang T.T., Epstein C.J., Roberts II L.J., Csete M., Faulkner J.A., and Van Remmen H. Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy. Free Radic. Biol. Med. 40 (2006) 1993-2004
85. Zou Y., Chen C.H., Fike J.R., and Huang T.T. A new mouse model for temporal- and tissue-specific control of extracellular superoxide dismutase. Genesis 47 (2009) 142-154