Redox balance- and radiation-mediated alteration in hippocampal neurogenesis

References

• Tonks NK. Redox redux: revisiting PTPs and the control of cell signaling. Cell 2005;121:667–670.
   PubMed Web of Science ®Google Scholar
• Salmeen A, Barford D. Functions and mechanisms of redox regulation of cysteine-based phosphatases. Antioxid Redox Signal 2005;7:560–577.
   PubMed Web of Science ®Google Scholar
• Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 2001;30: 1191–1212.
   PubMed Web of Science ®Google Scholar
• Smith J, Ladi E, Mayer-Proschel M, 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 2000;97:10032–10037.
   PubMed Web of Science ®Google Scholar
• Erecinska M, Cherian S, Silver IA. Energy metabolism in mammalian brain during development. Prog Neurobiol 2004;73:397–445.
   PubMed Web of Science ®Google Scholar
• Zeiger SL, Stankowski JN, McLaughlin B. Assessing neuronal bioenergetic status. Methods Mol Biol 2011;758: 215–235.
   PubMedGoogle Scholar
• Halliwell B. Reactive oxygen species and the central nervous system. J Neurochem 1992;59:1609–1623.
   PubMed Web of Science ®Google Scholar
• Dong XX, Wang Y, Qin ZH. Molecular mechanisms of excitotoxicity and their relevance to pathogenesis of neurodegenerative diseases. Acta Pharmacol Sin 2009;30:379–387.
   PubMed Web of Science ®Google Scholar
• Forder JP, Tymianski M. Postsynaptic mechanisms of excitotoxicity: Involvement of postsynaptic density proteins, radicals, and oxidant molecules. Neuroscience 2009;158: 293–300.
   PubMed Web of Science ®Google Scholar
• Atlante A, Calissano P, Bobba A, Giannattasio S, Marra E, Passarella S, . Glutamate neurotoxicity, oxidative stress and mitochondria. FEBS Lett 2001;497:1–5.
   PubMed Web of Science ®Google Scholar
• Paumier A, Cuenca X, Le Pechoux C. Prophylactic cranial irradiation in lung cancer. Cancer Treat Rev 2011;37: 261–265.
   PubMed Web of Science ®Google Scholar
• Rodriguez E, Lilenbaum RC. Small cell lung cancer: past, present, and future. Curr Oncol Rep 2010;12:327–334.
   PubMed Web of Science ®Google Scholar
• Riley PA. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 1994;65:27–33.
   PubMed Web of Science ®Google Scholar
• Limoli CL, Hartmann A, Shephard L, Yang CR, Boothman DA, Bartholomew J, . Apoptosis, reproductive failure, and oxidative stress in Chinese hamster ovary cells with compromised genomic integrity. Cancer Res 1998;58:3712–3718.
   PubMed Web of Science ®Google Scholar
• Rola R, Zou Y, Huang TT, Fishman K, Baure J, Rosi S, . Lack of extracellular superoxide dismutase (EC-SOD) in the microenvironment impacts radiation-induced changes in neurogenesis. Free Radic Biol Med 2007;42:1133–1145; discussion 1131–1132.
   PubMed Web of Science ®Google Scholar
• Sarkissian V. The sequelae of cranial irradiation on human cognition. Neurosci Lett 2005;382:118–123.
   PubMed Web of Science ®Google Scholar
• Laack NN, Brown PD. Cognitive sequelae of brain radiation in adults. Semin Oncol 2004;31:702–713.
   PubMed Web of Science ®Google Scholar
• Gondi V, Tome WA, Mehta MP. Why avoid the hippocampus? A comprehensive review. Radiother Oncol 2010;97: 370–376.
   PubMed Web of Science ®Google Scholar
• Abayomi O, Chun MS, Kelly K. Cerebral calcification and learning disabilities following cranial irradiation for medulloblastoma. J Natl Med Assoc 1990;82:833–836.
   PubMed Web of Science ®Google Scholar
• Panagiotakos G, Alshamy G, Chan B, Abrams R, Greenberg E, Saxena A, . Long-term impact of radiation on the stem cell and oligodendrocyte precursors in the brain. PLoS One 2007;2:e588.
   PubMed Web of Science ®Google Scholar
• Abayomi OK. Pathogenesis of irradiation-induced cognitive dysfunction. Acta Oncol 1996;35:659–663.
   PubMed Web of Science ®Google Scholar
• Mizumatsu S, Monje ML, Morhardt DR, Rola R, Palmer TD, Fike JR, . Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res 2003;63: 4021–4027.
   PubMed Web of Science ®Google Scholar
• Monje ML, Mizumatsu S, Fike JR, Palmer TD. Irradiation induces neural precursor-cell dysfunction. Nat Med 2002;8:955–962.
   PubMed Web of Science ®Google Scholar
• Sturtz LA, Diekert K, Jensen LT, Lill R, Culotta VC. A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J Biol Chem 2001;276:38084–38089.
   PubMed Web of Science ®Google Scholar
• Slot JW, Geuze HJ, Freeman BA, Crapo JD. Intracellular localization of the copper-zinc and manganese superoxide dismutases in rat liver parenchymal cells. Lab Invest 1986;55:363–371.
   PubMed Web of Science ®Google Scholar
• Oury TD, Crapo JD, Valnickova Z, Enghild JJ. Human extracellular superoxide dismutase is a tetramer composed of two disulphide-linked dimers: a simplified, high-yield purification of extracellular superoxide dismutase. Biochem J 1996;317(Pt 1):51–57.
   PubMed Web of Science ®Google Scholar
• Marklund S. Extracellular superoxide dismutase and other superoxide dismutase isoenzymes in tissues from nine mammalian species. Biochem J 1984;222:649–655.
   PubMed Web of Science ®Google Scholar
• Marklund S. Extracellular superoxide dismutase in human tissues and human cell lines. J Clin Invest 1984;74:138–403.
   Web of Science ®Google Scholar
• Gray B, Carmichael AJ. Kinetics of superoxide scavenging by dismutase enzymes and manganese mimics determined by electron spin resonance. Biochem J 1992;281 (Pt 3): 795–802.
   PubMed Web of Science ®Google Scholar
• Spitz DR, Oberley LW. Measurement of MnSOD and CuZnSOD activity in mammalian tissue homogenates. Curr Protoc Toxicol 2001;Chapter 7:Unit7 5.
   PubMedGoogle Scholar
• Carlsson LM, Jonsson J, Edlund T, Marklund SL. Mice lacking extracellular superoxide dismutase are more sensitive to hyperoxia. Proc Natl Acad Sci USA 1995;92:6264–6268.
   PubMed Web of Science ®Google Scholar
• Nakano R, Inuzuka T, Kikugawa K, Takahashi H, Sakimura K, Fujii J, . Instability of mutant Cu/Zn superoxide dismutase (Ala4Thr) associated with familial amyotrophic lateral sclerosis. Neurosci Lett 1996;211:129–131.
   PubMed Web of Science ®Google Scholar
• Berkovich A, Massaro D, Clerch LB. Pertussis toxin alters the concentration and turnover of manganese superoxide dismutase in rat lung. Am J Physiol 1996;271:L875–L879.
   Google Scholar
• Huang TT, Yasunami M, Carlson EJ, Gillespie AM, Reaume AG, Hoffman EK, . Superoxide-mediated cytotoxicity in superoxide dismutase-deficient fetal fibroblasts. Arch Biochem Biophys 1997;344:424–432.
   PubMed Web of Science ®Google Scholar
• Li Y, Huang TT, Carlson EJ, Melov S, Ursell PC, Olson JL, . Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 1995;11:376–381.
   PubMed Web of Science ®Google Scholar
• Elchuri S, Oberley TD, Qi W, Eisenstein RS, Jackson Roberts L, Van Remmen H, . CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 2005;24:367–380.
   PubMed Web of Science ®Google Scholar
• Jang YC, Lustgarten MS, Liu Y, Muller FL, Bhattacharya A, Liang H, . Increased superoxide in vivo accelerates age-associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration. FASEB J 2010;24:1376–1390.
   Google Scholar
• Flood DG, Reaume AG, Gruner JA, Hoffman EK, Hirsch JD, Lin YG, . Hindlimb motor neurons require Cu/Zn superoxide dismutase for maintenance of neuromuscular junctions. Am J Pathol 1999;155:663–672.
   PubMed Web of Science ®Google Scholar
• Kondo T, Reaume AG, Huang TT, Carlson E, Murakami K, Chen SF, . Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci 1997;17:4180–4189.
   PubMed Web of Science ®Google Scholar
• Kondo T, Reaume AG, Huang TT, Murakami K, Carlson E, Chen S, . Edema formation exacerbates neurological and histological outcomes after focal cerebral ischemia in CuZn-superoxide dismutase gene knockout mutant mice. Acta Neurochir Suppl 1997;70:62–64.
   PubMedGoogle Scholar
• Park JW, Qi WN, Cai Y, Zelko I, Liu JQ, Chen LE, . Skeletal muscle reperfusion injury is enhanced in extracellular superoxide dismutase knockout mouse. Am J Physiol Heart Circ Physiol 2005;289:H181–H187.
   Web of Science ®Google Scholar
• Huang TT, Naeemuddin M, Elchuri S, Yamaguchi M, Kozy HM, Carlson EJ, . Genetic modifiers of the phenotype of mice deficient in mitochondrial superoxide dismutase. Hum Mol Genet 2006;15:1187–1194.
   PubMed Web of Science ®Google Scholar
• Huang TT, Carlson EJ, Kozy HM, Mantha S, Goodman SI, Ursell PC, . Genetic modification of prenatal lethality and dilated cardiomyopathy in Mn superoxide dismutase mutant mice. Free Radic Biol Med 2001;31:1101–1110.
   PubMed Web of Science ®Google Scholar
• Van Remmen H, Ikeno Y, Hamilton M, Pahlavani M, Wolf N, Thorpe SR, . Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol Genomics 2003;16:29–37.
   PubMed Web of Science ®Google Scholar
• Van Remmen H, Williams MD, Guo Z, Estlack L, Yang H, Carlson EJ, . Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am J Physiol Heart Circ Physiol 2001;281: H1422–1432.
   Web of Science ®Google Scholar
• Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 2010;11: 339–350.
   PubMed Web of Science ®Google Scholar
• Suh H, Deng W, Gage FH. Signaling in adult neurogenesis. Annu Rev Cell Dev Biol 2009;25:253–275.
   PubMed Web of Science ®Google Scholar
• Aimone JB, Wiles J, Gage FH. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 2006;9:723–727.
   PubMed Web of Science ®Google Scholar
• Kempermann G, Gage FH. Neurogenesis in the adult hippocampus. Novartis Found Symp 2000;231:220–235; discussion 235–241, 302–226.
   PubMedGoogle Scholar
• Gage FH, Kempermann G, Palmer TD, Peterson DA, Ray J. Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol 1998;36:249–266.
   PubMedGoogle Scholar
• Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005;28: 223–250.
   PubMed Web of Science ®Google Scholar
• Fishman K, Baure J, Zou Y, Huang TT, Andres-Mach M, Rola R, . Radiation-induced reductions in neurogenesis are ameliorated in mice deficient in CuZnSOD or MnSOD. Free Radic Biol Med 2009;47:1459–1467.
   PubMed Web of Science ®Google Scholar
• Prozorovski T, Schulze-Topphoff U, Glumm R, Baumgart J, Schroter F, . Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat Cell Biol 2008;10:385–394.
   PubMed Web of Science ®Google Scholar
• Raber J, Villasana L, Rosenberg J, Zou Y, Huang TT, Fike JR, . Irradiation enhances hippocampus-dependent cognition in mice deficient in extracellular superoxide dismutase. Hippocampus 2011;21:72–80.
   PubMed Web of Science ®Google Scholar
• Levin ED, Brady TC, Hochrein EC, Oury TD, Jonsson LM, Marklund SL, . Molecular manipulations of extracellular superoxide dismutase: functional importance for learning. Behav Genet 1998;28:381–390.
   PubMed Web of Science ®Google Scholar
• Kamsler A, Avital A, Greenberger V, Segal M. Aged SOD overexpressing mice exhibit enhanced spatial memory while lacking hippocampal neurogenesis. Antioxid Redox Signal 2007;9:181–189.
   PubMed Web of Science ®Google Scholar
• Yoo DY, Shin BN, Kim IH, Kim W, Kim DW, Yoo KY, . Effects of Cu,Zn-Superoxide Dismutase on Cell Proliferation and Neuroblast Differentiation in the Mouse Dentate Gyrus. Neurochem Res 2012;37:261–267.
   PubMed Web of Science ®Google Scholar
• Potts MB, Rola R, Claus CP, Ferriero DM, Fike JR, Noble-Haeusslein LJ, . Glutathione peroxidase overexpression does not rescue impaired neurogenesis in the injured immature brain. J Neurosci Res 2009;87:1848–1857.
   PubMed Web of Science ®Google Scholar
• Hu D, Serrano F, Oury TD, Klann E. Aging-dependent alterations in synaptic plasticity and memory in mice that overexpress extracellular superoxide dismutase. J Neurosci 2006;26:3933–3941.
   PubMed Web of Science ®Google Scholar
• Thiels E, Urban NN, Gonzalez-Burgos GR, Kanterewicz BI, Barrionuevo G, Chu CT, . Impairment of long-term potentiation and associative memory in mice that overexpress extracellular superoxide dismutase. J Neurosci 2000;20: 7631–7639.
   PubMed Web of Science ®Google Scholar
• Gahtan E, Auerbach JM, Groner Y, Segal M. Reversible impairment of long-term potentiation in transgenic Cu/Zn-SOD mice. Eur J Neurosci 1998;10:538–544.
   PubMed Web of Science ®Google Scholar
• Kamsler A, Segal M. Paradoxical actions of hydrogen peroxide on long-term potentiation in transgenic superoxide dismutase-1 mice. J Neurosci 2003;23:10359–10367.
   PubMed Web of Science ®Google Scholar
• Hu D, Cao P, Thiels E, Chu CT, Wu GY, Oury TD, . Hippocampal long-term potentiation, memory, and longevity in mice that overexpress mitochondrial superoxide dismutase. Neurobiol Learn Mem 2007;87:372–384.
   PubMed Web of Science ®Google Scholar
• Grodstein F, Kang JH, Glynn RJ, Cook NR, Gaziano JM. A randomized trial of beta carotene supplementation and cognitive function in men: the Physicians’ Health Study II. Arch Intern Med 2007;167:2184–2190.
   PubMed Web of Science ®Google Scholar
• Kesse-Guyot E, Fezeu L, Jeandel C, Ferry M, Andreeva V, Amieva H, . French adults’ cognitive performance after daily supplementation with antioxidant vitamins and minerals at nutritional doses: a post hoc analysis of the Supplementation in Vitamins and Mineral Antioxidants (SU.VI.MAX) trial. Am J Clin Nutr 2011;94:892–899.
   PubMed Web of Science ®Google Scholar
• Kesse-Guyot E, Amieva H, Castetbon K, Henegar A, Ferry M, Jeandel C, . Adherence to nutritional recommendations and subsequent cognitive performance: findings from the prospective Supplementation with Antioxidant Vitamins and Minerals 2 (SU.VI.MAX 2) study. Am J Clin Nutr 2011;93:200–210.
   PubMed Web of Science ®Google Scholar
• Fotuhi M, Zandi PP, Hayden KM, Khachaturian AS, Szekely CA, Wengreen H, . Better cognitive performance in elderly taking antioxidant vitamins E and C supplements in combination with nonsteroidal anti-inflammatory drugs: the Cache County Study. Alzheimers Dement 2008;4:223–227.
   PubMed Web of Science ®Google Scholar
• Kang JH, Cook N, Manson J, Buring JE, Grodstein F. A randomized trial of vitamin E supplementation and cognitive function in women. Arch Intern Med 2006;166: 2462–2468.
   PubMed Web of Science ®Google Scholar
• Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003;302:1760–1765.
   PubMed Web of Science ®Google Scholar
• Conrad M, Sato H. The oxidative stress-inducible cystine/glutamate antiporter, system x(c) (-): cystine supplier and beyond. Amino Acids 2012;42:231–246.
   PubMed Web of Science ®Google Scholar
• Trotti D, Danbolt NC, Volterra A. Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration? Trends Pharmacol Sci 1998;19:328–334.
   PubMed Web of Science ®Google Scholar
• Nakagawa M, Bellinzona M, Seilhan TM, Gobbel GT, Lamborn KR, Fike JR, . Microglial responses after focal radiation-induced injury are affected by alpha-difluoromethylornithine. Int J Radiat Oncol Biol Phys 1996;36:113–123.
   PubMed Web of Science ®Google Scholar
• Fike JR, Gobbel GT, Chou D, Wijnhoven BP, Bellinzona M, Nakagawa M, . Cellular proliferation and infiltration following interstitial irradiation of normal dog brain is altered by an inhibitor of polyamine synthesis. Int J Radiat Oncol Biol Phys 1995;32:1035–1045.
   PubMed Web of Science ®Google Scholar
• Fike JR, Gobbel GT, Marton LJ, Seilhan TM. Radiation brain injury is reduced by the polyamine inhibitor alpha-difluoromethylornithine. Radiat Res 1994;138:99–106.
   PubMed Web of Science ®Google Scholar
• Gobbel GT, Marton LJ, Lamborn K, Seilhan TM, Fike JR. Modification of radiation-induced brain injury by alpha-difluoromethylornithine. Radiat Res 1991;128:306–315.
   PubMed Web of Science ®Google Scholar
• Carpenter M, Epperly MW, Agarwal A, Nie S, Hricisak L, Niu Y, . Inhalation delivery of manganese superoxide dismutase-plasmid/liposomes protects the murine lung from irradiation damage. Gene Ther 2005;12:685–693.
   PubMed Web of Science ®Google Scholar
• Greenberger JS, Epperly M, Luketich J, Gooding W, Belani CP. Manganese superoxide dismutase-plasmid/ liposome (MnSOD-PL) gene therapy protection of the esophagus from chemoradiotherapy damage during treatment of locally unresectable non-small-cell lung cancer (NSCLC). Clin Lung Cancer 2000;1:302–304.
   PubMedGoogle Scholar
• Greenberger JS, Epperly MW, Gretton J, Jefferson M, Nie S, Bernarding M, . Radioprotective gene therapy. Curr Gene Ther 2003;3:183–195.
   PubMedGoogle Scholar
• Guo H, Epperly MW, Bernarding M, Nie S, Gretton J, Jefferson M, . Manganese superoxide dismutase-plasmid/liposome (MnSOD-PL) intratracheal gene therapy reduction of irradiation-induced inflammatory cytokines does not protect orthotopic Lewis lung carcinomas. In Vivo 2003;17: 13–21.
   PubMed Web of Science ®Google Scholar
• Epperly MW, Defilippi S, Sikora C, Gretton J, Kalend A, Greenberger JS, . Intratracheal injection of manganese superoxide dismutase (MnSOD) plasmid/liposomes protects normal lung but not orthotopic tumors from irradiation. Gene Ther 2000;7:1011–1018.
   PubMed Web of Science ®Google Scholar
• Epperly M, Bray J, Kraeger S, Zwacka R, Engelhardt J, Travis E, . Prevention of late effects of irradiation lung damage by manganese superoxide dismutase gene therapy. Gene Ther 1998;5:196–208.
   PubMed Web of Science ®Google Scholar
• Zou Y, Chen CH, Fike JR, Huang TT. A new mouse model for temporal- and tissue-specific control of extracellular superoxide dismutase. Genesis 2009;47:142–154.
   PubMed Web of Science ®Google Scholar
• Raineri I, Carlson EJ, Gacayan R, Carra S, Oberley TD, Huang TT, . Strain-dependent high-level expression of a transgene for manganese superoxide dismutase is associated with growth retardation and decreased fertility. Free Radic Biol Med 2001;31:1018–1030.
   PubMed Web of Science ®Google Scholar
• Ikegami T, Suzuki Y, Shimizu T, Isono K, Koseki H, Shirasawa T, . Model mice for tissue-specific deletion of the manganese superoxide dismutase (MnSOD) gene. Biochem Biophys Res Commun 2002;296:729–736.
   PubMed Web of Science ®Google Scholar
• Somwar R, Erdjument-Bromage H, Larsson E, Shum D, Lockwood WW, Yang G, . Superoxide dismutase 1 (SOD1) is a target for a small molecule identified in a screen for inhibitors of the growth of lung adenocarcinoma cell lines. Proc Natl Acad Sci USA 2011;108:16375–16380.
   PubMed Web of Science ®Google Scholar