Neural stem cells genetically modified to overexpress Cu/Zn-superoxide dismutase enhance amelioration of ischemic stroke in mice

Stroke

Volumn 43, Issue 9, 2012, Pages 2423-2429

  Sakata, Hiroyuki ^a   Niizuma, Kuniyasu ^a   Wakai, Takuma ^a   Narasimhan, Purnima ^a   Maier, Carolina M ^a   Chan, Pak H ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

copper zinc superoxide dismutase; ischemic stroke; neural stem cell; neuroprotection

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DNA MODIFICATION; GENE EXPRESSION; HISTOLOGY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEURAL STEM CELL TRANSPLANTATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPERFUSION INJURY; UPREGULATION;

ANIMALS; BRAIN ISCHEMIA; CELL SEPARATION; CELL SURVIVAL; CELLS, CULTURED; GLUCOSE; HYPOXIA, BRAIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURAL STEM CELLS; REPERFUSION INJURY; STEM CELL TRANSPLANTATION; STROKE; SUPEROXIDE DISMUTASE; SUPEROXIDES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84865584997     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.112.656900     Document Type: Article

References (32)

1. Lindvall O, Kokaia Z. Stem cells in human neurodegenerative disorders\-time for clinical translation? J Clin Invest. 2010;120:29-40.
2. Savitz SI, Chopp M, Deans R, Carmichael ST, Phinney D, Wechsler L. Stem cell therapy as an emerging paradigm for stroke (STEPS) II. Stroke. 2011;42:825-829.
3. Lindvall O, Kokaia Z. Stem cell research in stroke. How far from the clinic? Stroke. 2011;42:2369-2375.
4. Nakagomi N, Nakagomi T, Kubo S, Nakano-Doi A, Saino O, Takata M, et al. Endothelial cells support survival, proliferation, and neuronal differentiation of transplanted adult ischemia-induced neural stem/progenitor cells after cerebral infarction. Stem Cells. 2009;27:2185-2195.
5. Chen H, Yoshioka H, Kim GS, Jung JE, Okami N, Sakata H, et al. Oxidative stress in ischemic brain damage: mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid Redox Signal. 2011;14:1505-1517.
6. Chan PH. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab. 2001;21:2-14.
7. McCord JM, Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969;244:6049-6055.
8. Chan PH, Kawase M, Murakami K, Chen SF, Li Y, Calagui B, et al. Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J Neurosci. 1998;18:8292-8299.
9. Yang G, Chan PH, Chen J, Carlson E, Chen SF, Weinstein P, et al. Human copper-zinc superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia. Stroke. 1994; 25:165-170.
10. Kinouchi H, Epstein CJ, Mizui T, Carlson E, Chen SF, Chan PH. Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase. Proc Natl Acad Sci U S A. 1991;88: 11158-11162.
11. Blurton-Jones M, Kitazawa M, Martinez-Coria H, Castello NA, Müller F-J, Loring JF, et al. Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci U S A. 2009; 106:13594-13599.
12. Murakami K, Kondo T, Kawase M, Li Y, Sato S, Chen SF, et al. Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J Neurosci. 1998;18: 205-213.
13. Kim GS, Jung JE, Niizuma K, Chan PH. CK2 is a novel negative regulator of NADPH oxidase and a neuroprotectant in mice after cerebral ischemia. J Neurosci. 2009;29:14779-14789.
14. Horie N, Pereira MP, Niizuma K, Sun G, Keren-Gill H, Encarnacion A, et al. Transplanted stem cell-secreted vascular endothelial growth factor effects poststroke recovery, inflammation, and vascular repair. Stem Cells. 2011;29:274-285.
15. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, Pyle AD, et al. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell. 2011;8:59-71.
16. Madhavan L, Ourednik V, Ourednik J. Increased 'vigilance' of anti-oxidant mechanisms in neural stem cells potentiates their capability to resist oxidative stress. Stem Cells. 2006;24:2110-2119.
17. Limoli CL, Rola R, Giedzinski E, Mantha S, Huang T-T, Fike Jr. Cell-density-dependent regulation of neural precursor cell function. Proc Natl Acad Sci U S A. 2004;101:16052-16057.
18. Acharya MM, Lan ML, Kan VH, Patel NH, Giedzinski E, Tseng BP, et al. Consequences of ionizing radiation-induced damage in human neural stem cells. Free Radic Biol Med. 2010;49:1846-1855.
19. Sahlgren CM, Pallari H-M, He T, Chou Y-H, Goldman RD, Eriksson JE. A nestin scaffold links Cdk5/p35 signaling to oxidant-induced cell death. EMBO J. 2006;25:4808-4819.
20. Theus MH, Wei L, Cui L, Francis K, Hu X, Keogh C, et al. In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain. Exp Neurol. 2008;210:656-670.
21. Wei L, Cui L, Snider BJ, Rivkin M, Yu SS, Lee C-S, et al. Transplantation of embryonic stem cells overexpressing Bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol Dis. 2005;19: 183-193.
22. Paik J-H, Ding Z, Narurkar R, Ramkissoon S, Muller F, Kamoun WS, et al. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell. 2009;5:540-553.
23. Renault VM, Rafalski VA, Morgan AA, Salih DAM, Brett JO, Webb AE, et al. FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell. 2009;5:527-539.
24. Gregorian C, Nakashima J, Le Belle J, Ohab J, Kim R, Liu A, et al. Pten deletion in adult neural stem/progenitor cells enhances constitutive neu-rogenesis. J Neurosci. 2009;29:1874-1886.
25. Groszer M, Erickson R, Scripture-Adams DD, Dougherty JD, Le Belle J, Zack JA, et al. PTEN negatively regulates neural stem cell self-renewal by modulating G#inf#0#/inf#-G#inf#1#/inf# cell cycle entry. Proc Natl Acad Sci U S A. 2006; 103:111-116.
26. Groszer M, Erickson R, Scripture-Adams DD, Lesche R, Trumpp A, Zack JA, et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science. 2001;294: 2186-2189.
27. Huang T-T, Carlson EJ, Raineri I, Gillespie AM, Kozy H, Epstein CJ. The use of transgenic and mutant mice to study oxygen free radical metabolism. Ann N Y Acad Sci. 1999;893:95-112.
28. Sugawara T, Noshita N, Lewén A, Gasche Y, Ferrand-Drake M, Fujimura M, et al. Overexpression of copper/zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci. 2002;22:209-217.
29. Saito A, Hayashi T, Okuno S, Ferrand-Drake M, Chan PH. Overex-pression of copper/zinc superoxide dismutase in transgenic mice protects against neuronal cell death after transient focal ischemia by blocking activation of the Bad cell death signaling pathway. J Neurosci. 2003;23: 1710-1718.
30. Kondo T, Reaume AG, Huang T-T, Carlson E, Murakami K, Chen SF, et al. Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci. 1997;17:4180-4189.
31. Kawase M, Murakami K, Fujimura M, Morita-Fujimura Y, Gasche Y, Kondo T, et al. Exacerbation of delayed cell injury after transient global ischemia in mutant mice with CuZn superoxide dismutase deficiency. Stroke. 1999;30:1962-1968.
32. Bliss TM, Andres RH, Steinberg GK. Optimizing the success of cell transplantation therapy for stroke. Neurobiol Dis. 2010;37:275-283.