Oxidative stress increases neurogenesis and oligodendrogenesis in adult neural progenitor cells

Stem Cells and Development

Volumn 23, Issue 19, 2014, Pages 2311-2327

  Pérez Estrada, Cynthia ^a   Covacu, Ruxandra ^a   Sankavaram, Sreenivasa R ^a   Svensson, Mikael ^a   Brundin, Lou ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; BETA ACTIN; BETA TUBULIN; DNA METHYLTRANSFERASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE PEROXIDASE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEMETHYLASE; HISTONE METHYLTRANSFERASE; HYDROGEN PEROXIDE; KI 67 ANTIGEN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; REACTIVE OXYGEN METABOLITE; SIRTUIN 2; TRANSCRIPTION FACTOR MASH1; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1;

ADULT; ANIMAL CELL; ANTIBODY LABELING; ARTICLE; ASTROCYTE; CELL COUNT; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CHROMATIN STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ANALYSIS; GLUTATHIONE METABOLISM; HISTONE PHOSPHORYLATION; HISTONE UBIQUITINATION; IN VITRO STUDY; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGENESIS; OLIGODENDROGLIA; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIMARY CELL CULTURE; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL CULTURE; WESTERN BLOTTING; ADULT STEM CELL; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; PHYSIOLOGY;

ADULT STEM CELLS; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; HYDROGEN PEROXIDE; NEURAL STEM CELLS; NEUROGENESIS; OLIGODENDROGLIA; OXIDATIVE STRESS; RATS;

EID: 84907916506     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0452     Document Type: Article

References (72)

1. van Horssen J, ME Witte, G Schreibelt and HE de Vries. (2011). Radical changes in multiple sclerosis pathogenesis. Biochim Biophys Acta 1812:141-150.
2. Niethammer P, C Grabher, AT Look and TJ Mitchison. (2009). A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459:996-999.
3. Alberts BJA, J Lewis, M Raff, K Roberts and P Walter. (2002). Molecular Biology of the Cell. Garland Science, a member of the Taylor & Francis Group.
4. Juarez JC, M Manuia, ME Burnett, O Betancourt, B Boivin, DE Shaw, NK Tonks, AP Mazar and F Donate. (2008). Su-peroxide dismutase 1 (SOD1) is essential for H2O2-mediated oxidation and inactivation of phosphatases in growth factor signaling. Proc Natl Acad Sci USA 105:7147-7152.
5. Zhu H, A Santo and Y Li. (2012). The antioxidant enzyme peroxiredoxin and its protective role in neurological disorders. Exp Biol Med 237:143-149.
6. Stone JR and S Yang. (2006). Hydrogen peroxide: a signaling messenger. Antioxid Redox Signal 8:243-270.
7. Renshaw SA, CA Loynes, S Elworthy, PW Ingham and MK Whyte. (2007). Modeling inflammation in the zebra-fish: how a fish can help us understand lung disease. Exp Lung Res 33:549-554.
8. Nikic I, D Merkler, C Sorbara, M Brinkoetter, M Kreutz-feldt, FM Bareyre, W Bruck, D Bishop, T Misgeld and M Kerschensteiner. (2011). A reversible form of axon damage in experimental autoimmune encephalomyelitis and multiple sclerosis. Nat Med 17:495-499.
9. Trachootham D, J Alexandre and P Huang. (2009). Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8:579-591.
10. Cadet J, T Douki, D Gasparutto and JL Ravanat. (2003). Oxidative damage to DNA: formation, measurement and biochemical features. Mutat Res 531:5-23.
11. Chen QM. (2000). Replicative senescence and oxidant-induced premature senescence. Beyond the control of cell cycle checkpoints. Ann N Y Acad Sci 908:111-125.
12. Johansson CB, S Momma, DL Clarke, M Risling, U Len-dahl and J Frisen. (1999). Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96:25-34.
13. Doetsch F, I Caille, DA Lim, JM Garcia-Verdugo and A Alvarez-Buylla. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703-716.
14. Kuhn HG, H Dickinson-Anson and FH Gage. (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
15. Reynolds BA and S Weiss. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
16. Arvidsson L, M Fagerlund, N Jaff, A Ossoinak, K Jans-son, A Hagerstrand, CB Johansson, L Brundin and M Svensson. (2011). Distribution and characterization of progenitor cells within the human filum terminale. PloS One 6:e27393.
17. Jha RM, X Liu, R Chrenek, JR Madsen and DL Cardozo. (2013). The postnatal human filum terminale is a source of autologous multipotent neurospheres capable of generating motor neurons. Neurosurgery 72:118-129; discussion 129.
18. Danilov AI, R Covacu, MC Moe, IA Langmoen, CB Johansson, T Olsson and L Brundin. (2006). Neurogenesis in the adult spinal cord in an experimental model of multiple sclerosis. Eur J Neurosci 23:394-400.
19. Nait-Oumesmar B, N Picard-Riera, C Kerninon, L Decker, D Seilhean, GU Hoglinger, EC Hirsch, R Reynolds and A Baron-Van Evercooren. (2007). Activation of the sub-ventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc Natl Acad Sci USA 104:4694-4699.
20. Imitola J, K Raddassi, KI Park, FJ Mueller, M Nieto, YD Teng, D Frenkel, J Li, RL Sidman, et al. (2004). Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci USA 101:18117-18122.
21. Kyritsis N, C Kizil and M Brand. (2013). Neuroin-flammation and central nervous system regeneration in vertebrates. Trends Cell Biol 24:128-135.
22. D'Autreaux B and MB Toledano. (2007). ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8:813-824.
23. Halliwell B and J Gutteridge. (2007). Free Radicals in Biology And Medicine. Oxford University Press, UK.
24. 2, a necessary evil for cell signaling. Science 312:1882-1883.
25. Veal EA, AM Day and BA Morgan. (2007). Hydrogen peroxide sensing and signaling. Mol Cell 26:1-14.
26. Le Belle JE, NM Orozco, AA Paucar, JP Saxe, J Motta-hedeh, AD Pyle, H Wu and HI Kornblum. (2011). Pro-liferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 8:59-71.
27. Dickinson BC, J Peltier, D Stone, DV Schaffer and CJ Chang. (2011). Nox2 redox signaling maintains essential cell populations in the brain. Nat Chem Biol 7:106-112.
28. Gutteridge BH. (2007). Free Radicals in Biology and Medicine. Oxford University Press, New York.
29. Block ML, L Zecca and JS Hong. (2007). Microglia-me-diated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8:57-69.
30. Dutta R, J McDonough, X Yin, J Peterson, A Chang, T Torres, T Gudz, WB Macklin, DA Lewis, et al. (2006). Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann Neurol 59:478-489.
31. Covacu R, AI Danilov, BS Rasmussen, K Hallen, MC Moe, A Lobell, CB Johansson, MA Svensson, T Olsson and L Brundin. (2006). Nitric oxide exposure diverts neural stem cell fate from neurogenesis towards astrogliogenesis. Stem Cells 24:2792-2800.
32. Huang da W, BT Sherman and RA Lempicki. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57.
33. Scholzen T and J Gerdes. (2000). The Ki-67 protein: from the known and the unknown. J Cell Physiol 182:311-322.
34. Kriegstein A and A Alvarez-Buylla. (2009). The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184.
35. Hack MA, A Saghatelyan, A de Chevigny, A Pfeifer, R Ashery-Padan, PM Lledo and M Gotz. (2005). Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8:865-872.
36. Ishibashi M, K Moriyoshi, Y Sasai, K Shiota, S Nakanishi and R Kageyama. (1994). Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J 13: 1799-1805.
37. Chiba S. (2006). Notch signaling in stem cell systems. Stem Cells 24:2437-2447.
38. Bertrand N, DS Castro and F Guillemot. (2002). Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3:517-530.
39. Sun Y, M Nadal-Vicens, S Misono, MZ Lin, A Zubiaga, X Hua, G Fan and ME Greenberg. (2001). Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104:365-376.
40. Gangemi RM, M Perera and G Corte. (2004). Regulatory genes controlling cell fate choice in embryonic and adult neural stem cells. J Neurochem 89:286-306.
41. Hsieh J, K Nakashima, T Kuwabara, E Mejia and FH Gage. (2004). Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci USA 101:16659-16664.
42. Ji S, JR Doucette and AJ Nazarali. (2011). Sirt2 is a novel in vivo downstream target of Nkx2.2 and enhances oligo-dendroglial cell differentiation. J Mol Cell Biol 3:351-359.
43. Fridovich I. (1986). Biological effects of the superoxide radical. Arch Biochem Biophys 247:1-11.
44. Wittko IM, A Schanzer, A Kuzmichev, FT Schneider, M Shibuya, S Raab and KH Plate. (2009). VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream in vivo. J Neu-rosci 29:8704-8714.
45. Byrne AM, DJ Bouchier-Hayes and JH Harmey. (2005). Angiogenic and cell survival functions of vascular endo-thelial growth factor (VEGF). J Cell Mol Med 9:777-794.
46. Kirk SL and SJ Karlik. (2003). VEGF and vascular changes in chronic neuroinflammation. J Autoimmun 21:353-363.
47. Kim EJ, JL Ables, LK Dickel, AJ Eisch and JE Johnson. (2011). Ascl1 (Mash1) defines cells with long-term neu-rogenic potential in subgranular and subventricular zones in adult mouse brain. PloS One 6:e18472.
48. Imayoshi I, A Isomura, Y Harima, K Kawaguchi, H Kori, H Miyachi, T Fujiwara, F Ishidate and R Kageyama. (2013). Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 342:1203-1208.
49. Fuentealba LC, K Obernier and A Alvarez-Buylla. (2012). Adult neural stem cells bridge their niche. Cell Stem Cell 10:698-708.
50. Wang X and EK Michaelis. (2010). Selective neuronal vulnerability to oxidative stress in the brain. Front Aging Neurosci 2:12.
51. Steinbeck MJ, JK Kim, MJ Trudeau, PV Hauschka and MJ Karnovsky. (1998). Involvement of hydrogen peroxide in the differentiation of clonal HD-11EM cells into osteoclast-like cells. J Cell Physiol 176:574-587.
52. Zhang L, X Qin, Y Zhao, L Fast, S Zhuang, P Liu, G Cheng and TC Zhao. (2012). Inhibition of histone deacetylases preserves myocardial performance and prevents cardiac remodeling through stimulation of endogenous angiomyo-genesis. J Pharmacol Exp Therapeut 341:285-293.
53. Montgomery RL, J Hsieh, AC Barbosa, JA Richardson and EN Olson. (2009). Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc Natl Acad Sci USA 106:7876-7881.
54. Zhou Q, CL Dalgard, C Wynder and ML Doughty. (2011). Histone deacetylase inhibitors SAHA and sodium butyrate block G1-to-S cell cycle progression in neurosphere formation by adult subventricular cells. BMC Neurosci 12:50.
55. Kao HY, P Ordentlich, N Koyano-Nakagawa, Z Tang, M Downes, CR Kintner, RM Evans and T Kadesch. (1998). A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev 12:2269-2277.
56. Ajamian F, T Suuronen, A Salminen and M Reeben. (2003). Upregulation of class II histone deacetylases mRNA during neural differentiation of cultured rat hippo-campal progenitor cells. Neurosci Lett 346:57-60.
57. Perdiz D, R Mackeh, C Pous and A Baillet. (2011). The ins and outs of tubulin acetylation: more than just a post-translational modification? Cell Signal 23:763-771.
58. Etienne-Manneville S. (2010). From signaling pathways to microtubule dynamics: the key players. Curr Opin Cell Biol 22:104-111.
59. Friedman HV, T Bresler, CC Garner and NE Ziv. (2000). Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27:57-69.
60. Dick O, S tom Dieck, WD Altrock, J Ammermuller, R Weiler, CC Garner, ED Gundelfinger and JH Brandstatter. (2003). The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37:775-786.
61. Becher A, A Drenckhahn, I Pahner, M Margittai, R Jahn and G Ahnert-Hilger. (1999). The synaptophysin-synaptobrevin complex: a hallmark of synaptic vesicle maturation. J Neu-rosci 19:1922-1931.
62. Park HC and B Appel. (2003). Delta-Notch signaling regulates oligodendrocyte specification. Development 130: 3747-3755.
63. Zhou Q, G Choi and DJ Anderson. (2001). The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31: 791-807.
64. Imai S, CM Armstrong, M Kaeberlein and L Guarente. (2000). Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403:795-800.
65. Li W, B Zhang, J Tang, Q Cao, Y Wu, C Wu, J Guo, EA Ling and F Liang. (2007). Sirtuin 2, a mammalian homolog of yeast silent information regulator-2 longevity regulator, is an oligodendroglial protein that decelerates cell differentiation through deacetylating alpha-tubulin. J Neurosci 27:2606-2616.
66. Dringen R. (2000). Metabolism and functions of glutathi-one in brain. Prog Neurobiol 62:649-671.
67. Fridovich I. (1995). Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97-112.
68. Smith J, E Ladi, M Mayer-Proschel and M Noble. (2000). 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 97:10032-10037.
69. Thorburne SK and BH Juurlink. (1996). Low glutathione and high iron govern the susceptibility of oligodendroglial precursors to oxidative stress. J Neurochem 67:1014-1022.
70. Khanna S, S Roy, D Bagchi, M Bagchi and CK Sen. (2001). Upregulation of oxidant-induced VEGF expression in cultured keratinocytes by a grape seed proanthocyanidin extract. Free Radic Biol Med 31:38-42.
71. Sondell M, G Lundborg and M Kanje. (1999). Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci 19:5731-5740.
72. Stone J, A Itin, T Alon, J Pe'er, H Gnessin, T Chan-Ling and E Keshet. (1995). Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15: 4738-4747.