Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2017, Article ID 9209127, 13 pages
https://doi.org/10.1155/2017/9209127
Review Article

Regulatory Role of Redox Balance in Determination of Neural Precursor Cell Fate

The Regenerative Medicine Program, Spinal Cord Research Centre, Department of Physiology and Pathophysiology, University of Manitoba, Winnipeg, MB, Canada R3E 0J9

Correspondence should be addressed to Eftekhar Eftekharpour; ac.abotinamu@rahketfe

Received 15 May 2017; Accepted 22 June 2017; Published 18 July 2017

Academic Editor: Gerald A. Colvin

Copyright © 2017 Mohamed Ariff Iqbal and Eftekhar Eftekharpour. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Altman and G. D. Das, “Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats,” The Journal of Comparative Neurology, vol. 124, no. 3, pp. 319–335, 1965. View at Google Scholar
  2. M. Berry and A. W. Rogers, “The migration of neuroblasts in the developing cerebral cortex,” Journal of Anatomy, vol. 99, Part 4, pp. 691–709, 1965. View at Google Scholar
  3. B. A. Reynolds, W. Tetzlaff, and S. Weiss, “A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes,” The Journal of Neuroscience, vol. 12, no. 11, pp. 4565–4574, 1992. View at Google Scholar
  4. B. A. Reynolds and S. Weiss, “Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system,” Science, vol. 255, no. 5052, pp. 1707–1710, 1992. View at Google Scholar
  5. S. Weiss, C. Dunne, J. Hewson et al., “Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis,” The Journal of Neuroscience, vol. 16, no. 23, pp. 7599–7609, 1996. View at Google Scholar
  6. C. M. Morshead, B. A. Reynolds, C. G. Craig et al., “Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells,” Neuron, vol. 13, no. 5, pp. 1071–1082, 1994. View at Google Scholar
  7. R. Galli, A. Gritti, L. Bonfanti, and A. L. Vescovi, “Neural stem cells: an overview,” Circulation Research, vol. 92, no. 6, pp. 598–608, 2003. View at Google Scholar
  8. L. L. Horky, F. Galimi, F. H. Gage, and P. J. Horner, “Fate of endogenous stem/progenitor cells following spinal cord injury,” The Journal of Comparative Neurology, vol. 498, no. 4, pp. 525–538, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Alizadeh, S. M. Dyck, and S. Karimi-Abdolrezaee, “Myelin damage and repair in pathologic CNS: challenges and prospects,” Frontiers in Molecular Neuroscience, vol. 8, p. 35, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. S. M. Dyck and S. Karimi-Abdolrezaee, “Chondroitin sulfate proteoglycans: key modulators in the developing and pathologic central nervous system,” Experimental Neurology, vol. 269, pp. 169–187, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. S. M. Dyck, A. Alizadeh, K. T. Santhosh, E. H. Proulx, C. L. Wu, and S. Karimi‐Abdolrezaee, “Chondroitin sulfate proteoglycans negatively modulate spinal cord neural precursor cells by signaling through LAR and RPTPsigma and modulation of the Rho/ROCK pathway,” Stem Cells, vol. 33, no. 8, pp. 2550–2563, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Paul, Z. Chaker, and F. Doetsch, “Hypothalamic regulation of regionally distinct adult neural stem cells and neurogenesis,” Science, 2017. View at Publisher · View at Google Scholar
  13. J. M. Garcia-Verdugo, F. Doetsch, H. Wichterle, D. A. Lim, and A. Alvarez‐Buylla, “Architecture and cell types of the adult subventricular zone: in search of the stem cells,” Journal of Neurobiology, vol. 36, no. 2, pp. 234–248, 1998. View at Google Scholar
  14. J. H. Schippers, H. M. Nguyen, D. Lu, R. Schmidt, and B. Mueller-Roeber, “ROS homeostasis during development: an evolutionary conserved strategy,” Cellular and Molecular Life Sciences, vol. 69, no. 19, pp. 3245–3257, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. D. P. Jones, “Redox sensing: orthogonal control in cell cycle and apoptosis signalling,” Journal of Internal Medicine, vol. 268, no. 5, pp. 432–448, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Brune, N. Dehne, N. Grossmann et al., “Redox control of inflammation in macrophages,” Antioxidants & Redox Signaling, vol. 19, no. 6, pp. 595–637, 2013. View at Google Scholar
  17. S. M. Bailey and C. C. Cunningham, “Acute and chronic ethanol increases reactive oxygen species generation and decreases viability in fresh, isolated rat hepatocytes,” Hepatology, vol. 28, no. 5, pp. 1318–1326, 1998. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. S. Bae, H. Oh, S. G. Rhee, and Y. D. Yoo, “Regulation of reactive oxygen species generation in cell signaling,” Molecules and Cells, vol. 32, no. 6, pp. 491–509, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Hou, X. Ouyang, R. Wan, H. Cheng, M. P. Mattson, and A. Cheng, “Mitochondrial superoxide production negatively regulates neural progenitor proliferation and cerebral cortical development,” Stem Cells, vol. 30, no. 11, pp. 2535–2547, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. J. P. Forder and M. Tymianski, “Postsynaptic mechanisms of excitotoxicity: involvement of postsynaptic density proteins, radicals, and oxidant molecules,” Neuroscience, vol. 158, no. 1, pp. 293–300, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. G. P. Bienert, J. K. Schjoerring, and T. P. Jahn, “Membrane transport of hydrogen peroxide,” Biochimica et Biophysica Acta, vol. 1758, no. 8, pp. 994–1003, 2006. View at Google Scholar
  22. M. Gerlach, K. L. Double, D. Ben-Shachar, L. Zecca, M. B. Youdim, and P. Riederer, “Neuromelanin and its interaction with iron as a potential risk factor for dopaminergic neurodegeneration underlying Parkinson’s disease,” Neurotoxicity Research, vol. 5, no. 1-2, pp. 35–44, 2003. View at Google Scholar
  23. E. Niki, “Interaction of ascorbate and alpha-tocopherol,” Annals of the new York Academy of Sciences, vol. 498, pp. 186–199, 1987. View at Google Scholar
  24. M. Schieber and N. S. Chandel, “ROS function in redox signaling and oxidative stress,” Current Biology, vol. 24, no. 10, pp. R453–R462, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. P. J. Kiley and G. Storz, “Exploiting thiol modifications,” PLoS Biology, vol. 2, no. 11, article e400, 2004. View at Google Scholar
  26. A. Miseta and P. Csutora, “Relationship between the occurrence of cysteine in proteins and the complexity of organisms,” Molecular Biology and Evolution, vol. 17, no. 8, pp. 1232–1239, 2000. View at Google Scholar
  27. Y. M. Go, J. D. Chandler, and D. P. Jones, “The cysteine proteome,” Free Radical Biology & Medicine, vol. 84, pp. 227–245, 2015. View at Google Scholar
  28. D. Spadaro, B. W. Yun, S. H. Spoel, C. Chu, Y. Q. Wang, and G. J. Loake, “The redox switch: dynamic regulation of protein function by cysteine modifications,” Physiologia Plantarum, vol. 138, no. 4, pp. 360–371, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Hwang, H. W. Suh, Y. H. Jeon et al., “The structural basis for the negative regulation of thioredoxin by thioredoxin-interacting protein,” Nature Communications, vol. 5, p. 2958, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Hoshi and S. Heinemann, “Regulation of cell function by methionine oxidation and reduction,” The Journal of Physiology, vol. 531, Part 1, pp. 1–11, 2001. View at Google Scholar
  31. V. Tropepe, M. Sibilia, B. G. Ciruna, J. Rossant, E. F. Wagner, and D. Kooy, “Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon,” Developmental Biology, vol. 208, no. 1, pp. 166–188, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. J. R. Lee and G. A. Koretzky, “Extracellular signal-regulated kinase-2, but not c-Jun NH2-terminal kinase, activation correlates with surface IgM-mediated apoptosis in the WEHI 231 B cell line,” Journal of Immunology, vol. 161, no. 4, pp. 1637–1644, 1998. View at Google Scholar
  33. P. Nagakannan, M. A. Iqbal, A. Yeung et al., “Perturbation of redox balance after thioredoxin reductase deficiency interrupts autophagy-lysosomal degradation pathway and enhances cell death in nutritionally stressed SH-SY5Y cells,” Free Radical Biology & Medicine, vol. 101, pp. 53–70, 2016. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Nagakannan and E. Eftekharpour, “Differential redox sensitivity of cathepsin B and L holds the key to autophagy-apoptosis interplay after Thioredoxin reductase inhibition in nutritionally stressed SH-SY5Y cells,” Free Radical Biology & Medicine, vol. 108, pp. 819–831, 2017. View at Publisher · View at Google Scholar
  35. J. Chiu and I. W. Dawes, “Redox control of cell proliferation,” Trends in Cell Biology, vol. 22, no. 11, pp. 592–601, 2012. View at Google Scholar
  36. H. Miki and Y. Funato, “Regulation of intracellular signalling through cysteine oxidation by reactive oxygen species,” Journal of Biochemistry, vol. 151, no. 3, pp. 255–261, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Pani, R. Colavitti, B. Bedogni, R. Anzevino, S. Borrello, and T. Galeotti, “A redox signaling mechanism for density-dependent inhibition of cell growth,” The Journal of Biological Chemistry, vol. 275, no. 49, pp. 38891–38899, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. C. L. Limoli, R. Rola, E. Giedzinski, S. Mantha, T. T. Huang, and J. R. Fike, “Cell-density-dependent regulation of neural precursor cell function,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 45, pp. 16052–16057, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Sundaresan, Y. U. Zu-Xi, V. J. Ferrans et al., “Regulation of reactive-oxygen-species generation in fibroblasts by Rac1,” The Biochemical Journal, vol. 318, Part 2, pp. 379–382, 1996. View at Google Scholar
  40. Y. S. Bae, S. W. Kang, M. S. Seo et al., “Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation,” The Journal of Biological Chemistry, vol. 272, no. 1, pp. 217–221, 1997. View at Google Scholar
  41. K. Pietz, P. Odin, K. Funa, and O. Lindvall, “Protective effect of platelet-derived growth factor against 6-hydroxydopamine-induced lesion of rat dopaminergic neurons in culture,” Neuroscience Letters, vol. 204, no. 1-2, pp. 101–104, 1996. View at Google Scholar
  42. M. C. Raff, L. E. Lillien, W. D. Richardson, J. F. Burne, and M. D. Noble, “Platelet-derived growth factor from astrocytes drives the clock that times oligodendrocyte development in culture,” Nature, vol. 333, no. 6173, pp. 562–565, 1988. View at Publisher · View at Google Scholar
  43. A. Smits, M. Kato, B. Westermark, M. Nister, C. H. Heldin, and K. Funa, “Neurotrophic activity of platelet-derived growth factor (PDGF): rat neuronal cells possess functional PDGF beta-type receptors and respond to PDGF,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 18, pp. 8159–8163, 1991. View at Google Scholar
  44. A. Erlandsson, M. Enarsson, and K. Forsberg-Nilsson, “Immature neurons from CNS stem cells proliferate in response to platelet-derived growth factor,” The Journal of Neuroscience, vol. 21, no. 10, pp. 3483–3491, 2001. View at Google Scholar
  45. T. Adachi, H. Togashi, A. Suzuki et al., “NAD(P)H oxidase plays a crucial role in PDGF-induced proliferation of hepatic stellate cells,” Hepatology, vol. 41, no. 6, pp. 1272–1281, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Sundaresan, Z. X. Yu, V. J. Ferrans, K. Irani, and T. Finkel, “Requirement for generation of H2O2 for platelet-derived growth factor signal transduction,” Science, vol. 270, no. 5234, pp. 296–299, 1995. View at Google Scholar
  47. J. E. Belle, N. M. Orozco, A. A. Paucar 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, vol. 8, no. 1, pp. 59–71, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Kim and P. K. Wong, “Loss of ATM impairs proliferation of neural stem cells through oxidative stress-mediated p38 MAPK signaling,” Stem Cells, vol. 27, no. 8, pp. 1987–1998, 2009. View at Google Scholar
  49. J. Smith, E. Ladi, M. Mayer-Pröschel, and M. Noble, “Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 18, pp. 10032–10037, 2000. View at Publisher · View at Google Scholar
  50. T. Prozorovski, U. Schulze-Topphoff, R. Glumm et al., “Sirt1 contributes critically to the redox-dependent fate of neural progenitors,” Nature Cell Biology, vol. 10, no. 4, pp. 385–394, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Prozorovski, R. Schneider, C. Berndt, H. P. Hartung, and O. Aktas, “Redox-regulated fate of neural stem progenitor cells,” Biochimica et Biophysica Acta, vol. 1850, no. 8, pp. 1543–1554, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Tsatmali, E. C. Walcott, and K. L. Crossin, “Newborn neurons acquire high levels of reactive oxygen species and increased mitochondrial proteins upon differentiation from progenitors,” Brain Research, vol. 1040, no. 1-2, pp. 137–150, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. L. Studer, M. Csete, S. H. Lee et al., “Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen,” The Journal of Neuroscience, vol. 20, no. 19, pp. 7377–7383, 2000. View at Google Scholar
  54. L. Filippis and D. Delia, “Hypoxia in the regulation of neural stem cells,” Cellular and Molecular Life Sciences, vol. 68, no. 17, pp. 2831–2844, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. L. Clarke and D. v. d. Kooy, “Low oxygen enhances primitive and definitive neural stem cell colony formation by inhibiting distinct cell death pathways,” Stem Cells, vol. 27, no. 8, pp. 1879–1886, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Chuikov, B. P. Levi, M. L. Smith, and S. J. Morrison, “Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress,” Nature Cell Biology, vol. 12, no. 10, pp. 999–1006, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. G. Nickenig, S. Baudler, C. Müller et al., “Redox-sensitive vascular smooth muscle cell proliferation is mediated by GKLF and Id3 in vitro and in vivo,” The FASEB Journal, vol. 16, no. 9, pp. 1077–1086, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. L. M. Randall, G. Ferrer-Sueta, and A. Denicola, “Peroxiredoxins as preferential targets in H2O2-induced signaling,” Methods in Enzymology, vol. 527, pp. 41–63, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Ditch and T. T. Paull, “The ATM protein kinase and cellular redox signaling: beyond the DNA damage response,” Trends in Biochemical Sciences, vol. 37, no. 1, pp. 15–22, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. D. M. Allen, D. M. Allen, H. Praag et al., “Ataxia telangiectasia mutated is essential during adult neurogenesis,” Genes & Development, vol. 15, no. 5, pp. 554–566, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. C. Barlow, K. D. Brown, C. X. Deng, D. A. Tagle, and A. Wynshaw-Boris, “Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways,” Nature Genetics, vol. 17, no. 4, pp. 453–456, 1997. View at Publisher · View at Google Scholar
  62. K. Lin, J. B. Dorman, A. Rodan, and C. Kenyon, “daf-16: an HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans,” Science, vol. 278, no. 5341, pp. 1319–1322, 1997. View at Google Scholar
  63. B. J. Willcox, T. A. Donlon, Q. He et al., “FOXO3A genotype is strongly associated with human longevity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 37, pp. 13987–13992, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. X. Zhang, S. Yalcin, D. F. Lee et al., “FOXO1 is an essential regulator of pluripotency in human embryonic stem cells,” Nature Cell Biology, vol. 13, no. 9, pp. 1092–9, 2011. View at Google Scholar
  65. D. Y. Kim, I. Hwang, F. L. Muller, and J. H. Paik, “Functional regulation of FoxO1 in neural stem cell differentiation,” Cell Death and Differentiation, vol. 22, no. 12, pp. 2034–2045, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. V. M. Renault, V. A. Rafalski, A. A. Morgan et al., “FoxO3 regulates neural stem cell homeostasis,” Cell Stem Cell, vol. 5, no. 5, pp. 527–539, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. M. K. Lehtinen, Z. Yuan, P. R. Boag et al., “A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span,” Cell, vol. 125, no. 5, pp. 987–1001, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. Z. Tothova, R. Kollipara, B. J. Huntly et al., “FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress,” Cell, vol. 128, no. 2, pp. 325–339, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. J. H. Paik, Z. Ding, R. Narurkar et al., “FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis,” Cell Stem Cell, vol. 5, no. 5, pp. 540–553, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. C. Neri, “Role and therapeutic potential of the pro-longevity factor FOXO and its regulators in neurodegenerative disease,” Frontiers in Pharmacology, vol. 3, p. 15, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Zhang, W. Huan, H. Wei et al., “FOXO3a/p27kip1 expression and essential role after acute spinal cord injury in adult rat,” Journal of Cellular Biochemistry, vol. 114, no. 2, pp. 354–365, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. H. Yeo, C. A. Lyssiotis, Y. Zhang et al., “FoxO3 coordinates metabolic pathways to maintain redox balance in neural stem cells,” The EMBO Journal, vol. 32, no. 19, pp. 2589–2602, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. M. C. Simon and B. Keith, “The role of oxygen availability in embryonic development and stem cell function,” Nature Reviews. Molecular Cell Biology, vol. 9, no. 4, pp. 285–296, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. T. Roitbak, L. Li, and L. A. Cunningham, “Neural stem/progenitor cells promote endothelial cell morphogenesis and protect endothelial cells against ischemia via HIF-1alpha-regulated VEGF signaling,” Journal of Cerebral Blood Flow and Metabolism, vol. 28, no. 9, pp. 1530–1542, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. L. Li, K. M. Candelario, K. Thomas et al., “Hypoxia inducible factor-1alpha (HIF-1alpha) is required for neural stem cell maintenance and vascular stability in the adult mouse SVZ,” The Journal of Neuroscience, vol. 34, no. 50, pp. 16713–16719, 2014. View at Publisher · View at Google Scholar · View at Scopus
  76. S. Tomita, M. Ueno, M. Sakamoto et al., “Defective brain development in mice lacking the Hif-1alpha gene in neural cells,” Molecular and Cellular Biology, vol. 23, no. 19, pp. 6739–6749, 2003. View at Google Scholar
  77. R. Rodrigo, R. Fernández-Gajardo, R. Gutiérrez et al., “Oxidative stress and pathophysiology of ischemic stroke: novel therapeutic opportunities,” CNS & Neurological Disorders Drug Targets, vol. 12, no. 5, pp. 698–714, 2013. View at Google Scholar
  78. B. D. Hoehn, T. D. Palmer, and G. K. Steinberg, “Neurogenesis in rats after focal cerebral ischemia is enhanced by indomethacin,” Stroke, vol. 36, no. 12, pp. 2718–2724, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. J. Marti-Fabregas, M. Romaguera-Ros, U. Gomez-Pinedo et al., “Proliferation in the human ipsilateral subventricular zone after ischemic stroke,” Neurology, vol. 74, no. 5, pp. 357–365, 2010. View at Publisher · View at Google Scholar
  80. H. L. Vieira, P. M. Alves, and A. Vercelli, “Modulation of neuronal stem cell differentiation by hypoxia and reactive oxygen species,” Progress in Neurobiology, vol. 93, no. 3, pp. 444–455, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. S. D. Westfall, S. Sachdev, P. Das et al., “Identification of oxygen-sensitive transcriptional programs in human embryonic stem cells,” Stem Cells and Development, vol. 17, no. 5, pp. 869–881, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Bonello, C. Zähringer, B. A. RS et al., “Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 4, pp. 755–761, 2007. View at Publisher · View at Google Scholar · View at Scopus
  83. G. Yuan, S. A. Khan, W. Luo, J. Nanduri, G. L. Semenza, and N. R. Prabhakar, “Hypoxia-inducible factor 1 mediates increased expression of NADPH oxidase-2 in response to intermittent hypoxia,” Journal of Cellular Physiology, vol. 226, no. 11, pp. 2925–2933, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. G. L. Semenza, “Hypoxia-inducible factors in physiology and medicine,” Cell, vol. 148, no. 3, pp. 399–408, 2012. View at Google Scholar
  85. W. Wu, X. Chen, C. Hu, J. Li, Z. Yu, and W. Cai, “Transplantation of neural stem cells expressing hypoxia-inducible factor-1alpha (HIF-1alpha) improves behavioral recovery in a rat stroke model,” Journal of Clinical Neuroscience, vol. 17, no. 1, pp. 92–95, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. P. A. Steck, M. A. Pershouse, S. A. Jasser et al., “Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers,” Nature Genetics, vol. 15, no. 4, pp. 356–362, 1997. View at Google Scholar
  87. J. Li, C. Yen, D. Liaw et al., “PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer,” Science, vol. 275, no. 5308, pp. 1943–1947, 1997. View at Google Scholar
  88. E. Napoli, C. Ross-Inta, S. Wong et al., “Mitochondrial dysfunction in Pten haplo-insufficient mice with social deficits and repetitive behavior: interplay between Pten and p53,” PloS One, vol. 7, no. 8, article e42504, 2012. View at Google Scholar
  89. A. D. Sinor and L. Lillien, “Akt-1 expression level regulates CNS precursors,” The Journal of Neuroscience, vol. 24, no. 39, pp. 8531–8541, 2004. View at Google Scholar
  90. M. Groszer, R. Erickson, D. D. Scripture-Adams et al., “PTEN negatively regulates neural stem cell self-renewal by modulating G0-G1 cell cycle entry,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 1, pp. 111–116, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Kwon, S. R. Lee, K. S. Yang et al., “Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 47, pp. 16419–16424, 2004. View at Google Scholar
  92. B. C. Dickinson, J. Peltier, D. Stone, D. V. Schaffer, and C. J. Chang, “Nox2 redox signaling maintains essential cell populations in the brain,” Nature Chemical Biology, vol. 7, no. 2, pp. 106–112, 2011. View at Google Scholar
  93. R. Requejo-Aguilar, I. Lopez-Fabuel, E. Fernandez, L. M. Martins, A. Almeida, and J. P. Bolaños, “PINK1 deficiency sustains cell proliferation by reprogramming glucose metabolism through HIF1,” Nature Communications, vol. 5, p. 4514, 2014. View at Publisher · View at Google Scholar · View at Scopus
  94. E. M. Valente, P. M. Abou-Sleiman, V. Caputo et al., “Hereditary early-onset Parkinson’s disease caused by mutations in PINK1,” Science, vol. 304, no. 5674, pp. 1158–1160, 2004. View at Google Scholar
  95. I. Choi, D. J. Choi, H. Yang et al., “PINK1 expression increases during brain development and stem cell differentiation, and affects the development of GFAP-positive astrocytes,” Molecular Brain, vol. 9, p. 5, 2016. View at Google Scholar
  96. K. Meletis, V. Wirta, S. M. Hede, M. Nistér, J. Lundeberg, and J. Frisén, “p53 suppresses the self-renewal of adult neural stem cells,” Development, vol. 133, no. 2, pp. 363–369, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. T. Lin, C. Chao, S. I. Saito et al., “p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression,” Nature Cell Biology, vol. 7, no. 2, pp. 165–171, 2005. View at Google Scholar
  98. A. Tedeschi and S. D. Giovanni, “The non-apoptotic role of p53 in neuronal biology: enlightening the dark side of the moon,” EMBO Reports, vol. 10, no. 6, pp. 576–583, 2009. View at Google Scholar
  99. F. Talos, A. Abraham, A. V. Vaseva et al., “p73 is an essential regulator of neural stem cell maintenance in embryonal and adult CNS neurogenesis,” Cell Death and Differentiation, vol. 17, no. 12, pp. 1816–1829, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. K. Forsberg, A. Wuttke, G. Quadrato, P. M. Chumakov, A. Wizenmann, and S. Giovanni, “The tumor suppressor p53 fine-tunes reactive oxygen species levels and neurogenesis via PI3 kinase signaling,” The Journal of Neuroscience, vol. 33, no. 36, pp. 14318–14330, 2013. View at Google Scholar
  101. Q. Ma, “Role of nrf2 in oxidative stress and toxicity,” Annual Review of Pharmacology and Toxicology, vol. 53, pp. 401–426, 2013. View at Google Scholar
  102. L. Madhavan, “Redox-based regulation of neural stem cell function and Nrf2,” Biochemical Society Transactions, vol. 43, no. 4, pp. 627–631, 2015. View at Google Scholar
  103. V. Karkkainen, Y. Pomeshchik, E. Savchenko et al., “Nrf2 regulates neurogenesis and protects neural progenitor cells against Abeta toxicity,” Stem Cells, vol. 32, no. 7, pp. 1904–1916, 2014. View at Publisher · View at Google Scholar · View at Scopus
  104. J. Li, D. Johnson, M. Calkins, L. Wright, C. Svendsen, and J. Johnson, “Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells,” Toxicological Sciences, vol. 83, no. 2, pp. 313–328, 2005. View at Google Scholar
  105. J. S. Nye, R. Kopan, and R. Axel, “An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells,” Development, vol. 120, no. 9, pp. 2421–2430, 1994. View at Google Scholar
  106. M. Khacho, A. Clark, D. S. Svoboda et al., “Mitochondrial dynamics impacts stem cell identity and fate decisions by regulating a nuclear transcriptional program,” Cell Stem Cell, vol. 19, no. 2, pp. 232–247, 2016. View at Google Scholar
  107. N. Shyh-Chang, G. Q. Daley, and L. C. Cantley, “Stem cell metabolism in tissue development and aging,” Development, vol. 140, no. 12, pp. 2535–2547, 2013. View at Google Scholar
  108. C. C. Homem, M. Repic, and J. A. Knoblich, “Proliferation control in neural stem and progenitor cells,” Nature Reviews. Neuroscience, vol. 16, no. 11, pp. 647–659, 2015. View at Google Scholar
  109. X. Zheng, L. Boyer, M. Jin et al., “Metabolic reprogramming during neuronal differentiation from aerobic glycolysis to neuronal oxidative phosphorylation,” eLife, vol. 5, 2016. View at Publisher · View at Google Scholar · View at Scopus
  110. S. Bartesaghi, V. Graziano, S. Galavotti et al., “Inhibition of oxidative metabolism leads to p53 genetic inactivation and transformation in neural stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 4, pp. 1059–1064, 2015. View at Google Scholar
  111. K. J. Ahlqvist, R. H. Hämäläinen, S. Yatsuga et al., “Somatic progenitor cell vulnerability to mitochondrial DNA mutagenesis underlies progeroid phenotypes in Polg mutator mice,” Cell Metabolism, vol. 15, no. 1, pp. 100–109, 2012. View at Google Scholar
  112. R. H. Hamalainen, K. J. Ahlqvist, P. Ellonen et al., “mtDNA mutagenesis disrupts pluripotent stem cell function by altering redox signaling,” Cell Reports, vol. 11, no. 10, pp. 1614–1624, 2015. View at Publisher · View at Google Scholar · View at Scopus
  113. R. Beckervordersandforth, B. Ebert, I. Schäffner et al., “Role of mitochondrial metabolism in the control of early lineage progression and aging phenotypes in adult hippocampal neurogenesis,” Neuron, vol. 93, no. 6, p. 1518, 2017. View at Google Scholar
  114. M. A. Bin-Umer, J. E. McLaughlin, M. S. Butterly, S. McCormick, and N. E. Tumer, “Elimination of damaged mitochondria through mitophagy reduces mitochondrial oxidative stress and increases tolerance to trichothecenes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 32, pp. 11798–11803, 2014. View at Google Scholar
  115. M. Frank, S. Duvezin-Caubet, S. Koob et al., “Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner,” Biochimica et Biophysica Acta, vol. 1823, no. 12, pp. 2297–2310, 2012. View at Publisher · View at Google Scholar · View at Scopus
  116. G. N. Paliouras, L. K. Hamilton, A. Aumont, S. E. Joppé, F. Barnabé-Heider, and K. J. Fernandes, “Mammalian target of rapamycin signaling is a key regulator of the transit-amplifying progenitor pool in the adult and aging forebrain,” The Journal of Neuroscience, vol. 32, no. 43, pp. 15012–15026, 2012. View at Publisher · View at Google Scholar · View at Scopus
  117. P. Vazquez, A. I. Arroba, F. Cecconi, E. J. Rosa, P. Boya, and F. Pablo, “Atg5 and Ambra1 differentially modulate neurogenesis in neural stem cells,” Autophagy, vol. 8, no. 2, pp. 187–199, 2012. View at Google Scholar
  118. L. Poillet-Perez, G. Despouy, R. Delage-Mourroux, and M. Boyer-Guittaut, “Interplay between ROS and autophagy in cancer cells, from tumor initiation to cancer therapy,” Redox Biology, vol. 4, pp. 184–192, 2015. View at Google Scholar
  119. G. Filomeni, D. D. Zio, and F. Cecconi, “Oxidative stress and autophagy: the clash between damage and metabolic needs,” Cell Death and Differentiation, vol. 22, no. 3, pp. 377–388, 2015. View at Google Scholar
  120. C. Wang, C. C. Liang, Z. C. Bian, Y. Zhu, and J. L. Guan, “FIP200 is required for maintenance and differentiation of postnatal neural stem cells,” Nature Neuroscience, vol. 16, no. 5, pp. 532–542, 2013. View at Google Scholar
  121. C. Wang, S. Chen, S. Yeo et al., “Elevated p62/SQSTM1 determines the fate of autophagy-deficient neural stem cells by increasing superoxide,” The Journal of Cell Biology, vol. 212, no. 5, pp. 545–560, 2016. View at Google Scholar
  122. A. Holmgren, “Reduction of disulfides by thioredoxin. Exceptional reactivity of insulin and suggested functions of thioredoxin in mechanism of hormone action,” The Journal of Biological Chemistry, vol. 254, no. 18, pp. 9113–9119, 1979. View at Google Scholar
  123. A. Holmgren, “Thioredoxin,” Annual Review of Biochemistry, vol. 54, pp. 237–271, 1985. View at Google Scholar
  124. M. Matsui, M. Oshima, H. Oshima et al., “Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene,” Developmental Biology, vol. 178, no. 1, pp. 179–185, 1996. View at Publisher · View at Google Scholar · View at Scopus
  125. J. E. Oblong, M. Berggren, P. Y. Gasdaska, and G. Powis, “Site-directed mutagenesis of active site cysteines in human thioredoxin produces competitive inhibitors of human thioredoxin reductase and elimination of mitogenic properties of thioredoxin,” The Journal of Biological Chemistry, vol. 269, no. 16, pp. 11714–11720, 1994. View at Google Scholar
  126. J. R. Gasdaska, M. Berggren, and G. Powis, “Cell growth stimulation by the redox protein thioredoxin occurs by a novel helper mechanism,” Cell Growth & Differentiation, vol. 6, no. 12, pp. 1643–1650, 1995. View at Google Scholar
  127. Y. Guo, L. Einhorn, M. Kelley et al., “Redox regulation of the embryonic stem cell transcription factor oct-4 by thioredoxin,” Stem Cells, vol. 22, no. 3, pp. 259–264, 2004. View at Google Scholar
  128. M. Bhatia, K. L. McGrath, G. Trapani et al., “The thioredoxin system in breast cancer cell invasion and migration,” Redox Biology, vol. 8, pp. 68–78, 2016. View at Publisher · View at Google Scholar · View at Scopus
  129. G. Powis, D. Mustacich, and A. Coon, “The role of the redox protein thioredoxin in cell growth and cancer,” Free Radical Biology & Medicine, vol. 29, no. 3-4, pp. 312–322, 2000. View at Google Scholar
  130. A. Rubartelli, A. Bajetto, G. Allavena, E. Wollman, and R. Sitia, “Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory pathway,” The Journal of Biological Chemistry, vol. 267, no. 34, pp. 24161–24164, 1992. View at Google Scholar
  131. I. Hattori, Y. Takagi, H. Nakamura et al., “Intravenous administration of thioredoxin decreases brain damage following transient focal cerebral ischemia in mice,” Antioxidants & Redox Signaling, vol. 6, no. 1, pp. 81–87, 2004. View at Publisher · View at Google Scholar
  132. L. Tian, H. Nie, Y. Zhang et al., “Recombinant human thioredoxin-1 promotes neurogenesis and facilitates cognitive recovery following cerebral ischemia in mice,” Neuropharmacology, vol. 77, pp. 453–464, 2014. View at Google Scholar
  133. M. Saitoh, H. Nishitoh, M. Fujii et al., “Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1,” The EMBO Journal, vol. 17, no. 9, pp. 2596–2606, 1998. View at Publisher · View at Google Scholar · View at Scopus
  134. H. Liu, H. Nishitoh, H. Ichijo, and J. M. Kyriakis, “Activation of apoptosis signal-regulating kinase 1 (ASK1) by tumor necrosis factor receptor-associated factor 2 requires prior dissociation of the ASK1 inhibitor thioredoxin,” Molecular and Cellular Biology, vol. 20, no. 6, pp. 2198–2208, 2000. View at Google Scholar
  135. Y. Takagi, T. Tokime, K. Nozaki, Y. Gon, H. Kikuchi, and J. Yodoi, “Redox control of neuronal damage during brain ischemia after middle cerebral artery occlusion in the rat: immunohistochemical and hybridization studies of thioredoxin,” Journal of Cerebral Blood Flow and Metabolism, vol. 18, no. 2, pp. 206–214, 1998. View at Google Scholar
  136. T. Lane, B. Flam, R. Lockey, and N. Kolliputi, “TXNIP shuttling: missing link between oxidative stress and inflammasome activation,” Frontiers in Physiology, vol. 4, p. 50, 2013. View at Publisher · View at Google Scholar · View at Scopus
  137. T. S. Devi, I. Lee, M. Hüttemann, A. Kumar, K. D. Nantwi, and L. P. Singh, “TXNIP links innate host defense mechanisms to oxidative stress and inflammation in retinal Muller glia under chronic hyperglycemia: implications for diabetic retinopathy,” Experimental Diabetes Research, vol. 2012, Article ID 438238, 19 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  138. L. K. Hamilton, M. Dufresne, S. E. Joppe et al., “Aberrant lipid metabolism in the forebrain niche suppresses adult neural stem cell proliferation in an animal model of Alzheimer’s disease,” Cell Stem Cell, vol. 17, no. 4, pp. 397–411, 2015. View at Publisher · View at Google Scholar · View at Scopus
  139. F. Barnabe-Heider, C. Göritz, H. Sabelström et al., “Origin of new glial cells in intact and injured adult spinal cord,” Cell Stem Cell, vol. 7, no. 4, pp. 470–482, 2010. View at Google Scholar
  140. G. U. Hoglinger, P. Rizk, M. P. Muriel et al., “Dopamine depletion impairs precursor cell proliferation in Parkinson disease,” Nature Neuroscience, vol. 7, no. 7, pp. 726–735, 2004. View at Publisher · View at Google Scholar · View at Scopus
  141. I. B. Leibiger and P. O. Berggren, “Sirt1: a metabolic master switch that modulates lifespan,” Nature Medicine, vol. 12, no. 1, pp. 34–36, 2006. View at Publisher · View at Google Scholar · View at Scopus
  142. X. Ou, M. R. Lee, X. Huang, S. Messina‐Graham, and H. E. Broxmeyer, “SIRT1 positively regulates autophagy and mitochondria function in embryonic stem cells under oxidative stress,” Stem Cells, vol. 32, no. 5, pp. 1183–1194, 2014. View at Publisher · View at Google Scholar · View at Scopus
  143. L. R. Stein and S. Imai, “Specific ablation of Nampt in adult neural stem cells recapitulates their functional defects during aging,” The EMBO Journal, vol. 33, no. 12, pp. 1321–1340, 2014. View at Publisher · View at Google Scholar · View at Scopus
  144. H. Zhang, D. Ryu, Y. Wu et al., “NAD(+) repletion improves mitochondrial and stem cell function and enhances life span in mice,” Science, vol. 352, no. 6292, pp. 1436–1443, 2016. View at Publisher · View at Google Scholar · View at Scopus