Advertisement

Molecular Neurobiology

, Volume 53, Issue 5, pp 2815–2825 | Cite as

SIRT1 and Neural Cell Fate Determination

  • Yulong Cai
  • Le Xu
  • Haiwei XuEmail author
  • Xiaotang FanEmail author
Article

Abstract

During the development of the central nervous system (CNS), neurons and glia are derived from multipotent neural stem cells (NSCs) undergoing self-renewal. NSC commitment and differentiation are tightly controlled by intrinsic and external regulatory mechanisms in space- and time-related fashions. SIRT1, a silent information regulator 2 (Sir2) ortholog, is expressed in several areas of the brain and has been reported to be involved in the self-renewal, multipotency, and fate determination of NSCs. Recent studies have highlighted the role of the deacetylase activity of SIRT1 in the determination of the final fate of NSCs. This review summarizes the roles of SIRT1 in the expansion and differentiation of NSCs, specification of neuronal subtypes and glial cells, and reprogramming of functional neurons from embryonic stem cells and fibroblasts. This review also discusses potential signaling pathways through which SIRT1 can exhibit versatile functions in NSCs to regulate the cell fate decisions of neurons and glia.

Keywords

SIRT1 Neural stem cells Neuron Differentiation Deacetylation 

Notes

Acknowledgments

This study was supported by the National Nature Science Foundation of China (No. (81371197, 31271051), Natural Science Foudation Project of CQ CSTC 2013jjB10028.

References

  1. 1.
    Donmez G (2012) The neurobiology of sirtuins and their role in neurodegeneration. Trends Pharmacol Sci 33(9):494–501PubMedCrossRefGoogle Scholar
  2. 2.
    Dali-Youcef N, Lagouge M, Froelich S, Koehl C, Schoonjans K, Auwerx J (2007) Sirtuins: the ‘magnificent seven’, function, metabolism and longevity. Ann Med 39(5):335–345PubMedCrossRefGoogle Scholar
  3. 3.
    Morselli E, Maiuri MC, Markaki M, Megalou E, Pasparaki A, Palikaras K, Criollo A, Galluzzi L et al (2010) Caloric restriction and resveratrol promote longevity through the Sirtuin-1-dependent induction of autophagy. Cell Death Dis 1:e10PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Frye RA (2000) Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem Biophys Res Commun 273(2):793–798PubMedCrossRefGoogle Scholar
  5. 5.
    Blander G, Guarente L (2004) The Sir2 family of protein deacetylases. Annu Rev Biochem 73:417–435PubMedCrossRefGoogle Scholar
  6. 6.
    Paraíso AF, Mendes KL, Santos SH (2013) Brain activation of SIRT1: role in neuropathology. Mol Neurobiol 48(3):681–689PubMedCrossRefGoogle Scholar
  7. 7.
    Barber MF, Michishita-Kioi E, Xi Y, Tasselli L, Kioi M, Moqtaderi Z, Tennen RI, Paredes S et al (2012) SIRT7 links H3K18 deacetylation to maintenance of oncogenic transformation. Nature 487(7405):114–118PubMedPubMedCentralGoogle Scholar
  8. 8.
    Vaquero A, Scher M, Lee D, Erdjument-Bromage H, Tempst P, Reinberg D (2004) Human SirT1 Interacts with Histone H1 and Promotes Formation of Facultative Heterochromatin. Mol Cell 16(1):93–105PubMedCrossRefGoogle Scholar
  9. 9.
    Kwon HS, Ott M (2008) The ups and downs of SIRT1. Trends Biochem Sci 33(11):517–525PubMedCrossRefGoogle Scholar
  10. 10.
    Harting K, Knöll B (2010) SIRT2-mediated protein deacetylation: an emerging key regulator in brain physiology and pathology. Eur J Cell Biol 89(2–3):262–269PubMedCrossRefGoogle Scholar
  11. 11.
    Michan S, Sinclair D (2007) Sirtuins in mammals: insights into their biological function. Biochem J 404(1):1–13PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Haigis MC, Sinclair DA (2010) Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol 5:253–295PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Guo W, Qian L, Zhang J, Zhang W, Morrison A, Hayes P, Wilson S, Chen T et al (2011) Sirt1 overexpression in neurons promotes neurite outgrowth and cell survival through inhibition of the mTOR signaling. J Neurosci Res 89(11):1723–1736PubMedCrossRefGoogle Scholar
  14. 14.
    Saharan S, Jhaveri DJ, Bartlett PF (2013) SIRT1 regulates the neurogenic potential of neural precursors in the adult subventricular zone and hippocampus. J Neurosci Res 91(5):642–659PubMedCrossRefGoogle Scholar
  15. 15.
    Lee OH, Kim J, Kim JM, Lee H, Kim EH, Bae SK, Choi Y, Nam HS et al (2013) Decreased expression of sirtuin 6 is associated with release of high mobility group box-1 after cerebral ischemia. Biochem Biophys Res Commun 438(2):388–394PubMedCrossRefGoogle Scholar
  16. 16.
    Suzuki K, Koike T (2007) Resveratrol abolishes resistance to axonal degeneration in slow Wallerian degeneration (WldS) mice: activation of SIRT2, an NAD-dependent tubulin deacetylase. Biochem Biophys Res Commun 359(3):665–671PubMedCrossRefGoogle Scholar
  17. 17.
    Donmez G, Outeiro TF (2013) SIRT1 and SIRT2: emerging targets in neurodegeneration. EMBO Mol Med 5(3):344–352PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Kim SH, Lu HF, Alano CC (2011) Neuronal Sirt3 Protects against Excitotoxic Injury in Mouse Cortical Neuron Culture. PLoS One 6(3):e14731PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Sakamoto J, Miura T, Shimamoto K, Horio Y (2004) Predominant expression of Sir2α, an NAD-dependent histone deacetylase, in the embryonic mouse heart and brain. FEBS Lett 556(1–3):281–286PubMedCrossRefGoogle Scholar
  20. 20.
    Ramadori G, Lee CE, Bookout AL, Lee S, Williams KW, Anderson J, Elmquist JK, Coppari R (2008) Brain SIRT1: anatomical distribution and regulation by energy availability. J Neurosci 28(40):9989–9996PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Satoh A, Brace CS, Ben-Josef G, West T, Wozniak DF, Holtzman DM, Herzog ED, Imai S (2010) SIRT1 promotes the central adaptive response to diet restriction through activation of the dorsomedial and lateralnuclei of the hypothalamus. J Neurosci 30(30):10220–10232PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Prozorovski T, Schulze-Topphoff U, Glumm R, Baumgart J, Schröter F, Ninnemann O, Siegert E, Bendix I et al (2008) Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat Cell Biol 10(4):385–394PubMedCrossRefGoogle Scholar
  23. 23.
    Revollo JR, Li X (2013) The ways and means that fine tune Sirt1 activity. Trends Biochem Sci 38(3):160–167PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Luo XY, Qu SL, Tang ZH, Zhang Y, Liu MH, Peng J, Tang H, Yu KL et al (2014) SIRT1 in cardiovascular aging. Clin Chim Acta 437:106–114PubMedCrossRefGoogle Scholar
  25. 25.
    Wang Y, Xu C, Liang Y, Vanhoutte PM (2012) SIRT1 in metabolic syndrome: where to target matters. Pharmacol Ther 136(3):305–318PubMedCrossRefGoogle Scholar
  26. 26.
    Peled T, Shoham H, Aschengrau D, Yackoubov D, Frei G, Rosenheimer GN, Lerrer B, Cohen HY et al (2012) Nicotinamide, a SIRT1 inhibitor, inhibits differentiation and facilitates expansion of hematopoietic progenitor cells with enhanced bone marrow homing and engraftment. Exp Hematol 40(4):342–355PubMedCrossRefGoogle Scholar
  27. 27.
    Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE et al (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303(5666):2011–2015PubMedCrossRefGoogle Scholar
  28. 28.
    Kim EJ, Kho JH, Kang MR, Um SJ (2007) Active regulator of SIRT1 cooperates with SIRT1 and facilitates suppression of p53 activity. Mol Cell 28(2):277–290PubMedCrossRefGoogle Scholar
  29. 29.
    Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW (2004) Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 23(12):2369–2380PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Seo JS, Moon MH, Jeong JK, Seol JW, Lee YJ, Park BH, Park SY (2012) SIRT1, a histone deacetylase, regulates prion protein-induced neuronal cell death. Neurobiol Aging 33(6):1110–1120PubMedCrossRefGoogle Scholar
  31. 31.
    Motta MC, Divecha N, Lemieux M, Kamel C, Chen D, Gu W, Bultsma Y, McBurney M et al (2004) Mammalian SIRT1 represses forkhead transcription factors. Cell 116(4):551–563PubMedCrossRefGoogle Scholar
  32. 32.
    Fusco S, Maulucci G, Pani G (2012) Sirt1: def-eating senescence? Cell Cycle 11(22):4135–4146PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Yamakuchi M (2012) MicroRNA Regulation of SIRT1. Front Physiol 3:68PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Saunders LR, Sharma AD, Tawney J, Nakagawa M, Okita K, Yamanaka S, Willenbring H, Verdin E (2010) miRNAs regulate SIRT1 expression during mouse embryonic stem cell differentiation and in adult mouse tissues. Aging (Albany NY) 2(7):415–431Google Scholar
  35. 35.
    Guo X, Williams JG, Schug TT, Li X (2010) DYRK1A and DYRK3 promote cell survival through phosphorylation and activation of SIRT1. J Biol Chem 285(17):13223–13232PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Liu X, Wang D, Zhao Y, Tu B, Zheng Z, Wang L, Wang H, Gu W et al (2011) Methyltransferase Set7/9 regulates p53 activity by interacting with Sirtuin1 (SIRT1). Proc Natl Acad Sci U S A 108(5):1925–1930PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Yang Y, Fu W, Chen J, Olashaw N, Zhang X, Nicosia SV, Bhalla K, Bai W (2007) SIRT1 sumoylation regulates its deacetylase activity and cellular response to genotoxic stress. Nat Cell Biol 9(11):1253–1262PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Kornberg MD, Sen N, Hara MR, Juluri KR, Nguyen JV, Snowman AM, Law L, Hester LD et al (2010) GAPDH mediates nitrosylation of nuclear proteins. Nat Cell Biol 12(11):1094–1100PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Lin Z, Yang H, Kong Q, Li J, Lee SM, Gao B, Dong H, Wei J et al (2012) USP22 antagonizes p53 transcriptional activation by deubiquitinating Sirt1 to suppress cell apoptosis and is required for mouse embryonic development. Mol Cell 46(4):484–494PubMedCrossRefGoogle Scholar
  40. 40.
    Hubbard BP, Sinclair DA (2014) Small molecule SIRT1 activators for the treatment of aging and age-related diseases. Trends Pharmacol Sci 35(3):146–154PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Jiang M, Wang J, Fu J, Du L, Jeong H, West T, Xiang L, Peng Q et al (2011) Neuroprotective role of Sirt1 in mammalian models of Huntington’s disease through activation of multiple Sirt1 targets. Nat Med 18(1):153–158PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Milne JC, Denu JM (2008) The Sirtuin family: therapeutic targets to treat diseases of aging. Curr Opin Chem Biol 12(1):11–17PubMedCrossRefGoogle Scholar
  43. 43.
    Borra MT, Smith BC, Denu JM (2005) Mechanism of human SIRT1 activation by resveratrol. J Biol Chem 280(17):17187–17195PubMedCrossRefGoogle Scholar
  44. 44.
    Milne JC, Lambert PD, Schenk S, Carney DP, Smith JJ, Gagne DJ, Jin L, Boss O et al (2007) Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450(7170):712–716PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Avalos JL, Bever KM, Wolberger C (2005) Mechanism of Sirtuin Inhibition by Nicotinamide:Altering the NAD+Cosubstrate Specificity of a Sir2 Enzyme. Mol Cell 17(6):855–868PubMedCrossRefGoogle Scholar
  46. 46.
    Gey C, Kyrylenko S, Hennig L, Nguyen LH, Buttner A, Pham HD, Giannis A (2007) Phloroglucinol derivatives guttiferone G, aristoforin, and hyperforin: inhibitors of human sirtuins SIRT1 and SIRT2. Angew Chem Int Ed Engl 46(27):5219–5222PubMedCrossRefGoogle Scholar
  47. 47.
    Oh WK, Cho KB, Hien TT, Kim TH, Kim HS, Dao TT, Han HK, Kwon SM et al (2010) Amurensin G, a potent natural SIRT1 inhibitor, rescues doxorubicin responsiveness via down-regulation of multidrug resistance 1. Mol Pharmacol 78(5):855–864PubMedCrossRefGoogle Scholar
  48. 48.
    Medda F, Russell RJ, Higgins M, McCarthy AR, Campbell J, Slawin AM, Lane DP, Lain S et al (2009) Novel cambinol analogs as sirtuin inhibitors: synthesis, biological evaluation, and rationalization of activity. J Med Chem 52(9):2673–2682PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Rotili D, Tarantino D, Carafa V, Lara E, Meade S, Botta G, Nebbioso A, Schemies J et al (2010) Identification of Tri- and Tetracyclic Pyrimidinediones as Sirtuin Inhibitors. ChemMedChem 5(5):674–677PubMedCrossRefGoogle Scholar
  50. 50.
    Solomon JM, Pasupuleti R, Xu L, McDonagh T, Curtis R, DiStefano PS, Huber LJ (2006) Inhibition of SIRT1 Catalytic Activity Increases p53 Acetylation but Does Not Alter Cell Survival following DNA Damage. Mol Cell Biol 26(1):28–38PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Arrowsmith CH, Bountra C, Fish PV, Lee K, Schapira M (2012) Epigenetic protein families: a new frontier for drug discovery. Nat Rev Drug Discov 11(5):384–400PubMedCrossRefGoogle Scholar
  52. 52.
    Bishop AE, Buttery LD, Polak JM (2002) Embryonic stem cells. J Pathol 197(4):424–429PubMedCrossRefGoogle Scholar
  53. 53.
    Han MK, Song EK, Guo Y, Ou X, Mantel C, Broxmeyer HE (2008) SIRT1 regulates apoptosis and Nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization. Cell Stem Cell 2(3):241–251PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Zhang ZN, Chung SK, Xu Z, Xu Y (2014) Oct4 maintains the pluripotency of human embryonic stem cells by inactivating p53 through Sirt1-mediated deacetylation. Stem Cells 32(1):157–165PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Yoon DS, Choi Y, Jang Y, Lee M, Choi WJ, Kim SH, Lee JW (2014) SIRT1 Directly Regulates SOX2 to Maintain Self-Renewal and Multipotency in Bone Marrow-Derived Mesenchymal Stem Cells. Stem Cells 32(12):3219–3231PubMedCrossRefGoogle Scholar
  56. 56.
    Lhee SJ, Song EK, Kim YR, Han MK (2012) SIRT1 Inhibits p53 but not NF-κB Transcriptional Activity during Differentiation of Mouse Embryonic Stem Cells into Embryoid Bodies. Int J Stem Cells 5(2):125–129Google Scholar
  57. 57.
    Sussman RT, Stanek TJ, Esteso P, Gearhart JD, Knudsen KE, McMahon SB (2013) The epigenetic modifier ubiquitin-specific protease 22 (USP22) regulates embryonic stem cell differentiation via transcriptional repression of sex-determining region Y-box 2 (SOX2). J Biol Chem 288(33):24234–24246PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Dvash T, Benvenisty N (2004) Human embryonic stem cells as a model for early human development. Best Pract Res Clin Obstet Gynaecol 18(6):929–940PubMedCrossRefGoogle Scholar
  59. 59.
    Calvanese V, Lara E, Suárez-Alvarez B, Abu Dawud R, Vázquez-Chantada M, Martinez-Chantar ML, Embade N, López-Nieva P et al (2010) Sirtuin 1 regulation of developmental genes during differentiation of stem cells. Proc Natl Acad Sci U S A 107(31):13736–13741Google Scholar
  60. 60.
    Bain G, Kitchens D, Yao M, Huettner JE, Gottlieb DI (1995) Embryonic stem cells express neuronal properties in vitro. Dev Biol 168(2):342–357PubMedCrossRefGoogle Scholar
  61. 61.
    Bain G, Ray WJ, Yao M, Gottlieb DI (1996) Retinoic Acid Promotes Neural and Represses Mesodermal Gene Expression in Mouse Embryonic Stem Cells in Culture. Biochem Biophys Res Commun 223(3):691–694PubMedCrossRefGoogle Scholar
  62. 62.
    Tang S, Huang G, Fan W, Chen Y, Ward JM, Xu X, Xu Q, Kang A et al (2014) SIRT1-Mediated Deacetylation of CRABPII Regulates Cellular Retinoic Acid Signaling and Modulates Embryonic Stem Cell Differentiation. Mol Cell 55(6):843–855PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Parsons XH (2012) MicroRNA Profiling Reveals Distinct Mechanisms Governing Cardiac and Neural Lineage-Specification of Pluripotent Human Embryonic Stem Cells. J Stem Cell Res Ther 2(3):124PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Lee YL, Peng Q, Fong SW, Chen AC, Lee KF, Ng EH, Nagy A, Yeung WS (2012) Sirtuin 1 facilitates generation of induced pluripotent stem cells from mouse embryonic fibroblasts through the miR-34a and p53 pathways. PLoS One 7(9):e45633PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Hu B, Guo Y, Chen C, Li Q, Niu X, Guo S, Zhang A, Wang Y et al (2014) Repression of SIRT1 promotes the differentiation of mouse induced pluripotent stem cells into neural stem cells. Cell Mol Neurobiol 34(6):905–912PubMedCrossRefGoogle Scholar
  66. 66.
    Kennea NL, Mehmet H (2002) Neural stem cells. J Pathol 197(4):536–550PubMedCrossRefGoogle Scholar
  67. 67.
    Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18(9):3206–3212Google Scholar
  68. 68.
    Kempermann G (2002) Regulation of adult hippocampal neurogenesis – implications for novel theories of major depression. Bipolar Disord 4(1):17–33PubMedCrossRefGoogle Scholar
  69. 69.
    Hisahara S, Chiba S, Matsumoto H, Tanno M, Yagi H, Shimohama S, Sato M, Horio Y (2008) Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation. Proc Natl Acad Sci U S A 105(40):15599–15604Google Scholar
  70. 70.
    Liu DJ, Hammer D, Komlos D, Chen KY, Firestein BL, Liu AY (2014) SIRT1 Knockdown Promotes Neural Differentiation and Attenuates the Heat Shock Response. J Cell Physiol 229(9):1224–1235PubMedCrossRefGoogle Scholar
  71. 71.
    Joe IS, Jeong SG, Cho GW (2015) Resveratrol-induced SIRT1 activation promotes neuronal differentiation of human bone marrow mesenchymal stem cells. Neurosci Lett 584:97–102PubMedCrossRefGoogle Scholar
  72. 72.
    Kageyama R, Shimojo H, Imayoshi I (2015) Dynamic expression and roles of Hes factors in neural development. Cell Tissue Res 359(1):125–133PubMedCrossRefGoogle Scholar
  73. 73.
    Kopan R, Ilagan MX (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137(2):216–233Google Scholar
  74. 74.
    Louvi A, Artavanis-Tsakonas S (2006) Notch signalling in vertebrate neural development. Nat Rev Neurosci 7(2):93–102PubMedCrossRefGoogle Scholar
  75. 75.
    Kageyama R, Ohtsuka T, Kobayashi T (2007) The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 134(7):1243–1251PubMedCrossRefGoogle Scholar
  76. 76.
    Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F (1995) Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev 9(24):3136–3148PubMedCrossRefGoogle Scholar
  77. 77.
    Tomita K, Ishibashi M, Nakahara K, Ang SL, Nakanishi S, Guillemot F, Kageyama R (1996) Mammalian hairy and Enhancer of Split Homolog 1 Regulates Differentiation of Retinal Neurons and Is Essential for Eye Morphogenesis. Neuron 16(4):723–734PubMedCrossRefGoogle Scholar
  78. 78.
    Cheng HL, Mostoslavsky R, Saito S, Manis JP, Gu Y, Patel P, Bronson R, Appella E et al (2003) Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc Natl Acad Sci U S A 100(19):10794–10799PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Ichi S, Boshnjaku V, Shen YW, Mania-Farnell B, Ahlgren S, Sapru S, Mansukhani N, McLone DG et al (2011) Role of Pax3 acetylation in the regulation of Hes1 and Neurog2. Mol Biol Cell 22(4):503–512PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Tiberi L, van den Ameele J, Dimidschstein J, Piccirilli J, Gall D, Herpoel A, Bilheu A, Bonnefont J et al (2012) BCL6 controls neurogenesis through Sirt1-dependent epigenetic repression of selective Notch targets. Nat Neurosci 15(12):1627–1635PubMedCrossRefGoogle Scholar
  81. 81.
    Tiberi L, Bonnefont J, van den Ameele J, Le Bon SD, Herpoel A, Bilheu A, Baron BW, Vanderhaeghen P (2014) A BCL6/BCOR/SIRT1 Complex Triggers Neurogenesis and Suppresses Medulloblastoma by Repressing Sonic Hedgehog Signaling. Cancer Cell 26(6):797–812PubMedCrossRefGoogle Scholar
  82. 82.
    Wang W, Osenbroch P, Skinnes R, Esbensen Y, Bjørås M, Eide L (2010) Mitochondrial DNA integrity is essential for mitochondrial maturation during differentiation of neural stem cells. Stem Cells 28(12):2195–2204PubMedCrossRefGoogle Scholar
  83. 83.
    Wang W, Esbensen Y, Kunke D, Suganthan R, Rachek L, Bjørås M, Eide L (2011) Mitochondrial DNA damage level determines neural stem cell differentiation fate. J Neurosci 31(26):9746–9751PubMedCrossRefGoogle Scholar
  84. 84.
    Santos DM, Santos MM, Moreira R, Solá S, Rodrigues CM (2013) Synthetic condensed 1,4-naphthoquinone derivative shifts neural stem cell differentiation by regulating redox state. Mol Neurobiol 47(1):313–324PubMedCrossRefGoogle Scholar
  85. 85.
    Sun G, Yu RT, Evans RM, Shi Y (2007) Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc Natl Acad Sci U S A 104(39):15282–15287PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Iwahara N, Hisahara S, Hayashi T, Horio Y (2009) Transcriptional activation of NAD+-dependent protein deacetylase SIRT1 by nuclear receptor TLX. Biochem Biophys Res Commun 386(4):671–675PubMedCrossRefGoogle Scholar
  87. 87.
    Yu RT, Chiang MY, Tanabe T, Kobayashi M, Yasuda K, Evans RM, Umesono K (2000) The orphan nuclear receptor Tlx regulates Pax2 and is essential for vision. Proc Natl Acad Sci U S A 97(6):2621–2625PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Horn V, Minucci S, Ogryzko VV, Adamson ED, Howard BH, Levin AA, Ozato K (1996) RAR and RXR selective ligands cooperatively induce apoptosis and neuronal differentiation in P19 embryonal carcinoma cells. FASEB J 10(9):1071–1077PubMedGoogle Scholar
  89. 89.
    Zhang C, Dowd DR, Staal A, Gu C, Lian JB, van Wijnen AJ, Stein GS, MacDonald PN (2003) Nuclear Coactivator-62 kDa/Ski-interacting Protein Is a Nuclear Matrix-associated Coactivator That May Couple Vitamin D Receptor-mediated Transcription and RNA Splicing. J Biol Chem 278(37):35325–35336PubMedCrossRefGoogle Scholar
  90. 90.
    Kang MR, Lee SW, Um E, Kang HT, Hwang ES, Kim EJ, Um SJ (2010) Reciprocal roles of SIRT1 and SKIP in the regulation of RAR activity: implication in the retinoic acid-induced neuronal differentiation of P19 cells. Nucleic Acids Res 38(3):822–831PubMedCrossRefGoogle Scholar
  91. 91.
    Yu S, Levi L, Siegel R, Noy N (2012) Retinoic acid induces neurogenesis by activating both retinoic acid receptors (RARs) and peroxisome proliferator-activated receptor beta/delta (PPARbeta/delta). J Biol Chem 287(50):42195–42205PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Xie Z, Kasschau KD, Carrington JC (2003) Negative Feedback Regulation of Dicer-Like1in Arabidopsis by microRNA-Guided mRNA Degradation. Curr Biol 13(9):784–789PubMedCrossRefGoogle Scholar
  93. 93.
    Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS et al (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433(7027):769–773PubMedCrossRefGoogle Scholar
  94. 94.
    Aranha MM, Santos DM, Sola S, Steer CJ, Rodrigues CM (2011) miR-34a regulates mouse neural stem cell differentiation. PLoS One 6(8):e21396PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Delaloy C, Liu L, Lee JA, Su H, Shen F, Yang GY, Young WL, Ivey KN et al (2010) MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 6(4):323–335PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Aranha MM, Solá S, Low WC, Steer CJ, Rodrigues CM (2009) Caspases and p53 Modulate FOXO3A/Id1 Signaling During Mouse Neural Stem Cell Differentiation. J Cell Biochem 107(4):748–758PubMedCrossRefGoogle Scholar
  97. 97.
    Meletis K, Wirta V, Hede SM, Nistér M, Lundeberg J, Frisen J (2006) p53 suppresses the self-renewal of adult neural stem cells. Development 133(2):363–369PubMedCrossRefGoogle Scholar
  98. 98.
    Armesilla-Diaz A, Bragado P, Del Valle I, Cuevas E, Lazaro I, Martin C, Cigudosa JC, Silva A (2009) p53 regulates the self-renewal and differentiation of neural precursors. Neuroscience 158(4):1378–1389PubMedCrossRefGoogle Scholar
  99. 99.
    Lee JS, Park JR, Kwon OS, Lee TH, Nakano I, Miyoshi H, Chun KH, Park MJ et al (2015) SIRT1 is required for oncogenic transformation of neural stem cells and for the survival of “cancer cells with neural stemness” in a p53-dependent manner. Neuro Oncol 17(1):95–106PubMedCrossRefGoogle Scholar
  100. 100.
    Pistritto G, Papaleo V, Sanchez P, Ceci C, Barbaccia ML (2012) Divergent modulation of neuronal differentiation by caspase-2 and -9. PLoS One 7(5):e36002PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Shin SDS, Stice SL (2005) Human Motor Neuron Differentiation from Human Embryonic Stem Cells. Stem Cells Dev 14(3):266–269PubMedCrossRefGoogle Scholar
  102. 102.
    Li XJ, Hu BY, Jones SA, Zhang YS, Lavaute T, Du ZW, Zhang SC (2008) Directed differentiation of ventral spinal progenitors and motor neurons from human embryonic stem cells by small molecules. Stem Cells 26(4):886–893PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Zhang Y, Wang J, Chen G, Fan D, Deng M (2011) Inhibition of Sirt1 promotes neural progenitors toward motoneuron differentiation from human embryonic stem cells. Biochem Biophys Res Commun 404(2):610–614PubMedCrossRefGoogle Scholar
  104. 104.
    Jacobs FM, van Erp S, van der Linden AJ, von Oerthel L, Burbach JP, Smidt MP (2009) Pitx3 potentiates Nurr1 in dopamine neuron terminal differentiation through release of SMRT-mediated repression. Development 136(4):531–540PubMedCrossRefGoogle Scholar
  105. 105.
    Kim TE, Seo JS, Yang JW, Kim MW, Kausar R, Joe E, Kim BY, Lee MA (2013) Nurr1 Represses Tyrosine Hydroxylase Expression via SIRT1 in Human Neural Stem Cells. PLoS One 8(8):e71469PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Kim MJ, Ahn K, Park SH, Kang HJ, Jang BG, Oh SJ, Oh SM, Jeong YJ et al (2009) SIRT1 regulates tyrosine hydroxylase expression and differentiation of neuroblastoma cells via FOXO3a. FEBS Lett 583(7):1183–1188PubMedCrossRefGoogle Scholar
  107. 107.
    Beuckmann CT, Yanagisawa M (2002) Orexins: from neuropeptides to energy homeostasis and sleep/wake regulation. J Mol Med (Berl) 80(6):329–342CrossRefGoogle Scholar
  108. 108.
    Hayakawa K, Hirosawa M, Tabei Y, Arai D, Tanaka S, Murakami N, Yagi S, Shiota K (2013) Epigenetic switching by the metabolism-sensing factors in the generation of orexin neurons from mouse embryonic stem cells. J Biol Chem 288(24):17099–17110PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Barbieri AM, Broccoli V, Bovolenta P, Alfano G, Marchitiello A, Mocchetti C, Crippa L, Bulfone A et al (2002) Vax2 inactivation in mouse determines alteration of the eye dorsal-ventral axis, misrouting of the optic fibres and eye coloboma. Development 129(3):805–813PubMedGoogle Scholar
  110. 110.
    Hasegawa K, Yoshikawa K (2008) Necdin regulates p53 acetylation via Sirtuin1 to modulate DNA damage response in cortical neurons. J Neurosci 28(35):8772–8784PubMedCrossRefGoogle Scholar
  111. 111.
    Hayakawa N, Shiozaki M, Shibata M, Koike M, Uchiyama Y, Matsuura N, Gotow T (2013) Resveratrol affects undifferentiated and differentiated PC12 cells differently, particularly with respect to possible differences in mitochondrial and autophagic functions. Eur J Cell Biol 92(1):30–43PubMedCrossRefGoogle Scholar
  112. 112.
    Fujino K, Ogura Y, Sato K, Nedachi T (2013) Potential neuroprotective effects of SIRT1 induced by glucose deprivation in PC12 cells. Neurosci Lett 557:148–153PubMedCrossRefGoogle Scholar
  113. 113.
    Uittenbogaard M, Baxter KK, Chiaramello A (2010) The neurogenic basic helix-loop-helix transcription factor NeuroD6 confers tolerance to oxidative stress by triggering an antioxidant response and sustaining the mitochondrial biomass. ASN Neuro 2(2):e00034PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Sansone L, Reali V, Pellegrini L, Villanova L, Aventaggiato M, Marfe G, Rosa R, Nebbioso M et al (2013) SIRT1 silencing confers neuroprotection through IGF-1 pathway activation. J Cell Physiol 228(8):1754–1761PubMedCrossRefGoogle Scholar
  115. 115.
    Taupin P, Gage FH (2002) Adult neurogenesis and neural stem cells of the central nervous system in mammals. J Neurosci Res 69(6):745–749PubMedCrossRefGoogle Scholar
  116. 116.
    Zakhary SM, Ayubcha D, Dileo JN, Jose R, Leheste JR, Horowitz JM, Torres G (2010) Distribution analysis of deacetylase SIRT1 in rodent and human nervous systems. Anat Rec (Hoboken) 293(6):1024–1032CrossRefGoogle Scholar
  117. 117.
    Ma CY, Yao MJ, Zhai QW, Jiao JW, Yuan XB, Poo MM (2014) SIRT1 suppresses self-renewal of adult hippocampal neural stem cells. Development 141(24):4697–4709PubMedCrossRefGoogle Scholar
  118. 118.
    Schmidt-Strassburger U, Schips TG, Maier HJ, Kloiber K, Mannella F, Braunstein KE, Holzmann K, Ushmorov A et al (2012) Expression of constitutively active FoxO3 in murine forebrain leads to a loss of neural progenitors. FASEB J 26(12):4990–5001PubMedCrossRefGoogle Scholar
  119. 119.
    Rafalski VA, Ho PP, Brett JO, Ucar D, Dugas JC, Pollina EA, Chow LM, Ibrahim A et al (2013) Expansion of oligodendrocyte progenitor cells following SIRT1 inactivation in the adult brain. Nat Cell Biol 15(6):614–624PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Xiang Z, Krainc D (2013) Pharmacological upregulation of PGC1alpha in oligodendrocytes: implications for Huntington’s Disease. J Huntingtons Dis 2(1):101–105PubMedGoogle Scholar
  121. 121.
    Stettner M, Wolffram K, Mausberg AK, Albrecht P, Derksen A, Methner A, Dehmel T, Hartung HP et al (2013) Promoting myelination in an in vitro mouse model of the peripheral nervous system: the effect of wine ingredients. PLoS One 8(6):e66079PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Stein LR, Imai S (2014) Specific ablation of Nampt in adult neural stem cells recapitulates their functional defects during aging. EMBO J 33(12):1321–1340Google Scholar
  123. 123.
    Parsons XH (2012) An Engraftable Human Embryonic Stem Cell Neuronal Lineage-Specific Derivative Retains Embryonic Chromatin Plasticity for Scale-Up CNS Regeneration. J Regen Med Tissue Eng 1(1):3PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Parsons XH (2013) Embedding the Future of Regenerative Medicine into the Open Epigenomic Landscape of Pluripotent Human Embryonic Stem Cells. Annu Res Rev Biol 3(4):323–349PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Developmental Neuropsychology, School of PsychologyThird Military Medical UniversityChongqingChina
  2. 2.Southwest Eye Hospital, Southwest Hospital, Third Military Medical UniversityChongqingChina

Personalised recommendations