SIRT1 regulates the neurogenic potential of neural precursors in the adult subventricular zone and hippocampus

Journal of Neuroscience Research

Volumn 91, Issue 5, 2013, Pages 642-659

  Saharan, Sumiti ^a   Jhaveri, Dhanisha J ^a   Bartlett, Perry F ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Adult neurogenesis; Epigenetic; Neural precursor cells; Neuronal differentiation; Sirt1

Indexed keywords

RESVERATROL; SIRTUIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL MEMBRANE POTENTIAL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SUBVENTRICULAR ZONE;

ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CEREBRAL VENTRICLES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; KI-67 ANTIGEN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; NEUROPEPTIDES; RNA, SMALL INTERFERING; SIRTUIN 1; STEM CELL NICHE; STILBENES; TRANSFECTION; TUBULIN;

EID: 84874815449     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23199     Document Type: Article

References (64)

1. Agathocleous M, Iordanova I, Willardsen MI, Xue XY, Vetter ML, et al. 2009. A directional Wnt/beta-catenin-Sox2-proneural pathway regulates the transition from proliferation to differentiation in the Xenopus retina. Development 136: 3289-3299.
2. Anderson ML, Sisti HM, Curlik DM2nd, Shors TJ. 2010. Associative learning increases adult neurogenesis during a critical period. Eur J Neurosci 33: 175-181.
3. Balasubramaniyan V, Boddeke E, Bakels R, Kust B, Kooistra S, et al. 2006. Effects of histone deacetylation inhibition on neuronal differentiation of embryonic mouse neural stem cells. Neuroscience 143: 939-951.
4. Ballas N, Mandel G. 2005. The many faces of REST oversee epigenetic programming of neuronal genes. Curr Opin Neurobiol 15: 500-506.
5. Baur JA. 2009. Biochemical effects of SIRT1 activators. Biochim Biophys Acta 1804: 1626-1634.
6. Borra MT, Smith BC, Denu JM. 2005. Mechanism of human SIRT1 activation by Resveratrol. J Biol Chem 280: 17187-17195.
7. Briscoe J. 2009. Making a grade: Sonic Hedgehog signalling and the control of neural cell fate. EMBO J 28: 457-465.
8. Bull ND, Bartlett PF. 2005. The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J Neurosci 25: 10815-10821.
9. Calvanese V, Lara E, Suarez-Alvarez B, Abu Dawud R, Vazquez-Chantada M, et al. 2010. Sirtuin 1 regulation of developmental genes during differentiation of stem cells. Proc Natl Acad Sci U S A 107: 13736-13741.
10. Cohen HY, Miller C, Bitterman KJ, Wall NR, Hekking B, et al. 2004. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 305: 390-392.
11. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, et al. 1998. A third-generation lentivirus vector with a conditional packaging system. J Virol 72: 8463-8471.
12. Follenzi A, Sabatino G, Lombardo A, Boccaccio C, Naldini L. 2002. Efficient gene delivery and targeted expression to hepatocytes in vivo by improved lentiviral vectors. Hum Gene Ther 13: 243-260.
13. Fremont L. 2000. Biological effects of Resveratrol. Life Sci 66: 663-673.
14. Fulco M, Cen Y, Zhao P, Hoffman EP, McBurney MW, et al. 2008. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell 14: 661-673.
15. Gao J, Wang W-Y, Mao Y-W, Gräff J, Guan J-S, et al. 2010. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466: 1105-1109.
16. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2: 260-265.
17. Haigis MC, Guarente LP. 2006. Mammalian sirtuins-emerging roles in physiology, aging, and calorie restriction. Genes Dev 20: 2913-2921.
18. Han MK, Song EK, Guo Y, Ou X, Mantel C, et al. 2008. SIRT1 regulates apoptosis and Nanog expression in mouse embryonic stem cells by controlling p53 subcellular localization. Cell Stem Cell 2: 241-251.
19. Hirabayashi Y, Gotoh Y. 2010. Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 11: 377-388.
20. Hisahara S, Chiba S, Matsumoto H, Tanno M, Yagi H, et al. 2008. Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation. Proc Natl Acad Sci U S A 105: 15599-15604.
21. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, et al. 2003. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425: 191-196.
22. Hsieh J, Eisch AJ. 2010. Epigenetics, hippocampal neurogenesis, and neuropsychiatric disorders: unraveling the genome to understand the mind. Neurobiol Dis 39: 73-84.
23. Hsieh J, Gage FH. 2004. Epigenetic control of neural stem cell fate. Curr Opin Genet Dev 14: 461-469.
24. Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage FH. 2004. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A 101: 16659-16664.
25. Jennemann R, Sandhoff R, Wang S, Kiss E, Gretz N, et al. 2005. Cell-specific deletion of glucosylceramide synthase in brain leads to severe neural defects after birth. Proc Natl Acad Sci U S A 102: 12459-12464.
26. Juliandi B, Abematsu M, Nakashima K. 2010. Chromatin remodeling in neural stem cell differentiation. Curr Opin Neurobiol 20: 408-415.
27. Kelly GS. 2011. A review of the sirtuin system, its clinical implications, and the potential role of dietary activators like Resveratrol: part 2. Altern Med Rev 15: 313-328.
28. Kim HJ, Leeds P, Chuang DM. 2009. The HDAC inhibitor, sodium butyrate, stimulates neurogenesis in the ischemic brain. J Neurochem 110: 1226-1240.
29. Kobayashi T, Mizuno H, Imayoshi I, Furusawa C, Shirahige K, et al. 2009. The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Genes Dev 23: 1870-1875.
30. Kohyama J, Kojima T, Takatsuka E, Yamashita T, Namiki J, et al. 2008. Epigenetic regulation of neural cell differentiation plasticity in the adult mammalian brain. Proc Natl Acad Sci U S A 105: 18012-18017.
31. Kulkarni VA, Jha S, Vaidya VA. 2002. Depletion of norepinephrine decreases the proliferation, but does not influence the survival and differentiation, of granule cell progenitors in the adult rat hippocampus. Eur J Neurosci 16: 2008-2012.
32. + in the deacetylase activity of the SIR2-like proteins. Biochem Biophys Res Commun 278: 685-690.
33. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, et al. 2010. Proliferative 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.
34. Lemaire V, Koehl M, Le Moal M, Abrous DN. 2000. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci U S A 97: 11032-11037.
35. Li H, Rajendran GK, Liu N, Ware C, Rubin BP, et al. 2007. SirT1 modulates the estrogen-insulin-like growth factor-1 signaling for postnatal development of mammary gland in mice. Breast Cancer Res 9: R1.
36. Lyssiotis CA, Walker J, Wu C, Kondo T, Schultz PG, et al. 2007. Inhibition of histone deacetylase activity induces developmental plasticity in oligodendrocyte precursor cells. Proc Natl Acad Sci U S A 104: 14982-14987.
37. Matsumori Y, Hong SM, Fan Y, Kayama T, Hsu CY, et al. 2006. Enriched environment and spatial learning enhance hippocampal neurogenesis and salvages ischemic penumbra after focal cerebral ischemia. Neurobiol Dis 22: 187-198.
38. Merson TD, Dixon MP, Collin C, Rietze RL, Bartlett PF, et al. 2006. The transcriptional coactivator Querkopf controls adult neurogenesis. J Neurosci 26: 11359-11370.
39. Michan S, Li Y, Chou MM-H, Parrella E, Ge H, et al. 2010. SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci 30: 9695-9707.
40. Nakamura Y, Sakakibara S, Miyata T, Ogawa M, Shimazaki T, et al. 2000. The bHLH gene hes1 as a repressor of the neuronal commitment of CNS stem cells. J Neurosci 20: 283-293.
41. Ogawa T, Wakai C, Saito T, Murayama A, Mimura Y, et al. 2011. Distribution of the longevity gene product, SIRT1, in developing mouse organs. Congenit Anom 51: 70-79.
42. Ohtsuka T, Ishibashi M, Gradwohl G, Nakanishi S, Guillemot F, et al. 1999. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J 18: 2196-2207.
43. Pallas M, Casadesus G, Smith MA, Coto-Montes A, Pelegri C, et al. 2009. Resveratrol and neurodegenerative diseases: activation of SIRT1 as the potential pathway toward neuroprotection. Curr Neurovasc Res 6: 70-81.
44. Pervaiz S, Holme AL. 2009. Resveratrol: its biologic targets and functional activity. Antiox Redox Signal 11: 2851-2897.
45. Prozorovski T, Schulze-Topphoff U, Glumm R, Baumgart J, Schroter F, et al. 2008. Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat Cell Biol 10: 385-394.
46. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
47. Reynolds BA, Weiss S. 1996. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175: 1-13.
48. Sakamoto J, Miura T, Shimamoto K, Horio Y. 2004. Predominant expression of Sir2alpha, an NAD-dependent histone deacetylase, in the embryonic mouse heart and brain. FEBS Lett 556: 281-286.
49. Sasaki T, Maier B, Bartke A, Scrable H. 2006. Progressive loss of SIRT1 with cell cycle withdrawal. Aging Cell 5: 413-422.
50. Schneider JW, Gao Z, Li S, Farooqi M, Tang TS, et al. 2008. Small-molecule activation of neuronal cell fate. Nat Chem Biol 4: 408-410.
51. Siebzehnrubl FA, Buslei R, Eyupoglu IY, Seufert S, Hahnen E, et al. 2007. Histone deacetylase inhibitors increase neuronal differentiation in adult forebrain precursor cells. Exp Brain Res 176: 672-678.
52. Stump G, Durrer A, Klein AL, Lutolf S, Suter U, et al. 2002. Notch1 and its ligands Delta-like and Jagged are expressed and active in distinct cell populations in the postnatal mouse brain. Mech Dev 114: 153-159.
53. Sui Y, Zhang Z, Guo Y, Sun Y, Zhang X, et al. 2009. The function of Notch1 signaling was increased in parallel with neurogenesis in rat hippocampus after chronic fluoxetine administration. Biol Pharm Bull 32: 1776-1782.
54. Takata T, Ishikawa F. 2003. Human Sir2-related protein SIRT1 associates with the bHLH repressors HES1 and HEY2 and is involved in HES1- and HEY2-mediated transcriptional repression. Biochem Biophys Res Commun 301: 250-257.
55. Tiscornia G, Singer O, Verma IM. 2006. Design and cloning of lentiviral vectors expressing small interfering RNAs. Nat Protoc 1: 234-240.
56. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, et al. 1999. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23: 99-103.
57. van Praag H, Christie BR, Sejnowski TJ, Gage FH. 1999. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96: 13427-13431.
58. Walker TL, White A, Black DM, Wallace RH, Sah P, et al. 2008. Latent stem and progenitor cells in the hippocampus are activated by neural excitation. J Neurosci 28: 5240-5247.
59. Wallenborg K, Vlachos P, Eriksson S, Huijbregts L, Arnér ESJ, et al. 2009. Red wine triggers cell death and thioredoxin reductase inhibition: effects beyond Resveratrol and SIRT1. Exp Cell Res 315: 1360-1371.
60. Wang X, Mao X, Xie L, Greenberg DA, Jin K. 2009. Involvement of Notch1 signaling in neurogenesis in the subventricular zone of normal and ischemic rat brain in vivo. J Cereb Blood Flow Metab 29: 1644-1654.
61. Wen S, Li H, Liu J. 2009. Epigenetic background of neuronal fate determination. Prog Neurobiol 87: 98-117.
62. Wexler EM, Paucer A, Kornblum HI, Palmer TD, Geschwind DH. 2009. Endogenous Wnt signaling maintains neural progenitor cell potency. Stem Cells 27: 1130-1141.
63. Yu IT, Park JY, Kim SH, Lee JS, Kim YS, et al. 2009. Valproic acid promotes neuronal differentiation by induction of proneural factors in association with H4 acetylation. Neuropharmacology 56: 473-480.
64. Zhang C, Zhang Z, Shu H, Liu S, Song Y, et al. 2009. The modulatory effects of bHLH transcription factors with the Wnt/beta-catenin pathway on differentiation of neural progenitor cells derived from neonatal mouse anterior subventricular zone. Brain Res 1315: 1-10.