Cross talk between microRNA and epigenetic regulation in adult neurogenesis

Journal of Cell Biology

Volumn 189, Issue 1, 2010, Pages 127-141

  Szulwach, Keith E ^a   Li, Xuekun ^b   Smrt, Richard D ^b   Li, Yujing ^a   Luo, Yuping ^b   Lin, Li ^a   Santistevan, Nicholas J ^b   Li, Wendi ^a   Zhao, Xinyu ^b   Jin, Peng ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; METHYL CPG BINDING PROTEIN 2; MICRORNA; PROTEIN; RETROVIRUS VECTOR; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN; CONTROLLED STUDY; EPIGENETICS; GENE CONTROL; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; LENTIVIRINAE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; CHROMATIN; EPIGENESIS, GENETIC; HISTONE-LYSINE N-METHYLTRANSFERASE; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, TRANSGENIC; MICRORNAS; NEUROGENESIS; REPRESSOR PROTEINS; STEM CELLS;

EID: 77950565107     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200908151     Document Type: Article

References (69)

1. Abel, T., and R.S. Zukin. 2008. Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders. Curr. Opin. Pharmacol. 8: 57-64. doi:10.1016/j.coph.2007.12.002
2. Amir, R.E., I.B. Van den Veyver, M. Wan, C.Q. Tran, U. Francke, and H.Y. Zoghbi. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23: 185-188. doi:10.1038/13810
3. Avilion, A.A., S.K. Nicolis, L.H. Pevny, L. Perez, N. Vivian, and R. Lovell-Badge. 2003. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17: 126-140. doi:10.1101/gad.224503
4. Ballas, N., D.T. Lioy, C. Grunseich, and G. Mandel. 2009. Non-cell autonomous influence of MeCP2-deficient glia on neuronal dendritic morphology. Nat. Neurosci. 12: 311-317. doi:10.1038/nn.2275
5. Barbarotto, E., T.D. Schmittgen, and G.A. Calin. 2008. MicroRNAs and cancer: profile, profile, profile. Int. J. Cancer. 122: 969-977. doi:10.1002/ijc.23343
6. Barkho, B.Z., H. Song, J.B. Aimone, R.D. Smrt, T. Kuwabara, K. Nakashima, F.H. Gage, and X. Zhao. 2006. Identification of astrocyte-expressed factors that modulate neural stem/progenitor cell differentiation. Stem Cells Dev. 15: 407-421. doi:10.1089/scd.2006.15.407
7. Bartel, D.P. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 116: 281-297. doi:10.1016/S0092-8674(04)00045-5
8. Bernstein, E., S.Y. Kim, M.A. Carmell, E.P. Murchison, H. Alcorn, M.Z. Li, A.A. Mills, S.J. Elledge, K.V. Anderson, and G.J. Hannon. 2003. Dicer is essential for mouse development. Nat. Genet. 35: 215-217. doi:10.1038/ng1253
9. Bernstein, B.E., A. Meissner, and E.S. Lander. 2007. The mammalian epigenome. Cell. 128: 669-681. doi:10.1016/j.cell.2007.01.033
10. Bienvenu, T., and J. Chelly. 2006. Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat. Rev. Genet. 7: 415-426. doi: 10.1038/nrg1878 (Pubitemid 43780485)
11. Bird, A. 2002. DNA methylation patterns and epigenetic memory. Genes Dev. 16: 6-21. doi: 10.1101/gad.947102 (Pubitemid 34049633)
12. Boyer, L.A., T.I. Lee, M.F. Cole, S.E. Johnstone, S.S. Levine, J.P. Zucker, M.G. Guenther, R.M. Kumar, H.L. Murray, R.G. Jenner, et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell. 122: 947-956. doi: 10.1016/j.cell.2005.08.020 (Pubitemid 41345211)
13. Boyer, L.A., K. Plath, J. Zeitlinger, T. Brambrink, L.A. Medeiros, T.I. Lee, S.S. Levine, M. Wernig, A. Tajonar, M.K. Ray, et al. 2006. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature. 441: 349-353. doi: 10.1038/nature04733 (Pubitemid 44050199)
14. Bylund, M., E. Andersson, B.G. Novitch, and J. Muhr. 2003. Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat. Neurosci. 6: 1162-1168. doi:10.1038/nn1131 (Pubitemid 37346036)
15. Cao, R., and Y. Zhang. 2004. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr. Opin. Genet. Dev. 14: 155-164. doi:10.1016/j.gde.2004.02.001 (Pubitemid 38520143)
16. Carninci, P., T. Kasukawa, S. Katayama, J. Gough, M.C. Frith, N. Maeda, R. Oyama, T. Ravasi, B. Lenhard, C. Wells, et al. 2005. The transcriptional landscape of the mammalian genome. Science. 309: 1559-1563. doi:10.1126/science. 1112014
17. Chahrour, M., and H.Y. Zoghbi. 2007. The story of Rett syndrome: from clinic to neurobiology. Neuron. 56: 422-437. doi:10.1016/j.neuron.2007.10.001 (Pubitemid 350026269)
18. Chahrour, M., S.Y. Jung, C. Shaw, X. Zhou, S.T. Wong, J. Qin, and H.Y. Zoghbi. 2008. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science. 320: 1224-1229. doi: 10.1126/science.1153252 (Pubitemid 351929512)
19. Chen, R.Z., S. Akbarian, M. Tudor, and R. Jaenisch. 2001. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27: 327-331. doi: 10.1038/85906
20. Cheng, L.C., M. Tavazoie, and F. Doetsch. 2005. Stem cells: from epigenetics to microRNAs. Neuron. 46: 363-367. doi:10.1016/j.neuron.2005.04.027
21. Cheng, L.C., E. Pastrana, M. Tavazoie, and F. Doetsch. 2009. miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 12: 399-408. doi:10.1038/nn.2294
22. Coffee, B., F. Zhang, S.T. Warren, and D. Reines. 1999. Acetylated histones are associated with FMR1 in normal but not fragile X-syndrome cells. Nat. Genet. 22: 98-101. doi:10.1038/8807 (Pubitemid 29214814)
23. De Haan, G., and A. Gerrits. 2007. Epigenetic control of hematopoietic stem cell aging the case of Ezh2. Ann. N. Y. Acad. Sci. 1106: 233-239. doi:10.1196/annals.1392.008 (Pubitemid 47443044)
24. Ellis, P., B.M. Fagan, S.T. Magness, S. Hutton, O. Taranova, S. Hayashi, A. McMahon, M. Rao, and L. Pevny. 2004. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev. Neurosci. 26: 148-165. doi:10.1159/000082134 (Pubitemid 40867972)
25. Ezhkova, E., H.A. Pasolli, J.S. Parker, N. Stokes, I.H. Su, G. Hannon, A. Tarakhovsky, and E. Fuchs. 2009. Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell. 136: 1122-1135. doi:10.1016/j.cell.2008.12.043
26. Ferri, A.L., M. Cavallaro, D. Braida, A. Di Cristofano, A. Canta, A. Vezzani, S. Ottolenghi, P.P. Pandolfi, M. Sala, S. DeBiasi, and S.K. Nicolis. 2004. Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development. 131: 3805-3819. doi:10.1242/dev.01204
27. Ge, S., E.L. Goh, K.A. Sailor, Y. Kitabatake, G.L. Ming, and H. Song. 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature. 439: 589-593. doi:10.1038/nature04404 (Pubitemid 43185382)
28. Graham, V., J. Khudyakov, P. Ellis, and L. Pevny. 2003. SOX2 functions to maintain neural progenitor identity. Neuron. 39: 749-765. doi:10.1016/S0896- 6273(03)00497-5 (Pubitemid 37088088)
29. Hsieh, J., and F.H. Gage. 2004. Epigenetic control of neural stem cell fate. Curr. Opin. Genet. Dev. 14: 461-469. doi: 10.1016/j.gde.2004.07.006 (Pubitemid 39360292)
30. Ivey, K.N., A. Muth, J. Arnold, F.W. King, R.F. Yeh, J.E. Fish, E.C. Hsiao, R.J. Schwartz, B.R. Conklin, H.S. Bernstein, and D. Srivastava. 2008. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell. 2: 219-229. doi:10.1016/j.stem.2008.01.016 (Pubitemid 351298595)
31. Jaenisch, R., and R. Young. 2008. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell. 132: 567-582. doi:10.1016/j.cell. 2008.01.015 (Pubitemid 351253686)
32. Jay, C., J. Nemunaitis, P. Chen, P. Fulgham, and A.W. Tong. 2007. miRNA profiling for diagnosis and prognosis of human cancer. DNA Cell Biol. 26: 293-300. doi:10.1089/dna.2006.0554 (Pubitemid 46799178)
33. John, B., A.J. Enright, A. Aravin, T. Tuschl, C. Sander, and D.S. Marks. 2004. Human MicroRNA targets. PLoS Biol. 2: e363. doi:10.1371/journal.pbio. 0020363
34. Kishi, N., and J.D. Macklis. 2004. MECP2 is progressively expressed in postmigratory neurons and is involved in neuronal maturation rather than cell fate decisions. Mol. Cell. Neurosci. 27: 306-321. (Pubitemid 39433843)
35. Kozaki, K., I. Imoto, S. Mogi, K. Omura, and J. Inazawa. 2008. Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res. 68: 2094-2105. doi:10.1158/0008-5472.CAN-07-5194 (Pubitemid 351521781)
36. Krek, A., D. Grun, M.N. Poy, R. Wolf, L. Rosenberg, E.J. Epstein, P. MacMenamin, I. da Piedade, K.C. Gunsalus, M. Stoffel, and N. Rajewsky. 2005. Combinatorial microRNA target predictions. Nat. Genet. 37: 495-500. doi:10.1038/ng1536
37. Lao, K., N.L. Xu, V. Yeung, C. Chen, K.J. Livak, and N.A. Straus. 2006. Multiplexing RT-PCR for the detection of multiple miRNA species in small samples. Biochem. Biophys. Res. Commun. 343: 85-89. doi:10.1016/j.bbrc.2006.02. 106
38. Larsen, F., G. Gundersen, R. Lopez, and H. Prydz. 1992. CpG islands as gene markers in the human genome. Genomics. 13: 1095-1107. doi:10.1016/0888- 7543(92)90024-M
39. Lee, T.I., R.G. Jenner, L.A. Boyer, M.G. Guenther, S.S. Levine, R.M. Kumar, B. Chevalier, S.E. Johnstone, M.F. Cole, K. Isono, et al. 2006. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell. 125: 301-313. doi:10.1016/j.cell.2006.02.043 (Pubitemid 44313811)
40. Lee, E.R., F.E. Murdoch, and M.K. Fritsch. 2007. High histone acetylation and decreased polycomb repressive complex 2 member levels regulate gene specific transcriptional changes during early embryonic stem cell differentiation induced by retinoic acid. Stem Cells. 25: 2191-2199. doi:10.1634/stemcells.2007-0203
41. Lewis, B.P., I.H. Shih, M.W. Jones-Rhoades, D.P. Bartel, and C.B. Burge. 2003. Prediction of mammalian microRNA targets. Cell. 115: 787-798. doi:10.1016/S0092-8674(03)01018-3
42. Li, X., B.Z. Barkho, Y. Luo, R.D. Smrt, N.J. Santistevan, C. Liu, T. Kuwabara, F.H. Gage, and X. Zhao. 2008. Epigenetic regulation of the stem cell mitogen Fgf-2 by Mbd1 in adult neural stem/progenitor cells. J. Biol. Chem. 283: 27644-27652. doi:10.1074/jbc.M804899200
43. Lim, D.A., Y.C. Huang, T. Swigut, A.L. Mirick, J.M. Garcia-Verdugo, J. Wysocka, P. Ernst, and A. Alvarez-Buylla. 2009. Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature. 458: 529-533. doi:10.1038/nature07726
44. Livak, K.J., and T.D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25: 402-408. doi:10.1006/meth.2001.1262 (Pubitemid 34164012)
45. Ma, D.K., M.H. Jang, J.U. Guo, Y. Kitabatake, M.L. Chang, N. Pow-Anpongkul, R.A. Flavell, B. Lu, G.L. Ming, and H. Song. 2009. Neuronal activityinduced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science. 323: 1074-1077. doi:10.1126/science.1166859
46. Ming, G.L., and H. Song. 2005. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28: 223-250. doi:10.1146/annurev. neuro.28.051804.101459 (Pubitemid 41098905)
47. O'Carroll, D., S. Erhardt, M. Pagani, S.C. Barton, M.A. Surani, and T. Jenuwein. 2001. The polycomb-group gene Ezh2 is required for early mouse development. Mol. Cell. Biol. 21: 4330-4336. doi:10.1128/MCB.21.13.4330-4336. 2001 (Pubitemid 32565314)
48. Paddison, P.J., A.A. Caudy, E. Bernstein, G.J. Hannon, and D.S. Conklin. 2002. Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cells. Genes Dev. 16: 948-958. doi:10.1101/gad.981002
49. Shahbazian, M.D., and H.Y. Zoghbi. 2002. Rett syndrome and MeCP2: linking epigenetics and neuronal function. Am. J. Hum. Genet. 71: 1259-1272. doi:10.1086/345360
50. Shen, X., Y. Liu, Y.J. Hsu, Y. Fujiwara, J. Kim, X. Mao, G.C. Yuan, and S.H. Orkin. 2008. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell. 32: 491-502. doi:10.1016/j.molcel.2008.10.016
51. Sher, F., R. Rossler, N. Brouwer, V. Balasubramaniyan, E. Boddeke, and S. Copray. 2008. Differentiation of neural stem cells into oligodendrocytes: involvement of the polycomb group protein Ezh2. Stem Cells. 26: 2875-2883. doi:10.1634/stemcells.2008-0121
52. Shiraki, T., S. Kondo, S. Katayama, K. Waki, T. Kasukawa, H. Kawaji, R. Kodzius, A. Watahiki, M. Nakamura, T. Arakawa, et al. 2003. Cap analysis gene expression for high-throughput analysis of transcriptional starting point and identification of promoter usage. Proc. Natl. Acad. Sci. USA. 100: 15776-15781. doi:10.1073/pnas.2136655100 (Pubitemid 38021066)
53. Silber, J., D.A. Lim, C. Petritsch, A.I. Persson, A.K. Maunakea, M. Yu, S.R. Vandenberg, D.G. Ginzinger, C.D. James, J.F. Costello, et al. 2008. miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med. 6: 14. doi:10.1186/1741- 7015-6-14 (Pubitemid 352003733)
54. Smrt, R.D., J. Eaves-Egenes, B.Z. Barkho, N.J. Santistevan, C. Zhao, J.B. Aimone, F.H. Gage, and X. Zhao. 2007. Mecp2 deficiency leads to delayed maturation and altered gene expression in hippocampal neurons. Neurobiol. Dis. 27: 77-89. doi:10.1016/j.nbd.2007.04.005
55. Suh, H., A. Consiglio, J. Ray, T. Sawai, K.A. D'Amour, and F.H. Gage. 2007. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell. 1: 515-528. doi:10.1016/j.stem.2007.09.002 (Pubitemid 350056408)
56. Tang, X., D.L. Falls, X. Li, T. Lane, and M.B. Luskin. 2007. Antigen-retrieval procedure for bromodeoxyuridine immunolabeling with concurrent labeling of nuclear DNA and antigens damaged by HCl pretreatment. J. Neurosci. 27: 5837-5844. doi:10.1523/JNEUROSCI.5048-06.2007 (Pubitemid 46849740)
57. Tao, J., K. Hu, Q. Chang, H. Wu, N.E. Sherman, K. Martinowich, R.J. Klose, C. Schanen, R. Jaenisch, W. Wang, and Y.E. Sun. 2009. Phosphorylation of MeCP2 at Serine 80 regulates its chromatin association and neurological function. Proc. Natl. Acad. Sci. USA. 106: 4882-4887. doi: 10.1073/pnas. 0811648106
58. Taranova, O.V., S.T. Magness, B.M. Fagan, Y. Wu, N. Surzenko, S.R. Hutton, and L.H. Pevny. 2006. SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev. 20: 1187-1202. doi:10.1101/gad.1407906
59. van Praag, H., A.F. Schinder, B.R. Christie, N. Toni, T.D. Palmer, and F.H. Gage. 2002. Functional neurogenesis in the adult hippocampus. Nature. 415: 1030-1034. doi:10.1038/4151030a
60. Wang, Y., R. Medvid, C. Melton, R. Jaenisch, and R. Blelloch. 2007. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat. Genet. 39: 380-385. doi:10.1038/ng1969 (Pubitemid 46328490)
61. Weber, M., J.J. Davies, D. Wittig, E.J. Oakeley, M. Haase, W.L. Lam, and D. Schubeler. 2005. Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet. 37: 853-862. doi:10.1038/ng1598 (Pubitemid 41077111)
62. Yekta, S., I.H. Shih, and D.P. Bartel. 2004. MicroRNA-directed cleavage of HOXB8 mRNA. Science. 304: 594-596. doi:10.1126/science.1097434
63. Yi, R., M.N. Poy, M. Stoffel, and E. Fuchs. 2008. A skin microRNA promotes differentiation by repressing 'stemness'. Nature. 452: 225-229. doi:10.1038/nature06642
64. Zappone, M.V., R. Galli, R. Catena, N. Meani, S. De Biasi, E. Mattei, C. Tiveron, A.L. Vescovi, R. Lovell-Badge, S. Ottolenghi, and S.K. Nicolis. 2000. Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development. 127: 2367-2382.
65. Zhao, X., T. Ueba, B.R. Christie, B. Barkho, M.J. McConnell, K. Nakashima, E.S. Lein, B.D. Eadie, A.R. Willhoite, A.R. Muotri, et al. 2003. Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc. Natl. Acad. Sci. USA. 100: 6777-6782. doi:10.1073/pnas.1131928100 (Pubitemid 36666656)
66. Zhao, C., E.M. Teng, R.G. Summers Jr., G.L. Ming, and F.H. Gage. 2006. Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J. Neurosci. 26: 3-11. doi:10.1523/JNEUROSCI.3648-05.2006 (Pubitemid 43089515)
67. Zhao, C., W. Deng, and F.H. Gage. 2008. Mechanisms and functional implications of adult neurogenesis. Cell. 132: 645-660. doi:10.1016/j.cell.2008. 01.033 (Pubitemid 351253687)
68. Zhao, C., G. Sun, S. Li, and Y. Shi. 2009. A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat. Struct. Mol. Biol. 16: 365-371. doi:10.1038/nsmb.1576
69. Zhou, Z., E.J. Hong, S. Cohen, W.N. Zhao, H.Y. Ho, L. Schmidt, W.G. Chen, Y. Lin, E. Savner, E.C. Griffith, et al. 2006. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron. 52: 255-269. doi:10.1016/j.neuron.2006.09.037 (Pubitemid 44548348)