Loss of the chromatin regulator MRG15 limits neural stem/progenitor cell proliferation via increased expression of the p21 Cdk inhibitor

Stem Cell Research

Volumn 7, Issue 1, 2011, Pages 75-88

  Chen, Meizhen ^a   Pereira Smith, Olivia M ^a,b   Tominaga, Kaoru ^a,b  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CYCLIN DEPENDENT KINASE INHIBITOR 1; HISTONE H2AX; PROTEIN P53; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL FUNCTION; CELL PROLIFERATION; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; EMBRYO; GENE; GENE SILENCING; IMMUNOHISTOCHEMISTRY; IONIZING RADIATION; MOUSE; MRG15 GENE; NEURAL STEM CELL; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; CELL GROWTH PROCESSES; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; TRANS-ACTIVATORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 79956346295     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2011.04.002     Document Type: Article

References (86)

1. Allen D.M., van Praag H., Ray J., Weaver Z., Winrow C.J., Carter T.A., Braquet R., Harrington E., Ried T., Brown K.D., Gage F.H., Barlow C. Ataxia telangiectasia mutated is essential during adult neurogenesis. Genes Dev. 2001, 15:554-566.
2. Armesilla-Diaz A., Bragado P., Del Valle I., Cuevas E., Lazaro I., Martin C., Cigudosa J.C., Silva A. p53 regulates the self-renewal and differentiation of neural precursors. Neuroscience 2009, 158:1378-1389.
3. Bertram M.J., Pereira-Smith O.M. Conservation of the MORF4 related gene family: identification of a new chromo domain subfamily and novel protein motif. Gene 2001, 266:111-121.
4. Bertram M.J., Berube N.G., Hang-Swanson X., Ran Q., Leung J.K., Bryce S., Spurgers K., Bick R.J., Baldini A., Ning Y., Clark L.J., Parkinson E.K., Barrett J.C., Smith J.R., Pereira-Smith O.M. Identification of a gene that reverses the immortal phenotype of a subset of cells and is a member of a novel family of transcription factor-like genes. Mol. Cell. Biol. 1999, 19:1479-1485.
5. Borrelli E., Nestler E.J., Allis C.D., Sassone-Corsi P. Decoding the epigenetic language of neuronal plasticity. Neuron 2008, 60:961-974.
6. Brehm A., Tufteland K.R., Aasland R., Becker P.B. The many colours of chromodomain. Bioessays 2004, 26:133-140.
7. Cai Y., Jin J., Tomomori-Sato C., Sato S., Sorokina I., Parmely T.J., Conaway R.C., Conaway J.W. Identification of new subunits of the multiprotein mammalian TRRAP/TIP60-containing histone acetyltransferase complex. J. Biol. Chem. 2003, 278:42733-42736.
8. Carrozza M.J., Li B., Florens L., Suganuma T., Swanson S.K., Lee K.K., Shia W.-J., Anderson S., Yates J., Washburn M.P., Workman J.L. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 2005, 123:581-592.
9. Cavalli G., Paro R. Chromo-domain proteins: linking chromatin structure to epigenetic regulation. Curr. Opin. Cell Biol. 1998, 10:354-360.
10. Chen M., Takano-Maruyama M., Pereira-Smith O.M., Gaufo G.O., Tominaga K. MRG15, a component of HAT and HDAC complexes, is essential for proliferation and differentiation of neural precursor cells. J. Neurosci. Res. 2009, 87:1522-1531.
11. Doyon Y., Cote J. The highly conserved and multifunctional NuA4 complex. Curr. Opin. Genet. Dev. 2004, 14:147-154.
12. Doyon Y., Selleck W., Lane W.S., Tan S., Cote J. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol. Cell. Biol. 2004, 24:1884-1896.
13. Doyon Y., Cayrou C., Ullah M., Landry A.-J., Cote V., Selleck W., Lane W.S., Tan S., Yang X.-J., Cote J. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol. Cell 2006, 21:51-64.
14. Eisen A., Utley R.T., Nourani A., Allard S., Schmidt P., Lane W.S., Lucchesi J.C., Cote J. The yeast NuA4 and Drosophila MSL complexes contain homologous subunits important for transcription regulation. J. Biol. Chem. 2001, 276:3484-3491.
15. Evans T.A., Raina A.K., Delacourte A., Aprelikova O., Lee H.-G., Zhu X., Perry G., Smith M.A. BRCA1 may modulate neuronal cell cycle re-entry in Alzheimer disease. Int. J. Med. Sci. 2007, 4:140-145.
16. Fasano C.A., Dimos J.T., Ivanova N.B., Lowry N., Lemischka I.R., Temple S. shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 2007, 1:87-99.
17. Fazzio T.G., Huff J.T., Panning B. An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 2008, 134:162-174.
18. Fazzio T.G., Huff J.T., Panning B. Chromatin regulation Tip(60)s the balance in embryonic stem cell self-renewal. Cell Cycle 2008, 7:3302-3306.
19. Ferron S.R., Marques-Torrejon M.A., Mira H., Flores I., Taylor K., Blasco M.A., Farinas I. Telomere shortening in neural stem cells disrupts neuronal differentiation and neuritogenesis. J. Neurosci. 2009, 29:14394-14407.
20. Frappart P.-O., McKinnon P.J. Mouse models of DNA double-strand break repair and neurological disease. DNA Repair 2008, 7:1051-1060.
21. Frappart P.-O., Tong W.-M., Demuth I., Radovanovic I., Herceg Z., Aguzzi A., Digweed M., Wang Z.-Q. An essential function for NBS1 in the prevention of ataxia and cerebellar defects. Nat. Med. 2005, 11:538-544.
22. Frappart P.-O., Lee Y., Lamont J., McKinnon P.J. BRCA2 is required for neurogenesis and suppression of medulloblastoma. EMBO J. 2007, 26:2732-2742.
23. Gage F.H. Mammalian neural stem cells. Science 2000, 287:1433-1438.
24. Garcia S.N., Kirtane B.M., Podlutsky A.J., Pereira-Smith O.M., Tominaga K. Mrg15 null and heterozygous mouse embryonic fibroblasts exhibit DNA-repair defects post exposure to gamma ionizing radiation. FEBS Lett. 2007, 581:5275-5281.
25. Gevry N., Chan H.M., Laflamme L., Livingston D.M., Gaudreau L. p21 transcription is regulated by differential localization of histone H2A.Z. Genes Dev. 2007, 21:1869-1881.
26. Gil-Perotin S., Marin-Husstege M., Li J., Soriano-Navarro M., Zindy F., Roussel M.F., Garcia-Verdugo J.M., Casaccia-Bonnefil P. Loss of p53 induces changes in the behavior of subventricular zone cells: implication for the genesis of glial tumors. J. Neurosci. 2006, 26:1107-1116.
27. Graff J., Mansuy I.M. Epigenetic dysregulation in cognitive disorders. Eur. J. Neurosci. 2009, 30:1-8.
28. Guan J.-S., Haggarty S.J., Giacometti E., Dannenberg J.-H., Joseph N., Gao J., Nieland T.J., Zhou Y., Wang X., Mazitschek R., Bradner J.E., DePinho R.A., Jaenisch R., Tsai L.-H. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009, 459:55-60.
29. Hayakawa T., Ohtani Y., Hayakawa N., Shinmyozu K., Saito M., Ishikawa F., Nakayama J. RBP2 is an MRG15 complex component and down-regulates intragenic histone H3 lysine 4 methylation. Genes Cells 2007, 12:811-826.
30. Hayakawa T., Zhang F., Hayakawa N., Ohtani Y., Shinmyozu K., Nakayama J., Andreassen P.R. MRG15 binds directly to PALB2 and stimulates homology-directed repair of chromosomal breaks. J. Cell Sci. 2010, 123:1124-1130.
31. Hsieh J., Eisch A.J. Epigenetics, hippocampal neurogenesis, and neuropsychiatric disorders: unraveling the genome to understand the mind. Neurobiol. Dis. 2010, 39:73-84.
32. Ikura T., Ogryzko V.V., Grigoriev M., Groisman R., Wang J., Horikoshi M., Scully R., Qin J., Nakatani Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000, 102:463-473.
33. Ikura T., Tashiro S., Kakino A., Shima H., Jacob N., Amunugama R., Yoder K., Izumi S., Kuraoka I., Tanaka K., Kimura H., Ikura M., Nishikubo S., Ito T., Muto A., Miyagawa K., Takeda S., Fishel R., Igarashi K., Kamiya K. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 2007, 27:7028-7040.
34. Jacobs J.J.L., Kieboom K., Marino S., DePinho R.A., van Lohuizen M. The oncogene and polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 1999, 397:164-168.
35. Jelinic P., Pellegrino J., David G. A novel mammalian complex containing Sin3B mitigates histone acetylation and RNA polymerase II progression within transcribed loci. Mol. Cell. Biol. 2011, 31:54-62.
36. Jones D.O., Cowell I.G., Singh P.B. Mammalian chromodomain proteins: their role in genome organisation and expression. Bioessays 2000, 22:124-137.
37. Joshi A.A., Struhl K. Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol. Cell 2005, 20:971-978.
38. Keogh M.-C., Kurdistani S.K., Morris S.A., Ahn S.H., Podolny V., Collins S.R., Schuldiner M., Chin K., Punna T., Thompson N.J., Boone C., Emili A., Weissman J.S., Hughes T.R., Strahl B.D., Grunstein M., Greenblatt J.F., Buratowski S., Krogan N.J. Cotranscriptional Set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 2005, 123:593-605.
39. Kippin T.E., Martens D.J., van der Kooy D. p21 loss compromises the relative quiescence of forebrain stem cell proliferation leading to exhaustion of their proliferation capacity. Genes Dev. 2005, 19:756-767.
40. Kusch T., Florens L., MacDonald W.H., Swanson S.K., Glaser R.L., Yates J.R., Abmayr S.M., Washburn M.P., Workman J.L. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 2004, 306:2084-2087.
41. Lee Y., Mckinnon P.J. Responding to DNA double strand breaks in the nervous system. Neuroscience 2007, 145:1365-1374.
42. Lee Y., Barnes D.E., Lindahl T., McKinnon P.J. Defective neurogenesis resulting from DNA ligase IV deficiency requires Atm. Genes Dev. 2000, 14:2576-2580.
43. Lee N., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. The H3K4 demethylase Lid associates with and inhibits histone deacetylase Rpd3. Mol. Cell. Biol. 2009, 29:1401-1410.
44. Li X., Zhao X. Epigenetic regulation of mammalian stem cells. Stem Cells Dev. 2008, 17:1043-1052.
45. Lim D.A., Huang Y.C., Swigut T., Mirick A.L., Garcia-Verdugo J.M., Wysocka J., Ernst P., Alvarez-Buylla A. Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 2009, 458:529-533.
46. Ma D.K., Bonaguidi M.A., Ming G.-L., Song H. Adult neural stem cells in the mammalian central nervous system. Cell Res. 2009, 19:672-682.
47. Marin I., Baker B.S. Origin and evolution of the regulatory gene male-specific lethal-3. Mol. Biol. Evol. 2000, 17:1240-1250.
48. McKinnon P.J. DNA repair deficiency and neurological disease. Nat. Rev. Neurosci. 2009, 10:100-112.
49. McShea A., Wahl A.F., Smith M.A. Re-entry into the cell cycle: a mechanism for neurodegeneration in Alzheimer disease. Med. Hypotheses 1999, 52:525-527.
50. Medrano S., Scrable H. Maintaining appearances-the role of p53 in adult neurogenesis. Biochem. Biophys. Res. Commun. 2005, 331:828-833.
51. Medrano S., Burns-Cusato M., Atienza M.B., Rahimi D., Scrable H. Regenerative capacity of neural precursors in the adult mammalian brain is under the control of p53. Neurobiol. Aging 2009, 30:483-497.
52. Mehler M.F. Epigenetics and the nervous system. Ann. Neurol. 2008, 64:602-617.
53. Meletis K., Wirta V., Hede S.M., Nister M., Lundeberg J., Frisen J. p53 suppresses the self-renewal of adult neural stem cells. Development 2006, 133:363-369.
54. Molofsky A.V., Slutsky S.G., Joseph N.M., He S., Pardal R., Krishnamurthy J., Sharpless N.E., Morrison S.J. Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 2006, 443:448-452.
55. Moshkin Y.M., Kan T.W., Goodfellow H., Bezstarosti K., Maeda R.K., Pilyugin M., Karch F., Bray S.J., Demmers J.A., Verrijzer C.P. Histone chaperones ASF1 and NAP1 differentially modulate removal of active histone marks by LID-RPD3 complexes during NOTCH silencing. Mol. Cell 2009, 35:782-793.
56. Murr R., Loizou J.I., Yang Y.-G., Cuenin C., Li H., Wang Z.-Q., Herceg Z. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol. 2006, 8:91-99.
57. Nicolas E., Yamada T., Cam H.P., FitzGerald P.C., Kobayashi R., Grewal S.I.S. Distinct roles of HDAC complexes in promoter silencing, antisense suppression and DNA damage protection. Nat. Struct. Mol. Biol. 2007, 14:372-380.
58. Nijnik A., Woodbine L., Marchetti C., Dawson S., Lambe T., Liu C., Rodrigues N.P., Crockford T.L., Cabuy E., Vindigni A., Enver T., Bell J.I., Slijepcevic P., Goodnow C.C., Jeggo P.A., Cornall R.J. DNA repair is limiting for haematopoietic stem cells during ageing. Nature 2007, 447:686-690.
59. Nishino J., Kim I., Chada K., Morrison S.J. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf expression. Cell 2008, 135:227-239.
60. O'Driscoll M., Cerosaletti K.M., Girard P.-M., Dai Y., Stumm M., Kysela B., Hirsch B., Gennery A., Palmer S.E., Seidel J., Gatti R.A., Varon R., Oettinger M.A., Neitzel H., Jeggo P.A., Concannon P. DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency. Mol. Cell 2001, 8:1175-1185.
61. Pardo P.S., Leung J.K., Lucchesi J.C., Pereira-Smith O.M. MRG15 a novel chromodomain protein is present in two distinct multiprotein complexes involved in transcriptional activation. J. Biol. Chem. 2002, 277:50860-50866.
62. Park J.H., Sun X.J., Roeder R.G. The SANT domain of p400 ATPase represses acetyltransferase activity and coactivator function of TIP60 in basal p21 gene expression. Mol. Cell. Biol. 2010, 30:2750-2761.
63. Pechnick R.N., Zonis S., Wawrowsky K., Pourmorady J., Chesnokova V. p21Cip1 restricts neuronal proliferation in the subgranular zone of the dentate gyrus of the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1358-1363.
64. Peleg S., Sananbenesi F., Zovoilis A., Burkhardt S., Bahari-Javan S., Agis-Balboa R.C., Cota P., Wittnam J.L., Gogol-Doering A., Opitz L., Salinas-Riester G., Dettenhofer M., Kang H., Farinelli L., Chen W., Fischer A. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 2010, 328:753-756.
65. Penner M.R., Roth T.L., Barnes C.A., Sweatt J.D. An epigenetic hypothesis of aging-related cognitive dysfunction. Front. Aging Neurosci. 2010, 2:9.
66. Phoenix T.N., Temple S. Spred1, anegative regulator of Ras-MAPK-ERK, is enriched in CNS germinal zones, dampens NSC proliferation, and maintains ventricular zone structure. Genes Dev. 2010, 24:45-56.
67. Raina A.K., Pardo P., Rottkamp C.A., Zhu X., Pereira-Smith O.M., Smith M.A. Neurons in Alzheimer disease emerge from senescence. Mech. Ageing Dev. 2001, 123:3-9.
68. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255:1707-1710.
69. Reynolds B.A., Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 1996, 175:1-13.
70. Rossi D.J., Bryder D., Seita J., Nussenzweig A., Hoeijmakers J., Weissman I.L. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 2007, 447:725-729.
71. Sardiu M.E., Cai Y., Jin J., Swanson S.K., Conaway R.C., Conaway J.W., Florens L., Washburn M.P. Probabilistic assembly of human protein interaction networks from label-free quantitative proteomics. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:1454-1459.
72. Shi Y., Sun G., Zhao C., Stewart R. Neural stem cell self-renewal. Crit. Rev. Oncol. Hematol. 2008, 65:43-53.
73. Shull E.R.P., Lee Y., Nakane H., Stracker T.H., Zhao J., Russell H.R., Petrini J.H.J., McKinnon P.J. Differential DNA damage signaling accounts for distinct neural apoptotic responses in ATLD and NBS. Genes Dev. 2009, 23:171-180.
74. Squatrito M., Gorrini C., Amati B. Tip60 in DNA damage response and growth control: many tricks in one HAT. Trends Cell Biol. 2006, 16:433-442.
75. Stewart G.S., Maser R.S., Stankovic T., Bressan D.A., Kaplan M.I., Jaspers N.G., Raams A., Byrd P.J., Petrini J.H., Taylor A.M. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 1999, 99:577-587.
76. Sun B., Hong J., Zhang P., Dong X., Shen X., Lin D., Ding J. Molecular basis of the interaction of Saccharomyces cerevisiae Eaf3 chromo domain with methylated H3K36. J. Biol. Chem. 2008, 283:36504-36512.
77. Sy S.M.-H., Huen M.S., Chen J. MRG15 is a novel PALB2-interacting factor involved in homologous recombination. J. Biol. Chem. 2009, 284:21127-21131.
78. Temple S. The development of neural stem cells. Nature 2001, 414:112-117.
79. Tominaga K., Leung J.K., Rookard P., Echigo J., Smith J.R., Pereira-Smith O.M. MRGX is a novel transcriptional regulator that exhibits activation or repression of the B-myb promoter in a cell type-dependent manner. J. Biol. Chem. 2003, 278:49618-49624.
80. Tominaga K., Kirtane B., Jackson J.G., Ikeno Y., Ikeda T., Hawks C., Smith J.R., Matzuk M.M., Pereira-Smith O.M. MRG15 regulates embryonic development and cell proliferation. Mol. Cell. Biol. 2005, 25:2924-2937.
81. Tyteca S., Vandromme M., Legube G., Chevillard-Briet M., Trouche D. Tip60 and p400 are both required for UV-induced apoptosis but play antagonistic roles in cell cycle progression. EMBO J. 2006, 25:1680-1689.
82. Ventura A., Meissner A., Dillon C.P., McManus M., Sharp P.A., Van Parijs L., Jaenisch R., Jacks T. Cre-lox-regulated conditional RNA interference from transgenes. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10380-10385.
83. Wang J., Weaver I.C.G., Gauthier-Fisher A., Wang H., He L., Yeomans J., Wondisford F., Kaplan D.R., Miller F.D. CBP histone acetyltransferase activity regulates embryonic neural differentiation in the normal and Rubinstein-Taybi syndrome brain. Dev. Cell 2010, 18:114-125.
84. Wen S., Li H., Liu J. Epigenetic background of neuronal fate determination. Prog. Neurobiol. 2009, 87:98-117.
85. Yochum G.S., Ayer D.E. Role for the mortality factors MORF4, MRGX, and MRG15 in transcriptional repression via associations with Pf1, mSin3A, and transducin-like enhancer of split. Mol. Cell. Biol. 2002, 22:7868-7876.
86. Zhang P., Du J., Sun B., Dong X., Xu G., Zhou J., Huang Q., Liu Q., Hao Q., Ding J. Structure of human MRG15 chromo domain and its binding to Lys36-methylated histone H3. Nucleic Acids Res. 2006, 34:6621-6628.