Gene-specific methylation control of H3K9 and H3K36 on neurotrophic BDNF versus astroglial GFAP genes by KDM4A/C regulates neural stem cell differentiation

Journal of Molecular Biology

Volumn 426, Issue 20, 2014, Pages 3467-3477

  Cascante, Anna ^a   Klum, Susanne ^a   Biswas, Moumita ^a   Antolin Fontes, Beatriz ^a   Barnabé Heider, Fanie ^a   Hermanson, Ola ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

acetylation; CNTF; neuronal differentiation; valproic acid

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; DOUBLECORTIN; FIBROBLAST GROWTH FACTOR 2; GLIAL FIBRILLARY ACIDIC PROTEIN; HISTONE DEMETHYLASE; HISTONE H3; INTRINSIC FACTOR; LYSINE; LYSINE DEMETHYLASE 4A; LYSINE DEMETHYLASE 4C; MITOGENIC AGENT; RNA POLYMERASE II; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VALPROIC ACID; HISTONE;

ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CELL CYCLE S PHASE; CELL DEATH; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DIENCEPHALON; ELECTROPORATION; EMBRYO; EXON; FOREBRAIN; GENE EXPRESSION; GLIOBLASTOMA; HISTONE ACETYLATION; HISTONE DEMETHYLATION; HISTONE METHYLATION; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PROMOTER REGION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SURVIVAL; TELENCEPHALON; UPREGULATION; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

ANIMALS; ASTROCYTES; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; HISTONES; IMMUNOBLOTTING; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; LYSINE; METHYLATION; MICE; MICROSCOPY, FLUORESCENCE; NEURAL STEM CELLS; PROMOTER REGIONS, GENETIC; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA POLYMERASE II;

EID: 84907574014     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.04.008     Document Type: Article

References (49)

1. T. Kouzarides Chromatin modifications and their function Cell 128 2007 693 705
2. T. Lilja, N. Heldring, and O. Hermanson Like a rolling histone: epigenetic regulation of neural stem cells and brain development by factors controlling histone acetylation and methylation Biochim Biophys Acta 1830 2013 2354 2360
3. C. Martin, and Y. Zhang The diverse functions of histone lysine methylation Nat Rev Mol Cell Biol 6 2005 838 849
4. Y. Shi, and J.R. Whetstine Dynamic regulation of histone lysine methylation by demethylases Mol Cell 25 2007 1 14
5. P.A. Cloos, J. Christensen, K. Agger, and K. Helin Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease Genes Dev 22 2008 1115 1140
6. Y.G. Shi, and Y. Tsukada The discovery of histone demethylases Cold Spring Harbor Perspect Biol 5 2013 10.1101/cshperspect.a017947
7. C.L. Fisher, and A.G. Fisher Chromatin states in pluripotent, differentiated, and reprogrammed cells Curr Opin Genet Dev 21 2011 140 146
8. D. Pasini, K.H. Hansen, J. Christensen, K. Agger, P.A. Cloos, and K. Helin Coordinated regulation of transcriptional repression by the RBP2 H3K4 demethylase and polycomb-repressive complex 2 Genes Dev 22 2008 1345 1355
9. N.S. Outchkourov, J.M. Muino, K. Kaufmann, W.F. van Ijcken, M.J. Groot Koerkamp, and D. van Leenen Balancing of histone H3K4 methylation states by the Kdm5c/SMCX histone demethylase modulates promoter and enhancer function Cell Rep 3 2013 1071 1079
10. K. Agger, P.A. Cloos, J. Christensen, D. Pasini, S. Rose, and J. Rappsilber UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development Nature 449 2007 731 734
11. A.A. Mansour, O. Gafni, L. Weinberger, A. Zviran, M. Ayyash, and Y. Rais The H3K27 demethylase Utx regulates somatic and germ cell epigenetic reprogramming Nature 488 2012 409 413
12. K. Jepsen, D. Solum, T. Zhou, R.J. McEvilly, H.J. Kim, and C.K. Glass SMRT-mediated repression of an H3K27 demethylase in progression from neural stem cell to neuron Nature 450 2007 415 419
13. Y. Tsukada, T. Ishitani, and K.I. Nakayama KDM7 is a dual demethylase for histone H3 Lys 9 and Lys 27 and functions in brain development Genes Dev 24 2010 432 437
14. Y. Tsukada, J. Fang, H. Erdjument-Bromage, M.E. Warren, C.H. Borchers, and P. Tempst Histone demethylation by a family of JmjC domain-containing proteins Nature 439 2006 811 816
15. P.A. Cloos, J. Christensen, K. Agger, A. Maiolica, J. Rappsilber, and T. Antal The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3 Nature 442 2006 307 311
16. R.J. Klose, K. Yamane, Y. Bae, D. Zhang, H. Erdjument-Bromage, and P. Tempst The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36 Nature 442 2006 312 316
17. J.R. Whetstine, A. Nottke, F. Lan, M. Huarte, S. Smolikov, and Z. Chen Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases Cell 125 2006 467 481
18. A.J. Bannister, R. Schneider, F.A. Myers, A.W. Thorne, C. Crane-Robinson, and T. Kouzarides Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes J Biol Chem 280 2005 17732 17736
19. A.A. Joshi, and K. Struhl Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation Mol Cell 20 2005 971 978
20. M.C. Keogh, S.K. Kurdistani, S.A. Morris, S.H. Ahn, V. Podolny, and S.R. Collins Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex Cell 123 2005 593 605
21. E.J. Wagner, and P.B. Carpenter Understanding the language of Lys36 methylation at histone H3 Nat Rev Mol Cell Biol 13 2012 115 126
22. M. Wissmann, N. Yin, J.M. Muller, H. Greschik, B.D. Fodor, and T. Jenuwein Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression Nat Cell Biol 9 2007 347 353
23. D. Zhang, H.G. Yoon, and J. Wong JMJD2A is a novel N-CoR-interacting protein and is involved in repression of the human transcription factor achaete scute-like homologue 2 (ASCL2/Hash2) Mol Cell Biol 25 2005 6404 6414
24. O. Hermanson, K. Jepsen, and M.G. Rosenfeld N-CoR controls differentiation of neural stem cells into astrocytes Nature 419 2002 934 939
25. W.L. Berry, and R. Janknecht KDM4/JMJD2 histone demethylases: epigenetic regulators in cancer cells Cancer Res 73 2013 2936 2942
26. Y.H. Loh, W. Zhang, X. Chen, J. George, and H.H. Ng Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells Genes Dev 21 2007 2545 2557
27. P.P. Das, Z. Shao, S. Beyaz, E. Apostolou, L. Pinello, and A.D. Angeles Distinct and combinatorial functions of Jmjd2b/Kdm4b and Jmjd2c/Kdm4c in mouse embryonic stem cell identity Mol Cell 53 2013 32 48
28. K.K. Johe, T.G. Hazel, T. Müller, M.M. Dugich-Djordjevic, and R.D. McKay Single factors direct the differentiation of stem cells from the fetal and adult central nervous system Genes Dev 10 1996 3129 3140
29. R. Ravin, D.J. Hoeppner, D.M. Munno, L. Carmel, J. Sullivan, and D.L. Levitt Potency and fate specification in CNS stem cell populations in vitro Cell Stem Cell 3 2008 670 680
30. T. Andersson, E. Södersten, J.K. Duckworth, A. Cascante, N. Fritz, and P. Sacchetti CXXC5 is a novel BMP4-regulated modulator of Wnt signaling in neural stem cells J Biol Chem 284 2009 3672 3681
31. K. Wallenborg, P. Vlachos, S. Eriksson, L. Huijbregts, E.S. Arner, and B. Joseph Red wine triggers cell death and thioredoxin reductase inhibition: effects beyond resveratrol and SIRT1 Exp Cell Res 315 2009 1360 1371
32. T. Andersson, J.K. Duckworth, N. Fritz, M. Lewicka, E. Södersten, and P. Uhlén Noggin and Wnt3a enable BMP4-dependent differentiation of telencephalic stem cells into GluR-agonist responsive neurons Mol Cell Neurosci 47 2011 10 18
33. J. Hsieh, K. Nakashima, T. Kuwabara, E. Mejia, and F.H. Gage Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells Proc Natl Acad Sci U S A 101 2004 16659 16664
34. P. Laeng, R.L. Pitts, A.L. Lemire, C.E. Drabik, A. Weiner, and H. Tang The mood stabilizer valproic acid stimulates GABA neurogenesis from rat forebrain stem cells J Neurochem 91 2004 238 251
35. D.J. Greenway, M. Street, A. Jeffries, and N.J. Buckley RE1 Silencing transcription factor maintains a repressive chromatin environment in embryonic hippocampal neural stem cells Stem Cells 25 2007 354 363
36. R.N. Leao, A. Reis, A. Emirandetti, M. Lewicka, O. Hermanson, and A. Fisahn A voltage-sensitive dye-based assay for the identification of differentiated neurons derived from embryonic neural stem cell cultures PLoS One 5 2010 e13833
37. S. Yasuda, M.H. Liang, Z. Marinova, A. Yahyavi, and D.M. Chuang The mood stabilizers lithium and valproate selectively activate the promoter IV of brain-derived neurotrophic factor in neurons Mol Psychiatry 14 2009 51 59
38. E.J. Huang, and L.F. Reichardt Neurotrophins: roles in neuronal development and function Annu Rev Neurosci 24 2001 677 736
39. K. Bartkowska, A. Paquin, A.S. Gauthier, D.R. Kaplan, and F.D. Miller Trk signaling regulates neural precursor cell proliferation and differentiation during cortical development Development 134 2007 4369 4380
40. F.D. Miller, and D.R. Kaplan Neurotrophin signalling pathways regulating neuronal apoptosis Cell Mol Life Sci 58 2001 1045 1053
41. S.P. Sardi, J. Murtie, S. Koirala, B.A. Patten, and G. Corfas Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain Cell 127 2006 185 197
42. C. Andreu-Agullo, J.M. Morante-Redolat, A.C. Delgado, and I. Farinas Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone Nat Neurosci 12 2009 1514 1523
43. N. Heldring, U. Nyman, P. Lönnerberg, S. Önnestam, A. Herland, and J. Holmberg NCoR controls glioblastoma tumor cell characteristics Neuro Oncol 16 2013 241 249
44. F. Barnabe-Heider, J.A. Wasylnka, K.J. Fernandes, C. Porsche, M. Sendtner, and D.R. Kaplan Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1 Neuron 48 2005 253 265
45. Y. Shi, F. Lan, C. Matson, P. Mulligan, J.R. Whetstine, and P.A. Cole Histone demethylation mediated by the nuclear amine oxidase homolog LSD1 Cell 119 2004 941 953
46. E. Metzger, M. Wissmann, N. Yin, J.M. Muller, R. Schneider, and A.H. Peters LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription Nature 437 2005 436 439
47. C.R. Vakoc, M.M. Sachdeva, H. Wang, and G.A. Blobel Profile of histone lysine methylation across transcribed mammalian chromatin Mol Cell Biol 26 2006 9185 9195
48. S. Barrand, I.S. Andersen, and P. Collas Promoter-exon relationship of H3 lysine 9, 27, 36 and 79 methylation on pluripotency-associated genes Biochem Biophys Res Commun 401 2010 611 617
49. Y. Hirabayashi, N. Suzki, M. Tsuboi, T.A. Endo, T. Toyoda, and J. Shinga Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition Neuron 63 2009 600 613