MacroH2A1 histone variant represses rDNA transcription

Nucleic Acids Research

Volumn 42, Issue 1, 2014, Pages 181-192

  Cong, Rong ^a   Das, Sadhan ^a   Douet, Julien ^b   Wong, Jiemin ^c   Buschbeck, Marcus ^b   Mongelard, Fabien ^a   Bouvet, Philippe ^a  

^a Laboratoire Joliot Curie   (France)

^b Institute of Predictive and Personalized Medicine of Cancer IMPPC   (Spain)

^c EAST CHINA NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DACTINOMYCIN; DNA DIRECTED RNA POLYMERASE; HISTONE; HISTONE H2A1; NUCLEOLIN; RIBOSOME DNA; UNCLASSIFIED DRUG; HISTONE H2A;

ANIMAL CELL; ARTICLE; CELL STRAIN HEPG2; CONTROLLED STUDY; DNA METHYLATION; DNA TRANSCRIPTION; EMBRYO; EMBRYONIC STEM CELL; HELA CELL; HUMAN; HUMAN CELL; INHIBITION KINETICS; MOUSE; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN LOCALIZATION; TRANSCRIPTION REGULATION; CELLULAR DISTRIBUTION; HELA CELL LINE; HEPG2 CELL LINE; MOUSE EMBRYONIC STEM CELL;

EID: 84891770045     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt863     Document Type: Article

References (37)

1. Moss, T., Langlois, F., Gagnon-Kugler, T. and Stefanovsky, V. (2007) A housekeeper with power of attorney: The rRNA genes in ribosome biogenesis. Cell. Mol. Life Sci., 64, 29-49
2. Henderson, A.S., Warburton, D. and Atwood, K.C. (1972) Location of ribosomal DNA in the human chromosome complement. Proc. Natl Acad. Sci. USA, 69, 3394-3398
3. McStay, B. and Grummt, I. (2008) The epigenetics of rRNA genes: From molecular to chromosome biology. Annu. Rev. Cell Dev. Biol., 24, 131-157
4. Grummt, I. and Langst, G. (2013) Epigenetic control of RNA polymerase I transcription in mammalian cells. Biochim. Biophys. Acta, 1829, 393-404
5. Santoro, R. (2011) The epigenetics of the nucleolus: Structure and function of active and silent ribosomal RNA genes. In: Olson, M.O.J. (ed.), The Nucleolus. Springer, New York, pp. 57-82, Protein Review 15. Series Editor: M Zouhair Atassi
6. Yuan, X., Feng, W., Imhof, A., Grummt, I. and Zhou, Y. (2007) Activation of RNA polymerase I transcription by cockayne syndrome group B protein and histone methyltransferase G9a. Mol. Cell, 27, 585-595
7. Gagnon-Kugler, T., Langlois, F., Stefanovsky, V., Lessard, F. and Moss, T. (2009) Loss of human ribosomal gene CpG methylation enhances cryptic RNA polymerase II transcription and disrupts ribosomal RNA processing. Mol. Cell, 35, 414-425
8. Xie, W., Ling, T., Zhou, Y., Feng, W., Zhu, Q., Stunnenberg, H.G., Grummt, I. and Tao, W. (2012) The chromatin remodeling complex NuRD establishes the poised state of rRNA genes characterized by bivalent histone modifications and altered nucleosome positions. Proc. Natl Acad. Sci. USA, 109, 8161-8166
9. Cong, R., Das, S., Ugrinova, I., Kumar, S., Mongelard, F., Wong, J. and Bouvet, P. (2012) Interaction of nucleolin with ribosomal RNA genes and its role in RNA polymerase I transcription. Nucleic Acids Res., 40, 9441-9454
10. Araya, I., Nardocci, G., Morales, J., Vera, M., Molina, A. and Alvarez, M. (2010) MacroH2A subtypes contribute antagonistically to the transcriptional regulation of the ribosomal cistron during seasonal acclimatization of the carp fish. Epigenetics Chromatin, 3, 14
11. Posavec, M., Timinszky, G. and Buschbeck, M. (2013) Macro domains as metabolite sensors on chromatin. Cell. Mol. Life Sci., 70, 1509-1524
12. Creppe, C., Janich, P., Cantarino, N., Noguera, M., Valero, V., Musulen, E., Douet, J., Posavec, M., Martin-Caballero, J., Sumoy, L. et al. (2012) MacroH2A1 regulates the balance between selfrenewal and differentiation commitment in embryonic and adult stem cells. Mol. Cell Biol., 32, 1442-1452
13. Gamble, M.J., Frizzell, K.M., Yang, C., Krishnakumar, R. and Kraus, W.L. (2010) The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev., 24, 21-32
14. Ouararhni, K., Hadj-Slimane, R., Ait-Si-Ali, S., Robin, P., Mietton, F., Harel-Bellan, A., Dimitrov, S. and Hamiche, A. (2006) The histone variant mH2A1.1 interferes with transcription by down-regulating PARP-1 enzymatic activity. Genes Dev., 20, 3324-3336
15. Angelov, D., Bondarenko, V.A., Almagro, S., Menoni, H., Mongelard, F., Hans, F., Mietton, F., Studitsky, V.M., Hamiche, A., Dimitrov, S. et al. (2006) Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J., 25, 1669-1679
16. Ugrinova, I., Monier, K., Ivaldi, C., Thiry, M., Storck, S., Mongelard, F. and Bouvet, P. (2007) Inactivation of nucleolin leads to nucleolar disruption, cell cycle arrest and defects in centrosome duplication. BMC Mol. Biol., 8, 66
17. Buschbeck, M., Uribesalgo, I., Wibowo, I., Rue, P., Martin, D., Gutierrez, A., Morey, L., Guigo, R., Lopez-Schier, H. and Di Croce, L. (2009) The histone variant macroH2A is an epigenetic regulator of key developmental genes. Nat. Struct. Mol. Biol., 16, 1074-1079
18. Santoro, R. and Grummt, I. (2001) Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol. Cell, 8, 719-725
19. Hernandez-Munoz, I., Lund, A.H., van der Stoop, P., Boutsma, E., Muijrers, I., Verhoeven, E., Nusinow, D.A., Panning, B., Marahrens, Y. and van Lohuizen, M. (2005) Stable X chromosome inactivation involves the PRC1 Polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc. Natl Acad. Sci. USA, 102, 7635-7640
20. Ghoshal, K., Majumder, S., Datta, J., Motiwala, T., Bai, S., Sharma, S.M., Frankel, W. and Jacob, S.T. (2004) Role of human ribosomal RNA (rRNA) promoter methylation and of methyl- CpG-binding protein MBD2 in the suppression of rRNA gene expression. J. Biol. Chem., 279, 6783-6793
21. Conconi, A., Widmer, R.M., Koller, T. and Sogo, J.M. (1989) Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell, 57, 753-761
22. Dammann, R., Lucchini, R., Koller, T. and Sogo, J.M. (1993) Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res., 21, 2331-2338
23. Rickards, B., Flint, S.J., Cole, M.D. and LeRoy, G. (2007) Nucleolin is required for RNA polymerase I transcription in vivo. Mol. Cell. Biol., 27, 937-948
24. Storck, S., Thiry, M. and Bouvet, P. (2009) Conditional knockout of nucleolin in DT40 cells reveals the functional redundancy of its RNA-binding domains. Biol. Cell, 101, 153-167
25. Andersen, J.S., Lyon, C.E., Fox, A.H., Leung, A.K., Lam, Y.W., Steen, H., Mann, M. and Lamond, A.I. (2002) Directed proteomic analysis of the human nucleolus. Curr. Biol., 12, 1-11
26. Scherl, A., Coute, Y., Deon, C., Calle, A., Kindbeiter, K., Sanchez, J.C., Greco, A., Hochstrasser, D. and Diaz, J.J. (2002) Functional proteomic analysis of human nucleolus. Mol. Biol. Cell, 13, 4100-4109.
27. Gaspar-Maia, A., Qadeer, Z.A., Hasson, D., Ratnakumar, K., Adrian Leu, N., Leroy, G., Liu, S., Costanzi, C., Valle-Garcia, D., Schaniel, C. et al. (2013) MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency. Nat. Commun., 4, 1565
28. Changolkar, L.N., Costanzi, C., Leu, N.A., Chen, D., McLaughlin, K.J. and Pehrson, J.R. (2007) Developmental changes in histone macroH2A1-mediated gene regulation. Mol. Cell. Biol., 27, 2758-2764
29. Boulard, M., Storck, S., Cong, R., Pinto, R., Delage, H. and Bouvet, P. (2010) Histone variant macroH2A1 deletion in mice causes female-specific steatosis. Epigenetics Chromatin, 3, 8
30. Pasque, V., Gillich, A., Garrett, N. and Gurdon, J.B. (2011) Histone variant macroH2A confers resistance to nuclear reprogramming. EMBO J., 30, 2373-2387
31. Mongelard, F. and Bouvet, P. (2007) Nucleolin: A multiFACeTed protein. Trends Cell Biol., 17, 80-86
32. Gaume, X., Monier, K., Argoul, F., Mongelard, F. and Bouvet, P. (2011) In vivo study of the histone chaperone activity of nucleolin by FRAP. Biochem. Res. Int., 2011, 187624
33. Csankovszki, G., Panning, B., Bates, B., Pehrson, J.R. and Jaenisch, R. (1999) Conditional deletion of Xist disrupts histone macroH2A localization but not maintenance of X inactivation. Nat. Genet., 22, 323-324
34. Mayer, C., Schmitz, K.M., Li, J., Grummt, I. and Santoro, R. (2006) Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol. Cell, 22, 351-361
35. Hochstatter, J., Holzel, M., Rohrmoser, M., Schermelleh, L., Leonhardt, H., Keough, R., Gonda, T.J., Imhof, A., Eick, D., Langst, G. et al. (2012) Myb-binding protein 1a (Mybbp1a) regulates levels and processing of pre-ribosomal RNA. J. Biol. Chem., 287, 24365-24377
36. Stefanovsky, V., Langlois, F., Gagnon-Kugler, T., Rothblum, L.I. and Moss, T. (2006) Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol. Cell, 21, 629-639
37. Tolstorukov, M.Y., Goldman, J.A., Gilbert, C., Ogryzko, V., Kingston, R.E. and Park, P.J. (2012) Histone variant H2A.Bbd is associated with active transcription and mRNA processing in human cells. Mol. Cell, 47, 596-607