Centromeric histone variant CENP-A represses acetylation-dependent chromatin transcription that is relieved by histone chaperone NPM1

Journal of Biochemistry

Volumn 156, Issue 4, 2014, Pages 221-227

  Shandilya, Jayasha ^a   Senapati, Parijat ^a   Hans, Fabienne ^b   Menoni, Hervé ^c   Bouvet, Philippe ^d   Dimitrov, Stefan ^b   Angelov, Dimitar ^c   Kundu, Tapas K ^a  

^a JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

^b UNIV GRENOBLE ALPES   (France)

^c UNIVERSITÉ DE LYON   (France)

^d Laboratoire Joliot Curie   (France)

Author keywords

Acetylation; CENP A; Histone chaperone; NPM1; Transcription

Indexed keywords

ACETYL COENZYME A; ADENOSINE TRIPHOSPHATE; CENTROMERE PROTEIN A; DNA FRAGMENT; NUCLEOPHOSMIN; AUTOANTIGEN; CHROMATIN; HISTONE; NONHISTONE PROTEIN; NUCLEAR PROTEIN;

ARTICLE; CELL MOTION; CHROMATIN; CONTROLLED STUDY; DNA PROBE; GEL MOBILITY SHIFT ASSAY; HISTONE ACETYLATION; IN VITRO STUDY; NONHUMAN; NUCLEOSOME; PROTEIN ANALYSIS; TRANSCRIPTION REGULATION; WESTERN BLOTTING; ACETYLATION; ANIMAL; CENTROMERE; GENETICS; METABOLISM; XENOPUS LAEVIS;

ACETYLATION; ANIMALS; AUTOANTIGENS; CENTROMERE; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; HISTONES; NUCLEAR PROTEINS; XENOPUS LAEVIS;

EID: 84933045174     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvu034     Document Type: Article

References (32)

1. McKittrick, E., Gafken, P.R., Ahmad, K., and Henikoff, S. (2004) Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl Acad. Sci. USA. 101, 1525-1530
2. Chadwick, B.P., Valley, C.M., and Willard, H.F. (2001) Histone variant macroH2A contains two distinct macrochromatin domains capable of directing macroH2A to the inactive X chromosome. Nucleic Acids Res. 29, 2699-2705
3. Nakano, M., Okamoto, Y., Ohzeki, J., and Masumoto, H. (2003) Epigenetic assembly of centromeric chromatin at ectopic alpha-satellite sites on human chromosomes. J. Cell. Sci. 116, 4021-4034
4. Yan, H., Ito, H., Nobuta, K., Ouyang, S., Jin, W., Tian, S., Lu, C, Venu, R.C., Wang, G.L., Green, P.J., Wing, R.A., Buell, C.R., Meyers, B.C., and Jiang, J. (2006) Genomic and genetic characterization of rice Cen3 reveals extensive transcription and evolutionary implications of a complex centromere. Plant Cell 18, 2123-2133
5. Wong, N.C., Wong, L.H., Quach, J.M., Canham, P., Craig, J.M., Song, J.Z., Clark, S.J., and Choo, K.H. (2006) Permissive transcriptional activity at the centromere through pockets of DNA hypomethylation. PLoS Genet. 2, e17
6. Chan, F.L., Marshall, O.J., Saffery, R., Kim, B.W., Earle, E., Choo, K.H.A., and Wong, L.H. (2012) Active transcription and essential role of RNA polymerase II at the centromere during mitosis. Proc. Natl Acad. Sci. 109, 1979-1984
7. Ohkuni, K. and Kitagawa, K. (2012) Endogenous transcription at the centromere facilitates centromere activity in budding yeast. Curr. Biol. 21, 1695-1703
8. Bergmann, J.H., Jakubsche, J.N., Martins, N.M., Kagansky, A., Nakano, M., Kimura, H., Kelly, D.A., Turner, B.M., Masumoto, H., Larionov, V. et al. (2012) Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function. J. Cell. Sci. 125, 411-421
9. Yoda, K, Ando, S., Morishita, S., Houmura, K, Hashimoto, K, Takeyasu, K, and Okazaki, T. (2000) Human centromere protein A (CENP-A) can replace histone H3 in nucleosome reconstitution in vitro. Proc. Natl Acad. Sci. USA. 97, 7266-7271
10. Black, B.E., Foltz, D.R., Chakravarthy, S., Luger, K, Woods, V.L., and Cleveland, D.W. (2004) Structural determinants for generating centromeric chromatin. Nature 430, 578-582
11. Black, B.E., Brock, M.A., Bédard, S., Woods, V.L., and Cleveland, D.W. (2007) An epigenetic mark generated by the incorporation of CENP-A into centromeric nucleosomes. Proc. Natl Acad. Sci. USA. 104, 5008-5013
12. Conde e Silva, N, Black, B.E., Sivolob, A., Filipski, J., Cleveland, D.W., and Prunell, A. (2007) CENP-A-containing nucleosomes: easier disassembly versus exclusive centromeric localization. J. Mol. Biol. 370, 555-573
13. Dalal, Y., Wang, H, Lindsay, S., and Henikoff, S. (2007) Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol. 5, e218
14. Camahort, R., Shivaraju, M., Mattingly, M., Li, B., Nakanishi, S., Zhu, D., Shilatifard, A., Workman, J.L., and Gerton, J.L. (2009) Cse4 is part of an octameric nucleosome in budding yeast. Mol. Cell 35, 794-805
15. Tachiwana, H, Kagawa, W., Shiga, T., Osakabe, A., Miya, Y., Saito, K, Hayashi-Takanaka, Y., Oda, T., Sato, M., Park, S.Y., Kimura, H., and Kurumizaka, H. (2011) Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476, 232-235
16. Furuyama, T., Dalal, Y., and Henikoff, S. (2006) Chaperone-mediated assembly of centromeric chromatin in vitro. Proc. Natl Acad. Sci. USA. 103, 6172-6177
17. Hayashi, T., Fujita, Y., Iwasaki, O., Adachi, Y., Takahashi, K, and Yanagida, M. (2004) Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 118, 715-729
18. Foltz, D.R., Jansen, L.E., Bailey, A.O., Yates, J.R., Bassett, E.A., Wood, S., Black, B.E., and Cleveland, D.W. (2009) Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137, 472-484
19. Shuaib, M., Ouararhni, K, Dimitrov, S., and Hamiche, A. (2010) HJURP binds CENP-A via a highly conserved N-terminal domain and mediates its deposition at centromeres. Proc. Natl Acad. Sci. USA. 107, 1349-1354
20. Foltz, D.R., Jansen, L.E., Black, B.E., Bailey, A.O., Yates, J.R., and Cleveland, D.W. (2006) The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 8, 458-469
21. Ekwall, K. (2007) Epigenetic control of centromere behavior. Annu. Rev. Genet. 41, 63-81
22. Lowary, P.T. and Widom, J. (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19-42
23. Luger, K, Rechsteiner, T.J., and Richmond, T.J. (1999) Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119, 1-16
24. Tanaka, Y., Tawaramoto-Sasanuma, M., Kawaguchi, S., Ohta, T., Yoda, K, Kurumizaka, H., and Yokoyama, S. (2004) Expression and purification of recombinant human histones. Methods 33, 3-11
25. Peterson, C.L. and Côté, J. (2004) Cellular machineries for chromosomal DNA repair. Genes Dev. 18, 602-616
26. Swaminathan, V., Kishore, A.H., Febitha, K.K., and Kundu, T.K. (2005) Human histone chaperone nucleophosmin enhances acetylation-dependent chromatin transcription. Mol. Cell. Biol. 25, 7534-7545
27. Hayes, J.J. and Lee, K.M. (1997) In vitro reconstitution and analysis of mononucleosomes containing defined DNAs and proteins. Methods 12, 2-9
28. Doyen, CM, Montel, F., Gautier, T., Menoni, H., Claudet, C, Delacour-Larose, M., Angelov, D., Hamiche, A., Bednar, J., Faivre-Moskalenko, C, Bouvet, P., and Dimitrov, S. (2006) Dissection of the unusual structural and functional properties of the variant H2A.Bbd nucleosome. EMBO J. 25, 4234-4244
29. Kundu, T., Palhan, V., Wang, Z., An, W., Cole, P., and Roeder, R. (2000) Activator-dependent transcription from chromatin in vitro involving targeted histone acetylation by p300. Mol. Cell 6, 551-561
30. Tomonaga, T., Matsushita, K, Yamaguchi, S., Oohashi, T., Shimada, H, Ochiai, T., Yoda, K, and Nomura, F. (2003) Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res. 63, 3511-3516
31. Li, Y., Zhu, Z., Zhang, S., Yu, D., Yu, H., Liu, L., Cao, X., Wang, L., Gao, H, and Zhu, M. (2011) ShRNAtargeted centromere protein A inhibits hepatocellular carcinoma growth. PLoS One 6, e17794
32. Yun, J.P., Miao, J., Chen, G.G., Tian, Q.H., Zhang, C.Q., Xiang, J., Fu, J., and Lai, P.B. (2007) Increased expression of nucleophosmin/B23 in hepatocellular carcinoma and correlation with clinicopathological parameters. Br. J. Cancer 96, 477-484