Identification of the post-translational modifications present in centromeric chromatin

Molecular and Cellular Proteomics

Volumn 15, Issue 3, 2016, Pages 918-931

  Bailey, Aaron O ^a,e   Panchenko, Tanya ^b,f   Shabanowitz, Jeffrey ^c   Lehman, Stephanie M ^c   Bai, Dina L ^c   Hunt, Donald F ^c   Black, Ben E ^b   Foltz, Daniel R ^a,d  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e Thermo Fisher Scientific   (United States)

^f ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; HISTONE H3; HISTONE H4; AUTOANTIGEN; DNA BINDING PROTEIN; HISTONE; HOLLIDAY JUNCTION RECOGNIZING PROTEIN, HUMAN; LYSINE; NONHISTONE PROTEIN; NUCLEOSOME; SERINE;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CENTROMERE; CHROMATIN; ELECTROSPRAY; FEMALE; HELA CELL LINE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN PROCESSING; CELL CYCLE; ELECTROSPRAY MASS SPECTROMETRY; METABOLISM; METHYLATION;

AUTOANTIGENS; CELL CYCLE; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; HELA CELLS; HISTONES; HUMANS; LYSINE; METHYLATION; NUCLEOSOMES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SERINE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 84962567856     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.053710     Document Type: Article

References (53)

1. Stellfox, M. E., Bailey, A. O., and Foltz, D. R. (2013) Putting CENP-A in its place. Cell Mol. Life Sci. 70, 387-406
2. Wevrick, R., and Willard, H. F. (1989) Long-range organization of tandem arrays of alpha satellite DNA at the centromeres of human chromosomes: high-frequency array-length polymorphism and meiotic stability. Proc. Natl. Acad. Sci. U. S. A. 86, 9394-9398
3. Barnhart, M. C., Kuich, P. H., Stellfox, M. E., Ward, J. A., Bassett, E. A., Black, B. E., and Foltz, D. R. (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J. Cell Biol. 194, 229-243
4. Dunleavy, E. M., Almouzni, G., and Karpen, G. H. H3.3 is deposited at centromeres in S phase as a placeholder for newly assembled CENP-A in G (1) phase. Nucleus 2, 146-157
5. Foltz, D. R., Jansen, L. E., Bailey, A. O., Yates, J. R., 3rd, 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
6. Moree, B., Meyer, C. B., Fuller, C. J., and Straight, A. F. CENP-C recruits M18BP1 to centromeres to promote CENP-A chromatin assembly. J. Cell Biol. 194, 855-871
7. Dambacher, S., Deng, W., Hahn, M., Sadic, D., Frohlich, J., Nuber, A., Hoischen, C., Diekmann, S., Leonhardt, H., and Schotta, G. (2012) CENP-C facilitates the recruitment of M18BP1 to centromeric chromatin. Nucleus 3, 101-110
8. Wang, J., Liu, X., Dou, Z., Chen, L., Jiang, H., Fu, C., Fu, G., Liu, D., Zhang, J., Zhu, T., Fang, J., Zang, J., Cheng, J., Teng, M., Ding, X., and Yao, X. (2014) Mitotic Regulator Mis18beta Interacts with and Specifies the Centromeric Assembly of Molecular Chaperone Holliday Junction Recognition Protein (HJURP). J. Biol. Chem. 289, 8326-8336
9. Partridge, J. F., Borgstrom, B., and Allshire, R. C. (2000) Distinct protein interaction domains and protein spreading in a complex centromere. Genes Dev. 14, 783-791
10. Blower, M. D., and Karpen, G. H. (2001) The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat. Cell Biol. 3, 730-739
11. Schalch, T., Job, G., Noffsinger, V. J., Shanker, S., Kuscu, C., Joshua-Tor, L., and Partridge, J. F. (2009) High-affinity binding of Chp1 chromodomain to K9 methylated histone H3 is required to establish centromeric heterochromatin. Mol. Cell. 34, 36-46
12. Blower, M. D., Sullivan, B. A., and Karpen, G. H. (2002) Conserved organization of centromeric chromatin in flies and humans. Dev. Cell 2, 319-330
13. Bergmann, J. H., Rodriguez, M. G., Martins, N. M., Kimura, H., Kelly, D. A., Masumoto, H., Larionov, V., Jansen, L. E., and Earnshaw, W. C. (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J. 30, 328-340
14. Sullivan, B. A., and Karpen, G. H. (2004) Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat. Struct. Mol. Biol. 11, 1076-1083
15. Alonso, A., Hasson, D., Cheung, F., and Warburton, P. E. (2010) A paucity of heterochromatin at functional human neocentromeres. Epigenetics Chromatin 3, 6
16. Bodor, D. L., Mata, J. F., Sergeev, M., David, A. F., Salimian, K. J., Panchenko, T., Cleveland, D. W., Black, B. E., Shah, J. V., and Jansen, L. E. (2014) The quantitative architecture of centromeric chromatin. Elife 3, e02137
17. Shelby, R. D., Vafa, O., and Sullivan, K. F. (1997) Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites. J. Cell Biol. 136, 501-513
18. Foltz, D. R., Jansen, L. E., Black, B. E., Bailey, A. O., Yates, J. R., 3rd, and Cleveland, D. W. (2006) The human CENP-A centromeric nucleosomeassociated complex. Nat. Cell Biol. 8, 458-469
19. Padeganeh, A., Ryan, J., Boisvert, J., Ladouceur, A. M., Dorn, J. F., and Maddox, P. S. (2013) Octameric CENP-A nucleosomes are present at human centromeres throughout the cell cycle. Curr. Biol. 23, 764-769
20. Lacoste, N., Woolfe, A., Tachiwana, H., Garea, A. V., Barth, T., Cantaloube, S., Kurumizaka, H., Imhof, A., and Almouzni, G. (2014) Mislocalization of the centromeric histone variant CenH3/CENP-A in human cells depends on the chaperone DAXX. Mol. Cell 53, 631-644
21. Bodor, D. L., Valente, L. P., Mata, J. F., Black, B. E., and Jansen, L. E. (2013) Assembly in G1 phase and long-term stability are unique intrinsic features of CENP-A nucleosomes. Mol. Biol. Cell 24, 923-932
22. Falk, S. J., Guo, L. Y., Sekulic, N., Smoak, E. M., Mani, T., Logsdon, G. A., Gupta, K., Jansen, L. E., Van Duyne, G. D., Vinogradov, S. A., Lampson, M. A., and Black, B. E. (2015) Chromosomes. CENP-C reshapes and stabilizes CENP-A nucleosomes at the centromere. Science 348, 699-703
23. Hasson, D., Panchenko, T., Salimian, K. J., Salman, M. U., Sekulic, N., Alonso, A., Warburton, P. E., and Black, B. E. (2013) The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat. Structural Mol. Biol. 20, 687-695
24. Hori, T., Amano, M., Suzuki, A., Backer, C. B., Welburn, J. P., Dong, Y., McEwen, B. F., Shang, W. H., Suzuki, E., Okawa, K., Cheeseman, I. M., and Fukagawa, T. (2008) CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135, 1039-1052
25. Black, B. E., and Cleveland, D. W. (2011) Epigenetic centromere propagation and the nature of CENP-A nucleosomes. Cell 144, 471-479
26. Ribeiro, S. A., Vagnarelli, P., Dong, Y., Hori, T., McEwen, B. F., Fukagawa, T., Flors, C., and Earnshaw, W. C. A super-resolution map of the vertebrate kinetochore. Proc. Natl. Acad. Sci. U. S. A. 107, 10484-10489
27. Lam, A. L., Boivin, C. D., Bonney, C. F., Rudd, M. K., and Sullivan, B. A. (2006) Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc. Natl. Acad. Sci. U. S. A. 103, 4186-4191
28. Hori, T., Shang, W. H., Toyoda, A., Misu, S., Monma, N., Ikeo, K., Molina, O., Vargiu, G., Fujiyama, A., Kimura, H., Earnshaw, W. C., and Fukagawa, T. (2014) Histone H4 Lys 20 monomethylation of the CENP-A nucleosome is essential for kinetochore assembly. Developmental cell 29, 740-749
29. Cardinale, S., Bergmann, J. H., Kelly, D., Nakano, M., Valdivia, M. M., Kimura, H., Masumoto, H., Larionov, V., and Earnshaw, W. C. (2009) Hierarchical inactivation of a synthetic human kinetochore by a chromatin modifier. Mol. Biol. Cell 20, 4194-4204
30. Nakano, M., Cardinale, S., Noskov, V. N., Gassmann, R., Vagnarelli, P., Kandels-Lewis, S., Larionov, V., Earnshaw, W. C., and Masumoto, H. (2008) Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev. Cell 14, 507-522
31. Bailey, A. O., Panchenko, T., Sathyan, K. M., Petkowski, J. J., Pai, P. J., Bai, D. L., Russell, D. H., Macara, I. G., Shabanowitz, J., Hunt, D. F., Black, B. E., and Foltz, D. R. (2013) Posttranslational modification of CENP-A influences the conformation of centromeric chromatin. Proc. Natl. Acad. Sci. U. S. A. 110, 11827-11832
32. Shechter, D., Dormann, H. L., Allis, C. D., and Hake, S. B. (2007) Extraction, purification and analysis of histones. Nat. Protoc. 2, 1445-1457
33. Geer, L. Y., Markey, S. P., Kowalak, J. A., Wagner, L., Xu, M., Maynard, D. M., Yang, X., Shi, W., and Bryant, S. H. (2004) Open mass spectrometry search algorithm. J. Proteome Res. 3, 958-964
34. Young, N. L., DiMaggio, P. A., Plazas-Mayorca, M. D., Baliban, R. C., Floudas, C. A., and Garcia, B. A. (2009) High throughput characterization of combinatorial histone codes. Mol. Cell. Proteomics 8, 2266-2284
35. Bergmann, J. H., Martins, N. M., Larionov, V., Masumoto, H., and Earnshaw, W. C. (2012) HACking the centromere chromatin code: insights from human artificial chromosomes. Chromosome Res. 20, 505-519
36. 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. U. S. A. 107, 1349-1354
37. Hu, H., Liu, Y., Wang, M., Fang, J., Huang, H., Yang, N., Li, Y., Wang, J., Yao, X., Shi, Y., Li, G., and Xu, R. M. (2011) Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP. Genes Dev. 25, 901-906
38. Bassett, E. A., DeNizio, J., Barnhart-Dailey, M. C., Panchenko, T., Sekulic, N., Rogers, D. J., Foltz, D. R., and Black, B. E. HJURP uses distinct CENP-A surfaces to recognize and to stabilize CENP-A/histone H4 for centromere assembly. Dev. Cell 22, 749-762
39. Yu, Z., Zhou, X., Wang, W., Deng, W., Fang, J., Hu, H., Wang, Z., Li, S., Cui, L., Shen, J., Zhai, L., Peng, S., Wong, J., Dong, S., Yuan, Z., Ou, G., Zhang, X., Xu, P., Lou, J., Yang, N., Chen, P., Xu, R. M., and Li, G. (2015) Dynamic phosphorylation of CENP-A at Ser68 orchestrates its cellcycle-dependent deposition at centromeres. Dev. Cell 32, 68-81
40. Logsdon, G. A., Barrey, E. J., Bassett, E. A., DeNizio, J. E., Guo, L. Y., Panchenko, T., Dawicki-McKenna, J. M., Heun, P., and Black, B. E. (2015) Both tails and the centromere targeting domain of CENP-A are required for centromere establishment. J. Cell Biol. 208, 521-531
41. Dunleavy, E. M., Roche, D., Tagami, H., Lacoste, N., Ray-Gallet, D., Nakamura, Y., Daigo, Y., Nakatani, Y., and Almouzni-Pettinotti, G. (2009) HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137, 485-497
42. Jansen, L. E., Black, B. E., Foltz, D. R., and Cleveland, D. W. (2007) Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176, 795-805
43. Silva, M. C., Bodor, D. L., Stellfox, M. E., Martins, N. M., Hochegger, H., Foltz, D. R., and Jansen, L. E. (2012) Cdk activity couples epigenetic centromere inheritance to cell cycle progression. Dev. Cell 22, 52-63
44. McKinley, K. L., and Cheeseman, I. M. (2014) Polo-like kinase 1 licenses CENP-A deposition at centromeres. Cell 158, 397-411
45. Dephoure, N., Zhou, C., Villen, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J., and Gygi, S. P. (2008) A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U. S. A. 105, 10762-10767
46. Mayya, V., Lundgren, D. H., Hwang, S. I., Rezaul, K., Wu, L., Eng, J. K., Rodionov, V., and Han, D. K. (2009) Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci. Signal 2, ra46
47. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M. L., Jensen, L. J., Gnad, F., Cox, J., Jensen, T. S., Nigg, E. A., Brunak, S., and Mann, M. (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3, ra3
48. Muller, S., Montes de Oca, R., Lacoste, N., Dingli, F., Loew, D., and Almouzni, G. (2014) Phosphorylation and DNA binding of HJURP determine its centromeric recruitment and function in CenH3 (CENP-A) loading. Cell Reports 8, 190-203
49. Luhn, P., Wang, H., Marcus, A. I., and Fu, H. (2007) Identification of FAKTS as a novel 14-3-3-associated nuclear protein. Proteins 67, 479-489
50. Hole, K., Van Damme, P., Dalva, M., Aksnes, H., Glomnes, N., Varhaug, J. E., Lillehaug, J. R., Gevaert, K., and Arnesen, T. (2011) The human N-alpha-acetyltransferase 40 (hNaa40p/hNatD) is conserved from yeast and N-terminally acetylates histones H2A and H4. PLoS ONE 6, e24713
51. Chang, L., Loranger, S. S., Mizzen, C., Ernst, S. G., Allis, C. D., and Annunziato, A. T. (1997) Histones in transit: cytosolic histone complexes and diacetylation of H4 during nucleosome assembly in human cells. Biochemistry 36, 469-480
52. Lu, X., Simon, M. D., Chodaparambil, J. V., Hansen, J. C., Shokat, K. M., and Luger, K. (2008) The effect of H3K79 dimethylation and H4K20 trimethylation on nucleosome and chromatin structure. Nat. Structural Mol. Biol. 15, 1122-1124
53. Yang, H., and Mizzen, C. A. (2009) The multiple facets of histone H4-lysine 20 methylation. Biochem. Cell Biol. 87, 151-161