Mitotic regulator Mis18β interacts with and specifies the centromeric assembly of molecular chaperone holliday junction recognition protein (HJURP)

Journal of Biological Chemistry

Volumn 289, Issue 12, 2014, Pages 8326-8336

  Wang, Jianyu ^a   Liu, Xing ^a,c   Dou, Zhen ^a   Chen, Liang ^b   Jiang, Hao ^a   Fu, Chuanhai ^a   Fu, Guosheng ^a   Liu, Dan ^a   Zhang, Jiancun ^a,d   Zhu, Tongge ^a,c   Fang, Jingwen ^a   Zang, Jianye ^a   Cheng, Jinke ^e   Teng, Maikun ^a   Ding, Xia ^b   Yao, Xuebiao ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b BEIJING UNIVERSITY OF CHINESE MEDICINE   (China)

^c MOREHOUSE SCHOOL OF MEDICINE   (United States)

^d GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

^e SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINS;

DAUGHTER CELLS; HISTONE H3; HOLLIDAY JUNCTIONS; MITOTIC REGULATORS; MOLECULAR CHAPERONES; MOLECULAR MECHANISM; RNA INTERFERENCE;

CHROMOSOMES;

CHAPERONE; HOLIDAY JUNCTION RECOGNITION PROTEIN; MIS18BETA PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CENTROMERE; COMPLEX FORMATION; CONTROLLED STUDY; MITOSIS; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE;

CELL DIVISION; CENTROMERES; CHROMATIN STRUCTURE; HISTONE CHAPERONE; PHOSPHORYLATION;

CELL LINE; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; HUMANS; MITOSIS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION MAPS;

EID: 84896916856     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.529958     Document Type: Article

References (49)

1. Black, B. E., Jansen, L. E., Foltz, D. R., and Cleveland, D. W. (2010) Centromere identity, function, and epigenetic propagation across cell divisions. Cold Spring Harb. Symp. Quant. Biol. 75, 403-418
2. Cleveland, D. W., Mao, Y., and Sullivan, K. F. (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112, 407-421 (Pubitemid 36263076)
3. Allshire, R. C., and Karpen, G. H. (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9, 923-937 (Pubitemid 50329068)
4. Morris, C. A., and Moazed, D. (2007) Centromere assembly and propagation. Cell 128, 647-650 (Pubitemid 46273576)
5. Oegema, K., Desai, A., Rybina, S., Kirkham, M., and Hyman, A. A. (2001) Functional analysis of kinetochore assembly in Caenorhabditis elegans. J. Cell Biol. 153, 1209-1226
6. Palmer, D. K., O'Day, K., Wener, M. H., Andrews, B. S., and Margolis, R. L. (1987) A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J. Cell Biol. 104, 805-815 (Pubitemid 17068653)
7. Meluh, P. B., Yang, P., Glowczewski, L., Koshland, D., and Smith, M. M. (1998) Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94, 607-613 (Pubitemid 28427579)
8. Henikoff, S., Ahmad, K., Platero, J. S., and van Steensel, B. (2000) Heterochromatic deposition of centromeric histone H3-like proteins. Proc. Natl. Acad. Sci. U.S.A. 97, 716-721 (Pubitemid 30070375)
9. Black, B. E., Brock, M. A., Bédard, S., Woods, V. L., Jr., and Cleveland, D. W. (2007) An epigenetic mark generated by the incorporation of CENP-A into centromeric nucleosomes. Proc. Natl. Acad. Sci. U.S.A. 104, 5008-5013 (Pubitemid 47186167)
10. 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 nucleosome-associated complex. Nat. Cell Biol. 8, 458-469
11. Guse, A., Carroll, C. W., Moree, B., Fuller, C. J., and Straight, A. F. (2011) In vitro centromere and kinetochore assembly on defined chromatin templates. Nature 477, 354-358
12. Liu, S. T., Rattner, J. B., Jablonski, S. A., and Yen, T. J. (2006) Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J. Cell Biol. 175, 41-53 (Pubitemid 44537197)
13. Régnier, V., Vagnarelli, P., Fukagawa, T., Zerjal, T., Burns, E., Trouche, D., Earnshaw, W., and Brown, W. (2005) CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol. Cell. Biol. 25, 3967-3981 (Pubitemid 40617647)
14. Goshima, G., Kiyomitsu, T., Yoda, K., and Yanagida, M. (2003) Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J. Cell Biol. 160, 25-39 (Pubitemid 36091714)
15. Howman, E. V., Fowler, K. J., Newson, A. J., Redward, S., MacDonald, A. C., Kalitsis, P., and Choo, K. H. (2000) Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc. Natl. Acad. Sci. U.S.A. 97, 1148-1153 (Pubitemid 30080827)
16. Amor, D. J., Bentley, K., Ryan, J., Perry, J., Wong, L., Slater, H., and Choo, K. H. (2004) Human centromere repositioning "in progress". Proc. Natl. Acad. Sci. U.S.A. 101, 6542-6547
17. Fachinetti, D., Folco, H. D., Nechemia-Arbely, Y., Valente, L. P., Nguyen, K., Wong, A. J., Zhu, Q., Holland, A. J., Desai, A., Jansen, L. E., and Cleveland, D. W. (2013) A two-step mechanism for epigenetic specification of centromere identity and function. Nat. Cell Biol. 15, 1056-1066
18. 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 (Pubitemid 46425540)
19. 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 (Pubitemid 39221731)
20. Fujita, Y., Hayashi, T., Kiyomitsu, T., Toyoda, Y., Kokubu, A., Obuse, C., and Yanagida, M. (2007) Priming of centromere for CENP-A recruitment by human hMis18α, hMis18β and M18BP1. Dev. Cell 12, 17-30 (Pubitemid 46002597)
21. Maddox, P. S., Hyndman, F., Monen, J., Oegema, K., and Desai, A. (2007) Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J. Cell Biol. 176, 757-763 (Pubitemid 46425535)
22. 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
23. Carroll, C. W., Milks, K. J., and Straight, A. F. (2010) Dual recognition of CENP-A nucleosomes is required for centromere assembly. J. Cell Biol. 189, 1143-1155
24. Carroll, C. W., Silva, M. C., Godek, K. M., Jansen, L. E., and Straight, A. F. (2009) Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat. Cell Biol. 11, 896-902
25. 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
26. 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
27. 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
28. Perpelescu, M., Nozaki, N., Obuse, C., Yang, H., and Yoda, K. (2009) Active establishment of centromeric CENP-A chromatin by RSF complex. J. Cell Biol. 185, 397-407
29. Camahort, R., Li, B., Florens, L., Swanson, S. K., Washburn, M. P., and Gerton, J. L. (2007) Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol. Cell 26, 853-865 (Pubitemid 46924838)
30. Mizuguchi, G., Xiao, H., Wisniewski, J., Smith, M. M., and Wu, C. (2007) Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129, 1153-1164 (Pubitemid 46900852)
31. Stoler, S., Rogers, K., Weitze, S., Morey, L., Fitzgerald-Hayes, M., and Baker, R. E. (2007) Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc. Natl. Acad. Sci. U.S.A. 104, 10571-10576 (Pubitemid 47185706)
32. Williams, J. S., Hayashi, T., Yanagida, M., and Russell, P. (2009) Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol. Cell 33, 287-298
33. Pidoux, A. L., Choi, E. S., Abbott, J. K., Liu, X., Kagansky, A., Castillo, A. G., Hamilton, G. L., Richardson, W., Rappsilber, J., He, X., and Allshire, R. C. (2009) Fission yeast Scm3. A CENP-A receptor required for integrity of subkinetochore chromatin. Mol. Cell 33, 299-311
34. Sanchez-Pulido, L., Pidoux, A. L., Ponting, C. P., and Allshire, R. C. (2009) Common ancestry of the CENP-A chaperones Scm3 and HJURP. Cell 137, 1173-1174
35. 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
36. Bassett, E. A., DeNizio, J., Barnhart-Dailey, M. C., Panchenko, T., Sekulic, N., Rogers, D. J., Foltz, D. R., and Black, B. E. (2012) HJURP uses distinct CENP-A surfaces to recognize and to stabilize CENP-A/histone H4 for centromere assembly. Dev. Cell 22, 749-762
37. Liu, D., Ding, X., Du, J., Cai, X., Huang, Y., Ward, T., Shaw, A., Yang, Y., Hu, R., Jin, C., and Yao, X. (2007) Human NUF2 interacts with centromere-associated protein E and is essential for a stable spindle microtubule-kinetochore attachment. J. Biol. Chem. 282, 21415-21424 (Pubitemid 47099950)
38. Zhu, M., Wang, F., Yan, F., Yao, P. Y., Du, J., Gao, X., Wang, X., Wu, Q., Ward, T., Li, J., Kioko, S., Hu, R., Xie, W., Ding, X., and Yao, X. (2008) Septin 7 interacts with centromere-associated protein E and is required for its kinetochore localization. J. Biol. Chem. 283, 18916-18925
39. Xia, P., Wang, Z., Liu, X., Wu, B., Wang, J., Ward, T., Zhang, L., Ding, X., Gibbons, G., Shi, Y., and Yao, X. (2012) EB1 acetylation by P300/CBP-associated factor (PCAF) ensures accurate kinetochore-microtubule interactions in mitosis. Proc. Natl. Acad. Sci. U.S.A. 109, 16564-16569
40. Zasadzińska, E., Barnhart-Dailey, M. C., Kuich, P. H., and Foltz, D. R. (2013) Dimerization of the CENP-A assembly factor HJURP is required for centromeric nucleosome deposition. EMBO J. 32, 2113-2124
41. Moree, B., Meyer, C. B., Fuller, C. J., and Straight, A. F. (2011) CENP-C recruits M18BP1 to centromeres to promote CENP-A chromatin assembly. J. Cell Biol. 194, 855-871
42. 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
43. Dephoure, N., Zhou, C., Villén, 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
44. Dambacher, S., Deng, W., Hahn, M., Sadic, D., Fröhlich, 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
45. Chu, Y., Yao, P. Y., Wang, W., Wang, D., Wang, Z., Zhang, L., Huang, Y., Ke, Y., Ding, X., and Yao, X. (2011) Aurora B kinase activation requires survivin priming phosphorylation by PLK1. J Mol. Cell. Biol. 3, 260-267
46. Chu, L., Zhu, T., Liu, X., Yu, R., Bacanamwo, M., Dou, Z., Chu, Y., Zou, H., Gibbons, G. H., Wang, D., Ding, X., and Yao, X. (2012) SUV39H1 orchestrates temporal dynamics of centromeric methylation essential for faithful chromosome segregation in mitosis. J Mol. Cell. Biol. 4, 331-340
47. Kim, I. S., Lee, M., Park, K. C., Jeon, Y., Park, J. H., Hwang, E. J., Jeon, T. I., Ko, S., Lee, H., Baek, S. H., and Kim, K. I. (2012) Roles of Mis18α in epigenetic regulation of centromeric chromatin and CENP-A loading. Mol. Cell. 46, 260-273
48. Rea, S., Eisenhaber, F., O'Carroll, D., Strahl, B. D., Sun, Z. W., Schmid, M., Opravil, S., Mechtler, K., Ponting, C. P., Allis, C. D., and Jenuwein, T. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406, 593-599 (Pubitemid 30641039)
49. Tao, Y., Jin, C., Li, X., Qi, S., Chu, L., Niu, L., Yao, X., and Teng, M. (2012) The structure of the FANCM-MHF complex reveals physical features for functional assembly. Nat. Commun. 3, 782-791