HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore

Journal of Cell Biology

Volumn 194, Issue 2, 2011, Pages 229-243

  Barnhart, Meghan C ^a   Kuich, P Henning J L ^a   Stellfox, Madison E ^a   Ward, Jared A ^a   Bassett, Emily A ^b   Black, Ben E ^b   Foltz, Daniel R ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; CHROMATIN ASSEMBLY FACTOR 1; LAC REPRESSOR; NDC80 COMPLEX; PROTEIN HJURP; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CENTROMERE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; EPIGENETICS; GENE LOCUS; HUMAN; HUMAN CELL; IN VITRO STUDY; LACTOSE OPERON; MICROTUBULE ASSEMBLY; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MICROARRAY;

ANIMALS; AUTOANTIGENS; CELLS, CULTURED; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; KINETOCHORES; MICE; NIH 3T3 CELLS;

EUKARYOTA;

EID: 79961113679     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201012017     Document Type: Article

References (64)

1. Allshire, R.C., and G.H. Karpen. 2008. Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9:923-937.
2. Bergmann, J.H., M.G. Rodríguez, N.M. Martins, H. Kimura, D.A. Kelly, H. Masumoto, V. Larionov, L.E. Jansen, and W.C. Earnshaw. 2011. Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J. 30:328-340.
3. Bernad, R., P. Sánchez, T. Rivera, M. Rodríguez-Corsino, E. Boyarchuk, I. Vassias, D. Ray-Gallet, A. Arnaoutov, M. Dasso, G. Almouzni, and A. Losada. 2011. Xenopus HJURP and condensin II are required for CENP-A assembly. J. Cell Biol. 192:569-582.
4. Black, B.E., D.R. Foltz, S. Chakravarthy, K. Luger, V.L. Woods Jr., and D.W. Cleveland. 2004. Structural determinants for generating centromeric chromatin. Nature. 430:578-582.
5. Black, B.E., M.A. Brock, S. Bédard, V.L. Woods Jr., and D.W. Cleveland. 2007. An epigenetic mark generated by the incorporation of CENP-A into centromeric nucleosomes. Proc. Natl. Acad. Sci. USA. 104:5008-5013.
6. Brinkley, B.R., and J. Cartwright Jr. 1975. Cold-labile and cold-stable microtubules in the mitotic spindle of mammalian cells. Ann. NY Acad. Sci. 253:428-439.
7. Camahort, R., B. Li, L. Florens, S.K. Swanson, M.P. Washburn, and J.L. Gerton. 2007. Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol. Cell. 26:853-865.
8. Camahort, R., M. Shivaraju, M. Mattingly, B. Li, S. Nakanishi, D. Zhu, A. Shilatifard, J.L. Workman, and J.L. Gerton. 2009. Cse4 is part of an octameric nucleosome in budding yeast. Mol. Cell. 35:794-805.
9. Carroll, C.W., M.C. Silva, K.M. Godek, L.E. Jansen, and A.F. Straight. 2009. Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat. Cell Biol. 11:896-902.
10. Carroll, C.W., K.J. Milks, and A.F. Straight. 2010. Dual recognition of CENP-A nucleosomes is required for centromere assembly. J. Cell Biol. 189:1143-1155.
11. Cheeseman, I.M., and A. Desai. 2008. Molecular architecture of the kinetochoremicrotubule interface. Nat. Rev. Mol. Cell Biol. 9:33-46.
12. Cleveland, D.W., Y. Mao, and K.F. Sullivan. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell. 112:407-421.
13. Dalal, Y., H. Wang, S. Lindsay, and S. Henikoff. 2007. Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol. 5:e218.
14. Dimitriadis, E.K., C. Weber, R.K. Gill, S. Diekmann, and Y. Dalal. 2010. Tetrameric organization of vertebrate centromeric nucleosomes. Proc. Natl. Acad. Sci. USA. 107:20317-20322.
15. Drané, P., K. Ouararhni, A. Depaux, M. Shuaib, and A. Hamiche. 2010. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 24:1253-1265.
16. Dunleavy, E.M., D. Roche, H. Tagami, N. Lacoste, D. Ray-Gallet, Y. Nakamura, Y. Daigo, Y. Nakatani, and G. Almouzni-Pettinotti. 2009. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell. 137:485-497.
17. Foltz, D.R., L.E. Jansen, B.E. Black, A.O. Bailey, J.R. Yates III, and D.W. Cleveland. 2006. The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 8:458-469.
18. Foltz, D.R., L.E. Jansen, A.O. Bailey, J.R. Yates III, E.A. Bassett, S. Wood, B.E. Black, and D.W. Cleveland. 2009. Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell. 137:472-484.
19. Frehlick, L.J., J.M. Eirín-López, and J. Ausió. 2007. New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. Bioessays. 29:49-59.
20. Fujita, Y., T. Hayashi, T. Kiyomitsu, Y. Toyoda, A. Kokubu, C. Obuse, and M. Yanagida. 2007. Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev. Cell. 12:17-30.
21. Furuyama, T., and S. Henikoff. 2009. Centromeric nucleosomes induce positive DNA supercoils. Cell. 138:104-113.
22. Fyodorov, D.V., and J.T. Kadonaga. 2003. Chromatin assembly in vitro with purified recombinant ACF and NAP-1. Methods Enzymol. 371:499-515.
23. Gascoigne, K.E., K. Takeuchi, A. Suzuki, T. Hori, T. Fukagawa, and I.M. Cheeseman. 2011. Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell. 145:410-422.
24. Goldberg, A.D., L.A. Banaszynski, K.M. Noh, P.W. Lewis, S.J. Elsaesser, S. Stadler, S. Dewell, M. Law, X. Guo, X. Li, et al. 2010. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell. 140:678-691.
25. Hayashi, T., Y. Fujita, O. Iwasaki, Y. Adachi, K. Takahashi, and M. Yanagida. 2004. Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell. 118:715-729.
26. Heun, P., S. Erhardt, M.D. Blower, S. Weiss, A.D. Skora, and G.H. Karpen. 2006. Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev. Cell. 10:303-315.
27. Hori, T., M. Amano, A. Suzuki, C.B. Backer, J.P. Welburn, Y. Dong, B.F. McEwen, W.H. Shang, E. Suzuki, K. Okawa, et al. 2008. CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell. 135:1039-1052.
28. Janicki, S.M., T. Tsukamoto, S.E. Salghetti, W.P. Tansey, R. Sachidanandam, K.V. Prasanth, T. Ried, Y. Shav-Tal, E. Bertrand, R.H. Singer, and D.L. Spector. 2004. From silencing to gene expression: real-time analysis in single cells. Cell. 116:683-698.
29. Jansen, L.E., B.E. Black, D.R. Foltz, and D.W. Cleveland. 2007. Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176:795-805.
30. Lagana, A., J.F. Dorn, V. De Rop, A.M. Ladouceur, A.S. Maddox, and P.S. Maddox. 2010. A small GTPase molecular switch regulates epigenetic centromere maintenance by stabilizing newly incorporated CENP-A. Nat. Cell Biol. 12:1186-1193.
31. Liu, S.T., J.B. Rattner, S.A. Jablonski, and T.J. Yen. 2006. Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J. Cell Biol. 175:41-53.
32. Luger, K., T.J. Rechsteiner, and T.J. Richmond. 1999. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 304:3-19.
33. Lusser, A., and J.T. Kadonaga. 2004. Strategies for the reconstitution of chromatin. Nat. Methods. 1:19-26.
34. Maddox, P.S., F. Hyndman, J. Monen, K. Oegema, and A. Desai. 2007. Functional genomics identifies a Myb domain-containing protein family required for assembly of CENP-A chromatin. J. Cell Biol. 176:757-763.
35. Marshall, O.J., A.C. Chueh, L.H. Wong, and K.H. Choo. 2008. Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am. J. Hum. Genet. 82:261-282.
36. Mizuguchi, G., X. Shen, J. Landry, W.H. Wu, S. Sen, and C. Wu. 2004. ATPdriven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science. 303:343-348.
37. Mizuguchi, G., H. Xiao, J. Wisniewski, M.M. Smith, and C. Wu. 2007. Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell. 129:1153-1164.
38. Moggs, J.G., P. Grandi, J.P. Quivy, Z.O. Jónsson, U. Hübscher, P.B. Becker, and G. Almouzni. 2000. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol. Cell. Biol. 20:1206-1218.
39. Musacchio, A., and E.D. Salmon. 2007. The spindle-assembly checkpoint in space and time. Nat. Rev. Mol. Cell Biol. 8:379-393.
40. Nakano, M., S. Cardinale, V.N. Noskov, R. Gassmann, P. Vagnarelli, S. Kandels-Lewis, V. Larionov, W.C. Earnshaw, and H. Masumoto. 2008. Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev. Cell. 14:507-522.
41. Obuse, C., H. Yang, N. Nozaki, S. Goto, T. Okazaki, and K. Yoda. 2004. Proteomics analysis of the centromere complex from HeLa interphase cells: UV-damaged DNA binding protein 1 (DDB-1) is a component of the CEN-complex, while BMI-1 is transiently co-localized with the centromeric region in interphase. Genes Cells. 9:105-120.
42. Okada, M., K. Okawa, T. Isobe, and T. Fukagawa. 2009. CENP-H-containing complex facilitates centromere deposition of CENP-A in cooperation with FACT and CHD1. Mol. Biol. Cell. 20:3986-3995.
43. Okuwaki, M., K. Matsumoto, M. Tsujimoto, and K. Nagata. 2001. Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett. 506:272-276.
44. Park, Y.J., and K. Luger. 2006. Structure and function of nucleosome assembly proteins. Biochem. Cell Biol. 84:549-558.
45. Perpelescu, M., N. Nozaki, C. Obuse, H. Yang, and K. Yoda. 2009. Active establishment of centromeric CENP-A chromatin by RSF complex. J. Cell Biol. 185:397-407.
46. Peterson, S., R. Danowit, A. Wunsch, and V. Jackson. 2007. NAP1 catalyzes the formation of either positive or negative supercoils on DNA on basis of the dimer-tetramer equilibrium of histones H3/H4. Biochemistry. 46:8634-8646.
47. Pidoux, A.L., E.S. Choi, J.K. Abbott, X. Liu, A. Kagansky, A.G. Castillo, G.L. Hamilton, W. Richardson, J. Rappsilber, X. He, and R.C. Allshire. 2009. Fission yeast Scm3: A CENP-A receptor required for integrity of subkinetochore chromatin. Mol. Cell. 33:299-311.
48. Podhraski, V., B. Campo-Fernandez, H. Wörle, P. Piatti, H. Niederegger, G. Böck, D.V. Fyodorov, and A. Lusser. 2010. CenH3/CID incorporation is not dependent on the chromatin assembly factor CHD1 in Drosophila. PLoS ONE. 5:e10120.
49. Ransom, M., B.K. Dennehey, and J.K. Tyler. 2010. Chaperoning histones during DNA replication and repair. Cell. 140:183-195.
50. Régnier, V., P. Vagnarelli, T. Fukagawa, T. Zerjal, E. Burns, D. Trouche, W. Earnshaw, and W. Brown. 2005. CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol. Cell. Biol. 25:3967-3981.
51. Sanchez-Pulido, L., A.L. Pidoux, C.P. Ponting, and R.C. Allshire. 2009. Common ancestry of the CENP-A chaperones Scm3 and HJURP. Cell. 137:1173-1174.
52. Schueler, M.G., and B.A. Sullivan. 2006. Structural and functional dynamics of human centromeric chromatin. Annu. Rev. Genomics Hum. Genet. 7:301-313.
53. Sekulic, N., E.A. Bassett, D.J. Rogers, and B.E. Black. 2010. The structure of (CENP-A-H4)(2) reveals physical features that mark centromeres. Nature. 467:347-351.
54. Shaiu, W.L., and T.S. Hsieh. 1998. Targeting to transcriptionally active loci by the hydrophilic N-terminal domain of Drosophila DNA topoisomerase I. Mol. Cell. Biol. 18:4358-4367.
55. Shibahara, K., and B. Stillman. 1999. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell. 96:575-585.
56. Shivaraju, M., R. Camahort, M. Mattingly, and J.L. Gerton. 2011. Scm3 is a centromeric nucleosome assembly factor. J. Biol. Chem. 286:12016-12023.
57. Shuaib, M., K. Ouararhni, S. Dimitrov, and A. Hamiche. 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.
58. Soutoglou, E., J.F. Dorn, K. Sengupta, M. Jasin, A. Nussenzweig, T. Ried, G. Danuser, and T. Misteli. 2007. Positional stability of single doublestrand breaks in mammalian cells. Nat. Cell Biol. 9:675-682.
59. Stoler, S., K. Rogers, S. Weitze, L. Morey, M. Fitzgerald-Hayes, and R.E. Baker. 2007. Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc. Natl. Acad. Sci. USA. 104:10571-10576.
60. Tagami, H., D. Ray-Gallet, G. Almouzni, and Y. Nakatani. 2004. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell. 116:51-61.
61. Van Hooser, A.A., I.I. Ouspenski, H.C. Gregson, D.A. Starr, T.J. Yen, M.L. Goldberg, K. Yokomori, W.C. Earnshaw, K.F. Sullivan, and B.R. Brinkley. 2001. Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J. Cell Sci. 114:3529-3542.
62. Williams, J.S., T. Hayashi, M. Yanagida, and P. Russell. 2009. Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol. Cell. 33:287-298.
63. Wong, L.H., J.D. McGhie, M. Sim, M.A. Anderson, S. Ahn, R.D. Hannan, A.J. George, K.A. Morgan, J.R. Mann, and K.H. Choo. 2010. ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res. 20:351-360.
64. Yoda, K., S. Ando, S. Morishita, K. Houmura, K. Hashimoto, K. Takeyasu, and T. Okazaki. 2000. Human centromere protein A (CENP-A) can replace histone H3 in nucleosome reconstitution in vitro. Proc. Natl. Acad. Sci. USA. 97:7266-7271.