A two-step mechanism for epigenetic specification of centromere identity and function

Nature Cell Biology

Volumn 15, Issue 9, 2013, Pages 1056-1066

  Fachinetti, Daniele ^a   Diego Folco, H ^a,d   Nechemia Arbely, Yael ^a   Valente, Luis P ^b   Nguyen, Kristen ^a   Wong, Alex J ^a   Zhu, Quan ^c   Holland, Andrew J ^a,e   Desai, Arshad ^a   Jansen, Lars E T ^b   Cleveland, Don W ^a  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

^b Instituto Gulbenkian de Ciência ^*  (Portugal)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; CENTROMERE PROTEIN B; HISTONE H3; NUCLEAR PROTEIN; PROTEIN CENP C; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL SPECIFICITY; CENTROMERE; CENTROMERE TARGETING DOMAIN; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; EPIGENETICS; GENE TARGETING; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION;

ADENOVIRIDAE; AUTOANTIGENS; CENTROMERE; CENTROMERE PROTEIN B; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; EPIGENESIS, GENETIC; EPITHELIAL CELLS; GENETIC VECTORS; HISTONES; HUMANS; PROTEIN STRUCTURE, TERTIARY; RETINA; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SIGNAL TRANSDUCTION;

EUKARYOTA; SCHIZOSACCHAROMYCETACEAE;

EID: 84883667139     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2805     Document Type: Article

References (67)

1. Palmer, D. K., O'Day, K., Wener, M. H., Andrews, B. S. & Margolis, R. L. A 17-kD centromere protein (CENP-A) copuri-es with nucleosome core particles and with histones. J. Cell Biol. 104, 805-815 (1987).
2. Earnshaw, W. C. & Roth-eld, N. Identi-cation of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91, 313-321 (1985).
3. Cleveland, D. W., Mao, Y. & Sullivan, K. F. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112, 407-421 (2003).
4. Karpen, G. H. & Allshire, R. C. The case for epigenetic effects on centromere identity and function. Trends Genet. 13, 489-496 (1997).
5. Ekwall, K. Epigenetic control of centromere behavior. Annu. Rev. Genet. 41, 63-81 (2007).
6. Du Sart, D. et al. A functional neo-centromere formed through activation of a latent human centromere and consisting of non-alpha-satellite DNA. Nat. Genet. 16, 144-153 (1997).
7. Ventura, M. et al. Recurrent sites for new centromere seeding. Genome Res. 14, 1696-1703 (2004).
8. Amor, D. J. et al. Human centromere repositioning ̀in progress'. Proc. Natl Acad. Sci. USA 101, 6542-6547 (2004).
9. Warburton, P. E. Chromosomal dynamics of human neocentromere formation. Chromosome Res. 12, 617-626 (2004).
10. Depinet, T. W. et al. Characterization of neo-centromeres in marker chromosomes lacking detectable alpha-satellite DNA. Hum. Mol. Genet. 6, 1195-1204 (1997).
11. Warburton, P. E. et al. Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr. Biol. 7, 901-904 (1997).
12. Jansen, L. E., Black, B. E., Foltz, D. R. & Cleveland, D. W. Propagation of centromeric chromatin requires exit from mitosis. J. Cell Biol. 176, 795-805 (2007).
13. Schuh, M., Lehner, C. F. & Heidmann, S. Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 17, 237-243 (2007).
14. Mellone, B. G. et al. Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genet. 7, e1002068 (2011).
15. Dimitriadis, E. K., Weber, C., Gill, R. K., Diekmann, S. & Dalal, Y. Tetrameric organization of vertebrate centromeric nucleosomes. Proc. Natl Acad. Sci. USA 107, 20317-20322 (2010).
16. Furuyama, T. & Henikoff, S. Centromeric nucleosomes induce positive DNA supercoils. Cell 138, 104-113 (2009).
17. Krassovsky, K., Henikoff, J. G. & Henikoff, S. Tripartite organization of centromeric chromatin in budding yeast. Proc. Natl Acad. Sci. USA 109, 243-248 (2012).
18. Mizuguchi, G., Xiao, H., Wisniewski, J., Smith, M. M. & Wu, C. Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-speci-c nucleosomes. Cell 129, 1153-1164 (2007).
19. Conde e Silva, N. et al. CENP-A-containing nucleosomes: easier disassembly versus exclusive centromeric localization. J. Mol. Biol. 370, 555-573 (2007).
20. Camahort, R. et al. Cse4 is part of an octameric nucleosome in budding yeast. Mol. Cell 35, 794-805 (2009).
21. Sekulic, N., Bassett, E. A., Rogers, D. J. & Black, B. E. The structure of (CENP-A-H4)(2) reveals physical features that mark centromeres. Nature 467, 347-351 (2010).
22. Tachiwana, H. et al. Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476, 232-235 (2011).
23. Zhang, W., Colmenares, S. U. & Karpen, G. H. Assembly of Drosophila centromeric nucleosomes requires CID dimerization. Mol. Cell 45, 263-269 (2012).
24. Black, B. E. & Cleveland, D. W. Epigenetic centromere propagation and the nature of CENP-a nucleosomes. Cell 144, 471-479 (2011).
25. Regnier, V. et al. CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol. Cell Biol. 25, 3967-3981 (2005).
26. Liu, S. T., Rattner, J. B., Jablonski, S. A. & Yen, T. J. Mapping the assembly pathways that specify formation of the trilaminar kinetochore plates in human cells. J. Cell Biol. 175, 41-53 (2006).
27. Black, B. E. et al. Centromere identity maintained by nucleosomes assembled with histone H3 containing the CENP-A targeting domain. Mol. Cell 25, 309-322 (2007).
28. Fujita, Y. et al. Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev. Cell 12, 17-30 (2007).
29. Guse, A., Carroll, C. W., Moree, B., Fuller, C. J. & Straight, A. F. In vitro centromere and kinetochore assembly on de-ned chromatin templates. Nature 477, 354-358 (2011).
30. Barnhart, M. C. et al. HJURP is a CENP-A chromatin assembly factor suf-cient to form a functional de novo kinetochore. J. Cell Biol. 194, 229-243 (2011).
31. Mendiburo, M. J., Padeken, J., Fulop, S., Schepers, A. & Heun, P. Drosophila CENH3 is suf-cient for centromere formation. Science 334, 686-690 (2011).
32. Gascoigne, K. E. et al. Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 145, 410-422 (2011).
33. Hori, T., Shang, W. H., Takeuchi, K. & Fukagawa, T. The CCAN recruits CENP-A to the centromere and forms the structural core for kinetochore assembly. J. Cell Biol. 200, 45-60 (2013).
34. Russell, D. W. & Hirata, R. K. Human gene targeting by viral vectors. Nat. Genet. 18, 325-330 (1998).
35. Berdougo, E., Terret, M. E. & Jallepalli, P. V. Functional dissection of mitotic regulators through gene targeting in human somatic cells. Methods Mol. Biol. 545, 21-37 (2009).
36. Black, B. E. et al. Structural determinants for generating centromeric chromatin. Nature 430, 578-582 (2004).
37. Carroll, C. W., Milks, K. J. & Straight, A. F. Dual recognition of CENP-A nucleosomes is required for centromere assembly. J. Cell Biol. 189, 1143-1155 (2010).
38. Carroll, C. W., Silva, M. C., Godek, K. M., Jansen, L. E. & Straight, A. F. Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat. Cell Biol. 11, 896-902 (2009).
39. Foltz, D. R. et al. The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 8, 458-469 (2006).
40. Nishino, T. et al. CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell 148, 487-501 (2012).
41. Hori, T. et al. CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135, 1039-1052 (2008).
42. Okada, M. et al. The CENP-H-I complex is required for the ef-cient incorporation of newly synthesized CENP-A into centromeres. Nat. Cell Biol. 8, 446-457 (2006).
43. Cheeseman, I. M., Chappie, J. S., Wilson-Kubalek, E. M. & Desai, A. The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127, 983-997 (2006).
44. Masumoto, H., Masukata, H., Muro, Y., Nozaki, N. & Okazaki, T. A human centromere antigen (CENP-B) interacts with a short speci-c sequence in alphoid DNA, a human centromeric satellite. J. Cell Biol. 109, 1963-1973 (1989).
45. Dunleavy, E. M. et al. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137, 485-497 (2009).
46. Foltz, D. R. et al. Centromere-speci-c assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137, 472-484 (2009).
47. Bassett, E. A. et al. HJURP uses distinct CENP-A surfaces to recognize and to stabilize CENP-A/histone H4 for centromere assembly. Dev. Cell 22, 749-762 (2012).
48. Hu, H. et al. Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP. Genes Dev. 25, 901-906 (2011).
49. Panchenko, T. et al. Replacement of histone H3 with CENP-A directs global nucleosome array condensation and loosening of nucleosome superhelical termini. Proc. Natl Acad. Sci. USA 108, 16588-16593 (2011).
50. Allshire, R. C. & Karpen, G. H. Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9, 923-937 (2008).
51. Castillo, A. G. et al. Plasticity of-ssion yeast CENP-A chromatin driven by relative levels of histone H3 and H4. PLoS Genet. 3, 1264-1274 (2007).
52. Torras-Llort, M., Moreno-Moreno, O. & Azorin, F. Focus on the centre: the role of chromatin on the regulation of centromere identity and function. EMBO J. 28, 2337-2348 (2009).
53. Ribeiro, S. A. et al. A super-resolution map of the vertebrate kinetochore. Proc. Natl Acad. Sci. USA 107, 10484-10489 (2010).
54. Black, B. E., Brock, M. A., Bedard, S., Woods, V. L. Jr & Cleveland, D. W. An epigenetic mark generated by the incorporation of CENP-A into centromeric nucleosomes. Proc. Natl Acad. Sci. USA 104, 5008-5013 (2007).
55. Trazzi, S. et al. The C-terminal domain of CENP-C displays multiple and critical functions for mammalian centromere formation. PLoS ONE 4, e5832 (2009).
56. Sugimoto, K., Yata, H., Muro, Y. & Himeno, M. Human centromere protein C (CENP-C) is a DNA-binding protein which possesses a novel DNA-binding motif. J. Biochem. 116, 877-881 (1994).
57. Suzuki, N. et al. CENP-B interacts with CENP-C domains containing Mif2 regions responsible for centromere localization. J. Biol. Chem. 279, 5934-5946 (2004).
58. Okada, T. et al. CENP-B controls centromere formation depending on the chromatin context. Cell 131, 1287-1300 (2007).
59. Sullivan, B. A. & Karpen, G. H. Centromeric chromatin exhibits a histone modi-cation pattern that is distinct from both euchromatin and heterochromatin. Nat. Struct. Mol. Biol. 11, 1076-1083 (2004).
60. Hasson, D. et al. The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat. Struct. Mol. Biol. 20, 687-695 (2013).
61. Tanaka, Y. et al. Human centromere protein B induces translational positioning of nucleosomes on alpha-satellite sequences. J. Biol. Chem. 280, 41609-41618 (2005).
62. Okamoto, Y., Nakano, M., Ohzeki, J., Larionov, V. & Masumoto, H. A minimal CENP-A core is required for nucleation and maintenance of a functional human centromere. EMBO J. 26, 1279-1291 (2007).
63. Sakuno, T., Tada, K. & Watanabe, Y. Kinetochore geometry de-ned by cohesion within the centromere. Nature 458, 852-858 (2009).
64. Shah, J. V. et al. Dynamics of centromere and kinetochore proteins; implications for checkpoint signaling and silencing. Curr. Biol. 14, 942-952 (2004).
65. Bodor, D. L., Rodriguez, M. G., Moreno, N. & Jansen, L. E. Analysis of protein turnover by quantitative SNAP-based pulse-chase imaging. Curr. Protoc. Cell Biol. Chapter 8, Unit8 8 (2012).
66. Moreno, S., Klar, A. & Nurse, P. Molecular genetic analysis of-ssion yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823 (1991).
67. Folco, H. D., Pidoux, A. L., Urano, T. & Allshire, R. C. Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319, 94-97 (2008).