Cell-cycle-dependent structural transitions in the human CENP-A nucleosome in vivo

Cell

Volumn 150, Issue 2, 2012, Pages 317-326

  Bui, Minh ^a   Dimitriadis, Emilios K ^b   Hoischen, Christian ^d   An, Eunkyung ^c   Quénet, Delphine ^a   Giebe, Sindy ^d   Nita Lazar, Aleksandra ^c   Diekmann, Stephan ^d   Dalal, Yamini ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; CHAPERONE; HISTONE H4; TETRAMER;

ARTICLE; CELL CYCLE; CENTROMERE; CHROMATIN; CHROMOSOME REPLICATION; CONTROLLED STUDY; EPIGENETICS; HUMAN; HUMAN CELL; IN VIVO STUDY; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE;

EUKARYOTA;

EID: 84864193502     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.05.035     Document Type: Article

References (55)

1. R.C. Allshire, and G.H. Karpen Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat. Rev. Genet. 9 2008 923 937 (Pubitemid 50329068)
2. E. An, X. Lu, J. Flippin, J.M. Devaney, B. Halligan, E.P. Hoffman, N. Strunnikova, K. Csaky, and Y. Hathout Secreted proteome profiling in human RPE cell cultures derived from donors with age related macular degeneration and age matched healthy donors J. Proteome Res. 5 2006 2599 2610 (Pubitemid 44595162)
3. S. Ando, H. Yang, N. Nozaki, T. Okazaki, and K. Yoda CENP-A, -B, and -C chromatin complex that contains the I-type alpha-satellite array constitutes the prekinetochore in HeLa cells Mol. Cell. Biol. 22 2002 2229 2241 (Pubitemid 34224629)
4. L. Bintu, M. Kopaczynska, C. Hodges, L. Lubkowska, M. Kashlev, and C. Bustamante The elongation rate of RNA polymerase determines the fate of transcribed nucleosomes Nat. Struct. Mol. Biol. 18 2011 1394 1399
5. B.E. Black, and D.W. Cleveland Epigenetic centromere propagation and the nature of CENP-a nucleosomes Cell 144 2011 471 479
6. B.E. Black, D.R. Foltz, S. Chakravarthy, K. Luger, V.L. Woods Jr., and D.W. Cleveland Structural determinants for generating centromeric chromatin Nature 430 2004 578 582 (Pubitemid 38998633)
7. K. Bloom, and A. Joglekar Towards building a chromosome segregation machine Nature 463 2010 446 456
8. R. Camahort, M. Shivaraju, M. Mattingly, B. Li, S. Nakanishi, D. Zhu, A. Shilatifard, J.L. Workman, and J.L. Gerton Cse4 is part of an octameric nucleosome in budding yeast Mol. Cell 35 2009 794 805
9. C.W. Carroll, K.J. Milks, and A.F. Straight Dual recognition of CENP-A nucleosomes is required for centromere assembly J. Cell Biol. 189 2010 1143 1155
10. N. Conde e Silva, B.E. Black, A. Sivolob, J. Filipski, D.W. Cleveland, and A. Prunell CENP-A-containing nucleosomes: easier disassembly versus exclusive centromeric localization J. Mol. Biol. 370 2007 555 573 (Pubitemid 46898434)
11. Y. Dalal, and M. Bui Down the rabbit hole of centromere assembly and dynamics Curr. Opin. Cell Biol. 22 2010 392 402
12. Y. Dalal, T.J. Fleury, A. Cioffi, and A. Stein Long-range oscillation in a periodic DNA sequence motif may influence nucleosome array formation Nucleic Acids Res. 33 2005 934 945 (Pubitemid 41430514)
13. Y. Dalal, H. Wang, S. Lindsay, and S. Henikoff Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells PLoS Biol. 5 2007 e218
14. M.L. Dechassa, K. Wyns, M. Li, M.A. Hall, M.D. Wang, and K. Luger Structure and Scm3-mediated assembly of budding yeast centromeric nucleosomes Nat Commun 2 2011 313
15. E.K. Dimitriadis, C. Weber, R.K. Gill, S. Diekmann, and Y. Dalal Tetrameric organization of vertebrate centromeric nucleosomes Proc. Natl. Acad. Sci. USA 107 2010 20317 20322
16. E.M. Dunleavy, D. Roche, H. Tagami, N. Lacoste, D. Ray-Gallet, Y. Nakamura, Y. Daigo, Y. Nakatani, and G. Almouzni-Pettinotti HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres Cell 137 2009 485 497
17. 1 phase Nucleus 2 2011 146 157
18. D.R. Foltz, L.E. Jansen, A.O. Bailey, J.R. Yates 3rd, E.A. Bassett, S. Wood, B.E. Black, and D.W. Cleveland Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP Cell 137 2009 472 484
19. T. Furuyama, and S. Henikoff Centromeric nucleosomes induce positive DNA supercoils Cell 138 2009 104 113
20. D. Hellwig, S. Emmerth, T. Ulbricht, V. Döring, C. Hoischen, R. Martin, C.P. Samora, A.D. McAinsh, C.W. Carroll, and A.F. Straight Dynamics of CENP-N kinetochore binding during the cell cycle J. Cell Sci. 124 2011 3871 3883
21. D. Hellwig, S. Munch, S. Orthaus, C. Hoischen, P. Hemmerich, and S. Diekmann Live-cell imaging reveals sustained centromere binding of CENP-T via CENP-A and CENP-B J. Biophotonics 1 2008 245 254
22. P. Hemmerich, S. Weidtkamp-Peters, C. Hoischen, L. Schmiedeberg, I. Erliandri, and S. Diekmann Dynamics of inner kinetochore assembly and maintenance in living cells J. Cell Biol. 180 2008 1101 1114 (Pubitemid 351468468)
23. S. Henikoff, and T. Furuyama Epigenetic inheritance of centromeres Cold Spring Harb. Symp. Quant. Biol. 75 2010 51 60
24. H. Hu, Y. Liu, M. Wang, J. Fang, H. Huang, N. Yang, Y. Li, J. Wang, X. Yao, and Y. Shi Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP Genes Dev. 25 2011 901 906
25. L.E. Jansen, B.E. Black, D.R. Foltz, and D.W. Cleveland Propagation of centromeric chromatin requires exit from mitosis J. Cell Biol. 176 2007 795 805 (Pubitemid 46425540)
26. P. Kalitsis, K.J. Fowler, E. Earle, B. Griffiths, E. Howman, A.J. Newson, and K.H. Choo Partially functional Cenpa-GFP fusion protein causes increased chromosome missegregation and apoptosis during mouse embryogenesis Chromosome Res. 11 2003 345 357 (Pubitemid 36871844)
27. O.J. Marshall, A.T. Marshall, and K.H. Choo Three-dimensional localization of CENP-A suggests a complex higher order structure of centromeric chromatin J. Cell Biol. 183 2008 1193 1202
28. G. Mizuguchi, H. Xiao, J. Wisniewski, M.M. Smith, and C. Wu Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes Cell 129 2007 1153 1164 (Pubitemid 46900852)
29. H. Neumann, S.M. Hancock, R. Buning, A. Routh, L. Chapman, J. Somers, T. Owen-Hughes, J. van Noort, D. Rhodes, and J.W. Chin A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation Mol. Cell 36 2009 153 163
30. M. Perpelescu, N. Nozaki, C. Obuse, H. Yang, and K. Yoda Active establishment of centromeric CENP-A chromatin by RSF complex J. Cell Biol. 185 2009 397 407
31. A.V. Probst, E. Dunleavy, and G. Almouzni Epigenetic inheritance during the cell cycle Nat. Rev. Mol. Cell Biol. 10 2009 192 206
32. M. Schuh, C.F. Lehner, and S. Heidmann Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase Curr. Biol. 17 2007 237 243 (Pubitemid 46186017)
33. E. Screpanti, A. De Antoni, G.M. Alushin, A. Petrovic, T. Melis, E. Nogales, and A. Musacchio Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore Curr. Biol. 21 2011 391 398
34. N. Sekulic, E.A. Bassett, D.J. Rogers, and B.E. Black The structure of (CENP-A-H4)(2) reveals physical features that mark centromeres Nature 467 2010 347 351
35. R.D. Shelby, K. Monier, and K.F. Sullivan Chromatin assembly at kinetochores is uncoupled from DNA replication J. Cell Biol. 151 2000 1113 1118
36. M. Shuaib, K. Ouararhni, S. Dimitrov, and A. Hamiche HJURP binds CENP-A via a highly conserved N-terminal domain and mediates its deposition at centromeres Proc. Natl. Acad. Sci. USA 107 2010 1349 1354
37. M.S. Shukla, S.H. Syed, F. Montel, C. Faivre-Moskalenko, J. Bednar, A. Travers, D. Angelov, and S. Dimitrov Remosomes: RSC generated non-mobilized particles with approximately 180 bp DNA loosely associated with the histone octamer Proc. Natl. Acad. Sci. USA 107 2010 1936 1941
38. M. Simon, J.A. North, J.C. Shimko, R.A. Forties, M.B. Ferdinand, M. Manohar, M. Zhang, R. Fishel, J.J. Ottesen, and M.G. Poirier Histone fold modifications control nucleosome unwrapping and disassembly Proc. Natl. Acad. Sci. USA 108 2011 12711 12716
39. B.A. Sullivan, and G.H. Karpen Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin Nat. Struct. Mol. Biol. 11 2004 1076 1083 (Pubitemid 39453336)
40. D.L. Tabb, W.H. McDonald, and J.R. Yates 3rd DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics J. Proteome Res. 1 2002 21 26
41. H. Tachiwana, W. Kagawa, T. Shiga, A. Osakabe, Y. Miya, K. Saito, Y. Hayashi-Takanaka, T. Oda, M. Sato, and S.Y. Park Crystal structure of the human centromeric nucleosome containing CENP-A Nature 476 2011 232 235
42. S.E. Torigoe, D.L. Urwin, H. Ishii, D.E. Smith, and J.T. Kadonaga Identification of a rapidly formed nonnucleosomal histone-DNA intermediate that is converted into chromatin by ACF Mol. Cell 43 2011 638 648
43. S. Trazzi, G. Perini, R. Bernardoni, M. Zoli, J.C. Reese, A. Musacchio, and G. Della Valle The C-terminal domain of CENP-C displays multiple and critical functions for mammalian centromere formation PLoS ONE 4 2009 e5832
44. L.T. Vassilev, C. Tovar, S. Chen, D. Knezevic, X. Zhao, H. Sun, D.C. Heimbrook, and L. Chen Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1 Proc. Natl. Acad. Sci. USA 103 2006 10660 10665 (Pubitemid 44078033)
45. X. Wan, R.P. O'Quinn, H.L. Pierce, A.P. Joglekar, W.E. Gall, J.G. DeLuca, C.W. Carroll, S.T. Liu, T.J. Yen, and B.F. McEwen Protein architecture of the human kinetochore microtubule attachment site Cell 137 2009 672 684
46. H. Wang, Y. Dalal, S. Henikoff, and S. Lindsay Single-epitope recognition imaging of native chromatin Epigenetics Chromatin 1 2008 10
47. H. Xiao, G. Mizuguchi, J. Wisniewski, Y. Huang, D. Wei, and C. Wu Nonhistone Scm3 binds to AT-rich DNA to organize atypical centromeric nucleosome of budding yeast Mol. Cell 43 2011 369 380
48. W. Zhang, S.U. Colmenares, and G.H. Karpen Assembly of Drosophila centromeric nucleosomes requires CID dimerization Mol. Cell 45 2012 263 269 Published online Dec 28, 2011
49. J. Zlatanova, and K. van Holde Single-molecule biology: what is it and how does it work? Mol. Cell 24 2006 317 329 (Pubitemid 44647909)
50. Chen, Y., Mills, J.D., and Periasamy, A. (2003). Protein localization in living cells and tissues using FRET and FLIM. Differentiation 71, 528-541. (Pubitemid 38091095)
51. Elder, A.D., Kaminski, C.F., and Frank, J.H. (2009). phi2FLIM: a technique for alias-free frequency domain fluorescence lifetime imaging. Opt. Express 17, 23181-23203.
52. Jares-Erijman, E.A., and Jovin, T.M. (2003). FRET imaging. Nat. Biotechnol. 21, 1387-1395. (Pubitemid 37356626)
53. Nagy, P., Bene, L., Balázs, M., Hyun, W.C., Lockett, S.J., Chiang, N.Y., Waldman, F., Feuerstein, B.G., Damjanovich, S., and Szöllosi, J. (1998). EGF-induced redistribution of erbB2 on breast tumor cells: flow and image cytometric energy transfer measurements. Cytometry 32, 120-131. (Pubitemid 28246759)
54. Orthaus, S., Biskup, C., Hoffmann, B., Hoischen, C., Ohndorf, S., Benndorf, K., and Diekmann, S. (2008). Assembly of the inner kinetochore proteins CENP-A and CENP-B in living human cells. ChemBioChem 9, 77-92.
55. Orthaus, S., Klement, K., Happel, N., Hoischen, C., and Diekmann, S. (2009). Linker histone H1 is present in centromeric chromatin of living human cells next to inner kinetochore proteins. Nucleic Acids Res. 37, 3391-3406.