Centromeres: Unique chromatin structures that drive chromosome segregation

Nature Reviews Molecular Cell Biology

Volumn 12, Issue 5, 2011, Pages 320-332

  Verdaasdonk, Jolien S ^a   Bloom, Kerry ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CENTROMERE PROTEIN A; HISTONE H2AZ; HISTONE H3;

CENTROMERE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CHROMOSOME SEGREGATION; ENTROPY; EPIGENETICS; HISTONE MODIFICATION; HUMAN; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN VARIANT; REVIEW;

ANIMALS; CENTROMERE; CHROMATIN; CHROMOSOME SEGREGATION; HISTONES; HUMANS; KINETOCHORES; MITOTIC SPINDLE APPARATUS; MODELS, GENETIC;

EID: 79955413557     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3107     Document Type: Review

References (177)

1. Moore, L.-L. & Roth, M.-B. HCP4, a CENPClike protein in Caenorhabditis elegans, is required for resolution of sister centromeres. J.-Cell Biol. 153, 1199-1208 (2001).
2. Sullivan, B.-A. & Karpen, G.-H. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nature Struct. Mol. Biol. 11, 1076-1083 (2004).
3. Cheeseman, I.-M. & Desai, A. Molecular architecture of the kinetochore-microtubule interface. Nature Rev. Mol. Cell Biol. 9, 33-46 (2008).
4. Bouck, D.-C., Joglekar, A.-P. & Bloom, K.-S. Design features of a mitotic spindle: balancing tension and compression at a single microtubule kinetochore interface in budding yeast. Annu. Rev. Genet. 42, 335-359 (2008).
5. Santaguida, S. & Musacchio, A. The life and miracles of kinetochores. EMBO J. 28, 2511-2531 (2009).
6. Fukagawa, T. & De Wulf, P. in The Kinetochore - From Molecular Discoveries to Cancer Therapy (eds De-Wulf, P. & Earnshaw, W.-C.) 133-191 (Springer Science + Business Media, New York, 2009).
7. Przewloka, M.-R. & Glover, D.-M. The kinetochore and the centromere: a working long distance relationship. Annu. Rev. Genet. 43, 439-465 (2009).
8. Clarke, L. & Carbon, J. Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287, 504-509 (1980). (Pubitemid 11232847)
9. Clarke, L. & Carbon, J. Genomic substitutions of centromeres in Saccharomyces cerevisiae. Nature 305, 23-28 (1983). (Pubitemid 13041970)
10. Fitzgerald-Hayes, M., Clarke, L. & Carbon, J. Nucleotide sequence comparisons and functional analysis of yeast centromere DNAs. Cell 29, 235-244 (1982). (Pubitemid 12027685)
11. Hieter, P. et al. Functional selection and analysis of yeast centromeric DNA. Cell 42, 913-921 (1985).
12. McGrew, J., Diehl, B. & Fitzgerald-Hayes, M. Single base-pair mutations in centromere element III cause aberrant chromosome segregation in Saccharomyces cerevisiae. Mol. Cell. Biol. 6, 530-538 (1986). (Pubitemid 16158128)
13. Sullivan, B.-A. in The Kinetochore - From Molecular Discoveries to Cancer Therapy (eds De Wulf, P. & Earnshaw, W.-C.) 45-76 (Springer Science + Business Media, New York, 2009).
14. Joglekar, A.-P. et al. Molecular architecture of the kinetochore- microtubule attachment site is conserved between point and regional centromeres. J.-Cell Biol. 181, 587-594 (2008).
15. Chikashige, Y. et al. Composite motifs and repeat symmetry in S.-pombe centromeres: direct analysis by integration of NotI restriction sites. Cell 57, 739-751 (1989). (Pubitemid 19149814)
16. Clarke, L., Amstutz, H., Fishel, B. & Carbon, J. Analysis of centromeric DNA in the fission yeast Schizosaccharomyces pombe. Proc. Natl Acad. Sci. USA 83, 8253-8257 (1986). (Pubitemid 17182479)
17. Baum, M., Ngan, V.-K. & Clarke, L. The centromeric Ktype repeat and the central core are together sufficient to establish a functional Schizosaccharomyces pombe centromere. Mol. Biol. Cell 5, 747-761 (1994). (Pubitemid 24254345)
18. Pidoux, A.-L. & Allshire, R.-C. Kinetochore and heterochromatin domains of the fission yeast centromere. Chromosome Res. 12, 521-534 (2004).
19. Sanyal, K., Baum, M. & Carbon, J. Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc. Natl Acad. Sci. USA 101, 11374-11379 (2004). (Pubitemid 39038354)
20. Centola, M. & Carbon, J. Cloning and characterization of centromeric DNA from Neurospora crassa. Mol. Cell. Biol. 14, 1510-1519 (1994). (Pubitemid 24036601)
21. Copenhaver, G.-P. et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286, 2468-2474 (1999).
22. Sun, X., Le, H.-D., Wahlstrom, J.-M. & Karpen, G.-H. Sequence analysis of a functional Drosophila centromere. Genome Res. 13, 182-194 (2003).
23. Schueler, M.-G., Higgins, A.-W., Rudd, M.-K., Gustashaw, K. & Willard, H.-F. Genomic and genetic definition of a functional human centromere. Science 294, 109-115 (2001). (Pubitemid 32952957)
24. Maio, J.-J. DNA strand reassociation and polyribonucleotide binding in the African green monkey, Cercopithecus aethiops. J.-Mol. Biol. 56, 579-595 (1971).
25. Choo, K.-H. Domain organization at the centromere and neocentromere. Dev. Cell 1, 165-177 (2001).
26. Malik, H.-S. & Henikoff, S. Major evolutionary transitions in centromere complexity. Cell 138, 1067-1082 (2009).
27. Foltz, D.-R. et al. The human CENPA centromeric nucleosome-associated complex. Nature Cell Biol. 8, 458-469 (2006).
28. Panchenko, T. & Black, B.-E. The epigenetic basis for centromere identity. Prog. Mol. Subcell. Biol. 48, 1-32 (2009).
29. Sullivan, K.-F., Hechenberger, M. & Masri, K. Human CENPA contains a histone H3 related histone fold domain that is required for targeting to the centromere. J.-Cell Biol. 127, 581-592 (1994). (Pubitemid 24332958)
30. Howman, E.-V. et al. Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc. Natl Acad. Sci. USA 97, 1148-1153 (2000).
31. Blower, M.-D. & Karpen, G.-H. The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nature Cell Biol. 3, 730-739 (2001).
32. Oegema, K., Desai, A., Rybina, S., Kirkham, M. & Hyman, A.-A. Functional analysis of kinetochore assembly in Caenorhabditis elegans. J.-Cell Biol. 153, 1209-1226 (2001).
33. Palmer, D.-K., O'Day, K., Wener, M.-H., Andrews, B.-S. & Margolis, R.-L. A 17kD centromere protein (CENPA) copurifies with nucleosome core particles and with histones. J.-Cell Biol. 104, 805-815 (1987). (Pubitemid 17068653)
34. Saitoh, H. et al. CENPC, an autoantigen in scleroderma, is a component of the human inner kinetochore plate. Cell 70, 115-125 (1992).
35. Dawe, R.-K., Reed, L.-M., Yu, H.-G., Muszynski, M.-G. & Hiatt, E.-N. A maize homolog of mammalian CENPC is a constitutive component of the inner kinetochore. Plant Cell 11, 1227-1238 (1999).
36. Fukagawa, T., Regnier, V. & Ikemura, T. Creation and characterization of temperature-sensitive CENPC mutants in vertebrate cells. Nucleic Acids Res. 29, 3796-3803 (2001). (Pubitemid 32910520)
37. Ogura, Y., Shibata, F., Sato, H. & Murata, M. Characterization of a CENPC homolog in Arabidopsis thaliana. Genes Genet. Syst. 79, 139-144 (2004). (Pubitemid 39243764)
38. Schuh, M., Lehner, C.-F. & Heidmann, S. Incorporation of Drosophila CID/CENPA and CENPC into centromeres during early embryonic anaphase. Curr. Biol. 17, 237-243 (2007). (Pubitemid 46186017)
39. Tomkiel, J., Cooke, C.-A., Saitoh, H., Bernat, R.-L. & Earnshaw, W.-C. CENPC is required for maintaining proper kinetochore size and for a timely transition to anaphase. J.-Cell Biol. 125, 531-545 (1994). (Pubitemid 24149836)
40. Erhardt, S. et al. Genome-wide analysis reveals a cell cycle-dependent mechanism controlling centromere propagation. J.-Cell Biol. 183, 805-818 (2008).
41. Screpanti, E. et al. Direct binding of CenpC to the Mis12 complex joins the inner and outer kinetochore. Curr. Biol. 21, 391-398 (2011).
42. Przewloka, M.-R. et al. CENPC is a structural platform for kinetochore assembly. Curr. Biol. 21, 399-405 (2011).
43. Carroll, C.-W., Milks, K.-J. & Straight, A.-F. Dual recognition of CENPA nucleosomes is required for centromere assembly. J.-Cell Biol. 189, 1143-1155 (2010).
44. Hori, T. et al. CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135, 1039-1052 (2008).
45. Okada, M. et al. The CENPH-I complex is required for the efficient incorporation of newly synthesized CENPA into centromeres. Nature Cell Biol. 8, 446-457 (2006).
46. Hori, T., Okada, M., Maenaka, K. & Fukagawa, T. CENPO class proteins form a stable complex and are required for proper kinetochore function. Mol. Biol. Cell 19, 843-854 (2008). (Pubitemid 351481802)
47. Amano, M. et al. The CENPS complex is essential for the stable assembly of outer kinetochore structure. J.-Cell Biol. 186, 173-182 (2009).
48. Earnshaw, W.-C. & Migeon, B.-R. Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma 92, 290-296 (1985).
49. Ekwall, K. Epigenetic control of centromere behavior. Annu. Rev. Genet. 41, 63-81 (2007).
50. Mythreye, K. & Bloom, K.-S. Differential kinetochore protein requirements for establishment versus propagation of centromere activity in Saccharomyces cerevisiae. J.-Cell Biol. 160, 833-843 (2003). (Pubitemid 36350839)
51. Mishra, P.-K., Baum, M. & Carbon, J. Centromere size and position in Candida albicans are evolutionarily conserved independent of DNA sequence heterogeneity. Mol. Genet. Genomics 278, 455-465 (2007). (Pubitemid 47437689)
52. Folco, H.-D., Pidoux, A.-L., Urano, T. & Allshire, R.-C. Heterochromatin and RNAi are required to establish CENPA chromatin at centromeres. Science 319, 94-97 (2008).
53. Morris, C.-A. & Moazed, D. Centromere assembly and propagation. Cell 128, 647-650 (2007). (Pubitemid 46273576)
54. Glynn, M., Kaczmarczyk, A., Prendergast, L., Quinn, N. & Sullivan, K.-F. Centromeres: assembling and propagating epigenetic function. Subcell. Biochem. 50, 223-249 (2010).
55. Bernard, P. et al. Requirement of heterochromatin for cohesion at centromeres. Science 294, 2539-2542 (2001). (Pubitemid 34027292)
56. Giet, R. & Glover, D.-M. Drosophila Aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J.-Cell Biol. 152, 669-682 (2001).
57. Hagstrom, K.-A., Holmes, V.-F., Cozzarelli, N.-R. & Meyer, B.-J.-C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev. 16, 729-742 (2002).
58. Hendzel, M.-J. et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106, 348-360 (1997).
59. Jager, H., Rauch, M. & Heidmann, S. The Drosophila melanogaster condensin subunit CapG interacts with the centromere-specific histone H3 variant CID. Chromosoma 113, 350-361 (2005). (Pubitemid 40253957)
60. Maddox, P.-S., Hyndman, F., Monen, J., Oegema, K. & Desai, A. Functional genomics identifies a Myb domain-containing protein family required for assembly of CENPA chromatin. J.-Cell Biol. 176, 757-763 (2007). (Pubitemid 46425535)
61. Dunleavy, E., Pidoux, A. & Allshire, R. Centromeric chromatin makes its mark. Trends Biochem. Sci. 30, 172-175 (2005). (Pubitemid 40463305)
62. Bergmann, J.-H. et al. Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENPA assembly on a synthetic human kinetochore. EMBO J. 30, 328-340 (2011).
63. Guenatri, M., Bailly, D., Maison, C. & Almouzni, G. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J.-Cell Biol. 166, 493-505 (2004). (Pubitemid 39097169)
64. Greaves, I.-K., Rangasamy, D., Ridgway, P. & Tremethick, D.-J. H2A.Z contributes to the unique 3D structure of the centromere. Proc. Natl Acad. Sci. USA 104, 525-530 (2007). (Pubitemid 46123058)
65. Martens, J.-H. et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24, 800-812 (2005).
66. Peters, A.-H. et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12, 1577-1589 (2003).
67. Nonaka, N. et al. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Naure Cell Biol. 4, 89-93 (2002). (Pubitemid 34071986)
68. Guetg, C. et al. The NoRC complex mediates the heterochromatin formation and stability of silent rRNA genes and centromeric repeats. EMBO J. 29, 2135-2146 (2010).
69. Fraga, M.-F. et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nature Genet. 37, 391-400 (2005).
70. Zhang, W., Lee, H.-R., Koo, D.-H. & Jiang, J. Epigenetic modification of centromeric chromatin: hypomethylation of DNA sequences in the CENH3associated chromatin in Arabidopsis thaliana and maize. Plant Cell 20, 25-34 (2008). (Pubitemid 352844031)
71. Nakano, M. et al. Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev. Cell 14, 507-522 (2008). (Pubitemid 351492128)
72. Cardinale, S. et al. Hierarchical inactivation of a synthetic human kinetochore by a chromatin modifier. Mol. Biol. Cell 20, 4194-4204 (2009).
73. Luger, K., Mader, A.-W., Richmond, R.-K., Sargent, D.-F. & Richmond, T.-J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389, 251-260 (1997). (Pubitemid 27406632)
74. Henikoff, S. & Dalal, Y. Centromeric chromatin: what makes it unique? Curr. Opin. Genet. Dev. 15, 177-184 (2005). (Pubitemid 40410664)
75. Van Hooser, A.-A. et al. Specification of kinetochore-forming chromatin by the histone H3 variant CENPA. J.-Cell Sci. 114, 3529-3542 (2001).
76. Black, B.-E. et al. Structural determinants for generating centromeric chromatin. Nature 430, 578-582 (2004).
77. Black, B.-E. et al. Centromere identity maintained by nucleosomes assembled with histone H3 containing the CENPA targeting domain. Mol. Cell 25, 309-322 (2007).
78. Zhou, Z. et al. Structural basis for recognition of centromere histone variant CenH3 by the chaperone Scm3. Nature 16-Mar 2011 (doi:10.1038/ nature09854).
79. Furuyama, S. & Biggins, S. Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc. Natl Acad. Sci. USA 104, 14706-14711 (2007). (Pubitemid 350003207)
80. Blower, M.-D., Sullivan, B.-A. & Karpen, G.-H. Conserved organization of centromeric chromatin in flies and humans. Dev. Cell 2, 319-330 (2002).
81. Sekulic, N., Bassett, E.-A., Rogers, D.-J. & Black, B.-E. The structure of (CENPA-H4)2 reveals physical features that mark centromeres. Nature 467, 347-351 (2010).
82. Conde Silva, N. et al. CENPAcontaining nucleosomes: easier disassembly versus exclusive centromeric localization. J.-Mol. Biol. 370, 555-573 (2007).
83. Shelby, R.-D., Vafa, O. & Sullivan, K.-F. Assembly of CENPA into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites. J.-Cell Biol. 136, 501-513 (1997). (Pubitemid 27083754)
84. Chen, Y. et al. The N terminus of the centromere H3like protein Cse4p performs an essential function distinct from that of the histone fold domain. Mol. Cell. Biol. 20, 7037-7048 (2000).
85. Camahort, R. et al. Cse4 is part of an octameric nucleosome in budding yeast. Mol. Cell 35, 794-805 (2009).
86. Williams, J.-S., Hayashi, T., Yanagida, M. & Russell, P. Fission yeast Scm3 mediates stable assembly of Cnp1/CENPA into centromeric chromatin. Mol. Cell 33, 287-298 (2009).
87. Dalal, Y., Furuyama, T., Vermaak, D. & Henikoff, S. Structure, dynamics, and evolution of centromeric nucleosomes. Proc. Natl Acad. Sci. USA 104, 15974-15981 (2007). (Pubitemid 350099363)
88. Furuyama, T. & Henikoff, S. Centromeric nucleosomes induce positive DNA supercoils. Cell 138, 104-113 (2009).
89. Dalal, Y., Wang, H., Lindsay, S. & Henikoff, S. Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol. 5, e218 (2007).
90. Mizuguchi, G., Xiao, H., Wisniewski, J., Smith, M.-M. & Wu, C. Nonhistone Scm3 and histones CenH3H4 assemble the core of centromere-specific nucleosomes. Cell 129, 1153-1164 (2007). (Pubitemid 46900852)
91. Camahort, R. et al. Scm3 is essential to recruit the histone H3 variant Cse4 to centromeres and to maintain a functional kinetochore. Mol. Cell 26, 853-865 (2007). (Pubitemid 46924838)
92. Stoler, S. et al. Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc. Natl Acad. Sci. USA 104, 10571-10576 (2007). (Pubitemid 47185706)
93. Pidoux, A.-L. et al. Fission yeast Scm3: a CENPA receptor required for integrity of subkinetochore chromatin. Mol. Cell 33, 299-311 (2009).
94. Sanchez-Pulido, L., Pidoux, A.-L., Ponting, C.-P. & Allshire, R.-C. Common ancestry of the CENPA chaperones Scm3 and HJURP. Cell 137, 1173-1174 (2009).
95. Dunleavy, E.-M. et al. HJURP is a cellcycledependent maintenance and deposition factor of CENPA at centromeres. Cell 137, 485-497 (2009).
96. Aravind, L., Iyer, L.-M. & Wu, C. Domain architectures of the Scm3p protein provide insights into centromere function and evolution. Cell Cycle 6, 2511-2515 (2007). (Pubitemid 350058669)
97. Shuaib, M., Ouararhni, K., Dimitrov, S. & Hamiche, A. HJURP binds CENPA via a highly conserved Nterminal domain and mediates its deposition at centromeres. Proc. Natl Acad. Sci. USA 107, 1349-1354 (2010).
98. Foltz, D.-R. et al. Centromere-specific assembly of CENPA nucleosomes is mediated by HJURP. Cell 137, 472-484 (2009).
99. Hewawasam, G. et al. Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol. Cell 40, 444-454 (2010).
100. Ranjitkar, P. et al. An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol. Cell 40, 455-464 (2010).
101. Furuyama, T., Dalal, Y. & Henikoff, S. Chaperone-mediated assembly of centromeric chromatin in-vitro. Proc. Natl Acad. Sci. USA 103, 6172-6177 (2006).
102. Lavelle, C. et al. Right-handed nucleosome: myth or reality? Cell 139, 1216-1217; author reply 1217-1218 (2009).
103. Suto, R.-K., Clarkson, M.-J., Tremethick, D.-J. & Luger, K. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nature Struct. Biol. 7, 1121-1124 (2000).
104. Bruce, K. et al. The replacement histone H2A.Z in a hyperacetylated form is a feature of active genes in the chicken. Nucleic Acids Res. 33, 5633-5639 (2005). (Pubitemid 41548829)
105. Meneghini, M.-D., Wu, M. & Madhani, H.-D. Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112, 725-736 (2003). (Pubitemid 36331783)
106. Abbott, D.-W., Ivanova, V.-S., Wang, X., Bonner, W.-M. & Ausio, J. Characterization of the stability and folding of H2A.Z chromatin particles: implications for transcriptional activation. J.-Biol. Chem. 276, 41945-41949 (2001).
107. Fan, J.-Y., Gordon, F., Luger, K., Hansen, J.-C. & Tremethick, D.-J. The essential histone variant H2A.Z regulates the equilibrium between different chromatin conformational states. Nature Struct. Biol. 9, 172-176 (2002). (Pubitemid 34171307)
108. Mellone, B.-G. & Allshire, R.-C. Stretching it: putting the CEN(PA) in centromere. Curr. Opin. Genet. Dev. 13, 191-198 (2003).
109. Henikoff, S., Ahmad, K., Platero, J.-S. & van Steensel, B. Heterochromatic deposition of centromeric histone H3like proteins. Proc. Natl Acad. Sci. USA 97, 716-721 (2000). (Pubitemid 30070375)
110. Shelby, R.-D., Monier, K. & Sullivan, K.-F. Chromatin assembly at kinetochores is uncoupled from DNA replication. J.-Cell Biol. 151, 1113-1118 (2000).
111. 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).
112. Ahmad, K. & Henikoff, S. Centromeres are specialized replication domains in heterochromatin. J.-Cell Biol. 153, 101-110 (2001).
113. Lermontova, I. et al. Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18, 2443-2451 (2006). (Pubitemid 44749881)
114. Lermontova, I., Fuchs, J., Schubert, V. & Schubert, I. Loading time of the centromeric histone H3 variant differs between plants and animals. Chromosoma 116, 507-510 (2007). (Pubitemid 350120986)
115. Takahashi, K., Takayama, Y., Masuda, F., Kobayashi, Y. & Saitoh, S. Two distinct pathways responsible for the loading of CENPA to centromeres in the fission yeast cell cycle. Phil. Trans. R.-Soc. B Biol. Sci. 360, 595-606; discussion 606-607 (2005).
116. Pearson, C.-G. et al. Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase. Curr. Biol. 14, 1962-1967 (2004).
117. Mellone, B.-G., Zhang, W. & Karpen, G. Frodos found: behold the CENPA "Ring" bearers. Cell 137, 409-412 (2009).
118. Hayashi, T. et al. Mis16 and Mis18 are required for CENPA loading and histone deacetylation at centromeres. Cell 118, 715-729 (2004). (Pubitemid 39221731)
119. Fujita, Y. et al. Priming of centromere for CENPA recruitment by human hMis18α, hMis18β, and M18BP1. Dev. Cell 12, 17-30 (2007). (Pubitemid 46002597)
120. Kato, T. et al. Activation of Holliday junction recognizing protein involved in the chromosomal stability and immortality of cancer cells. Cancer Res. 67, 8544-8553 (2007). (Pubitemid 47437429)
121. Perpelescu, M., Nozaki, N., Obuse, C., Yang, H. & Yoda, K. Active establishment of centromeric CENPA chromatin by RSF complex. J.-Cell Biol. 185, 397-407 (2009).
122. Kaufman, P.-D., Cohen, J.-L. & Osley, M.-A. Hir proteins are required for position-dependent gene silencing in Saccharomyces cerevisiae in the absence of chromatin assembly factor I. Mol. Cell. Biol. 18, 4793-4806 (1998).
123. Sharp, J.-A., Franco, A.-A., Osley, M.-A. & Kaufman, P.-D. Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in S.-cerevisiae. Genes Dev. 16, 85-100 (2002).
124. Lopes da Rosa, J., Holik, J., Green, E.-M., Rando, O.-J. & Kaufman, P.-D. Overlapping regulation of CenH3 localization and histone H3 turnover by CAF1 and HIR proteins in Saccharomyces cerevisiae. Genetics 187, 9-19 (2011).
125. Galvani, A. et al. In-vivo study of the nucleosome assembly functions of ASF1 histone chaperones in human cells. Mol. Cell. Biol. 28, 3672-3685 (2008). (Pubitemid 351732904)
126. Sharp, J.-A., Krawitz, D.-C., Gardner, K.-A., Fox, C.-A. & Kaufman, P.-D. The budding yeast silencing protein Sir1 is a functional component of centromeric chromatin. Genes Dev. 17, 2356-2361 (2003).
127. Lee, M.-T. & Bachant, J. SUMO modification of DNA topoisomerase II: trying to get a CENse of it all. DNA Repair (Amst.) 8, 557-568 (2009).
128. Hsu, J.-M., Huang, J., Meluh, P.-B. & Laurent, B.-C. The yeast RSC chromatin-remodeling complex is required for kinetochore function in chromosome segregation. Mol. Cell. Biol. 23, 3202-3215 (2003). (Pubitemid 36459233)
129. Xue, Y. et al. The human SWI/SNFB chromatin-remodeling complex is related to yeast rsc and localizes at kinetochores of mitotic chromosomes. Proc. Natl Acad. Sci. USA 97, 13015-13020 (2000).
130. Glynn, E.-F. et al. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol. 2, e259 (2004).
131. Wood, A.-J., Severson, A.-F. & Meyer, B.-J. Condensin and cohesin complexity: the expanding repertoire of functions. Nature Rev. Genet. 11, 391-404 (2010).
132. Nasmyth, K. & Haering, C.-H. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 43, 525-558 (2009).
133. Hirano, T. At the heart of the chromosome: SMC proteins in action. Nature Rev. Mol. Cell Biol. 7, 311-322 (2006).
134. Ocampo-Hafalla, M.-T., Katou, Y., Shirahige, K. & Uhlmann, F. Displacement and re-accumulation of centromeric cohesin during transient pre-anaphase centromere splitting. Chromosoma 116, 531-544 (2007). (Pubitemid 350120989)
135. Yeh, E. et al. Pericentric chromatin is organized into an intramolecular loop in mitosis. Curr. Biol. 18, 81-90 (2008).
136. Dewar, H., Tanaka, K., Nasmyth, K. & Tanaka, T.-U. Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle. Nature 428, 93-97 (2004). (Pubitemid 38332364)
137. Tanaka, T., Fuchs, J., Loidl, J. & Nasmyth, K. Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nature Cell Biol. 2, 492-499 (2000).
138. Sakuno, T., Tada, K. & Watanabe, Y. Kinetochore geometry defined by cohesion within the centromere. Nature 458, 852-858 (2009).
139. Stumpff, J. & Asbury, C.-L. Chromosome bi-orientation: euclidian euploidy. Curr. Biol. 18, R81-R83 (2008).
140. Indjeian, V.-B. & Murray, A.-W. Budding yeast mitotic chromosomes have an intrinsic bias to biorient on the spindle. Curr. Biol. 17, 1837-1846 (2007).
141. Maresca, T.-J. & Salmon, E.-D. Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J.-Cell Biol. 184, 373-381 (2009).
142. Maresca, T.-J. & Salmon, E.-D. Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal. J.-Cell Sci. 123, 825-835 (2010).
143. Zinkowski, R.-P., Meyne, J. & Brinkley, B.-R. The centromere-kinetochore complex: a repeat subunit model. J.-Cell Biol. 113, 1091-1110 (1991). (Pubitemid 21909741)
144. Birchler, J.-A., Gao, Z. & Han, F. A tale of two centromeres- diversity of structure but conservation of function in plants and animals. Funct. Integr. Genomics 9, 7-13 (2009).
145. Ribeiro, S.-A. et al. A super-resolution map of the vertebrate kinetochore. Proc. Natl Acad. Sci. USA 107, 10484-10489 (2010).
146. Anderson, M., Haase, J., Yeh, E. & Bloom, K. Function and assembly of DNA looping, clustering, and microtubule attachment complexes within a eukaryotic kinetochore. Mol. Biol. Cell 20, 4131-4139 (2009).
147. Joglekar, A.-P., Bouck, D.-C., Molk, J.-N., Bloom, K.-S. & Salmon, E.-D. Molecular architecture of a kinetochore-microtubule attachment site. Nature Cell Biol. 8, 581-585 (2006).
148. Joglekar, A.-P., Bloom, K. & Salmon, E.-D. In-vivo protein architecture of the eukaryotic kinetochore with nanometer scale accuracy. Curr. Biol. 19, 694-699 (2009).
149. Wan, X. et al. Protein architecture of the human kinetochore microtubule attachment site. Cell 137, 672-684 (2009).
150. Johnston, K. et al. Vertebrate kinetochore protein architecture: protein copy number. J.-Cell Biol. 189, 937-943 (2010).
151. Dong, Y., Vanden Beldt, K.-J., Meng, X., Khodjakov, A. & McEwen, B.-F. The outer plate in vertebrate kinetochores is a flexible network with multiple microtubule interactions. Nature Cell Biol. 9, 516-522 (2007). (Pubitemid 46696532)
152. McEwen, B.-F. & Dong, Y. Contrasting models for kinetochore microtubule attachment in mammalian cells. Cell. Mol. Life Sci. 67, 2163-2172 (2010).
153. Duan, Z. et al. A three-dimensional model of the yeast genome. Nature 465, 363-367 (2010).
154. Bloom, K. Centromere dynamics. Curr. Opin. Genet. Dev. 17, 151-156 (2007). (Pubitemid 46551720)
155. Grosberg, A.-Y. & Khokhlov, A.-R. Giant Molecules: Here, There, And Everywhere. (Academic Press, San Diego, 1997).
156. Jun, S. & Wright, A. Entropy as the driver of chromosome segregation. Nature Rev. Microbiol. 8, 600-607 (2010).
157. Finan, K., Cook, P.-R. & Marenduzzo, D. Non-specific (entropic) forces as major determinants of the structure of mammalian chromosomes. Chromosome Res. 19, 53-61 (2010).
158. Marko, J.-F. Linking topology of tethered polymer rings with applications to chromosome segregation and estimation of the knotting length. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 79, 051905 (2009).
159. Koszul, R. & Kleckner, N. Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol. 19, 716-724 (2009).
160. Marenduzzo, D., Micheletti, C. & Cook, P.-R. Entropy-driven genome organization. Biophys. J. 90, 3712-3721 (2006).
161. Marenduzzo, D., Finan, K. & Cook, P.-R. The depletion attraction: an underappreciated force driving cellular organization. J.-Cell Biol. 175, 681-686 (2006). (Pubitemid 44878499)
162. Bohn, M. & Heermann, D.-W. Repulsive forces between looping chromosomes induce entropy-driven segregation. PLoS ONE 6, e14428 (2011).
163. Jannink, G., Duplantier, B. & Sikorav, J.-L. Forces on chromosomal DNA during anaphase. Biophys. J. 71, 451-465 (1996). (Pubitemid 26227331)
164. Nicklas, R.-B. Measurements of the force produced by the mitotic spindle in anaphase. J.-Cell Biol. 97, 542-548 (1983).
165. Zhang, T., Lim, H.-H., Cheng, C.-S. & Surana, U. Deficiency of centromere-associated protein Slk19 causes premature nuclear migration and loss of centromeric elasticity. J.-Cell Sci. 119, 519-531 (2006).
166. Chai, C.-C., Teh, E.-M. & Yeong, F.-M. Unrestrained spindle elongation during recovery from spindle checkpoint activation in cdc15-2 cells results in mis-segregation of chromosomes. Mol. Biol. Cell 21, 2384-2398 (2010).
167. Tanaka, T.-U., Stark, M.-J. & Tanaka, K. Kinetochore capture and bi-orientation on the mitotic spindle. Nature Rev. Mol. Cell Biol. 6, 929-942 (2005). (Pubitemid 41778712)
168. Bouck, D.-C. & Bloom, K. Pericentric chromatin is an elastic component of the mitotic spindle. Curr. Biol. 17, 741-748 (2007). (Pubitemid 46635113)
169. Marshall, W.-F., Marko, J.-F., Agard, D.-A. & Sedat, J.-W. Chromosome elasticity and mitotic polar ejection force measured in living Drosophila embryos by four-dimensional microscopy-based motion analysis. Curr. Biol. 11, 569-578 (2001).
170. Brinkley, B.-R. & Stubblefield, E. The fine structure of the kinetochore of a mammalian cell in-vitro. Chromosoma 19, 28-43 (1966).
171. Jokelainen, P.-T. The ultrastructure and spatial organization of the metaphase kinetochore in mitotic rat cells. J.-Ultrastruct. Res. 19, 19-44 (1967).
172. Welburn, J.-P. & Cheeseman, I.-M. Toward a molecular structure of the eukaryotic kinetochore. Dev. Cell 15, 645-655 (2008).
173. Sedwick, C. Ted Salmon: kinetochores at the core of it all. J.-Cell Biol. 191, 896-897 (2010).
174. Canman, J.-C. et al. Determining the position of the cell division plane. Nature 424, 1074-1078 (2003).
175. Bancaud, A. et al. Nucleosome chiral transition under positive torsional stress in single chromatin fibers. Mol. Cell 27, 135-147 (2007). (Pubitemid 46991385)
176. Black, B.-E. & Cleveland, D.-W. Epigenetic centromere propagation and the nature of CENPA nucleosomes. Cell 144, 471-479 (2011).
177. Ohta, S. et al. The protein composition of mitotic chromosomes determined using multiclassifier combinatorial proteomics. Cell 142, 810-821 (2010).