Diversity in the organization of centromeric chromatin

Current Opinion in Genetics and Development

Volumn 31, Issue , 2015, Pages 28-35

  Steiner, Florian A ^a,b   Henikoff, Steven ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CELL FUNCTION; CELLULAR DISTRIBUTION; CENH3 NUCLEOSOME; CENTROMERE; CHROMATIN; CHROMATIN STRUCTURE; HETEROCHROMATIN; HOLOCENTROMERE; HUMAN; IN VIVO STUDY; NEOCENTROMERE; NONHUMAN; NUCLEOSOME; PERICENTRIC CHROMATIN; PERICENTRIC HETEROCHROMATIN; PRIORITY JOURNAL; REVIEW; YEAST; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; SACCHAROMYCETALES;

SACCHAROMYCETALES; SCHIZOSACCHAROMYCETACEAE;

CHROMATIN; NUCLEOSOME;

ANIMALS; CENTROMERE; CHROMATIN; HUMANS; NUCLEOSOMES; SACCHAROMYCETALES;

EID: 84929456653     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2015.03.010     Document Type: Review

References (88)

1. Flemming W. Zellsubstanz, Kern und Zelltheilung 1882, F.C.W. Vogel, Leipzig.
2. Earnshaw W.C., Rothfield N. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 1985, 91:313-321.
3. Palmer D.K., Margolis R.L. Kinetochore components recognized by human autoantibodies are present on mononucleosomes. Mol Cell Biol 1985, 5:173-186.
4. Furuyama S., Biggins S. Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc Natl Acad Sci USA 2007, 104:14706-14711.
5. Pluta A.F., Mackay A.M., Ainsztein A.M., Goldberg I.G., Earnshaw W.C. The centromere: hub of chromosomal activities. Science 1995, 270:1591-1594.
6. Hasson D., Panchenko T., Salimian K.J., Salman M.U., Sekulic N., Alonso A., Warburton P.E., Black B.E. The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat Struct Mol Biol 2013, 20:687-695.
7. Zhang T., Talbert P.B., Zhang W., Wu Y., Yang Z., Henikoff J.G., Henikoff S., Jiang J. The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres. Proc Natl Acad Sci USA 2013, 110:E4875-E4883.
8. Melters D.P., Bradnam K.R., Young H.A., Telis N., May M.R., Ruby J.G., Sebra R., Peluso P., Eid J., Rank D., et al. Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol 2013, 14:R10.
9. Masumoto H., Nakano M., Ohzeki J. The role of CENP-B and alpha-satellite DNA: de novo assembly and epigenetic maintenance of human centromeres. Chromosome Res 2004, 12:543-556.
10. Bodor D.L., Mata J.F., Sergeev M., David A.F., Salimian K.J., Panchenko T., Cleveland D.W., Black B.E., Shah J.V., Jansen L.E. The quantitative architecture of centromeric chromatin. eLife 2014, 3:e02137.
11. Alexandrov I., Kazakov A., Tumeneva I., Shepelev V., Yurov Y. Alpha-satellite DNA of primates: old and new families. Chromosoma 2001, 110:253-266.
12. Henikoff J.G., Thakur J., Kasinathan S., Henikoff S. A unique chromatin complex occupies young α-satellite arrays of human centromeres. Sci Adv 2015, 1:e1400234.
13. Melters D.P., Paliulis L.V., Korf I.F., Chan S.W. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res 2012, 20:579-593.
14. Steiner F.A., Henikoff S. Holocentromeres are dispersed point centromeres localized at transcription factor hotspots. eLife 2014, 3:e02025.
15. Gassmann R., Rechtsteiner A., Yuen K.W., Muroyama A., Egelhofer T., Gaydos L., Barron F., Maddox P., Essex A., Monen J., et al. An inverse relationship to germline transcription defines centromeric chromatin in C. elegans. Nature 2012, 484:534-537.
16. Drinnenberg I.A., deYoung D., Henikoff S., Malik H.S. Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. eLife 2014, 3.
17. Akiyoshi B., Gull K. Discovery of unconventional kinetochores in kinetoplastids. Cell 2014, 156:1247-1258.
18. Bernard P., Maure J.F., Partridge J.F., Genier S., Javerzat J.P., Allshire R.C. Requirement of heterochromatin for cohesion at centromeres. Science 2001, 294:2539-2542.
19. Nonaka N., Kitajima T., Yokobayashi S., Xiao G., Yamamoto M., Grewal S.I., Watanabe Y. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast. Nat Cell Biol 2002, 4:89-93.
20. Allshire R.C., Nimmo E.R., Ekwall K., Javerzat J.P., Cranston G. Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. Genes Dev 1995, 9:218-233.
21. Ekwall K., Javerzat J.P., Lorentz A., Schmidt H., Cranston G., Allshire R. The chromodomain protein Swi6: a key component at fission yeast centromeres. Science 1995, 269:1429-1431.
22. Folco H.D., Pidoux A.L., Urano T., Allshire R.C. Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 2008, 319:94-97.
23. Brown W.R., Thomas G., Lee N.C., Blythe M., Liti G., Warringer J., Loose M.W. Kinetochore assembly and heterochromatin formation occur autonomously in Schizosaccharomyces pombe. Proc Natl Acad Sci USA 2014, 111:1903-1908.
24. Shang W.H., Hori T., Martins N.M., Toyoda A., Misu S., Monma N., Hiratani I., Maeshima K., Ikeo K., Fujiyama A., et al. Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell 2013, 24:635-648.
25. Ribeiro S.A., Vagnarelli P., Earnshaw W.C. DNA content of a functioning chicken kinetochore. Chromosome Res 2014, 22:7-13.
26. Sullivan B.A. Centromere round-up at the heterochromatin corral. Trends Biotechnol 2002, 20:89-92.
27. Scott K.C., White C.V., Willard H.F. An RNA polymerase III-dependent heterochromatin barrier at fission yeast centromere 1. PLoS One 2007, 2:e1099.
28. Sullivan B.A., Karpen G.H. Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat Struct Mol Biol 2004, 11:1076-1083.
29. Hori T., Shang W.H., Toyoda A., Misu S., Monma N., Ikeo K., Molina O., Vargiu G., Fujiyama A., Kimura H., et al. Histone H4 Lys 20 monomethylation of the CENP-A nucleosome is essential for kinetochore assembly. Dev Cell 2014, 29:740-749.
30. Volpe T.A., Kidner C., Hall I.M., Teng G., Grewal S.I., Martienssen R.A. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 2002, 297:1833-1837.
31. Hall I.M., Shankaranarayana G.D., Noma K., Ayoub N., Cohen A., Grewal S.I. Establishment and maintenance of a heterochromatin domain. Science 2002, 297:2232-2237.
32. Quenet D., Dalal Y. A long non-coding RNA is required for targeting centromeric protein A to the human centromere. eLife 2014, 3:e03254.
33. Carone D.M., Longo M.S., Ferreri G.C., Hall L., Harris M., Shook N., Bulazel K.V., Carone B.R., Obergfell C., O'Neill M.J., et al. A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres. Chromosoma 2009, 118:113-125.
34. Chan F.L., Marshall O.J., Saffery R., Kim B.W., Earle E., Choo K.H., Wong L.H. Active transcription and essential role of RNA polymerase II at the centromere during mitosis. Proc Natl Acad Sci USA 2012, 109:1979-1984.
35. Bergmann J.H., Rodriguez M.G., Martins N.M., Kimura H., Kelly D.A., Masumoto H., Larionov V., Jansen L.E., Earnshaw W.C. Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-a assembly on a synthetic human kinetochore. EMBO J 2011, 30:328-340.
36. Chueh A.C., Northrop E.L., Brettingham-Moore K.H., Choo K.H., Wong L.H. LINE retrotransposon RNA is an essential structural and functional epigenetic component of a core neocentromeric chromatin. PLoS Genet 2009, 5:e1000354.
37. Choi E.S., Stralfors A., Castillo A.G., Durand-Dubief M., Ekwall K., Allshire R.C. Identification of noncoding transcripts from within CENP-A chromatin at fission yeast centromeres. J Biol Chem 2011, 286:23600-23607.
38. Choi E.S., Stralfors A., Catania S., Castillo A.G., Svensson J.P., Pidoux A.L., Ekwall K., Allshire R.C. Factors that promote H3 chromatin integrity during transcription prevent promiscuous deposition of CENP-A(Cnp1) in fission yeast. PLoS Genet 2012, 8:e1002985.
39. Camahort R., Shivaraju M., Mattingly M., Li B., Nakanishi S., Zhu D., Shilatifard A., Workman J.L., Gerton J.L. Cse4 is part of an octameric nucleosome in budding yeast. Mol Cell 2009, 35:794-805.
40. Lefrancois P., Euskirchen G.M., Auerbach R.K., Rozowsky J., Gibson T., Yellman C.M., Gerstein M., Snyder M. Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC Genom 2009, 10:37.
41. Krassovsky K., Henikoff J.G., Henikoff S. Tripartite organization of centromeric chromatin in budding yeast. Proc Natl Acad Sci USA 2012, 109:243-248.
42. Lefrancois P., Auerbach R.K., Yellman C.M., Roeder G.S., Snyder M. Centromere-like regions in the budding yeast genome. PLoS Genet 2013, 9:e1003209.
43. Ranjitkar P., Press M.O., Yi X., Baker R., MacCoss M.J., Biggins S. An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol Cell 2010, 40:455-464.
44. Hewawasam G., Shivaraju M., Mattingly M., Venkatesh S., Martin-Brown S., Florens L., Workman J.L., Gerton J.L. Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol Cell 2010, 40:444-454.
45. Lacoste N., Woolfe A., Tachiwana H., Garea A.V., Barth T., Cantaloube S., Kurumizaka H., Imhof A., Almouzni G. Mislocalization of the centromeric histone variant CenH3/CENP-A in human cells depends on the chaperone DAXX. Mol Cell 2014, 53:631-644.
46. Athwal R.K., Walkiewicz M.P., Baek S., Fu S., Bui M., Camps J., Ried T., Sung M.H., Dalal Y. CENP-A nucleosomes localize to transcription factor hotspots and subtelomeric sites in human cancer cells. Epigenet Chromatin 2015, 8:2.
47. Gascoigne K.E., Takeuchi K., Suzuki A., Hori T., Fukagawa T., Cheeseman I.M. Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 2011, 145:410-422.
48. Van Hooser A.A., Ouspenski I.I., Gregson H.C., Starr D.A., Yen T.J., Goldberg M.L., Yokomori K., Earnshaw W.C., Sullivan K.F., Brinkley B.R. Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J Cell Sci 2001, 114:3529-3542.
49. Tomonaga T., Matsushita K., Yamaguchi S., Oohashi T., Shimada H., Ochiai T., Yoda K., Nomura F. Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res 2003, 63:3511-3516.
50. Amato A., Schillaci T., Lentini L., Di Leonardo A. CENPA overexpression promotes genome instability in pRb-depleted human cells. Mol Cancer 2009, 8:119.
51. Heun P., Erhardt S., Blower M.D., Weiss S., Skora A.D., Karpen G.H. Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell 2006, 10:303-315.
52. Ahmad K., Henikoff S. Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci USA 2002, 99(Suppl. 4):16477-16484.
53. Marshall O.J., Chueh A.C., Wong L.H., Choo K.H. Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 2008, 82:261-282.
54. Warburton P.E. Chromosomal dynamics of human neocentromere formation. Chromosome Res 2004, 12:617-626.
55. Platero J.S., Ahmad K., Henikoff S. A distal heterochromatic block displays centromeric activity when detached from a natural centromere. Mol Cell 1999, 4:995-1004.
56. Ishii K., Ogiyama Y., Chikashige Y., Soejima S., Masuda F., Kakuma T., Hiraoka Y., Takahashi K. Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science 2008, 321:1088-1091.
57. Ketel C., Wang H.S., McClellan M., Bouchonville K., Selmecki A., Lahav T., Gerami-Nejad M., Berman J. Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 2009, 5:e 1000400.
58. Thakur J., Sanyal K. Efficient neocentromere formation is suppressed by gene conversion to maintain centromere function at native physical chromosomal loci in Candida albicans. Genome Res 2013, 23:638-652.
59. Nasuda S., Hudakova S., Schubert I., Houben A., Endo T.R. Stable barley chromosomes without centromeric repeats. Proc Natl Acad Sci USA 2005, 102:9842-9847.
60. Olszak A.M., van Essen D., Pereira A.J., Diehl S., Manke T., Maiato H., Saccani S., Heun P. Heterochromatin boundaries are hotspots for de novo kinetochore formation. Nat Cell Biol 2011, 13:799-808.
61. 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 2013, 200:45-60.
62. Mendiburo M.J., Padeken J., Fulop S., Schepers A., Heun P. Drosophila CENH3 is sufficient for centromere formation. Science 2011, 334:686-690.
63. Tachiwana H., Kagawa W., Shiga T., Osakabe A., Miya Y., Saito K., Hayashi-Takanaka Y., Oda T., Sato M., Park S.Y., et al. Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 2011, 476:232-235.
64. Furuyama T., Codomo C.A., Henikoff S. Reconstitution of hemisomes on budding yeast centromeric DNA. Nucleic Acids Res 2013, 41:5769-5783.
65. Dalal Y., Wang H., Lindsay S., Henikoff S. Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol 2007, 5:e218.
66. Foltz D.R., Jansen L.E., Black B.E., Bailey A.O., Yates J.R., Cleveland D.W. The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 2006, 8:458-469.
67. Mizuguchi G., Xiao H., Wisniewski J., Smith M.M., Wu C. Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 2007, 129:1153-1164.
68. Furuyama T., Henikoff S. Centromeric nucleosomes induce positive DNA supercoils. Cell 2009, 138:104-113.
69. Huang C.C., Chang K.M., Cui H., Jayaram M. Histone H3-variant Cse4-induced positive DNA supercoiling in the yeast plasmid has implications for a plasmid origin of a chromosome centromere. Proc Natl Acad Sci USA 2011, 108:13671-13676.
70. Fukagawa T., Earnshaw W.C. The centromere: chromatin foundation for the kinetochore machinery. Dev Cell 2014, 30:496-508.
71. Coffman V.C., Wu P., Parthun M.R., Wu J.Q. CENP-A exceeds microtubule attachment sites in centromere clusters of both budding and fission yeast. J Cell Biol 2011, 195:563-572.
72. Lawrimore J., Bloom K.S., Salmon E.D. Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. J Cell Biol 2011, 195:573-582.
73. Shivaraju M., Unruh J.R., Slaughter B.D., Mattingly M., Berman J., Gerton J.L. Cell-cycle-coupled structural oscillation of centromeric nucleosomes in yeast. Cell 2012, 150:304-316.
74. Wisniewski J., Hajj B., Chen J., Mizuguchi G., Xiao H., Wei D., Dahan M., Wu C. Imaging the fate of histone Cse4 reveals de novo replacement in S phase and subsequent stable residence at centromeres. eLife 2014, 3:e02203.
75. Aravamudhan P., Felzer-Kim I., Joglekar A.P. The budding yeast point centromere associates with two Cse4 molecules during mitosis. Curr Biol 2013, 23:770-774.
76. Haase J., Mishra P.K., Stephens A., Haggerty R., Quammen C., Taylor R.M., Yeh E., Basrai M.A., Bloom K. A 3D map of the yeast kinetochore reveals the presence of core and accessory centromere-specific histone. Curr Biol 2013, 23:1939-1944.
77. Xiao H., Mizuguchi G., Wisniewski J., Huang Y., Wei D., Wu C. Nonhistone Scm3 binds to AT-rich DNA to organize atypical centromeric nucleosome of budding yeast. Mol Cell 2011, 43:369-380.
78. Henikoff S., Ramachandran S., Krassovsky K., Bryson T.D., Codomo C.A., Brogaard K., Widom J., Wang J., Henikoff J.G. The budding yeast Centromere DNA element II wraps a stable Cse4 hemisome in either orientation in vivo. eLife 2014, 3:e01861.
79. Wieland G., Orthaus S., Ohndorf S., Diekmann S., Hemmerich P. Functional complementation of human centromere protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae. Mol Cell Biol 2004, 24:6620-6630.
80. Dunleavy E.M., Roche D., Tagami H., Lacoste N., Ray-Gallet D., Nakamura Y., Daigo Y., Nakatani Y., Almouzni-Pettinotti G. HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 2009, 137:485-497.
81. Foltz D.R., Jansen L.E., Bailey A.O., Yates J.R., Bassett E.A., Wood S., Black B.E., Cleveland D.W. Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 2009, 137:472-484.
82. Camahort R., Li B., Florens L., Swanson S.K., Washburn M.P., Gerton J.L. Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol Cell 2007, 26:853-865.
83. 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., et al. Fission yeast Scm3: a CENP-A receptor required for integrity of subkinetochore chromatin. Mol Cell 2009, 33:299-311.
84. Stoler S., Rogers K., Weitze S., Morey L., Fitzgerald-Hayes M., Baker R.E. Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc Natl Acad Sci USA 2007, 104:10571-10576.
85. Williams J.S., Hayashi T., Yanagida M., Russell P. Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol Cell 2009, 33:287-298.
86. Chen C.C., Dechassa M.L., Bettini E., Ledoux M.B., Belisario C., Heun P., Luger K., Mellone B.G. CAL1 is the Drosophila CENP-A assembly factor. J Cell Biol 2014, 204:313-329.
87. Wang J., Liu X., Dou Z., Chen L., Jiang H., Fu C., Fu G., Liu D., Zhang J., Zhu T., et al. Mitotic regulator Mis18beta interacts with and specifies the centromeric assembly of molecular chaperone HJURP. J Biol Chem 2014, 289:8326-8336.
88. Muller S., Montes de Oca R., Lacoste N., Dingli F., Loew D., Almouzni G. Phosphorylation and DNA binding of HJURP determine its centromeric recruitment and function in CenH3(CENP-A) loading. Cell Rep 2014, 8:190-203.