Stretching it: Putting the CEN(P-A) in centromere

Current Opinion in Genetics and Development

Volumn 13, Issue 2, 2003, Pages 191-198

  Mellone, Barbara G ^a   Allshire, Robin C ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN;

CENTROMERE; CHROMOSOME SEGREGATION; MEIOSIS; MITOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0037380151     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(03)00019-4     Document Type: Review

References (66)

1. Sharpe M.E., Errington J. Upheaval in the bacterial nucleoid. An active chromosome segregation mechanism. Trends Genet. 15:1999;70-74.
2. Errington J. Septation and chromosome segregation during sporulation in Bacillus subtilis. Curr. Opin. Microbiol. 4:2001;660-666.
3. Dworkin J., Losick R. Does RNA polymerase help drive chromosome segregation in bacteria? Proc. Natl. Acad. Sci. U.S.A. 99:2002;14089-14094.
4. Buchwitz B.J., Ahmad K., Moore L.L., Roth M.B., Henikoff S. A histone-H3-like protein in C. elegans. Nature. 401:1999;547-548.
5. Dernburg A.F. Here, there, and everywhere: kinetochore function on holocentric chromosomes. J. Cell Biol. 153:2001;33-38.
6. Karpen G.H., Allshire R.C. The case for epigenetic effects on centromere identity and function. Trends Genet. 13:1997;489-496.
7. Wiens G.R., Sorger P.K. Centromeric chromatin and epigenetic effects in kinetochore assembly. Cell. 93:1998;313-316.
8. Sullivan B.A., Blower M.D., Karpen G.H. Determining centromere identity: cyclical stories and forking paths. Nat. Rev. Genet. 2:2001;584-596.
9. Sullivan K.F. A solid foundation: functional specialization of centromeric chromatin. Curr. Opin. Genet. Dev. 11:2001;182-188 An excellent review where possible models accounting for CENP-A deposition are proposed and discussed.
10. Choo K.H. Domain organisation at the centromere and neocentromere. Dev. Cell. 1:2001;165-177.
11. Malik H.S., Henikoff S. Conflict begets complexity: the evolution of centromeres. Curr. Opin. Genet. Dev. 12:2002;711-718.
12. Lo A.W., Craig J.M., Saffery R., Kalitsis P., Irvine D.V., Earle E., Magliano D.J., Choo K.H. A 330 kb CENP-A binding domain and altered replication timing at a human neocentromere. EMBO J. 20:2001;2087-2096.
13. Warburton P.E., Dolled M., Mahmood R., Alonso A., Li S., Naritomi K., Tohma T., Nagai T., Hasegawa T., Ohashi H.et al. Molecular cytogenetic analysis of eight inversion duplications of human chromosome 13q that each contain a neocentromere. Am. J. Hum. Genet. 66:2000;1794-1806.
14. Spence J.M., Critcher R., Ebersole T.A., Valdivia M.M., Earnshaw W.C., Fukagawa T., Farr C.J. Co-localization of centromere activity, proteins and topoisomerase II within a subdomain of the major human X alpha-satellite array. EMBO J. 21:2002;5269-5280 Telomere-mediated chromosome breakage is used to generate a series of left and right deletion derivatives of human X centromere followed by a comprehensive analysis exploring mitotic stability, centromeric protein association, restriction analysis and Topo II cleavage activity. Centromere activity maps to a ∼50 kb region of the 3 Mb DXZ1 α-satellite array. Within this active region resides a major site of Topo II cleavage. The position of Topo II cleavage shifts in derivatives with a nearby telomere. The fact that all derivatives with a functional centromere share the same ∼50 kb region within a much longer array of similar sequences indicates that the site of kinetochore assembly is propagated.
15. Schueler M.G., Higgins A.W., Rudd M.K., Gustashaw K., Willard H.F. Genomic and genetic definition of a functional human centromere. Science. 294:2001;109-115 The human X chromosome region is explored in detail with respect to its repetitive sequence, the evolution of these sequences and their surrounding context. In addition, breakpoints on naturally occurring rearranged X chromosomes were mapped, with a broad region of ∼3 Mb (DXZ1 α-satellite) being designated as responsible for centromere function. These sequences also allow de novo kinetochore assembly.
16. Floridia G., Zatterale A., Zuffardi O., Tyler-Smith C. Mapping of a human centromere onto the DNA by topoisomerase II cleavage. EMBO Rep. 1:2000;489-493.
17. Ikeno M., Grimes B., Okazaki T., Nakano M., Saitoh K., Hoshino H., McGill N.I., Cooke H., Masumoto H. Construction of YAC-based mammalian artificial chromosomes. Nat. Biotechnol. 16:1998;431-439.
18. Ohzeki J., Nakano M., Okada T., Masumoto H. CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J. Cell Biol. 159:2002;765-775 Synthetic α-satellite arrays with and without CENP-B boxes are used to demonstrate convincingly that CENP-B plays a role in promoting de novo kinetochore assembly. CENP-B boxes alone are not sufficient, however, suggesting that it is some other feature of α-satellite (e.g. the fact that it is AT rich) that makes it a preferred substrate.
19. Kapoor M., Montes de Oca Luna R., Liu G., Lozano G., Cummings C., Mancini M., Ouspenski I., Brinkley B.R., May G.S. The cenpB gene is not essential in mice. Chromosoma. 107:1998;570-576.
20. Hudson D.F., Fowler K.J., Earle E., Saffery R., Kalitsis P., Trowell H., Hill J., Wreford N.G., de Kretser D.M., Cancilla M.R.et al. Centromere protein B null mice are mitotically and meiotically normal but have lower body and testis weights. J. Cell Biol. 141:1998;309-319.
21. Vermaak D., Hayden H.S., Henikoff S. Centromere targeting element within the histone fold domain of Cid. Mol. Cell Biol. 22:2002;7553-7561.
22. Blower M.D., Sullivan B.A., Karpen G.H. Conserved organization of centromeric chromatin in flies and humans. Dev. Cell. 2:2002;319-330 Stretched chromosome fibres from fly and human cells show a similar organisation characterised by interspersed domains containing histone H3 and CID/CENP-A. The authors propose a model in which these two domains become distinct upon chromosome condensation with CENP-A being presented on the outer face of the kinetochore.
23. Blower M.D., Karpen G.H. The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat. Cell Biol. 3:2001;730-739.
24. Shelby R.D., Vafa O., Sullivan K.F. Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites. J. Cell Biol. 136:1997;501-513.
25. Takahashi K., Chen E.S., Yanagida M. Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science. 288:2000;2215-2219.
26. Kim SM, Dubey DD, Huberman JA: Early-replicating heterochromatin. Genes Dev 2003, in press.
27. Sullivan B., Karpen G. Centromere identity in Drosophila is not determined in vivo by replication timing. J. Cell Biol. 154:2001;683-690.
28. Ahmad K., Henikoff S. Centromeres are specialised replication domains in heterochromatin. J. Cell Biol. 153:2001;101-110.
29. Shelby R.D., Monier K., Sullivan K.F. Chromatin assembly at kinetochores is uncoupled from DNA replication. J. Cell Biol. 151:2000;1113-1118.
30. Ahmad K., Henikoff S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell. 9:2002;1191-1200 The role of the H3.3 histone H3 variant relative to H3 is investigated. Induction of GFP-tagged H3.3 demonstrates that it is targeted to chromatin outside S phase. This replication-independent deposition of H3.3, which differs from the replication coupling of H3, is tracked to differences between the two at residues 31, 87, 89 and 90. The authors propose that deposition of H3.3 could overcome histone-modification-dependent silencing.
31. •].
32. 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. 16:2002;85-100 A novel role for CAF-1 in building centromeric chromatin is revealed: cells lacking components from the two overlapping pathways involved in chromatin assembly, Cac and Hir, show a delay in anaphase, increased rate of chromosome loss, genetic interaction with kinetochore components and de-clustered Cse4/CENP-A localisation.
33. Mis6 results in prolonged prometaphase arrest with defective chromosome alignment and eventual apoptosis. CENP-C and CENP-H, but not CENP-A, required CENP-I for recruitment to centromeres. CENP-I is also dependent on CENP-H. Two-hybrid analyses indicate that CENP-H interacts with CENP-I.
34. Goshima G., Kiyomitsu T., Yoda K., Yanagida M. Human centromere protein hMis12 essential for equal segregation is independent of CENP-A loading pathway. J. Cell Biol. 160:2003;25-39 The human homologue of the SpMis12/ScMtw protein, hMis12, is identified and shown to be a novel component of the inner kinetochore with a localisation indistinguishable from that of CENP-A. Depletion of hMis12 does not alter CENP-A localisation, but causes chromosome segregation defects. Depletion of hMis6 does not cause delocalisation of CENP-A, in contrast to data shown in fission yeast. CENP-A depletion dramatically reduces hMis6 and CENP-C signals, but does not affect hMis12 localisation, indicating that this inner kinetochore component acts via a CENP-A-independent pathway.
35. Measday V., Hailey D.W., Pot I., Givan S.A., Hyland K.M., Cagney G., Fields S., Davis T.N., Hieter P. Ctf3p, the Mis6 budding yeast homolog, interacts with Mcm22p and Mcm16p at the yeast outer kinetochore. Genes Dev. 16:2002;101-113.
36. Chen E.S., Saitoh S., Yanagida M., Takahashi K. A cell cycle-regulated GATA factor promotes centromeric localisation of CENP-A in fission yeast. Mol. Cell. 11:2003;175-187 A suppressor screen for a temperature-sensitive allele of SpCENP-A identified histone H4 and a GATA-like factor, Ams2. In cells lacking Ams2 SpCENP-A-GFP localisation is dispersed, but Mis6 is not; thus, Ams2 appears to act upstream of Mis6 in SpCENP-A deposition. How Ams2 acts to direct SpCENP-A localisation is not known - the two proteins do not interact in vivo. Perhaps Ams2 acts to regulate the histones' level relative to SpCENP-A.
37. Howman E.V., Fowler K.J., Newson A.J., Redward S., MacDonald A.C., Kalitsis P., Choo K.H. Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc. Natl. Acad. Sci. U.S.A. 97:2000;1148-1153.
38. Oegema K., Desai A., Rybina S., Kirkham M., Hyman A.A. Functional analysis of kinetochore assembly in Caenorhabditis elegans. J. Cell Biol. 153:2001;1209-1226 Depletion of three kinetochore components, CeCENP-A, CeCENP-C and CeINCENP, at the one-cell stage of the C. elegans embryo is used to analyse the functional consequences of defective kinetochores. Depletion of CeCENP-A results in loss of CeCENP-C and depletion of either component results in a 'kinetochore null' phenotype and failure to assemble a mechanically stable spindle. Depletion of CeINCENP causes defects in anaphase and telophase.
39. Moore L.L., Roth M.B. HCP-4, a CENP-C-like protein in Caenorhabditis elegans, is required for resolution of sister centromeres. J. Cell Biol. 153:2001;1199-1208.
40. 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. 114:2001;3529-3542 This paper address the hypothesis that the presence of CENP-A at a chromosomal site can drive kinetochore assembly. Overproducing CENP-A causes its incorporation along chromosome arms and CENP-C, hSMC1 and Hzwint-1 also become ectopically localised. However, their presence alone is not sufficient to allow kinetochore function, not even in fragmented chromosomes or in dicentric chromosomes. The authors propose that additional factors, which are required for kinetochore assembly, may be loaded independently of CENP-A.
41. Shelby R.D., Hahn K.M., Sullivan K.F. Dynamic elastic behavior of alpha-satellite DNA domains visualized in situ in living human cells. J. Cell Biol. 135:1996;545-557.
42. Tanaka T., Fuchs J., Loidl J., Nasmyth K. Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nat. Cell Biol. 2:2000;492-499.
43. Nabeshima K., Nakagawa T., Straight A.F., Murray A., Chikashige Y., Yamashita Y.M., Hiraoka Y., Yanagida M. Dynamics of centromeres during metaphase-anaphase transition in fission yeast: Dis1 is implicated in force balance in metaphase bipolar spindle. Mol. Biol. Cell. 9:1998;3211-3225.
44. Goshima G., Yanagida M. Establishing biorientation occurs with precocious separation of the sister kinetochores, but not the arms, in the early spindle of budding yeast. Cell. 100:2000;619-633.
45. He X., Asthana S., Sorger P.K. Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell. 101:2000;763-775.
46. Bickmore W.A., Oghene K. Visualizing the spatial relationships between defined DNA sequences and the axial region of extracted metaphase chromosomes. Cell. 84:1996;95-104.
47. Van Hooser A.A., Heald R. Kinetochore function: the complications of becoming attached. Curr. Biol. 11:2001;855-857.
48. Kitagawa K., Hieter P. Evolutionary conservation between budding yeast and human kinetochores. Nat. Rev. Mol. Cell Biol. 2:2001;678-687.
49. He X., Rines D.R., Espelin C.W., Sorger P.K. Molecular analysis of kinetochore-microtubule attachment in budding yeast. Cell. 106:2001;195-206 Detailed analyses and measurement of centromere behaviour in live yeast cells is utilised to assign a role to several kinetochore proteins in microtubule attachment and the generation of tension between sister kinetochores.
50. Pot I, Measday V, Snydsman B, Cagney G, Fields, Davis TN, Muller EGD, Hieter P: Chl4p and Iml3p are two new members of the budding yeast outer kinetochore. Mol Biol Cell 2003 in press.
51. Cheeseman I.M., Anderson S., Jwa M., Green E.M., Kang J., Yates J.R. III, Chan C.S., Drubin D.G., Barnes G. Phospho-regulation of kinetochore-microtubule attachments by the Aurora kinase Ipl1p. Cell. 111:2002;163-172 A protein purification strategy is used to isolate a Ndc80p, a Ctf19, a Dam1 and an Ipl1 complex. Among the components identified, five novel kinetochore components - Dad3, Dad4, Nkp1, Nkp2 and Ame1 - are also isolated. Mass spectrometry identified several phosphorylation sites, a subset of which are direct targets of the Ipl1 kinase. Phosphorylation of the Dam1 protein is probably of fundamental importance in regulating kinetochore-microtubule interactions. Abolition of all of the Ipl1 phosphorylation sites within Dam1 results in lethality, whereas double or triple mutations combined with mutations in Spc34 (another Ipl1 target) result in massive uneven chromosome segregation (without affecting spindle formation) and reduced centromere association of Dam1p.
52. + cells; however, in ipl1 mutants they all remain attached to the old SPB, decreasing the chances of normally occurring turnover. The authors raise the possibility that Ipl1-Sli15 facilitates biorientation by allowing frequent turnover between kinetochores and SPB until tension is successfully established.
53. Adams R.R., Maiato H., Earnshaw W.C., Carmena M. Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J. Cell Biol. 153:2001;865-880.
54. Lachner M., O'Carroll D., Rea S., Mechtler K., Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature. 410:2001;116-120.
55. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature. 410:2001;120-124.
56. Partridge J.F., Scott K.S., Bannister A.J., Kouzarides T., Allshire R.C. cis-acting DNA from fission yeast centromeres mediates histone H3 methylation and recruitment of silencing factors and cohesin to an ectopic site. Curr. Biol. 12:2002;1652-1660.
57. 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. 297:2002;1833-1837 This pioneering work reports the discovery of a role in centromeric heterochromatin formation for components of the RNA interference pathway in fission yeast cells. Deletion of either the Dicer, Argonaute or RNA-dependent RNA polymerase homologues leads to the loss of histone H3 lysine 9 methylation, Swi6 recruitment and alleviation of transcriptional silencing. In addition, discrete transcripts are produced from the outer centromereic repeats in these mutants. The authors propose a model in which double-stranded RNAs arising from the centromere are processed to mediate heterochromatin formation.
58. Zhong C.X., Marshall J.B., Topp C., Mroczek R., Kato A., Nagaki K., Birchler J.A., Jiang J., Dawe R.K. Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell. 14:2002;2825-2836.
59. + disrupt the localisation of the chromo domain protein Swi6p and impair centromere function. J. Cell Sci. 109:1996;2637-2648.
60. Ekwall K., Cranston G., Allshire R.C. Fission yeast mutants that alleviate transcriptional silencing in centromeric flanking repeats and disrupt chromosome segregation. Genetics. 153:1999;1153-1169.
61. Pidoux A.L., Uzawa S., Perry P.E., Cande W.Z., Allshire R.C. Live analysis of lagging chromosomes during anaphase and their effect on spindle elongation rate in fission yeast. J. Cell Sci. 113:2000;4177-4191.
62. •].
63. Volpe T, Schramke V, Hamilton GL, White SA, Teng G, Martienssen RA, Allshire RC: RNA interference is required for normal centromere function. Chromosome Res, 2003, in press.
64. Hall I.M., Noma K., Grewal S.I. RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast. Proc. Natl. Acad. Sci. U.S.A. 100:2003;193-198 Together these three papers demonstrate that the RNAi machinery is required for centromere function and acts to recruit cohesin via Swi6 at endogenous and ectopic centromeric repeats.
65. Bernard P., Maure J.F., Partridge J.F., Genier S., Javerzat J.P., Allshire R.C. Requirement of heterochromatin for cohesion at centromeres. Science. 294:2001;2539-2542.
66. 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. 4:2002;89-93.