Abstract
Faithful chromosome segregation during cell division depends on the centromere, a complex DNA/protein structure that links chromosomes to spindle microtubules. This chromosomal domain has to be marked throughout cell division and its chromosomal localization preserved across cell generations. From fission yeast to human, centromeres are established on a series of repetitive DNA sequences and on specialized centromeric chromatin. This chromatin is enriched with the histone H3 variant, named CENP-A, that was demonstrated to be the epigenetic mark that maintains centromere identity and function indefinitely. Although centromere identity is thought to be exclusively epigenetic, the presence of specific DNA sequences in the majority of eukaryotes and of the centromeric protein CENP-B that binds to these sequences, suggests the existence of a genetic component as well. In this review, we will highlight the importance of centromeric sequences for centromere formation and function, and discuss the centromere DNA sequence/CENP-B paradox.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Aguilar-Arnal L, Marsellach F-X, Azorín F (2008) The fission yeast homologue of CENP-B, Abp1, regulates directionality of mating-type switching. EMBO J 27:1029–1038. doi:10.1038/emboj.2008.53
Aldrup-MacDonald ME, Kuo ME, Sullivan LL et al (2016) Genomic variation within alpha satellite DNA influences centromere location on human chromosomes with metastable epialleles. Genome Res 26:1301–1311. doi:10.1101/gr.206706.116
Alexandrov I, Kazakov A, Tumeneva I et al (2001) Alpha-satellite DNA of primates: old and new families. Chromosoma 110:253–266. doi:10.1007/s004120100146
Alkan C, Cardone MF, Catacchio CR et al (2011) Genome-wide characterization of centromeric satellites from multiple mammalian genomes. Genome Res 21:137–145. doi:10.1101/gr.111278.110
Allshire RC, Karpen GH (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9:923–937. doi:10.1038/nrg2466
Almouzni G, Probst AV (2011) Heterochromatin maintenance and establishment: lessons from the mouse pericentromere. Nucleus 2:332–338. doi:10.4161/nucl.2.5.17707
Alonso A, Fritz B, Hasson D et al (2007) Co-localization of CENP-C and CENP-H to discontinuous domains of CENP-A chromatin at human neocentromeres. Genome Biol 8:R148. doi:10.1186/gb-2007-8-7-r148
Alonso A, Hasson D, Cheung F, Warburton PE (2010) A paucity of heterochromatin at functional human neocentromeres. Epigenetics Chromatin 3:6. doi:10.1186/1756-8935-3-6
Amor DJ, Bentley K, Ryan J et al (2004) Human centromere repositioning in progress. Proc Natl Acad Sci USA 101:6542–6547. doi:10.1073/pnas.0308637101
Ando S, Yang H, Nozaki N et al (2002) CENP-A, -B, and -C chromatin complex that contains the I-type alpha-satellite array constitutes the prekinetochore in HeLa cells. Mol Cell Biol 22:2229–2241. doi:10.1128/MCB.22.7.-2229-2241.2002
Andrews AJ, Chen X, Zevin A et al (2010) The histone chaperone Nap1 promotes nucleosome assembly by eliminating nonnucleosomal histone DNA interactions. Mol Cell 37:834–842. doi:10.1016/j.molcel.2010.01.037
Aze A, Sannino V, Soffientini P et al (2016) Centromeric DNA replication reconstitution reveals DNA loops and ATR checkpoint suppression. Nat Cell Biol 18:684–691. doi:10.1038/ncb3344
Bachman KE, Rountree MR, Baylin SB (2001) Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem 276:32282–32287. doi:10.1074/jbc.M104661200
Bailis JM, Bernard P, Antonelli R et al (2003) Hsk1-Dfp1 is required for heterochromatin-mediated cohesion at centromeres. Nat Cell Biol 5:1111–1116. doi:10.1038/ncb1069
Barbosa-Cisneros O, Herrera-Esparza R (2002) CENP-B is a conserved gene among vegetal species. Genet Mol Res 1:241–245
Bassett EA, Wood S, Salimian KJ et al (2010) Epigenetic centromere specification directs aurora B accumulation but is insufficient to efficiently correct mitotic errors. J Cell Biol 190:177–185. doi:10.1083/jcb.201001035
Baum M, Clarke L (2000) Fission yeast homologs of human CENP-B have redundant functions affecting cell growth and chromosome segregation. Mol Cell Biol 20:2852–2864
Baumann C, Körner R, Hofmann K, Nigg EA (2007) PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 128:101–114. doi:10.1016/j.cell.2006.11.041
Bergmann JH, Rodríguez MG, Martins NMC et al (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 30:328–340. doi:10.1038/emboj.2010.329
Bernard P, Maure JF, Partridge JF et al (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294:2539–2542. doi:10.1126/science.1064027
Bierhoff H, Postepska-Igielska A, Grummt I (2014) Noisy silence: non-coding RNA and heterochromatin formation at repetitive elements. Epigenetics 9:53–61. doi:10.4161/epi.26485
Biscotti MA, Canapa A, Forconi M et al (2015) Transcription of tandemly repetitive DNA: functional roles. Chromosome Res 23:463–477. doi:10.1007/s10577-015-9494-4
Black BE, Cleveland DW (2011) Epigenetic centromere propagation and the nature of CENP-A nucleosomes. Cell 144:471–479. doi:10.1016/j.cell.2011.02.002
Blower MD, Sullivan BA, Karpen GH (2002) Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2:319–330
Bodor DL, Mata JF, Sergeev M et al (2014) The quantitative architecture of centromeric chromatin. eLife 3:819–826. doi:10.7554/eLife.02137
Brenner S, Pepper D, Berns MW et al (1981) Kinetochore structure, duplication, and distribution in mammalian cells: analysis by human autoantibodies from scleroderma patients. J Cell Biol 91:95–102
Buchwitz BJ, Ahmad K, Moore LL et al (1999) A histone-H3-like protein in C. elegans. Nature 401:547–548. doi:10.1038/44062
Cam HP, Noma K-I, Ebina H et al (2008) Host genome surveillance for retrotransposons by transposon-derived proteins. Nature 451:431–436. doi:10.1038/nature06499
Carroll CW, Milks KJ, Straight AF (2010) Dual recognition of CENP-A nucleosomes is required for centromere assembly. J Cell Biol 189:1143–1155. doi:10.1083/jcb.201001013
Casola C, Hucks D, Feschotte C (2008) Convergent domestication of pogo-like transposases into centromere-binding proteins in fission yeast and mammals. Mol Biol Evol 25:29–41. doi:10.1093/molbev/msm221
Chan KL, North PS, Hickson ID (2007) BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J 26:3397–3409. doi:10.1038/sj.emboj.7601777
Chan FL, Marshall OJ, Saffery R et al (2012) Active transcription and essential role of RNA polymerase II at the centromere during mitosis. Proc Natl Acad Sci USA 109:1979–1984. doi:10.1073/pnas.1108705109
Chen T, Tsujimoto N, Li E (2004) The PWWP domain of Dnmt3a and Dnmt3b is required for directing DNA methylation to the major satellite repeats at pericentric heterochromatin. Mol Cell Biol 24:9048–9058. doi:10.1128/MCB.24.20.9048-9058.2004
Chmátal L, Gabriel SI, Mitsainas GP et al (2014) Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Curr Biol 24:2295–2300. doi:10.1016/j.cub.2014.08.017
Choo KH, Vissel B, Nagy A et al (1991) A survey of the genomic distribution of alpha satellite DNA on all the human chromosomes, and derivation of a new consensus sequence. Nucleic Acid Res 19:1179–1182
Clarke L, Carbon J (1980) Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287:504–509
Cleveland DW, Mao Y, Sullivan KF (2003) Centromeres and kinetochores: From epigenetics to mitotic checkpoint signaling. Cell 112:407–421
Cooke CA, Bernat RL, Earnshaw WC (1990) CENP-B: a major human centromere protein located beneath the kinetochore. J Cell Biol 110:1475–1488
Cumberledge S, Carbon J (1987) Mutational analysis of meiotic and mitotic centromere function in Saccharomyces cerevisiae. Genetics 117:203–212
Dai X, Otake K, You C et al (2013) Identification of novel α-n-methylation of CENP-B that regulates its binding to the centromeric DNA. J Proteome Res 12:4167–4175. doi:10.1021/pr400498y
d’Alençon E, Nègre N, Stanojcic S et al (2011) Characterization of a CENP-B homolog in the holocentric Lepidoptera Spodoptera frugiperda. Gene 485:91–101. doi:10.1016/j.gene.2011.06.007
Depinet TW, Zackowski JL, Earnshaw WC et al (1997) Characterization of neo-centromeres in marker chromosomes lacking detectable alpha-satellite DNA. Hum Mol Genet 6:1195–1204
Drinnenberg IA, Henikoff S, Malik HS (2016) Evolutionary turnover of kinetochore proteins: a ship of theseus? Trends Cell Biol 26:498–510. doi:10.1016/j.tcb.2016.01.005
Dumanski JP, Rasi C, Lönn M et al (2015) Mutagenesis. Smoking is associated with mosaic loss of chromosome Y. Science 347:81–83. doi:10.1126/science.1262092
Earnshaw WC, Rothfield N (1985) Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91:313–321
Earnshaw WC, Sullivan KF, Machlin PS et al (1987) Molecular cloning of cDNA for CENP-B, the major human centromere autoantigen. J Cell Biol 104:817–829
Edwards NS, Murray AW (2005) Identification of xenopus CENP-A and an associated centromeric DNA repeat. Mol Biol Cell 16:1800–1810. doi:10.1091/mbc.E04-09-0788
Ehrlich M, Sanchez C, Shao C et al (2008) ICF, an immunodeficiency syndrome: DNA methyltransferase 3B involvement, chromosome anomalies, and gene dysregulation. Autoimmunity 41:253–271. doi:10.1080/08916930802024202
Epifanova OI (1958) The mitotic behavior of the epithelium of the uterus at different stages of the sexual cycle in mice. Bull Exp Bio Med 46:1399–1402. doi:10.1007/BF00845190
Erliandri I, Fu H, Nakano M et al (2014) Replication of alpha-satellite DNA arrays in endogenous human centromeric regions and in human artificial chromosome. Nucleic Acids Res 42:11502–11516. doi:10.1093/nar/gku835
Fachinetti D, Folco HD, Nechemia-Arbely Y et al (2013) A two-step mechanism for epigenetic specification of centromere identity and function. Nat Cell Biol 15:1–13. doi:10.1038/ncb2805
Fachinetti D, Han JS, McMahon MA et al (2015) DNA sequence-specific binding of CENP-B enhances the fidelity of human centromere function. Dev Cell 33:314–327. doi:10.1016/j.devcel.2015.03.020
Folco HD, Pidoux AL, Urano T, Allshire RC (2008) Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319:94–97. doi:10.1126/science.1150944
Foltz DR, Jansen LET, Black BE et al (2006) The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8:458–469. doi:10.1038/ncb1397
Forsberg LA, Rasi C, Malmqvist N et al (2014) Mosaic loss of chromosome Y in peripheral blood is associated with shorter survival and higher risk of cancer. 46:624–628. doi:10.1038/ng.2966 (Nature Publishing Group)
Fowler KJ, Hudson DF, Salamonsen LA et al (2000) Uterine dysfunction and genetic modifiers in centromere protein B-deficient mice. Genome Res 10:30–41. doi:10.1101/gr.10.1.30
Fowler KJ, Wong LH, Griffiths BK et al (2004) Centromere protein b-null mice display decreasing reproductive performance through successive generations of breeding due to diminishing endometrial glands. Reproduction 127:367–377. doi:10.1530/rep.1.00102
Fujita Y, Hayashi T, Kiyomitsu T et al (2007) Priming of centromere for CENP-A recruitment by human hMis18α, hMis18β, and M18BP1. Dev Cell 12:17–30. doi:10.1016/j.devcel.2006.11.002
Fujita R, Otake K, Arimura Y et al (2015) Stable complex formation of CENP-B with the CENP-A nucleosome. Nucleic Acids Res 43:4909–4922. doi:10.1093/nar/gkv405
Fuks F (2005) DNA methylation and histone modifications: teaming up to silence genes. Curr Opin Genet Dev 15:490–495. doi:10.1016/j.gde.2005.08.002
Garavís M, Méndez-Lago M, Gabelica V et al (2015) The structure of an endogenous Drosophila centromere reveals the prevalence of tandemly repeated sequences able to form i-motifs. 5:13307. doi:10.1038/srep13307 (Nature Publishing Group)
Goldberg IG, Sawhney H, Pluta AF et al (1996) Surprising deficiency of CENP-B binding sites in African green monkey alpha-satellite DNA: implications for CENP-B function at centromeres. Mol Cell Biol 16:5156–5168
Gong Z, Wu Y, Koblízková A et al (2012) Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24:3559–3574. doi:10.1105/tpc.112.100511
Gopalakrishnan S, Sullivan BA, Trazzi S et al (2009) DNMT3B interacts with constitutive centromere protein CENP-C to modulate DNA methylation and the histone code at centromeric regions. Hum Mol Genet 18:3178–3193. doi:10.1093/hmg/ddp256
Grady DL, Ratliff RL, Robinson DL et al (1992) Highly conserved repetitive DNA sequences are present at human centromeres. Proc Natl Acad Sci USA 89:1695–1699
Haaf T, Mater AG, Wienberg J, Ward DC (1995) Presence and abundance of CENP-B box sequences in great ape subsets of primate-specific alpha-satellite DNA. J Mol Evol 41:487–491
Halverson D, Baum M, Stryker J et al (1997) A centromere DNA-binding protein from fission yeast affects chromosome segregation and has homology to human CENP-B. J Cell Biol 136:487–500
Harrington JJ, Van Bokkelen G, Mays RW et al (1997) Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat Genet 15:345–355. doi:10.1038/ng0497-345
Hasson D, Panchenko T, Salimian KJ et al (2013) The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat Struct Mol Biol 20:687–695. doi:10.1038/nsmb.2562
Hayden KE, Strome ED, Merrett SL et al (2013) Sequences associated with centromere competency in the human genome. Mol Cell Biol 33:763–772. doi:10.1128/MCB.01198-12
Hemmerich P, Weidtkamp-Peters S, Hoischen C et al (2008) Dynamics of inner kinetochore assembly and maintenance in living cells. J Cell Biol 180:1101–1114. doi:10.1083/jcb.200710052
Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102. doi:10.1126/science.1062939
Henikoff JG, Thakur J, Kasinathan S, Henikoff S (2015) A unique chromatin complex occupies young α-satellite arrays of human centromeres. Sci Adv 1:e1400234. doi:10.1126/sciadv.1400234
Hoffmann S, Dumont M, Barra V et al (2016) CENP-A is dispensable for mitotic centromere function after initial centromere/kinetochore assembly. Cell Rep. doi:10.1016/j.celrep.2016
Hori T, Shang W-H, Takeuchi K, Fukagawa T (2013) The CCAN recruits CENP-A to the centromere and forms the structural core for kinetochore assembly. J Cell Biol 200:45–60. doi:10.1083/jcb.201210106
Howman EV, Fowler KJ, Newson AJ et al (2000) Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc Natl Acad Sci USA 97:1148–1153
Hudson DF, Fowler KJ, Earle E et al (1998) Centromere protein B null mice are mitotically and meiotically normal but have lower body and testis weights. J Cell Biol 141:309–319
Ideue T, Cho Y, Nishimura K, Tani T (2014) Involvement of satellite I noncoding RNA in regulation of chromosome segregation. Genes Cells 19:528–538. doi:10.1111/gtc.12149
Ikeno M, Masumoto H, Okazaki T (1994) Distribution of CENP-B boxes reflected in CREST centromere antigenic sites on long-range α-satellite DNA arrays of human chromosome 21. Hum Mol Genet 3:1245–1257. doi:10.1093/hmg/3.8.1245
Ikeno M, Grimes B, Okazaki T et al (1998) Construction of YAC-based mammalian artificial chromosomes. Nat Biotechnol 16:431–439. doi:10.1038/nbt0598-431
Irelan JT, Gutkin GI, Clarke L (2001) Functional redundancies, distinct localizations and interactions among three fission yeast homologs of centromere protein-B. Genetics 157:1191–1203
Jaco I, Canela A, Vera E, Blasco MA (2008) Centromere mitotic recombination in mammalian cells. J Cell Biol 181:885–892. doi:10.1083/jcb.200803042
Jeganathan K, Malureanu L, Baker DJ et al (2007) Bub1 mediates cell death in response to chromosome missegregation and acts to suppress spontaneous tumorigenesis. J Cell Biol 179:255–267. doi:10.1083/jcb.200706015
Kapoor M, de Oca Montes, Luna R, Liu G et al (1998) The cenpB gene is not essential in mice. Chromosoma 107:570–576
Ketel C, Wang HSW, McClellan M et al (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5:e1000400. doi:10.1371/journal.pgen.1000400
Kim IS, Lee M, Park KC et al (2012) Roles of Mis18α in epigenetic regulation of centromeric chromatin and CENP-A loading. Mol Cell 46:260–273. doi:10.1016/j.molcel.2012.03.021
Kipling D, Warburton PE (1997) Centromeres, CENP-B and tigger too. Trends Genet 13:141–145
Koga A, Hirai Y, Terada S et al (2014) Evolutionary origin of higher-order repeat structure in alpha-satellite DNA of primate centromeres. DNA Res 21:407–415. doi:10.1093/dnares/dsu005
Krings G, Bastia D (2005) Sap1p binds to Ter1 at the ribosomal DNA of Schizosaccharomyces pombe and causes polar replication fork arrest. J Biol Chem 280:39135–39142. doi:10.1074/jbc.M508996200
Kugou K, Hirai H, Masumoto H, Koga A (2016) Formation of functional CENP-B boxes at diverse locations in repeat units of centromeric DNA in new world monkeys. 6:27833. doi:10.1038/srep27833 (Nature Publishing Group)
Lee JK, Huberman JA, Hurwitz J (1997) Purification and characterization of a CENP-B homologue protein that binds to the centromeric K-type repeat DNA of Schizosaccharomyces pombe. Proc Natl Acad Sci USA 94:8427–8432
Lo AW, Liao GC, Rocchi M, Choo KH (1999) Extreme reduction of chromosome-specific alpha-satellite array is unusually common in human chromosome 21. Genome Res 9:895–908
Locke DP, Hillier LW, Warren WC et al (2011) Comparative and demographic analysis of orang-utan genomes. Nature 469:529–533. doi:10.1038/nature09687
Locovei AM, Spiga M-G, Tanaka K et al (2006) The CENP-B homolog, Abp1, interacts with the initiation protein Cdc23 (MCM10) and is required for efficient DNA replication in fission yeast. Cell Div 1:27. doi:10.1186/1747-1028-1-27
López CC, Edström JE (1998) Interspersed centromeric element with a CENP-B box-like motif in Chironomus pallidivittatus. Nucleic Acids Res 26:4168–4172
Lorite P, Carrillo JA, Tinaut A, Palomeque T (2004) Evolutionary dynamics of satellite DNA in species of the Genus Formica (Hymenoptera, Formicidae). Gene 332:159–168. doi:10.1016/j.gene.2004.02.049
Ly P, Teitz LS, Kim DH et al (2016) Selective Y centromere inactivation triggers chromosome shattering in micronuclei and repair by canonical NHEJ. Nat Cell Biol. doi:10.1038/ncb3450
Malik HS, Henikoff S (2001) Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics 157:1293–1298
Maloney KA, Sullivan LL, Matheny JE et al (2012) Functional epialleles at an endogenous human centromere. Proc Natl Acad Sci USA 109:13704–13709. doi:10.1073/pnas.1203126109
Manuelidis L (1978) Chromosomal localization of complex and simple repeated human DNAs. Chromosoma 66:23–32
Marshall OJ, Choo KHA (2012) Putative CENP-B paralogues are not present at mammalian centromeres. Chromosoma 121:169–179. doi:10.1007/s00412-011-0348-3
Marshall OJ, Chueh AC, Wong LH, Choo KHA (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82:261–282. doi:10.1016/j.ajhg.2007.11.009
Masumoto H, Masukata H, Muro Y et al (1989) A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite. J Cell Biol 109:1963–1973. doi:10.1083/jcb.109.5.1963
Masumoto H, Yoda K, Ikeno M et al (1993) Properties of CENP-B and its target sequence in a satellite DNA. Chromosome segregation and aneuploidy. (NATO ASI series). Springer, Berlin, pp 31–43. doi:10.1007/978-3-642-84938-1_3
Masumoto H, Ikeno M, Nakano M et al (1998) Assay of centromere function using a human artificial chromosome. Chromosoma 107:406–416
Mateo L, González J (2014) Pogo-like transposases have been repeatedly domesticated into CENP-B-related proteins. Genome Biol Evol 6:2008–2016. doi:10.1093/gbe/evu153
McFarlane RJ, Humphrey TC (2010) A role for recombination in centromere function. Trends Genet 26:209–213. doi:10.1016/j.tig.2010.02.005
McGrew J, Diehl B, Fitzgerald-Hayes M (1986) Single base-pair mutations in centromere element III cause aberrant chromosome segregation in Saccharomyces cerevisiae. Mol Cell Biol 6:530–538. doi:10.1128/MCB.6.2.530
Mejía JE, Alazami A, Willmott A et al (2002) Efficiency of de novo centromere formation in human artificial chromosomes. Genomics 79:297–304. doi:10.1006/geno.2002.6704
Melters DP, Bradnam KR, Young HA et al (2013) Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol 14:R10. doi:10.1186/gb-2013-14-1-r10
Mendiburo MJ, Padeken J, Fulop S et al (2011) Drosophila CENH3 is sufficient for centromere formation. Science 334:686–690. doi:10.1126/science.1206880
Meštrović N, Pavlek M, Car A et al (2013) Conserved DNA Motifs, Including the CENP-B Box-like, are possible promoters of satellite DNA array rearrangements in nematodes. PLoS ONE 8:e67328. doi:10.1371/journal.pone.0067328
Michel LS, Liberal V, Chatterjee A et al (2001) MAD2 haplo-insufficiency causes premature anaphase and chromosome instability in mammalian cells. Nature 409:355–359. doi:10.1038/35053094
Miga KH, Newton Y, Jain M et al (2014) Centromere reference models for human chromosomes X and Y satellite arrays. Genome Res 24:697–707. doi:10.1101/gr.159624.113
Mitchell AR, Jeppesen P, Nicol L et al (1996) Epigenetic control of mammalian centromere protein binding: does DNA methylation have a role? J Cell Sci 109(Pt 9):2199–2206
Mohibi S, Srivastava S, Wang-France J et al (2015) Alteration/deficiency in activation 3 (ADA3) protein, a cell cycle regulator, associates with the centromere through CENP-B and regulates chromosome segregation. J Biol Chem 290:28299–28310. doi:10.1074/jbc.M115.685511
Moree B, Meyer CB, Fuller CJ, Straight AF (2011) CENP-C recruits M18BP1 to centromeres to promote CENP-A chromatin assembly. J Cell Biol 194:855–871. doi:10.1083/jcb.201106079
Mravinac B, Ugarković E, Franjević D, Plohl M (2005) Long inversely oriented subunits form a complex monomer of Tribolium brevicornis satellite DNA. J Mol Evol 60:513–525. doi:10.1007/s00239-004-0236-z
Murakami Y, Huberman JA, Hurwitz J (1996) Identification, purification, and molecular cloning of autonomously replicating sequence-binding protein 1 from fission yeast Schizosaccharomyces pombe. Proc Natl Acad Sci USA 93:502–507
Muro Y, Masumoto H, Yoda K et al (1992) Centromere protein B assembles human centromeric alpha-satellite DNA at the 17-bp sequence, CENP-B box. J Cell Biol 116:585–596
Murray AW, Szostak JW (1983) Construction of artificial chromosomes in yeast. Nature 305:189–193
Murray AW, Szostak JW (1986) Construction and behavior of circularly permuted and telocentric chromosomes in Saccharomyces cerevisiae. Mol Cell Biol 6:3166–3172
Nakagawa H, Lee J-K, Hurwitz J et al (2002) Fission yeast CENP-B homologs nucleate centromeric heterochromatin by promoting heterochromatin-specific histone tail modifications. Genes Dev 16:1766–1778. doi:10.1101/gad.997702
Ng R, Carbon J (1987) Mutational and in vitro protein-binding studies on centromere DNA from Saccharomyces cerevisiae. Mol Cell Biol 7:4522–4534. doi:10.1128/MCB.7.12.4522
Nishino T, Takeuchi K, Gascoigne KE et al (2012) CENP-T-W-S-X forms a unique centromeric chromatin structure with a histone-like fold. Cell 148:487–501. doi:10.1016/j.cell.2011.11.061
Noma K-I, Cam HP, Maraia RJ, Grewal SIS (2006) A role for TFIIIC transcription factor complex in genome organization. Cell 125:859–872. doi:10.1016/j.cell.2006.04.028
Noveski P, Madjunkova S, Sukarova Stefanovska E et al (2016) Loss of Y chromosome in peripheral blood of colorectal and prostate cancer patients. PLOS One 11:e0146264. doi:10.1371/journal.pone.0146264
Ohzeki J-I, Nakano M, Okada T, Masumoto H (2002) CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J Cell Biol 159:765–775. doi:10.1083/jcb.200207112
Ohzeki J-I, Bergmann JH, Kouprina N et al (2012) Breaking the HAC Barrier: Histone H3K9 acetyl/methyl balance regulates CENP-A assembly. EMBO J 31:2391–2402. doi:10.1038/emboj.2012.82
Okada T, Ohzeki J-I, Nakano M et al (2007) CENP-B controls centromere formation depending on the chromatin context. Cell 131:1287–1300. doi:10.1016/j.cell.2007.10.045
Okamoto Y, Nakano M, Ohzeki J-I et al (2007) A minimal CENP-A core is required for nucleation and maintenance of a functional human centromere. EMBO J 26:1279–1291. doi:10.1038/sj.emboj.7601584
Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257
Olszak AM, van Essen D, Pereira AJ et al (2011) Heterochromatin boundaries are hotspots for de novo kinetochore formation. Nat Cell Biol 13:799–808. doi:10.1038/ncb2272
Orpinell M, Fournier M, Riss A et al (2010) The ATAC acetyl transferase complex controls mitotic progression by targeting non-histone substrates. EMBO J 29:2381–2394. doi:10.1038/emboj.2010.125
Palmer DK, O’Day K, Wener MH et al (1987) A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J Cell Biol 104:805–815
Perez-Castro AV, Shamanski FL, Meneses JJ et al (1998) Centromeric protein B null mice are viable with no apparent abnormalities. Dev Biol 201:135–143. doi:10.1006/dbio.1998.9005
Plohl M, Meštrović N, Mravinac B (2014) Centromere identity from the DNA point of view. Chromosoma 123:313–325. doi:10.1007/s00412-014-0462-0
Politi V, Perini G, Trazzi S et al (2002) CENP-C binds the alpha-satellite DNA in vivo at specific centromere domains. J Cell Sci 115:2317–2327
Quénet D, Dalal Y (2014) A long non-coding RNA is required for targeting centromeric protein A to the human centromere. eLife 3:e03254. doi:10.7554/eLife.03254
Régnier V, Novelli J, Fukagawa T et al (2003) Characterization of chicken CENP-A and comparative sequence analysis of vertebrate centromere-specific histone H3-like proteins. Gene 316:39–46. doi:10.1016/S0378-1119(03)00768-6
Romanova LY, Deriagin GV, Mashkova TD et al (1996) Evidence for selection in evolution of alpha satellite DNA: the central role of CENP-B/pJ alpha binding region. J Mol Biol 261:334–340. doi:10.1006/jmbi.1996.0466
Rosandić M, Paar V, Basar I et al (2006) CENP-B box and pJalpha sequence distribution in human alpha satellite higher-order repeats (HOR). Chromosome Res 14:735–753. doi:10.1007/s10577-006-1078-x
Rosandić M, Glunčić M, Paar V, Basar I (2008) The role of alphoid higher order repeats (HORs) in the centromere folding. J Theor Biol 254:555–560. doi:10.1016/j.jtbi.2008.06.012
Rošić S, Erhardt S (2016) No longer a nuisance: long non-coding RNAs join CENP-A in epigenetic centromere regulation. Cell Mol Life Sci 73:1387–1398. doi:10.1007/s00018-015-2124-7
Rošić S, Köhler F, Erhardt S (2014) Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division. J Cell Biol 207:335–349. doi:10.1083/jcb.201404097
Rudd MK, Willard HF (2004) Analysis of the centromeric regions of the human genome assembly. Trends Genet 20:529–533. doi:10.1016/j.tig.2004.08.008
Rudd MK, Wray GA, Willard HF (2006) The evolutionary dynamics of alpha-satellite. Genome Res 16:88–96. doi:10.1101/gr.3810906
Schueler MG, Higgins AW, Rudd MK et al (2001) Genomic and genetic definition of a functional human centromere. Science 294:109–115. doi:10.1126/science.1065042
Scott KC, Merrett SL, Willard HF (2006) A heterochromatin barrier partitions the fission yeast centromere into discrete chromatin domains. Curr Biol 16:119–129. doi:10.1016/j.cub.2005.11.065
Shang W-H, Hori T, Toyoda A et al (2010) Chickens possess centromeres with both extended tandem repeats and short non-tandem-repetitive sequences. Genome Res 20:1219–1228. doi:10.1101/gr.106245.110
Shang W-H, Hori T, Martins NMC et al (2013) Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell 24:635–648. doi:10.1016/j.devcel.2013.02.009
Shepelev VA, Alexandrov AA, Yurov YB, Alexandrov IA (2009) The evolutionary origin of man can be traced in the layers of defunct ancestral alpha satellites flanking the active centromeres of human chromosomes. PLoS Genet 5:e1000641. doi:10.1371/journal.pgen.1000641
Shono N, Ohzeki J-I, Otake K et al (2015) CENP-C and CENP-I are key connecting factors for kinetochore and CENP-A assembly. J Cell Sci 128:4572–4587. doi:10.1242/jcs.180786
Smit AF, Riggs AD (1996) Tiggers and DNA transposon fossils in the human genome. Proc Natl Acad Sci USA 93:1443–1448
Smith KM, Galazka JM, Phatale PA et al (2012) Centromeres of filamentous fungi. Chromosome Res 20:635–656. doi:10.1007/s10577-012-9290-3
Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M (1995) A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev 9:573–586. doi:10.1101/gad.9.5.573
Sugimoto K, Yata H, Muro Y, Himeno M (1994) Human centromere protein C (CENP-C) is a DNA-binding protein which possesses a novel DNA-binding motif. J Biochem 116:877–881
Sugimoto K, Kuriyama K, Shibata A, Himeno M (1997) Characterization of internal DNA-binding and C-terminal dimerization domains of human centromere/kinetochore autoantigen CENP-C in vitro: role of DNA-binding and self-associating activities in kinetochore organization. Chromosome Res 5:132–141
Sullivan KF (1994) Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol 127:581–592. doi:10.1083/jcb.127.3.581
Sullivan KF, Glass CA (1991) CENP-B is a highly conserved mammalian centromere protein with homology to the helix-loop-helix family of proteins. Chromosoma 100:360–370
Sullivan BA, Willard HF (1998) Stable dicentric X chromosomes with two functional centromeres. Nat Genet 20:227–228. doi:10.1038/3024
Suntronpong A, Kugou K, Masumoto H et al (2016) CENP-B box, a nucleotide motif involved in centromere formation, occurs in a New World monkey. Biol Lett 12:20150817. doi:10.1098/rsbl.2015.0817
Suzuki N, Nakano M, Nozaki N et al (2004) CENP-B interacts with CENP-C domains containing Mif2 regions responsible for centromere localization. J Biol Chem 279:5934–5946. doi:10.1074/jbc.M306477200
Tachiwana H, Miya Y, Shono N et al (2013) Nap1 regulates proper CENP-B binding to nucleosomes. Nucleic Acids Res 41:2869–2880. doi:10.1093/nar/gks1464
Takahashi K (2000) Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science 288:2215–2219. doi:10.1126/science.288.5474.2215
Tanaka Y, Nureki O, Kurumizaka H et al (2001) Crystal structure of the CENP-B protein-DNA complex: the DNA-binding domains of CENP-B induce kinks in the CENP-B box DNA. EMBO J 20:6612–6618. doi:10.1093/emboj/20.23.6612
Tanaka Y, Kurumizaka H, Yokoyama S (2004) CpG methylation of the CENP-B box reduces human CENP-B binding. FEBS J 272:282–289. doi:10.1111/j.1432-1033.2004.04406.x
Tawaramoto MS, Park SY, Tanaka Y et al (2003) Crystal structure of the human centromere protein B (CENP-B) dimerization domain at 1.65-A resolution. J Biol Chem 278:51454–51461. doi:10.1074/jbc.M310388200
Taylor SS, Larin Z, Tyler-Smith C (1996) Analysis of extrachromosomal structures containing human centromeric alphoid satellite DNA sequences in mouse cells. Chromosoma 105:70–81
Thakur J, Henikoff S (2016) CENPT bridges adjacent CENPA nucleosomes on young human α-satellite dimers. Genome Res 26:1178–1187. doi:10.1101/gr.204784.116
Tsuduki T, Nakano M, Yasuoka N et al (2006) An artificially constructed de novo human chromosome behaves almost identically to its natural counterpart during metaphase and anaphase in living cells. Mol Cell Biol 26:7682–7695. doi:10.1128/MCB.00355-06
Ventura M, Antonacci F, Cardone MF et al (2007) Evolutionary formation of new centromeres in macaque. Science 316:243–246. doi:10.1126/science.1140615
Vissel B, Choo KH (1987) Human alpha satellite DNA–consensus sequence and conserved regions. Nucleic Acids Res 15:6751–6752
Voullaire LE, Slater HR, Petrovic V, Choo KH (1993) A functional marker centromere with no detectable alpha-satellite, satellite III, or CENP-B protein: activation of a latent centromere? Am J Hum Genet 52:1153–1163
Wade CM, Giulotto E, Sigurdsson S et al (2009) Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 326:865–867. doi:10.1126/science.1178158
Warren WC, Jasinska AJ, García-Pérez R et al (2015) The genome of the vervet (Chlorocebus aethiops sabaeus). Genome Res 25:1921–1933. doi:10.1101/gr.192922.115
Waye JS, Willard HF (1986) Structure, organization, and sequence of alpha satellite DNA from human chromosome 17: evidence for evolution by unequal crossing-over and an ancestral pentamer repeat shared with the human X chromosome. Mol Cell Biol 6:3156–3165
Weaver BAA, Silk AD, Montagna C et al (2007) Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell 11:25–36. doi:10.1016/j.ccr.2006.12.003
Wevrick R, Willard HF (1991) Physical map of the centromeric region of human chromosome 7: relationship between two distinct alpha satellite arrays. Nucleic Acids Res 19:2295–2301
Wijmenga C, van den Heuvel LP, Strengman E et al (1998) Localization of the ICF syndrome to chromosome 20 by homozygosity mapping. Am J Hum Genet 63:803–809. doi:10.1086/302021
Willard HF (1985) Chromosome-specific organization of human alpha satellite DNA. Am J Hum Genet 37:524–532
Willard HF, Waye JS (1987) Chromosome-specific subsets of human alpha satellite DNA: analysis of sequence divergence within and between chromosomal subsets and evidence for an ancestral pentameric repeat. J Mol Evol 25:207–214
Woo SS, Jiang J, Gill BS et al (1994) Construction and characterization of a bacterial artificial chromosome library of Sorghum bicolor. Nucleic Acids Res 22:4922–4931
Wood L, Booth DG, Vargiu G et al (2016) Auxin/AID versus conventional knockouts: distinguishing the roles of CENP-T/W in mitotic kinetochore assembly and stability. Open Biol 6:150230. doi:10.1098/rsob.150230
Wu JC, Manuelidis L (1980) Sequence definition and organization of a human repeated DNA. J Mol Biol 142:363–386. doi:10.1016/0022-2836(80)90277-6
Xu GL, Bestor TH, Bourc’his D et al (1999) Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402:187–191. doi:10.1038/46052
Yang CH, Tomkiel J, Saitoh H et al (1996) Identification of overlapping DNA-binding and centromere-targeting domains in the human kinetochore protein CENP-C. Mol Cell Biol 16:3576–3586
Yoda K, Kitagawa K, Masumoto H et al (1992) A human centromere protein, CENP-B, has a DNA binding domain containing four potential alpha helices at the NH2 terminus, which is separable from dimerizing activity. J Cell Biol 119:1413–1427
Yoda K, Nakamura T, Masumoto H et al (1996) Centromere protein B of African green monkey cells: gene structure, cellular expression, and centromeric localization. Mol Cell Biol 16:5169–5177
Yoda K, Ando S, Okuda A et al (1998) In vitro assembly of the CENP-B/alpha-satellite DNA/core histone complex: CENP-B causes nucleosome positioning. Genes Cells 3:533–548
Zaratiegui M, Vaughn MW, Irvine DV et al (2011) CENP-B preserves genome integrity at replication forks paused by retrotransposon LTR. Nature 469:112–115. doi:10.1038/nature09608
Zedek F, Bureš P (2016) CenH3 evolution reflects meiotic symmetry as predicted by the centromere drive model. 6:33308. doi:10.1038/srep33308 (Nature Publishing Group)
Acknowledgements
The authors would like to thank I. Drinnenberg (Institut Curie, Paris), H. Masumoto (Kazusa, JP), S. McClelland (BCI, UK), K.H. Miga (UCSC, US), C. Bartocci (Institut Curie, Paris), P. Ly (Ludwig, UCSD, La Jolla), A. Musacchio (Max Planck Dortmund, Germany) and all members of the Fachinetti lab for helpful suggestions and discussion. We also thank Y. Nechemia-Arbely and D.W. Cleveland (Ludwig, UCSD, La Jolla), S. Kasinathan and S. Henikoff (FHCRC, Seattle, US), A. Straight (Stanford, US) and V. Costanzo (IFOM, Italy) for sharing unpublished results or observations. We apologize to our colleagues whose important contributions could not be cited due to space constraints. D.F. receives salary support from the CNRS. D.F. has received support by Labex «CelTisPhyBio», the Institut Curie and the ATIP-Avenir 2015 program. This work has also received support under the program “Investissements d’Avenir,” launched by the French Government and implemented by ANR with the references ANR-10-LABX-0038 and ANR-10-IDEX-0001-02 PSL.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Dumont, M., Fachinetti, D. (2017). DNA Sequences in Centromere Formation and Function. In: Black, B. (eds) Centromeres and Kinetochores. Progress in Molecular and Subcellular Biology, vol 56. Springer, Cham. https://doi.org/10.1007/978-3-319-58592-5_13
Download citation
DOI: https://doi.org/10.1007/978-3-319-58592-5_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-58591-8
Online ISBN: 978-3-319-58592-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)