Critical Foundation of the Kinetochore: The Constitutive Centromere-Associated Network (CCAN)

  • Masatoshi Hara
  • Tatsuo FukagawaEmail author
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 56)


The kinetochore is a large protein complex, which is assembled at the centromere of a chromosome to ensure faithful chromosome segregation during M-phase. The centromere in most eukaryotes is epigenetically specified by DNA sequence-independent mechanisms. The constitutive centromere-associated network (CCAN) is a subcomplex in the kinetochore that localizes to the centromere throughout the cell cycle. The CCAN has interfaces bound to the centromeric chromatin and the spindle microtubule-binding complex; therefore, it functions as a foundation of kinetochore formation. Here, we summarize recent progress in our understanding of the structure and organization of the CCAN. We also discuss an additional role of the CCAN in the maintenance of centromere position and dynamic reorganization of the CCAN.



The authors thank Tetsuya Hori and other members in the Fukagawa Lab for helpful discussions. This work is supported by JSPS KAKENHI Grant Numbers P25221106, JP16H06279, and JP15H05972 to TF and JP16K18491 to MH.


  1. Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL, Arellano-Santoyo H, Gonen T, Ranish JA, Asbury CL, Biggins S (2010) Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468:576–579. doi: 10.1038/nature09594 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Albertson DG, Thomson JN (1982) The kinetochores of Caenorhabditis elegans. Chromosoma. doi: 10.1007/BF00292267 PubMedGoogle Scholar
  3. Aldrup-Macdonald ME, Sullivan BA (2014) The past, present, and future of human centromere genomics. Genes (Basel) 5:33–50. doi: 10.3390/genes5010033 CrossRefGoogle Scholar
  4. Amano M, Suzuki A, Hori T, Backer C, Okawa K, Cheeseman IM, Fukagawa T (2009) The CENP-S complex is essential for the stable assembly of outer kinetochore structure. J Cell Biol 186:173–182. doi: 10.1083/jcb.200903100 PubMedPubMedCentralCrossRefGoogle Scholar
  5. Amaro AC, Samora CP, Holtackers R, Wang E, Kingston IJ, Alonso M, Lampson M, McAinsh AD, Meraldi P (2010) Molecular control of kinetochore-microtubule dynamics and chromosome oscillations. Nat Cell Biol 12:319–329. doi: 10.1038/ncb2033 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bailey AO, Panchenko T, Shabanowitz J, Lehman SM, Bai DL, Hunt DF, Black BE, Foltz DR (2016) Identification of the post-translational modifications present in centromeric chromatin. Mol Cell Proteomics 15:918–931. doi: 10.1074/mcp.M115.053710 PubMedCrossRefGoogle Scholar
  7. Barnhart MC, Kuich PHJL, Stellfox ME, Ward JA, Bassett EA, Black BE, Foltz DR (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J Cell Biol 194:229–243. doi: 10.1083/jcb.201012017 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Basilico F, Maffini S, Weir JR, Prumbaum D, Rojas AM, Zimniak T, De Antoni A, Jeganathan S, Voss B, van Gerwen S, Krenn V, Massimiliano L, Valencia A, Vetter IR, Herzog F, Raunser S, Pasqualato S, Musacchio A (2014) The pseudo GTPase CENP-M drives human kinetochore assembly. Elife 3:e02978. doi: 10.7554/eLife.02978 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Benson KR (2001) T.H. Morgan’s resistance to the chromosome theory. Nat Rev Genet 2:469–474. doi: 10.1038/35076532 PubMedCrossRefGoogle Scholar
  10. Bergmann JH, Martins NMC, Larionov V, Masumoto H, Earnshaw WC (2012) HACking the centromere chromatin code: insights from human artificial chromosomes. Chromosome Res 20:505–519. doi: 10.1007/s10577-012-9293-0 PubMedCrossRefGoogle Scholar
  11. Bergmann JH, Rodríguez MG, Martins NMC, Kimura H, Kelly DA, Masumoto H, Larionov V, Jansen LET, Earnshaw WC (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 PubMedCrossRefGoogle Scholar
  12. Birchler JA (2015) Mendel, mechanism, models, marketing, and more. Cell 163:9–11. doi: 10.1016/j.cell.2015.09.008 PubMedCrossRefGoogle Scholar
  13. Blower MD, Karpen GH (2001) The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat Cell Biol 3:730–739. doi: 10.1038/35087045 PubMedPubMedCentralCrossRefGoogle Scholar
  14. Blower MD, Sullivan BA, Karpen GH (2002) Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2:319–330PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bock LJ, Pagliuca C, Kobayashi N, Grove RA, Oku Y, Shrestha K, Alfieri C, Golfieri C, Oldani A, Dal Maschio M, Bermejo R, Hazbun TR, Tanaka TU, De Wulf P (2012) Cnn1 inhibits the interactions between the KMN complexes of the yeast kinetochore. Nat Cell Biol 14:614–624. doi: 10.1038/ncb2495 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Boveri T (1904) Ergebnisse über die Konstitution der chromatischen Substanz des Zellkerns. Verlag von Gustav Fischer, JenaCrossRefGoogle Scholar
  17. Brown MT (1995) Sequence similarities between the yeast chromosome segregation protein Mif2 and the mammalian centromere protein CENP-C. Gene 160:111–116. doi: 10.1016/0378-1119(95)00163-Z PubMedCrossRefGoogle Scholar
  18. Brown MT, Goetsch L, Hartwell LH (1993) MIF2 is required for mitotic spindle integrity during anaphase spindle elongation in Saccharomyces cerevisiae. J Cell Biol 123:387–403PubMedCrossRefGoogle Scholar
  19. Buchwitz BJ, Ahmad K, Moore LL, Roth MB, Henikoff S (1999) A histone-H3-like protein in C. elegans. Nature 401:547–548. doi: 10.1038/44062 PubMedCrossRefGoogle Scholar
  20. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Carroll CW, Silva MCC, Godek KM, Jansen LET, Straight AF (2009) Centromere assembly requires the direct recognition of CENP-A nucleosomes by CENP-N. Nat Cell Biol 11:896–902. doi: 10.1038/ncb1899 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643–655. doi: 10.1016/S0092-8674(03)00392-1 PubMedCrossRefGoogle Scholar
  23. Cheeseman IM, Chappie JS, Wilson-Kubalek EM, Desai A (2006) The conserved KMN network constitutes the core microtubule-binding site of the kinetochore. Cell 127:983–997. doi: 10.1016/j.cell.2006.09.039 PubMedCrossRefGoogle Scholar
  24. Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore-microtubule interface. Nat Rev Mol Cell Biol 9:33–46. doi: 10.1038/nrm2310 PubMedCrossRefGoogle Scholar
  25. Chen C-C, Dechassa ML, Bettini E, Ledoux MB, Belisario C, Heun P, Luger K, Mellone BG (2014) CAL1 is the Drosophila CENP-A assembly factor. J Cell Biol 204:313–329. doi: 10.1083/jcb.201305036 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Clarke L (1998) Centromeres: proteins, protein complexes, and repeated domains at centromeres of simple eukaryotes. Curr Opin Genet Dev 8:212–218. doi: 10.1016/S0959-437X(98)80143-3 PubMedCrossRefGoogle Scholar
  27. Correns CE (1900) G. Mendel’s Regel über das Verhalten der Nachkommenschaft der Rassenbastarde. Berichte der Deutsche Botanischen 18:158–168. doi: 10.1111/j.1438-8677.1900.tb04893.x Google Scholar
  28. Darlington CD (1936) The external mechanics of the chromosomes. Proc R Soc Lond 121:264–319. doi: 10.2307/82059 CrossRefGoogle Scholar
  29. de Vries H (1900) Sur la loi de disjonction des hybrides. Comptes rendus de l’Académie des Sciences 130:845–847Google Scholar
  30. De Wulf P, McAinsh AD, Sorger PK (2003) Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev 17:2902–2921. doi: 10.1101/gad.1144403 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Dernburg AF (2001) Here, there, and everywhere. J Cell Biol 153:F33–F38. doi: 10.1083/jcb.153.6.F33 PubMedPubMedCentralCrossRefGoogle Scholar
  32. Drinnenberg IA, deYoung D, Henikoff S, Malik HS (2014) Recurrent loss of CenH3 is associated with independent transitions to holocentricity in insects. Elife 3:2104–2119. doi: 10.7554/eLife.03676 CrossRefGoogle Scholar
  33. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Dunleavy EM, Roche D, Tagami H, Lacoste N, Ray-Gallet D, Nakamura Y, Daigo Y, Nakatani Y, Almouzni-Pettinotti G (2009) HJURP is a cell-cycle-dependent maintenance and deposition factor of CENP-A at centromeres. Cell 137:485–497. doi: 10.1016/j.cell.2009.02.040 PubMedCrossRefGoogle Scholar
  35. Earnshaw WC, Rothfield N (1985) Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91:313–321PubMedCrossRefGoogle Scholar
  36. Falk SJ, Guo LY, Sekulic N, Smoak EM, Mani T, Logsdon GA, Gupta K, Jansen LET, Van Duyne GD, Vinogradov SA, Lampson MA, Black BE (2015) Chromosomes. CENP-C reshapes and stabilizes CENP-A nucleosomes at the centromere. Science 348:699–703. doi: 10.1126/science.1259308 PubMedPubMedCentralCrossRefGoogle Scholar
  37. Falk SJ, Lee J, Sekulic N, Sennett MA, Lee T-H, Black BE (2016) CENP-C directs a structural transition of CENP-A nucleosomes mainly through sliding of DNA gyres. Nat Struct Mol Biol 23:204–208. doi: 10.1038/nsmb.3175 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Flemming W (1882) Zellsubstanz, kern und zelltheilung. F.C.W. Vogel, LeipzigGoogle Scholar
  39. Foley EA, Kapoor TM (2013) Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat Rev Mol Cell Biol 14:25–37. doi: 10.1038/nrm3494 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Foltz DR, Jansen LET, Bailey AO, Yates JR, Bassett EA, Wood S, Black BE, Cleveland DW (2009) Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137:472–484. doi: 10.1016/j.cell.2009.02.039 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Foltz DR, Jansen LET, Black BE, Bailey AO, Yates JR, Cleveland DW (2006) The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8:458–469. doi: 10.1038/ncb1397 PubMedCrossRefGoogle Scholar
  42. Fukagawa T, Brown W (1997) Efficient conditional mutation of the vertebrate CENP-C gene. Hum Mol Genet. doi: 10.1093/hmg/6.13.2301 PubMedGoogle Scholar
  43. Fukagawa T, Earnshaw WC (2014a) The centromere: chromatin foundation for the kinetochore machinery. Dev Cell 30:496–508. doi: 10.1016/j.devcel.2014.08.016 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Fukagawa T, Earnshaw WC (2014b) Neocentromeres. Curr Biol 24:R946–R947. doi: 10.1016/j.cub.2014.08.032 PubMedCrossRefGoogle Scholar
  45. Fukagawa T, Mikami Y, Nishihashi A, Regnier V, Haraguchi T, Hiraoka Y, Sugata N, Todokoro K, Brown W, Ikemura T (2001) CENP-H, a constitutive centromere component, is required for centromere targeting of CENP-C in vertebrate cells. EMBO J 20:4603–4617. doi: 10.1093/emboj/20.16.4603 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Fukagawa T, Pendon C, Morris J, Brown W (1999) CENP-C is necessary but not sufficient to induce formation of a functional centromere. EMBO J 18:4196–4209. doi: 10.1093/emboj/18.15.4196 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Gascoigne KE, Takeuchi K, Suzuki A, Hori T, Fukagawa T, Cheeseman IM (2011) Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 145:410–422. doi: 10.1016/j.cell.2011.03.031 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Goshima G, Kiyomitsu T, Yoda K, Yanagida M (2003) Human centromere chromatin protein hMis12, essential for equal segregation, is independent of CENP-A loading pathway. J Cell Biol 160:25–39. doi: 10.1083/jcb.200210005 PubMedPubMedCentralCrossRefGoogle Scholar
  49. Harrington JJ, Van Bokkelen G, Mays RW, Gustashaw K, Willard HF (1997) Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat Genet 15:345–355. doi: 10.1038/ng0497-345 PubMedCrossRefGoogle Scholar
  50. Heeger S, Leismann O, Schittenhelm R, Schraidt O, Heidmann S, Lehner CF (2005) Genetic interactions of separase regulatory subunits reveal the diverged Drosophila Cenp-C homolog. Genes Dev 19:2041–2053. doi: 10.1101/gad.347805 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hegemann JH, Fleig UN (1993) The centromere of budding yeast. BioEssays 15:451–460. doi: 10.1002/bies.950150704 PubMedCrossRefGoogle Scholar
  52. Hemmerich P, Weidtkamp-Peters S, Hoischen C, Schmiedeberg L, Erliandri I, Diekmann S (2008) Dynamics of inner kinetochore assembly and maintenance in living cells. J Cell Biol 180:1101–1114. doi: 10.1083/jcb.200710052 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Heun P, Erhardt S, Blower MD, Weiss S, Skora AD, Karpen GH (2006) Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell 10:303–315. doi: 10.1016/j.devcel.2006.01.014 PubMedPubMedCentralCrossRefGoogle Scholar
  54. Holland S, Ioannou D, Haines S, Brown WRA (2005) Comparison of Dam tagging and chromatin immunoprecipitation as tools for the identification of the binding sites for S. pombe CENP-C. Chromosome Res 13:73–83. doi: 10.1007/s10577-005-7062-z PubMedCrossRefGoogle Scholar
  55. Hori T, Amano M, Suzuki A, Backer CB, Welburn JP, Dong Y, McEwen BF, Shang W-H, Suzuki E, Okawa K, Cheeseman IM, Fukagawa T (2008a) CCAN makes multiple contacts with centromeric DNA to provide distinct pathways to the outer kinetochore. Cell 135:1039–1052. doi: 10.1016/j.cell.2008.10.019 PubMedCrossRefGoogle Scholar
  56. Hori T, Kagawa N, Toyoda A, Fujiyama A, Misu S, Monma N, Makino F, Ikeo K, Fukagawa T (2017) Constitutive centromere-associated network controls centromere drift in vertebrate cells. J Cell Biol 216:101–113. doi: 10.1083/jcb.201605001 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hori T, Okada M, Maenaka K, Fukagawa T (2008b) CENP-O class proteins form a stable complex and are required for proper kinetochore function. Mol Biol Cell 19:843–854. doi: 10.1091/mbc.E07-06-0556 PubMedPubMedCentralCrossRefGoogle Scholar
  58. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hori T, Shang W-H, Toyoda A, Misu S, Monma N, Ikeo K, Molina O, Vargiu G, Fujiyama A, Kimura H, Earnshaw WC, Fukagawa T (2014) Histone H4 Lys 20 monomethylation of the CENP-A nucleosome is essential for kinetochore assembly. Dev Cell 29:740–749. doi: 10.1016/j.devcel.2014.05.001 PubMedPubMedCentralCrossRefGoogle Scholar
  60. Howman EV, Fowler KJ, Newson AJ, Redward S, MacDonald AC, Kalitsis P, Choo KH (2000) Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc Natl Acad Sci USA 97:1148–1153PubMedPubMedCentralCrossRefGoogle Scholar
  61. Hua S, Wang Z, Jiang K, Huang Y, Ward T, Zhao L, Dou Z, Yao X (2011) CENP-U cooperates with Hec1 to orchestrate kinetochore-microtubule attachment. J Biol Chem 286:1627–1638. doi: 10.1074/jbc.M110.174946 PubMedCrossRefGoogle Scholar
  62. Ikeno M, Grimes B, Okazaki T, Nakano M, Saitoh K, Hoshino H, McGill NI, Cooke H, Masumoto H (1998) Construction of YAC-based mammalian artificial chromosomes. Nat Biotechnol 16:431–439. doi: 10.1038/nbt0598-431 PubMedCrossRefGoogle Scholar
  63. Ishii K, Ogiyama Y, Chikashige Y, Soejima S, Masuda F, Kakuma T, Hiraoka Y, Takahashi K (2008) Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science 321:1088–1091. doi: 10.1126/science.1158699 PubMedCrossRefGoogle Scholar
  64. Izuta H, Ikeno M, Suzuki N, Tomonaga T, Nozaki N, Obuse C, Kisu Y, Goshima N, Nomura F, Nomura N, Yoda K (2006) Comprehensive analysis of the ICEN (interphase centromere complex) components enriched in the CENP-A chromatin of human cells. Genes Cells 11:673–684. doi: 10.1111/j.1365-2443.2006.00969.x PubMedCrossRefGoogle Scholar
  65. Jansen LET, Black BE, Foltz DR, Cleveland DW (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176:795–805. doi: 10.1083/jcb.200701066 PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kagawa N, Hori T, Hoki Y, Hosoya O, Tsutsui K, Saga Y, Sado T, Fukagawa T (2014) The CENP-O complex requirement varies among different cell types. Chromosome Res 22:293–303. doi: 10.1007/s10577-014-9404-1 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kato H, Jiang J, Zhou B-R, Rozendaal M, Feng H, Ghirlando R, Xiao TS, Straight AF, Bai Y (2013) A conserved mechanism for centromeric nucleosome recognition by centromere protein CENP-C. Science 340:1110–1113. doi: 10.1126/science.1235532 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Ketel C, Wang HSW, McClellan M, Bouchonville K, Selmecki A, Lahav T, Gerami-Nejad M, Berman J (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5:e1000400. doi: 10.1371/journal.pgen.1000400 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kim S, Yu H (2015) Multiple assembly mechanisms anchor the KMN spindle checkpoint platform at human mitotic kinetochores. J Cell Biol 208:181–196. doi: 10.1083/jcb.201407074 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Klare K, Weir JR, Basilico F, Zimniak T, Massimiliano L, Ludwigs N, Herzog F, Musacchio A (2015) CENP-C is a blueprint for constitutive centromere-associated network assembly within human kinetochores. J Cell Biol 210:11–22. doi: 10.1083/jcb.201412028 PubMedCrossRefGoogle Scholar
  71. Kursel LE, Malik HS (2016) Centromeres. Curr Biol 26:R487–R490. doi: 10.1016/j.cub.2016.05.031 PubMedCrossRefGoogle Scholar
  72. Kwon M-S, Hori T, Okada M, Fukagawa T (2007) CENP-C is involved in chromosome segregation, mitotic checkpoint function, and kinetochore assembly. Mol Biol Cell 18:2155–2168. doi: 10.1091/mbc.E07-01-0045 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Locke DP, Hillier LW, Warren WC, Worley KC, Nazareth LV, Muzny DM, Yang S-P, Wang Z, Chinwalla AT, Minx P, Mitreva M, Cook L, Delehaunty KD, Fronick C, Schmidt H, Fulton LA, Fulton RS, Nelson JO, Magrini V, Pohl C, Graves TA, Markovic C, Cree A, Dinh HH, Hume J, Kovar CL, Fowler GR, Lunter G, Meader S, Heger A, Ponting CP, Marques-Bonet T, Alkan C, Chen L, Cheng Z, Kidd JM, Eichler EE, White S, Searle S, Vilella AJ, Chen Y, Flicek P, Ma J, Raney B, Suh B, Burhans R, Herrero J, Haussler D, Faria R, Fernando O, Darré F, Farré D, Gazave E, Oliva M, Navarro A, Roberto R, Capozzi O, Archidiacono N, Valle Della G, Purgato S, Rocchi M, Konkel MK, Walker JA, Ullmer B, Batzer MA, Smit AFA, Hubley R, Casola C, Schrider DR, Hahn MW, Quesada V, Puente XS, Ordoñez GR, López-Otín C, Vinar T, Brejova B, Ratan A, Harris RS, Miller W, Kosiol C, Lawson HA, Taliwal V, Martins AL, Siepel A, Roychoudhury A, Ma X, Degenhardt J, Bustamante CD, Gutenkunst RN, Mailund T, Dutheil JY, Hobolth A, Schierup MH, Ryder OA, Yoshinaga Y, de Jong PJ, Weinstock GM, Rogers J, Mardis ER, Gibbs RA, Wilson RK (2011) Comparative and demographic analysis of orang-utan genomes. Nature 469:529–533. doi: 10.1038/nature09687 PubMedPubMedCentralCrossRefGoogle Scholar
  74. London N, Biggins S (2014) Signalling dynamics in the spindle checkpoint response. Nat Rev Mol Cell Biol 15:736–747. doi: 10.1038/nrm3888 PubMedPubMedCentralCrossRefGoogle Scholar
  75. Maresca TJ, Salmon ED (2009) Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity. J Cell Biol 184:373–381. doi: 10.1083/jcb.200808130 PubMedPubMedCentralCrossRefGoogle Scholar
  76. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  77. McClelland SE, Borusu S, Amaro AC, Winter JR, Belwal M, McAinsh AD, Meraldi P (2007) The CENP-A NAC/CAD kinetochore complex controls chromosome congression and spindle bipolarity. EMBO J 26:5033–5047. doi: 10.1038/sj.emboj.7601927 PubMedPubMedCentralCrossRefGoogle Scholar
  78. McKinley KL, Cheeseman IM (2016) The molecular basis for centromere identity and function. Nat Rev Mol Cell Biol 17:16–29PubMedCrossRefGoogle Scholar
  79. McKinley KL, Sekulic N, Guo LY, Tsinman T, Black BE, Cheeseman IM (2015) The CENP-L-N complex forms a critical node in an integrated meshwork of interactions at the centromere-kinetochore interface. Mol Cell 60:886–898. doi: 10.1016/j.molcel.2015.10.027 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Meluh PB, Koshland D (1995) Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the Mammalian centromere protein CENP-C. Mol Biol Cell 6:793–807. doi: 10.1091/mbc.6.7.793 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Mendiburo MJ, Padeken J, Fülöp S, Schepers A, Heun P (2011) Drosophila CENH3 is sufficient for centromere formation. Science 334:686–690. doi: 10.1126/science.1206880 PubMedCrossRefGoogle Scholar
  82. Milks KJ, Moree B, Straight AF (2009) Dissection of CENP-C-directed centromere and kinetochore assembly. Mol Biol Cell 20:4246–4255. doi: 10.1091/mbc.E09-05-0378 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Miller MP, Asbury CL, Biggins S (2016) A TOG protein confers tension sensitivity to kinetochore-microtubule attachments. Cell 165:1428–1439. doi: 10.1016/j.cell.2016.04.030 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Minoshima Y, Hori T, Okada M, Kimura H, Haraguchi T, Hiraoka Y, Bao Y-C, Kawashima T, Kitamura T, Fukagawa T (2005) The constitutive centromere component CENP-50 is required for recovery from spindle damage. Mol Cell Biol 25:10315–10328. doi: 10.1128/MCB.25.23.10315-10328.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631–642. doi: 10.1016/S0092-8674(03)00393-3 PubMedCrossRefGoogle Scholar
  86. Moore LL, Roth MB (2001) Hcp-4, a Cenp-C–Like protein in Caenorhabditis elegans, is required for resolution of sister centromeres. J Cell Biol 153:1199–1208. doi: 10.1083/jcb.153.6.1199 PubMedPubMedCentralCrossRefGoogle Scholar
  87. Morgan TH (1915) The mechanism of Mendelian heredity. HoltGoogle Scholar
  88. Murakami A, Imai HT (1974) Cytological evidence for holocentric chromosomes of the silkworms, Bombyx mori and B. mandarina, (Bombycidae, Lepidoptera). Chromosoma 47:167–178. doi: 10.1007/BF00331804 PubMedCrossRefGoogle Scholar
  89. Musacchio A (2015) The molecular biology of spindle assembly checkpoint signaling dynamics. Curr Biol 25:R1002–R1018. doi: 10.1016/j.cub.2015.08.051 PubMedCrossRefGoogle Scholar
  90. Nagpal H, Fukagawa T (2016) Kinetochore assembly and function through the cell cycle. Chromosoma 125:645–659. doi: 10.1007/s00412-016-0608-3 PubMedCrossRefGoogle Scholar
  91. Nagpal H, Hori T, Furukawa A, Sugase K, Osakabe A, Kurumizaka H, Fukagawa T (2015) Dynamic changes in CCAN organization through CENP-C during cell-cycle progression. Mol Biol Cell 26:3768–3776. doi: 10.1091/mbc.E15-07-0531 PubMedPubMedCentralCrossRefGoogle Scholar
  92. Nishihashi A, Haraguchi T, Hiraoka Y, Ikemura T, Regnier V, Dodson H, Earnshaw WC, Fukagawa T (2002) CENP-I is essential for centromere function in vertebrate cells. Dev Cell 2:463–476PubMedCrossRefGoogle Scholar
  93. Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M (2009) An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods 6:917–922. doi: 10.1038/nmeth.1401 PubMedCrossRefGoogle Scholar
  94. Nishino T, Rago F, Hori T, Tomii K, Cheeseman IM, Fukagawa T (2013) CENP-T provides a structural platform for outer kinetochore assembly. EMBO J 32:424–436. doi: 10.1038/emboj.2012.348 PubMedPubMedCentralCrossRefGoogle Scholar
  95. Nishino T, Takeuchi K, Gascoigne KE, Suzuki A, Hori T, Oyama T, Morikawa K, Cheeseman IM, Fukagawa T (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 PubMedPubMedCentralCrossRefGoogle Scholar
  96. Novo CL, Tang C, Ahmed K, Djuric U, Fussner E, Mullin NP, Morgan NP, Hayre J, Sienerth AR, Elderkin S, Nishinakamura R, Chambers I, Ellis J, Bazett-Jones DP, Rugg-Gunn PJ (2016) The pluripotency factor Nanog regulates pericentromeric heterochromatin organization in mouse embryonic stem cells. Genes Dev 30:1101–1115. doi: 10.1101/gad.275685.115 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Obuse C, Yang H, Nozaki N, Goto S, Okazaki T, Yoda K (2004) Proteomics analysis of the centromere complex from HeLa interphase cells: UV-damaged DNA binding protein 1 (DDB-1) is a component of the CEN-complex, while BMI-1 is transiently co-localized with the centromeric region in interphase. Genes Cells 9:105–120PubMedCrossRefGoogle Scholar
  98. Oegema K, Desai A, Rybina S, Kirkham M, Hyman AA (2001) Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol 153:1209–1226PubMedPubMedCentralCrossRefGoogle Scholar
  99. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Okada M, Cheeseman IM, Hori T, Okawa K, McLeod IX, Yates JR, Desai A, Fukagawa T (2006) The CENP-H–I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat Cell Biol 8:446–457. doi: 10.1038/ncb1396 PubMedCrossRefGoogle Scholar
  101. Palmer DK, O’Day K, Wener MH, Andrews BS, Margolis RL (1987) A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones. J Cell Biol 104:805–815PubMedCrossRefGoogle Scholar
  102. Perpelescu M, Fukagawa T (2011) The ABCs of CENPs. Chromosoma 120:425–446. doi: 10.1007/s00412-011-0330-0 PubMedCrossRefGoogle Scholar
  103. Pesenti ME, Weir JR, Musacchio A (2016) Progress in the structural and functional characterization of kinetochores. Curr Opin Struct Biol 37:152–163. doi: 10.1016/ PubMedCrossRefGoogle Scholar
  104. Peters AHFM, O’Carroll D, Scherthan H, Mechtler K, Sauer S, Schöfer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337. doi: 10.1016/S0092-8674(01)00542-6 PubMedCrossRefGoogle Scholar
  105. Petrovic A, Keller J, Liu Y, Overlack K, John J, Dimitrova YN, Jenni S, van Gerwen S, Stege P, Wohlgemuth S, Rombaut P, Herzog F, Harrison SC, Vetter IR, Musacchio A (2016) Structure of the MIS12 complex and molecular basis of its interaction with CENP-C at human kinetochores. Cell 167(1028–1040):e15. doi: 10.1016/j.cell.2016.10.005 Google Scholar
  106. Piras FM, Nergadze SG, Magnani E, Bertoni L, Attolini C, Khoriauli L, Raimondi E, Giulotto E (2010) Uncoupling of satellite DNA and centromeric function in the genus Equus. PLoS Genet 6:e1000845. doi: 10.1371/journal.pgen.1000845 PubMedPubMedCentralCrossRefGoogle Scholar
  107. Pluta AF, Mackay AM, Ainsztein AM, Goldberg IG, Earnshaw WC (1995) The centromere: hub of chromosomal activities. Science 270:1591–1594PubMedCrossRefGoogle Scholar
  108. Prendergast L, Müller S, Liu Y, Huang H, Dingli F, Loew D, Vassias I, Patel DJ, Sullivan KF, Almouzni G (2016) The CENP-T/-W complex is a binding partner of the histone chaperone FACT. Genes Dev 30:1313–1326. doi: 10.1101/gad.275073.115 PubMedPubMedCentralCrossRefGoogle Scholar
  109. Prendergast L, van Vuuren C, Kaczmarczyk A, Doering V, Hellwig D, Quinn N, Hoischen C, Diekmann S, Sullivan KF (2011) Premitotic assembly of human CENPs -T and -W switches centromeric chromatin to a mitotic state. PLoS Biol 9:e1001082. doi: 10.1371/journal.pbio.1001082 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Przewloka MR, Glover DM (2009) The kinetochore and the centromere: a working long distance relationship. Annu Rev Genet 43:439–465. doi: 10.1146/annurev-genet-102108-134310 PubMedCrossRefGoogle Scholar
  111. Przewloka MR, Venkei Z, Bolanos-Garcia VM, Debski J, Dadlez M, Glover DM (2011) CENP-C is a structural platform for kinetochore assembly. Curr Biol 21:399–405. doi: 10.1016/j.cub.2011.02.005 PubMedCrossRefGoogle Scholar
  112. Purgato S, Belloni E, Piras FM, Zoli M, Badiale C, Cerutti F, Mazzagatti A, Perini G, Valle Della G, Nergadze SG, Sullivan KF, Raimondi E, Rocchi M, Giulotto E (2015) Centromere sliding on a mammalian chromosome. Chromosoma 124:277–287. doi: 10.1007/s00412-014-0493-6 PubMedCrossRefGoogle Scholar
  113. Rago F, Gascoigne KE, Cheeseman IM (2015) Distinct organization and regulation of the outer kinetochore KMN network downstream of CENP-C and CENP-T. Curr Biol 25:671–677. doi: 10.1016/j.cub.2015.01.059 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Regnier V, Vagnarelli P, Fukagawa T, Zerjal T, Burns E, Trouche D, Earnshaw W, Brown W (2005) CENP-A is required for accurate chromosome segregation and sustained kinetochore association of BubR1. Mol Cell Biol 25:3967–3981. doi: 10.1128/MCB.25.10.3967-3981.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  115. Saitoh H, Tomkiel J, Cooke CA, Ratrie H, Maurer M, Rothfield NF, Earnshaw WC (1992) CENP-C, an autoantigen in scleroderma, is a component of the human inner kinetochore plate. Cell 70:115–125PubMedCrossRefGoogle Scholar
  116. Saitoh S, Takahashi K, Yanagida M (1997) Mis6, a fission yeast inner centromere protein, acts during G1/S and forms specialized chromatin required for equal segregation. Cell 90:131–143. doi: 10.1016/S0092-8674(00)80320-7 PubMedCrossRefGoogle Scholar
  117. Satzinger H (2008) Theodor and Marcella Boveri: chromosomes and cytoplasm in heredity and development. Nat Rev Genet 9(3):231–238PubMedCrossRefGoogle Scholar
  118. Schleiffer A, Maier M, Litos G, Lampert F, Hornung P, Mechtler K, Westermann S (2012) CENP-T proteins are conserved centromere receptors of the Ndc80 complex. Nat Cell Biol 14:604–613. doi: 10.1038/ncb2493 PubMedCrossRefGoogle Scholar
  119. Screpanti E, De Antoni A, Alushin GM, Petrovic A, Melis T, Nogales E, Musacchio A (2011) Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr Biol 21:391–398. doi: 10.1016/j.cub.2010.12.039 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Shang W-H, Hori T, Martins NMC, Toyoda A, Misu S, Monma N, Hiratani I, Maeshima K, Ikeo K, Fujiyama A, Kimura H, Earnshaw WC, Fukagawa T (2013) Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell 24:635–648. doi: 10.1016/j.devcel.2013.02.009 PubMedPubMedCentralCrossRefGoogle Scholar
  121. Shang W-H, Hori T, Toyoda A, Kato J, Popendorf K, Sakakibara Y, Fujiyama A, Fukagawa T (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 PubMedPubMedCentralCrossRefGoogle Scholar
  122. Shang W-H, Hori T, Westhorpe FG, Godek KM, Toyoda A, Misu S, Monma N, Ikeo K, Carroll CW, Takami Y, Fujiyama A, Kimura H, Straight AF, Fukagawa T (2016) Acetylation of histone H4 lysine 5 and 12 is required for CENP-A deposition into centromeres. Nat Commun 7:13465. doi: 10.1038/ncomms13465 PubMedPubMedCentralCrossRefGoogle Scholar
  123. Singh TR, Saro D, Ali AM, Zheng X-F, Du C-H, Killen MW, Sachpatzidis A, Wahengbam K, Pierce AJ, Xiong Y, Sung P, Meetei AR (2010) MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol Cell 37:879–886. doi: 10.1016/j.molcel.2010.01.036 PubMedPubMedCentralCrossRefGoogle Scholar
  124. 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 9:573–586PubMedCrossRefGoogle Scholar
  125. Stukenberg PT, Burke DJ (2015) Connecting the microtubule attachment status of each kinetochore to cell cycle arrest through the spindle assembly checkpoint. Chromosoma 124:463–480. doi: 10.1007/s00412-015-0515-z PubMedCrossRefGoogle Scholar
  126. Sugata N, Li S, Earnshaw WC, Yen TJ, Yoda K, Masumoto H, Munekata E, Warburton PE, Todokoro K (2000) Human CENP-H multimers colocalize with CENP-A and CENP-C at active centromere–kinetochore complexes. Hum Mol Genet 9:2919–2926PubMedCrossRefGoogle Scholar
  127. Sugata N, Munekata E, Todokoro K (1999) Characterization of a novel kinetochore protein, CENP-H. J Biol Chem 274:27343–27346PubMedCrossRefGoogle Scholar
  128. Sullivan BA, Karpen GH (2004) Centromeric chromatin exhibits a histone modification pattern that is distinct from both euchromatin and heterochromatin. Nat Struct Mol Biol 11:1076–1083. doi: 10.1038/nsmb845 PubMedPubMedCentralCrossRefGoogle Scholar
  129. Sutton WS (1902) On the morphology of the chromosome group in Brachystola magna. Biol Bull 4:24–39CrossRefGoogle Scholar
  130. Sutton WS (1903) The chromosomes in heredity. Biol Bull 4:231–250CrossRefGoogle Scholar
  131. Suzuki A, Badger BL, Wan X, DeLuca JG, Salmon ED (2014) The architecture of CCAN proteins creates a structural integrity to resist spindle forces and achieve proper intrakinetochore stretch. Dev Cell 30:717–730. doi: 10.1016/j.devcel.2014.08.003 PubMedPubMedCentralCrossRefGoogle Scholar
  132. Suzuki A, Hori T, Nishino T, Usukura J, Miyagi A, Morikawa K, Fukagawa T (2011) Spindle microtubules generate tension-dependent changes in the distribution of inner kinetochore proteins. J Cell Biol 193:125–140. doi: 10.1083/jcb.201012050 PubMedPubMedCentralCrossRefGoogle Scholar
  133. Takahashi K, Chen ES, Yanagida M (2000) Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science 288:2215–2219PubMedCrossRefGoogle Scholar
  134. Takeuchi K, Fukagawa T (2012) Molecular architecture of vertebrate kinetochores. Exp Cell Res 318:1367–1374. doi: 10.1016/j.yexcr.2012.02.016 PubMedCrossRefGoogle Scholar
  135. Takeuchi K, Nishino T, Mayanagi K, Horikoshi N, Osakabe A, Tachiwana H, Hori T, Kurumizaka H, Fukagawa T (2014) The centromeric nucleosome-like CENP-T-W-S-X complex induces positive supercoils into DNA. Nucleic Acids Res 42:1644–1655. doi: 10.1093/nar/gkt1124 PubMedCrossRefGoogle Scholar
  136. Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S (2002) Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053–1066. doi: 10.1105/tpc.010425 PubMedPubMedCentralCrossRefGoogle Scholar
  137. Tipton AR, Wang K, Oladimeji P, Sufi S, Gu Z, Liu S-T (2012) Identification of novel mitosis regulators through data mining with human centromere/kinetochore proteins as group queries. BMC Cell Biol 13(1):15. doi: 10.1186/1471-2121-13-15 PubMedPubMedCentralCrossRefGoogle Scholar
  138. Tomkiel J, Cooke CA, Saitoh H, Bernat RL, Earnshaw WC (1994) CENP-C is required for maintaining proper kinetochore size and for a timely transition to anaphase. J Cell Biol 125:531–545PubMedCrossRefGoogle Scholar
  139. Tschermak E (1900) Über künstliche Kreuzung bei Pisum sativum. Berichte der Deutsche Botanischen Gessellschaft 28:232–239Google Scholar
  140. Uchida KSK, Takagaki K, Kumada K, Hirayama Y, Noda T, Hirota T (2009) Kinetochore stretching inactivates the spindle assembly checkpoint. J Cell Biol 184:383–390. doi: 10.1083/jcb.200811028 PubMedPubMedCentralCrossRefGoogle Scholar
  141. Van Hooser AA, Ouspenski II, Gregson HC, Starr DA, Yen TJ, Goldberg ML, Yokomori K, Earnshaw WC, Sullivan KF, Brinkley BR (2001) Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J Cell Sci 114:3529–3542. doi: 10.1007/BF00332792 PubMedGoogle Scholar
  142. Varma D, Salmon ED (2012) The KMN protein network—chief conductors of the kinetochore orchestra. J Cell Sci 125:5927–5936. doi: 10.1242/jcs.093724 PubMedPubMedCentralCrossRefGoogle Scholar
  143. 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 52:1153–1163PubMedPubMedCentralGoogle Scholar
  144. Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR, Blöcker H, Distl O, Edgar RC, Garber M, Leeb T, Mauceli E, MacLeod JN, Penedo MCT, Raison JM, Sharpe T, Vogel J, Andersson L, Antczak DF, Biagi T, Binns MM, Chowdhary BP, Coleman SJ, Valle Della G, Fryc S, Guérin G, Hasegawa T, Hill EW, Jurka J, Kiialainen A, Lindgren G, Liu J, Magnani E, Mickelson JR, Murray J, Nergadze SG, Onofrio R, Pedroni S, Piras MF, Raudsepp T, Rocchi M, Røed KH, Ryder OA, Searle S, Skow L, Swinburne JE, Syvänen AC, Tozaki T, Valberg SJ, Vaudin M, White JR, Zody MC, Broad institute genome sequencing platform, broad institute whole genome assembly team, Lander ES, Lindblad-Toh K (2009) Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 326:865–867. doi: 10.1126/science.1178158 PubMedPubMedCentralCrossRefGoogle Scholar
  145. Wan X, O’Quinn RP, Pierce HL, Joglekar AP, Gall WE, DeLuca JG, Carroll CW, Liu S-T, Yen TJ, McEwen BF, Stukenberg PT, Desai A, Salmon ED (2009) Protein architecture of the human kinetochore microtubule attachment site. Cell 137:672–684. doi: 10.1016/j.cell.2009.03.035 PubMedPubMedCentralCrossRefGoogle Scholar
  146. Warburton PE, Cooke CA, Bourassa S, Vafa O, Sullivan BA, Stetten G, Gimelli G, Warburton D, Tyler-Smith C, Sullivan KF, Poirier GG, Earnshaw WC (1997) Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr Biol 7:901–904PubMedCrossRefGoogle Scholar
  147. Weir JR, Faesen AC, Klare K, Petrovic A, Basilico F, Fischböck J, Pentakota S, Keller J, Pesenti ME, Pan D, Vogt D, Wohlgemuth S, Herzog F, Musacchio A (2016) Insights from biochemical reconstitution into the architecture of human kinetochores. Nature 537:249–253. doi: 10.1038/nature19333 PubMedCrossRefGoogle Scholar
  148. Yamagishi Y, Sakuno T, Shimura M, Watanabe Y (2008) Heterochromatin links to centromeric protection by recruiting shugoshin. Nature 455:251–255. doi: 10.1038/nature07217 PubMedCrossRefGoogle Scholar
  149. Yan Z, Delannoy M, Ling C, Daee D, Osman F, Muniandy PA, Shen X, Oostra AB, Du H, Steltenpool J, Lin T, Schuster B, Décaillet C, Stasiak A, Stasiak AZ, Stone S, Hoatlin ME, Schindler D, Woodcock CL, Joenje H, Sen R, de Winter JP, Li L, Seidman MM, Whitby MC, Myung K, Constantinou A, Wang W (2010) A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol Cell 37:865–878. doi: 10.1016/j.molcel.2010.01.039 PubMedPubMedCentralCrossRefGoogle Scholar
  150. Yoda K, Ando S, Morishita S, Houmura K, Hashimoto K, Takeyasu K, Okazaki T (2000) Human centromere protein A (CENP-A) can replace histone H3 in nucleosome reconstitution in vitro. PNAS 97:7266–7271. doi: 10.1073/pnas.130189697 PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Graduate School of Frontier BiosciencesOsaka UniversitySuitaJapan

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