Skip to main content
SpringerLink
Log in

Epigenetic regulation of centromere function

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

The centromere is a specialized region on the chromosome that directs equal chromosome segregation. Centromeres are usually not defined by DNA sequences alone. How centromere formation and function are determined by epigenetics is still not fully understood. Active centromeres are often marked by the presence of centromeric-specific histone H3 variant, centromere protein A (CENP-A). How CENP-A is assembled into the centromeric chromatin during the cell cycle and propagated to the next cell cycle or the next generation to maintain the centromere function has been intensively investigated. In this review, we summarize current understanding of how post-translational modifications of CENP-A and other centromere proteins, centromeric and pericentric histone modifications, non-coding transcription and transcripts contribute to centromere function, and discuss their intricate relationships and potential feedback mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Furuyama S, Biggins S (2007) Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc Natl Acad Sci 104(37):14706–14711

    CAS  PubMed  Google Scholar 

  2. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293(5532):1098–1102

    CAS  PubMed  Google Scholar 

  3. 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(11):1076–1083

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Bernard P, Maure JF, Partridge JF, Genier S, Javerzat JP, Allshire RC (2001) Requirement of heterochromatin for cohesion at centromeres. Science 294(5551):2539–2542

    CAS  PubMed  Google Scholar 

  5. Blower MD, Sullivan BA, Karpen GH (2002) Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2(3):319–330

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Ribeiro SA, Vagnarelli P, Dong Y, Hori T, McEwen BF, Fukagawa T, Flors C, Earnshaw WC (2010) A super-resolution map of the vertebrate kinetochore. Proc Natl Acad Sci USA 107(23):10484–10489

    CAS  PubMed  Google Scholar 

  7. Jin W, Lamb JC, Zhang W, Kolano B, Birchler JA, Jiang J (2008) Histone modifications associated with both A and B chromosomes of maize. Chromosome Res 16(8):1203–1214

    CAS  PubMed  Google Scholar 

  8. Aldrup-MacDonald ME, Sullivan BA (2014) The past, present, and future of human centromere genomics. Genes 5(1):33–50

    PubMed  PubMed Central  Google Scholar 

  9. 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(6):1153–1163

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Amor DJ, Choo KH (2002) Neocentromeres: role in human disease, evolution, and centromere study. Am J Hum Genet 71(4):695–714

    PubMed  PubMed Central  Google Scholar 

  11. 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(2):261–282

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Earnshaw WC, Rothfield N (1985) Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91(3–4):313–321

    CAS  PubMed  Google Scholar 

  13. Shang W-H, Hori T, Martins NM, Toyoda A, Misu S, Monma N, Hiratani I, Maeshima K, Ikeo K, Fujiyama A (2013) Chromosome engineering allows the efficient isolation of vertebrate neocentromeres. Dev Cell 24(6):635–648

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Fukagawa T, Earnshaw WC (2014) Neocentromeres. Curr Biol 24(19):R946–R947

    CAS  PubMed  Google Scholar 

  15. Cheeseman IM, Desai A (2008) Molecular architecture of the kinetochore–microtubule interface. Nat Rev Mol Cell Biol 9(1):33–46

    CAS  PubMed  Google Scholar 

  16. Shelby RD, Monier K, Sullivan KF (2000) Chromatin assembly at kinetochores is uncoupled from DNA replication. J Cell Biol 151(5):1113–1118

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Pearson CG, Yeh E, Gardner M, Odde D, Salmon ED, Bloom K (2004) Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase. Curr Biol 14(21):1962–1967

    CAS  PubMed  Google Scholar 

  18. Gassmann R, A Rechtsteiner, KW Yuen, A Muroyama, T Egelhofer, L Gaydos, F Barron, Maddox P, A. Essex, J. Monen, S. Ercan, JD Lieb, K Oegema, S Strome, Desai AP (2012) An inverse relationship to germline transcription defines centromeric chromatin in C. elegans. Nature, 484(7395), 534–7.

  19. Nechemia-Arbely Y, Fachinetti D, Cleveland DW (2012) Replicating centromeric chromatin: spatial and temporal control of CENP-A assembly. Exp Cell Res 318(12):1353–1360

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Hayashi T, Fujita Y, Iwasaki O, Adachi Y, Takahashi K, Yanagida M (2004) Mis16 and Mis18 are required for CENP-A loading and histone deacetylation at centromeres. Cell 118(6):715–729

    CAS  PubMed  Google Scholar 

  21. 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(3):485–497

    CAS  PubMed  Google Scholar 

  22. Foltz DR, Jansen LE, Bailey AO, Yates JR 3rd, Bassett EA, Wood S, Black BE, Cleveland DW (2009) Centromere-specific assembly of CENP-a nucleosomes is mediated by HJURP. Cell 137(3):472–484

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Camahort R, Li B, Florens L, Swanson SK, Washburn MP, Gerton JL (2007) Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol Cell 26(6):853–865

    CAS  PubMed  Google Scholar 

  24. Williams JS, Hayashi T, Yanagida M, Russell P (2009) Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol Cell 33(3):287–298

    CAS  PubMed  PubMed Central  Google 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(3):313–329

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Furuyama T, Dalal Y, Henikoff S (2006) Chaperone-mediated assembly of centromeric chromatin in vitro. Proc Natl Acad Sci 103(16):6172–6177

    CAS  PubMed  Google Scholar 

  27. Lee BCH, Lin Z, Yuen KWY (2016) RbAp46/48 LIN-53 is required for holocentromere assembly in caenorhabditis elegans. Cell Rep 14(8):1819–1828

    CAS  PubMed  Google Scholar 

  28. Stankovic A, Guo LY, Mata JF, Bodor DL, Cao X-J, Bailey AO, Shabanowitz J, Hunt DF, Garcia BA, Black BE (2017) A dual inhibitory mechanism sufficient to maintain cell-cycle-restricted CENP-A assembly. Mol Cell 65(2):231–246

    CAS  PubMed  Google Scholar 

  29. An S, P Koldewey, J Chik, L Subramanian, U-S Cho, Mis16 switches function from a histone H4 chaperone to a CENP-ACnp1-specific assembly factor through Eic1 interaction. Structure, 2018. 26(7): 960e4–971e4.

  30. Bade D, Pauleau A-L, Wendler A, Erhardt S (2014) The E3 ligase CUL3/RDX controls centromere maintenance by ubiquitylating and stabilizing CENP-A in a CAL1-dependent manner. Dev Cell 28(5):508–519

    CAS  PubMed  Google Scholar 

  31. Maddox PS, Hyndman F, Monen J, Oegema K, Desai A (2007) Functional genomics identifies a Myb domain–containing protein family required for assembly of CENP-A chromatin. J Cell Biol 176(6):757–763

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Lagana A, Dorn JF, De Rop V, Ladouceur AM, Maddox AS, Maddox PS (2010) A small GTPase molecular switch regulates epigenetic centromere maintenance by stabilizing newly incorporated CENP-A. Nat Cell Biol 12(12):1186–1193

    CAS  PubMed  Google Scholar 

  33. Falk SJ, Guo LY, Sekulic N, Smoak EM, Mani T, Logsdon GA, Gupta K, Jansen LE, Van Duyne GD, Vinogradov SA, Lampson MA, Black BE (2015) Chromosomes CENP-C reshapes and stabilizes CENP-A nucleosomes at the centromere. Science 348(6235):699–703

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Jansen LE, Black BE, Foltz DR, Cleveland DW (2007) Propagation of centromeric chromatin requires exit from mitosis. J Cell biol 176(6):795–805

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Takada M, Zhang W, Suzuki A, Kuroda TS, Yu Z, Inuzuka H, Gao D, Wan L, Zhuang M, Hu L (2017) FBW7 loss promotes chromosomal instability and tumorigenesis via cyclin E1/CDK2–mediated phosphorylation of CENP-A. Can Res 77(18):4881–4893

    CAS  Google Scholar 

  36. Yu Z, Zhou X, Wang W, Deng W, Fang J, Hu H, Wang Z, Li S, Cui L, Shen J, Zhai L, Peng S, Wong J, Dong S, Yuan Z, Ou G, Zhang X, Xu P, Lou J, Yang N, Chen P, Xu RM, Li G (2015) Dynamic phosphorylation of CENP-A at Ser68 orchestrates its cell-cycle-dependent deposition at centromeres. Dev Cell 32(1):68–81

    PubMed  Google Scholar 

  37. Wang K, Yu Z, Liu Y, Li G (2017) Ser68 phosphorylation ensures accurate cell-cycle-dependent CENP-A deposition at centromeres. Dev Cell 40:5–6

    CAS  PubMed  Google Scholar 

  38. Zhao H, Winogradoff D, Bui M, Dalal Y, Papoian GA (2016) Promiscuous histone mis-assembly is actively prevented by chaperones. J Am Chem Soc 138(40):13207–13218

    CAS  PubMed  Google Scholar 

  39. Fachinetti D, Logsdon GA, Abdullah A, Selzer EB, Cleveland DW, Black BE (2017) CENP-A modifications on Ser68 and Lys124 are dispensable for establishment, maintenance, and long-term function of human centromeres. Dev Cell 40(1):104–113

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Schuh M, Lehner CF, Heidmann S (2007) Incorporation of drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17(3):237–243

    CAS  PubMed  Google Scholar 

  41. Bernad R, Sánchez P, Rivera T, Rodríguez-Corsino M, Boyarchuk E, Vassias I, Ray-Gallet D, Arnaoutov A, Dasso M, Almouzni G, Losada A (2011) Xenopus HJURP and condensin II are required for CENP-A assembly. J Cell Biol 192(4):569–582

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Ohkuni K, Takahashi Y, Fulp A, Lawrimore J, Au W-C, Pasupala N, Levy-Myers R, Warren J, Strunnikov A, Baker RE (2016) SUMO-targeted ubiquitin ligase (STUbL) Slx5 regulates proteolysis of centromeric histone H3 variant Cse4 and prevents its mislocalization to euchromatin. Mol Biol Cell 27(9):1500–1510

    CAS  PubMed Central  Google Scholar 

  43. Ranjitkar P, Press MO, Yi X, Baker R, MacCoss MJ, Biggins S (2010) An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol Cell 40(3):455–464

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Hewawasam G, Shivaraju M, Mattingly M, Venkatesh S, Martin-Brown S, Florens L, Workman JL, Gerton JL (2010) Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol Cell 40(3):444–454

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Moreno-Moreno O, Medina-Giró S, Torras-Llort M, Azorín F (2011) The F box protein partner of paired regulates stability of drosophila centromeric histone H3, CenH3 CID. Curr Biol 21(17):1488–1493

    CAS  PubMed  Google Scholar 

  46. Nechemia-Arbely Y, Miga KH, Shoshani O, Aslanian A, McMahon MA, Lee AY, Fachinetti D, Yates JR, Ren B, Cleveland DW (2019) DNA replication acts as an error correction mechanism to maintain centromere identity by restricting CENP-A to centromeres. Nat Cell Biol 21(6):743

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Niikura Y, Kitagawa R, Ogi H, Abdulle R, Pagala V, Kitagawa K (2015) CENP-A K124 ubiquitylation is required for CENP-A deposition at the centromere. Dev Cell 32(5):589–603

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Niikura Y, Kitagawa R, Kitagawa K (2017) CENP-A ubiquitylation is required for CENP-A deposition at the centromere. Dev Cell 40(1):7–8

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Bui M, Dimitriadis EK, Hoischen C, An E, Quenet D, Giebe S, Nita-Lazar A, Diekmann S, Dalal Y (2012) Cell-cycle-dependent structural transitions in the human CENP-A nucleosome in vivo. Cell 150(2):317–326

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Bui M, Pitman M, Nuccio A, Roque S, Donlin-Asp PG, Nita-Lazar A, Papoian GA, Dalal Y (2017) Internal modifications in the CENP-A nucleosome modulate centromeric dynamics. Epigenetics Chromatin 10:17

    PubMed  PubMed Central  Google Scholar 

  51. Bailey AO, Panchenko T, Sathyan KM, Petkowski JJ, Pai PJ, Bai DL, Russell DH, Macara IG, Shabanowitz J, Hunt DF, Black BE, Foltz DR (2013) Posttranslational modification of CENP-A influences the conformation of centromeric chromatin. Proc Natl Acad Sci USA 110(29):11827–11832

    CAS  PubMed  Google Scholar 

  52. Fachinetti D, Folco HD, Nechemia-Arbely Y, Valente LP, Nguyen K, Wong AJ, Zhu Q, Holland AJ, Desai A, Jansen LE (2013) A two-step mechanism for epigenetic specification of centromere identity and function. Nat Cell Biol 15(9):1056

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Logsdon GA, Barrey EJ, Bassett EA, DeNizio JE, Guo LY, Panchenko T, Dawicki-McKenna JM, Heun P, Black BE (2015) Both tails and the centromere targeting domain of CENP-A are required for centromere establishment. J Cell Biol, jcb. 201412011.

  54. Goutte-Gattat D, Shuaib M, Ouararhni K, Gautier T, Skoufias DA, Hamiche A, Dimitrov S (2013) Phosphorylation of the CENP-A amino-terminus in mitotic centromeric chromatin is required for kinetochore function. Proc Natl Acad Sci USA 110(21):8579–8584

    CAS  PubMed  Google Scholar 

  55. Li D, Liu R, Song L, Zhou H, Chen J, Huang X (2008) The special location of p-H3 and p-CENP-A on heterochromatin during mitosis in MCF-7. Mol Biol Rep 35(4):657–662

    CAS  PubMed  Google Scholar 

  56. Kunitoku N, Sasayama T, Marumoto T, Zhang D, Honda S, Kobayashi O, Hatakeyama K, Ushio Y, Saya H, Hirota T (2003) CENP-A phosphorylation by Aurora-A in prophase is required for enrichment of Aurora-B at inner centromeres and for kinetochore function. Dev Cell 5(6):853–864

    CAS  PubMed  Google Scholar 

  57. Eot-Houllier G, Magnaghi-Jaulin L, Fulcrand G, Moyroud F-X, Monier S, Jaulin C (2018) Aurora A-dependent CENP-A phosphorylation at inner centromeres protects bioriented chromosomes against cohesion fatigue. Nature communications 9(1):1888

    PubMed  PubMed Central  Google Scholar 

  58. Zeitlin SG, Shelby RD, Sullivan KF (2001) CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. J Cell Biol 155(7):1147–1157

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Barra V, Logsdon GA, Scelfo A, Hoffmann S, Hervé S, Aslanian A, Nechemia-Arbely Y, Cleveland DW, Black BE, Fachinetti D (2019) Phosphorylation of CENP-A on serine 7 does not control centromere function. Nature communications 10(1):175

    PubMed  PubMed Central  Google Scholar 

  60. Zhang X, Li X, Marshall JB, Zhong CX, Dawe RK (2005) Phosphoserines on maize CENTROMERIC HISTONE H3 and histone H3 demarcate the centromere and pericentromere during chromosome segregation. Plant Cell 17(2):572–583

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Samel A, Cuomo A, Bonaldi T, Ehrenhofer-Murray AE (2012) Methylation of CenH3 arginine 37 regulates kinetochore integrity and chromosome segregation. Proc Natl Acad Sci USA 109(23):9029–9034

    CAS  PubMed  Google Scholar 

  62. Wang J, Liu X, Dou Z, Chen L, Jiang H, Fu C, Fu G, Liu D, Zhang J, Zhu T, Fang J, Zang J, Cheng J, Teng M, Ding X, Yao X (2014) Mitotic regulator Mis18beta interacts with and specifies the centromeric assembly of molecular chaperone holliday junction recognition protein (HJURP). The Journal of biological chemistry 289(12):8326–8336

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Muller S, Montes de Oca R, Lacoste N, Dingli F, Loew D, Almouzni G (2014) Phosphorylation and DNA binding of HJURP determine its centromeric recruitment and function in CenH3(CENP-A) loading. Cell Rep 8(1):190–203

    CAS  PubMed  Google Scholar 

  64. Silva MC, Bodor DL, Stellfox ME, Martins NM, Hochegger H, Foltz DR, Jansen LE (2012) Cdk activity couples epigenetic centromere inheritance to cell cycle progression. Dev Cell 22(1):52–63

    CAS  PubMed  Google Scholar 

  65. Pan D, Klare K, Petrovic A, Take A, Walstein K, Singh P, Rondelet A, Bird AW, Musacchio A (2017) CDK-regulated dimerization of M18BP1 on a Mis18 hexamer is necessary for CENP-A loading. Elife 6:e23352

    PubMed  PubMed Central  Google Scholar 

  66. Spiller F, Medina-Pritchard B, Abad MA, Wear MA, Molina O, Earnshaw WC, Jeyaprakash AA (2017) Molecular basis for Cdk1-regulated timing of Mis18 complex assembly and CENP-A deposition. EMBO Rep 18(6):894–905

    CAS  PubMed  PubMed Central  Google Scholar 

  67. McKinley KL, Cheeseman IM (2014) Polo-like kinase 1 licenses CENP-A deposition at centromeres. Cell 158(2):397–411

    CAS  PubMed  PubMed Central  Google Scholar 

  68. French BT, Westhorpe FG, Limouse C, Straight AF (2017) Xenopus laevis M18BP1 directly binds existing CENP-A nucleosomes to promote centromeric chromatin assembly. Dev Cell 42(2):190–199.e10

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Shahbazian MD, Grunstein M (2007) Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76:75–100

    CAS  PubMed  Google Scholar 

  70. Jasencakova Z, Meister A, Schubert I (2001) Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley. Chromosoma 110(2):83–92

    CAS  PubMed  Google Scholar 

  71. Choy JS, Acuna R, Au WC, Basrai MA (2011) A role for histone H4K16 hypoacetylation in Saccharomyces cerevisiae kinetochore function. Genetics 189(1):11–21

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Shang W-H, Hori T, Westhorpe FG, Godek KM, Toyoda A, Misu S, Monma N, Ikeo K, Carroll CW, Takami Y (2016) Acetylation of histone H4 lysine 5 and 12 is required for CENP-A deposition into centromeres. Nature communications. 7

  73. Yan H, Jin W, Nagaki K, Tian S, Ouyang S, Buell CR, Talbert PB, Henikoff S, Jiang J (2005) Transcription and histone modifications in the recombination-free region spanning a rice centromere. Plant Cell 17(12):3227–3238

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Fujita Y, Hayashi T, Kiyomitsu T, Toyoda Y, Kokubu A, Obuse C, Yanagida M (2007) Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev Cell 12(1):17–30

    CAS  PubMed  Google Scholar 

  75. Wako T, Fukuda M, Furushima-Shimogawara R, Belyaev ND, Fukui K (2002) Cell cycle-dependent and lysine residue-specific dynamic changes of histone H4 acetylation in barley. Plant Mol Biol 49(6):645–653

    CAS  PubMed  Google Scholar 

  76. Müller S, Almouzni G (2017) Chromatin dynamics during the cell cycle at centromeres. Nat Rev Genet 18(3):192–208

    PubMed  Google Scholar 

  77. Fukagawa T, William CE (2014) The centromere: chromatin foundation for the kinetochore machinery. Dev Cell. 30(5):496–508

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Mravinac B, Sullivan LL, Reeves JW, Yan CM, Kopf KS, Farr CJ, Schueler MG, Sullivan BA (2009) Histone modifications within the human X centromere region. PLoS ONE 4(8):e6602

    PubMed  PubMed Central  Google Scholar 

  79. May BP, Lippman ZB, Fang Y, Spector DL, Martienssen RA (2005) Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet 1(6):e79

    PubMed  PubMed Central  Google Scholar 

  80. Cam HP, Sugiyama T, Chen ES, Chen X, FitzGerald PC, Grewal SI (2005) Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet 37(8):809–819

    CAS  PubMed  Google Scholar 

  81. Folco HD, Pidoux AL, Urano T, Allshire RC (2008) Heterochromatin and RNAi are required to establish CENP-A chromatin at centromeres. Science 319(5859):94–97

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Shi J, Dawe RK (2006) Partitioning of the maize epigenome by the number of methyl groups on histone H3 lysines 9 and 27. Genetics 173(3):1571–1583

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Bergmann JH, Rodriguez MG, Martins NM, Kimura H, Kelly DA, Masumoto H, Larionov V, Jansen LE, Earnshaw WC (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 30(2):328–340

    CAS  PubMed  Google Scholar 

  84. Chu L, Zhu T, Liu X, Yu R, Bacanamwo M, Dou Z, Chu Y, Zou H, Gibbons GH, Wang D, Ding X, Yao X (2012) SUV39H1 orchestrates temporal dynamics of centromeric methylation essential for faithful chromosome segregation in mitosis. J Mol Cell Biol 4(5):331–340

    CAS  PubMed  PubMed Central  Google Scholar 

  85. McManus KJ, Biron VL, Heit R, Underhill DA, Hendzel MJ (2006) Dynamic changes in histone H3 lysine 9 methylations identification of a mitosis-specific function for dynamic methylation in chromosome congression and segregation. J Biol Chem 281(13):8888–8897

    CAS  PubMed  Google Scholar 

  86. Alonso A, Hasson D, Cheung F, Warburton PE (2010) A paucity of heterochromatin at functional human neocentromeres. Epigenetics Chromatin 3(1):6

    PubMed  PubMed Central  Google Scholar 

  87. Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36(2):138–145

    CAS  PubMed  Google Scholar 

  88. Hori T, Shang WH, 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(6):740–749

    CAS  PubMed  PubMed Central  Google Scholar 

  89. 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(3):918–931

    CAS  PubMed  Google Scholar 

  90. Wang F, Dai J, Daum JR, Niedzialkowska E, Banerjee B, Stukenberg PT, Gorbsky GJ, Higgins JM (2010) Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330(6001):231–235

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Kawashima SA, Yamagishi Y, Honda T, Ishiguro K, Watanabe Y (2010) Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327(5962):172–177

    CAS  PubMed  Google Scholar 

  92. Yamagishi Y, Honda T, Tanno Y, Watanabe Y (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330(6001):239–243

    CAS  PubMed  Google Scholar 

  93. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, Funabiki H (2010) Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330(6001):235–239

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Liu H, Qu Q, Warrington R, Rice A, Cheng N, Yu H (2015) Mitotic transcription installs Sgo1 at centromeres to coordinate chromosome segregation. Mol Cell 59(3):426–436

    CAS  PubMed  Google Scholar 

  95. Dong Q, Han F (2012) Phosphorylation of histone H2A is associated with centromere function and maintenance in meiosis. Plant J 71(5):800–809

    CAS  PubMed  Google Scholar 

  96. Demidov D, Schubert V, Kumke K, Weiss O, Karimi-Ashtiyani R, Buttlar J, Heckmann S, Wanner G, Dong Q, Han F, Houben A (2014) Anti-phosphorylated histone H2AThr120: a universal microscopic marker for centromeric chromatin of mono- and holocentric plant species. Cytogenet Genome Res 143(1–3):150–156

    CAS  PubMed  Google Scholar 

  97. Wanner G, Schroeder-Reiter E, Ma W, Houben A, Schubert V (2015) The ultrastructure of mono- and holocentric plant centromeres: an immunological investigation by structured illumination microscopy and scanning electron microscopy. Chromosoma.

  98. Karp G, Pruitt NL (1996) Cell and molecular biology: concepts and experiments. Wiley, New York

    Google Scholar 

  99. Ohkuni K, Kitagawa K (2011) Endogenous transcription at the centromere facilitates centromere activity in budding yeast. Curr Biol 21(20):1695–1703

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Ling YH, Yuen KWY (2019) Point centromere activity requires an optimal level of centromeric noncoding RNA. Proc Natl Acad Sci 116(13):6270–6279

    CAS  PubMed  Google Scholar 

  101. Volpe T, Schramke V, Hamilton GL, White SA, Teng G, Martienssen RA, Allshire RC (2003) RNA interference is required for normal centromere function in fission yeast. Chromosome Res 11(2):137–146

    CAS  PubMed  Google Scholar 

  102. Djupedal I, Kos-Braun IC, Mosher RA, Söderholm N, Simmer F, Hardcastle TJ, Fender A, Heidrich N, Kagansky A, Bayne E (2009) Analysis of small RNA in fission yeast; centromeric siRNAs are potentially generated through a structured RNA. EMBO J 28(24):3832–3844

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Bouzinba-Segard H, Guais A, Francastel C (2006) Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc Natl Acad Sci USA 103(23):8709–8714

    CAS  PubMed  Google Scholar 

  104. Ideue T, Cho Y, Nishimura K, Tani T (2014) Involvement of satellite I noncoding RNA in regulation of chromosome segregation. Genes Cells 19(6):528–538

    CAS  PubMed  Google Scholar 

  105. Pezer Z, Ugarkovic D (2008) RNA Pol II promotes transcription of centromeric satellite DNA in beetles. PLoS ONE 3(2):e1594

    PubMed  PubMed Central  Google Scholar 

  106. Rošić S, Köhler F, Erhardt S (2014) Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division. J Cell Biol 207(3):335–349

    PubMed  PubMed Central  Google Scholar 

  107. Topp CN, Zhong CX, Dawe RK (2004) Centromere-encoded RNAs are integral components of the maize kinetochore. Proc Natl Acad Sci USA 101(45):15986–15991

    CAS  PubMed  Google Scholar 

  108. Quénet D, Dalal Y (2014) A long non-coding RNA is required for targeting centromeric protein A to the human centromere. Elife 3:e03254

    PubMed  Google Scholar 

  109. Gent JI, Dawe RK (2012) RNA as a structural and regulatory component of the centromere. Annu Rev Genet 46:443–453

    CAS  PubMed  Google Scholar 

  110. Chan FL, Wong LH (2012) Transcription in the maintenance of centromere chromatin identity. Nucleic Acids Res 40(22):11178–11188

    CAS  PubMed  PubMed Central  Google Scholar 

  111. McNulty SM, Sullivan LL, Sullivan BA (2017) Human centromeres produce chromosome-specific and array-specific alpha satellite transcripts that are complexed with CENP-A and CENP-C. Dev Cell 42(3):226–240.e6

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Wong LH, Brettingham-Moore KH, Chan L, Quach JM, Anderson MA, Northrop EL, Hannan R, Saffery R, Shaw ML, Williams E, Choo KH (2007) Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere. Genome Res 17(8):1146–1160

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Du Y, Topp CN, Dawe RK (2010) DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA. PLoS Genet 6(2):e1000835

    PubMed  PubMed Central  Google Scholar 

  114. Ferri F, Bouzinba-Segard H, Velasco G, Hube F, Francastel C (2009) Non-coding murine centromeric transcripts associate with and potentiate Aurora B kinase. Nucleic Acids Res 37(15):5071–5080

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Blower MD (2016) Centromeric transcription regulates Aurora-B localization and activation. Cell Rep 15(8):1624–1633

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Grenfell AW, Heald R, Strzelecka M (2016) Mitotic noncoding RNA processing promotes kinetochore and spindle assembly in Xenopus. J Cell Biol.

  117. Kato H, Goto DB, Martienssen RA, Urano T, Furukawa K, Murakami Y (2005) RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science 309(5733):467–469

    CAS  PubMed  Google Scholar 

  118. Djupedal I, Portoso M, Spahr H, Bonilla C, Gustafsson CM, Allshire RC, Ekwall K (2005) RNA Pol II subunit Rpb7 promotes centromeric transcription and RNAi-directed chromatin silencing. Genes Dev 19(19):2301–2306

    CAS  PubMed  PubMed Central  Google Scholar 

  119. Chan FL, Marshall OJ, Saffery R, Kim BW, Earle E, Choo KH, Wong LH (2012) Active transcription and essential role of RNA polymerase II at the centromere during mitosis. Proc Natl Acad Sci USA 109(6):1979–1984

    CAS  PubMed  Google Scholar 

  120. Ling YH, Yuen KWY (2020) Point centromere activity requires an optimal level of centromeric non-coding RNA. Proc Natl Acad Sci (In press).

  121. Foltz DR, Jansen LE, Black BE, Bailey AO, Yates JR 3rd, Cleveland DW (2006) The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8(5):458–469

    CAS  PubMed  Google Scholar 

  122. 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(11):1313–1326

    CAS  PubMed  PubMed Central  Google Scholar 

  123. Okada M, Okawa K, Isobe T, Fukagawa T (2009) CENP-H-containing complex facilitates centromere deposition of CENP-A in cooperation with FACT and CHD1. Mol Biol Cell 20(18):3986–3995

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Chen CC, Bowers S, Lipinszki Z, Palladino J, Trusiak S, Bettini E, Rosin L, Przewloka MR, Glover DM, O'Neill RJ, Mellone BG (2015) Establishment of centromeric chromatin by the CENP-A assembly factor CAL1 requires FACT-mediated transcription. Dev Cell 34(1):73–84

    PubMed  PubMed Central  Google Scholar 

  125. Choi ES, Strålfors A, Catania S, Castillo AG, Svensson JP, Pidoux AL, Ekwall K, Allshire RC (2012) Factors that promote H3 chromatin integrity during transcription prevent promiscuous deposition of CENP-A Cnp1 in fission yeast. PLoS Genet 8(9):e1002985

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Deyter GM, Biggins S (2014) The FACT complex interacts with the E3 ubiquitin ligase Psh1 to prevent ectopic localization of CENP-A. Genes Dev 28(16):1815–1826

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Catania S, Pidoux AL, Allshire RC (2015) Sequence features and transcriptional stalling within centromere DNA promote establishment of CENP-A chromatin. PLoS Genet 11(3):e1004986

    PubMed  PubMed Central  Google Scholar 

  128. Fukagawa T, Nogami M, Yoshikawa M, Ikeno M, Okazaki T, Takami Y, Nakayama T, Oshimura M (2004) Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 6(8):784–791

    CAS  PubMed  Google Scholar 

  129. Frescas D, Guardavaccaro D, Kuchay SM, Kato H, Poleshko A, Basrur V, Elenitoba-Johnson KS, Katz RA, Pagano M (2008) KDM2A represses transcription of centromeric satellite repeats and maintains the heterochromatic state. Cell Cycle 7(22):3539–3547

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Gopalakrishnan S, Sullivan BA, Trazzi S, Della Valle G, Robertson KD (2009) DNMT3B interacts with constitutive centromere protein CENP-C to modulate DNA methylation and the histone code at centromeric regions. Hum Mol Genet 18(17):3178–3193

    CAS  PubMed  PubMed Central  Google Scholar 

  131. Zhu Q, Pao GM, Huynh AM, Suh H, Tonnu N, Nederlof PM, Gage FH, Verma IM (2011) BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 477(7363):179–184

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Schwartz BE, Ahmad K (2005) Transcriptional activation triggers deposition and removal of the histone variant H33. Genes Dev 19(7):804–814

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Ahmad K, Henikoff S (2002) Epigenetic consequences of nucleosome dynamics. Cell 111(3):281–284

    CAS  PubMed  Google Scholar 

  134. Dunleavy EM, Almouzni G, Karpen GH (2011) H3.3 is deposited at centromeres in S phase as a placeholder for newly assembled CENP-A in G(1) phase. Nucleus 2(2):146–157

  135. Athwal RK, Walkiewicz MP, Baek S, Fu S, Bui M, Camps J, Ried T, Sung MH, Dalal Y (2015) CENP-A nucleosomes localize to transcription factor hotspots and subtelomeric sites in human cancer cells. Epigenet Chromatin 8:2

    CAS  Google Scholar 

  136. Huang C, Cheng J, Bawa-Khalfe T, Yao X, Chin YE, Yeh ET (2016) SUMOylated ORC2 recruits a histone demethylase to regulate centromeric histone modification and genomic stability. Cell Rep 15(1):147–157

    CAS  PubMed  Google Scholar 

  137. Nakano M, Cardinale S, Noskov VN, Gassmann R, Vagnarelli P, Kandels-Lewis S, Larionov V, Earnshaw WC, Masumoto H (2008) Inactivation of a human kinetochore by specific targeting of chromatin modifiers. Dev Cell 14(4):507–522

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Molina O, Vargiu G, Abad MA, Zhiteneva A, Jeyaprakash AA, Masumoto H, Kouprina N, Larionov V, Earnshaw WC (2016) Epigenetic engineering reveals a balance between histone modifications and transcription in kinetochore maintenance. Nat Commun 7.

  139. Allshire RC (2004) RNA interference, heterochromatin, and centromere function. Cold Spring Harb Symp Quant Biol 69:389–395

    CAS  PubMed  Google Scholar 

  140. Allshire RC, Javerzat J-P, Redhead NJ, Cranston G (1994) Position effect variegation at fission yeast centromeres. Cell 76(1):157–169

    CAS  PubMed  Google Scholar 

  141. Thakur J, Sanyal K (2013) Efficient neocentromere formation is suppressed by gene conversion to maintain centromere function at native physical chromosomal loci in Candida albicans. Genome Res 23(4):638–652

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Bergmann JH, Jakubsche JN, Martins NM, Kagansky A, Nakano M, Kimura H, Kelly DA, Turner BM, Masumoto H, Larionov V, Earnshaw WC (2012) Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function. J Cell Sci 125(Pt 2):411–421

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Hill A, Bloom K (1987) Genetic manipulation of centromere function. Mol Cell Biol 7(7):2397–2405

    CAS  PubMed  PubMed Central  Google Scholar 

  144. Cardinale S, Bergmann JH, Kelly D, Nakano M, Valdivia MM, Kimura H, Masumoto H, Larionov V, Earnshaw WC (2009) Hierarchical inactivation of a synthetic human kinetochore by a chromatin modifier. Mol Biol Cell 20(19):4194–4204

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Collins KA, Castillo AR, Tatsutani SY, Biggins S (2005) De novo kinetochore assembly requires the centromeric histone H3 variant. Mol Biol Cell 16(12):5649–5660

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Vourc’h C, Biamonti G (2011) Transcription of satellite DNAs in mammals, in long non-coding RNAs, Springer, Berlin, pp 95–118.

  147. Choi IR, Ostrovsky M, Zhang G, White KA (2001) Regulatory activity of distal and core RNA elements in Tombusvirus subgenomic mRNA2 transcription. J Biol Chem 276(45):41761–41768

    CAS  PubMed  Google Scholar 

  148. Ling YH, Yuen KWY (2019) Centromeric non-coding RNA as a hidden epigenetic factor of the point centromere. Curr Genet 1–7.

  149. Lachner M, O'Sullivan RJ, Jenuwein T (2003) An epigenetic road map for histone lysine methylation. J Cell Sci 116(Pt 11):2117–2124

    CAS  PubMed  Google Scholar 

  150. Hall IM, Shankaranarayana GD, Noma K, Ayoub N, Cohen A, Grewal SI (2002) Establishment and maintenance of a heterochromatin domain. Science 297(5590):2232–2237

    CAS  PubMed  Google Scholar 

  151. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410(6824):120–124

    CAS  PubMed  Google Scholar 

  152. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI (2001) Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292(5514):110–113

    CAS  PubMed  Google Scholar 

  153. Kagansky A, Folco HD, Almeida R, Pidoux AL, Boukaba A, Simmer F, Urano T, Hamilton GL, Allshire RC (2009) Synthetic heterochromatin bypasses RNAi and centromeric repeats to establish functional centromeres. Science 324(5935):1716–1719

    CAS  PubMed  PubMed Central  Google Scholar 

  154. Maison C, Bailly D, Peters AH, Quivy JP, Roche D, Taddei A, Lachner M, Jenuwein T, Almouzni G (2002) Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat Genet 30(3):329–334

    PubMed  Google Scholar 

  155. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ (2005) Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci USA 102(34):12135–12140

    CAS  PubMed  Google Scholar 

  156. Kanellopoulou C, Muljo SA, Kung AL, Ganesan S, Drapkin R, Jenuwein T, Livingston DM, Rajewsky K (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19(4):489–501

    CAS  PubMed  PubMed Central  Google Scholar 

  157. Brower-Toland B, Findley SD, Jiang L, Liu L, Yin H, Dus M, Zhou P, Elgin SC, Lin H (2007) Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev 21(18):2300–2311

    CAS  PubMed  PubMed Central  Google Scholar 

  158. Gu T, Elgin SC (2013) Maternal depletion of Piwi, a component of the RNAi system, impacts heterochromatin formation in Drosophila. PLoS Genet 9(9):e1003780

    CAS  PubMed  PubMed Central  Google Scholar 

  159. Yuen KW, Nabeshima K, Oegema K, Desai A (2011) Rapid de novo centromere formation occurs independently of heterochromatin protein 1 in C elegans embryos. Curr Biol. 21(21):1800–1807

    CAS  PubMed  PubMed Central  Google Scholar 

  160. Claycomb JM, Batista PJ, Pang KM, Gu W, Vasale JJ, van Wolfswinkel JC, Chaves DA, Shirayama M, Mitani S, Ketting RF, Conte D, Mello CC (2009) The Argonaute CSR-1 and its 22G-RNA cofactors are required for holocentric chromosome segregation. Cell 139(1):123–134

    CAS  PubMed  PubMed Central  Google Scholar 

  161. Gerson-Gurwitz A, Wang S, Sathe S, Green R, Yeo GW, Oegema K, Desai A (2016) A small RNA-catalytic Argonaute pathway tunes germline transcript levels to ensure embryonic divisions. Cell 165(2):396–409

    CAS  PubMed  PubMed Central  Google Scholar 

  162. Wedeles CJ, Wu MZ, Claycomb JM (2013) Protection of germline gene expression by the C Elegans Argonaute CSR-1. Dev Cell 27(6):664–671

    CAS  PubMed  Google Scholar 

  163. Black BE, Foltz DR, Chakravarthy S, Luger K, Woods VL, Cleveland DW (2004) Structural determinants for generating centromeric chromatin. Nature 430(6999):578–582

    CAS  PubMed  Google Scholar 

  164. Keith KC, Baker RE, Chen Y, Harris K, Stoler S, Fitzgerald-Hayes M (1999) Analysis of primary structural determinants that distinguish the centromere-specific function of histone variant Cse4p from histone H3. Mol Cell Biol 19(9):6130–6139

    CAS  PubMed  PubMed Central  Google Scholar 

  165. Bernatavichute YV, Zhang X, Cokus S, Pellegrini M, Jacobsen SE (2008) Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3(9):e3156

    PubMed  PubMed Central  Google Scholar 

  166. Jih G, Iglesias N, Currie MA, Bhanu NV, Paulo JA, Gygi SP, Garcia BA, Moazed D (2017) Unique roles for histone H3K9me states in RNAi and heritable silencing of transcription. Nature 547(7664):463–467

    CAS  PubMed  PubMed Central  Google Scholar 

  167. Choi ES, Strålfors A, Castillo AG, Durand-Dubief M, Ekwall K, Allshire RC (2011) Identification of noncoding transcripts from within CENP-A chromatin at fission yeast centromeres. J Biol Chem 286(26):23600–23607

    CAS  PubMed  PubMed Central  Google Scholar 

  168. Carone DM, Longo MS, Ferreri GC, Hall L, Harris M, Shook N, Bulazel KV, Carone BR, Obergfell C, O'Neill MJ, O'Neill RJ (2009) A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres. Chromosoma 118(1):113–125

    CAS  PubMed  Google Scholar 

  169. Bayne EH, White SA, Kagansky A, Bijos DA, Sanchez-Pulido L, Hoe K-L, Kim D-U, Park H-O, Ponting CP, Rappsilber J (2010) Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140(5):666–677

    CAS  PubMed  PubMed Central  Google Scholar 

  170. Scott KC, White CV, Willard HF (2007) An RNA polymerase III-dependent heterochromatin barrier at fission yeast centromere 1. PLoS ONE 2(10):e1099

    PubMed  PubMed Central  Google Scholar 

  171. Pal-Bhadra M, Leibovitch BA, Gandhi SG, Rao M, Bhadra U, Birchler JA, Elgin SC (2004) Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303(5658):669–672

    CAS  PubMed  Google Scholar 

  172. Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer 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(3):323–337

    CAS  PubMed  Google Scholar 

  173. Huang C, Wang X, Liu X, Cao S, Shan G (2015) RNAi pathway participates in chromosome segregation in mammalian cells. Cell Discovery 1:15029

    CAS  PubMed  PubMed Central  Google Scholar 

  174. Muchardt C, Guillemé M, Seeler JS, Trouche D, Dejean A, Yaniv M (2002) Coordinated methyl and RNA binding is required for heterochromatin localization of mammalian HP1α. EMBO Rep 3(10):975–981

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the General Research Grant [grant numbers 17126717, 17113418] and the Collaborative Research Fund [grant numbers C7058-18G]. We thank our lab members for critical reading and helpful suggestions on the manuscript.

Author information

Authors and Affiliations

  1. School of Biological Sciences, The University of Hong Kong, Kadoorie Biological Sciences Building, Pokfulam Road, Hong Kong, China

    Charmaine Yan Yu Wong, Bernard Chi Hang Lee & Karen Wing Yee Yuen

Authors
  1. Charmaine Yan Yu Wong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bernard Chi Hang Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karen Wing Yee Yuen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karen Wing Yee Yuen.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wong, C.Y.Y., Lee, B.C.H. & Yuen, K.W.Y. Epigenetic regulation of centromere function. Cell. Mol. Life Sci. 77, 2899–2917 (2020). https://doi.org/10.1007/s00018-020-03460-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-020-03460-8

Keywords

Search

Navigation