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No longer a nuisance: long non-coding RNAs join CENP-A in epigenetic centromere regulation

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Abstract

Centromeres represent the basis for kinetochore formation, and are essential for proper chromosome segregation during mitosis. Despite these essential roles, centromeres are not defined by specific DNA sequences, but by epigenetic means. The histone variant CENP-A controls centromere identity epigenetically and is essential for recruiting kinetochore components that attach the chromosomes to the mitotic spindle during mitosis. Recently, a new player in centromere regulation has emerged: long non-coding RNAs transcribed from repetitive regions of centromeric DNA function in regulating centromeres epigenetically. This review summarizes recent findings on the essential roles that transcription, pericentromeric transcripts, and centromere-derived RNAs play in centromere biology.

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References

  1. Akiyoshi B, Gull K (2013) Evolutionary cell biology of chromosome segregation: insights from trypanosomes. Open Biol 3:130023

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Alfenito MR, Birchler JA (1993) Molecular characterization of a maize B chromosome centric sequence. Genetics 135:589–597

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Allshire RC, Karpen GH (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9:923–937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bade D, Pauleau AL, 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 28:508–519

    Article  CAS  PubMed  Google Scholar 

  6. 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 110:11827–11832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Barry AE, Howman EV, Cancilla MR, Saffery R, Choo KH (1999) Sequence analysis of an 80 kb human neocentromere. Hum Mol Genet 8:217–227

    Article  CAS  PubMed  Google Scholar 

  8. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–1093

    Article  CAS  PubMed  Google Scholar 

  9. Bergmann J, Rodríguez M, Martins N, Kimura H, Kelly D, Masumoto H, Larionov V, Jansen L, Earnshaw W (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 30:328–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 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 125:411–421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bernard P, Schmidt CK, Vaur S, Dheur S, Drogat J, Genier S, Ekwall K, Uhlmann F, Javerzat JP (2008) Cell-cycle regulation of cohesin stability along fission yeast chromosomes. EMBO J 27:111–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Biscotti MA, Olmo E, Heslop-Harrison JS (2015) Repetitive DNA in eukaryotic genomes. Chromosome Res 23:415–420

    Article  CAS  PubMed  Google Scholar 

  13. Black BE, Cleveland DW (2011) Epigenetic centromere propagation and the nature of CENP-a nucleosomes. Cell 144:471–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 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 103:8709–8714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Carmena M, Wheelock M, Funabiki H, Earnshaw WC (2012) The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat Rev Mol Cell Biol 13:789–803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Carone DM, Zhang C, Hall LE, Obergfell C, Carone BR, O’Neill MJ, O’Neill RJ (2013) Hypermorphic expression of centromeric retroelement-encoded small RNAs impairs CENP-A loading. Chromosome Res 21:49–62

    Article  CAS  PubMed  Google Scholar 

  18. Carroll CW, Straight AF (2006) Centromere formation: from epigenetics to self-assembly. Trends Cell Biol 16:70–78

    Article  CAS  PubMed  Google Scholar 

  19. Castillo AG, Mellone BG, Partridge JF, Richardson W, Hamilton GL, Allshire RC, Pidoux AL (2007) Plasticity of fission yeast CENP-A chromatin driven by relative levels of histone H3 and H4. PLoS Genet 3:e121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  21. 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 109:1979–1984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. 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 34:73–84

    Article  PubMed  CAS  Google Scholar 

  24. Chen ES, Saitoh S, Yanagida M, Takahashi K (2003) A cell cycle-regulated GATA factor promotes centromeric localization of CENP-A in fission yeast. Mol Cell 11:175–187

    Article  CAS  PubMed  Google Scholar 

  25. Chen ES, Zhang K, Nicolas E, Cam HP, Zofall M, Grewal SI (2008) Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451:734–737

    Article  CAS  PubMed  Google Scholar 

  26. Choi ES, Stralfors 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 286:23600–23607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Choi ES, Stralfors 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:e1002985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chueh AC, Northrop EL, Brettingham-Moore KH, Choo KH, Wong LH (2009) LINE retrotransposon RNA is an essential structural and functional epigenetic component of a core neocentromeric chromatin. PLoS Genet 5:e1000354

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Colmenares SU, Buker SM, Buhler M, Dlakic M, Moazed D (2007) Coupling of double-stranded RNA synthesis and siRNA generation in fission yeast RNAi. Mol Cell 27:449–461

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 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 19:2301–2306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Doudna JA, Rath VL (2002) Structure and function of the eukaryotic ribosome: the next frontier. Cell 109:153–156

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google 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

    Article  CAS  PubMed  Google Scholar 

  35. Earnshaw WC, Allshire RC, Black BE, Bloom K, Brinkley BR, Brown W, Cheeseman IM, Choo KH, Copenhaver GP, DeLuca JG, Desai A, Diekmann S, Erhardt S, Fitzgerald-Hayes M, Foltz D, Fukagawa T, Gassmann R, Gerlich DW, Glover DM, Gorbsky GJ, Harrison SC, Heun P, Hirota T, Jansen LE, Karpen G, Kops GJ, Lampson MA, Lens SM, Losada A, Luger K, Maiato H, Maddox PS, Margolis RL, Masumoto H, McAinsh AD, Mellone BG, Meraldi P, Musacchio A, Oegema K, O’Neill RJ, Salmon ED, Scott KC, Straight AF, Stukenberg PT, Sullivan BA, Sullivan KF, Sunkel CE, Swedlow JR, Walczak CE, Warburton PE, Westermann S, Willard HF, Wordeman L, Yanagida M, Yen TJ, Yoda K, Cleveland DW (2013) Esperanto for histones: CENP-A, not CenH3, is the centromeric histone H3 variant. Chromosome Res 21:101–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Eymery A, Callanan M, Vourc’h C (2009) The secret message of heterochromatin: new insights into the mechanisms and function of centromeric and pericentric repeat sequence transcription. Int J Dev Biol 53:259–268

    Article  CAS  PubMed  Google Scholar 

  37. Eymery A, Horard B, El Atifi-Borel M, Fourel G, Berger F, Vitte AL, Van den Broeck A, Brambilla E, Fournier A, Callanan M, Gazzeri S, Khochbin S, Rousseaux S, Gilson E, Vourc’h C (2009) A transcriptomic analysis of human centromeric and pericentric sequences in normal and tumor cells. Nucleic Acids Res 37:6340–6354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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 348:699–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 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 37:5071–5080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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 137:472–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  42. Fukagawa T, Earnshaw WC (2014) The centromere: chromatin foundation for the kinetochore machinery. Dev Cell 30:496–508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  44. Gottesfeld JM, Forbes DJ (1997) Mitotic repression of the transcriptional machinery. Trends Biochem Sci 22:197–202

    Article  CAS  PubMed  Google Scholar 

  45. 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 110:8579–8584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hall LE, Mitchell SE, O’Neill RJ (2012) Pericentric and centromeric transcription: a perfect balance required. Chromosome Res 20:535–546

    Article  CAS  PubMed  Google Scholar 

  47. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70

    Article  CAS  PubMed  Google Scholar 

  48. Hasson D, Panchenko T, Salimian KJ, Salman MU, Sekulic N, Alonso A, Warburton PE, Black BE (2013) The octamer is the major form of CENP-A nucleosomes at human centromeres. Nat Struct Mol Biol 20:687–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Henikoff S (2013) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1102

    Article  Google Scholar 

  50. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Holoch D, Moazed D (2015) RNA-mediated epigenetic regulation of gene expression. Nat Rev Genet 16:71–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. 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 29:740–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. 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

    Article  CAS  PubMed  Google Scholar 

  54. 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

    Article  CAS  PubMed  Google Scholar 

  55. 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

    Article  CAS  PubMed  Google Scholar 

  56. Jain C, Belasco JG (2001) Structural model for the cooperative assembly of HIV-1 Rev multimers on the RRE as deduced from analysis of assembly-defective mutants. Mol Cell 7:603–614

    Article  CAS  PubMed  Google Scholar 

  57. Jolly C (2004) Stress-induced transcription of satellite III repeats. J Cell Biol 164:25–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 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 19:489–501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  60. Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120

    Article  CAS  PubMed  Google Scholar 

  61. Lacoste N, Woolfe A, Tachiwana H, Garea AV, Barth T, Cantaloube S, Kurumizaka H, Imhof A, Almouzni G (2014) Mislocalization of the centromeric histone variant CenH3/CENP-A in human cells depends on the chaperone DAXX. Mol Cell 53:631–644

    Article  CAS  PubMed  Google Scholar 

  62. Lam AL (2006) Human centromeric chromatin is a dynamic chromosomal domain that can spread over noncentromeric DNA. Proc Natl Acad Sci 103:4186–4191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Maison C, Bailly D, Roche D, Oca RM, Probst AV, Vassias I, Dingli F, Lombard B, Loew D, Quivy J, Almouzni G (2011) SUMOylation promotes de novo targeting of HP1 alpha to pericentric heterochromatin. Nat Genet 43:220–227

    Article  CAS  PubMed  Google Scholar 

  64. Murchison EP (2005) Characterization of Dicer-deficient murine embryonic stem cells. Proc Natl Acad Sci 102:12135–12140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. 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 32:589–603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Ohzeki J, Larionov V, Earnshaw WC, Masumoto H (2015) Genetic and epigenetic regulation of centromeres: a look at HAC formation. Chromosome Res 23:87–103

    Article  CAS  PubMed  Google Scholar 

  68. Olszak AM, Essen D, Pereira AJ, Diehl S, Manke T, Maiato H, Saccani S, Heun P (2011) Heterochromatin boundaries are hotspots for de novo kinetochore formation. Nat Cell Biol 13:799–808

    Article  CAS  PubMed  Google Scholar 

  69. Perrod S, Gasser SM (2003) Long-range silencing and position effects at telomeres and centromeres: parallels and differences. Cell Mol Life Sci CMLS 60:2303–2318

    Article  CAS  PubMed  Google Scholar 

  70. Pezer Z, Ugarković D (2008) RNA Pol II promotes transcription of centromeric satellite DNA in beetles. PLoS One 3:e1594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Pidoux AL, Allshire RC (2005) The role of heterochromatin in centromere function. Philos Trans R Soc B Biol Sci 360:569–579

    Article  CAS  Google Scholar 

  72. Probst AV, Okamoto I, Casanova M, Marjou FE, Marjou F, Baccon PL, Baccon P, Almouzni G (2010) A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell 19:625–638

    Article  CAS  PubMed  Google Scholar 

  73. Qiu JJ, Guo JJ, Lv TJ, Jin HY, Ding JX, Feng WW, Zhang Y, Hua KQ (2013) Prognostic value of centromere protein-A expression in patients with epithelial ovarian cancer. Tumour Biol 34:2971–2975

    Article  CAS  PubMed  Google Scholar 

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

  75. 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 107:10484–10489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Saksouk N, Simboeck E, Dejardin J (2015) Constitutive heterochromatin formation and transcription in mammals. Epigenet Chromatin 8:3

    Article  CAS  Google Scholar 

  78. Sakuno T, Tada K, Watanabe Y (2009) Kinetochore geometry defined by cohesion within the centromere. Nature 458:852–858

    Article  CAS  PubMed  Google Scholar 

  79. Salvany L, Aldaz S, Corsetti E, Azpiazu N (2009) A new role for hth in the early pre-blastodermic divisions in Drosophila. Cell Cycle 8:2748–2755

    Article  CAS  PubMed  Google Scholar 

  80. 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 109:9029–9034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Schueler MG, Higgins A, Rudd M, Gustashaw K, Willard H (2001) Genomic and genetic definition of a functional human centromere. Science 294:109–115

    Article  CAS  PubMed  Google Scholar 

  82. Scott KC, Merrett SL, Willard HF (2006) A heterochromatin barrier partitions the fission yeast centromere into discrete chromatin domains. Curr Biol 16:119–129

    Article  CAS  PubMed  Google Scholar 

  83. Sciortino S, Gurtner A, Manni I, Fontemaggi G, Dey A, Sacchi A, Ozato K, Piaggio G (2001) The cyclin B1 gene is actively transcribed during mitosis in HeLa cells. EMBO Rep 2:1018–1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Shuaib M, Ouararhni K, Dimitrov S, Hamiche A (2010) HJURP binds CENP-A via a highly conserved N-terminal domain and mediates its deposition at centromeres. Proc Natl Acad Sci USA 107:1349–1354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Steiner N, Hahnenberger K, Clarke L (1993) Centromeres of the fission yeast Schizosaccharomyces pombe are highly variable genetic loci. Mol Cell Biol 13:4578–4587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Sugiyama T, Cam H, Verdel A, Moazed D, Grewal SI (2005) RNA-dependent RNA polymerase is an essential component of a self-enforcing loop coupling heterochromatin assembly to siRNA production. Proc Natl Acad Sci USA 102:152–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Sun X, Wahlstrom J, Karpen G (1997) Molecular structure of a functional Drosophila centromere. Cell 91:1007–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Talbert PB, Ahmad K, Almouzni G, Ausio J, Berger F, Bhalla PL, Bonner WM, Cande WZ, Chadwick BP, Chan SW, Cross GA, Cui L, Dimitrov SI, Doenecke D, Eirin-Lopez JM, Gorovsky MA, Hake SB, Hamkalo BA, Holec S, Jacobsen SE, Kamieniarz K, Khochbin S, Ladurner AG, Landsman D, Latham JA, Loppin B, Malik HS, Marzluff WF, Pehrson JR, Postberg J, Schneider R, Singh MB, Smith MM, Thompson E, Torres-Padilla ME, Tremethick DJ, Turner BM, Waterborg JH, Wollmann H, Yelagandula R, Zhu B, Henikoff S (2012) A unified phylogeny-based nomenclature for histone variants. Epigenet Chromatin 5:7

    Article  CAS  Google Scholar 

  90. Ting DT, Lipson D, Paul S, Brannigan BW, Akhavanfard S, Coffman EJ, Contino G, Deshpande V, Iafrate AJ, Letovsky S, Rivera MN, Bardeesy N, Maheswaran S, Haber DA (2011) Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 331:593–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Tomonaga T, Matsushita K, Yamaguchi S, Oohashi T, Shimada H, Ochiai T, Yoda K, Nomura F (2003) Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res 63:3511–3516

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Torras-Llort M, Moreno-Moreno O, Azorin F (2009) Focus on the centre: the role of chromatin on the regulation of centromere identity and function. EMBO J 28:2337–2348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Usakin L, Abad J, Vagin VV, Pablos B, Villasante A, Gvozdev AV (2007) Transcription of the 1.688 satellite DNA family is under the control of RNA interference machinery in Drosophila melanogaster ovaries. Genetics 176:1343–1349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Vakoc CR, Sachdeva MM, Wang H, Blobel GA (2006) Profile of histone lysine methylation across transcribed mammalian chromatin. Mol Cell Biol 26(24):9185–9195. doi:10.1128/MCB.01529-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Valgardsdottir R, Chiodi I, Giordano M, Rossi A, Bazzini S, Ghigna C, Riva S, Biamonti G (2007) Transcription of Satellite III non-coding RNAs is a general stress response in human cells. Nucleic Acids Res 36:423–434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Volpe TA, Kidner C, Hall I, Teng G, Grewal S, Martienssen R (2002) Regulation of heterochromatic silencing and histone H3 Lysine-9 methylation by RNAi. Science 297:1833–1837

    Article  CAS  PubMed  Google Scholar 

  98. Walfridsson J, Bjerling P, Thalen M, Yoo E, Park SD, Ekwall K (2005) The CHD remodeling factor Hrp1 stimulates CENP-A loading to centromeres. Nucleic Acids Res 33:2868–2879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Warburton PE (2004) Chromosomal dynamics of human neocentromere formation. Chromosome Res 12(6):617–626

    Article  CAS  PubMed  Google Scholar 

  100. Williams BC, Murphy TD, Goldberg ML, Karpen GH (1998) Neocentromere activity of structurally acentric mini-chromosomes in Drosophila. Nat Genet 18:30–37

    Article  CAS  PubMed  Google Scholar 

  101. 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 17:1146–1160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Wutz A (2003) RNAs templating chromatin structure for dosage compensation in animals. BioEssays News Rev Mol Cell Dev Biol 25:434–442

    Article  CAS  Google Scholar 

  103. Yamagishi Y, Sakuno T, Shimura M, Watanabe Y (2008) Heterochromatin links to centromeric protection by recruiting shugoshin. Nature 455:251–255

    Article  CAS  PubMed  Google Scholar 

  104. Yan H, Ito H, Nobuta K, Ouyang S, Jin W, Tian S, Lu C, Venu RC, Wang GL, Green PJ, Wing RA, Buell CR, Meyers BC, Jiang J (2006) Genomic and genetic characterization of rice Cen3 reveals extensive transcription and evolutionary implications of a complex centromere. Plant Cell 18:2123–2133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Zinkowski RP, Meyne J, Brinkley BR (1991) The centromere-kinetochore complex: a repeat subunit model. J Cell Biol 113:1091–1110

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We apologize to our colleagues whose work on centromeres and repetitive RNA could not be cited due to space limitations. We gratefully acknowledge members of the Erhardt lab for fruitful discussions and Aubry K. Miller for constructive comments on the manuscript and the Deutsche Forschungsgesellschaft (ER576 and EXC81) and the Boehringer Ingelheim Stiftung for funding our research on centromeres and RNA. SR is an alumna of the Hartmut Hoffmann-Berling International Graduate School of Molecular and Cellular Biology.

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Correspondence to Sylvia Erhardt.

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Rošić, S., Erhardt, S. No longer a nuisance: long non-coding RNAs join CENP-A in epigenetic centromere regulation. Cell. Mol. Life Sci. 73, 1387–1398 (2016). https://doi.org/10.1007/s00018-015-2124-7

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  • DOI: https://doi.org/10.1007/s00018-015-2124-7

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