Sequence Features and Transcriptional Stalling within Centromere DNA Promote Establishment of CENP-A Chromatin

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The kinetochore directs the separation of chromosomes and is assembled at a special region of the chromosome—the centromere. DNA is wrapped around particles called nucleosomes, which contain histone proteins. The nucleosomes at centromeres are specialized, and contain the centromere-specific histone CENP-A. CENP-A nucleosomes form the platform upon which the kinetochore is built. Thus, CENP-A and centromere function go hand-in-hand. How the cell ensures that CENP-A is deposited at centromeres and not elsewhere is not well understood. We investigated the role that DNA sequence plays in defining centromere function in fission yeast. Our observations suggest that it is not the DNA sequence per se that is important for attracting CENP-A, but rather, the particular environment that the sequence creates. During transcription of centromeric DNA, RNA polymerase (RNAPII) appears to get stuck or stalled. Particular proteins—such as TFIIS and Ubp3—are known to help restart RNAPII so it can continue transcribing. We found that when cells lack Ubp3 or TFIIS, CENP-A becomes deposited on centromere sequences. We propose that persistent stalling of RNAPII on centromere DNA attracts factors that help deposit CENP-A. This study highlights the influence of DNA sequence in creating an attractive environment for CENP-A assembly.

Vyšlo v časopise: Sequence Features and Transcriptional Stalling within Centromere DNA Promote Establishment of CENP-A Chromatin. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1004986
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004986

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1. Westermann S, Schleiffer A (2013) Family matters: structural and functional conservation of centromere-associated proteins from yeast to humans. Trends in Cell Biology 23: 260–269. doi: 10.1016/j.tcb.2013.01.010 23481674

2. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293: 1098–1102. 11498581

3. Meraldi P, McAinsh AD, Rheinbay E, Sorger PK (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7: R23. 16563186

4. Buscaino A, Allshire R, Pidoux AL (2010) Building centromeres: home sweet home or a nomadic existence? Current Opinion in Genetics & Development: 1–9.

5. Melters DP, Bradnam KR, Young HA, Telis N, May MR, et al. (2013) Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol 14: R10. doi: 10.1186/gb-2013-14-1-r10 23363705

6. Biggins S (2013) The composition, functions, and regulation of the budding yeast kinetochore. Genetics 194: 817–846. doi: 10.1534/genetics.112.145276 23908374

7. Steiner FA, Henikoff S (2014) Holocentromeres are dispersed point centromeres localized at transcription factor hotspots. eLife Sciences 3: e02025. doi: 10.7554/eLife.02025 24714495

8. Maddox PS, Oegema K, Desai A, Cheeseman IM (2004) “Holo”er than thou: chromosome segregation and kinetochore function in C. elegans. Chromosome Res 12: 641–653. 15289669

9. Willard HF (1985) Chromosome-specific organization of human alpha satellite DNA. Am J Hum Genet 37: 524–532. 2988334

10. Willard HF (1989) The genomics of long tandem arrays of satellite DNA in the human genome. Genome 31: 737–744. 2698839

11. Marçais B, Laurent AM, Charlieu JP, Roizès G (1993) Organization of the variant domains of alpha satellite DNA on human chromosome 21. J Mol Evol 37: 171–178. 8411206

12. Pidoux AL, Allshire RC (2004) Kinetochore and heterochromatin domains of the fission yeast centromere. Chromosome Res 12: 521–534. 15289660

13. Sanyal K, Baum M, Carbon J (2004) Centromeric DNA sequences in the pathogenic yeast Candida albicans are all different and unique. Proc Natl Acad Sci USA 101: 11374–11379. 15272074

14. Shang WH, Hori T, Toyoda A, Kato J, Popendorf K, et al. (2010) Chickens possess centromeres with both extended tandem repeats and short non-tandem-repetitive sequences. Genome Research 20: 1219–1228. doi: 10.1101/gr.106245.110 20534883

15. Gong Z, Wu Y, Koblízková A, Torres GA, Wang K, et al. (2012) Repeatless and repeat-based centromeres in potato: implications for centromere evolution. Plant Cell 24: 3559–3574. doi: 10.1105/tpc.112.100511 22968715

16. Allshire RC, Karpen GH (2008) Epigenetic regulation of centromeric chromatin: old dogs, new tricks? Nat Rev Genet 9: 923–937. doi: 10.1038/nrg2466 19002142

17. Burrack LS, Berman J (2012) Neocentromeres and epigenetically inherited features of centromeres. Chromosome Res 20: 607–619. doi: 10.1007/s10577-012-9296-x 22723125

18. 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 18252209

19. Ishii K, Ogiyama Y, Chikashige Y, Soejima S, Masuda F, et al. (2008) Heterochromatin Integrity Affects Chromosome Reorganization After Centromere Dysfunction. Science 321: 1088–1091. doi: 10.1126/science.1158699 18719285

20. Stimpson KM, Matheny JE, Sullivan BA (2012) Dicentric chromosomes: unique models to study centromere function and inactivation. Chromosome Res 20: 595–605. doi: 10.1007/s10577-012-9302-3 22801777

21. Sato H, Masuda F, Takayama Y, Takahashi K, Saitoh S (2012) Epigenetic inactivation and subsequent heterochromatinization of a centromere stabilize dicentric chromosomes. Curr Biol 22: 658–667. doi: 10.1016/j.cub.2012.02.062 22464190

22. Catania S, Allshire RC (2014) Anarchic centromeres: deciphering order from apparent chaos. Current Opinion in Cell Biology 26: 41–50. doi: 10.1016/j.ceb.2013.09.004 24529245

23. Falk SJ, Black BE (2012) Centromeric chromatin and the pathway that drives its propagation. Biochim Biophys Acta 1819: 313–321. doi: 10.1016/j.bbagrm.2011.11.002 22154124

24. 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 22053052

25. Barnhart MC, Kuich PHJL, Stellfox ME, Ward JA, Bassett EA, et al. (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. The Journal of Cell Biology 194: 229–243. doi: 10.1083/jcb.201012017 21768289

26. Fachinetti D, Diego Folco H, Nechemia-Arbely Y, Valente LP, Nguyen K, et al. (2013) A two-step mechanism for epigenetic specification of centromere identity and function. Nature Cell Biology 15: 1056–1066. doi: 10.1038/ncb2805 23873148

27. Valente LP, Dehé P-M, Klutstein M, Aligianni S, Watt S, et al. (2013) Myb-domain protein Teb1 controls histone levels and centromere assembly in fission yeast. EMBO J.

28. Malik HS, Henikoff S (2009) Major evolutionary transitions in centromere complexity. Cell 138: 1067–1082. doi: 10.1016/j.cell.2009.08.036 19766562

29. Nakano M (2003) Epigenetic assembly of centromeric chromatin at ectopic-satellite sites on human chromosomes. Journal of Cell Science 116: 4021–4034. 12953060

30. 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 22825423

31. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959–3970. 1935914

32. Yuen KWY, 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: 1800–1807. doi: 10.1016/j.cub.2011.09.016 22018540

33. Scott KC (2013) Transcription and ncRNAs: at the cent(rome)re of kinetochore assembly and maintenance. Chromosome Res.

34. Rošić S, Köhler F, Erhardt S (2014) Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division. The Journal of Cell Biology 207: 335–349. doi: 10.1083/jcb.201404097 25365994

35. Ohkuni K, Kitagawa K (2011) Endogenous Transcription at the Centromere Facilitates Centromere Activity in Budding Yeast. Curr Biol.

36. 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. 15514020

37. Choi ES, Stralfors A, Castillo AG, Durand-Dubief M, Ekwall K, et al. (2011) Identification of noncoding transcripts from within CENP-A chromatin at fission yeast centromeres. J Biol Chem 286: 23600–23607. doi: 10.1074/jbc.M111.228510 21531710

38. Chan FL, Marshall OJ, Saffery R, Won Kim B, Earle E, et al. (2012) Active transcription and essential role of RNA polymerase II at the centromere during mitosis. Proceedings of the National Academy of Sciences 109: 1979–1984. doi: 10.1073/pnas.1108705109 22308327

39. Bergmann JH, Rodríguez MG, Martins NMC, Kimura H, Kelly DA, et al. (2011) Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J 30: 328–340. doi: 10.1038/emboj.2010.329 21157429

40. Bergmann JH, Jakubsche JN, Martins NM, Kagansky A, Nakano M, et al. (2012) Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function. Journal of Cell Science 125: 411–421. doi: 10.1242/jcs.090639 22331359

41. Choi ES, Strålfors A, Catania S, Castillo AG, Svensson JP, et al. (2012) Factors That Promote H3 Chromatin Integrity during Transcription Prevent Promiscuous Deposition of CENP-ACnp1 in Fission Yeast. PLoS Genet 8: e1002985. doi: 10.1371/journal.pgen.1002985 23028377

42. Sadeghi L, Siggens L, Svensson JP, Ekwall K (2014) Centromeric histone H2B monoubiquitination promotes noncoding transcription and chromatin integrity. Nat Struct Mol Biol: 236–243.

43. Chueh AC, Northrop EL, Brettingham-Moore KH, Choo KHA, Wong LH (2009) LINE retrotransposon RNA is an essential structural and functional epigenetic component of a core neocentromeric chromatin. PLoS Genet 5: e1000354. doi: 10.1371/journal.pgen.1000354 19180186

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

45. Folco HD, Pidoux AL, Urano T, Allshire RC (2008) Heterochromatin and RNAi Are Required to Establish CENP-A Chromatin at Centromeres. Science 319: 94–97. doi: 10.1126/science.1150944 18174443

46. Kagansky A, Folco HD, Almeida R, Pidoux AL, Boukaba A, et al. (2009) Synthetic Heterochromatin Bypasses RNAi and Centromeric Repeats to Establish Functional Centromeres. Science 324: 1716–1719. doi: 10.1126/science.1172026 19556509

47. Castillo AG, Pidoux AL, Catania S, Durand-Dubief M, Choi ES, et al. (2013) Telomeric Repeats Facilitate CENP-A(Cnp1) Incorporation via Telomere Binding Proteins. PLoS ONE 8: e69673. doi: 10.1371/journal.pone.0069673 23936074

48. Niwa O, Matsumoto T, Chikashige Y, Yanagida M (1989) Characterization of Schizosaccharomyces pombe minichromosome deletion derivatives and a functional allocation of their centromere. EMBO J 8: 3045–3052. 2583093

49. Lando D, Endesfelder U, Berger H, Subramanian L, Dunne PD, et al. (2012) Quantitative single-molecule microscopy reveals that CENP-A(Cnp1) deposition occurs during G2 in fission yeast. Open Biol 2: 120078. doi: 10.1098/rsob.120078 22870388

50. Baum M, Ngan VK, Clarke L (1994) The centromeric K-type repeat and the central core are together sufficient to establish a functional Schizosaccharomyces pombe centromere. Mol Biol Cell 5: 747–761. 7812044

51. Allshire RC, Nimmo ER, Ekwall K, Javerzat JP, Cranston G (1995) Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. Genes & Development 9: 218–233.

52. Struhl K, Segal E (2013) Determinants of nucleosome positioning. Nature Publishing Group 20: 267–273.

53. Kanizay L, Dawe RK (2009) Centromeres: long intergenic spaces with adaptive features. Funct Integr Genomics 9: 287–292. doi: 10.1007/s10142-009-0124-0 19434433

54. Segal E, Widom J (2009) What controls nucleosome positions? Trends in Genetics 25: 335–343. doi: 10.1016/j.tig.2009.06.002 19596482

55. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, et al. (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362–366. doi: 10.1038/nature07667 19092803

56. Wilson MD, Harreman M, Taschner M, Reid J, Walker J, et al. (2013) Proteasome-mediated processing of def1, a critical step in the cellular response to transcription stress. Cell 154: 983–995. doi: 10.1016/j.cell.2013.07.028 23993092

57. Selth LA, Sigurdsson S, Svejstrup JQ (2010) Transcript Elongation by RNA Polymerase II. Annu Rev Biochem 79: 271–293. doi: 10.1146/annurev.biochem.78.062807.091425 20367031

58. Kulish D, Struhl K (2001) TFIIS enhances transcriptional elongation through an artificial arrest site in vivo. Molecular and Cellular Biology 21: 4162–4168. 11390645

59. Cheung ACM, Cramer P (2011) Structural basis of RNA polymerase II backtracking, arrest and reactivation. Nature 471: 249–253. doi: 10.1038/nature09785 21346759

60. Sigurdsson S, Dirac-Svejstrup AB, Svejstrup JQ (2010) Evidence that Transcript Cleavage Is Essential for RNA Polymerase II Transcription and Cell Viability. Molecular Cell 38: 202–210. doi: 10.1016/j.molcel.2010.02.026 20417599

61. Kvint K, Uhler JP, Taschner MJ, Sigurdsson S, Erdjument-Bromage H, et al. (2008) Reversal of RNA polymerase II ubiquitylation by the ubiquitin protease Ubp3. Molecular Cell 30: 498–506. doi: 10.1016/j.molcel.2008.04.018 18498751

62. Linton MF, Raabe M, Pierotti V, Young SG (1997) Reading-frame restoration by transcriptional slippage at long stretches of adenine residues in mammalian cells. J Biol Chem 272: 14127–14132. 9162040

63. Kiyama R, Oishi M (1996) In Vitro Transcription of a Poly(dA){middle dot}Poly(dT)-Containing Sequence is Inhibited by Interaction between the Template and Its Transcripts. Nucleic Acids Research 24: 4577–4583. 8948652

64. Reyes-Turcu FE, Zhang K, Zofall M, Chen E, Grewal SIS (2011) Defects in RNA quality control factors reveal RNAi-independent nucleation of heterochromatin. Nature Structural & Molcular Biology 18: 1132–1138.

65. Black BE, Cleveland DW (2011) Epigenetic Centromere Propagation and the Nature of CENP-A Nucleosomes. Cell 144: 471–479. doi: 10.1016/j.cell.2011.02.002 21335232

66. Takahashi K, Murakami S, Chikashige Y, Funabiki H, Niwa O, et al. (1992) A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere. Mol Biol Cell 3: 819–835. 1515677

67. Polizzi C, Clarke L (1991) The chromatin structure of centromeres from fission yeast: differentiation of the central core that correlates with function. The Journal of Cell Biology 112: 191–201. 1988457

68. Wood V, Gwilliam R, Rajandream M- A, Lyne M, Lyne R, et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415: 871–880 11859360

69. Weber CM, Henikoff S (2014) Histone variants: dynamic punctuation in transcription. Genes & Development 28: 672–682.

70. Ray-Gallet D, Almouzni G (2010) Nucleosome dynamics and histone variants. Essays Biochem 48: 75–87. doi: 10.1042/bse0480075 20822487

71. Kiyama R, Oishi M (1994) Instability of plasmid DNA maintenance caused by transcription of poly(dT)-containing sequences in Escherichia coli. Gene 150: 57–61. 7959063

72. Segal E, Widom J (2009) Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol 19: 65–71. doi: 10.1016/j.sbi.2009.01.004 19208466

73. Raveh-Sadka T, Levo M, Shabi U, Shany B, Keren L, et al. (2012) Manipulating nucleosome disfavoring sequences allows fine-tune regulation of gene expression in yeast. Nat Genet 44: 743–750. doi: 10.1038/ng.2305 22634752

74. Buratowski S (2009) Progression through the RNA Polymerase II CTD Cycle. Molecular Cell 36: 541–546. doi: 10.1016/j.molcel.2009.10.019 19941815

75. Heidemann M, Hintermair C, Voß K, Eick D (2013) Dynamic phosphorylation patterns of RNA polymerase II CTD during transcription. Biochim Biophys Acta 1829: 55–62. doi: 10.1016/j.bbagrm.2012.08.013 22982363

76. Somesh BP, Reid J, Liu W-F, Søgaard TMM, Erdjument-Bromage H, et al. (2005) Multiple mechanisms confining RNA polymerase II ubiquitylation to polymerases undergoing transcriptional arrest. Cell 121: 913–923. 15960978

77. Martinez-Rucobo FW, Cramer P (2013) Structural basis of transcription elongation. Biochim Biophys Acta 1829: 9–19. doi: 10.1016/j.bbagrm.2012.09.002 22982352

78. Marguerat S, Schmidt A, Codlin S, Chen W, Aebersold R, et al. (2012) Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 151: 671–683. doi: 10.1016/j.cell.2012.09.019 23101633

79. Shandilya J, Senapati P, Hans F, Menoni H, Bouvet P, et al. (2014) Centromeric histone variant CENP-A represses acetylation-dependent chromatin transcription that is relieved by histone chaperone NPM1. J Biochem.

80. Funabiki H, Hagan I, Uzawa S, Yanagida M (1993) Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. The Journal of Cell Biology 121: 961–976. 8388878

81. 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 G₁ phase. Nucleus 2: 146–157. doi: 10.4161/nucl.2.2.15211 21738837

82. Nakano M, Cardinale S, Noskov VN, Gassmann R, Vagnarelli P, et al. (2008) Inactivation of a Human Kinetochore by Specific Targeting of Chromatin Modifiers. Developmental Cell 14: 507–522. doi: 10.1016/j.devcel.2008.02.001 18410728

83. Moreno S, Klar A, Nurse P (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Meth Enzymol 194: 795–823. 2005825

84. Castillo AG, Mellone BG, Partridge JF, Richardson W, Hamilton GL, et al. (2007) Plasticity of Fission Yeast CENP-A Chromatin Driven by Relative Levels of Histone H3 and H4. PLoS Genet 3: e121. 17677001

85. Guarente L (1983) Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Meth Enzymol 101: 181–191. 6310321

86. Pidoux AL, Choi ES, Abbott JKR, Liu X, Kagansky A, et al. (2009) Fission Yeast Scm3: A CENP-A Receptor Required for Integrity of Subkinetochore Chromatin. Molecular Cell 33: 299–311. doi: 10.1016/j.molcel.2009.01.019 19217404