Histone H3 Localizes to the Centromeric DNA in Budding Yeast

English version České info

During cell division, segregation of sister chromatids to daughter cells is achieved by the poleward pulling force of microtubules, which attach to the chromatids by means of a multiprotein complex, the kinetochore. Kinetochores assemble at the centromeric DNA organized by specialized centromeric nucleosomes. In contrast to other eukaryotes, which typically have large repetitive centromeric regions, budding yeast CEN DNA is defined by a 125 bp sequence and assembles a single centromeric nucleosome. In budding yeast, as well as in other eukaryotes, the Cse4 histone variant (known in vertebrates as CENP-A) is believed to substitute for histone H3 at the centromeric nucleosome. However, the exact composition of the CEN nucleosome remains a subject of debate. We report the use of a novel ChIP approach to reveal the composition of the centromeric nucleosome and its localization on CEN DNA in budding yeast. Surprisingly, we observed a strong interaction of H3, as well as Cse4, H4, H2A, and H2B, but not histone chaperone Scm3 (HJURP in human) with the centromeric DNA. H3 localizes to centromeric DNA at all stages of the cell cycle. Using a sequential ChIP approach, we could demonstrate the co-occupancy of H3 and Cse4 at the CEN DNA. Our results favor a H3-Cse4 heterotypic octamer at the budding yeast centromere. Whether or not our model is correct, any future model will have to account for the stable association of histone H3 with the centromeric DNA.

Vyšlo v časopise: Histone H3 Localizes to the Centromeric DNA in Budding Yeast. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002739
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002739

Souhrn

Zdroje

1. BlowerMDSullivanBAKarpenGH 2002 Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2 319 330

2. MeluhPBYangPGlowczewskiLKoshlandDSmithMM 1998 Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94 607 613

3. SullivanKFHechenbergerMMasriK 1994 Human CENP-A contains a histone H3 related histone fold domain that is required for targeting to the centromere. J Cell Biol 127 581 592

4. FoltzDRJansenLEBlackBEBaileyAOYatesJR3rd 2006 The human CENP-A centromeric nucleosome-associated complex. Nat Cell Biol 8 458 469

5. CollinsKACastilloARTatsutaniSYBigginsS 2005 De novo kinetochore assembly requires the centromeric histone H3 variant. Mol Biol Cell 16 5649 5660

6. BlackBEFoltzDRChakravarthySLugerKWoodsVLJr 2004 Structural determinants for generating centromeric chromatin. Nature 430 578 582

7. BlackBEJansenLEMaddoxPSFoltzDRDesaiAB 2007 Centromere identity maintained by nucleosomes assembled with histone H3 containing the CENP-A targeting domain. Mol Cell 25 309 322

8. FujitaYHayashiTKiyomitsuTToyodaYKokubuA 2007 Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. Dev Cell 12 17 30

9. Sanchez-PulidoLPidouxALPontingCPAllshireRC 2009 Common ancestry of the CENP-A chaperones Scm3 and HJURP. Cell 137 1173 1174

10. ChenYBakerREKeithKCHarrisKStolerS 2000 The N terminus of the centromere H3-like protein Cse4p performs an essential function distinct from that of the histone fold domain. Mol Cell Biol 20 7037 7048

11. MizuguchiGXiaoHWisniewskiJSmithMMWuC 2007 Nonhistone Scm3 and histones CenH3-H4 assemble the core of centromere-specific nucleosomes. Cell 129 1153 1164

12. CamahortRLiBFlorensLSwansonSKWashburnMP 2007 Scm3 is essential to recruit the histone h3 variant cse4 to centromeres and to maintain a functional kinetochore. Mol Cell 26 853 865

13. StolerSRogersKWeitzeSMoreyLFitzgerald-HayesM 2007 Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization. Proc Natl Acad Sci U S A 104 10571 10576

14. PidouxALChoiESAbbottJKLiuXKaganskyA 2009 Fission yeast Scm3: A CENP-A receptor required for integrity of subkinetochore chromatin. Mol Cell 33 299 311

15. WilliamsJSHayashiTYanagidaMRussellP 2009 Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. Mol Cell 33 287 298

16. ZhouZFengHZhouBRGhirlandoRHuK 2011 Structural basis for recognition of centromere histone variant CenH3 by the chaperone Scm3. Nature 472 234 237

17. XiaoHMizuguchiGWisniewskiJHuangYWeiD 2011 Nonhistone Scm3 Binds to AT-Rich DNA to Organize Atypical Centromeric Nucleosome of Budding Yeast. Molecular cell 43 369 380

18. ChoUSHarrisonSC 2011 Recognition of the centromere-specific histone Cse4 by the chaperone Scm3. Proceedings of the National Academy of Sciences of the United States of America 108 9367 9371

19. HeunPErhardtSBlowerMDWeissSSkoraAD 2006 Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell 10 303 315

20. KrassovskyKHenikoffJGHenikoffS 2012 Tripartite organization of centromeric chromatin in budding yeast. Proceedings of the National Academy of Sciences of the United States of America 109 243 248

21. CollinsKAFuruyamaSBigginsS 2004 Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr Biol 14 1968 1972

22. PearsonCGYehEGardnerMOddeDSalmonED 2004 Stable kinetochore-microtubule attachment constrains centromere positioning in metaphase. Curr Biol 14 1962 1967

23. DunleavyEMPidouxALMonetMBonillaCRichardsonW 2007 A NASP (N1/N2)-related protein, Sim3, binds CENP-A and is required for its deposition at fission yeast centromeres. Mol Cell 28 1029 1044

24. TakayamaYSatoHSaitohSOgiyamaYMasudaF 2008 Biphasic incorporation of centromeric histone CENP-A in fission yeast. Mol Biol Cell 19 682 690

25. SchuhMLehnerCFHeidmannS 2007 Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17 237 243

26. JansenLEBlackBEFoltzDRClevelandDW 2007 Propagation of centromeric chromatin requires exit from mitosis. J Cell Biol 176 795 805

27. SekulicNBassettEARogersDJBlackBE 2010 The structure of (CENP-A-H4)(2) reveals physical features that mark centromeres. Nature 467 347 351

28. BlackBEClevelandDW 2011 Epigenetic Centromere Propagation and the Nature of CENP-A Nucleosomes. Cell 144 471 479

29. DalalYFuruyamaTVermaakDHenikoffS 2007 Structure, dynamics, and evolution of centromeric nucleosomes. Proc Natl Acad Sci U S A 104 15974 15981

30. DalalYWangHLindsaySHenikoffS 2007 Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol 5 e218 doi:10.1371/journal.pbio.0050218

31. FuruyamaTHenikoffS 2009 Centromeric nucleosomes induce positive DNA supercoils. Cell 138 104 113

32. DimitriadisEKWeberCGillRKDiekmannSDalalY 2010 Tetrameric organization of vertebrate centromeric nucleosomes. Proc Natl Acad Sci U S A 107 20317 20322

33. BloomKSCarbonJ 1982 Yeast centromere DNA is in a unique and highly ordered structure in chromosomes and small circular minichromosomes. Cell 29 305 317

34. FunkMHegemannJHPhilippsenP 1989 Chromatin digestion with restriction endonucleases reveals 150–160 bp of protected DNA in the centromere of chromosome XIV in Saccharomyces cerevisiae. Mol Gen Genet 219 153 160

35. CamahortRShivarajuMMattinglyMLiBNakanishiS 2009 Cse4 is part of an octameric nucleosome in budding yeast. Mol Cell 35 794 805

36. KennaMAmayaEBloomK 1988 Selective excision of the centromere chromatin complex from Saccharomyces cerevisiae. The Journal of cell biology 107 9 15

37. FuruyamaSBigginsS 2007 Centromere identity is specified by a single centromeric nucleosome in budding yeast. Proc Natl Acad Sci U S A 104 14706 14711

38. SaundersMFitzgerald-HayesMBloomK 1988 Chromatin structure of altered yeast centromeres. Proceedings of the National Academy of Sciences of the United States of America 85 175 179

39. SaundersMJYehEGrunsteinMBloomK 1990 Nucleosome depletion alters the chromatin structure of Saccharomyces cerevisiae centromeres. Molecular and cellular biology 10 5721 5727

40. PetersenMWengelJ 2003 LNA: a versatile tool for therapeutics and genomics. Trends Biotechnol 21 74 81

41. TachiwanaHKagawaWShigaTOsakabeAMiyaY 2011 Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 476 232 235

42. LugerKMaderAWRichmondRKSargentDFRichmondTJ 1997 Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389 251 260

43. Camerini-OteroRDFelsenfeldG 1977 Histone H3 disulfide dimers and nucleosome structure. Proc Natl Acad Sci U S A 74 5519 5523

44. BodeJ 1979 Inter- and intramolecular crosslinks in histone H3 induced by 5,5′-dithiobis(2-nitrobenzoic acid). Anal Biochem 94 465 469

45. CottarelGSheroJHHieterPHegemannJH 1989 A 125-base-pair CEN6 DNA fragment is sufficient for complete meiotic and mitotic centromere functions in Saccharomyces cerevisiae. Mol Cell Biol 9 3342 3349

46. HegemannJHFleigUN 1993 The centromere of budding yeast. Bioessays 15 451 460

47. KeithKCFitzgerald-HayesM 2000 CSE4 genetically interacts with the Saccharomyces cerevisiae centromere DNA elements CDE I and CDE II but not CDE III. Implications for the path of the centromere dna around a cse4p variant nucleosome. Genetics 156 973 981

48. KingstonIJYungJSSingletonMR 2011 Biophysical characterization of the centromere-specific nucleosome from budding yeast. The Journal of biological chemistry 286 4021 4026

49. DechassaMLWynsKLiMHallMAWangMD 2011 Structure and Scm3-mediated assembly of budding yeast centromeric nucleosomes. Nature communications 2 313

50. ZhangWColmenaresSUKarpenGH 2012 Assembly of Drosophila Centromeric Nucleosomes Requires CID Dimerization. Molecular cell 45 263 269

51. ColeHAHowardBHClarkDJ 2011 The centromeric nucleosome of budding yeast is perfectly positioned and covers the entire centromere. Proceedings of the National Academy of Sciences of the United States of America 108 12687 12692

52. HuHLiuYWangMFangJHuangH 2011 Structure of a CENP-A-histone H4 heterodimer in complex with chaperone HJURP. Genes & development 25 901 906

53. BassettEADenizioJBarnhart-DaileyMCPanchenkoTSekulicN 2012 HJURP Uses Distinct CENP-A Surfaces to Recognize and to Stabilize CENP-A/Histone H4 for Centromere Assembly. Developmental cell 22 749 762

54. LawrimoreJBloomKSSalmonED 2011 Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. The Journal of cell biology 195 573 582

55. CoffmanVCWuPParthunMRWuJQ 2011 CENP-A exceeds microtubule attachment sites in centromere clusters of both budding and fission yeast. The Journal of cell biology 195 563 572

56. HenikoffSHenikoffJG 2012 “Point” centromeres of Saccharomyces harbor single centromere-specific nucleosomes. Genetics 190 1575 1577

57. IvanovDNasmythK 2005 A topological interaction between cohesin rings and a circular minichromosome. Cell 122 849 860

58. IvanovDNasmythK 2007 A physical assay for sister chromatid cohesion in vitro. Mol Cell 27 300 310

59. GaussRTrautweinMSommerTSpangA 2005 New modules for the repeated internal and N-terminal epitope tagging of genes in Saccharomyces cerevisiae. Yeast 22 1 12

60. DeshaiesRJKirschnerM 1995 G1 cyclin-dependent activation of p34CDC28 (Cdc28p) in vitro. Proc Natl Acad Sci U S A 92 1182 1186

61. WhiteCLSutoRKLugerK 2001 Structure of the yeast nucleosome core particle reveals fundamental changes in internucleosome interactions. The EMBO journal 20 5207 5218