Centromere-Like Regions in the Budding Yeast Genome

English version České info

Accurate chromosome segregation requires centromeres (CENs), the DNA sequences where kinetochores form, to attach chromosomes to microtubules. In contrast to most eukaryotes, which have broad centromeres, Saccharomyces cerevisiae possesses sequence-defined point CENs. Chromatin immunoprecipitation followed by sequencing (ChIP–Seq) reveals colocalization of four kinetochore proteins at novel, discrete, non-centromeric regions, especially when levels of the centromeric histone H3 variant, Cse4 (a.k.a. CENP-A or CenH3), are elevated. These regions of overlapping protein binding enhance the segregation of plasmids and chromosomes and have thus been termed Centromere-Like Regions (CLRs). CLRs form in close proximity to S. cerevisiae CENs and share characteristics typical of both point and regional CENs. CLR sequences are conserved among related budding yeasts. Many genomic features characteristic of CLRs are also associated with these conserved homologous sequences from closely related budding yeasts. These studies provide general and important insights into the origin and evolution of centromeres.

Vyšlo v časopise: Centromere-Like Regions in the Budding Yeast Genome. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003209
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003209

Souhrn

Zdroje

1. MalikHS, HenikoffS (2009) Major evolutionary transitions in centromere complexity. Cell 138: 1067–1082.

2. ClarkeL, CarbonJ (1980) Isolation of a yeast centromere and construction of functional small circular chromosomes. Nature 287: 504–509.

3. MeluhPB, YangP, GlowczewskiL, KoshlandD, SmithMM (1998) Cse4p is a component of the core centromere of Saccharomyces cerevisiae. Cell 94: 607–613.

4. TomonagaT, MatsushitaK, YamaguchiS, OohashiT, ShimadaH, et al. (2003) Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res 63: 3511–3516.

5. LefrancoisP, EuskirchenGM, AuerbachRK, RozowskyJ, GibsonT, et al. (2009) Efficient yeast ChIP-Seq using multiplex short-read DNA sequencing. BMC Genomics 10: 37.

6. CrottiLB, BasraiMA (2004) Functional roles for evolutionarily conserved Spt4p at centromeres and heterochromatin in Saccharomyces cerevisiae. Embo J 23: 1804–1814.

7. HewawasamG, ShivarajuM, MattinglyM, VenkateshS, Martin-BrownS, et al. (2010) Psh1 is an E3 ubiquitin ligase that targets the centromeric histone variant Cse4. Mol Cell 40: 444–454.

8. RanjitkarP, PressMO, YiX, BakerR, MacCossMJ, et al. (2010) An E3 ubiquitin ligase prevents ectopic localization of the centromeric histone H3 variant via the centromere targeting domain. Mol Cell 40: 455–464.

9. LefrancoisP, ZhengW, SnyderM (2010) ChIP-Seq using high-throughput DNA sequencing for genome-wide identification of transcription factor binding sites. Methods Enzymol 470: 77–104.

10. RozowskyJ, EuskirchenG, AuerbachRK, ZhangZD, GibsonT, et al. (2009) PeakSeq enables systematic scoring of ChIP-seq experiments relative to controls. Nat Biotechnol 27: 66–75.

11. ZhengW, ZhaoH, ManceraE, SteinmetzLM, SnyderM (2010) Genetic analysis of variation in transcription factor binding in yeast. Nature 464: 1187–1191.

12. CamahortR, ShivarajuM, MattinglyM, LiB, NakanishiS, et al. (2009) Cse4 is part of an octameric nucleosome in budding yeast. Mol Cell 35: 794–805.

13. BurrackLS, ApplenSE, BermanJ (2011) The Requirement for the Dam1 Complex Is Dependent upon the Number of Kinetochore Proteins and Microtubules. Curr Biol 21: 889–896.

14. YehE, HaaseJ, PaliulisLV, JoglekarA, BondL, et al. (2008) Pericentric chromatin is organized into an intramolecular loop in mitosis. Curr Biol 18: 81–90.

15. StephensAD, HaaseJ, VicciL, TaylorRM2nd, BloomK (2011) Cohesin, condensin, and the intramolecular centromere loop together generate the mitotic chromatin spring. J Cell Biol 193: 1167–1180.

16. AndersonM, HaaseJ, YehE, BloomK (2009) Function and assembly of DNA looping, clustering, and microtubule attachment complexes within a eukaryotic kinetochore. Mol Biol Cell 20: 4131–4139.

17. LacefieldS, LauDT, MurrayAW (2009) Recruiting a microtubule-binding complex to DNA directs chromosome segregation in budding yeast. Nat Cell Biol 11: 1116–1120.

18. SikorskiRS, HieterP (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19–27.

19. MurrayAW, SzostakJW (1983) Pedigree analysis of plasmid segregation in yeast. Cell 34: 961–970.

20. HajraS, GhoshSK, JayaramM (2006) The centromere-specific histone variant Cse4p (CENP-A) is essential for functional chromatin architecture at the yeast 2-microm circle partitioning locus and promotes equal plasmid segregation. J Cell Biol 174: 779–790.

21. IvanovD, NasmythK (2005) A topological interaction between cohesin rings and a circular minichromosome. Cell 122: 849–860.

22. KeithKC, BakerRE, ChenY, HarrisK, StolerS, et al. (1999) Analysis of primary structural determinants that distinguish the centromere-specific function of histone variant Cse4p from histone H3. Mol Cell Biol 19: 6130–6139.

23. AkiyoshiB, NelsonCR, RanishJA, BigginsS (2009) Quantitative proteomic analysis of purified yeast kinetochores identifies a PP1 regulatory subunit. Genes Dev 23: 2887–2899.

24. HieterP, MannC, SnyderM, DavisRW (1985) Mitotic stability of yeast chromosomes: a colony color assay that measures nondisjunction and chromosome loss. Cell 40: 381–392.

25. HillA, BloomK (1987) Genetic manipulation of centromere function. Mol Cell Biol 7: 2397–2405.

26. WellsWA, MurrayAW (1996) Aberrantly segregating centromeres activate the spindle assembly checkpoint in budding yeast. J Cell Biol 133: 75–84.

27. OrtizJ, StemmannO, RankS, LechnerJ (1999) A putative protein complex consisting of Ctf19, Mcm21, and Okp1 represents a missing link in the budding yeast kinetochore. Genes Dev 13: 1140–1155.

28. PearsonCG, MaddoxPS, ZarzarTR, SalmonED, BloomK (2003) Yeast kinetochores do not stabilize Stu2p-dependent spindle microtubule dynamics. Mol Biol Cell 14: 4181–4195.

29. GohPY, KilmartinJV (1993) NDC10: a gene involved in chromosome segregation in Saccharomyces cerevisiae. J Cell Biol 121: 503–512.

30. BakerRE, RogersK (2005) Genetic and genomic analysis of the AT-rich centromere DNA element II of Saccharomyces cerevisiae. Genetics 171: 1463–1475.

31. HuangCC, HajraS, GhoshSK, JayaramM (2011) Cse4 (CenH3) association with the Saccharomyces cerevisiae plasmid partitioning locus in its native and chromosomally integrated states: implications in centromere evolution. Mol Cell Biol 31: 1030–1040.

32. KetelC, WangHS, McClellanM, BouchonvilleK, SelmeckiA, et al. (2009) Neocentromeres form efficiently at multiple possible loci in Candida albicans. PLoS Genet 5: e1000400 doi:10.1371/journal.pgen.1000400.

33. KorenA, TsaiHJ, TiroshI, BurrackLS, BarkaiN, et al. (2010) Epigenetically-inherited centromere and neocentromere DNA replicates earliest in S-phase. PLoS Genet 6: e1001068 doi:10.1371/journal.pgen.1001068.

34. AuerbachRK, EuskirchenG, RozowskyJ, Lamarre-VincentN, MoqtaderiZ, et al. (2009) Mapping accessible chromatin regions using Sono-Seq. Proc Natl Acad Sci U S A 106: 14926–14931.

35. CollinsK, FuruyamaS, BigginsS (2004) Proteolysis contributes to the exclusive centromere localization of the yeast Cse4/CENP-A histone H3 variant. Curr Biol 14: 1968–1972.

36. StolerS, RogersK, WeitzeS, MoreyL, Fitzgerald-HayesM, et al. (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.

37. da RosaJL, HolikJ, GreenEM, RandoOJ, KaufmanPD (2011) Overlapping regulation of CenH3 localization and histone H3 turnover by CAF-1 and HIR proteins in Saccharomyces cerevisiae. Genetics 187: 9–19.

38. XiaoH, MizuguchiG, WisniewskiJ, HuangY, WeiD, et al. (2011) Nonhistone Scm3 binds to AT-rich DNA to organize atypical centromeric nucleosome of budding yeast. Mol Cell 43: 369–380.

39. KrassovskyK, HenikoffJG, HenikoffS (2012) Tripartite organization of centromeric chromatin in budding yeast. Proc Natl Acad Sci U S A 109: 243–248.

40. KoshlandD, RutledgeL, Fitzgerald-HayesM, HartwellLH (1987) A genetic analysis of dicentric minichromosomes in Saccharomyces cerevisiae. Cell 48: 801–812.

41. MeraldiP, McAinshAD, RheinbayE, SorgerPK (2006) Phylogenetic and structural analysis of centromeric DNA and kinetochore proteins. Genome Biol 7: R23.

42. ScannellDR, ZillOA, RokasA, PayenC, DunhamMJ, et al. (2011) The Awesome Power of Yeast Evolutionary Genetics: New Genome Sequences and Strain Resources for the Saccharomyces sensu stricto Genus. G3 (Bethesda) 1: 11–25.

43. MishraPK, AuWC, ChoyJS, KuichPH, BakerRE, et al. (2011) Misregulation of Scm3p/HJURP causes chromosome instability in Saccharomyces cerevisiae and human cells. PLoS Genet 7: e1002303 doi:10.1371/journal.pgen.1002303.

44. HeunP, ErhardtS, BlowerMD, WeissS, SkoraAD, et al. (2006) Mislocalization of the Drosophila centromere-specific histone CID promotes formation of functional ectopic kinetochores. Dev Cell 10: 303–315.

45. MarshallOJ, ChuehAC, WongLH, ChooKH (2008) Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am J Hum Genet 82: 261–282.

46. GuseA, CarrollCW, MoreeB, FullerCJ, StraightAF (2011) In vitro centromere and kinetochore assembly on defined chromatin templates. Nature 477: 354–358.

47. MendiburoMJ, PadekenJ, FulopS, SchepersA, HeunP (2011) Drosophila CENH3 is sufficient for centromere formation. Science 334: 686–690.

48. BarnhartMC, KuichPH, StellfoxME, WardJA, BassettEA, et al. (2011) HJURP is a CENP-A chromatin assembly factor sufficient to form a functional de novo kinetochore. J Cell Biol 194: 229–243.

49. AlonsoA, HassonD, CheungF, WarburtonPE (2010) A paucity of heterochromatin at functional human neocentromeres. Epigenetics Chromatin 3: 6.

50. VenturaM, WeiglS, CarboneL, CardoneMF, MisceoD, et al. (2004) Recurrent sites for new centromere seeding. Genome Res 14: 1696–1703.

51. TeytelmanL, OzaydinB, ZillO, LefrancoisP, SnyderM, et al. (2009) Impact of chromatin structures on DNA processing for genomic analyses. PLoS ONE 4: e6700 doi:10.1371/journal.pone.0006700.

52. EdgarR, DomrachevM, LashA (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207–210.

53. EuskirchenGM, AuerbachRK, DavidovE, GianoulisTA, ZhongG, et al. (2011) Diverse roles and interactions of the SWI/SNF chromatin remodeling complex revealed using global approaches. PLoS Genet 7: e1002008 doi:10.1371/journal.pgen.1002008.

54. GersteinMB, LuZJ, Van NostrandEL, ChengC, ArshinoffBI, et al. (2010) Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330: 1775–1787.

55. EuskirchenG, RozowskyJ, WeiC, LeeW, ZhangZ, et al. (2007) Mapping of transcription factor binding regions in mammalian cells by ChIP: comparison of array- and sequencing-based technologies. Genome Res 17: 898–909.

56. ConsortiumEP (2011) A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol 9: e1001046 doi:10.1371/journal.pbio.1001046.

57. PfafflM (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.

58. ZhuLJ, GazinC, LawsonND, PagesH, LinSM, et al. (2010) ChIPpeakAnno: a Bioconductor package to annotate ChIP-seq and ChIP-chip data. BMC Bioinformatics 11: 237.

59. KushnirovVV (2000) Rapid and reliable protein extraction from yeast. Yeast 16: 857–860.

60. LeaDEC, C.A. (1949) The distribution of the numbers of mutants in bacterial populations. J Genetics 49: 264–285.

61. CummingsL, RileyL, BlackL, SouvorovA, ResenchukS, et al. (2002) Genomic BLAST: custom-defined virtual databases for complete and unfinished genomes. FEMS Microbiol Lett 216: 133–138.

62. Van HooserAA, OuspenskiII, GregsonHC, StarrDA, YenTJ, et al. (2001) Specification of kinetochore-forming chromatin by the histone H3 variant CENP-A. J Cell Sci 114: 3529–3542.

63. DionMF, KaplanT, KimM, BuratowskiS, FriedmanN, et al. (2007) Dynamics of replication-independent histone turnover in budding yeast. Science 315: 1405–1408.