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Competition between Heterochromatic Loci Allows the Abundance of the Silencing Protein, Sir4, to Regulate Assembly of Heterochromatin


Heterochromatin, characterized by the repression of transcription, is a specialized chromatin structure that plays both structural and functional roles on chromosomes. Heterochromatic domains are dynamic, switching between active and inactive states, and this property is used by cells during developmental switches and may generate phenotypic diversity. We have shown that competition between different heterochromatic domains for limiting amounts of a heterochromatin protein, Sir4, plays a critical role in the switch from an active to an inactive state. Previous work has suggested that this switch is regulated by turnover of histone modifications in these regions and our data suggests that modulating Sir4 abundance acts in parallel to these changes to influence the rate of de novo assembly. This work supports a model in which competition between different chromosomal domains is exploited by cells to regulate cell identity.


Vyšlo v časopise: Competition between Heterochromatic Loci Allows the Abundance of the Silencing Protein, Sir4, to Regulate Assembly of Heterochromatin. PLoS Genet 11(11): e32767. doi:10.1371/journal.pgen.1005425
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005425

Souhrn

Heterochromatin, characterized by the repression of transcription, is a specialized chromatin structure that plays both structural and functional roles on chromosomes. Heterochromatic domains are dynamic, switching between active and inactive states, and this property is used by cells during developmental switches and may generate phenotypic diversity. We have shown that competition between different heterochromatic domains for limiting amounts of a heterochromatin protein, Sir4, plays a critical role in the switch from an active to an inactive state. Previous work has suggested that this switch is regulated by turnover of histone modifications in these regions and our data suggests that modulating Sir4 abundance acts in parallel to these changes to influence the rate of de novo assembly. This work supports a model in which competition between different chromosomal domains is exploited by cells to regulate cell identity.


Zdroje

1. Kueng S, Oppikofer M, Gasser SM. SIR Proteins and the Assembly of Silent Chromatin in Budding Yeast. Annu Rev Genet. 2013. doi: 10.1146/annurev-genet-021313-173730

2. Rusche LN, Kirchmaier AL, Rine J. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem. 2003;72: 481–516. doi: 10.1146/annurev.biochem.72.121801.161547 12676793

3. Imai S, Armstrong CM, Kaeberlein M, Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature. 2000;403: 795–800. doi: 10.1038/35001622 10693811

4. Tanny JC, Dowd GJ, Huang J, Hilz H, Moazed D. An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing. Cell. 1999;99: 735–745. 10619427

5. Tanner KG, Landry J, Sternglanz R, Denu JM. Silent information regulator 2 family of NAD- dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proceedings of the National Academy of Sciences of the United States of America. 2000;97: 14178–14182. doi: 10.1073/pnas.250422697 11106374

6. Hecht A, Laroche T, Strahl-Bolsinger S, Gasser SM, Grunstein M. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell. 1995;80: 583–592. 7867066

7. Johnson A, Li G, Sikorski TW, Buratowski S, Woodcock CL, Moazed D. Reconstitution of heterochromatin-dependent transcriptional gene silencing. Mol Cell. 2009;35: 769–781. doi: 10.1016/j.molcel.2009.07.030 19782027

8. Martino F, Kueng S, Robinson P, Tsai-Pflugfelder M, van Leeuwen F, Ziegler M, et al. Reconstitution of yeast silent chromatin: multiple contact sites and O-AADPR binding load SIR complexes onto nucleosomes in vitro. Mol Cell. 2009;33: 323–334. doi: 10.1016/j.molcel.2009.01.009 19217406

9. Aparicio OM, Billington BL, Gottschling DE. Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae. Cell. 1991;66: 1279–1287. 1913809

10. Klar AJ, Fogel S, Macleod K. MAR1-a Regulator of the HMa and HMalpha Loci in SACCHAROMYCES CEREVISIAE. Genetics. 1979;93: 37–50. 17248968

11. Ivy JM, Klar AJ, Hicks JB. Cloning and characterization of four SIR genes of Saccharomyces cerevisiae. Mol Cell Biol. 1986;6: 688–702. 3023863

12. Rine J, Herskowitz I. Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics. 1987;116: 9–22. 3297920

13. Haber JE, George JP. A mutation that permits the expression of normally silent copies of mating-type information in Saccharomyces cerevisiae. Genetics. 1979;93: 13–35. 16118901

14. Hopper AK, Hall BD. Mutation of a heterothallic strain to homothallism. Genetics. 1975;80: 77–85. 1093938

15. Luo K, Vega-Palas MA, Grunstein M. Rap1-Sir4 binding independent of other Sir, yKu, or histone interactions initiates the assembly of telomeric heterochromatin in yeast. Genes Dev. 2002;16: 1528–1539. doi: 10.1101/gad.988802 12080091

16. Rusche LN, Kirchmaier AL, Rine J. Ordered nucleation and spreading of silenced chromatin in Saccharomyces cerevisiae. Mol Biol Cell. 2002;13: 2207–2222. doi: 10.1091/mbc.E02-03-0175 12134062

17. Hoppe GJ, Tanny JC, Rudner AD, Gerber SA, Danaie S, Gygi SP, et al. Steps in assembly of silent chromatin in yeast: Sir3-independent binding of a Sir2/Sir4 complex to silencers and role for Sir2-dependent deacetylation. Mol Cell Biol. 2002;22: 4167–4180. 12024030

18. Kitada T, Kuryan BG, Tran NNH, Song C, Xue Y, Carey M, et al. Mechanism for epigenetic variegation of gene expression at yeast telomeric heterochromatin. Genes Dev. 2012;26: 2443–2455. doi: 10.1101/gad.201095.112 23124068

19. Katan-Khaykovich Y, Struhl K. Heterochromatin formation involves changes in histone modifications over multiple cell generations. EMBO J. 2005;24: 2138–2149. doi: 10.1038/sj.emboj.7600692 15920479

20. Kirchmaier AL, Rine J. Cell cycle requirements in assembling silent chromatin in Saccharomyces cerevisiae. Mol Cell Biol. 2006;26: 852–862. doi: 10.1128/MCB.26.3.852-862.2006 16428441

21. Miller AM, Nasmyth KA. Role of DNA replication in the repression of silent mating type loci in yeast. Nature. 1984;312: 247–251. 6390211

22. Lau A, Blitzblau H, Bell SP. Cell-cycle control of the establishment of mating-type silencing in S. cerevisiae. Genes Dev. 2002;16: 2935–2945. doi: 10.1101/gad.764102 12435634

23. Fox CA, Ehrenhofer-Murray AE, Loo S, Rine J. The origin recognition complex, SIR1, and the S phase requirement for silencing. Science. 1997;276: 1547–1551. 9171055

24. Li YC, Cheng TH, Gartenberg MR. Establishment of transcriptional silencing in the absence of DNA replication. Science. 2001;291: 650–653. doi: 10.1126/science.291.5504.650 11158677

25. Kirchmaier AL, Rine J. DNA replication-independent silencing in S. cerevisiae. Science. 2001;291: 646–650. doi: 10.1126/science.291.5504.646 11158676

26. Osborne EA, Dudoit S, Rine J. The establishment of gene silencing at single-cell resolution. Nat Genet. 2009;41: 800–806. doi: 10.1038/ng.402 19543267

27. Venkatasubrahmanyam S, Hwang WW, Meneghini MD, Tong AHY, Madhani HD. Genome-wide, as opposed to local, antisilencing is mediated redundantly by the euchromatic factors Set1 and H2A.Z. Proceedings of the National Academy of Sciences of the United States of America. 2007;104: 16609–16614. doi: 10.1073/pnas.0700914104 17925448

28. Martins-Taylor K, Sharma U, Rozario T, Holmes SG. H2A.Z (Htz1) controls the cell-cycle-dependent establishment of transcriptional silencing at Saccharomyces cerevisiae telomeres. Genetics. 2011;187: 89–104. doi: 10.1534/genetics.110.123844 20980239

29. Lacoste N, Utley RT, Hunter JM, Poirier GG, Côté J. Disruptor of telomeric silencing-1 is a chromatin-specific histone H3 methyltransferase. 2002;277: 30421–30424. doi: 10.1074/jbc.C200366200 12097318

30. Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, Dent SY, et al. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 2001;15: 3286–3295. doi: 10.1101/gad.940201 11751634

31. Fingerman IM, Li H-C, Briggs SD. A charge-based interaction between histone H4 and Dot1 is required for H3K79 methylation and telomere silencing: identification of a new trans-histone pathway. Genes Dev. 2007;21: 2018–2029. doi: 10.1101/gad.1560607 17675446

32. van Leeuwen F, Gafken PR, Gottschling DE. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell. 2002;109: 745–756. 12086673

33. Ng HH, Feng Q, Wang H, Erdjument-Bromage H, Tempst P, Zhang Y, et al. Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev. 2002;16: 1518–1527. doi: 10.1101/gad.1001502 12080090

34. Osborne EA, Hiraoka Y, Rine J. Symmetry, asymmetry, and kinetics of silencing establishment in Saccharomyces cerevisiae revealed by single-cell optical assays. Proceedings of the National Academy of Sciences of the United States of America. 2011;108: 1209–1216. doi: 10.1073/pnas.1018742108 21262833

35. Sussel L, Vannier D, Shore D. Epigenetic switching of transcriptional states: cis- and trans-acting factors affecting establishment of silencing at the HMR locus in Saccharomyces cerevisiae. Mol Cell Biol. 1993;13: 3919–3928. 8321199

36. Gotta M, Laroche T, Formenton A, Maillet L, Scherthan H, Gasser SM. The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae. J Cell Biol. 1996;134: 1349–1363. 8830766

37. Laroche T, Martin SG, Tsai-Pflugfelder M, Gasser SM. The dynamics of yeast telomeres and silencing proteins through the cell cycle. J Struct Biol. 2000;129: 159–174. doi: 10.1006/jsbi.2000.4240 10806066

38. Gao CY, Pinkham JL. Tightly regulated, beta-estradiol dose-dependent expression system for yeast. BioTechniques. 2000;29: 1226–1231. 11126125

39. Marshall M, Mahoney D, Rose A, Hicks JB, Broach JR. Functional domains of SIR4, a gene required for position effect regulation in Saccharomyces cerevisiae. Mol Cell Biol. 1987;7: 4441–4452. 3325825

40. Cockell M, Palladino F, Laroche T, Kyrion G, Liu C, Lustig AJ, et al. The carboxy termini of Sir4 and Rap1 affect Sir3 localization: evidence for a multicomponent complex required for yeast telomeric silencing. J Cell Biol. 1995;129: 909–924. 7744964

41. Singer MS, Kahana A, Wolf AJ, Meisinger LL, Peterson SE, Goggin C, et al. Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics. 1998;150: 613–632. 9755194

42. Marcand S, Buck SW, Moretti P, Gilson E, Shore D. Silencing of genes at nontelomeric sites in yeast is controlled by sequestration of silencing factors at telomeres by Rap 1 protein. Genes Dev. 1996;10: 1297–1309. 8647429

43. Buck SW, Shore D. Action of a RAP1 carboxy-terminal silencing domain reveals an underlying competition between HMR and telomeres in yeast. Genes Dev. 1995;9: 370–384. 7867933

44. Smeal T, Claus J, Kennedy B, Cole F, Guarente L. Loss of transcriptional silencing causes sterility in old mother cells of S. cerevisiae. Cell. 1996;84: 633–642. 8598049

45. Kennedy BK, Austriaco NR, Zhang J, Guarente L. Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae. Cell. 1995;80: 485–496. 7859289

46. Gardner RG, Nelson ZW, Gottschling DE. Ubp10/Dot4p regulates the persistence of ubiquitinated histone H2B: distinct roles in telomeric silencing and general chromatin. Mol Cell Biol. 2005;25: 6123–6139. doi: 10.1128/MCB.25.14.6123-6139.2005 15988024

47. Emre NCT, Ingvarsdottir K, Wyce A, Wood A, Krogan NJ, Henry KW, et al. Maintenance of low histone ubiquitylation by Ubp10 correlates with telomere-proximal Sir2 association and gene silencing. Mol Cell. 2005;17: 585–594. doi: 10.1016/j.molcel.2005.01.007 15721261

48. Orlandi I, Bettiga M, Alberghina L, Vai M. Transcriptional profiling of ubp10 null mutant reveals altered subtelomeric gene expression and insurgence of oxidative stress response. 2004;279: 6414–6425. doi: 10.1074/jbc.M306464200

49. Boulton SJ, Jackson SP. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 1998;17: 1819–1828. doi: 10.1093/emboj/17.6.1819 9501103

50. Lopez CR, Ribes-Zamora A, Indiviglio SM, Williams CL, Haricharan S, Bertuch AA. Ku must load directly onto the chromosome end in order to mediate its telomeric functions. Cohen-Fix O, editor. PLoS Genet. Public Library of Science; 2011;7: e1002233. doi: 10.1371/journal.pgen.1002233

51. Gartenberg MR, Neumann FR, Laroche T, Blaszczyk M, Gasser SM. Sir-mediated repression can occur independently of chromosomal and subnuclear contexts. Cell. 2004;119: 955–967. doi: 10.1016/j.cell.2004.11.008 15620354

52. Patterson EE, Fox CA. The Ku complex in silencing the cryptic mating-type loci of Saccharomyces cerevisiae. Genetics. 2008;180: 771–783. doi: 10.1534/genetics.108.091710 18716325

53. Vandre CL, Kamakaka RT, Rivier DH. The DNA end-binding protein Ku regulates silencing at the internal HML and HMR loci in Saccharomyces cerevisiae. Genetics. 2008;180: 1407–1418. doi: 10.1534/genetics.108.094490 18791224

54. Mishra K, Shore D. Yeast Ku protein plays a direct role in telomeric silencing and counteracts inhibition by rif proteins. Curr Biol. 1999;9: 1123–1126. 10531008

55. Wotton D, Shore D. A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes Dev. 1997;11: 748–760. 9087429

56. Hardy CF, Sussel L, Shore D. A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes Dev. 1992;6: 801–814. 1577274

57. Moretti P, Freeman K, Coodly L, Shore D. Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1. Genes Dev. 1994;8: 2257–2269. 7958893

58. Moretti P, Shore D. Multiple interactions in Sir protein recruitment by Rap1p at silencers and telomeres in yeast. Mol Cell Biol. 2001;21: 8082–8094. doi: 10.1128/MCB.21.23.8082-8094.2001 11689698

59. Liu C, Lustig AJ. Genetic analysis of Rap1p/Sir3p interactions in telomeric and HML silencing in Saccharomyces cerevisiae. Genetics. 1996;143: 81–93. 8722764

60. Liu C, Mao X, Lustig AJ. Mutational analysis defines a C-terminal tail domain of RAP1 essential for Telomeric silencing in Saccharomyces cerevisiae. Genetics. 1994;138: 1025–1040. 7896088

61. Rudner AD, Hall BE, Ellenberger T, Moazed D. A nonhistone protein-protein interaction required for assembly of the SIR complex and silent chromatin. Mol Cell Biol. 2005;25: 4514–4528. doi: 10.1128/MCB.25.11.4514-4528.2005 15899856

62. Onishi M, Liou G-G, Buchberger JR, Walz T, Moazed D. Role of the conserved Sir3-BAH domain in nucleosome binding and silent chromatin assembly. Mol Cell. 2007;28: 1015–1028. doi: 10.1016/j.molcel.2007.12.004 18158899

63. Armache K-J, Garlick JD, Canzio D, Narlikar GJ, Kingston RE. Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 Å resolution. Science. 2011;334: 977–982. doi: 10.1126/science.1210915 22096199

64. Moazed D. Mechanisms for the inheritance of chromatin States. Cell. 2011;146: 510–518. doi: 10.1016/j.cell.2011.07.013 21854979

65. Miao F, Natarajan R. Mapping global histone methylation patterns in the coding regions of human genes. Mol Cell Biol. 2005;25: 4650–4661. doi: 10.1128/MCB.25.11.4650-4661.2005 15899867

66. Schübeler D, MacAlpine DM, Scalzo D, Wirbelauer C, Kooperberg C, van Leeuwen F, et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 2004;18: 1263–1271. doi: 10.1101/gad.1198204 15175259

67. Schulze JM, Jackson J, Nakanishi S, Gardner JM, Hentrich T, Haug J, et al. Linking cell cycle to histone modifications: SBF and H2B monoubiquitination machinery and cell-cycle regulation of H3K79 dimethylation. Mol Cell. 2009;35: 626–641. doi: 10.1016/j.molcel.2009.07.017 19682934

68. Altaf M, Utley RT, Lacoste N, Tan S, Briggs SD, Côté J. Interplay of chromatin modifiers on a short basic patch of histone H4 tail defines the boundary of telomeric heterochromatin. Mol Cell. 2007;28: 1002–1014. doi: 10.1016/j.molcel.2007.12.002 18158898

69. Oppikofer M, Kueng S, Martino F, Soeroes S, Hancock SM, Chin JW, et al. A dual role of H4K16 acetylation in the establishment of yeast silent chromatin. EMBO J. 2011;30: 2610–2621. doi: 10.1038/emboj.2011.170 21666601

70. Yang B, Britton J, Kirchmaier AL. Insights into the impact of histone acetylation and methylation on Sir protein recruitment, spreading, and silencing in Saccharomyces cerevisiae. J Mol Biol. 2008;381: 826–844. doi: 10.1016/j.jmb.2008.06.059 18619469

71. Lazarus AG, Holmes SG. A cis-acting tRNA gene imposes the cell cycle progression requirement for establishing silencing at the HMR locus in yeast. Genetics. 2011;187: 425–439. doi: 10.1534/genetics.110.124099 21135074

72. Ren J, Wang C-L, Sternglanz R. Promoter Strength Influences the S Phase Requirement for Establishment of Silencing at the Saccharomyces cerevisiae Silent Mating Type Loci. Genetics. 2010;186: 551–U172. doi: 10.1534/genetics.110.120592 20679515

73. Triolo T, Sternglanz R. Role of interactions between the origin recognition complex and SIR1 in transcriptional silencing. Nature. 1996;381: 251–253. doi: 10.1038/381251a0 8622770

74. Connelly JJ, Yuan P, Hsu H-C, Li Z, Xu R-M, Sternglanz R. Structure and function of the Saccharomyces cerevisiae Sir3 BAH domain. Mol Cell Biol. 2006;26: 3256–3265. doi: 10.1128/MCB.26.8.3256-3265.2006 16581798

75. van Welsem T, Frederiks F, Verzijlbergen KF, Faber AW, Nelson ZW, Egan DA, et al. Synthetic lethal screens identify gene silencing processes in yeast and implicate the acetylated amino terminus of Sir3 in recognition of the nucleosome core. Mol Cell Biol. 2008;28: 3861–3872. doi: 10.1128/MCB.02050-07 18391024

76. Kennedy BK, Gotta M, Sinclair DA, Mills K, McNabb DS, Murthy M, et al. Redistribution of silencing proteins from telomeres to the nucleolus is associated with extension of life span in S. cerevisiae. Cell. 1997;89: 381–391. 9150138

77. Mills KD, Sinclair DA, Guarente L. MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks. Cell. 1999;97: 609–620. 10367890

78. Martin SG, Laroche T, Suka N, Grunstein M, Gasser SM. Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell. 1999;97: 621–633. 10367891

79. McAinsh AD, Scott-Drew S, Murray JA, Jackson SP. DNA damage triggers disruption of telomeric silencing and Mec1p-dependent relocation of Sir3p. Curr Biol. 1999;9: 963–966. 10508591

80. Maillet L, Boscheron C, Gotta M, Marcand S, Gilson E, Gasser SM. Evidence for silencing compartments within the yeast nucleus: a role for telomere proximity and Sir protein concentration in silencer-mediated repression. Genes Dev. 1996;10: 1796–1811. 8698239

81. Taddei A, Van Houwe G, Nagai S, Erb I, van Nimwegen E, Gasser SM. The functional importance of telomere clustering: global changes in gene expression result from SIR factor dispersion. Genome Research. 2009;19: 611–625. doi: 10.1101/gr.083881.108 19179643

82. Smith JS, Brachmann CB, Pillus L, Boeke JD. Distribution of a limited Sir2 protein pool regulates the strength of yeast rDNA silencing and is modulated by Sir4p. Genetics. 1998;149: 1205–1219. 9649515

83. Tadeo X, Wang J, Kallgren SP, Liu J, Reddy BD, Qiao F, et al. Elimination of shelterin components bypasses RNAi for pericentric heterochromatin assembly. Genes Dev. 2013;27: 2489–2499. doi: 10.1101/gad.226118.113 24240238

84. Ai W, Bertram PG, Tsang CK, Chan TF, Zheng XFS. Regulation of subtelomeric silencing during stress response. Mol Cell. 2002;10: 1295–1305. 12504006

85. Halme A, Bumgarner S, Styles C, Fink GR. Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell. 2004;116: 405–415. 15016375

86. Tonkin CJ, Carret CK, Duraisingh MT, Voss TS, Ralph SA, Hommel M, et al. Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol. 2009;7: e84. doi: 10.1371/journal.pbio.1000084 19402747

87. Freitas-Junior LH, Hernandez-Rivas R, Ralph SA, Montiel-Condado D, Ruvalcaba-Salazar OK, Rojas-Meza AP, et al. Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell. 2005;121: 25–36. doi: 10.1016/j.cell.2005.01.037 15820676

88. Pérez-Martín J, Uría JA, Johnson AD. Phenotypic switching in Candida albicans is controlled by a SIR2 gene. EMBO J. 1999;18: 2580–2592. doi: 10.1093/emboj/18.9.2580 10228170

89. Juárez-Reyes A, Ramírez-Zavaleta CY, Medina-Sánchez L, Las Peñas De A, Castaño I. A protosilencer of subtelomeric gene expression in Candida glabrata with unique properties. Genetics. 2012;190: 101–111. doi: 10.1534/genetics.111.135251 22048024

90. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, et al. Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell. 1998;9: 3273–3297. 9843569

91. Goranov AI, Cook M, Ricicova M, Ben-Ari G, Gonzalez C, Hansen C, et al. The rate of cell growth is governed by cell cycle stage. Genes Dev. 2009;23: 1408–1422. doi: 10.1101/gad.1777309 19528319

92. Aparicio OM, Gottschling DE. Overcoming telomeric silencing: a trans-activator competes to establish gene expression in a cell cycle-dependent way. Genes Dev. 1994;8: 1133–1146. 7926719

93. Motwani T, Poddar M, Holmes SG. Sir3 and Epigenetic Inheritance of Silent Chromatin in Saccharomyces cerevisiae. Mol Cell Biol. 2012;32: 2784–2793. doi: 10.1128/MCB.06399-11 22586263

94. Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 1998;14: 953–961. doi: 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U 9717241

95. Goldstein AL, McCusker JH. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast. 1999;15: 1541–1553. doi: 10.1002/(SICI)1097-0061(199910)15:14<1541::AID-YEA476>3.0.CO;2-K 10514571

96. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, Maekawa H, et al. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast. 2004;21: 947–962. doi: 10.1002/yea.1142 15334558

97. Sheff MA, Thorn KS. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast. 2004;21: 661–670. doi: 10.1002/yea.1130 15197731

98. Roy N, Runge KW. Two paralogs involved in transcriptional silencing that antagonistically control yeast life span. Curr Biol. 2000;10: 111–114. 10662670

99. Cuperus G, Shore D. Restoration of silencing in Saccharomyces cerevisiae by tethering of a novel Sir2-interacting protein, Esc8. Genetics. 2002;162: 633–645. 12399377

100. Sikorski RS, Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989;122: 19–27. 2659436

101. Lianga N, Williams EC, Kennedy EK, Doré C, Pilon S, Girard SL, et al. A Wee1 checkpoint inhibits anaphase onset. J Cell Biol. 2013;201: 843–862. doi: 10.1083/jcb.201212038 23751495

102. Moazed D, Kistler A, Axelrod A, Rine J, Johnson AD. Silent information regulator protein complexes in Saccharomyces cerevisiae: a SIR2/SIR4 complex and evidence for a regulatory domain in SIR4 that inhibits its interaction with SIR3. Proceedings of the National Academy of Sciences of the United States of America. 1997;94: 2186–2191. 9122169

103. Liang C, Stillman B. Persistent initiation of DNA replication and chromatin-bound MCM proteins during the cell cycle in cdc6 mutants. Genes Dev. 1997;11: 3375–3386. 9407030

104. Gottschling DE, Aparicio OM, Billington BL, Zakian VA. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell. 1990;63: 751–762. 2225075

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