Global regulation of heterochromatin spreading by Leo1

Open Biology

Volumn 5, Issue 5, 2015, Pages

  Verrier, Laure ^a   Taglini, Francesca ^a   Barrales, Ramon R ^c   Webb, Shaun ^b   Urano, Takeshi ^d   Braun, Sigurd ^c   Bayne, Elizabeth H ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF MUNICH   (Germany)

^d SHIMANE UNIVERSITY   (Japan)

Author keywords

Epigenetics; Fission yeast; Genome regulation; Heterochromatin; Leo1

Indexed keywords

EUKARYOTA; SCHIZOSACCHAROMYCETACEAE;

HETEROCHROMATIN; HISTONE; PROTEIN BINDING; RNA BINDING PROTEIN;

ACETYLATION; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; FUNGAL GENOME; GENE EXPRESSION REGULATION; GENE ORDER; GENETICS; HETEROCHROMATIN; HIGH THROUGHPUT SEQUENCING; INVERTED REPEAT; METABOLISM; SCHIZOSACCHAROMYCES;

ACETYLATION; BINDING SITES; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION, FUNGAL; GENE ORDER; GENOME, FUNGAL; HETEROCHROMATIN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HISTONES; INVERTED REPEAT SEQUENCES; PROTEIN BINDING; RNA-BINDING PROTEINS; SCHIZOSACCHAROMYCES;

EID: 84935000852     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.150045     Document Type: Article

References (83)

1. Bannister AJ, Kouzarides T. 2011 Regulation of chromatin by histone modifications. Cell Res. 21, 381-395. (doi:10.1038/cr.2011.22)
2. Grewal SI, Jia S. 2007 Heterochromatin revisited. Nat. Rev. Genet. 8, 35-46. (doi:10.1038/nrg2008)
3. Talbert PB, Henikoff S. 2006 Spreading of silent chromatin: inaction at a distance. Nat. Rev. Genet. 7, 793-803. (doi:10.1038/nrg1920)
4. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T. 2001 Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410, 120-124. (doi:10.1038/35065138)
5. 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. (doi:10.1038/35065132)
6. Haldar S, Saini A, Nanda JS, Saini S, Singh J. 2011 Role of Swi6/HP1 self-association-mediated recruitment of Clr4/Suv39 in establishment and maintenance of heterochromatin in fission yeast. J. Biol. Chem. 286, 9308-9320. (doi:10.1074/jbc. M110.143198)
7. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, Rea S, Jenuwein T, Dorn R, Reuter G. 2002 Central role of Drosophila SU (VAR) 3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J. 21, 1121-1131. (doi:10.1093/emboj/21.5. 1121)
8. Zhang K, Mosch K, Fischle W, Grewal SI. 2008 Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat. Struct. Mol. Biol. 15, 381-388. (doi:10.1038/nsmb.1406)
9. Nakayama J-I, Klar AJS, Grewal S I S. 2000 A chromodomain protein, Swi6, performs imprinting functions in fission yeast during mitosis and meiosis. Cell 101, 307-317. (doi:10.1016/S0092-8674 (00) 80840-5)
10. Eissenberg JC, Morris GD, Reuter G, Hartnett T. 1992 The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosagedependent effects on position-effect variegation. Genetics 131, 345-352.
11. Valenzuela L, Kamakaka RT. 2006 Chromatin insulators. Annu. Rev. Genet. 40, 107-138. (doi:10. 1146/annurev. genet.39.073003.113546)
12. Gaszner M, Felsenfeld G. 2006 Insulators: exploiting transcriptional and epigenetic mechanisms. Nat. Rev. Genet. 7, 703-713. (doi:10.1038/nrg1925)
13. Dhillon N, Raab J, Guzzo J, Szyjka SJ, Gangadharan S, Aparicio OM, Andrews B, Kamakaka RT. 2009 DNA polymerase 1, acetylases and remodellers cooperate to form a specialized chromatin structure at a tRNA insulator. EMBO J. 28, 2583-2600. (doi:10.1038/emboj.2009.198)
14. Oki M, Valenzuela L, Chiba T, Ito T, Kamakaka RT. 2004 Barrier proteins remodel and modify chromatin to restrict silenced domains. Mol. Cell. Biol. 24, 1956-1967. (doi:10.1128/MCB.24.5.1956-1967.2004)
15. Ishii K, Arib G, Lin C, Van Houwe G, Laemmli UK. 2002 Chromatin boundaries in budding yeast: the nuclear pore connection. Cell 109, 551-562. (doi:10.1016/S0092-8674 (02) 00756-0)
16. Noma KI, Cam HP, Maraia RJ, Grewal S I S. 2006 A role for TFIIIC transcription factor complex in genome organization. Cell 125, 859-872. (doi:10. 1016/j.cell.2006.04.028)
17. Buscaino A, Lejeune E, Audergon P, Hamilton G, Pidoux A, Allshire RC. 2013 Distinct roles for Sir2 and RNAi in centromeric heterochromatin nucleation, spreading and maintenance. EMBO J. 32, 1250-1264. (doi:10.1038/emboj.2013.72)
18. Kanoh J, Sadaie M, Urano T, Ishikawa F. 2005 Telomere binding protein Taz1 establishes Swi6 heterochromatin independently of RNAi at telomeres. Curr. Biol. 15, 1808-1819. (doi:10.1016/j.cub.2005.09.041)
19. Jia S, Noma K, Grewal SI. 2004 RNAi-independent heterochromatin nucleation by the stress-activated ATF/CREB family proteins. Science 304, 1971-1976. (doi:10.1126/science.1099035)
20. Kim HS, Choi ES, Shin JA, Jang YK, Park SD. 2004 Regulation of Swi6/HP1-dependent heterochromatin assembly by cooperation of components of the mitogen-activated protein kinase pathway and a histone deacetylase Clr6. J. Biol. Chem. 279, 42 850-42 859. (doi:10.1074/jbc. M407259200)
21. Hansen KR, Ibarra PT, Thon G. 2006 Evolutionaryconserved telomere-linked helicase genes of fission yeast are repressed by silencing factors, RNAi components and the telomere-binding protein Taz1. Nucleic Acids Res. 34, 78-88. (doi:10.1093/nar/gkj415)
22. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D. 2004 RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303, 672-676. (doi:10.1126/science. 1093686)
23. Grewal S I S. 2010 RNAi-dependent formation of heterochromatin and its diverse functions. Curr. Opin. Genet. Dev. 20, 134-141. (doi:10.1016/j.gde. 2010.02.003)
24. Castel SE, Martienssen RA. 2013 RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 14, 100-112. (doi:10.1038/nrg3355)
25. Bayne EH et al. 2010 Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140, 666-677. (doi:10.1016/j.cell.2010.01.038)
26. Al-Sady B, Madhani HD, Narlikar GJ. 2013 Division of labor between the chromodomains of HP1 and Suv39 methylase enables coordination of heterochromatin spread. Mol. Cell 51, 80-91. (doi:10.1016/j.molcel.2013.06.013)
27. Yamada T, Fischle W, Sugiyama T, Allis CD, Grewal S I S. 2005 The nucleation and maintenance of heterochromatin by a histone deacetylase in fission yeast. Mol. Cell 20, 173-185. (doi:10.1016/j.molcel. 2005.10.002)
28. Shankaranarayana GD, Motamedi MR, Moazed D, Grewal SI. 2003 Sir2 regulates histone H3 lysine 9 methylation and heterochromatin assembly in fission yeast. Curr. Biol. 13, 1240-1246. (doi:10. 1016/S0960-9822 (03) 00489-5)
29. Noma K, Allis CD, Grewal S I S. 2001 Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293, 1150-1155. (doi:10.1126/science.1064150)
30. Thon G, Bjerling P, Bunner CM, Verhein-Hansen J. 2002 Expression-state boundaries in the mating-type region of fission yeast. Genetics 161, 611-622.
31. Cam HP, Sugiyama T, Chen ES, Chen X, Fitz Gerald PC, Grewal S I S. 2005 Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat. Genet. 37, 809-819. (doi:10.1038/ng1602)
32. Scott KC, Merrett SL, Willard HF. 2006 A heterochromatin barrier partitions the fission yeast centromere into discrete chromatin domains. Curr. Biol. 16, 119-129. (doi:10.1016/j.cub.2005.11.065)
33. Scott KC, White CV, Willard HF. 2007 An RNA polymerase III-dependent heterochromatin barrier at fission yeast Centromere 1. PLoS ONE 2, e1099. (doi:10.1371/journal.pone.0001099)
34. Lan F et al. 2007 S. pombe LSD1 homologs regulate heterochromatin propagation and euchromatic gene transcription. Mol. Cell 26, 89-101. (doi:10.1016/j. molcel.2007.02.023)
35. Braun S, Garcia JF, Rowley M, Rougemaille M, Shankar S, Madhani HD. 2011 The Cul4-Ddb1Cdt2 ubiquitin ligase inhibits invasion of a boundaryassociated antisilencing factor into heterochromatin. Cell 144, 41-54. (doi:10.1016/j.cell.2010.11.051)
36. Buchanan L et al. 2009 The Schizosaccharomyces pombe JmjC-protein, Msc1, prevents H2A. Z localization in centromeric and subtelomeric chromatin domains. PLoS Genet. 5, e1000726. (doi:10.1371/journal.pgen. 1000726)
37. Stralfors A, Walfridsson J, Bhuiyan H, Ekwall K. 2011 The FUN30 chromatin remodeler, Fft3, protects centromeric and subtelomeric domains from euchromatin formation. PLoS Genet. 7, e1001334. (doi:10.1371/journal.pgen. 1001334)
38. Trewick SC, Minc E, Antonelli R, Urano T, Allshire RC. 2007 The JmjC domain protein Epe1 prevents unregulated assembly and disassembly of heterochromatin. EMBO J. 26, 4670-4682. (doi:10. 1038/sj.emboj.7601892)
39. Ayoub N, Noma K, Isaac S, Kahan T, Grewal SIS, Cohen A. 2003 A novel JmjC domain protein modulates heterochromatization in fission yeast. Mol. Cell. Biol. 23, 4356-4370. (doi:10.1128/MCB. 23.12.4356-4370.2003)
40. Zofall M, Grewal S I S. 2006 Swi6/HP1 recruits a JmjC domain protein to facilitate transcription of heterochromatic repeats. Mol. Cell 22, 681-692. (doi:10.1016/j.molcel.2006.05.010)
41. Tsukada Y-I, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y. 2006 Histone demethylation by a family of JmjC domaincontaining proteins. Nature 439, 811-816. (doi:10. 1038/nature04433)
42. Trewick SC, McLaughlin PJ, Allshire RC. 2005 Methylation: lost in hydroxylation? EMBO Rep. 6, 315-320. (doi:10.1038/sj.embor.7400379)
43. Wang J, Tadeo X, Hou H, Tu PG, Thompson J, Yates III JR, Jia S. 2013 Epe1 recruits BET family bromodomain protein Bdf2 to establish heterochromatin boundaries. Genes Dev. 27, 1886-1902. (doi:10.1101/gad.221010.113)
44. Allshire RC, Nimmo ER, Ekwall K, Javerzat JP, Cranston G. 1995 Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. Genes Dev. 9, 218-233. (doi:10.1101/gad.9.2.218)
45. Kim D-U et al. 2010 Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat. Biotech. 28, 617-623. (doi:10.1038/nbt.1628)
46. Tomson BN, Arndt KM. 2013 The many roles of the conserved eukaryotic Paf1 complex in regulating transcription, histone modifications, and disease states. Biochim. Biophys. Acta 1829, 116-126. (doi:10.1016/j.bbagrm.2012.08. 011)
47. Mbogning J, Nagy S, Pagé V, Schwer B, Shuman S, Fisher RP, Tanny JC. 2013 The PAF complex and Prf1/Rtf1 delineate distinct Cdk9-dependent pathways regulating transcription elongation in fission yeast. PLoS Genet. 9, e1004029. (doi:10. 1371/journal.pgen. 1004029)
48. Jaehning JA. 2010 The Paf1 complex: platform or player in RNA polymerase II transcription? Biochim. Biophys. Acta 1799, 379-388. (doi:10.1016/j. bbagrm.2010.01.001)
49. Chu Y, Simic R, Warner MH, Arndt KM, Prelich G. 2007 Regulation of histone modification and cryptic transcription by the Bur1 and Paf1 complexes. EMBO J. 26, 4646-4656. (doi:10.1038/sj.emboj. 7601887)
50. Krogan NJ et al. 2003 Methylation of histone H3 by Set2 in Saccharomyces cerevisiae is linked to transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 23, 4207-4218. (doi:10.1128/MCB. 23.12.4207-4218.2003)
51. Krogan NJ et al. 2003 The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol. Cell 11, 721-729. (doi:10.1016/S1097-2765 (03) 00091-1)
52. Ng HH, Robert F, Young RA, Struhl K. 2003 Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11, 709-719. (doi:10.1016/S1097-2765 (03) 00092-3)
53. Wood A, Schneider J, Dover J, Johnston M, Shilatifard A. 2003 The Paf1 complex is essential for histone monoubiquitination by the Rad6-Bre1 complex, which signals for histone methylation by COMPASS and Dot1p. J. Biol. Chem. 278, 34 739-34 742. (doi:10.1074/jbc. C300269200)
54. Ng HH, Dole S, Struhl K. 2003 The Rtf1 component of the Paf1 transcriptional elongation complex is required for ubiquitination of histone H2B. J. Biol. Chem. 278, 33 625-33 628. (doi:10.1074/jbc. C300270200)
55. Piro AS, Mayekar MK, Warner MH, Davis CP, Arndt KM. 2012 Small region of Rtf1 protein can substitute for complete Paf1 complex in facilitating global histone H2B ubiquitylation in yeast. Proc. Natl Acad. Sci. USA 109, 10 837-10 842. (doi:10. 1073/pnas.1116994109)
56. Banks CAS, Kong SE, Spahr H, Florens L, Martin-Brown S, Washburn MP, Conaway JW, Mushegian A, Conaway RC. 2007 Identification and characterization of a Schizosaccharomyces pombe RNA polymerase II elongation factor with similarity to the metazoan transcription factor ELL. J. Biol. Chem. 282, 5761-5769. (doi:10.1074/jbc. M610393200)
57. Williams LA, Kane CM. 1996 Isolation and characterization of the Schizosaccharomyces pombe gene encoding transcript elongation factor TFIIS. Yeast 12, 227-236. (doi:10.1002/(SICI) 1097-0061 (1996 0315) 12:3, 227::AID-YEA905.3.0. CO;2-9)
58. Roguev A, Schaft D, Shevchenko A, Aasland R, Shevchenko A, Stewart AF. 2003 High conservation of the Set1/Rad6 axis of histone 3 lysine 4 methylation in budding and fission yeasts. J. Biol. Chem. 278, 8487-8493. (doi:10.1074/jbc. M209562200)
59. Morris SA, Shibata Y, Noma K-I, Tsukamoto Y, Warren E, Temple B, Grewal SIS, Strahl BD. 2005 Histone H3 K36 methylation is associated with transcription elongation in Schizosaccharomyces pombe. Eukaryot. Cell 4, 1446-1454. (doi:10.1128/EC.4.8.1446-1454.2005)
60. Zofall M, Yamanaka S, Reyes-Turcu FE, Zhang K, Rubin C, Grewal S I S. 2012 RNA elimination machinery targeting meiotic mRNAs promotes facultative heterochromatin formation. Science 335, 96-100. (doi:10.1126/science.1211651)
61. Hiriart E et al. 2012 Mmi1 RNA surveillance machinery directs RNAi complex RITS to specific meiotic genes in fission yeast. EMBO J. 31, 2296-2308. (doi:10.1038/emboj.2012.105)
62. Partridge JF, Scott KSC, Bannister AJ, Kouzarides T, Allshire RC. 2002 cis-Acting DNA from fission yeast centromeres mediates histone H3 methylation and recruitment of silencing factors and cohesin to an ectopic site. Curr. Biol. 12, 1652-1660. (doi:10. 1016/S0960-9822 (02) 01177-6)
63. Betz JL, Chang M, Washburn TM, Porter SE, Mueller CL, Jaehning JA. 2002 Phenotypic analysis of Paf1/RNA polymerase II complex mutations reveals connections to cell cycle regulation, protein synthesis, and lipid and nucleic acid metabolism. Mol. Genet. Genomics 268, 272-285. (doi:10.1007/s00438-002-0752-8)
64. Penheiter KL, Washburn TM, Porter SE, Hoffman MG, Jaehning JA. 2005 A posttranscriptional role for the yeast Paf1-RNA polymerase II complex is revealed by identification of primary targets. Mol. Cell. 20, 213-223. (doi:10.1016/j.molcel.2005.08.023)
65. Mayekar MK, Gardner RG, Arndt KM. 2013 The recruitment of the Saccharomyces cerevisiae Paf1 complex to active genes requires a domain of Rtf1 that directly interacts with the Spt4-Spt5 complex. Mol. Cell. Biol. 33, 3259-3273. (doi:10.1128/MCB. 00270-13)
66. Qiu H, Hu C, Gaur NA, Hinnebusch AG. 2012 Pol II CTD kinases Bur1 and Kin28 promote Spt5 CTRindependent recruitment of Paf1 complex. EMBO J. 31, 3494-3505. (doi:10.1038/emboj.2012.188)
67. Wier AD, Mayekar MK, Héroux A, Arndt KM, Van Demark AP. 2013 Structural basis for Spt5-mediated recruitment of the Paf1 complex to chromatin. Proc. Natl Acad. Sci. USA 110, 17 290-17 295. (doi:10.1073/pnas.1314754110)
68. Dermody JL, Buratowski S. 2010 Leo1 subunit of the yeast Paf1 complex binds RNA and contributes to complex recruitment. J. Biol. Chem. 285, 33 671-33 679. (doi:10.1074/jbc. M110.140764)
69. Keller C, Kulasegaran-Shylini R, Shimada Y, Hotz HR, Buhler M. 2013 Noncoding RNAs prevent spreading of a repressive histone mark. Nat. Struct. Mol. Biol. 20, 994-1000. (doi:10.1038/nsmb.2619)
70. Pokholok DK, Hannett NM, Young RA. 2002 Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell. 9, 799-809. (doi:10.1016/S1097-2765 (02) 00502-6)
71. Kim M, Ahn SH, Krogan NJ, Greenblatt JF, Buratowski S. 2004 Transitions in RNA polymerase II elongation complexes at the 30 ends of genes. EMBO J. 23, 354-364. (doi:10.1038/sj.emboj.7600053)
72. Kowalik KM, Shimada Y, Flury V, Stadler MB, Batki J, Buhler M. 2015 The Paf1 complex represses small-RNA-mediated epigenetic gene silencing. Nature 520, 248-252. (doi:10.1038/nature14337).
73. Kimura A, Horikoshi M. 2004 Partition of distinct chromosomal regions: negotiable border and fixed border. Genes Cells 9, 499-508. (doi:10.1111/j. 1356-9597.2004.00740.x)
74. Suka N, Luo K, Grunstein M. 2002 Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat. Genet. 32, 378-383. (doi:10.1038/ng1017)
75. Kimura A, Umehara T, Horikoshi M. 2002 Chromosomal gradient of histone acetylation established by Sas2p and Sir2p functions as a shield against gene silencing. Nat. Genet. 32, 370-377. (doi:10.1038/ng993)
76. Bahler J, Wu JQ, Longtine MS, Shah NG, McKenzie A, Steever AB, Wach A, Philippsen P, Pringle JR. 1998 Heterologous modules for efficient and versatile PCRbased gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951. (doi:10.1002/(SICI) 1097-0061 (199807) 14:10, 943::AID-YEA292.3.0. CO;2-Y)
77. Roguev A, Wiren M, Weissman JS, Krogan NJ. 2007 High-throughput genetic interaction mapping in the fission yeast Schizosaccharomyces pombe. Nat. Methods 4, 861-866. (doi:10.1038/nmeth1098)
78. Nakagawachi T et al. 2003 Silencing effect of CpG island hypermethylation and histone modifications on O6-methylguanine-DNA methyltransferase (MGMT) gene expression in human cancer. Oncogene 22, 8835-8844.
79. Bolger AM, Lohse M, Usadel B. 2014 Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. (doi:10.1093/bioinformatics/btu170)
80. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011 Integrative genomics viewer. Nat. Biotech. 29, 24-26. (doi:10.1038/nbt.1754)
81. Ramírez F, Dündar F, Diehl S, Grüning BA, Manke T. 2014 deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187-W191. (doi:10.1093/nar/gku365)
82. Dixon SJ et al. 2008 Significant conservation of synthetic lethal genetic interaction networks between distantly related eukaryotes. Proc. Natl Acad. Sci. USA 105, 16 653-16 658. (doi:10.1073/pnas.0806261105)
83. Collins SR, Schuldiner M, Krogan NJ, Weissman JS. 2006 A strategy for extracting and analyzing largescale quantitative epistatic interaction data. Genome Biol. 7, R63. (doi:10.1186/gb-2006-7-7-r63)