Multifaceted Genome Control by Set1 Dependent and Independent of H3K4 Methylation and the Set1C/COMPASS Complex

PLoS Genetics

Volumn 10, Issue 10, 2014, Pages

  Mikheyeva, Irina V ^a   Grady, Patrick J R ^a   Tamburini, Fiona B ^a   Lorenz, David R ^a   Cam, Hugh P ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPASS PROTEIN; FUNGAL PROTEIN; HISTONE H3; LYSINE; LYSINE 4; METHYLTRANSFERASE; SET1C PROTEIN; UNCLASSIFIED DRUG; EUCHROMATIN; HISTONE; HISTONE DEMETHYLASE; HISTONE LYSINE METHYLTRANSFERASE; MULTIPROTEIN COMPLEX; SCHIZOSACCHAROMYCES POMBE PROTEIN; SET1 PROTEIN, S POMBE; TRANSCRIPTION FACTOR;

ACETYLATION; ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; EUCHROMATIN; FUNGAL GENOME; FUNGUS IDENTIFICATION; GENE; GENE CLUSTER; GENE CONTROL; GENE REPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; GENOME ANALYSIS; HETEROCHROMATIN; HISTONE METHYLATION; HISTONE UBIQUITINATION; HOUSEKEEPING GENE; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DOMAIN; RETROPOSON; RNA BINDING; SCHIZOSACCHAROMYCES POMBE; SIGNAL TRANSDUCTION; TF2 GENE; DNA METHYLATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; PROTEIN TERTIARY STRUCTURE; SCHIZOSACCHAROMYCES; UBIQUITINATION;

DNA METHYLATION; EUCHROMATIN; GENOME, FUNGAL; HISTONE DEMETHYLASES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; IN SITU HYBRIDIZATION, FLUORESCENCE; MULTIPROTEIN COMPLEXES; PROTEIN STRUCTURE, TERTIARY; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION FACTORS; UBIQUITINATION;

EID: 84908320093     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004740     Document Type: Article

References (72)

1. Campos EI, Reinberg D, (2009) Histones: annotating chromatin. Annu Rev Genet 43: 559–599.
2. Badeaux AI, Shi Y, (2013) Emerging roles for chromatin as a signal integration and storage platform. Nat Rev Mol Cell Biol 14: 211–224.
3. Kouzarides T, (2007) Chromatin modifications and their function. Cell 128: 693–705.
4. Noma K, Allis CD, Grewal SI, (2001) Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293: 1150–1155.
5. Litt MD, Simpson M, Gaszner M, Allis CD, Felsenfeld G, (2001) Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science 293: 2453–2455.
6. Kusch T, (2012) Histone H3 lysine 4 methylation revisited. Transcription 3: 310–314.
7. Shilatifard A, (2012) The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. Annu Rev Biochem 81: 65–95.
8. Morillon A, Karabetsou N, Nair A, Mellor J, (2005) Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol Cell 18: 723–734.
9. Schneider J, Wood A, Lee JS, Schuster R, Dueker J, et al. (2005) Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 19: 849–856.
10. Dehe PM, Dichtl B, Schaft D, Roguev A, Pamblanco M, et al. (2006) Protein interactions within the Set1 complex and their roles in the regulation of histone 3 lysine 4 methylation. J Biol Chem 281: 35404–35412.
11. Kim J, Kim JA, McGinty RK, Nguyen UT, Muir TW, et al. (2013) The n-SET domain of Set1 regulates H2B ubiquitylation-dependent H3K4 methylation. Mol Cell 49: 1121–1133.
12. Soares LM, Radman-Livaja M, Lin SG, Rando OJ, Buratowski S, (2014) Feedback control of Set1 protein levels is important for proper H3K4 methylation patterns. Cell Rep 6: 961–972.
13. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, et al. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517–527.
14. Cam HP, Sugiyama T, Chen ES, Chen X, FitzGerald PC, et al. (2005) Comprehensive analysis of heterochromatin- and RNAi-mediated epigenetic control of the fission yeast genome. Nat Genet 37: 809–819.
15. 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.
16. Krogan NJ, Dover J, Wood A, Schneider J, Heidt J, 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.
17. Berretta J, Pinskaya M, Morillon A, (2008) A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae. Genes Dev 22: 615–626.
18. Camblong J, Beyrouthy N, Guffanti E, Schlaepfer G, Steinmetz LM, et al. (2009) Trans-acting antisense RNAs mediate transcriptional gene cosuppression in S. cerevisiae. Genes Dev 23: 1534–1545.
19. van Dijk EL, Chen CL, d'Aubenton-Carafa Y, Gourvennec S, Kwapisz M, et al. (2011) XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475: 114–117.
20. Weiner A, Chen HV, Liu CL, Rahat A, Klien A, et al. (2012) Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol 10: e1001369.
21. Margaritis T, Oreal V, Brabers N, Maestroni L, Vitaliano-Prunier A, et al. (2012) Two Distinct Repressive Mechanisms for Histone 3 Lysine 4 Methylation through Promoting 3′-End Antisense Transcription. PLoS Genet 8: e1002952.
22. Noma K, Grewal SI, (2002) Histone H3 lysine 4 methylation is mediated by Set1 and promotes maintenance of active chromatin states in fission yeast. Proc Natl Acad Sci U S A 99 Suppl 4: 16438–16445.
23. Kanoh J, Francesconi S, Collura A, Schramke V, Ishikawa F, et al. (2003) The fission yeast spSet1p is a histone H3-K4 methyltransferase that functions in telomere maintenance and DNA repair in an ATM kinase Rad3-dependent pathway. J Mol Biol 326: 1081–1094.
24. Roguev A, Schaft D, Shevchenko A, Aasland R, 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.
25. Grewal SI, (2010) RNAi-dependent formation of heterochromatin and its diverse functions. Curr Opin Genet Dev 20: 134–141.
26. Yamanaka S, Mehta S, Reyes-Turcu FE, Zhuang F, Fuchs RT, et al. (2013) RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature 493: 557–560.
27. Lorenz DR, Mikheyeva IV, Johansen P, Meyer L, Berg A, et al. (2012) CENP-B Cooperates with Set1 in Bidirectional Transcriptional Silencing and Genome Organization of Retrotransposons. Mol Cell Biol 32: 4215–4225.
28. Schlichter A, Cairns BR, (2005) Histone trimethylation by Set1 is coordinated by the RRM, autoinhibitory, and catalytic domains. EMBO J 24: 1222–1231.
29. Tresaugues L, Dehe PM, Guerois R, Rodriguez-Gil A, Varlet I, et al. (2006) Structural characterization of Set1 RNA recognition motifs and their role in histone H3 lysine 4 methylation. J Mol Biol 359: 1170–1181.
30. Thornton JL, Westfield GH, Takahashi YH, Cook M, Gao X, et al. (2014) Context dependency of Set1/COMPASS-mediated histone H3 Lys4 trimethylation. Genes Dev 28: 115–120.
31. Takahashi YH, Lee JS, Swanson SK, Saraf A, Florens L, et al. (2009) Regulation of H3K4 trimethylation via Cps40 (Spp1) of COMPASS is monoubiquitination independent: implication for a Phe/Tyr switch by the catalytic domain of Set1. Mol Cell Biol 29: 3478–3486.
32. Krogan NJ, Dover J, Khorrami S, Greenblatt JF, Schneider J, et al. (2002) COMPASS, a histone H3 (Lysine 4) methyltransferase required for telomeric silencing of gene expression. J Biol Chem 277: 10753–10755.
33. Southall SM, Wong PS, Odho Z, Roe SM, Wilson JR, (2009) Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks. Mol Cell 33: 181–191.
34. Takahashi YH, Westfield GH, Oleskie AN, Trievel RC, Shilatifard A, et al. (2011) Structural analysis of the core COMPASS family of histone H3K4 methylases from yeast to human. Proc Natl Acad Sci U S A 108: 20526–20531.
35. Matsumoto S, Yanagida M, (1985) Histone gene organization of fission yeast: a common upstream sequence. EMBO J 4: 3531–3538.
36. Mellone BG, Ball L, Suka N, Grunstein MR, Partridge JF, et al. (2003) Centromere silencing and function in fission yeast is governed by the amino terminus of histone H3. Curr Biol 13: 1748–1757.
37. Xhemalce B, Kouzarides T, (2010) A chromodomain switch mediated by histone H3 Lys 4 acetylation regulates heterochromatin assembly. Genes Dev 24: 647–652.
38. Steward MM, Lee JS, O'Donovan A, Wyatt M, Bernstein BE, et al. (2006) Molecular regulation of H3K4 trimethylation by ASH2L, a shared subunit of MLL complexes. Nat Struct Mol Biol 13: 852–854.
39. Mueller JE, Canze M, Bryk M, (2006) The requirements for COMPASS and Paf1 in transcriptional silencing and methylation of histone H3 in Saccharomyces cerevisiae. Genetics 173: 557–567.
40. Latham JA, Chosed RJ, Wang S, Dent SY, (2011) Chromatin signaling to kinetochores: transregulation of Dam1 methylation by histone H2B ubiquitination. Cell 146: 709–719.
41. Mersman DP, Du HN, Fingerman IM, South PF, Briggs SD, (2012) Charge-based interaction conserved within histone H3 lysine 4 (H3K4) methyltransferase complexes is needed for protein stability, histone methylation, and gene expression. J Biol Chem 287: 2652–2665.
42. Nagy PL, Griesenbeck J, Kornberg RD, Cleary ML, (2002) A trithorax-group complex purified from Saccharomyces cerevisiae is required for methylation of histone H3. Proc Natl Acad Sci U S A 99: 90–94.
43. Dichtl B, Aasland R, Keller W, (2004) Functions for S. cerevisiae Swd2p in 3′ end formation of specific mRNAs and snoRNAs and global histone 3 lysine 4 methylation. RNA 10: 965–977.
44. Nedea E, Nalbant D, Xia D, Theoharis NT, Suter B, et al. (2008) The Glc7 phosphatase subunit of the cleavage and polyadenylation factor is essential for transcription termination on snoRNA genes. Mol Cell 29: 577–587.
45. Sun ZW, Allis CD, (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418: 104–108.
46. Briggs SD, Bryk M, Strahl BD, Cheung WL, Davie JK, et al. (2001) Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15: 3286–3295.
47. Dover J, Schneider J, Tawiah-Boateng MA, Wood A, Dean K, et al. (2002) Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J Biol Chem 277: 28368–28371.
48. Hwang WW, Venkatasubrahmanyam S, Ianculescu AG, Tong A, Boone C, et al. (2003) A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol Cell 11: 261–266.
49. Wood A, Krogan NJ, Dover J, Schneider J, Heidt J, et al. (2003) Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol Cell 11: 267–274.
50. Tanny JC, Erdjument-Bromage H, Tempst P, Allis CD, (2007) Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation. Genes Dev 21: 835–847.
51. Zofall M, Grewal SI, (2007) HULC, a histone H2B ubiquitinating complex, modulates heterochromatin independent of histone methylation in fission yeast. J Biol Chem 282: 14065–14072.
52. Cheng H, He X, Moore C, (2004) The essential WD repeat protein Swd2 has dual functions in RNA polymerase II transcription termination and lysine 4 methylation of histone H3. Mol Cell Biol 24: 2932–2943.
53. Roguev A, Schaft D, Shevchenko A, Pijnappel WW, Wilm M, et al. (2001) The Saccharomyces cerevisiae Set1 complex includes an Ash2 homologue and methylates histone 3 lysine 4. EMBO J 20: 7137–7148.
54. Soares LM, Buratowski S, (2012) Yeast Swd2 Is Essential Because of Antagonism between Set1 Histone Methyltransferase Complex and APT (Associated with Pta1) Termination Factor. J Biol Chem 287: 15219–15231.
55. Shevchenko A, Roguev A, Schaft D, Buchanan L, Habermann B, et al. (2008) Chromatin Central: towards the comparative proteome by accurate mapping of the yeast proteomic environment. Genome Biol 9: R167.
56. Nislow C, Ray E, Pillus L, (1997) SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol Biol Cell 8: 2421–2436.
57. Bryk M, Briggs SD, Strahl BD, Curcio MJ, Allis CD, et al. (2002) Evidence that Set1, a factor required for methylation of histone H3, regulates rDNA silencing in S. cerevisiae by a Sir2-independent mechanism. Curr Biol 12: 165–170.
58. Kim T, Buratowski S, (2009) Dimethylation of H3K4 by Set1 recruits the Set3 histone deacetylase complex to 5′ transcribed regions. Cell 137: 259–272.
59. Zhang K, Lin W, Latham JA, Riefler GM, Schumacher JM, et al. (2005) The Set1 methyltransferase opposes Ipl1 aurora kinase functions in chromosome segregation. Cell 122: 723–734.
60. Wood V, Harris MA, McDowall MD, Rutherford K, Vaughan BW, et al. (2012) PomBase: a comprehensive online resource for fission yeast. Nucleic Acids Res 40: D695–699.
61. Moazed D, (2011) Mechanisms for the inheritance of chromatin states. Cell 146: 510–518.
62. Reyes-Turcu FE, Grewal SI, (2012) Different means, same end-heterochromatin formation by RNAi and RNAi-independent RNA processing factors in fission yeast. Curr Opin Genet Dev 22: 156–163.
63. Yamada T, Fischle W, Sugiyama T, Allis CD, Grewal SI, (2005) The nucleation and maintenance of heterochromatin by a histone deacetylase in fission yeast. Mol Cell 20: 173–185.
64. 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.
65. Alper BJ, Job G, Yadav RK, Shanker S, Lowe BR, et al. (2013) Sir2 is required for Clr4 to initiate centromeric heterochromatin assembly in fission yeast. EMBO J 32: 2321–2335.
66. Guillemette B, Drogaris P, Lin HH, Armstrong H, Hiragami-Hamada K, et al. (2011) H3 lysine 4 is acetylated at active gene promoters and is regulated by H3 lysine 4 methylation. PLoS Genet 7: e1001354.
67. Tanaka A, Tanizawa H, Sriswasdi S, Iwasaki O, Chatterjee AG, et al. (2012) Epigenetic regulation of condensin-mediated genome organization during the cell cycle and upon DNA damage through histone H3 lysine 56 acetylation. Mol Cell 48: 532–546.
68. Cam HP, Noma K, Ebina H, Levin HL, Grewal SI, (2008) Host genome surveillance for retrotransposons by transposon-derived proteins. Nature 451: 431–436.
69. Bahler J, Wu JQ, Longtine MS, Shah NG, McKenzie A, 3rdet al. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14: 943–951.
70. Moreno S, Klar A, Nurse P, (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795–823.
71. Mudge DK, Hoffman CA, Lubinski TJ, Hoffman CS, (2012) Use of a ura5+-lys7+ cassette to construct unmarked gene knock-ins in Schizosaccharomyces pombe. Curr Genet 58: 59–64.
72. Lyne R, Burns G, Mata J, Penkett CJ, Rustici G, et al. (2003) Whole-genome microarrays of fission yeast: characteristics, accuracy, reproducibility, and processing of array data. BMC Genomics 4: 27.