The Mi-2 homolog Mit1 actively positions nucleosomes within heterochromatin to suppress transcription

Molecular and Cellular Biology

Volumn 34, Issue 11, 2014, Pages 2046-2061

  Creamer, Kevin M ^a,b   Job, Godwin ^a   Shanker, Sreenath ^a   Neale, Geoffrey A ^a   Lin, Yuan Chi ^c   Bartholomew, Blaine ^c,d   Partridgea, Janet F ^b  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; HISTONE; HISTONE DEACETYLASE; HISTONE H3; HISTONE METHYLTRANSFERASE; PROTEIN CLR3; PROTEIN MIT1; PROTEIN SET2; RNA POLYMERASE II; SNF2 HISTONE DEACETYLASE REPRESSOR COMPLEX; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA SEQUENCE; ENZYME ACTIVITY; EPISTASIS; GENE EXPRESSION; HETEROCHROMATIN; NONHUMAN; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; SEQUENCE ALIGNMENT; TRANSCRIPTION TERMINATION;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION REGULATION, FUNGAL; HETEROCHROMATIN; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MOLECULAR SEQUENCE DATA; NUCLEOSOMES; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA POLYMERASE II; RNA, SMALL INTERFERING; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84899869152     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01609-13     Document Type: Article

References (95)

1. Elgin SC, Grewal SI. 2003. Heterochromatin: silence is golden. Curr. Biol. 13:R895-R898. http://dx.doi.org/10.1016/j.cub.2003.11.006.
2. Nakayama J, Rice JC, Strahl BD, Allis CD, Grewal SI. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292:110-113. http://dx.doi.org/10.1126/science.1060118.
3. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593-599. http://dx.doi.org/10.1038/35020506.
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. http://dx.doi.org/10.1038/35065138.
5. Sadaie M, Kawaguchi R, Ohtani Y, Arisaka F, Tanaka K, Shirahige K, Nakayama J. 2008. Balance between distinct HP1 family proteins controls heterochromatin assembly in fission yeast. Mol. Cell. Biol. 28:6973-6988. http://dx.doi.org/10.1128/MCB.00791-08.
6. Motamedi MR, Hong EJ, Li X, Gerber S, Denison C, Gygi S, Moazed D. HP1 proteins form distinct complexes and mediate heterochromatic gene silencing by nonoverlapping mechanisms. Mol. Cell 32:778-790. http://dx.doi.org/10.1016/j.molcel.2008.10.026.
7. Yamane K, Mizuguchi T, Cui B, Zofall M, Noma K, Grewal SI. 2011. Asf1/HIRA facilitate global histone deacetylation and associate with HP1 to promote nucleosome occupancy at heterochromatic loci. Mol. Cell 41:56-66. http://dx.doi.org/10.1016/j.molcel.2010.12.009.
8. Fischer T, Cui B, Dhakshnamoorthy J, Zhou M, Rubin C, Zofall M, Veenstra TD, Grewal SI. 2009. Diverse roles of HP1 proteins in heterochromatin assembly and functions in fission yeast. Proc. Natl. Acad. Sci. U. S. A. 106:8998-9003. http://dx.doi.org/10.1073/pnas.0813063106.
9. Sugiyama T, Cam HP, Sugiyama R, Noma K, Zofall M, Kobayashi R, Grewal SI. 2007. SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128:491-504. http://dx.doi.org/10.1016/j.cell.2006.12.035.
10. Bjerling P, Silverstein RA, Thon G, Caudy A, Grewal S, Ekwall K. 2002. Functional divergence between histone deacetylases in fission yeast by distinct cellular localization and in vivo specificity. Mol. Cell. Biol. 22: 2170-2181. http://dx.doi.org/10.1128/MCB.22.7.2170-2181.2002.
11. Bjerling P, Ekwall K, Egel R, Thon G. 2004. A novel type of silencing factor, Clr2, is necessary for transcriptional silencing at various chromosomal locations in the fission yeast Schizosaccharomyces pombe. Nucleic Acids Res. 32:4421-4428. http://dx.doi.org/10.1093/nar/gkh780.
12. Thon G, Klar AJ. 1992. The clr1 locus regulates the expression of the cryptic mating-type loci of fission yeast. Genetics 131:287-296.
13. Thon G, Cohen A, Klar AJ. 1994. Three additional linkage groups that repress transcription and meiotic recombination in the mating-type region of Schizosaccharomyces pombe. Genetics 138:29-38.
14. Ekwall K, Ruusala T. 1994. Mutations in rik1, clr2, clr3 and clr4 genes asymmetrically derepress the silent mating-type loci in fission yeast. Genetics 136:53-64.
15. Fazzio TG, Rando OJ. 2012. NURDs are required for diversity. EMBO J. 31:3036-3037. http://dx.doi.org/10.1038/emboj.2012.137.
16. Sims JK, Wade PA. 2011. Mi-2/NuRD complex function is required for normal S phase progression and assembly of pericentric heterochromatin. Mol. Biol. Cell 22:3094-3102. http://dx.doi.org/10.1091/mbc. E11-03-0258.
17. Pegoraro G, Kubben N, Wickert U, Gohler H, Hoffmann K, Misteli T. Ageing-related chromatin defects through loss of the NURD complex. Nat. Cell Biol. 11:1261-1267. http://dx.doi.org/10.1038/ncb1971.
18. Denslow SA, Wade PA. 2007. The human Mi-2/NuRD complex and gene regulation. Oncogene 26:5433-5438. http://dx.doi.org/10.1038/sj.onc.1210611.
19. Lantermann AB, Straub T, Stralfors A, Yuan GC, Ekwall K, Korber P. Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae. Nat. Struct. Mol. Biol. 17:251-257. http://dx.doi.org/10.1038/nsmb.1741.
20. Garcia JF, Dumesic PA, Hartley PD, El-Samad H, Madhani HD. 2010. Combinatorial, site-specific requirement for heterochromatic silencing factors in the elimination of nucleosome-free regions. Genes Dev. 24: 1758-1771. http://dx.doi.org/10.1101/gad.1946410.
21. Carvalho S, Raposo AC, Martins FB, Grosso AR, Sridhara SC, Rino J, Carmo-Fonseca M, de Almeida SF. 2013. Histone methyltransferase SETD2 coordinates FACT recruitment with nucleosome dynamics during transcription. Nucleic Acids Res. 41:2881-2893. http://dx.doi.org/10.1093/nar/gks1472.
22. Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ, Anderson S, Yates J, Washburn MP, Workman JL. 2005. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581-592. http://dx.doi.org/10.1016/j.cell.2005.10.023.
23. Petrie VJ, Wuitschick JD, Givens CD, Kosinski AM, Partridge JF. 2005. RNA interference (RNAi)-dependent and RNAi-independent association of the Chp1 chromodomain protein with distinct heterochromatic loci in fission yeast. Mol. Cell. Biol. 25:2331-2346. http://dx.doi.org/10.1128/MCB.25.6.2331-2346.2005.
24. Forsburg SL. 1993. Comparison of Schizosaccharomyces pombe expression systems. Nucleic Acids Res. 21:2955-2956. http://dx.doi.org/10.1093/nar/21.12.2955.
25. Guan KL, Dixon JE. 1991. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192:262-267. http://dx.doi.org/10.1016/0003-2697(91)90534-Z.
26. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer EL, Eddy SR, Bateman A, Finn RD. 2012. The Pfam protein families database. Nucleic Acids Res. 40:D290-D301. http://dx.doi.org/10.1093/nar/gkr1065.
27. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371. http://dx.doi.org/10.1038/nprot.2009.2.
28. Leeds P, Peltz SW, Jacobson A, Culbertson MR. 1991. The product of the yeast UPF1 gene is required for rapid turnover of mRNAs containing a premature translational termination codon. Genes Dev. 5:2303-2314. http://dx.doi.org/10.1101/gad.5.12a.2303.
29. Hansen KR, Hazan I, Shanker S, Watt S, Verhein-Hansen J, Bahler J, Martienssen RA, Partridge JF, Cohen A, Thon G. 2011. H3K9meindependent gene silencing in fission yeast heterochromatin by Clr5 and histone deacetylases. PLoS Genet. 7:e1001268. http://dx.doi.org/10.1371/journal.pgen.1001268.
30. Chang PY, Hom RA, Musselman CA, Zhu L, Kuo A, Gozani O, Kutateladze TG, Cleary ML. 2010. Binding of the MLL PHD3 finger to histone H3K4me3 is required for MLL-dependent gene transcription. J. Mol. Biol. 400:137-144. http://dx.doi.org/10.1016/j.jmb.2010.05.005.
31. Partridge JF, Debeauchamp JL, Kosinski AM, Ulrich DL, Hadler MJ, Noffsinger VJ. 2007. Functional separation of the requirements for establishment and maintenance of centromeric heterochromatin. Mol. Cell 26:593-602. http://dx.doi.org/10.1016/j.molcel.2007.05.004.
32. Moreno S, Klar A, Nurse P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795-823. http://dx.doi.org/10.1016/0076-6879(91)94059-L.
33. Sengupta SM, VanKanegan M, Persinger J, Logie C, Cairns BR, Peterson CL, Bartholomew B. 2001. The interactions of yeast SWI/SNF and RSC with the nucleosome before and after chromatin remodeling. J. Biol. Chem. 276:12636-12644.
34. Shen X, Xiao H, Ranallo R, Wu WH, Wu C. 2003. Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science 299:112-114. http://dx.doi.org/10.1126/science.1078068.
35. Lantermann A, Stralfors A, Fagerstrom-Billai F, Korber P, Ekwall K. Genome-wide mapping of nucleosome positions in Schizosaccharomyces pombe. Methods 48:218-225. http://dx.doi.org/10.1016/j.ymeth.2009.02.004.
36. Lai AY, Wade PA. 2011. Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat. Rev. Cancer 11:588-596. http://dx.doi.org/10.1038/nrc3091.
37. Hu G, Wade PA. 2012. NuRD and pluripotency: a complex balancing act. Cell Stem Cell 10:497-503. http://dx.doi.org/10.1016/j.stem.2012.04.011.
38. Pointner J, Persson J, Prasad P, Norman-Axelsson U, Stralfors A, Khorosjutina O, Krietenstein N, Svensson JP, Ekwall K, Korber P. 2012. CHD1 remodelers regulate nucleosome spacing in vitro and align nucleosomal arrays over gene coding regions in S. pombe. EMBO J. 31:4388-4403. http://dx.doi.org/10.1038/emboj.2012.289.
39. 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. http://dx.doi.org/10.1016/j.molcel.2005.10.002.
40. Marina DB, Shankar S, Natarajan P, Finn KJ, Madhani HD. 2013. A conserved ncRNA-binding protein recruits silencing factors to heterochromatin through an RNAi-independent mechanism. Genes Dev. 27: 1851-1856. http://dx.doi.org/10.1101/gad.226019.113.
41. Buhler M, Haas W, Gygi SP, Moazed D. 2007. RNAi-dependent and-independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell 129:707-721. http://dx.doi.org/10.1016/j.cell.2007.03.038.
42. Schalch T, Job G, Shanker S, Partridge JF, Joshua-Tor L. 2011. The Chp1-Tas3 core is a multifunctional platform critical for gene silencing by RITS. Nat. Struct. Mol. Biol. 18:1351-1357. http://dx.doi.org/10.1038/nsmb.2151.
43. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SI, Martienssen RA. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833-1837. http://dx.doi.org/10.1126/science.1074973.
44. Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S, Grewal SI, Moazed D. RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672-676. http://dx.doi.org/10.1126/science.1093686.
45. Mueller-Planitz F, Klinker H, Ludwigsen J, Becker PB. 2013. The ATPase domain of ISWI is an autonomous nucleosome remodeling machine. Nat. Struct. Mol. Biol. 20:82-89.
46. Okuda M, Horikoshi M, Nishimura Y. 2007. Structural polymorphism of chromodomains in Chd1. J. Mol. Biol. 365:1047-1062. http://dx.doi.org/10.1016/j.jmb.2006.10.039.
47. Bienz M. 2006. The PHD finger, a nuclear protein-interaction domain. Trends Biochem. Sci. 31:35-40. http://dx.doi.org/10.1016/j.tibs.2005.11.001.
48. Eissenberg JC. 2012. Structural biology of the chromodomain: form and function. Gene 496:69-78. http://dx.doi.org/10.1016/j.gene.2012.01.003.
49. Marfella CG, Imbalzano AN. 2007. The Chd family of chromatin remodelers. Mutat. Res. 618:30-40. http://dx.doi.org/10.1016/j.mrfmmm.2006.07.012.
50. Hall JA, Georgel PT. 2007. CHD proteins: a diverse family with strong ties. Biochem. Cell Biol. 85:463-476. http://dx.doi.org/10.1139/O07-063.
51. Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR, Lacoste N, Cayrou C, Davrazou F, Saha A, Cairns BR, Ayer DE, Kutateladze TG, Shi Y, Cote J, Chua KF, Gozani O. 2006. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442:96-99. http://dx.doi.org/10.1038/nature04835.
52. Mansfield RE, Musselman CA, Kwan AH, Oliver SS, Garske AL, Davrazou F, Denu JM, Kutateladze TG, Mackay JP. 2011. Plant homeodomain (PHD) fingers of CHD4 are histone H3-binding modules with preference for unmodified H3K4 and methylated H3K9. J. Biol. Chem. 286:11779-11791. http://dx.doi.org/10.1074/jbc. M110.208207.
53. Musselman CA, Mansfield RE, Garske AL, Davrazou F, Kwan AH, Oliver SS, O'Leary H, Denu JM, Mackay JP, Kutateladze TG. 2009. Binding of theCHD4PHD2 finger to histone H3 is modulated by covalent modifications. Biochem. J. 423:179-187. http://dx.doi.org/10.1042/BJ20090870.
54. Musselman CA, Ramirez J, Sims JK, Mansfield RE, Oliver SS, Denu JM, Mackay JP, Wade PA, Hagman J, Kutateladze TG. 2012. Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression. Proc. Natl. Acad. Sci. U. S. A. 109:787-792. http://dx.doi.org/10.1073/pnas.1113655109.
55. Hota SK, Bartholomew B. 2011. Diversity of operation in ATPdependent chromatin remodelers. Biochim. Biophys. Acta 1809:476-487. http://dx.doi.org/10.1016/j.bbagrm.2011.05.007.
56. Meersseman G, Pennings S, Bradbury EM. 1992. Mobile nucleosomes- a general behavior. EMBO J. 11:2951-2959.
57. Lowary PT, Widom J. 1998. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276:19-42. http://dx.doi.org/10.1006/jmbi.1997.1494.
58. Tsukiyama T, Palmer J, Landel CC, Shiloach J, Wu C. 1999. Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev. 13:686-697. http://dx.doi.org/10.1101/gad.13.6.686.
59. Peterson CL. 2000. ATP-dependent chromatin remodeling: going mobile. FEBS Lett. 476:68-72. http://dx.doi.org/10.1016/S0014-5793(00)01673-2.
60. Gangaraju VK, Bartholomew B. 2007. Dependency of ISW1a chromatin remodeling on extranucleosomal DNA. Mol. Cell. Biol. 27:3217-3225. http://dx.doi.org/10.1128/MCB.01731-06.
61. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, LeProust EM, Hughes TR, Lieb JD, Widom J, Segal E. 2009. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458:362-366. http://dx.doi.org/10.1038/nature07667.
62. Xi L, Fondufe-Mittendorf Y, Xia L, Flatow J, Widom J, Wang JP. 2010. Predicting nucleosome positioning using a duration Hidden Markov Model. BMC Bioinformatics 11:346. http://dx.doi.org/10.1186/1471-2105-11-346.
63. Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309:626-630. http://dx.doi.org/10.1126/science.1112178.
64. 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. http://dx.doi.org/10.1073/pnas.182436399.
65. Chen ES, Zhang K, Nicolas E, Cam HP, Zofall M, Grewal SI. 2008. Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451:734-737. http://dx.doi.org/10.1038/nature06561.
66. Morris SA, Shibata Y, Noma K, Tsukamoto Y, Warren E, Temple B, Grewal SI, Strahl BD. 2005. Histone H3 K36 methylation is associated with transcription elongation in Schizosaccharomyces pombe. Eukaryot. Cell 4:1446-1454. http://dx.doi.org/10.1128/EC.4.8.1446-1454.2005.
67. Ekwall K, Nimmo ER, Javerzat JP, Borgstrom B, Egel R, Cranston G, Allshire R. 1996. Mutations in the fission yeast silencing factors clr4+and rik1+ disrupt the localisation of the chromo domain protein Swi6p and impair centromere function. J. Cell Sci. 109(Part 11):2637-2648.
68. Kuryan BG, Kim J, Tran NN, Lombardo SR, Venkatesh S, Workman JL, Carey M. 2012. Histone density is maintained during transcription mediated by the chromatin remodeler RSC and histone chaperone NAP1 in vitro. Proc. Natl. Acad. Sci. U. S. A. 109:1931-1936. http://dx.doi.org/10.1073/pnas.1109994109.
69. Lorch Y, Griesenbeck J, Boeger H, Maier-Davis B, Kornberg RD. 2011. Selective removal of promoter nucleosomes by the RSC chromatinremodeling complex. Nat. Struct. Mol. Biol. 18:881-885. http://dx.doi.org/10.1038/nsmb.2072.
70. Wang Y, Kallgren SP, Reddy BD, Kuntz K, Lopez-Maury L, Thompson J, Watt S, Ma C, Hou H, Shi Y, Yates JR, III, Bahler J, O'Connell MJ, Jia S. 2012. Histone H3 lysine 14 acetylation is required for activation of a DNA damage checkpoint in fission yeast. J. Biol. Chem. 287:4386-4393. http://dx.doi.org/10.1074/jbc. M111.329417.
71. Reddy BD, Wang Y, Niu L, Higuchi EC, Marguerat SB, Bahler J, Smith GR, Jia S. 2011. Elimination of a specific histone H3K14 acetyltransferase complex bypasses the RNAi pathway to regulate pericentric heterochromatin functions. Genes Dev. 25:214-219. http://dx.doi.org/10.1101/gad.1993611.
72. Bouazoune K, Mitterweger A, Langst G, Imhof A, Akhtar A, Becker PB, Brehm A. 2002. The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization. EMBO J. 21: 2430-2440. http://dx.doi.org/10.1093/emboj/21.10.2430.
73. Brehm A, Langst G, Kehle J, Clapier CR, Imhof A, Eberharter A, Muller J, Becker PB. 2000. dMi-2 and ISWI chromatin remodelling factors have distinct nucleosome binding and mobilization properties. EMBO J. 19: 4332-4341. http://dx.doi.org/10.1093/emboj/19.16.4332.
74. Watson AA, Mahajan P, Mertens HD, Deery MJ, Zhang W, Pham P, Du X, Bartke T, Zhang W, Edlich C, Berridge G, Chen Y, Burgess-Brown NA, Kouzarides T, Wiechens N, Owen-Hughes T, Svergun DI, Gileadi O, Laue ED. 2012. The PHD and chromo domains regulate the ATPase activity of the human chromatin remodeler CHD4. J. Mol. Biol. 422:3-17. http://dx.doi.org/10.1016/j.jmb.2012.04.031.
75. Wang HB, Zhang Y. 2001. Mi2, an auto-antigen for dermatomyositis, is an ATP-dependent nucleosome remodeling factor. Nucleic Acids Res. 29: 2517-2521. http://dx.doi.org/10.1093/nar/29.12.2517.
76. Shim YS, Choi Y, Kang K, Cho K, Oh S, Lee J, Grewal SI, Lee D. 2012. Hrp3 controls nucleosome positioning to suppress non-coding transcription in eu-and heterochromatin. EMBO J. 31:4375-4387. http://dx.doi.org/10.1038/emboj.2012.267.
77. Whitehouse I, Tsukiyama T. 2006. Antagonistic forces that position nucleosomes in vivo. Nat. Struct. Mol. Biol. 13:633-640. http://dx.doi.org/10.1038/nsmb1111.
78. Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, Qi J, Schuster SC, Albert I, Pugh BF. 2008. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res. 18:1073-1083. http://dx.doi.org/10.1101/gr.078261.108.
79. Joshi AA, Struhl K. 2005. Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol. Cell 20:971-978. http://dx.doi.org/10.1016/j.molcel.2005.11.021.
80. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, Boone C, Emili A, Weissman JS, Hughes TR, Strahl BD, Grunstein M, Greenblatt JF, Buratowski S, Krogan NJ. 2005. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123:593-605. http://dx.doi.org/10.1016/j.cell.2005.10.025.
81. Strahl BD, Grant PA, Briggs SD, Sun ZW, Bone JR, Caldwell JA, Mollah S, Cook RG, Shabanowitz J, Hunt DF, Allis CD. 2002. Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol. Cell. Biol. 22:1298-1306. http://dx.doi.org/10.1128/MCB.22.5.1298-1306.2002.
82. Smolle M, Venkatesh S, Gogol MM, Li H, Zhang Y, Florens L, Washburn MP, Workman JL. 2012. Chromatin remodelers Isw1 and Chd1 maintain chromatin structure during transcription by preventing histone exchange. Nat. Struct. Mol. Biol. 19:884-892. http://dx.doi.org/10.1038/nsmb.2312.
83. Venkatesh S, Smolle M, Li H, Gogol MM, Saint M, Kumar S, Natarajan K, Workman JL. 2012. Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489:452-455. http://dx.doi.org/10.1038/nature11326.
84. Hennig BP, Bendrin K, Zhou Y, Fischer T. 2012. Chd1 chromatin remodelers maintain nucleosome organization and repress cryptic transcription. EMBO Rep. 13:997-1003. http://dx.doi.org/10.1038/embor.2012.146.
85. Kiely CM, Marguerat S, Garcia JF, Madhani HD, Bahler J, Winston F. Spt6 is required for heterochromatic silencing in the fission yeast Schizosaccharomyces pombe. Mol. Cell. Biol. 31:4193-4204. http://dx.doi.org/10.1128/MCB.05568-11.
86. Alper BJ, Job G, Yadav RK, Shanker S, Lowe BR, Partridge JF. 2013. Sir2 is required for Clr4 to initiate centromeric heterochromatin assembly in fission yeast. EMBO J. 32:2321-2335. http://dx.doi.org/10.1038/emboj.2013.143.
87. Kato H, Okazaki K, Iida T, Nakayama J, Murakami Y, Urano T. 2013. Spt6 prevents transcription-coupled loss of posttranslationally modified histone H3. Sci. Rep. 3:2186. http://dx.doi.org/10.1038/srep02186.
88. Aygun O, Mehta S, Grewal SI. 2013. HDAC-mediated suppression of histone turnover promotes epigenetic stability of heterochromatin. Nat. Struct. Mol. Biol. 20:547-554. http://dx.doi.org/10.1038/nsmb.2565.
89. van Vugt JJ, de Jager M, Murawska M, Brehm A, van Noort J, Logie C. Multiple aspects of ATP-dependent nucleosome translocation by RSC and Mi-2 are directed by the underlying DNA sequence. PLoS One 4:e6345. http://dx.doi.org/10.1371/journal.pone.0006345.
90. Lorch Y, Maier-Davis B, Kornberg RD. 2006. Chromatin remodeling by nucleosome disassembly in vitro. Proc. Natl. Acad. Sci. U. S. A. 103:3090-3093. http://dx.doi.org/10.1073/pnas.0511050103.
91. Whitehouse I, Rando OJ, Delrow J, Tsukiyama T. 2007. Chromatin remodelling at promoters suppresses antisense transcription. Nature 450: 1031-1035. http://dx.doi.org/10.1038/nature06391.
92. Hartley PD, Madhani HD. 2009. Mechanisms that specify promoter nucleosome location and identity. Cell 137:445-458. http://dx.doi.org/10.1016/j.cell.2009.02.043.
93. Guschin D, Wade PA, Kikyo N, Wolffe AP. 2000. ATP-dependent histone octamer mobilization and histone deacetylation mediated by the Mi-2 chromatin remodeling complex. Biochemistry 39:5238-5245. http://dx.doi.org/10.1021/bi000421t.
94. Helbling Chadwick L, Chadwick BP, Jaye DL, Wade PA. 2009. The Mi-2/NuRD complex associates with pericentromeric heterochromatin during S phase in rapidly proliferating lymphoid cells. Chromosoma 118: 445-457. http://dx.doi.org/10.1007/s00412-009-0207-7.
95. Hayden KE. 2012. Human centromere genomics: now it's personal. Chromosome Res. 20:621-633. http://dx.doi.org/10.1007/s10577-012-9295-y.