Identification of lysine 37 of histone H2B as a novel site of methylation

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Gardner, Kathryn E ^a   Zhou, Li ^a   Parra, Michael A ^a   Chen, Xian ^a   Strahl, Brian D ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2B; LYSINE; HISTONE;

ANTIBODY SPECIFICITY; ARTICLE; CHROMATIN; EUKARYOTE; GENE MUTATION; GENETIC CONSERVATION; HISTONE METHYLATION; IN VIVO STUDY; MASS SPECTROMETRY; NONHUMAN; PROTEIN PROCESSING; SACCHAROMYCES CEREVISIAE; GENETICS; HISTONE CODE; METABOLISM; METHODOLOGY; METHYLATION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

HISTONE CODE; HISTONES; LYSINE; MASS SPECTROMETRY; METHYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SACCHAROMYCES CEREVISIAE;

EID: 79251551440     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016244     Document Type: Article

References (107)

1. Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98: 285-294.
2. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
3. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693-705.
4. Campos EI, Reinberg D (2009) Histones: annotating chromatin. Annu Rev Genet 43: 559-599.
5. Freitas MA, Sklenar AR, Parthun MR (2004) Application of mass spectrometry to the identification and quantification of histone post-translational modifications. J Cell Biochem 92: 691-700.
6. Mersfelder EL, Parthun MR (2006) The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Nucleic Acids Res 34: 2653-2662.
7. Chen Y, Sprung R, Tang Y, Ball H, Sangras B, et al. (2007) Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol Cell Proteomics 6: 812-819.
8. Sakabe K, Wang Z, Hart GW (2010) Beta-N-acetylglucosamine (O-GlcNAc) is part of the histone code. Proc Natl Acad Sci U S A 107: 19915-19920.
9. Hong L, Schroth GP, Matthews HR, Yau P, Bradbury EM (1993) Studies of the DNA binding properties of histone H4 amino terminus. Thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 ''tail'' to DNA. J Biol Chem 268: 305-314.
10. Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, et al. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311: 844-847.
11. Wolffe AP, Hayes JJ (1999) Chromatin disruption and modification. Nucleic Acids Res 27: 711-720.
12. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ (2007) How chromatinbinding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 14: 1025-1040.
13. Collins RE, Northrop JP, Horton JR, Lee DY, Zhang X, et al. (2008) The ankyrin repeats of G9a and GLP histone methyltransferases are mono- and dimethyllysine binding modules. Nat Struct Mol Biol 15: 245-250.
14. Vezzoli A, Bonadies N, Allen MD, Freund SM, Santiveri CM, et al. (2010) Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat Struct Mol Biol 17: 617-619.
15. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293: 1074-1080.
16. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45.
17. Jacobson RH, Ladurner AG, King DS, Tjian R (2000) Structure and function of a human TAFII250 double bromodomain module. Science 288: 1422-1425.
18. Mizzen CA, Yang XJ, Kokubo T, Brownell JE, Bannister AJ, et al. (1996) The TAF(II)250 subunit of TFIID has histone acetyltransferase activity. Cell 87: 1261-1270.
19. Fischle W, Tseng BS, Dormann HL, Ueberheide BM, Garcia BA, et al. (2005) Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 438: 1116-1122.
20. Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, et al. (2006) A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442: 86-90.
21. Shi X, Hong T, Walter KL, Ewalt M, Michishita E, et al. (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442: 96-99.
22. Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, et al. (2006) Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HAT activity at K14 of H3 and transcription at a subset of targeted ORFs. Mol Cell 24:785-796.
23. Agalioti T, Chen G, Thanos D (2002) Deciphering the transcriptional histone acetylation code for a human gene. Cell 111: 381-392.
24. Zippo A, Serafini R, Rocchigiani M, Pennacchini S, Krepelova A, et al. (2009) Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138: 1122-1136.
25. Garcia BA, Shabanowitz J, Hunt DF (2007) Characterization of histones and their post-translational modifications by mass spectrometry. Curr Opin Chem Biol 11: 66-73.
26. Han J, Borchers CH (2010) Top-down analysis of recombinant histone H3 and its methylated analogs by ESI/FT-ICR mass spectrometry. Proteomics.
27. Borchers CH, Thapar R, Petrotchenko EV, Torres MP, Speir JP, et al. (2006) Combined top-down and bottom-up proteomics identifies a phosphorylation site in stem-loop-binding proteins that contributes to high-affinity RNA binding. Proc Natl Acad Sci U S A 103: 3094-3099.
28. Garcia BA, Mollah S, Ueberheide BM, Busby SA, Muratore TL, et al. (2007) Chemical derivatization of histones for facilitated analysis by mass spectrometry. Nat Protoc 2: 933-938.
29. Pesavento JJ, Bullock CR, LeDuc RD, Mizzen CA, Kelleher NL (2008) Combinatorial Modification of Human Histone H4 Quantitated by Twodimensional Liquid Chromatography Coupled with Top Down Mass Spectrometry. Journal of Biological Chemistry 283: 14927-14937.
30. Zhang K, Williams KE, Huang L, Yau P, Siino JS, et al. (2002) Histone acetylation and deacetylation: identification of acetylation and methylation sites of HeLa histone H4 by mass spectrometry. Mol Cell Proteomics 1: 500-508.
31. Boyne MT, Pesavento JJ, Mizzen CA, Kelleher NL (2006) Precise characterization of human histories in the H2A gene family by top down mass spectrometry. Journal of Proteome Research 5: 248-253.
32. Kelleher NL (2004) Top-down proteomics. Anal Chem 76: 197A-203A.
33. Siuti N, Roth MJ, Mizzen CA, Kelleher NL, Pesavento JJ (2006) Gene-specific characterization of human histone H2B by electron capture dissociation. Journal of Proteome Research 5: 233-239.
34. Taverna SD, Ueberheide BM, Liu YF, Tackett AJ, Diaz RL, et al. (2007) Long-distance combinatorial linkage between methylation and acetylation on histone H3N termini. Proceedings of the National Academy of Sciences of the United States of America 104: 2086-2091.
35. Thomas CE, Kelleher NL, Mizzen CA (2006) Mass spectrometric characterization of human histone H3: A bird's eye view. Journal of Proteome Research 5: 240-247.
36. Zubarev RA, Kelleher NL, McLafferty FW (1998) Electron capture dissociation of multiply charged protein cations. A nonergodic process. Journal of the American Chemical Society 120: 3265-3266.
37. Pesavento JJ, Kim YB, Taylor GK, Kelleher NL (2004) Shotgun annotation of histone modifications: a new approach for streamlined characterization of proteins by top down mass spectrometry. J Am Chem Soc 126: 3386-3387.
38. Ueberheide BM, Mollah S (2007) Deciphering the histone code using mass spectrometry. International Journal of Mass Spectrometry 259: 46-56.
39. Millar CB, Grunstein M (2006) Genome-wide patterns of histone modifications in yeast. Nat Rev Mol Cell Biol 7: 657-666.
40. Martin C, Zhang Y (2005) The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 6: 838-849.
41. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, et al. (2007) Highresolution profiling of histone methylations in the human genome. Cell 129: 823-837.
42. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, et al. (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897-903.
43. DeLange RJ, Fambrough DM, Smith EL, Bonner J (1969) Calf and Pea Histone IV. Journal of Biological Chemistry 244: 319-334.
44. Song O-k, Wang X, Waterborg JH, Sternglanz R (2003) An Nalpha-Acetyltransferase Responsible for Acetylation of the N-terminal Residues of Histones H4 and H2A. Journal of Biological Chemistry 278: 38109-38112.
45. Zhang K, Chen Y, Zhang Z, Zhao Y (2009) Identification and verification of lysine propionylation and butyrylation in yeast core histones using PTMap software. J Proteome Res 8: 900-906.
46. Parra MA, Kerr D, Fahy D, Pouchnik DJ, Wyrick JJ (2006) Deciphering the roles of the histone H2B N-terminal domain in genome-wide transcription. Mol Cell Biol 26: 3842-3852.
47. Nakanishi S, Lee JS, Gardner KE, Gardner JM, Takahashi YH, et al. (2009) Histone H2BK123 monoubiquitination is the critical determinant for H3K4 and H3K79 trimethylation by COMPASS and Dot1. J Cell Biol 186: 371-377.
48. Sun ZW, Allis CD (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418: 104-108.
49. Briggs SD, Xiao T, Sun ZW, Caldwell JA, Shabanowitz J, et al. (2002) Gene silencing: trans-histone regulatory pathway in chromatin. Nature 418: 498.
50. 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.
51. Ng HH, Xu RM, Zhang Y, Struhl K (2002) Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J Biol Chem 277: 34655-34657.
52. Dillon SC, Zhang X, Trievel RC, Cheng X (2005) The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 6: 227.
53. Petrossian T, Clarke S (2009) Bioinformatic Identification of Novel Methyltransferases. Epigenomics 1: 163-175.
54. 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.
55. 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.
56. Strahl BD, Grant PA, Briggs SD, Sun ZW, Bone JR, et al. (2002) Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol 22: 1298-1306.
57. Jenuwein T, Laible G, Dorn R, Reuter G (1998) SET domain proteins modulate chromatin domains in eu- and heterochromatin. Cell Mol Life Sci 54: 80-93.
58. Ng HH, Feng Q, Wang H, Erdjument-Bromage H, Tempst P, et al. (2002) Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev 16:1518-1527.
59. Sawada K, Yang Z, Horton JR, Collins RE, Zhang X, et al. (2004) Structure of the conserved core of the yeast Dot1p, a nucleosomal histone H3 lysine 79 methyltransferase. J Biol Chem 279: 43296-43306.
60. Polevoda B, Martzen MR, Das B, Phizicky EM, Sherman F (2000) Cytochrome c methyltransferase, Ctm1p, of yeast. J Biol Chem 275:20508-20513.
61. Porras-Yakushi TR, Whitelegge JP, Clarke S (2006) A novel SET domain methyltransferase in yeast: Rkm2-dependent trimethylation of ribosomal protein L12ab at lysine 10. J Biol Chem 281: 35835-35845.
62. Porras-Yakushi TR, Whitelegge JP, Miranda TB, Clarke S (2005) A novel SET domain methyltransferase modifies ribosomal protein Rpl23ab in yeast. J Biol Chem 280: 34590-34598.
63. Webb KJ, Laganowsky A, Whitelegge JP, Clarke SG (2008) Identification of two SET domain proteins required for methylation of lysine residues in yeast ribosomal protein Rpl42ab. J Biol Chem 283: 35561-35568.
64. Gary JD, Lin WJ, Yang MC, Herschman HR, Clarke S (1996) The predominant protein-arginine methyltransferase from Saccharomyces cerevisiae. J Biol Chem 271: 12585-12594.
65. Niewmierzycka A, Clarke S (1999) S-Adenosylmethionine-dependent methylation in Saccharomyces cerevisiae. Identification of a novel protein arginine methyltransferase. J Biol Chem 274: 814-824.
66. Lee JH, Cook JR, Pollack BP, Kinzy TG, Norris D, et al. (2000) Hsl7p, the yeast homologue of human JBP1, is a protein methyltransferase. Biochem Biophys Res Commun 274: 105-111.
67. Kalhor HR, Penjwini M, Clarke S (2005) A novel methyltransferase required for the formation of the hypermodified nucleoside wybutosine in eukaryotic tRNA. Biochem Biophys Res Commun 334: 433-440.
68. Polevoda B, Span L, Sherman F (2006) The yeast translation release factors Mrf1p and Sup45p (eRF1) are methylated, respectively, by the methyltransferases Mtq1p and Mtq2p. J Biol Chem 281: 2562-2571.
69. Petrossian TC, Clarke SG (2009) Multiple Motif Scanning to identify methyltransferases from the yeast proteome. Mol Cell Proteomics 8: 1516-1526.
70. Katz JE, Dlakic M, Clarke S (2003) Automated identification of putative methyltransferases from genomic open reading frames. Mol Cell Proteomics 2: 525-540.
71. Webb KJ, Lipson RS, Al-Hadid Q, Whitelegge JP, Clarke SG (2010) Identification of protein N-terminal methyltransferases in yeast and humans. Biochemistry 49: 5225-5235.
72. Xiao B, Jing C, Wilson JR, Walker PA, Vasisht N, et al. (2003) Structure and catalytic mechanism of the human histone methyltransferase SET7/9. Nature 421: 652-656.
73. Shilatifard A (2006) Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75: 243-269.
74. Klose RJ, Kallin EM, Zhang Y (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7: 715-727.
75. Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, et al. (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439: 811-816.
76. Klose RJ, Zhang Y (2007) Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8: 307-318.
77. Fang J, Hogan GJ, Liang G, Lieb JD, Zhang Y (2007) The Saccharomyces cerevisiae histone demethylase Jhd1 fine-tunes the distribution of H3K36me2. Mol Cell Biol 27: 5055-5065.
78. Kim T, Buratowski S (2007) Two Saccharomyces cerevisiae JmjC domain proteins demethylate histone H3 Lys36 in transcribed regions to promote elongation. J Biol Chem 282: 20827-20835.
79. Klose RJ, Gardner KE, Liang G, Erdjument-Bromage H, Tempst P, et al. (2007) Demethylation of histone H3K36 and H3K9 by Rph1: a vestige of an H3K9 methylation system in Saccharomyces cerevisiae? Mol Cell Biol 27:3951-3961.
80. Liang G, Klose RJ, Gardner KE, Zhang Y (2007) Yeast Jhd2p is a histone H3 Lys4 trimethyl demethylase. Nat Struct Mol Biol 14: 243-245.
81. Seward DJ, Cubberley G, Kim S, Schonewald M, Zhang L, et al. (2007) Demethylation of trimethylated histone H3 Lys4 in vivo by JARID1 JmjC proteins. Nat Struct Mol Biol 14: 240-242.
82. Baker SP, Phillips J, Anderson S, Qiu Q, Shabanowitz J, et al. (2010) Histone H3 Thr 45 phosphorylation is a replication-associated post-translational modification in S. cerevisiae. Nat Cell Biol 12: 294-298.
83. Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, et al. (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/ PP1 phosphatase in budding yeast and nematodes. Cell 102: 279-291.
84. Hogan E, Koshland D (1992) Addition of extra origins of replication to a minichromosome suppresses its mitotic loss in cdc6 and cdc14 mutants of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 89: 3098-3102.
85. 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.
86. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, et al. (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301: 1090-1093.
87. Biswas D, Dutta-Biswas R, Mitra D, Shibata Y, Strahl BD, et al. (2006) Opposing roles for Set2 and yFACT in regulating TBP binding at promoters. EMBO J 25: 4479-4489.
88. Mason PB, Struhl K (2003) The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol Cell Biol 23: 8323-8333.
89. Saunders A, Werner J, Andrulis ED, Nakayama T, Hirose S, et al. (2003) Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 301: 1094-1096.
90. Unnikrishnan A, Gafken PR, Tsukiyama T (2010) Dynamic changes in histone acetylation regulate origins of DNA replication. Nat Struct Mol Biol 17: 430-437.
91. Kyriss MN, Jin Y, Gallegos IJ, Sanford JA, Wyrick JJ (2010) Novel functional residues in the core domain of histone H2B regulate yeast gene expression and silencing and affect the response to DNA damage. Mol Cell Biol 30: 3503-3518.
92. Daujat S, Weiss T, Mohn F, Lange UC, Ziegler-Birling C, et al. (2009) H3K64 trimethylation marks heterochromatin and is dynamically remodeled during developmental reprogramming. Nat Struct Mol Biol 16: 777-781.
93. Cocklin RR, Wang M (2003) Identification of methylation and acetylation sites on mouse histone H3 using matrix-assisted laser desorption/ionization time-offlight and nanoelectrospray ionization tandem mass spectrometry. J Protein Chem 22: 327-334.
94. Gietz RD, Schiestl RH (2007) Quick and easy yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 35-37.
95. Boeke JD, Trueheart J, Natsoulis G, Fink GR (1987) 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol 154: 164-175.
96. Edmondson DG, Smith MM, Roth SY (1996) Repression domain of the yeast lobal repressor Tup1 interacts directly with histones H3 and H4. Genes Dev 10: 1247-1259.
97. Strahl BD, Ohba R, Cook RG, Allis CD (1999) Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proc Natl Acad Sci U S A 96: 14967-14972.
98. Waterborg JH (2000) Steady-state levels of histone acetylation in Saccharomyces cerevisiae. J Biol Chem 275: 13007-13011.
99. Collart MA, Oliviero S (2001) Preparation of yeast RNA. Curr Protoc Mol Biol;Chapter 13: Unit13 12.
100. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 319: 1097-1113.
101. Dai J, Hyland EM, Norris A, Boeke JD (2010) Yin and Yang of Histone H2B Roles in Silencing and Longevity: A Tale of Two Arginines. Genetics.
102. Fleming AB, Kao CF, Hillyer C, Pikaart M, Osley MA (2008) H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol Cell 31: 57-66.
103. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
104. Hirschhorn JN, Bortvin AL, Ricupero-Hovasse SL, Winston F (1995) A new class of histone H2A mutations in Saccharomyces cerevisiae causes specific transcriptional defects in vivo. Mol Cell Biol 15: 1999-2009.
105. Robzyk K, Recht J, Osley MA (2000) Rad6-dependent ubiquitination of histone H2B in yeast. Science 287: 501-504.
106. Schlichter A, Cairns BR (2005) Histone trimethylation by Set1 is coordinated by the RRM, autoinhibitory, and catalytic domains. EMBO J 24: 1222-1231.
107. Watson AD, Edmondson DG, Bone JR, Mukai Y, Yu Y, et al. (2000) Ssn6- Tup1 interacts with class I histone deacetylases required for repression. Genes Dev 14: 2737-2744.