Substrate and product specificities of SET domain methyltransferases

Epigenetics

Volumn 6, Issue 9, 2011, Pages 1059-1067

  del Rizzo, Paul A ^a   Trievel, Raymond C ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Crystal structure; Lysine methylation; Product specificity; S Adenosylmethionine; SET domain; Substrate specificity; Transcription

Indexed keywords

HISTONE LYSINE METHYLTRANSFERASE; MIXED LINEAGE LEUKEMIA PROTEIN;

ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; NONHUMAN; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REVIEW; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION;

EID: 80052591715     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.9.16069     Document Type: Review

References (81)

1. Luger K, Hansen JC. Nucleosome and chromatin fiber dynamics. Curr Opin Struct Biol 2005; 15:188-96.
2. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128:693-705.
3. Mosammaparast N, Shi Y. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 2010; 79:155-79.
4. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007; 447:407-12.
5. Taverna SD, Li H, Ruthenburg AJ, Allis CD, Patel DJ. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 2007; 14:1025-40.
6. Rea S, Eisenhaber F, O'Carroll D, Strahl BD, Sun ZW, Schmid M, et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000; 406:593-9.
7. Couture JF, Trievel RC. Histone-modifying enzymes: encrypting an enigmatic epigenetic code. Curr Opin Struct Biol 2006; 16:753-60.
8. Dillon SC, Zhang X, Trievel RC, Cheng X. The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 2005; 6:227.
9. Qian C, Zhou MM. SET domain protein lysine methyltransferases: Structure, specificity and catalysis. Cell Mol Life Sci 2006; 63:2755-63.
10. Cao R, Zhang Y. The functions of E(Z)/EZH2-mediated methylation of lysine 27 in histone H3. Curr Opin Genet Dev 2004; 14:155-64.
11. Mohan M, Lin C, Guest E, Shilatifard A. Licensed to elongate: a molecular mechanism for MLL-based leukaemogenesis. Nat Rev Cancer 2010; 10:721-8.
12. Huang J, Berger SL. The emerging field of dynamic lysine methylation of non-histone proteins. Curr Opin Genet Dev 2008; 18:152-8.
13. Chuikov S, Kurash JK, Wilson JR, Xiao B, Justin N, Ivanov GS, et al. Regulation of p53 activity through lysine methylation. Nature 2004; 432:353-60.
14. Shi X, Kachirskaia I, Yamaguchi H, West LE, Wen H, Wang EW, et al. Modulation of p53 function by SET8-mediated methylation at lysine 382. Mol Cell 2007; 27:636-46.
15. Huang J, Perez-Burgos L, Placek BJ, Sengupta R, Richter M, Dorsey JA, et al. Repression of p53 activity by Smyd2-mediated methylation. Nature 2006; 444:629-32.
16. Huang J, Dorsey J, Chuikov S, Zhang XY, Jenuwein T, Reinberg D, et al. G9a and Glp Methylate Lysine 373 in the Tumor Suppressor p53. J Biol Chem 2010; 285:9636-41.
17. Kouskouti A, Scheer E, Staub A, Tora L, Talianidis I. Gene-specific modulation of TAF10 function by SET9-mediated methylation. Mol Cell 2004; 14:175-82.
18. Pagans S, Kauder SE, Kaehlcke K, Sakane N, Schroeder S, Dormeyer W, et al. The Cellular lysine methyltransferase Set7/9-KMT7 binds HIV-1 TAR RNA, monomethylates the viral transactivator Tat, and enhances HIV transcription. Cell Host Microbe 2010; 7:234-44.
19. Van Duyne R, Easley R, Wu W, Berro R, Pedati C, Klase Z, et al. Lysine methylation of HIV-1 Tat regulates transcriptional activity of the viral LTR. Retrovirology 2008; 5:40.
20. Porras-Yakushi TR, Whitelegge JP, Clarke S. A novel SET domain methyltransferase in yeast: Rkm2-dependent trimethylation of ribosomal protein L12ab at lysine 10. J Biol Chem 2006; 281:35835-45.
21. Porras-Yakushi TR, Whitelegge JP, Clarke S. Yeast ribosomal/cytochrome c SET domain methyltransferase subfamily: identification of Rpl23ab methylation sites and recognition motifs. J Biol Chem 2007; 282:12368-76.
22. Porras-Yakushi TR, Whitelegge JP, Miranda TB, Clarke S. A novel SET domain methyltransferase modifies ribosomal protein Rpl23ab in yeast. J Biol Chem 2005; 280:34590-8.
23. Webb KJ, Laganowsky A, Whitelegge JP, Clarke SG. Identification of two SET domain proteins required for methylation of lysine residues in yeast ribosomal protein Rpl42ab. J Biol Chem 2008; 283:35561-8.
24. Esteve PO, Chang Y, Samaranayake M, Upadhyay AK, Horton JR, Feehery GR, et al. A methylation and phosphorylation switch between an adjacent lysine and serine determines human DNMT1 stability. Nat Struct Mol Biol 2011; 18:42-8.
25. Esteve PO, Chin HG, Benner J, Feehery GR, Samaranayake M, Horwitz GA, et al. Regulation of DNMT1 stability through SET7-mediated lysine methylation in mammalian cells. Proc Natl Acad Sci USA 2009; 106:5076-81.
26. Pradhan S, Chin HG, Esteve PO, Jacobsen SE. SET7/9 mediated methylation of non-histone proteins in mammalian cells. Epigenetics 2009; 4.
27. Wang J, Hevi S, Kurash JK, Lei H, Gay F, Bajko J, et al. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nature Genet 2009; 41:125-9.
28. Masatsugu T, Yamamoto K. Multiple lysine methylation of PCAF by Set9 methyltransferase. Biochem Biophys Res Commun 2009; 381:22-6.
29. Carr SM, Munro S, Kessler B, Oppermann U, La Thangue NB. Interplay between lysine methylation and Cdk phosphorylation in growth control by the retinoblastoma protein. EMBO J 2011; 30:317-27.
30. Nielsen SJ, Schneider R, Bauer UM, Bannister AJ, Morrison A, O'Carroll D, et al. Rb targets histone H3 methylation and HP1 to promoters. Nature 2001; 412:561-5.
31. Saddic LA, West LE, Aslanian A, Yates JR, Rubin SM, Gozani O, et al. Methylation of the retinoblastoma tumor suppressor by SMYD2. J Biol Chem 2010.
32. Kunizaki M, Hamamoto R, Silva FP, Yamaguchi K, Nagayasu T, Shibuya M, et al. The lysine 831 of vascular endothelial growth factor receptor 1 is a novel target of methylation by SMYD3. Cancer Res 2007; 67:10759-65.
33. Ea CK, Baltimore D. Regulation of NFkappaB activity through lysine monomethylation of p65. Proc Natl Acad Sci USA 2009; 106:18972-7.
34. Lu T, Jackson MW, Wang B, Yang M, Chance MR, Miyagi M, et al. Regulation of NFkappaB by NSD1/ FBXL11-dependent reversible lysine methylation of p65. Proc Natl Acad Sci USA 2010; 107:46-51.
35. Yang XD, Huang B, Li M, Lamb A, Kelleher NL, Chen LF. Negative regulation of NFkappaB action by Set9-mediated lysine methylation of the RelA subunit. EMBO J 2009; 28:1055-66.
36. Levy D, Kuo AJ, Chang Y, Schaefer U, Kitson C, Cheung P, et al. Lysine methylation of the NFkappaB subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NFkappaB signaling. Nat Immunol 2011; 12:29-36.
37. Subramanian K, Jia D, Kapoor-Vazirani P, Powell DR, Collins RE, Sharma D, et al. Regulation of estrogen receptor alpha by the SET7 lysine methyltransferase. Mol Cell 2008; 30:336-47.
38. Gaughan L, Stockley J, Wang N, McCracken SR, Treumann A, Armstrong K, et al. Regulation of the androgen receptor by SET9-mediated methylation. Nucleic Acids Res 2010.
39. Ko S, Ahn J, Song CS, Kim S, Knapczyk-Stwora K, Chatterjee B. Lysine methylation and functional modulation of androgen receptor by set9 methyltransferase. Mol Endocrinol 2011; 25:433-44.
40. Kontaki H, Talianidis I. Lysine methylation regulates E2F1-induced cell death. Mol Cell 2010; 39:152-60.
41. Yang J, Huang J, Dasgupta M, Sears N, Miyagi M, Wang B, et al. Reversible methylation of promoter-bound STAT3 by histone-modifying enzymes. Proc Natl Acad Sci USA 2010.
42. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell 2007; 128:707-19.
43. Shilatifard A. Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation. Curr Opin Cell Biol 2008; 20:341-8.
44. Vermeulen M, Mulder KW, Denissov S, Pijnappel WW, van Schaik FM, Varier RA, et al. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 2007; 131:58-69.
45. Eissenberg JC, Shilatifard A. Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol 2009.
46. Milne TA, Briggs SD, Brock HW, Martin ME, Gibbs D, Allis CD, et al. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell 2002; 10:1107-17.
47. Dou Y, Hess JL. Mechanisms of transcriptional regulation by MLL and its disruption in acute leukemia. Int J Hematol 2008; 87:10-8.
48. Liedtke M, Cleary ML. Therapeutic targeting of MLL. Blood 2009; 113:6061-8.
49. Southall SM, Wong PS, Odho Z, Roe SM, Wilson JR. Structural basis for the requirement of additional factors for MLL1 SET domain activity and recognition of epigenetic marks. Mol Cell 2009; 33:181-91.
50. Zhang X, Yang Z, Khan SI, Horton JR, Tamaru H, Selker EU, et al. Structural basis for the product specificity of histone lysine methyltransferases. Mol Cell 2003; 12:177-85.
51. Cosgrove MS, Patel A. Mixed lineage leukemia: a structure-function perspective of the MLL1 protein. Febs J 2010; 277:1832-42.
52. Patel A, Dharmarajan V, Vought VE, Cosgrove MS. On the Mechanism of Multiple Lysine Methylation by the Human Mixed Lineage Leukemia Protein-1 (MLL1) Core Complex. J Biol Chem 2009; 284:24242-56.
53. Patel A, Vought VE, Dharmarajan V, Cosgrove MS. A conserved arginine-containing motif crucial for the assembly and enzymatic activity of the mixed lineage leukemia protein-1 core complex. J Biol Chem 2008; 283:32162-75.
54. Song JJ, Kingston RE. WDR5 interacts with mixed lineage leukemia (MLL) protein via the histone H3-binding pocket. J Biol Chem 2008; 283:35258-64.
55. Dou Y, Milne TA, Ruthenburg AJ, Lee S, Lee JW, Verdine GL, et al. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat Struct Mol Biol 2006; 13:713-9.
56. Patel A, Dharmarajan V, Cosgrove MS. Structure of WDR5 bound to mixed lineage leukemia protein-1 peptide. J Biol Chem 2008; 283:32158-61.
57. Takahashi YH, Lee JS, Swanson SK, Saraf A, Florens L, Washburn MP, et al. 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 2009; 29:3478-86.
58. Schneider J, Wood A, Lee JS, Schuster R, Dueker J, Maguire C, et al. Molecular regulation of histone H3 trimethylation by COMPASS and the regulation of gene expression. Mol Cell 2005; 19:849-56.
59. Cao F, Chen Y, Cierpicki T, Liu Y, Basrur V, Lei M, et al. An Ash2L/RbBP5 heterodimer stimulates the MLL1 methyltransferase activity through coordinated substrate interactions with the MLL1 SET domain. Plos One 2010; 5:14102.
60. Patel A, Vought VE, Dharmarajan V, Cosgrove MS. A novel non-SET domain multi-subunit methyltransferase required for sequential nucleosomal histone H3 methylation by the mixed lineage leukemia protein-1 (MLL1) core complex. J Biol Chem 2011; 286:3359-69.
61. Nishioka K, Chuikov S, Sarma K, Erdjument-Bromage H, Allis CD, Tempst P, et al. Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes Dev 2002; 16:479-89.
62. Wang H, Cao R, Xia L, Erdjument-Bromage H, Borchers C, Tempst P, et al. Purification and functional characterization of a histone H3-lysine 4-specific methyltransferase. Mol Cell 2001; 8:1207-17.
63. Xiao B, Jing C, Wilson JR, Walker PA, Vasisht N, Kelly G, et al. Structure and catalytic mechanism of the human histone methyltransferase SET7/9. Nature 2003; 421:652-6.
64. Zhang X, Yang Z, Khan SI, Horton JR, Tamaru H, Selker EU, et al. Structural basis for the product specificity of histone lysine methyltransferases. Molecular Cell 2003; 12:177-85.
65. Munro S, Khaire N, Inche A, Carr S, La Thangue NB. Lysine methylation regulates the pRb tumour suppressor protein. Oncogene 2010; 29:2357-67.
66. Ivanov GS, Ivanova T, Kurash J, Ivanov A, Chuikov S, Gizatullin F, et al. Methylation-acetylation interplay activates p53 in response to DNA damage. Mol Cell Biol 2007; 27:6756-69.
67. Kurash JK, Lei H, Shen Q, Marston WL, Granda BW, Fan H, et al. Methylation of p53 by Set7/9 mediates p53 acetylation and activity in vivo. Mol Cell 2008; 29:392-400.
68. Yang XD, Tajkhorshid E, Chen LF. Functional interplay between acetylation and methylation of the RelA subunit of NFkappaB. Mol Cell Biol 2010; 30:2170-80.
69. Couture JF, Collazo E, Hauk G, Trievel RC. Structural basis for the methylation site specificity of SET7/9. Nat Struct Mol Biol 2006; 13:140-6.
70. Dhayalan A, Kudithipudi S, Rathert P, Jeltsch A. Specificity analysis-based identification of new methylation targets of the SET7/9 protein lysine methyltransferase. Chem Biol 2011; 18:111-20.
71. Wilson JR, Jing C, Walker PA, Martin SR, Howell SA, Blackburn GM, et al. Crystal structure and functional analysis of the histone methyltransferase SET7/9. Cell 2002; 111:105-15.
72. Demirci H, Gregory ST, Dahlberg AE, Jogl G. Multiple-site trimethylation of ribosomal protein L11 by the PrmA methyltransferase. Structure 2008; 16:1059-66.
73. Kuzmichev A, Jenuwein T, Tempst P, Reinberg D. Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol Cell 2004; 14:183-93.
74. Kuzmichev A, Margueron R, Vaquero A, Preissner TS, Scher M, Kirmizis A, et al. Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci USA 2005; 102:1859-64.
75. Avdic V, Zhang P, Lanouette S, Groulx A, Tremblay V, Brunzelle J, et al. Structural and biochemical insights into MLL1 core complex assembly. Structure 2011; 19:101-8.
76. Odho Z, Southall SM, Wilson JR. Characterization of a novel WDR5-binding site that recruits RbBP5 through a conserved motif to enhance methylation of histone H3 lysine 4 by mixed lineage leukemia protein-1. J Biol Chem 2010; 285:32967-76.
77. Chen Y, Wan B, Wang KC, Cao F, Yang Y, Protacio A, et al. Crystal structure of the N-terminal region of human Ash2L shows a winged-helix motif involved in DNA binding. EMBO Rep 2011.
78. Sarvan S, Avdic V, Tremblay V, Chaturvedi CP, Zhang P, Lanouette S, et al. Crystal structure of the trithorax group protein ASH2L reveals a forkheadlike DNA binding domain. Nat Struct Mol Biol 2011.
79. Schultz J, Milpetz F, Bork P, Ponting CP. SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 1998; 95:5857-64.
80. Rathert P, Dhayalan A, Murakami M, Zhang X, Tamas R, Jurkowska R, et al. Protein lysine methyltransferase G9a acts on non-histone targets. Nat Chem Biol 2008; 4:344-6.
81. Huang J, Sengupta R, Espejo AB, Lee MG, Dorsey JA, Richter M, et al. p53 is regulated by the lysine demethylase LSD1. Nature 2007; 449:105-8.