Bioinformatic identification of novel methyltransferases

Epigenomics

Volumn 1, Issue 1, 2009, Pages 163-175

  Petrossian, Tanya ^a   Clarke, Steven ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hidden Markov model profiling; Methyltransferases; Protein methylation; RNA methylation; S adenosylmethionine; SET domain; SPOUT domain

Indexed keywords

EID: 70449498768     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.09.3     Document Type: Article

References (87)

1. Cheng X, Blumenthal RM (Eds): S-adenosylmethionine-dependent methyltransferases: structures and Junctions. World Scientific, Singapore (1999).
2. Berman BP, Weisenberger DJ, Laird PW: Locking in on the human methylome. Nature 27(4), 341-342 (2009).
3. Jeltsch A: Molecular enzymology of mammalian DNA methyltransferases. Curr. Top. Microbiol. Immunol. 301, 203-225 (2006). (Pubitemid 43022673)
4. Kim JK, Samaranayake M, Pardhan S: Epigenetics mechanisms in mammals. Cell. Mol. Life Sci. 66(4), 596-612 (2009).
5. Ng SS, Yue WW, Oppermann U, Klose RJ: Dynamic protein methylation in chromatin biology. Cell. Mot. LifeSci. 66(3), 407-422 (2009).
6. Zhao Q, Rank G, Tan YT et al.: PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat. Struct. Mol. Biol. 16(3), 304-311 (2009).
7. Couture JF, Trievel RC: Histone-modifying enzymes: encrypting an enigmatic epigenetic code. Curr. Opin. Struct. Biol. 16(6), 753-760 (2006). (Pubitemid 44827726)
8. Horwich MD, Li C, Matranga C et al.: The Drosophila RNA methyltransferase, DmHenl, modifies germline piRNAs and single-stranded siRNAs in RISC. Current Biol. 17(14), 1265-1272 (2007). (Pubitemid 47043434)
9. Wassenegger M: The role of the RNAi machinery in heterochromatin formation. Cell 122(1), 13-16(2005). (Pubitemid 40977935)
10. Yu B, Yang Z, Li J et al.: Methylation as a crucial step in plant microRNA biogenesis. Science 307(5711), 932-935 (2005). (Pubitemid 40229231)
11. Li J. Yang Z. Yu B, Liu J, Chen X: Methylation protects miRNAs and siRNAs from a 3'-end uridylation activity in Arabidopsis. Current Biol. 15(16), 1501-1507 (2005). (Pubitemid 41187490)
12. Tkaczuk KL, Dunin-Horkawicz S, Purta E., Bujnicki JM: Structural and evolutionary bioinformatics of the SPOUT superfamily of methyltransferases. BMC Bioinformatics 8, 73 (2007).
13. Petrossian TC, Clarke SG: Multiple motif scanning to identify methyltransferases from the yeast proteome. Mol. Cell. Proteomics 8(7), 1516-1526 (2009).
14. Kozbial PZ, Mushegian AR: Natural history of S-adenosylmethionine-binding proteins. BMC Struct. Biol. 5, 19 (2005).
15. Schubert HL, Blumenthal RM, Cheng X: Many paths to methyltransfer: a chronicle of convergence. Trends Biochem. Sci. 28(6), 329-335 (2003). (Pubitemid 36776296)
16. Martin JL, McMillan FM: SAM (dependent) 1 AM: the S-adenosylmethionine- dependent methyltransferase fold. Curr. Opin. Struct. Biol. 12(6), 783-793 (2002). (Pubitemid 36009496)
17. Okano M, Bell DW, Haber D.A., Li E: DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell99{3), 247-257 (1999). (Pubitemid 29519904)
18. Pavlopoulou A, Kossida S: Plant cytosine-5 DNA methyltransferases: structure, function and molecular evolution. Genomics 90(4), 530-541 (2007). (Pubitemid 47407765)
19. Sawada K, Yang Z, Horton J.R., Collins RE, Zhang X, Cheng X: Structure of the conserved core of the yeast Dotlp, a nucleosomal histone H3 lysine 79 methyltransferase. J. Biol. Chem. 279(41), 43296-43306 (2004). (Pubitemid 39372225)
20. Ingrosso D, Fowler AV, Bleibaum J, Clarke S: Sequence of the D-aspartyl/L-isoaspartyl protein methyltransferase from human erythrocytes. Common sequence motifs for protein, DNA, RNA and small molecule S-adenosylmethioninc-dependent methyltransferases. J. Biol. Chem. 264(33), 20131-20139 (1989). (Pubitemid 20008135)
21. Niewmierzycka A, Clarke S: 5-sdenosylmethionine-dependent methylation in Saccharomyces cerevisiae. Identification of a novel protein arginine methyltransferase. J. Biol. Chem. 274(2), 814-824 (1999).
22. Kossykh VG, Schtagman SL, Hattman S: Conserved sequence motif DPPY in region IV of the phage T4 Dam DNA-[N6-adenine]-methyltransferase is important for S-adenosyl-L-methionine binding. AW. Acids Res. 21(20), 4659-4662 (1993). (Pubitemid 23312736)
23. Zhang X, Zhou L, Cheng X: Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J. 19(14), 3509-3519 (2000). (Pubitemid 30462110)
24. Singer MS, Kahana A, Wolf AJ et al.: Identification of high-copy disruptors of telomeric silencing in Saccharomyccs cerevisiae. Genetics 150(2), 613-632 (1998). (Pubitemid 28463040)
25. Fingerman 1M, Li HC, Briggs SD: A charge-based interaction between histone H4 and Dotl is required for H3K79 methylation and telomere silencing: identification of a new trans-histone pathway. Genes Develop. 21(16), 2018-2029 (2007). (Pubitemid 47267288)
26. Cheng XD, Collins RE, Zhang X: Structural and sequence motifs of protein (histone) methylation enzymes. Annu. Rev. Biophys. Biomol. Struct. 34, 267-294 (2005). (Pubitemid 40847726)
27. Ng HH, Feng Q, Wang H et al.: Lysine methylation within the globular domain of histone H3 by Dotl is important for telomeric silencing and Sir protein association. Genes Develop. 16(12), 1518-1527 (2002). (Pubitemid 34686333)
28. Gary JD, Lin WJ, Yang M.C., Herschman HR, Clarke S: The predominant protein-arginine methyltransferase from Saccharomyccs cerevisiae. J. Biol. Chem. 271(21), 12585-12594 (1996). (Pubitemid 26160933)
29. Kagan RM, Clarke S: Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. Arch. Biochem. Biophys. 310(2), 417-427 (1994).
30. Timothy LB, Charles E: Fitting a mixture model by expectation maximization to discover motifs in biopolymers, in proceedings of the second international conference on intelligent systems for molecular biology, AAAI Press, CA, USA, 28-36 (1994).
31. Katz JE, Dlakil M, Clarke S: Automated identification of putative methyltransferases from genomic open reading frames. Mol. Cell. Proteomics 2(8), 525-540 (2003).
32. Bailey TL, Gribskov M: Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14(1), 48-54 (1998). (Pubitemid 28395676)
33. Ansari MZ, Sharma J, Gokhale R.S., Mohanty D: In silico analysis of methyltransferase domains involved in biosynthesis of secondary metabolites. BMC Bioinformatics 9, 454 (2008).
34. Soding J, Biegert A, Lupas AN: The HHpred interactive server for protein homology detection and structure prediction. Nucl. Acids Res. 33, W244-W248 (2005). (Pubitemid 44529917)
35. Huerta-Cepas J., Bueno A, Dopazo J., Gabaldon T: PhylomeDB: a database for genome-wide collections of gene phytogenies. Nucl. Acids Res. 36, D491-D496 (2007). (Pubitemid 351149772)
36. Atkinson HJ, Morris JH, Ferrin T.E., Babbitt PC: Using sequence similarity networks for visualization of relationships across diverse protein superfamilies. PLoS ONE 4(2), e4345(2009).
37. Rea S, Eisenhaber F, O'Carroll D et al.: Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406(6796), 593-599 (2000). (Pubitemid 30641039)
38. Wang Y: Methylation and demethylation of histone arg and lys residues in chromatin structure and function. In: The Enzymes: Protein Methyltransferases. Clarke SG, Tamanoi F (Eds). Elsevier, Amsterdam, The Netherlands, 123-153 (2006).
39. Southall SM, Wong PS, Odho Z, Roe S.M., Wilson JR: Structural basis for the requirement of additional factors for mill set domain activity and recognition of epigenetic marks. Mol. Cell. 33(2), 181-191 (2009).
40. Dillon SC, Zhang X, Trievel R.C., Cheng X: The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol. 6(8), 227 (2005).
41. Xiao B, Gamblin SJ, Wilson JR: Structure of set domain protein lysine methyltransferases, In: The Enzymes: Protein Methyltransferases. Clarke SG, Tamanoi F (Eds.). Elsevier, Amsterdam, The Netherlands (2006).
42. Aravind L, Iyer LM: Provenance of SET-domain histone methyltransferases through duplication of a simple structural unit. Cell Cycle 2(4), 369-376 (2003).
43. Xiao B, Jing C, Wilson JR et al.: Structure and catalytic mechanism of the human histone methyltransferase SET7/9. Nature 421(6923), 652-656 (2003). (Pubitemid 36227675)
44. Couture JF, Dirk LM, Brunzelle J.S., Houtz RL, Trievel RC: Structural origins for the product specificity of SET domain protein methyltransferases. Proc. Natl Acad. Sci. USA 105(52), 20659-20664 (2008).
45. Zhang X, Yang Z, Khan SI et al.: Structural basis for the product specificity of histone lysine methyltransferases. Mol. Cell 12(1). 177-185 (2003). (Pubitemid 36957834)
46. Qian C, Zhou M: SET domain protein lysine methyltransferases: structure, specificity and catalysis. Cell. Mol. Life Sci. 63(23), 2755-2763 (2006). (Pubitemid 44913316)
47. Marmorstein R: Structure of SET domain proteins: a new twist on histone methylation. Trends Biochem. Sci. 28(2), 59-62 (2003). (Pubitemid 36165131)
48. Porras-Yakushi T.R., Whitelegge JP, Clarke S: A novel SET domain methyltransferase in yeast: Rkm2-dependent trimethylation of ribosomal protein L12ab at lysine 10. J. Biol-Chem. 281(47), 35835-35835 (2006).
49. Bottomley MJ: Structure of protein domains that create or recognize histone modifications. EMBO Reports 5(5), 464-469 (2004). (Pubitemid 38745036)
50. Letunic I, Doerks T, Bork P: SMART 6: recent updates and new developments. Nucleic Acids Res. 37(Database issue), D229-D232 (2009).
51. Baumbusch LO, Thorstensen T, Krauss V et al.: The Arahidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to Four evolutionary conserved classes. Nucl. Acids Res. 29(21), 4319-4333 (2001). (Pubitemid 33064772)
52. Springer NM, Napoli CA, Selinger DA et al.: Comparative analysis of set domain proteins in maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol. 132(2), 907-925 (2003). (Pubitemid 36715089)
53. Ng DW, Wang T, Chandrasekharan M.B., Aramayo R., Kertbundit S, Hall TC: Plant SET domain-containing proteins: structure, function and regulation. Biochim. Biophys. Acta 1769(5-6), 316-329 (2007). (Pubitemid 46855950)
54. Dirk LMA, Trievel RC, Houtz RL: Nonhistone protein lysine methyltransftrascs: structure and catalytic roles, in the enzymes: protein methyltransferases. Clarke SG, Tamanoi F (Eds.), Elsevier, Amsterdam, The Netherlands, 178-228 (2006).
55. Anantharaman V, Koonin EV, Aravind L: SPOUT: a class of methyltransferases that includes spoU and trmD RNA methylase supcrfamilies and novel superfamilies of predicted prokaryotic RNA methylases. J. Mol. Microbiol. Biotechnol. 4(1), 71-75 (2002). (Pubitemid 33121215)
56. Das K, Acton T, Chiang Y., Shih L, Arnold E, Montelione GT: Crystal structure of RlmAI: implications for understanding the 23S rRNA G745/G748-methylation at the macrolide antibiotic-binding site. Proc. Natl Acad. Sci. USA 101(12), (2003).
57. Michel G, Sauve V, Larocque R., Li Y, Matte A, Cygler M: The structure of the RlmB 23S rRNA methyltransferase reveals a new methyltransferase fold with a unique knot. Structure 10(10), 1303-1315 (2002). (Pubitemid 35232380)
58. Nureki O, Watanabe K, Fukai S et al.: Deep knot structure for construction of active site and cofactor binding site of tRNA modification enzyme. Structure 12(4), 593-602 (2004). (Pubitemid 38447162)
59. Watanabe K, Nureki O, Fukai S et al.: Roles of conserved amino acid sequence motifs in the SpoU (Trm H) RNA methyltransferase family. J. Biol. Chem. 280(11), 10368-10377 (2005). (Pubitemid 40395893)
60. Taylor AB, Meyer B, Leal BZ et al.: The crystal structure of Nepl reveals an extended SPOUT-class methyltransferase fold and a preorganized SAM-binding site. Nucleic Acids Res. 36(5), 1542-1554 (2008). (Pubitemid 351426107)
61. Leulliot N, Bohnsack MT, Graille M, Tollervey D., Van TH: The yeast ribosome synthesis factor Emgl is a novel member of the supetfamily of α/β knot fold methyltransferases. Nucleic Acids Res. 36(2), 626-639 (2008).
62. Matthews RG, Koutmos M, Datta S: Cobalamin-dependent and cobamide-dependent methyltransferases. Curr. Opin. Struct. Biol. 18(6), 658-666 (2009).
63. Dixon MM, Huang S, Matthews R.G., Ludwig M: The structure of the C-terminal domain of methionine synthase: presenting 5-adenosylmethionine for reductive methylation of B12. Structure 4(11), 1263-1275 (1996). (Pubitemid 26420496)
64. Sali A, Potterton L, Yuan F., van Vlijmen H, Karplus M: Evaluation of comparative protein modelling by MODELLER. Proteins 23(3), 318-326 (1995).
65. Kelley LA, Sternberg MJE: Protein structure prediction on the web: a case study using the Phyre server. Nat. Protoc. 4(3), 363-371 (2009).
66. Vinci CR, Clarke SG: Recognition of age-damaged Cff, 5)-adenosyl-i- merhionine by two methyltransferases in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 282(12), 8604-8612 (2007). (Pubitemid 47093473)
67. Koutmos M, Pejchal R, Bomer T.M., Matthews RG, Smith J L, Ludwig ML: Met al. active site elasticity linked to activation of homocysteine in methionine synthases. Proc. Natl Acad. Sci. USA 105(9), 3286-3291 (2008). (Pubitemid 351723545)
68. Ferrer J-L, Ravanel S., Robert M, Dumas R: Crystal structures of cobalamin-independent methionine synthase complexed with zinc, homocysteine, and methyltetrahydrofolate. J. Biol. Chem. 279(43), 44235-44238 (2004). (Pubitemid 39430825)
69. Sofia HJ, Chen G, Hetzler B.G., Reyes-Spindola JF, Miller NE: Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucl. Acids Res. 29(5), 1097-1106 (2001). (Pubitemid 32186195)
70. Berkovitch F, Nicolet Y, Wan J.T., Jarrett JT, Drennan CL: Crystal structure of biotin synthase, an S-adenosylmethionine-dependent radical enzyme. Science 303(5654), 76-79 (2004). (Pubitemid 38055773)
71. Wang SC, Frey PA: 5-adenosylmethionine as an oxidant: the radical SAM superfamily. Cell 32(3), 101-110(2007). (Pubitemid 46367690)
72. Booker SJ: Anaerobic functionalization of unactivated C-H bonds. Curr. Opin. Chem. Biol. 13(1), 58-73 (2009).
73. Pruitt KD, Tatusova T, Maglott DR: NCBI reference sequences (RefSeq): a curated nonredundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35(Database issue), D61-D65 (2007). (Pubitemid 46056171)
74. Schubert HL, Wilson KS Raux E, Woodcock SC, Warren MJ: The X-ray structure of a cobalamin biosynthetic enzyme, cobalt-precorrin-4 methyltransferase. Nature Struct. Biol. 5(7), 585-592 (1998).
75. Romano JD, Michaelis S: Topological and mutational analysis of Saccharomyces cerevisiae Stel4p, founding member of the isoprenylcysteine carboxyl methyltransferase family. Mol. Biol. Cell 12(7), 1957-1971 (2001). (Pubitemid 33049691)
76. Finn RD, Tate J, Mistry J et al.: The Pfam protein families database. Nucleic Acids Res. 36(Database Issue), D281-D288 (2008). (Pubitemid 351149737)
77. Clancy MJ, Shambaugh ME, Timpte C.S., Bokar JA: Induction of sporulation in Saccharomyces cerevisiae leads to the formation of N6-methyladenosine in mRNA: a potential mechanism for the activity of the IME4 gene. Nucl. Acids Res. 30(20), 4509-4518 (2002). (Pubitemid 35277261)
78. Subbaramaiah K, Simms SA: Photolabeling of CheR methyltransferase with 5-adenosyl-L-methionine (AdoMet). Studies on the AdoMet binding site. J. Biol. Chem. 267(12), 8636-8642 (1992).
79. Zhou S, Bailey MJ, Dunn M.J., Preedy VR, Emery PW: A systematic investigation into the recovery of radioactively labeled proteins from sodium dodecyl sulfate-polyacrylamide gels. Electrophoresis 25(1), 1-7 (2003).
80. Zhou S, Mann CJ, Dunn M.J., Preedy VR, Emery PW: Measurement of specific radioactivity in proteins separated by two-dimensional gel electrophoresis. Electrophoresis 27(5-6), 1147-1153 (2006).
81. Zhu H, Bilgin M, Bangham R et al.: Global analysis of protein activities using proteome chips. Science 293(5537), 2101-2105 (2001). (Pubitemid 32848060)
82. Rathert P, Dhayalan A, Ma H., Jeltsch A: Specificity of protein lysine methyltransferases and methods for detection of lysine methylation of nonhistone proteins. Mol. Biosyst. 4 (12), 1186-1190 (2008).
83. Laskowski RA: PDBsum new things. Nucl. Acids Res. 37, D355-D359 (2009).
84. Tatusov RL, Fedorova ND, Jackson JD et al.: The COG database: an updated version includes eukaryotes. BMC Bioinjbrmatics 4, 41 (2003).
85. Download of the Multiple Motif Scanning program, which is freely available www.chem.ucla.edu/files/MotifSetup. Zip
86. Saccharomyces Genome Database (SGD), the scientific database for the molecular biology and genetics of the yeast Saccharomyces cerevisiae www.yeastgenome.org/
87. UniProt website: comprehensive database of protein information www.uniprot.org