Automethylation of protein arginine methyltransferase 8 (PRMT8) regulates activity by impeding S-adenosylmethionine sensitivity

Journal of Biological Chemistry

Volumn 288, Issue 39, 2013, Pages 27872-27880

  Dillon, Myles B C ^a   Rust, Heather L ^b   Thompson, Paul R ^b   Mowen, Kerri A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHYLTRANSFERASES; N TERMINUS; PROTEIN-ARGININE METHYLTRANSFERASE; REGULATORY MECHANISM; S-ADENOSYLMETHIONINE; SELECTIVE REDUCTION;

ALKYLATION; ARGININE;

PROTEINS;

LYSINE; PHENYLALANINE; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 8; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG;

ARTICLE; AUTOMETHYLATION; BINDING AFFINITY; CELLULAR DISTRIBUTION; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENZYME ACTIVITY; HELA CELL; MEMBRANE BINDING; METHYLATION; MYRISTYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN;

ENZYME CATALYSIS; ENZYME INACTIVATION; ENZYME KINETICS; HISTONE METHYLATION; PROTEIN METHYLATION; S-ADENOSYLMETHIONINE (SAM);

CATALYSIS; HELA CELLS; HUMANS; LYSINE; MEMBRANE PROTEINS; METHYLATION; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHENYLALANINE; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN-ARGININE N-METHYLTRANSFERASES; S-ADENOSYLMETHIONINE;

EID: 84884799210     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.491092     Document Type: Article

References (53)

1. Bedford, M. T., and Richard, S. (2005) Arginine methylation: an emerging regulator of protein function. Mol. Cell 18, 263-272
2. Pahlich, S., Zakaryan, R. P., and Gehring, H. (2006) Protein arginine methylation: cellular functions and methods of analysis. Biochim. Biophys. Acta 1764, 1890-1903
3. Bedford, M. T., and Clarke, S. G. (2009) Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33, 1-13
4. Yu, Z., Chen, T., Hébert, J., Li, E., and Richard, S. (2009) A mouse PRMT1 null allele defines an essential role for arginine methylation in genome maintenance and cell proliferation. Mol. Cell. Biol. 29, 2982-2996
5. Lee, J., Sayegh, J., Daniel, J., Clarke, S., and Bedford, M. T. (2005) PRMT8, a new membrane-bound tissue-specific member of the protein arginine methyltransferase family. J. Biol. Chem. 280, 32890-32896
6. Sayegh, J., Webb, K., Cheng, D., Bedford, M. T., and Clarke, S. G. (2007) Regulation of protein arginine methyltransferase 8 (PRMT8) activity by its N-terminal domain. J. Biol. Chem. 282, 36444-36453
7. Taneda, T., Miyata, S., Kousaka, A., Inoue, K., Koyama, Y., Mori, Y., and Tohyama, M. (2007) Specific regional distribution of protein arginine methyltransferase 8 (PRMT8) in the mouse brain. Brain Res. 1155, 1-9
8. Lin, Y. L., Tsai, Y. J., Liu, Y. F., Cheng, Y. C., Hung, C. M., Lee, Y. J., Pan, H., and Li, C. (2013) The critical role of protein arginine methyltransferase prmt8 in zebrafish embryonic and neural development is non-redundant with its paralogue prmt1. PLoS ONE 8, e55221
9. Lin, W. J., Gary, J. D., Yang, M. C., Clarke, S., and Herschman, H. R. (1996) The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J. Biol. Chem. 271, 15034-15044
10. Gary, J. D., and Clarke, S. (1998) RNA and protein interactions modulated by protein arginine methylation. Prog. Nucleic Acid Res. Mol. Biol. 61, 65-131
11. Cheng, D., Yadav, N., King, R. W., Swanson, M. S., Weinstein, E. J., and Bedford, M. T. (2004) Small molecule regulators of protein arginine methyltransferases. J. Biol. Chem. 279, 23892-23899
12. Blanchet, F., Cardona, A., Letimier, F. A., Hershfield, M. S., and Acuto, O. (2005) CD28 costimulatory signal induces protein arginine methylation in T cells. J. Exp. Med. 202, 371-377
13. Krause, C. D., Yang, Z. H., Kim, Y. S., Lee, J. H., Cook, J. R., and Pestka, S. (2007) Protein arginine methyltransferases: evolution and assessment of their pharmacological and therapeutic potential. Pharmacol. Ther. 113, 50-87
14. Lee, D. Y., Ianculescu, I., Purcell, D., Zhang, X., Cheng, X., and Stallcup, M. R. (2007) Surface-scanning mutational analysis of protein arginine methyltransferase 1: roles of specific amino acids in methyltransferase substrate specificity, oligomerization, and coactivator function. Mol. Endocrinol. 21, 1381-1393
15. Williams-Ashman, H. G., Seidenfeld, J., and Galletti, P. (1982) Trends in the biochemical pharmacology of 5-deoxy-5-methylthioadenosine. Biochem. Pharmacol. 31, 277-288
16. Mowen, K. A., Schurter, B. T., Fathman, J. W., David, M., and Glimcher, L. H. (2004) Arginine methylation of NIP45 modulates cytokine gene expression in effector T lymphocytes. Mol. Cell 15, 559-571
17. Zurita-Lopez, C. I., Sandberg, T., Kelly, R., and Clarke, S. G. (2012) Human protein arginine methyltransferase 7 (PRMT7) is a type III enzyme forming-NG-monomethylated arginine residues. J. Biol. Chem. 287, 7859-7870
18. Troffer-Charlier, N., Cura, V., Hassenboehler, P., Moras, D., and Cavarelli, J. (2007) Functional insights from structures of coactivator- associated arginine methyltransferase 1 domains. EMBO J. 26, 4391-4401
19. Yue, W. W., Hassler, M., Roe, S. M., Thompson-Vale, V., and Pearl, L. H. (2007) Insights into histone code syntax from structural and biochemical studies of CARM1 methyltransferase. EMBO J. 26, 4402-4412
20. Zhang, X., and Cheng, X. (2003) Structure of the predominant protein arginine methyltransferase PRMT1 and analysis of its binding to substrate peptides. Structure 11, 509-520
21. Zhang, X., Zhou, L., and Cheng, X. (2000) Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J. 19, 3509-3519
22. Najbauer, J., Johnson, B. A., Young, A. L., and Aswad, D. W. (1993) Peptides with sequences similar to glycine, arginine-rich motifs in proteins interacting with RNA are efficiently recognized by methyltransferase( s) modifying arginine in numerous proteins. J. Biol. Chem. 268, 10501-10509
23. Lee, J., and Bedford, M. T. (2002) PABP1 identified as an arginine methyltransferase substrate using high-density protein arrays. EMBO Rep. 3, 268-273
24. Cheng, D., Côté, J., Shaaban, S., and Bedford, M. T. (2007) The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Mol. Cell 25, 71-83
25. Lakowski, T. M., and Frankel, A. (2008) A kinetic study of human protein arginine N-methyltransferase 6 reveals a distributive mechanism. J. Biol. Chem. 283, 10015-10025
26. Obianyo, O., Osborne, T. C., and Thompson, P. R. (2008) Kinetic mechanism of protein arginine methyltransferase. Biochemistry 47, 10420-10427
27. Wooderchak, W. L., Zang, T., Zhou, Z. S., Acuña, M., Tahara, S. M., and Hevel, J. M. (2008) Substrate profiling of PRMT1 reveals amino acid sequences that extend beyond the "RGG" paradigm. Biochemistry 47, 9456-9466
28. Bicker, K. L., Obianyo, O., Rust, H. L., and Thompson, P. R. (2011) A combinatorial approach to characterize the substrate specificity of protein arginine methyltransferase 1. Mol. Biosyst. 7, 48-51
29. Gui, S., Wooderchak, W. L., Daly, M. P., Porter, P. J., Johnson, S. J., and Hevel, J. M. (2011) Investigation of the molecular origins of protein-arginine methyltransferase I (PRMT1) product specificity reveals a role for two conserved methionine residues. J. Biol. Chem. 286, 29118-29126
30. Rust, H. L., and Thompson, P. R. (2011) Kinase consensus sequences: a breeding ground for crosstalk. ACS Chem. Biol. 6, 881-892
31. Obianyo, O., and Thompson, P. R. (2012) Kinetic mechanism of protein arginine methyltransferase 6 (PRMT6). J. Biol. Chem. 287, 6062-6071
32. Singh, V., Miranda, T. B., Jiang, W., Frankel, A., Roemer, M. E., Robb, V. A., Gutmann, D. H., Herschman, H. R., Clarke, S., and Newsham, I. F. (2004) DAL-1/4.1B tumor suppressor interacts with protein arginine Nmethyltransferase 3 (PRMT3) and inhibits its ability to methylate substrates in vitro and in vivo. Oncogene 23, 7761-7771
33. Xu, W., Cho, H., Kadam, S., Banayo, E. M., Anderson, S., Yates, J. R., 3rd, Emerson, B. M., and Evans, R. M. (2004)Amethylation-mediator complex in hormone signaling. Genes Dev. 18, 144-156
34. Robin-Lespinasse, Y., Sentis, S., Kolytcheff, C., Rostan, M. C., Corbo, L., and Le Romancer, M. (2007) hCAF1, a new regulator of PRMT1-dependent arginine methylation. J. Cell Sci. 120, 638-647
35. Aggarwal, P., Vaites, L. P., Kim, J. K., Mellert, H., Gurung, B., Nakagawa, H., Herlyn, M., Hua, X., Rustgi, A. K., McMahon, S. B., and Diehl, J. A. (2010) Nuclear cyclin D1/CDK4 kinase regulates CUL4 expression and triggers neoplastic growth via activation of the PRMT5 methyltransferase. Cancer Cell 18, 329-340
36. Frankel, A., and Clarke, S. (2000) PRMT3 is a distinct member of the protein arginine N-methyltransferase family. Conferral of substrate specificity by a zinc-finger domain. J. Biol. Chem. 275, 32974-32982
37. Weiss, V. H., McBride, A. E., Soriano, M. A., Filman, D. J., Silver, P. A., and Hogle, J. M. (2000) The structure and oligomerization of the yeast arginine methyltransferase, Hmt1. Nat. Struct. Biol. 7, 1165-1171
38. Rho, J., Choi, S., Seong, Y. R., Cho, W. K., Kim, S. H., and Im, D. S. (2001) Prmt5, which forms distinct homo-oligomers, is a member of the proteinarginine methyltransferase family. J. Biol. Chem. 276, 11393-11401
39. Cheng, X., Collins, R. E., and Zhang, X. (2005) Structural and sequence motifs of protein (histone) methylation enzymes. Annu. Rev. Biophys. Biomol. Struct. 34, 267-294
40. Lim, Y., Kwon, Y. H., Won, N. H., Min, B. H., Park, I. S., Paik, W. K., and Kim, S. (2005) Multimerization of expressed protein-arginine methyltransferases during the growth and differentiation of rat liver. Biochim. Biophys. Acta 1723, 240-247
41. Pak, M. L., Lakowski, T. M., Thomas, D., Vhuiyan, M. I., Hüsecken, K., and Frankel, A. (2011)Aprotein arginineN-methyltransferase 1 (PRMT1) and 2 heteromeric interaction increases PRMT1 enzymatic activity. Biochemistry 50, 8226-8240
42. Liu, F., Zhao, X., Perna, F., Wang, L., Koppikar, P., Abdel-Wahab, O., Harr, M. W., Levine, R. L., Xu, H., Tefferi, A., Deblasio, A., Hatlen, M., Menendez, S., and Nimer, S. D. (2011) JAK2V617F-mediated phosphorylation of PRMT5 downregulates its methyltransferase activity and promotes myeloproliferation. Cancer Cell 19, 283-294
43. Chin, H. G., Estève, P. O., Pradhan, M., Benner, J., Patnaik, D., Carey, M. F., and Pradhan, S. (2007) Automethylation of G9a and its implication in wider substrate specificity and HP1 binding. Nucleic Acids Res. 35, 7313-7323
44. Siddique, A. N., Jurkowska, R. Z., Jurkowski, T. P., and Jeltsch, A. (2011) Auto-methylation of the mouse DNA-(cytosine C5)-methyltransferase Dnmt3a at its active site cysteine residue. FEBS J. 278, 2055-2063
45. Kuhn, P., Chumanov, R., Wang, Y., Ge, Y., Burgess, R. R., and Xu, W. (2011) Automethylation of CARM1 allows coupling of transcription and mRNA splicing. Nucleic Acids Res. 39, 2717-2726
46. Singhroy, D. N., Mesplède, T., Sabbah, A., Quashie, P. K., Falgueyret, J. P., and Wainberg, M. A. (2013) Automethylation of protein arginine methyltransferase 6 (PRMT6) regulates its stability and its anti-HIV-1 activity. Retrovirology 10, 73
47. Bolte, S., and Cordelières, F. P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213-232
48. Rust, H. L., Zurita-Lopez, C. I., Clarke, S., and Thompson, P. R. (2011) Mechanistic studies on transcriptional coactivator protein arginine methyltransferase. Biochemistry 50, 3332-3345
49. Mostaqul Huq, M. D., Gupta, P., Tsai, N. P., White, R., Parker, M. G., and Wei, L. N. (2006) Suppression of receptor interacting protein 140 repressive activity by protein arginine methylation. EMBO J. 25, 5094-5104
50. Wilcox, C., Hu, J. S., and Olson, E. N. (1987) Acylation of proteins with myristic acid occurs cotranslationally. Science 238, 1275-1278
51. Deichaite, I., Casson, L. P., Ling, H. P., and Resh, M. D. (1988) In vitro synthesis of pp60v-src: myristylation in a cell-free system. Mol. Cell. Biol. 8, 4295-4301
52. Wei, Y., Horng, J. C., Vendel, A. C., Raleigh, D. P., and Lumb, K. J. (2003) Contribution to stability and folding of a buried polar residue at the CARM1 methylation site of the KIX domain of CBP. Biochemistry 42, 7044-7049
53. Higashimoto, K., Kuhn, P., Desai, D., Cheng, X., and Xu, W. (2007) Phosphorylation-mediated inactivation of coactivator-associated arginine methyltransferase. Proc. Natl. Acad. Sci. U.S.A. 104, 12318-12323