Ribosomal protein S2 is a substrate for mammalian PRMT3 (protein arginine methyltransferase 3)

Biochemical Journal

Volumn 386, Issue 1, 2005, Pages 85-91

  Swiercz, Rafal ^a   Person, Maria D ^b   Bedford, Mark T ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Arginine methylation; Protein arginine N methyltransferase 3 (PRMT3); Ribosomal protein S2 (rpS2); Ribosome; Zinc finger

Indexed keywords

BIOCHEMISTRY; CATALYSIS; CELLS; SEDIMENTS; SUBSTRATES; ZINC;

CYTOPLASM; DIMETHYLARGININE; MOLECULAR MASS; RIBOSOMAL PROTEIN;

PROTEINS;

FIBRILLARIN; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; N(G),N(G) DIMETHYLARGININE; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 3; PROTEIN S II; PROTEIN SAM68; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME SPECIFICITY; GENE DELETION; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN METHYLATION; PROTEIN SYNTHESIS; RIBOSOME; ZINC FINGER MOTIF;

ANIMALS; ARGININE; CHROMATOGRAPHY, AFFINITY; HELA CELLS; HUMANS; METHYLATION; MICE; NIH 3T3 CELLS; PROTEIN BIOSYNTHESIS; PROTEIN INTERACTION MAPPING; PROTEIN-ARGININE N-METHYLTRANSFERASE; RECOMBINANT FUSION PROTEINS; RIBOSOMAL PROTEINS; RIBOSOMES; ZINC FINGERS;

MAMMALIA;

EID: 14244255860     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041466     Document Type: Article

References (38)

1. McBride, A. E. and Silver, P. A. (2001) State of the arg: protein methylation at arginine comes of age. Cell 106, 5-8
2. 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
3. Miranda, T. B., Miranda, M., Frankel, A. and Clarke, S. (2004) PRMT7 is a member of the protein arginine methyltransferase family with a distinct substrate specificity. J. Biol. Chem. 279, 22902-22907
4. Gary, J. D., Lin, W. J., Yang, M. C., Herschman, H. R. and Clarke, S. (1996) The predominant protein-arginine methyltransferase from Saccharomyces cerevisiae. J. Biol. Chem. 271, 12585-12594
5. Tang, J., Gary, J. D., Clarke, S. and Herschman, H. R. (1998) PRMT 3, a type I protein arginine N-methyltransferase that differs from PRMT1 in its oligomerization, subcellular localization, substrate specificity, and regulation. J. Biol. Chem. 273, 16935-16945
6. Frankel, A., Yadav, N., Lee, J., Branscombe, T. L., Clarke, S. and Bedford, M. T. (2002) The novel human protein arginine N-methyltransferase PRMT6 is a nuclear enzyme displaying unique substrate specificity. J. Biol. Chem. 277, 3537-3543
7. Branscombe, T. L., Frankel, A., Lee, J. H., Cook, J. R., Yang, Z., Pestka, S. and Clarke, S. (2001) Prmt5 (janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J. Biol. Chem. 276, 32971-32976
8. Smith, J. J., Rucknagel, K. P., Schierhorn, A., Tang, J., Nemeth, A., Linder, M., Herschman, H. R. and Wahle, E. (1999) Unusual sites of arginine methylation in Poly(A)-binding protein II and in vitro methylation by protein arginine methyltransferases PRMT1 and PRMT3. J. Biol. Chem. 274, 13229-13234
9. Lee, J. and Bedford, M. T. (2002) PABP1 identified as an arginine methyltransferase substrate using high-density protein arrays. EMBO Rep. 3, 268-273
10. Cote, J., Boisvert, F. M., Boulanger, M. C., Bedford, M. T. and Richard, S. (2003) Sam68 RNA binding protein is an in vivo substrate for protein arginine N-methyltransferase 1. Mol. Biol. Cell 14, 274-287
11. 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
12. Zhang, X., Zhou, L. and Cheng, X. (2000) Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J. 19, 3509-3519
13. 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
14. Xu, W., Chen, H., Du, K., Asahara, H., Tini, M., Emerson, B. M., Montminy, M. and Evans, R. M. (2001) A transcriptional switch mediated by cofactor methylation. Science 294, 2507-2511
15. Pawlak, M. R., Scherer, C. A., Chen, J., Roshon, M. J. and Ruley, H. E. (2000) Arginine N-methyltransferase 1 is required for early postimplantation mouse development, but cells deficient in the enzyme are viable. Mol. Cell. Biol. 20, 4859-4869
16. Yadav, N., Lee, J., Kim, J., Shen, J., Hu, M. C., Aldaz, C. M. and Bedford, M. T. (2003) Specific protein methylation defects and gene expression perturbations in coactivator-associated arginine methyltransferase 1-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 100, 6464-6468
17. Shen, E. C., Henry, M. F., Weiss, V. H., Valentini, S. R., Silver, P. A. and Lee, M. S. (1998) Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes Dev. 12, 679-691
18. Bachand, F. and Silver, P. A. (2004) PRMT3 is a ribosomal protein methyltransferase that affects the cellular levels of ribosomal subunits. EMBO J. 23, 2641-2650
19. Bedford, M. T., Frankel, A., Yaffe, M. B., Clarke, S., Leder, P. and Richard, S. (2000) Arginine methylation inhibits the binding of proline-rich ligands to Src homology 3, but not WW, domains. J. Biol. Chem. 275, 16030-16036
20. Friesen, W. J., Massenet, S., Paushkin, S., Wyce, A. and Dreyfuss, G. (2001) SMN, the product of the spinal muscular atrophy gene, binds preferentially to dimethylarginine-containing protein targets. Mol. Cell 7, 1111-1117
21. Valentini, S. R., Weiss, V. H. and Silver, P. A. (1999) Arginine methylation and binding of Hrp1p to the efficiency element for mRNA 3′-end formation. RNA 5, 272-280
22. Kwak, Y. T., Guo, J., Prajapati, S., Park, K. J., Surabhi, R. M., Miller, B., Gehrig, P. and Gaynor, R. B. (2003) Methylation of SPT5 regulates its interaction with RNA polymerase II and transcriptional elongation properties. Mol. Cell 11, 1055-1066
23. Chen, D., Ma, H., Hong, H., Koh, S. S., Huang, S. M., Schurter, B. T., Aswad, D. W. and Stallcup, M. R. (1999) Regulation of transcription by a protein methyltransferase. Science 284, 2174-2177
24. Boisvert, F. M., Cote, J., Boulanger, M. C., Cleroux, P., Bachand, F., Autexier, C. and Richard, S. (2002) Symmetrical dimethylarginine methylation is required for the localization of SMN in Cajal bodies and pre-mRNA splicing. J. Cell Biol. 159, 957-969
25. 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
26. Rosenfeld, J., Capdevielle, J., Guillemot, J. C. and Ferrara, P. (1992) In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem. 203, 173-179
27. Person, M. D., Lo, H. H., Towndrow, K. M., Jia, Z., Monks, T. J. and Lau, S. S. (2003) Comparative identification of prostanoid inducible proteins by LC-ESI-MS/MS and MALDI-TOF mass spectrometry. Chem. Res. Toxicol. 16, 757-767
28. Jia, Z., Person, M. D., Dong, J., Shen, J., Hensley, S. C., Stevens, J. L., Monks, T. J. and Lau, S. S. (2004) Grp78 is essential for 11-deoxy, 16,16-dimethyl prostaglandin E2 mediated cytoprotection in renal epithelial cells. Am. J. Physiol. Renal. Physiol. 287, F1113-F1122
29. Liu, Q. and Dreyfuss, G. (1995) In vivo and in vitro arginine methylation of RNA-binding proteins. Mol. Cell. Biol. 15, 2800-2808
30. Boisvert, F. M., Cote, J., Boulanger, M. C. and Richard, S. (2003) A proteomic analysis of arginine-methylated protein complexes. Mol. Cell. Proteomics 2, 1319-1330
31. Chevillard-Briet, M., Trouche, D. and Vandel, L. (2002) Control of CBP co-activating activity by arginine methylation. EMBO J. 21, 5457-5466
32. Lee, Y. H., Koh, S. S., Zhang, X., Cheng, X. and Stallcup, M. R. (2002) Synergy among nuclear receptor coactivators: selective requirement for protein methyltransferase and acetyltransferase activities. Mol. Cell. Biol. 22, 3621-3632
33. Holland, E. C., Sonenberg, N., Pandolfi, P. P. and Thomas, G. (2004) Signaling control of mRNA translation in cancer pathogenesis. Oncogene 23, 3138-3144
34. Kwiatkowski, D. J., Zhang, H., Bandura, J. L., Heiberger, K. M., Glogauer, M., el-Hashemite, N. and Onda, H. (2002) A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells. Hum. Mol. Genet. 11, 525-534
35. Jaeschke, A., Dennis, P. B. and Thomas, G. (2004) mTOR: a mediator of intracellular homeostasis. Curr. Top. Microbiol. Immunol. 279, 283-298
36. Chang, F. N., Navickas, I. J., Chang, C. N. and Dancis, B. M. (1976) Methylation of ribosomal proteins in HeLa cells. Arch. Biochem. Biophys. 172, 627-633
37. Zobel-Thropp, P., Yang, M. C., Machado, L. and Clarke, S. (2000) A novel posttranslational modification of yeast elongation factor 1A. Methylesterification at the C terminus. J. Biol. Chem. 275, 37150-37158
38. Cavallius, J., Zoll, W., Chakraburtty, K. and Merrick, W. C. (1993) Characterization of yeast EF-1 alpha: non-conservation of post-translational modifications. Biochim. Biophys. Acta 1163, 75-80