Arginine methylation controls the subcellular localization and functions of the oncoprotein splicing factor SF2/ASF

Molecular and Cellular Biology

Volumn 30, Issue 11, 2010, Pages 2762-2774

  Sinha, Rahul ^a,b   Allemand, Eric ^a,c   Zhang, Zuo ^a,d   Karni, Rotem ^a,e   Myers, Michael P ^a,f   Krainer, Adrian R ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c INSTITUT PASTEUR   (France)

^d MERCK RESEARCH LABORATORIES   (United States)

^e HEBREW UNIVERSITY   (Israel)

^f INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; ASF PROTEIN; MESSENGER RNA; ONCOPROTEIN; SF2 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; CYTOPLASM; GENE TARGETING; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; METHYLATION; MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEOMICS;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ARGININE; HELA CELLS; HUMANS; METHYLATION; NUCLEAR PROTEINS; ONCOGENE PROTEINS; RNA PRECURSORS; SUBCELLULAR FRACTIONS; TANDEM MASS SPECTROMETRY;

EUKARYOTA;

EID: 77952614701     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01270-09     Document Type: Article

References (65)

1. Alex, D., and K. A. Lee. 2005. RGG-boxes of the EWS oncoprotein repress a range of transcriptional activation domains. Nucleic Acids Res. 33:1323-1331. (Pubitemid 41439925)
2. Allemand, E., M. L. Hastings, M. V. Murray, M. P. Myers, and A. R. Krainer. 2007. Alternative splicing regulation by interaction of phosphatase PP2Cgamma with nucleic acid-binding protein YB-1. Nat. Struct. Mol. Biol. 14:630-638.
3. Araya, N., H. Hiraga, K. Kako, Y. Arao, S. Kato, and A. Fukamizu. 2005. Transcriptional down-regulation through nuclear exclusion of EWS methylated by PRMT1. Biochem. Biophys. Res. Commun. 329:653-660.
4. Bedford, M. T., A. Frankel, M. B. Yaffe, S. Clarke, P. Leder, and S. Richard. 2000. Arginine methylation inhibits the binding of proline-rich ligands to Src homology 3, but not WW, domains. J. Biol. Chem. 275:16030-16036.
5. Belyanskaya, L. L., P. M. Gehrig, and H. Gehring. 2001. Exposure on cell surface and extensive arginine methylation of Ewing sarcoma (EWS) protein. J. Biol. Chem. 276:18681-18687.
6. Bergamini, G., T. Preiss, and M. W. Hentze. 2000. Picornavirus IRESes and the poly(A) tail jointly promote cap-independent translation in a mammalian cell-free system. RNA 6:1781-1790. (Pubitemid 32001949)
7. Birney, E., S. Kumar, and A. R. Krainer. 1993. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 21:5803-5816. (Pubitemid 24023691)
8. Bish, R. A., O. I. Fregoso, A. Piccini, and M. P. Myers. 2008. Conjugation of complex polyubiquitin chains to WRNIP1. J. Proteome Res. 7:3481-3489.
9. Black, D. L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72:291-336.
10. Borders, C. L., Jr., J. A. Broadwater, P. A. Bekeny, J. E. Salmon, A. S. Lee, A. M. Eldridge, and V. B. Pett. 1994. A structural role for arginine in proteins: multiple hydrogen bonds to backbone carbonyl oxygens. Protein Sci. 3:541-548.
11. Bressan, G. C., E. C. Moraes, A. O. Manfiolli, T. M. Kuniyoshi, D. O. Passos, M. D. Gomes, and J. Kobarg. 2009. Arginine methylation analysis of the splicing-associated SR protein SFRS9/SRP30C. Cell. Mol. Biol. Lett. 14:657-669.
12. Cáceres, J. F., T. Misteli, G. R. Screaton, D. L. Spector, and A. R. Krainer. 1997. Role of the modular domains of SR proteins in subnuclear localization and alternative splicing specificity. J. Cell Biol. 138:225-238.
13. Cáceres, J. F., G. R. Screaton, and A. R. Krainer. 1998. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12:55-66.
14. Cáceres, J. F., S. Stamm, D. M. Helfman, and A. R. Krainer. 1994. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265:1706-1709.
15. Calnan, B. J., B. Tidor, S. Biancalana, D. Hudson, and A. D. Frankel. 1991. Arginine-mediated RNA recognition: the arginine fork. Science 252:1167-1171.
16. Cartegni, L., S. L. Chew, and A. R. Krainer. 2002. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat. Rev. Genet. 3:285-298.
17. Cazalla, D., J. Zhu, L. Manche, E. Huber, A. R. Krainer, and J. F. Cáceres. 2002. Nuclear export and retention signals in the RS domain of SR proteins. Mol. Cell. Biol. 22:6871-6882.
18. Côté, J., and S. Richard. 2005. Tudor domains bind symmetrical dimethylated arginines. J. Biol. Chem. 280:28476-28483.
19. Craig, R., J. P. Cortens, and R. C. Beavis. 2004. Open source system for analyzing, validating, and storing protein identification data. J. Proteome Res. 3:1234-1242. (Pubitemid 40040378)
20. Durocher, Y., S. Perret, and A. Kamen. 2002. High-level and high-through-put recombinant protein production by transient transfection of suspensiongrowing human 293-EBNA1 cells. Nucleic Acids Res. 30:E9.
21. Goulet, I., G. Gauvin, S. Boisvenue, and J. Côté. 2007. Alternative splicing yields protein arginine methyltransferase 1 isoforms with distinct activity, substrate specificity, and subcellular localization. J. Biol. Chem. 282:33009-33021.
22. Graveley, B. R. 2000. Sorting out the complexity of SR protein functions. RNA 6:1197-1211.
23. Hemann, M. T., J. T. Zilfou, Z. Zhao, D. J. Burgess, G. J. Hannon, and S. W. Lowe. 2004. Suppression of tumorigenesis by the p53 target PUMA. Proc. Natl. Acad. Sci. U. S. A. 101:9333-9338.
24. Herrmann, F., M. Bossert, A. Schwander, E. Akgun, and F. O. Fackelmayer. 2004. Arginine methylation of scaffold attachment factor A by heterogeneous nuclear ribonucleoprotein particle-associated PRMT1. J. Biol. Chem. 279:48774-48779.
25. Huang, Y., and G. G. Carmichael. 1996. A suboptimal 5′ splice site is a cis-acting determinant of nuclear export of polyomavirus late mRNAs. Mol. Cell. Biol. 16:6046-6054.
26. Huang, Y., and J. A. Steitz. 2005. SRprises along a messenger's journey. Mol. Cell 17:613-615.
27. Huang, Y., T. A. Yario, and J. A. Steitz. 2004. A molecular link between SR protein dephosphorylation and mRNA export. Proc. Natl. Acad. Sci. U. S. A. 101:9666-9670.
28. Hyun, Y. L., D. B. Lew, S. H. Park, C. W. Kim, W. K. Paik, and S. Kim. 2000. Enzymic methylation of arginyl residues in -gly-arg-gly- peptides. Biochem. J. 348:573-578.
29. Jobert, L., M. Argentini, and L. Tora. 2009. PRMT1 mediated methylation of TAF15 is required for its positive gene regulatory function. Exp. Cell Res. 315:1273-1286.
30. Karni, R., E. de Stanchina, S. W. Lowe, R. Sinha, D. Mu, and A. R. Krainer. 2007. The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat. Struct. Mol. Biol. 14:185-193.
31. Kim, S., B. M. Merrill, R. Rajpurohit, A. Kumar, K. L. Stone, V. V. Papov, J. M. Schneiders, W. Szer, S. H. Wilson, W. K. Paik, and K. R. Williams. 1997. Identification of N(G)-methylarginine residues in human heterogeneous RNP protein A1: Phe/Gly-Gly-Gly-Arg-Gly-Gly-Gly/Phe is a preferred recognition motif. Biochemistry 36:5185-5192.
32. Koizumi, J., Y. Okamoto, H. Onogi, A. Mayeda, A. R. Krainer, and M. Hagiwara. 1999. The subcellular localization of SF2/ASF is regulated by direct interaction with SR protein kinases (SRPKs). J. Biol. Chem. 274:11125-11131. (Pubitemid 129528322)
33. Krainer, A. R., G. C. Conway, and D. Kozak. 1990. Purification and characterization of pre-mRNA splicing factor SF2 from HeLa cells. Genes Dev. 4:1158-1171. (Pubitemid 20220268)
34. Krainer, A. R., T. Maniatis, B. Ruskin, and M. R. Green. 1984. Normal and mutant human beta-globin pre-mRNAs are faithfully and efficiently spliced in vitro. Cell 36:993-1005.
35. Krainer, A. R., A. Mayeda, D. Kozak, and G. Binns. 1991. Functional expression of cloned human splicing factor SF2: homology to RNA-binding proteins, U1 70K, and Drosophila splicing regulators. Cell 66:383-394.
36. Lai, M. C., R. I. Lin, and W. Y. Tarn. 2001. Transportin-SR2 mediates nuclear import of phosphorylated SR proteins. Proc. Natl. Acad. Sci. U. S. A. 98:10154-10159.
37. Lai, M. C., and W. Y. Tarn. 2004. Hypophosphorylated ASF/SF2 binds TAP and is present in messenger ribonucleoproteins. J. Biol. Chem. 279:31745-31749.
38. Lee, M. S., and P. A. Silver. 1997. RNA movement between the nucleus and the cytoplasm. Curr. Opin. Genet. Dev. 7:212-219.
39. Li, X., J. Wang, and J. L. Manley. 2005. Loss of splicing factor ASF/SF2 induces G2 cell cycle arrest and apoptosis, but inhibits internucleosomal DNA fragmentation. Genes Dev. 19:2705-2714. (Pubitemid 41627937)
40. Liu, Q., and G. Dreyfuss. 1995. In vivo and in vitro arginine methylation of RNA-binding proteins. Mol. Cell. Biol. 15:2800-2808.
41. Long, J. C., and J. F. Cáceres. 2009. The SR protein family of splicing factors: master regulators of gene expression. Biochem. J. 417:15-27.
42. Maris, C., C. Dominguez, and F. H. Allain. 2005. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J. 272:2118-2131. (Pubitemid 40655326)
43. Mayeda, A., and A. R. Krainer. 1999. Mammalian in vitro splicing assays. Methods Mol. Biol. 118:315-321.
44. Mayeda, A., and A. R. Krainer. 1999. Preparation of HeLa cell nuclear and cytosolic S100 extracts for in vitro splicing. Methods Mol. Biol. 118:309-314.
45. McBride, A. E., J. T. Cook, E. A. Stemmler, K. L. Rutledge, K. A. McGrath, and J. A. Rubens. 2005. Arginine methylation of yeast mRNA-binding protein Npl3 directly affects its function, nuclear export, and intranuclear protein interactions. J. Biol. Chem. 280:30888-30898.
46. Misteli, T. 1999. RNA splicing: what has phosphorylation got to do with it? Curr. Biol. 9:R198-R200.
47. Nichols, R. C., X. W. Wang, J. Tang, B. J. Hamilton, F. A. High, H. R. Herschman, and W. F. Rigby. 2000. The RGG domain in hnRNP A2 affects subcellular localization. Exp. Cell Res. 256:522-532.
48. Ong, S. E., G. Mittler, and M. Mann. 2004. Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat. Methods 1:119-126.
49. Piñol-Roma, S., and G. Dreyfuss. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355:730-732.
50. Sanford, J. R., N. K. Gray, K. Beckmann, and J. F. Cáceres. 2004. A novel role for shuttling SR proteins in mRNA translation. Genes Dev. 18:755-768. (Pubitemid 38480888)
51. Sato, H., N. Hosoda, and L. E. Maquat. 2008. Efficiency of the pioneer round of translation affects the cellular site of nonsense-mediated mRNA decay. Mol. Cell 29:255-262. (Pubitemid 351172823)
52. Shen, E. C., M. F. Henry, V. H. Weiss, S. R. Valentini, P. A. Silver, and M. S. Lee. 1998. Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes Dev. 12:679-691.
53. Siebel, C. W., and C. Guthrie. 1996. The essential yeast RNA binding protein Np13p is methylated. Proc. Natl. Acad. Sci. U. S. A. 93:13641-13646.
54. Singleton, D. R., S. Chen, M. Hitomi, C. Kumagai, and A. M. Tartakoff. 1995. A yeast protein that bidirectionally affects nucleocytoplasmic transport. J. Cell Sci. 108:265-272.
55. Sun, S., Z. Zhang, R. Sinha, R. Karni, and A. R. Krainer. 2010. SF2/ASF autoregulation involves multiple layers of post-transcriptional and translational control. Nat. Struct. Mol. Biol. 17:306-312.
56. Thermann, R., G. Neu-Yilik, A. Deters, U. Frede, K. Wehr, C. Hagemeier, M. W. Hentze, and A. E. Kulozik. 1998. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J. 17:3484-3494. (Pubitemid 28279521)
57. Tockman, M. S., Y. S. Erozan, P. Gupta, S. Piantadosi, J. L. Mulshine, and J. C. Ruckdeschel. 1994. The early detection of second primary lung cancers by sputum immunostaining. LCEWDG Investigators. Lung Cancer Early Detection Group. Chest 106:385S-390S.
58. Wang, H., Z. Q. Huang, L. Xia, Q. Feng, H. Erdjument-Bromage, B. D. Strahl, S. D. Briggs, C. D. Allis, J. Wong, P. Tempst, and Y. Zhang. 2001. Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science 293:853-857. (Pubitemid 32743973)
59. Weiss, V. H., A. E. McBride, M. A. Soriano, D. J. Filman, P. A. Silver, and J. M. Hogle. 2000. The structure and oligomerization of the yeast arginine methyltransferase, Hmt1. Nat. Struct. Biol. 7:1165-1171.
60. Wooderchak, W. L., T. Zang, Z. S. Zhou, M. Acuña, S. M. Tahara, and J. M. Hevel. 2008. Substrate profiling of PRMT1 reveals amino acid sequences that extend beyond the "RGG" paradigm. Biochemistry 47:9456-9466.
61. Xu, C., and M. F. Henry. 2004. Nuclear export of hnRNP Hrp1p and nuclear export of hnRNP Npl3p are linked and influenced by the methylation state of Npl3p. Mol. Cell. Biol. 24:10742-10756.
62. Yang, L., H. A. Chansky, and D. D. Hickstein. 2000. EWS.Fli-1 fusion protein interacts with hyperphosphorylated RNA polymerase II and interferes with serine-arginine protein-mediated RNA splicing. J. Biol. Chem. 275:37612-37618.
63. Yun, C. Y., and X. D. Fu. 2000. Conserved SR protein kinase functions in nuclear import and its action is counteracted by arginine methylation in Saccharomyces cerevisiae. J. Cell Biol. 150:707-718.
64. Zhang, J., X. Sun, Y. Qian, and L. E. Maquat. 1998. Intron function in the nonsense-mediated decay of beta-globin mRNA: indications that premRNA splicing in the nucleus can influence mRNA translation in the cytoplasm. RNA 4:801-815. (Pubitemid 28317828)
65. Zhang, Z., and A. R. Krainer. 2004. Involvement of SR proteins in mRNA surveillance. Mol. Cell 16:597-607.