PRMT1 is required for RAP55 to localize to processing bodies

RNA Biology

Volumn 9, Issue 5, 2012, Pages 610-623

  Matsumoto, Ken ^a,b   Nakayama, Hiroshi ^a   Yoshimura, Mami ^a   Masuda, Akiko ^a   Dohmae, Naoshi ^a   Matsumoto, Shogo ^a   Tsujimoto, Masafumi ^a  

^a RIKEN   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Lsm14A; Lsm14B; mRNP granule; P body; PRMT1; RAP55

Indexed keywords

CELL PROTEIN; MESSENGER RIBONUCLEOPROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 1; PROTEIN ARGININE METHYLTRANSFERASE 5; RAP55A PROTEIN; RAP55B PROTEIN; RIBONUCLEOPROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL GRANULE; CELL STRESS GRANULE; CYTOPLASM; DEMETHYLATION; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROCESSING BODY; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

EID: 84862225516     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.19527     Document Type: Article

References (64)

1. Moore MJ. From birth to death: the complex lives of eukaryotic mRNAs. Science 2005; 309:1514-8; PMID:16141059; http://dx.doi.org/10.1126/science. 1111443.
2. Eulalio A, Behm-Ansmant I, Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 2007; 8:9-22; PMID:17183357; http://dx.doi.org/10.1038/nrm2080.
3. Franks TM, Lykke-Andersen J. The control of mRNA decapping and P-body formation. Mol Cell 2008; 32:605-15; PMID:19061636; http://dx.doi. org/10.1016/j.molcel.2008.11.001.
4. Anderson P, Kedersha N. RNA granules: posttranscriptional and epigenetic modulators of gene expression. Nat Rev Mol Cell Biol 2009; 10:430-6; PMID:19461665; http://dx.doi.org/10.1038/nrm2694.
5. Balagopal V, Parker R. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr Opin Cell Biol 2009; 21:403-8; PMID:19394210; http://dx.doi.org/10.1016/j.ceb.2009.03.005.
6. Parker R, Sheth U. P bodies and the control of mRNA translation and degradation. Mol Cell 2007; 25:635-46; PMID:17349952; http://dx.doi.org/10.1016/ j. molcel.2007.02.011.
7. Buchan JR, Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol Cell 2009; 36:932-41; PMID:20064460; http://dx.doi.org/10.1016/ j.molcel. 2009.11.020.
8. Kedersha NL, Gupta M, Li W, Miller I, Anderson P. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol 1999; 147:1431- 42; PMID:10613902; http://dx.doi.org/10.1083/ jcb.147.7.1431.
9. Gilks N, Kedersha N, Ayodele M, Shen L, Stoecklin G, Dember LM, et al. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 2004; 15:5383-98; PMID:15371533; http://dx.doi. org/10.1091/mbc.E04-08- 0715.
10. Wilczynska A, Aigueperse C, Kress M, Dautry F, Weil D. The translational regulator CPEB1 provides a link between dcp1 bodies and stress granules. J Cell Sci 2005; 118:981-92; PMID:15731006; http://dx.doi. org/10.1242/jcs.01692.
11. Lieb B, Carl M, Hock R, Gebauer D, Scheer U. Identification of a novel mRNA-associated protein in oocytes of Pleurodeles waltl and Xenopus laevis. Exp Cell Res 1998; 245:272-81; PMID:9851867; http://dx.doi. org/10.1006/excr.1998. 4249.
12. Decker CJ, Parker R. CAR-1 and trailer hitch: driving mRNP granule function at the ER? J Cell Biol 2006; 173:159-63; PMID:16636142; http://dx.doi. org/10.1083/jcb.200601153.
13. Marnef A, Sommerville J, Ladomery MR. RAP55: insights into an evolutionarily conserved protein family. Int J Biochem Cell Biol 2009; 41:977-81; PMID:18723115; http://dx.doi.org/10.1016/j.biocel. 2008.06.015.
14. Tanaka KJ, Ogawa K, Takagi M, Imamoto N, Matsumoto K, Tsujimoto M. RAP55, a cytoplasmic mRNP component, represses translation in Xenopus oocytes. J Biol Chem 2006; 281:40096- 106; PMID:17074753; http://dx.doi.org/10.1074/jbc. M609059200.
15. Minshall N, Reiter MH, Weil D, Standart N. CPEB interacts with an ovary-specific eIF4E and 4E-T in early Xenopus oocytes. J Biol Chem 2007; 282:37389-401; PMID:17942399; http://dx.doi.org/10.1074/jbc.M704629200.
16. Arthur PK, Claussen M, Koch S, Tarbashevich K, Jahn O, Pieler T. Participation of Xenopus Elr-type proteins in vegetal mRNA localization during oogenesis. J Biol Chem 2009; 284:19982-92; PMID:19458392; http:// dx.doi.org/10.1074/jbc.M109.009928.
17. Coller J, Parker R. General translational repression by activators of mRNA decapping. Cell 2005; 122:875-86; PMID:16179257; http://dx.doi.org/10.1016/ j.cell.2005.07.012.
18. Andrei MA, Ingelfinger D, Heintzmann R, Achsel T, Rivera-Pomar R, Lührmann R. A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 2005; 11:717-27; PMID:15840819; http://dx.doi.org/10.1261/rna.2340405.
19. Rajyaguru P, Parker R. CGH-1 and the control of maternal mRNAs. Trends Cell Biol 2009; 19:24-8; PMID:19062290; http://dx.doi.org/10.1016/j.tcb.2008.11. 001.
20. Yang WH, Yu JH, Gulick T, Bloch KD, Bloch DB. RNA-associated protein 55 (RAP55) localizes to mRNA processing bodies and stress granules. RNA 2006; 12:547-54; PMID:16484376; http://dx.doi. org/10.1261/rna.2302706.
21. Gache V, Waridel P, Winter C, Juhem A, Schroeder M, Shevchenko A, et al. Xenopus meiotic microtubule- associated interactome. PLoS One 2010; 5:9248; PMID:20174651; http://dx.doi.org/10.1371/journal.pone.0009248.
22. Albrecht M, Lengauer T. Novel Sm-like proteins with long C-terminal tails and associated methyltransferases. FEBS Lett 2004; 569:18-26; PMID:15225602; http://dx.doi.org/10.1016/j.febslet.2004.03.126.
23. Anantharaman V, Aravind L. Novel conserved domains in proteins with predicted roles in eukaryotic cell cycle regulation, decapping and RNA stability. BMC Genomics 2004; 5:45; PMID:15257761; http:// dx.doi.org/10.1186/ 1471-2164-5-45.
24. Tritschler F, Eulalio A, Helms S, Schmidt S, Coles M, Weichenrieder O, et al. Similar modes of interaction enable Trailer Hitch and EDC3 to associate with DCP1 and Me31B in distinct protein complexes. Mol Cell Biol 2008; 28:6695-708; PMID:18765641; http:// dx.doi.org/10.1128/MCB.00759-08.
25. Nissan T, Rajyaguru P, She M, Song H, Parker R. Decapping activators in Saccharomyces cerevisiae act by multiple mechanisms. Mol Cell 2010; 39:773-83; PMID:20832728; http://dx.doi.org/10.1016/j.molcel.2010.08.025.
26. Najbauer J, Johnson BA, Young AL, Aswad DW. Peptides with sequences similar to glycine, argininerich motifs in proteins interacting with RNA are efficiently recognized by methyltransferase(s) modifying arginine in numerous proteins. J Biol Chem 1993; 268:10501-9; PMID:7683681.
27. Wada K, Inoue K, Hagiwara M. Identification of methylated proteins by protein arginine N-methyltransferase 1, PRMT1, with a new expression cloning strategy. Biochim Biophys Acta 2002; 1591:1-10; PMID:12183049; http://dx.doi.org/10.1016/S0167-4889(02)00202-1.
28. Aoki K, Ishii Y, Matsumoto K, Tsujimoto M. Methylation of Xenopus CIRP2 regulates its arginineand glycine-rich region-mediated nucleocytoplasmic distribution. Nucleic Acids Res 2002; 30:5182-92; PMID:12466543; http://dx.doi.org/10.1093/nar/gkf638.
29. Pahlich S, Zakaryan RP, Gehring H. Protein arginine methylation: Cellular functions and methods of analysis. Biochim Biophys Acta 2006; 1764:1890-903; PMID:17010682.
30. Bedford MT, Clarke SG. Protein arginine methylation in mammals: who, what and why. Mol Cell 2009; 33:1-13; PMID:19150423; http://dx.doi.org/10.1016/j. molcel.2008.12.013.
31. Weston A, Sommerville J. Xp54 and related (DDX6- like) RNA helicases: roles in messenger RNP assembly, translation regulation and RNA degradation. Nucleic Acids Res 2006; 34:3082-94; PMID:16769775; http:// dx.doi.org/10.1093/ nar/gkl409.
32. Jud MC, Czerwinski MJ, Wood MP, Young RA, Gallo CM, Bickel JS, et al. Large P body-like RNPs form in C. elegans oocytes in response to arrested ovulation, heat shock, osmotic stress and anoxia and are regulated by the major sperm protein pathway. Dev Biol 2008; 318:38-51; PMID:18439994; http://dx.doi. org/10.1016/j.ydbio.2008.02.059.
33. Tang J, Frankel A, Cook RJ, Kim S, Paik WK, Williams KR, et al. PRMT1 is the predominant type I protein arginine methyltransferase in mammalian cells. J Biol Chem 2000; 275:7723-30; PMID:10713084; http:// dx.doi.org/10.1074/jbc.275. 11.7723.
34. Herrmann F, Lee J, Bedford MT, Fackelmayer FO. Dynamics of human protein arginine methyltransferase 1(PRMT1) in vivo. J Biol Chem 2005; 280:38005- 10; PMID:16159886; http://dx.doi.org/10.1074/jbc.M502458200.
35. Lee J, Bedford MT. PABP1 identified as an arginine methyltransferase substrate using high-density protein arrays. EMBO Rep 2002; 3:268-73; PMID:11850402; http://dx.doi.org/10.1093/embo-reports/kvf052.
36. Pollack BP, Kotenko SV, He W, Izotova LS, Barnoski BL, Pestka S. The human homologue of the yeast proteins Skb1 and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J Biol Chem 1999; 274:31531-42; PMID:10531356; http:// dx.doi.org/10.1074/jbc.274.44.31531.
37. Friesen WJ, Paushkin S, Wyce A, Massenet S, Pesiridis GS, Van Duyne G, et al. The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol Cell Biol 2001; 21:8289-300; PMID:11713266; http://dx.doi. org/10.1128/MCB.21.24.8289-300.2001.
38. Meister G, Eggert C, Bühler D, Brahms H, Kambach C, Fischer U. Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor pICln. Curr Biol 2001; 11:1990-4; PMID:11747828; http://dx.doi.org/10.1016/S0960-9822(01)00592-9.
39. Friesen WJ, Wyce A, Paushkin S, Abel L, Rappsilber J, Mann M, et al. A novel WD repeat protein component of the methylosome binds Sm proteins. J Biol Chem 2002; 277:8243-7; PMID:11756452; http://dx.doi.org/10.1074/jbc.M109984200.
40. Nishioka K, Reinberg D. Methods and tips for the purification of human histone methyltransferases. Methods 2003; 31:49-58; PMID:12893173; http:// dx.doi.org/10.1016/S1046-2023(03)00087-2.
41. Gonzalez J, Besada V, Garay H, Reyes O, Padron G, Tambara Y, et al. Effect of the position of a basic amino acid on C-terminal rearrangement of protonated peptides upon collision-induced dissociation. J Mass Spectrom 1996; 31:150-8; PMID:8799268; http://dx.doi.org/10.1002/(SICI)1096-9888(199602)31: 2<150::AID-JMS287>3.0.CO;2-5.
42. Zou Y, Wang Y. Tandem mass spectrometry for the examination of the posttranslational modifications of high-mobility group A1 proteins: symmetric and asymmetric dimethylation of Arg25 in HMGA1a protein. Biochemistry 2005; 44:6293-301; PMID:15835918; http://dx.doi.org/10.1021/bi0475525.
43. Noble SL, Allen BL, Goh LK, Nordick K, Evans TC. Maternal mRNAs are regulated by diverse P body-related mRNP granules during early Caenorhabditis elegans development. J Cell Biol 2008; 182:559-72; PMID:18695046; http://dx.doi.org/10.1083/jcb.200802128.
44. Lacroix M, El Messaoudi S, Rodier G, Le Cam A, Sardet C, Fabbrizio E. The histone-binding protein COPR5 is required for nuclear functions of the protein arginine methyltransferase PRMT5. EMBO Rep 2008; 9:452-8; PMID:18404153; http://dx.doi.org/10.1038/embor.2008.45.
45. Dolzhanskaya N, Merz G, Aletta JM, Denman RB. Methylation regulates the intracellular protein-protein and protein-RNA interactions of FMRP. J Cell Sci 2006; 119:1933-46; PMID:16636078; http://dx.doi.org/10.1242/jcs.02882.
46. Anne J, Mechler BM. Valois, a component of the nuage and pole plasm, is involved in assembly of these structures, and binds to Tudor and the methyltransferase Capsuléen. Development 2005; 132:2167-77; PMID:15800004; http://dx.doi.org/10.1242/ dev.01809.
47. Cavey M, Hijal S, Zhang X, Suter B. Drosophila valois encodes a divergent WD protein that is required for Vasa localization and Oskar protein accumulation. Development 2005; 132:459-68; PMID:15634703; http://dx.doi.org/10. 1242/dev.01590.
48. Anne J, Ollo R, Ephrussi A, Mechler BM. Arginine methyltransferase Capsuleen is essential for methylation of spliceosomal Sm proteins and germ cell formation in Drosophila. Development 2007; 134:137-46; PMID:17164419; http://dx.doi.org/10.1242/dev.02687.
49. Decker CJ, Teixeira D, Parker R. Edc3p and a glutamine/ asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J Cell Biol 2007; 179:437-49; PMID:17984320; http:// dx.doi.org/10.1083/jcb.200704147.
50. Reijns MA, Alexander RD, Spiller MP, Beggs JD. A role for Q/N-rich aggregation-prone regions in P-body localization. J Cell Sci 2008; 121:2463-72; PMID:18611963; http://dx.doi.org/10.1242/jcs.024976.
51. Fenger-Grøn M, Fillman C, Norrild B, Lykke- Andersen J. Multiple processing body factors and the ARE binding protein TTP activate mRNA decapping. Mol Cell 2005; 20:905-15; PMID:16364915; http:// dx.doi.org/10.1016/j.molcel. 2005.10.031.
52. Tritschler F, Eulalio A, Truffault V, Hartmann MD, Helms S, Schmidt S, et al. A divergent Sm fold in EDC3 proteins mediates DCP1 binding and P-body targeting. Mol Cell Biol 2007; 27:8600-11; PMID:17923697; http://dx.doi.org/10. 1128/MCB.01506-07
53. Tay WL, Yip GW, Tan PH, Matsumoto K, Yeo R, Ng TP, et al. Y-Box-binding protein-1 is a promising predictive marker of radioresistance and chemoradioresistance in nasopharyngeal cancer. Mod Pathol 2009; 22:282-90; PMID:18978732; http://dx.doi. org/10.1038/modpathol.2008.181.
54. Suzuki Y, Minami M, Suzuki M, Abe K, Zenno S, Tsujimoto M, et al. The Hsp90 inhibitor geldanamycin abrogates colocalization of eIF4E and eIF4Etransporter into stress granules and association of eIF4E with eIF4G. J Biol Chem 2009; 284:35597-604; PMID:19850929; http://dx.doi.org/10.1074/jbc. M109.036285.
55. Matsumoto K, Tanaka KJ, Tsujimoto M. An acidic protein, YBAP1, mediates the release of YB-1 from mRNA and relieves the translational repression activity of YB-1. Mol Cell Biol 2005; 25:1779-92; PMID:15713634; http://dx.doi.org/10. 1128/MCB.25.5.1779-92.2005.
56. Matsumoto K, Nagata K, Miyaji-Yamaguchi M, Kikuchi A, Tsujimoto M. Sperm chromatin decondensation by template activating factor I through direct interaction with basic proteins. Mol Cell Biol 1999; 19:6940-52; PMID:10490631.
57. Wagner S, Weber S, Kleinschmidt MA, Nagata K, Bauer UM. SET-mediated promoter hypoacetylation is a prerequisite for coactivation of the estrogenresponsive pS2 gene by PRMT1. J Biol Chem 2006; 281:27242-50; PMID:16861234; http://dx.doi. org/10.1074/jbc.M605172200.
58. Teyssier C, Ma H, Emter R, Kralli A, Stallcup MR. Activation of nuclear receptor coactivator PGC-1alpha by arginine methylation. Genes Dev 2005; 19:1466-73; PMID:15964996; http://dx.doi.org/10.1101/gad.1295005.
59. Kawahara H, Imai T, Imataka H, Tsujimoto M, Matsumoto K, Okano H. Neural RNA-binding protein Musashi1 inhibits translation initiation by competing with eIF4G for PABP. J Cell Biol 2008; 181:639-53; PMID:18490513; http://dx.doi.org/10.1083/jcb.200708004.
60. Masuda A, Dohmae N. Automated Protein Hydrolysis Delivering Sample to a Solid Acid Catalyst for Amino Acid Analysis. Anal Chem 2010; 82:8939-45; PMID:20923146; http://dx.doi.org/10.1021/ac101718x.
61. Masuda A, Dohmae N. Amino acid analysis of sub-picomolar amounts of proteins by precolumn fluorescence derivatization with 6-aminoquinolyl- Nhydroxysuccinimidyl carbamate. Biosci Trends 2011; 5:231-8; PMID:22281536; http://dx.doi.org/10.5582/bst.2011.v5.6.231.
62. Kodama K, Fukuzawa S, Nakayama H, Kigawa T, Sakamoto K, Yabuki T, et al. Regioselective carbon-carbon bond formation in proteins with palladium catalysis; new protein chemistry by organometallic chemistry. Chembiochem 2006; 7:134-9; PMID:16307466; http://dx.doi.org/10.1002/cbic.200500290.
63. Park N, Katikaneni P, Skern T, Gustin KE. Differential targeting of nuclear pore complex proteins in poliovirus-infected cells. J Virol 2008; 82:1647-55; PMID:18045934; http://dx.doi.org/10.1128/JVI.01670-07.
64. Piotrowska J, Hansen SJ, Park N, Jamka K, Sarnow P, Gustin KE. Stable formation of compositionally unique stress granules in virus-infected cells. J Virol 2010; 84:3654-65; PMID:20106928; http://dx.doi.org/10.1128/JVI.01320-09.