Different methylation characteristics of protein arginine methyltransferase 1 and 3 toward the Ewing Sarcoma protein and a peptide

Proteins: Structure, Function and Genetics

Volumn 61, Issue 1, 2005, Pages 164-175

  Pahlich, Steffen ^a   Bschir, Karim ^a   Chiavi, Claudio ^a   Belyanskaya, Larisa ^a,b   Gehring, Heinz ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

AdoHcy inhibition; Asymmetric dimethylation of arginine residues; MALDI TOF MS; MS MS; Posttranslational modification; RNA binding protein

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; RNA BINDING PROTEIN; RNA BINDING PROTEIN EWS; S ADENOSYLHOMOCYSTEINE;

ARTICLE; CONSENSUS SEQUENCE; ENZYME SPECIFICITY; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METHYLATION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN PROCESSING; PROTEIN RNA BINDING; QUANTITATIVE ANALYSIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; TANDEM MASS SPECTROMETRY;

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; KINETICS; METHYLATION; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN-ARGININE N-METHYLTRANSFERASE; RECOMBINANT PROTEINS; RNA-BINDING PROTEIN EWS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 24344468254     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20579     Document Type: Article

References (42)

1. Lee HW, Kim S, Paik WK. S-adenosylmethionine: protein-arginine methyltransferase. Purification and mechanism of the enzyme. Biochemistry 1977;16:78-85.
2. Flach J, Bossie M, Vogel J, Corbett A, Jinks T, Willins DA, Silver PA. A yeast RNA-binding protein shuttles between the nucleus and the cytoplasm. Mol Cell Biol 1994;14:8399-8407.
3. Shen EC, Henry MF, Weiss VH, Valentini SR, Silver PA, Lee MS. Arginine methylation facilitates the nuclear export of hnRNP proteins. Genes Dev 1998;12:679-691.
4. Mowen K, David M. Response to matters arising. Cell 2004;119: 589-590.
5. Meissner T, Krause E, Lodige I, Vinkemeier U. Arginine methylation of STAT1: a reassessment. Cell 2004;119:587-590.
6. Rajpurohit R, Paik WK, Kim S. Effect of enzymatic methylation of heterogeneous ribonucleoprotein particle A1 on its nucleic-acid binding and controlled proteolysis. Biochem J 1994;304:903-909.
7. Klein S, Carroll JA, Chen Y, Henry MF, Henry PA, Ortonowski IE, Pintucci G, Beavis RC, Burgess WH, Rifkin DB. Biochemical analysis of the arginine methylation of high molecular weight fibroblast growth factor-2. J Biol Chem 2000;275:3150-3157.
8. Gary JD, Clarke S. RNA and protein interactions modulated by protein arginine methylation. Prog Nucleic Acid Res Mol Biol 1998;61:65-131.
9. Gary JD, Lin WJ, Yang MC, Herschman HR, Clarke S. The predominant protein-arginine methyltransferase from Saccharomyces cerevisiae. J Biol Chem 1996;271:12585-12594.
10. Lin WJ, Gary JD, Yang MC, Clarke S, Herschman HR. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J Biol Chem 1996;271:15034-15044.
11. Tang J, Gary JD, Clarke S, Herschman HR. 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 1998;273:16935-16945.
12. Chen D, Ma H, Hong H, Koh SS, Huang SM, Schurter BT, Aswad DW, Stallcup MR. Regulation of transcription by a protein methyltransferase. Science 1999;284:2174-2177.
13. Frankel A, Yadav N, Lee J, Branscombe TL, Clarke S, Bedford MT. The novel human protein arginine N-methyltransferase PRMT6 is a nuclear enzyme displaying unique substrate specificity. J Biol Chem 2002;277:3537-3543.
14. Branscombe TL, Frankel A, Lee JH, Cook JR, Yang Z, Pestka S, Clarke S. PRMT5 (Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J Biol Chem 2001;276:32971-32976.
15. Lee JH, Cook JR, Yang ZH, Mirochnitchenko O, Gunderson S, Felix AM, Herth N, Hoffmann R, Pestka S. PRMT7: a new protein arginine methyltransferase that synthesizes symmetric dimethyl-arginine. J Biol Chem 2005;280:3656-3664.
16. Baldwin GS, Carnegie PR. Specific enzymic methylation of an arginine in the experimental allergic encephalomyelitis protein from human myelin. Science 1971;171:579-581.
17. Friesen WJ, Paushkin S, Wyce A, Massenet S, Pesiridis GS, Van Duyne G, Rappsilber J, Mann M, Dreyfuss G. The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol Cell Biol 2001;21:8289-8300.
18. Tang J, Frankel A, Cook RJ, Kim S, Paik WK, Williams KR, Clarke S, Herschman HR. PRMT1 is the predominant type I protein arginine methyltransferase in mammalian cells. J Biol Chem 2000;275:7723-7730.
19. Bachand F, Silver PA. PRMT3 is a ribosomal protein methyltransferase that affects the cellular levels of ribosomal subunits. Embo J 2004;23:2641-2650.
20. Belyanskaya LL, Gehrig PM, Gehring H. Exposure on cell surface and extensive arginine methylation of ewing sarcoma (EWS) protein. J Biol Chem 2001;276:18681-18687.
21. Arvand A, Denny CT. Biology of EWS/ETS fusions in Ewing's family tumors. Oncogene 2001;20:5747-5754.
22. Plougastel B, Zucman J, Peter M, Thomas G, Delattre O. Genomic structure of the EWS gene and its relationship to EWSR1, a site of tumor-associated chromosome translocation. Genomics 1993;18: 609-615.
23. Delattre O, Zucman J, Plougastel B, Desmaze C, Melot T, Peter M, Kovar H, Joubert I, Dejong P, Rouleau G, and others. Gene fusion with an Ets DNA-binding domain caused by chromosome-translocation in human tumors. Nature 1992;359:162-165.
24. Rossow KL, Janknecht R. The Ewing's sarcoma gene product functions as a transcriptional activator. Cancer Res 2001;61:2690-2695.
25. Li KKC, Lee KAW. Transcriptional activation by the Ewing's sarcoma (EWS) oncogene can be cis-repressed by the EWS RNA-binding domain. J Biol Chem 2000;275:23053-23058.
26. Kzhyshkowska J, Schutt H, Liss M, Kremmer E, Staubert R, Wolf H, Dobner T. Heterogeneous nuclear ribonucleoprotein E1B-AP5 is methylated in its Arg-Gly-Gly (RGG) box and interacts with human arginine methyltransferase HRMT1L1. Biochem J 2001; 358:305-314.
27. Weighardt F, Biamonti G, Riva S. Nucleocytoplasmic distribution of human Hnrnp proteins-a search for the targeting domains in Hnrnp A1. J Cell Sci 1995;108:545-555.
28. Zamore PD, Patton JG, Green MR. Cloning and domain-structure of the mammalian splicing factor U2af. Nature 1992;355:609-614.
29. Krainer AR, Mayeda A, Kozak D, Binns G. Functional expression of cloned human splicing factor Sf2-homology to RNA-binding proteins, U1-70k, and Drosophila splicing regulators. Cell 1991;66: 383-394.
30. Belyanskaya LL, Delattre O, Gehring H. Expression and subcellular localization of Ewing sarcoma (EWS) protein is affected by the methylation process. Exp Cell Res 2003;288:374-381.
31. Zhen Y, Xu N, Richardson B, Becklin R, Savage JR, Blake K, Peltier JM. Development of an LC-MALDI method for the analysis of protein complexes. J Am Soc Mass Spectrom 2004;15:803-822.
32. Gehrig PM, Hunziker PE, Zahariev S, Pongor S. Fragmentation pathways of N(G)-methylated and unmodified arginine residues in peptides studied by ESI-MS/MS and MALDI-MS. J Am Soc Mass Spectrom 2004;15:142-149.
33. Rappsilber J, Friesen WJ, Paushkin S, Dreyfuss G, Mann M. Detection of arginine dimethylated peptides by parallel precursor ion scanning mass spectrometry in positive ion mode. Anal Chem 2003;75:3107-3114.
34. Merrill BM, Lopresti MB, Stone KL, Williams KR. Amino acid sequence of UP1, an hnRNP-derived single-stranded nucleic acid binding protein from calf thymus. Int J Pept Protein Res 1987;29: 21-39.
35. Liu Q, Dreyfuss G. In vivo and in vitro arginine methylation of RNA-binding proteins. Mol Cell Biol 1995;15:2800-2808.
36. Frankel A, Clarke S. PRMT3 is a distinct member of the protein arginine N-methyltransferase family. Conferral of substrate specificity by a zinc-finger domain. J Biol Chem 2000;275:32974-32982.
37. Mackay JP, Crossley M. Zinc fingers are sticking together. Trends Biochem Sci 1998;23:1-4.
38. Brahms H, Meheus L, de Brabandere V, Fischer U, Luhrmann R. Symmetrical dimethylation of arginine residues in spliceosomal Sm protein B/B′ and the Sm-like protein LSm4, and their interaction with the SMN protein. RNA 2001;7:1531-542.
39. Chevillard-Briet M, Trouche D, Vandel L. Control of CBP coactivating activity by arginine methylation. EMBO J 2002;21: 5457-5466.
40. Cote J, Boisvert FM, Boulanger MC, Bedford MT, Richard S. Sam68 RNA binding protein is an in vivo substrate for protein arginine N-methyltransferase 1. Mol Biol Cell 2003;14:274-287.
41. Xu C, Henry MF. Nuclear export of hnRNP Hrp1p and nuclear export of hnRNP Np13p are linked and influenced by the methylation state of Np13p. Mol Cell Biol 2004;24:10742-10756.
42. Smith WA, Schurter BT, Wong-Staal F, David M. Arginine methylation of RNA helicase a determines its subcellular localization. J Biol Chem 2004;279:22795-22798.