Methylation of SPT5 regulates its interaction with RNA polymerase II and transcriptional elongation properties

Molecular Cell

Volumn 11, Issue 4, 2003, Pages 1055-1066

  Kwak, Youn Tae ^a   Guo, Jun ^a   Prajapati, Shashi ^a   Park, Kyu Jin ^a   Surabhi, Rama M ^a   Miller, Brady ^a   Gehrig, Peter ^b   Gaynor, Richard B ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; PROTEIN ARGININE METHYLTRANSFERASE; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SPT5; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME KINETICS; FEMALE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MASS SPECTROMETRY; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN RNA BINDING; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 0037623333     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00101-1     Document Type: Article

References (51)

1. Andrulis E.D., Guzman E., Doring P., Werner J., Lis J.T. High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo. roles in promoter proximal pausing and transcription elongation Genes Dev. 14:2000;2635-2649.
2. Bannister A.J., Schneider R., Kouzarides T. Histone methylation. dynamic or static? Cell. 109:2002;801-806.
3. Barboric M., Nissen R.M., Kanazawa S., Jabrane-Ferrat N., Peterlin B.M. NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol. Cell. 8:2001;327-337.
4. Belyanskaya L.L., Gehrig P.M., Gehring H. Exposure on cell surface and extensive arginine methylation of ewing sarcoma (EWS) protein. J. Biol. Chem. 276:2001;18681-18687.
5. Bourgeois C.F., Kim Y.K., Churcher M.J., West M.J., Karn J. Spt5 cooperates with human immunodeficiency virus type 1 Tat by preventing premature RNA release at terminator sequences. Mol. Cell. Biol. 22:2002;1079-1093.
6. Brahms H., Mehens L., DeBrabandere L., Fisher 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. 7:2001;1531-1542.
7. Branscombe T.L., Frankel A., Lee J.H., Cook J.R., Yang Zh Z., Pestka S., Clarke S. PRMT5 (the Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J. Biol. Chem. 18:2001;32971-32976.
8. Chen D., Ma H., Hong H., Koh S.S., Huang S.M., Schurter B.T., Aswad D.W., Stallcup M.R. Regulation of transcription by a protein methyltransferase. Science. 284:1999;2174-2177.
9. Fabbrizio E., El Messaoudi S., Polanowska J., Paul C., Cook J.R., Lee J.H., Negre V., Rousset M., Pestka S., Le Cam A.et al. Negative regulation of transcription by the type II arginine methyltransferase PRMT5. EMBO Rep. 3:2002;641-645.
10. Frankel A., Yadav N., Lee J., Branscombe T.L., Clarke S., Bedford M.T. The novel human protein arginine N-methyltransferase PRMT6 is a nuclear enzyme displaying unique substrate specificity. J. Biol. Chem. 277:2002;3537-3543.
11. Friesen W.J., Paushkin S., Wyce A., Massenet S., Pesiridis G.S., 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. 21:2001;8289-8300.
12. Gary J.D., Clarke S. RNA and protein interactions modulated by protein arginine methylation. Prog. Nucleic Acid Res. Mol. Biol. 61:1998;65-131.
13. Gatlin C.L., Kleemann G.R., Hays L.G., Link A.J., Yates J.R. III. Protein identification at the low femtomole level from silver-stained gels using a new fritless electrospray interface for liquid chromatography-microspray and nanospray mass spectrometry. Anal. Biochem. 263:1998;93-101.
14. Guo S., Yamaguchi Y., Schilbach S., Wada T., Lee J., Goddard A., French D., Handa H., Rosenthal A. A regulator of transcriptional elongation controls vertebrate neuronal development. Nature. 408:2000;366-369.
15. Hartzog G.A., Wada T., Handa H., Winston F. Evidence that Spt4, Spt5, and Spt6 control transcription elongation by RNA polymerase II in Saccharomyces cerevisiae. Genes Dev. 12:1998;357-369.
16. Isomura M., Okui K., Fujiwara T., Shin S., Nakamura Y. Cloning and mapping of a novel human cDNA homologous to DROER, the enhancer of the Drosophila melanogaster rudimentary gene. Genomics. 32:1996;125-127.
17. Ivanov D., Kwak Y.T., Guo J., Gaynor R.B. Domains in the SPT5 protein that modulate its transcriptional regulatory properties. Mol. Cell. Biol. 20:2000;2970-2983.
18. Kaplan C.D., Morris J.R., Wu C., Winston F. Spt5 and spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster. Genes Dev. 14:2000;2623-2634.
19. Karn J. Tackling Tat. J. Mol. Biol. 293:1999;235-254.
20. Keegan B.R., Feldman J.L., Lee D.H., Koos D.S., Ho R.K., Stainier D.Y.R., Yelon D. The elongation factors Pandora/SPT6 and Foggy/SPT5 promote transcription in the zebrafish embryo. Development. 129:2002;1623-1632.
21. Kim J.B., Sharp P.A. Positive transcription elongation factor B phosphorylates hSPT5 and RNA polymerase II carboxyl-terminal domain independently of cyclin-dependent kinase-activating kinase. J. Biol. Chem. 276:2001;12317-12323.
22. Kim J.B., Yamaguchi Y., Wada T., Handa H., Sharp P.A. Tat-SF1 protein associates with RAP30 and human SPT5 proteins. Mol. Cell. Biol. 19:1999;5960-5968.
23. Lin W.J., Gary J.D., Yang M.C., Clarke S., Herschman H.R. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J. Biol. Chem. 271:1996;15034-15044.
24. McBride A.E., Silver P.A. State of the arg. protein methylation at arginine comes of age Cell. 106:2001;5-8.
25. McBride A.E., Weiss V.H., Kim H.K., Hogle J.M., Silver P.A. Analysis of the yeast arginine methyltransferase Hmt1p/Rmt1p and its in vivo function. Cofactor binding and substrate interactions. J. Biol. Chem. 275:2000;3128-3136.
26. Mowen K.A., Tang J., Zhu W., Schurter B.T., Shuai K., Herschman H.R., David M. Arginine methylation of STAT1 modulates IFNalpha/beta-induced transcription. Cell. 104:2001;731-741.
27. Orphanides G., Reinberg D. A unified theory of gene expression. Cell. 108:2002;439-451.
28. Parada C.A., Roeder R.G. A novel RNA polymerase II-containing complex potentiates Tat-enhanced HIV-1 transcription. EMBO J. 18:1999;3688-3701.
29. Pokholok D.K., Hannett N.M., Young R.A. Exchange of RNA polymerase II Initiation and elongation factors during gene expression in vivo. Mol. Cell. 9:2002;799-809.
30. Pollack B.P., Kotenko S.V., He W., Izotova L.S., Barnoski B.L., Pestka S. The human homologue of the yeast proteins Skb1 and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J. Biol. Chem. 274:1999;31531-31542.
31. Ponting C.P. Novel domains and orthologues of eukaryotic transcription elongation factors. Nucleic Acids Res. 17:2002;3643-3652.
32. Qi C., Chang J., Zhu Y., Yeldandi A.V., Rao S.M., Zhu Y.J. Identification of protein arginine methyltransferase 2 as a coactivator for estrogen receptor alpha. J. Biol. Chem. 277:2002;28624-28630.
33. Rho J., Choi S., Seong Y.R., Cho W.K., Kim S.H., Im D.S. Prmt5, which forms distinct homo-oligomers, is a member of the protein-arginine methyltransferase family. J. Biol. Chem. 276:2001;11393-11401.
34. Shim E.Y., Walker A.K., Shi Y., Blackwell T.K. CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C-elegans embryo. Genes Dev. 16:2002;2135-2146.
35. Squazzo S.L., Costa P.J., Lindstrom D.L., Kumer K.E., Simic R.R., Jennings J.L., Link A.J., Arndt K.M., Hartzog G.A. The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J. 7:2002;1764-1774.
36. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature. 403:2000;41-45.
37. Strahl B.D., Briggs S.D., Brame C.J., Caldwell J.A., Koh S.S., Ma H., Cook R.G., Shabanowitz J., Hunt D.F., Stallcup M.R.et al. Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr. Biol. 11:2001;996-1000.
38. Tang J., Gary J.D., Clarke S., Herschman H.R. 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. 273:1998;16935-16945.
39. Tang J., Frankel A., Cook R.J., Kim S., Paik W.K., Williams K.R., Clarke S., Herschman H.R. PRMT1 is the predominant type I protein arginine methyltransferase in mammalian cells. J. Biol. Chem. 275:2000;7723-7730.
40. Wada T., Takagi T., Yamaguchi Y., Ferdous A., Imai T., Hirose S., Sugimoto S., Yano K., Hartzog G.A., Winston F.et al. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev. 12:1998;343-356. a.
41. Wada T., Takagi T., Yamaguchi Y., Watanabe D., Handa H. Evidence that P-TEFb alleviates the negative effect of DSIF on RNA polymerase II-dependent transcription in vitro. EMBO J. 17:1998;7395-7403. b.
42. Wada T., Orphanides G., Hasegawa J., Kim D.K., Shima D., Yamaguchi Y., Fukuda A., Hisatake K., Oh S., Reinberg D.et al. FACT relieves DSIF/NELF-mediated inhibition of transcriptional elongation and reveals functional differences between P-TEFb and TFIIH. Mol. Cell. 5:2000;1067-1072.
43. Wang H., Huang Z.Q., Xia L., Feng Q., Erdjument-Bromage H., Strahl B.D., Briggs S.D., Allis C.D., Wong J., Tempst P.et al. Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science. 293:2001;853-857.
44. Wen Y., Shatkin A.J. Transcription elongation factor hSPT5 stimulates mRNA capping. Genes Dev. 13:1999;1774-1779.
45. Wu-Baer F., Lane W.S., Gaynor R.B. Role of the human homolog of the yeast transcription factor SPT5 in HIV- 1 Tat-activation. J. Mol. Biol. 277:1998;179-197.
46. Xu W., Chen H., Du K., Asahara H., Tini M., Emerson B.M., Montminy M., Evans R.M. A transcriptional switch mediated by cofactor methylation. Science. 294:2001;2507-2511.
47. Yamaguchi Y., Takagi T., Wada T., Yano K., Furuya A., Sugimoto S., Hasegawa J., Handa H. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell. 97:1999;41-51. a.
48. Yamaguchi Y., Wada T., Watanabe D., Takagi T., Hasegawa J., Handa H. Structure and function of the human transcription elongation factor DSIF. J. Biol. Chem. 274:1999;8085-8092. b.
49. Yamaguchi Y., Inukai N., Narita T., Wada T., Handa H. Evidence that negative elongation factor represses transcription elongation through binding to a DRB sensitivity-inducing factor/RNA polymerase II complex and RNA. Mol. Cell. Biol. 22:2002;2918-2927.
50. Zhang Y., Reinberg D. Transcription regulation by histone methylation. interplay between different covalent modifications of the core histone tails Genes Dev. 15:2001;2343-2360.
51. Zhou M., Halanski M.A., Radonovich M.F., Kashanchi F., Peng J., Price D.H., Brady J.N. Tat modifies the activity of CDK9 to phosphorylate serine 5 of the RNA polymerase II carboxyl-terminal domain during human immunodeficiency virus type 1 transcription. Mol. Cell. Biol. 14:2000;5077-5086.