Arginine methylation initiates BMP-induced Smad signaling

Molecular Cell

Volumn 51, Issue 1, 2013, Pages 5-19

  Xu, Jian ^a   Wang, A Hongjun ^a,c   Oses Prieto, Juan ^a   Makhijani, Kalpana ^a   Katsuno, Yoko ^a   Pei, Ming ^a   Yan, Leilei ^b   Zheng, Y George ^b   Burlingame, Alma ^a   Brückner, Katja ^a   Derynck, Rik ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; BONE MORPHOGENETIC PROTEIN; METHYLTRANSFERASE; PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN DART1; SMAD PROTEIN; SMAD6 PROTEIN; UNCLASSIFIED DRUG; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; PRMT1 PROTEIN, HUMAN; REPRESSOR PROTEIN; SMAD6 PROTEIN, HUMAN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; FORELIMB; GENE EXPRESSION; METHYLATION; MOLECULAR BIOLOGY; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; CELL LINE; CHEMISTRY; HEK293 CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; CELL STRAIN HEK293;

ARGININE; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; BONE MORPHOGENETIC PROTEINS; CELL LINE; HEK293 CELLS; HUMANS; METHYLATION; PHOSPHORYLATION; PROTEIN-ARGININE N-METHYLTRANSFERASES; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD6 PROTEIN;

EID: 84891674956     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.05.004     Document Type: Article

References (42)

1. Affolter M., Basler K. The Decapentaplegic morphogen gradient: from pattern formation to growth regulation. Nat. Rev. Genet. 2007, 8:663-674.
2. Bedford M.T., Richard S. Arginine methylation an emerging regulator of protein function. Mol. Cell 2005, 18:263-272.
3. Bedford M.T., Clarke S.G. Protein arginine methylation in mammals: who, what, and why. Mol. Cell 2009, 33:1-13.
4. Bicker K.L., Obianyo O., Rust H.L., Thompson P.R. A combinatorial approach to characterize the substrate specificity of protein arginine methyltransferase 1. Mol. Biosyst. 2011, 7:48-51.
5. Blair S.S. Wing vein patterning in Drosophila and the analysis of intercellular signaling. Annu. Rev. Cell Dev. Biol. 2007, 23:293-319.
6. Boulanger M.C., Miranda T.B., Clarke S., Di Fruscio M., Suter B., Lasko P., Richard S. Characterization of the Drosophila protein arginine methyltransferases DART1 and DART4. Biochem. J. 2004, 379:283-289.
7. Chen Y.G., Liu F., Massague J. Mechanism of TGFbeta receptor inhibition by FKBP12. EMBO J. 1997, 16:3866-3876.
8. Ehrlich M., Horbelt D., Marom B., Knaus P., Henis Y.I. Homomeric and heteromeric complexes among TGF-β and BMP receptors and their roles in signaling. Cell. Signal. 2011, 23:1424-1432.
9. Feng X.H., Derynck R. Specificity and versatility in tgf-β signaling through Smads. Annu. Rev. Cell Dev. Biol. 2005, 21:659-693.
10. Goulet I., Gauvin G., Boisvenue S., Côté J. Alternative splicing yields protein arginine methyltransferase 1 isoforms with distinct activity, substrate specificity, and subcellular localization. J.Biol. Chem. 2007, 282:33009-33021.
11. Gromova K.V., Friedrich M., Noskov A., Harms G.S. Visualizing Smad1/4 signaling response to bone morphogenetic protein-4 activation by FRET biosensors. Biochim. Biophys. Acta 2007, 1773:1759-1773.
12. Hanyu A., Ishidou Y., Ebisawa T., Shimanuki T., Imamura T., Miyazono K. The N domain of Smad7 is essential for specific inhibition of transforming growth factor-beta signaling. J.Cell Biol. 2001, 155:1017-1027.
13. Herrmann F., Fackelmayer F.O. Nucleo-cytoplasmic shuttling of protein arginine methyltransferase 1 (PRMT1) requires enzymatic activity. Genes Cells 2009, 14:309-317.
14. Holt L.J., Tuch B.B., Villén J., Johnson A.D., Gygi S.P., Morgan D.O. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 2009, 325:1682-1686.
15. Huang B., Yang X.D., Lamb A., Chen L.F. Posttranslational modifications of NF-kappaB: another layer of regulation for NF-kappaB signaling pathway. Cell. Signal. 2010, 22:1282-1290.
16. Ichijo T., Voutetakis A., Cotrim A.P., Bhattachryya N., Fujii M., Chrousos G.P., Kino T. The Smad6-histone deacetylase 3 complex silences the transcriptional activity of the glucocorticoid receptor: potential clinical implications. J.Biol. Chem. 2005, 280:42067-42077.
17. Imamura T., Takase M., Nishihara A., Oeda E., Hanai J., Kawabata M., Miyazono K. Smad6 inhibits signalling by the TGF-β superfamily. Nature 1997, 389:622-626.
18. Inamitsu M., Itoh S., Hellman U., Ten Dijke P., Kato M. Methylation of Smad6 by protein arginine N-methyltransferase 1. FEBS Lett. 2006, 580:6603-6611.
19. Ismail M.A., Brun R., Easterbrook J.D., Tanious F.A., Wilson W.D., Boykin D.W. Synthesis and antiprotozoal activity of aza-analogues of furamidine. J.Med. Chem. 2003, 46:4761-4769.
20. Jeon H.S., Dracheva T., Yang S.H., Meerzaman D., Fukuoka J., Shakoori A., Shilo K., Travis W.D., Jen J. SMAD6 contributes to patient survival in non-small cell lung cancer and its knockdown reestablishes TGF-beta homeostasis in lung cancer cells. Cancer Res. 2008, 68:9686-9692.
21. Katagiri T., Suda T., Miyazono K. The bone morphogenetic proteins. The TGF-β Family 2008, 121-150. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. R. Derynck, K. Miyazono (Eds.).
22. Lemmon M.A., Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010, 141:1117-1134.
23. Levy D., Kuo A.J., Chang Y., Schaefer U., Kitson C., Cheung P., Espejo A., Zee B.M., Liu C.L., Tangsombatvisit S., et al. Lysine methylation of the NF-κB subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NF-κB signaling. Nat. Immunol. 2011, 12:29-36.
24. Lin X., Liang Y.Y., Sun B., Liang M., Shi Y., Brunicardi F.C., Shi Y., Feng X.H. Smad6 recruits transcription corepressor CtBP to repress bone morphogenetic protein-induced transcription. Mol. Cell. Biol. 2003, 23:9081-9093.
25. Lu T., Jackson M.W., Wang B., Yang M., Chance M.R., Miyagi M., Gudkov A.V., Stark G.R. Regulation of NF-kappaB by NSD1/FBXL11-dependent reversible lysine methylation of p65. Proc. Natl. Acad. Sci. USA 2010, 107:46-51.
26. Mantri M., Loik N.D., Hamed R.B., Claridge T.D., McCullagh J.S., Schofield C.J. The 2-oxoglutarate-dependent oxygenase JMJD6 catalyses oxidation of lysine residues to give 5S-hydroxylysine residues. ChemBioChem 2011, 12:531-534.
27. Margueron R., Reinberg D. Chromatin structure and the inheritance of epigenetic information. Nat. Rev. Genet. 2010, 11:285-296.
28. Massagué J., Seoane J., Wotton D. Smad transcription factors. Genes Dev. 2005, 19:2783-2810.
29. Miyazono K. Regulation of TGF-β family signaling by inhibitory Smads. The TGF-β Family 2008, 363-388. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. R. Derynck, K. Miyazono (Eds.).
30. Miyazono K., Miyazawa K. Id: a target of BMP signaling. Sci. STKE 2002, 2002:pe40.
31. Miyazono K., Kamiya Y., Morikawa M. Bone morphogenetic protein receptors and signal transduction. J.Biochem. 2010, 147:35-51.
32. O'Connor M.B., Umulis D., Othmer H.G., Blair S.S. Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 2006, 133:183-193.
33. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 2005, 5:375-386.
34. Shi Y., Whetstine J.R. Dynamic regulation of histone lysine methylation by demethylases. Mol. Cell 2007, 25:1-14.
35. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., Casero R.A., Shi Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
36. Shuai K., Ziemiecki A., Wilks A.F., Harpur A.G., Sadowski H.B., Gilman M.Z., Darnell J.E. Polypeptide signalling to the nucleus through tyrosine phosphorylation of Jak and Stat proteins. Nature 1993, 366:580-583.
37. Smith F.D., Langeberg L.K., Cellurale C., Pawson T., Morrison D.K., Davis R.J., Scott J.D. AKAP-Lbc enhances cyclic AMP control of the ERK1/2 cascade. Nat. Cell Biol. 2010, 12:1242-1249.
38. Tsuneizumi K., Nakayama T., Kamoshida Y., Kornberg T.B., Christian J.L., Tabata T. Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature 1997, 389:627-631.
39. Wartlick O., Mumcu P., Jülicher F., Gonzalez-Gaitan M. Understanding morphogenetic growth control-lessons from flies. Nat. Rev. Mol. Cell Biol. 2011, 12:594-604.
40. Webby C.J., Wolf A., Gromak N., Dreger M., Kramer H., Kessler B., Nielsen M.L., Schmitz C., Butler D.S., Yates J.R., et al. Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing. Science 2009, 325:90-93.
41. Wooderchak W.L., Zang T., Zhou Z.S., Acuña M., Tahara S.M., Hevel J.M. Substrate profiling of PRMT1 reveals amino acid sequences that extend beyond the "RGG" paradigm. Biochemistry 2008, 47:9456-9466.
42. Yamagata K., Daitoku H., Takahashi Y., Namiki K., Hisatake K., Kako K., Mukai H., Kasuya Y., Fukamizu A. Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol. Cell 2008, 32:221-231.