Kinetic mechanism of protein arginine methyltransferase

Biochemistry

Volumn 47, Issue 39, 2008, Pages 10420-10427

  Obianyo, Obiamaka ^a   Osborne, Tanesha C ^a   Thompson, Paul R ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CATALYSTS; CHEMOTHERAPY; CHLORINE COMPOUNDS; ENZYMES; FOOD ADDITIVES; MACHINE DESIGN; MECHANISMS; PROTEINS;

ARGININE RESIDUES; CATALYTIC MECHANISMS; HEART DISEASES; HISTONE H4; IN-VIVO; INITIAL VELOCITIES; KINETIC MECHANISMS; METHYLTRANSFERASES; POTENT INHIBITORS; PROTEIN ARGININE; PROTEIN-ARGININE METHYLTRANSFERASE; RAPID EQUILIBRIUM;

AMINO ACIDS;

ARGININE; HISTONE H4; ISOENZYME; N(G),N(G) DIMETHYLARGININE; NITRIC OXIDE SYNTHASE INHIBITOR; PROTEIN ARGININE METHYLTRANSFERASE; SYMMETRICALLY DIMETHYLATED ARGININE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; COMPLEX FORMATION; ENZYME INHIBITION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; METHYLATION; PRIORITY JOURNAL;

CATALYSIS; HEART DISEASES; HUMANS; ISOENZYMES; KINETICS; METHYLATION; PEPTIDE FRAGMENTS; PROTEIN-ARGININE N-METHYLTRANSFERASE;

EID: 52949145297     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800904m     Document Type: Article

References (40)

1. Hong, H., Kao, C., Jeng, M. H., Eble, J. N., Koch, M. O., Gardner, T. A., Zhang, S., Li, L., Pan, C. X., Hu, Z., MacLennan, G. T., and Cheng, L. (2004) Aberrant expression of CARM1, a transcriptional coactivator of androgen receptor, in the development of prostate carcinoma and androgen-independent status. Cancer 101, 83-89.
2. Majumder, S., Liu, Y., Ford, O. H., 3rd, Mohler, J. L., and Whang, Y. E. (2006) Involvement of arginine methyltransferase CARM1 in androgen receptor function and prostate cancer cell viability. Prostate 66, 1292-1301.
3. Boger, R. H., Sydow, K., Borlak, J., Thum, T., Lenzen, H., Schubert, B., Tsikas, D., and Bode-Boger, S. M. (2000) LDL cholesterol upregulates synthesis of asymmetrical dimethylarginine in human endothelial cells: involvement of S-adenosylmethionine-dependent methyltransferases. Circ. Res. 87, 99-105.
4. Tran, C. T., Leiper, J. M., and Vallance, P. (2003) The DDAH/ADMA/NOS pathway. Atheroscler. Suppl. 4, 33-40.
5. Vallance, P., and Leiper, J. (2004) Cardiovascular biology of the asymmetric dimethylarginine:dimethylarginine dimethylaminohydrolase pathway. Arterioscler. Thromb. Vasc. Biol. 24, 1023-1030.
6. Leiper, J., Murray-Rust, J., McDonald, N., and Vallance, P. (2002) S-nitrosylation of dimethylarginine dimethylaminohydrolase regulates enzyme activity: further interactions between nitric oxide synthase and dimethylarginine dimethylaminohydrolase. Proc. Natl. Acad. Sci. U.S.A. 99, 13527-13532.
7. Vallance, P., Leone, A., Calver, A., Collier, J., and Moncada, S. (1992) Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet 339, 572-575.
8. Leiper, J., Nandi, M., Torondel, B., Murray-Rust, J., Malaki, M., O'Hara, B., Rossiter, S., Anthony, S., Madhani, M., Selwood, D., Smith, C., Wojciak-Stothard, B., Rudiger, A., Stidwill, R., McDonald, N. Q., and Vallance, P. (2007) Disruption of methylarginine metabolism impairs vascular homeostasis. Nat. Med. 13, 198-203.
9. Chen, X., Niroomand, F., Liu, Z., Zankl, A., Katus, H. A., Jahn, L., and Tiefenbacher, C. P. (2006) Expression of nitric oxide related enzymes in coronary heart disease. Basic Res. Cardiol. 101, 346-353.
10. Koh, S. S., Chen, D., Lee, Y. H., and Stallcup, M. R. (2001) Synergistic enhancement of nuclear receptor function by p160 coactivators and two coactivators with protein methyltransferase activities. J. Biol. Chem. 276, 1089-1098.
11. 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., and Allis, C. D. (2001) Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr. Biol. 11, 996-1000.
12. 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., and Zhang, Y. (2001) Methylation of Histone H4 at Arginine 3 Facilitating Transcriptional Activation by Nuclear Hormone Receptor. Science 293, 853-857.
13. Anzick, S. L., Kononen, J., Walker, R. L., Azorsa, D. O., Tanner, M. M., Guan, X. Y., Sauter, G., Kallioniemi, O. P., Trent, J. M., and Meltzer, P. S. (1997) AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science 277, 965-968.
14. Torchia, J., Rose, D. W., Inostroza, J., Kamei, Y., Westin, S., Glass, C. K., and Rosenfeld, M. G. (1997) The transcriptional co-activator p/CIP binds CBP and mediates nuclear-receptor function. Nature 387, 677-684.
15. Lee, S. K., Anzick, S. L., Choi, J. E., Bubendorf, L., Guan, X. Y., Jung, Y. K., Kallioniemi, O. P., Kononen, J., Trent, J. M., Azorsa, D., Jhun, B. H., Cheong, J. H., Lee, Y. C., Meltzer, P. S., and Lee, J. W. (1999) A nuclear factor, ASC-2, as a cancer-amplified transcriptional coactivator essential for ligand-dependent transactivation by nuclear receptors in vivo. J. Biol. Chem. 274, 34283-34293.
16. Zhu, Y., Qi, C., Jain, S., Le Beau, M. M., Espinosa, R., 3rd., Atkins, G. B., Lazar, M. A., Yeldandi, A. V., Rao, M. S., and Reddy, J. K. (1999) Amplification and overexpression of peroxisome proliferator-activated receptor binding protein (PBP/PPARBP) gene in breast cancer. Proc. Natl. Acad. Sci. U.S.A. 96, 10848-10853.
17. Lin, W. J., Gary, J. D., Yang, M. C., Clarke, S., and Herschman, H. R. (1996) The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J. Biol. Chem. 271, 15034-15044.
18. Abramovich, C., Yakobson, B., Chebath, J., and Revel, M. (1997) A protein-arginine methyltransferase binds to the intracytoplasmic domain of the IFNAR1 chain in the type I interferon receptor. EMBO J. 16, 260-266.
19. Bachand, F. (2007) Protein arginine methyltransferases: from unicellular eukaryotes to humans. Eukaryotic Cell 6, 889-898.
20. Bedford, M. T., and Richard, S. (2005) Arginine methylation an emerging regulator of protein function. Mol. Cell 18, 263-272.
21. Krause, C. D., Yang, Z. H., Kim, Y. S., Lee, J. H., Cook, J. R., and Pestka, S. (2007) Protein arginine methyltransferases: evolution and assessment of their pharmacological and therapeutic potential. Pharmacol. Ther. 113, 50-87.
22. Bedford, M. T. (2007) Arginine methylation at a glance. J. Cell Sci. 120, 4243-4246.
23. An, W., Kim, J., and Roeder, R. G. (2004) Ordered Cooperative Functions of PRMT1, p300, and CARM1 in Transcriptional Activation by p53. Cell 117, 735-748.
24. Rezai-Zadeh, N., Zhang, X., Namour, F., Fejer, G., Wen, Y. D., Yao, Y. L., Gyory, I., Wright, K., and Seto, E. (2003) Targeted recruitment of a histone H4-specific methyltransferase by the transcription factor YY1. Genes Dev. 17, 1019-1029.
25. Hassa, P. O., Covic, M., Bedford, M. T., and Hottiger, M. O. (2008) Protein arginine methyltransferase 1 coactivates NF-kappaB-dependent gene expression synergistically with CARM1 and PARP1. J. Mol. Biol. 377, 668-678.
26. Zhang, X., and Cheng, X. (2003) Structure of the predominant protein arginine methyltransferase PRMT1 and analysis of its binding to substrate peptides. Structure 11, 509-520.
27. Zhang, X., Zhou, L., and Cheng, X. (2000) Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J. 19, 3509-3519.
28. Weiss, V. H., McBride, A. E., Soriano, M. A., Filman, D. J., Silver, P. A., and Hogle, J. M. (2000) The structure and oligomerization of the yeast arginine methyltransferase, Hmt1. Nat. Struct. Biol. 7, 1165-1171.
29. Cook, J. R., Lee, J. H., Yang, Z. H., Krause, C. D., Herth, N., Hoffmann, R., and Pestka, S. (2006) FBXO11/PRMT9, a new protein arginine methyltransferase, symmetrically dimethylates arginine residues. Biochem. Biophys. Res. Commun. 342, 472-481.
30. Fielenbach, N., Guardavaccaro, D., Neubert, K., Chan, T., Li, D., Feng, Q., Hutter, H., Pagano, M., and Antebi, A. (2007) DRE-1: an evolutionarily conserved F box protein that regulates C. elegans developmental age. Dev. Cell 12, 443-455.
31. Osborne, T. C., Obianyo, O., Zhang, X., Cheng, X., and Thompson, P. R. (2007) Protein arginine methyltransferase 1: positively charged residues in substrate peptides distal to the site of methylation are important for substrate binding and catalysis. Biochemistry 46, 13370-13381.
32. Leatherbarrow, R. J. (2004) Grafit Ver. 5, Erathicus Software, Staines, U.K.
33. Segel, I. H. (1975) Enzyme kinetics: Behavior and analysis of rapid equilibrium and steady-state enzyme systems; Wiley-Interscience, New York.
34. Osborne, T., Roska, R. L., Rajski, S. R., and Thompson, P. R. (2008) In situ generation of a bisubstrate analogue for protein arginine methyltransferase 1. J. Am. Chem. Soc. 130, 4574-4575.
35. Coward, J. K. (1977) Chemical mechanisms of methyl transfer reactions: comparison of methylases with nonenzymic model reactions, in The biochemistry of adenosylmethionine (Salvatore, F., Borek, E., Zappia, V., and Williams-Ashman, H. G., Eds.) pp 127-144, Columbia University Press, New York, NY.
36. Dirk, L. M., Flynn, E. M., Dietzel, K., Couture, J. F., Trievel, R. C., and Houtz, R. L. (2007) Kinetic manifestation of processivity during multiple methylations catalyzed by SET domain protein methyltransferases. Biochemistry 46, 3905-3915.
37. Lakowski, T. M., and Frankel, A. (2008) A kinetic study of human protein arginine N-methyltransferase 6 reveals a distributive mechanism. J. Biol. Chem. 283, 10015-10025.
38. Yue, W. W., Hassler, M., Roe, S. M., Thompson-Vale, V., and Pearl, L. H. (2007) Insights into histone code syntax from structural and biochemical studies of CARM1 methyltransferase. EMBO J. 26, 4402-4412.
39. Schimerlik, M. I., and Cleland, W. W. (1973) Inhibition of creatine kinase by chromium nucleotides. J. Biol. Chem. 248, 8418-8423.
40. Cook, P. F., Kenyon, G. L., and Cleland, W. W. (1981) Use of pH studies to elucidate the catalytic mechanism of rabbit muscle creatine kinase. Biochemistry 20, 1204-1210.