Protein arginine methyltransferase product specificity is mediated by distinct active-site architectures

Journal of Biological Chemistry

Volumn 291, Issue 35, 2016, Pages 18299-18308

  Jain, Kanishk ^a   Warmack, Rebeccah A ^a   Debler, Erik W ^a   Hadjikyriacou, Andrea ^a   Stavropoulos, Peter ^b   Clarke, Steven G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACRYLIC MONOMERS; ALKYLATION; AMINO ACIDS; ARGININE; GENE EXPRESSION; KNOWLEDGE MANAGEMENT; PROTEINS;

ACTIVE SITE RESIDUES; CATION EXCHANGE CHROMATOGRAPHY; DISTINCT ACTIVE SITES; PRODUCT SPECIFICITY; PROTEIN-ARGININE METHYLTRANSFERASE; PROTOZOAN TRYPANOSOMA; SPECIFIC INHIBITORS; SYMMETRIC DIMETHYLARGININE;

PRODUCT DESIGN;

PROTEIN ARGININE METHYLTRANSFERASE; ARGININE; PROTOZOAL PROTEIN;

ARTICLE; BINDING AFFINITY; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; METHYLATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS; TRYPANOSOMA BRUCEI; AMINO ACID SUBSTITUTION; CHEMISTRY; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; MISSENSE MUTATION; PROTEIN SECONDARY STRUCTURE; TRYPANOSOMA BRUCEI BRUCEI;

AMINO ACID SUBSTITUTION; ARGININE; CATALYTIC DOMAIN; HUMANS; MUTATION, MISSENSE; PROTEIN STRUCTURE, SECONDARY; PROTEIN-ARGININE N-METHYLTRANSFERASES; PROTOZOAN PROTEINS; SUBSTRATE SPECIFICITY; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84984669538     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.740399     Document Type: Article

References (40)

1. Walsh, G., and Jefferis, R. (2006) Post-translational modifications in the context of therapeutic proteins. Nat. Biotechnol. 24, 1241-1252
2. Fuhrmann, J., and Clancy., K. W., and Thompson, P. R. (2015) Chemical biology of protein arginine modifications in epigenetic regulation. Chem. Rev. 115, 5413-5461
3. Morales, Y., Cáceres, T., May, K., and Hevel, J. M. (2016) Biochemistry and regulation of the protein arginine methyltransferases (PRMTs). Arch. Biochem. Biophys. 590, 138-152
4. Baldwin, R. M., Haghandish, N., Daneshmand, M., Amin, S., Paris, G., Falls, T. J., Bell, J. C, Islam, S., and Côté, J. (2015) Protein arginine methyltransferase 7 promotes breast cancer cell invasion through the induction of MMP9 expression. Oncotarget. 6, 3013-3032
5. Yao, R., Jiang, H., Ma, Y., Wang, L., Wang, L., Du, J., Hou, P., Gao, Y., Zhao, L., Wang, G., Zhang, Y., Liu, D.-X., Huang, B., and Lu, J. (2014) PRMT7 induces epithelial-to-mesenchymal transition and promotes metastasis in breast cancer. Cancer Res. 74, 5656-5667
6. Yang, Y., and Bedford, M. T. (2013) Protein arginine methyltransferases and cancer. Nat. Rev. Cancer 13, 37-50
7. Karkhanis, V., Wang, L., Tae, S., Hu, Y. J., and Imbalzano., A. N., and Sif, S. (2012) Protein arginine methyltransferase 7 regulates cellular response to DNA damage by methylating promoter histones H2A and H4 of the polymerase S catalytic subunit gene, POLD1. J. Biol. Chem. 287, 29801-29814
8. Wang, Y.-C, Peterson, S. E., and Loring, J. F. (2014) Protein post-translational modifications and regulation of pluripotency in human stem cells. Cell Res. 24, 143-160
9. Lott, K., Zhu, L., Fisk, J. C, Tomasello, D. L., and Read, L. K. (2014) Functional interplay between protein arginine methyltransferases in Trypanosoma brucei. Microbiologyopen 3, 595-609
10. Ferreira, T. R., Alves-Ferreira, E. V., Defina, T. P., Walrad, P., Papadopoulou, B., and Cruz, A. K. (2014) Altered expression of an RBP-associated arginine methyltransferase 7 in Leishmania major affects parasite infection. Mol. Microbiol. 94, 1085-1102
11. Bedford, M. T., and Clarke, S. G. (2009) Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33, 1-13
12. Martens-Lobenhoffer, J., Bode-Böger, S. M., and Clement, B. (2016) First detection and quantification of N(S)-monomethylarginine, a structural isomer of N (G)-monomethylarginine, in humans using MS(3). Anal. Biochem. 493, 14-20
13. Wang, H., and Huang., Z. Q., Xia, L., Feng, Q., Erdjument-Bromage, H., Strahl, B. D., and 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
14. Sun, L., Wang, M., Lv, Z., Yang, N., Liu, Y., Bao, S., Gong, W., and Xu, R.-M. (2011) Structural insights into protein arginine symmetric dimethylation by PRMT5. Proc. Natl. Acad. Sci. 108, 20538-20543
15. Dhar, S. S., Lee, S.-H., Kan, P.-Y., Voigt, P., Ma, L., Shi, X., Reinberg, D., and Lee, M. G. (2012) Trans-tail regulation of MLL4-catalyzed H3K4 methylation by H4R3 symmetric dimethylation is mediated by a tandem PHD of MLL4. Genes Dev. 26, 2749-2762
16. Migliori, V., Müller, J., Phalke, S., Low, D., Bezzi, M., Mok, W. C, Sahu, S. K., Gunaratne, J., Capasso, P., Bassi, C, Cecatiello, V., De Marco, A., Blackstock, W., Kuznetsov, V., Amati, B., et al. (2012) Symmetric dimethylation of H3R2 is a newly identified histone mark that supports euchromatin maintenance. Nat. Struct. Mol. Biol. 19, 136-144
17. Gayatri, S., and Bedford, M. T. (2014) Readers of histone methylarginine marks. Biochim. Biophys. Acta 1839, 702-710
18. Suárez-Calvet, M., Neumann, M., Arzberger, T., Abou-Ajram, C., Funk, E., Hartmann, H., Edbauer, D., Kremmer, E., Göbl, C., Resch, M., Bourgeois, B., Madl, T., Reber, S., Jutzi, D., Ruepp, M.-D., et al. (2016) Monomethylated and unmethylated FUS exhibit increased bindingto Transportin and distinguish FTLD-FUS from ALS-FUS. Acta Neuropathol. 131, 587-604
19. Dhar, S., Vemulapalli, V., Patananan, A. N., and Huang., G. L., Di Lorenzo, A., Richard, S., Comb, M. J., Guo, A., and Clarke., S. G., and Bedford, M. T. (2013) Loss of the major type I arginine methyltransferase PRMT1 causes substrate scavenging by other PRMTs. Sci. Rep. 3, 1311
20. Fuhrmann, J., and Thompson, P. R. (2016) Protein arginine methylation and citrullination in epigenetic regulation. ACS Chem. Biol. 11, 654-668
21. Schapira, M., and Ferreira de Freitas, R. (2014) Structural biology and chemistry of protein arginine methyltransferases. Medchemcomm 5, 1779-1788
22. Cura, V., Troffer-Charlier, N., Wurtz, J. M., Bonnefond, L., and Cavarelli, J. (2014) Structural insight into arginine methylationby the mouse protein arginine methyltransferase7:azinc finger freezes the mimicof the dimeric state into a single active site. Acta Crystallogr. D Biol. Crystallogr 70, 2401-2412
23. Hasegawa, M., Toma-Fukai, S., Kim, J. D., Fukamizu, A., and Shimizu, T. (2014) Protein arginine methyltransferase 7 has a novel homodimer-like structure formed by tandem repeats. FEBS Lett. 588, 1942-1948
24. Gui, S., Gathiaka, S., Li, J., Qu, J., Acevedo, O., and Hevel, J. M. (2014) A remodeled protein arginine methyltransferase 1 (PRMT1) generates symmetric dimethylarginine. J. Biol. Chem. 289, 9320-9327
25. Debler, E. W., Jain, K., Warmack, R. A., Feng, Y., and Clarke., S. G., Blobel, G., and Stavropoulos, P. (2016) A glutamate/aspartate switch controls product specificity in a protein arginine methyltransferase. Proc. Natl. Acad. Sci. U.S.A. 113, 2068-2073
26. Fisk, J. C., Sayegh, J., Zurita-Lopez, C., Menon, S., Presnyak, V., Clarke, S. G., and Read, L. K. (2009) A type III protein arginine methyltransferase from the protozoan parasite Trypanosoma brucei. J. Biol. Chem. 284, 11590-11600
27. Wang, C., Zhu, Y., Caceres, T. B., Liu, L., Peng, J., Wang, J., Chen, J., Chen, X., Zhang, Z., Zuo, X., Gong, Q., Teng, M., Hevel, J. M., Wu, J., and Shi, Y. (2014) Structural determinants for the strict monomethylation activity by Trypanosoma brucei protein arginine methyltransferase 7. Structure 22, 756-768
28. Hadjikyriacou, A., Yang, Y., Espejo, A., Bedford, M. T., and Clarke, S. G. (2015) Unique features of human protein arginine methyltransferase 9 (PRMT9) and its substrate RNA splicing factor SF3B2. J. Biol. Chem. 290, 16723-16743
29. Yang, Y., Hadjikyriacou, A., Xia, Z., Gayatri, S., Kim, D., Zurita-Lopez, C., Kelly, R., Guo, A., Li, W., Clarke, S. G., and Bedford, M. T. (2015) PRMT9 is a type II methyltransferase that methylates the splicing factor SAP145. Nat. Commun. 6, 6428
30. Feng, Y., Maity, R., Whitelegge, J. P., Hadjikyriacou, A., Li, Z., ZuritaLopez, C., Al-Hadid, Q., Clark, A. T., and Bedford., M. T., Masson, J. Y., and Clarke, S. G. (2013) Mammalian protein arginine methyltransferase 7 (PRMT7) specifically targets RXR sites in lysine- and arginine-rich regions. J. Biol. Chem. 288, 37010-37025
31. Feng, Y., Xie, N., Jin, M., Stahley, M. R., and Stivers., J. T., and Zheng, Y. G. (2011) A transient kinetic analysis of PRMT1 catalysis. Biochemistry 50, 7033-7044
32. Huang, S., Litt, M., and Felsenfeld, G. (2005) Methylation of histone H4 by arginine methyltransferase PRMT1 is essential in vivo for many subsequent histone modifications. Genes Dev. 19, 1885-1893
33. Wang, M., Xu, R.-M., and Thompson, P. R. (2013) Substrate specificity, processivity, and kinetic mechanismofprotein arginine methyltransferase 5. Biochemistry 52, 5430-5440
34. Bao, X., Zhao, S., Liu, T., Liu, Y., Liu, Y., and Yang, X. (2013) Overexpression of PRMT5 promotes tumor cell growth and is associated with poor disease prognosis in epithelial ovarian cancer. J. Histochem. Cytochem. 61, 206-217
35. Tarighat, S. S., Santhanam, R., Frankhouser, D., Radomska, H. S., Lai, H., Anghelina, M., Wang, H., Huang, X., Alinari, L., Walker, A., Caligiuri, M. A., and Croce., C. M., Li, L., Garzon, R., Li, C., et al. (2016) The dual epigenetic role of PRMT5 in acute myeloid leukemia: gene activation and repression via histone arginine methylation. Leukemia 30, 789-799
36. Schapira, M., and Arrowsmith, C. H. (2016) Methyltransferase inhibitors for modulation of the epigenome and beyond. Curr. Opin. Chem. Biol. 33, 81-87
37. Hu, H., Qian, K., Ho, M.-C., and Zheng, Y. G. (2016) Small molecule inhibitors of protein arginine methyltransferases. Expert Opin. Investig. Drugs. 25, 335-358
38. 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
39. G-monomethylated arginine residues. J. Biol. Chem. 287, 7859-7870
40. Gottschling, H., and Freese, E. (1962) A tritium isotope effect on ion exchange chromatography. Nature 196, 829-831