A glutamate/aspartate switch controls product specificity in a protein arginine methyltransferase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 8, 2016, Pages 2068-2073

  Debler, Erik W ^a   Jain, Kanishk ^b   Warmack, Rebeccah A ^b   Feng, You ^b   Clarke, Steven G ^b   Blobel, Günter ^a   Stavropoulos, Pete ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Crystal structure; Enzyme catalysis; Epigenetics; Histone methylation; PRMT

Indexed keywords

ASPARTIC ACID; GLUTAMIC ACID; N(G),N(G) DIMETHYLARGININE; PROTEIN ARGININE METHYLTRANSFERASE; S ADENOSYLHOMOCYSTEINE; PROTOZOAL PROTEIN;

ARTICLE; CONTROLLED STUDY; DIMERIZATION; GENE MUTATION; ISOTHERMAL TITRATION CALORIMETRY; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; TRYPANOSOMA BRUCEI BRUCEI; X RAY CRYSTALLOGRAPHY;

ASPARTIC ACID; CRYSTALLOGRAPHY, X-RAY; GLUTAMIC ACID; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN-ARGININE N-METHYLTRANSFERASES; PROTOZOAN PROTEINS; S-ADENOSYLHOMOCYSTEINE; SUBSTRATE SPECIFICITY; TRYPANOSOMA BRUCEI BRUCEI;

EID: 84959244304     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1525783113     Document Type: Article

References (41)

1. Walsh G, Jefferis R (2006) Post-translational modifications in the context of therapeutic proteins. Nat Biotechnol 24(10):1241-1252.
2. Carr SM, Poppy Roworth A, Chan C, La Thangue NB (2015) Post-translational control of transcription factors: Methylation ranks highly. FEBS J 282(23):4450-4465.
3. Dhar SS, et al. (2012) Trans-tail regulation of MLL4-catalyzed H3K4 methylation by H4R3 symmetric dimethylation ismediated by a tandem PHD ofMLL4. Genes Dev 26(24):2749-2762.
4. Baldwin RM, et al. (2015) Protein arginine methyltransferase 7 promotes breast cancer cell invasion through the induction of MMP9 expression. Oncotarget 6(5):3013-3032.
5. Biggar KK, Li SS (2015) Non-histone protein methylation as a regulator of cellular signalling and function. Nat Rev Mol Cell Biol 16(1):5-17.
6. Bedford MT, Clarke SG (2009) Protein arginine methylation in mammals: Who, what, and why. Mol Cell 33(1):1-13.
7. Herrmann F, Pably P, Eckerich C, Bedford MT, Fackelmayer FO (2009) Human protein arginine methyltransferases in vivo: Distinct properties of eight canonical members of the PRMT family. J Cell Sci 122(Pt 5):667-677.
8. Niewmierzycka A, Clarke S (1999) S-Adenosylmethionine-dependent methylation in Saccharomyces cerevisiae: Identification of a novel protein arginine methyltransferase. J Biol Chem 274(2):814-824.
9. Feng Y, Hadjikyriacou A, Clarke SG (2014) Substrate specificity of human protein arginine methyltransferase 7 (PRMT7): The importance of acidic residues in the double E loop. J Biol Chem 289(47):32604-32616.
10. Feng Y, et al. (2013)Mammalian protein arginine methyltransferase 7 (PRMT7) specifically targets RXR sites in lysine- and arginine-rich regions. J Biol Chem 288(52):37010-37025.
11. Zurita-Lopez CI, Sandberg T, Kelly R, Clarke SG (2012) Human protein arginine methyltransferase 7 (PRMT7) is a type III enzyme forming ω-NG-monomethylated arginine residues. J Biol Chem 287(11):7859-7870.
12. Fisk JC, et al. (2009) A type III protein arginine methyltransferase from the protozoan parasite Trypanosoma brucei. J Biol Chem 284(17):11590-11600.
13. Wang C, et al. (2014) Structural determinants for the strict monomethylation activity by trypanosoma brucei protein arginine methyltransferase 7. Structure 22(5):756-768.
14. Yao R, et al. (2014) PRMT7 induces epithelial-to-mesenchymal transition and promotes metastasis in breast cancer. Cancer Res 74(19):5656-5667.
15. Yang Y, Bedford MT (2013) Protein arginine methyltransferases and cancer. Nat Rev Cancer 13(1):37-50.
16. Karkhanis V, et al. (2012) Protein arginine methyltransferase 7 regulates cellular response to DNA damage by methylating promoter histones H2A and H4 of the polymerase δ catalytic subunit gene, POLD1. J Biol Chem 287(35):29801-29814.
17. Wang YC, Peterson SE, Loring JF (2014) Protein post-translational modifications and regulation of pluripotency in human stem cells. Cell Res 24(2):143-160.
18. Ferreira TR, et al. (2014) Altered expression of an RBP-associated arginine methyltransferase 7 in Leishmania major affects parasite infection. Mol Microbiol 94(5): 1085-1102.
19. Hasegawa M, Toma-Fukai S, Kim JD, Fukamizu A, Shimizu T (2014) Protein arginine methyltransferase 7 has a novel homodimer-like structure formed by tandem repeats. FEBS Lett 588(10):1942-1948.
20. Cura V, Troffer-Charlier N, Wurtz JM, Bonnefond L, Cavarelli J (2014) Structural insight into arginine methylation by the mouse protein arginine methyltransferase 7: A zinc finger freezes the mimic of the dimeric state into a single active site. Acta Crystallogr D Biol Crystallogr 70(Pt 9):2401-2412.
21. Yang Y, et al. (2015) PRMT9 is a type II methyltransferase that methylates the splicing factor SAP145. Nat Commun 6:6428.
22. Hadjikyriacou A, Yang Y, Espejo A, Bedford MT, Clarke SG (2015) Unique features of human protein arginine methyltransferase 9 (PRMT9) and its substrate RNA splicing factor SF3B2. J Biol Chem 290(27):16723-16743.
23. Weiss VH, et al. (2000) The structure and oligomerization of the yeast arginine methyltransferase, Hmt1. Nat Struct Biol 7(12):1165-1171.
24. Zhang X, Zhou L, Cheng X (2000) Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J 19(14):3509-3519.
25. Sun L, et al. (2011) Structural insights into protein arginine symmetric dimethylation by PRMT5. Proc Natl Acad Sci USA 108(51):20538-20543.
26. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372(3):774-797.
27. Fuhrmann J, Clancy KW, Thompson PR (2015) Chemical biology of protein arginine modifications in epigenetic regulation. Chem Rev 115(11):5413-5461.
28. Lee HW, Kim S, Paik WK (1977) S-adenosylmethionine: Protein-arginine methyltransferase. Purification and mechanism of the enzyme. Biochemistry 16(1):78-85.
29. Migliori V, et al. (2012) Symmetric dimethylation of H3R2 is a newly identified histone mark that supports euchromatin maintenance. Nat Struct Mol Biol 19(2):136-144.
30. Xiao B, et al. (2003) Structure and catalytic mechanism of the human histone methyltransferase SET7/9. Nature 421(6923):652-656.
31. Zhang X, et al. (2003) Structural basis for the product specificity of histone lysine methyltransferases. Mol Cell 12(1):177-185.
32. Gottschling H, Freese E (1962) A tritium isotope effect on ion exchange chromatography. Nature 196:829-831.
33. Hayman ML, Read LK (1999) Trypanosoma brucei RBP16 is a mitochondrial Y-box family protein with guide RNA binding activity. J Biol Chem 274(17):12067-12074.
34. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326.
35. Adams PD, et al. (2011) The Phenix software for automated determination of macromolecular structures. Methods 55(1):94-106.
36. Jones TA, Zou J-Y, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47(Pt 2):110-119.
37. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
38. Davis IW, et al. (2007) MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35(Web Server issue):W375-W383.
39. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc Natl Acad Sci USA 98(18): 10037-10041.
40. Wyatt PJ (1997) Multiangle light scattering: The basic tool for macromolecular characterization. Instrum Sci Technol 25:1-18.
41. Karplus PA, Diederichs K (2012) Linking crystallographic model and data quality. Science 336(6084):1030-1033.