Automethylation of protein arginine methyltransferase 6 (PRMT6) regulates its stability and its anti-HIV-1 activity

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Singhroy, Diane N ^a,b   Mesplède, Thibault ^a   Sabbah, Arielle ^a   Quashie, Peter K ^a,c   Falgueyret, Jean Pierre ^d   Wainberg, Mark A ^a,b,c  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d Gina Cody School of Engineering and Computer Science   (Canada)

Author keywords

Antiretroviral activity; Automethylation; HIV 1; PRMT6; Protein stability

Indexed keywords

ANTIRETROVIRUS AGENT; RECOMBINANT PROTEIN; RECOMBINANT PROTEIN ARGININE METHYLTRANSFERASE 6; UNCLASSIFIED DRUG; VIRUS RNA;

AMINO ACID SEQUENCE; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME STABILITY; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN METHYLATION; VIRUS INHIBITION; VIRUS REPLICATION; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ARGININE; CELL LINE; CHROMATOGRAPHY, LIQUID; ENZYME STABILITY; HIV-1; HUMANS; MASS SPECTROMETRY; METHYLATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; NUCLEAR PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-ARGININE N-METHYLTRANSFERASES;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84880183511     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-73     Document Type: Article

References (43)

1. Krause CD, Yang ZH, Kim YS, Lee JH, Cook JR, Pestka S. Protein arginine methyltransferases: evolution and assessment of their pharmacological and therapeutic potential. Pharmacol Ther 2007, 113:50-87. 10.1016/j.pharmthera.2006.06.007, 17005254.
2. Konig R, Zhou Y, Elleder D, Diamond TL, Bonamy GM, Irelan JT, Chiang CY, Tu BP, De Jesus PD, Lilley CE, et al. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 2008, 135:49-60. 10.1016/j.cell.2008.07.032, 2628946, 18854154.
3. Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A, Xavier RJ, Lieberman J, Elledge SJ. Identification of host proteins required for HIV infection through a functional genomic screen. Science 2008, 319:921-926. 10.1126/science.1152725, 18187620.
4. Le Clerc S, Limou S, Coulonges C, Carpentier W, Dina C, Taing L, Delaneau O, Labib T, Sladek R, Deveau C, et al. Genomewide association study of a rapid progression cohort identifies new susceptibility alleles for AIDS (ANRS Genomewide Association Study 03). J Infect Dis 2009, 200:1194-1201. 10.1086/605892, 19754311.
5. Zhou H, Xu M, Huang Q, Gates AT, Zhang XD, Castle JC, Stec E, Ferrer M, Strulovici B, Hazuda DJ, Espeseth AS. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe 2008, 4:495-504. 10.1016/j.chom.2008.10.004, 18976975.
6. Liu L, Oliveira NM, Cheney KM, Pade C, Dreja H, Bergin AM, Borgdorff V, Beach DH, Bishop CL, Dittmar MT, McKnight A. A whole genome screen for HIV restriction factors. Retrovirology 2011, 8:94. 10.1186/1742-4690-8-94, 3228845, 22082156.
7. Kiernan RE, Vanhulle C, Schiltz L, Adam E, Xiao H, Maudoux F, Calomme C, Burny A, Nakatani Y, Jeang KT, et al. HIV-1 tat transcriptional activity is regulated by acetylation. EMBO J 1999, 18:6106-6118. 10.1093/emboj/18.21.6106, 1171675, 10545121.
8. Yang X, Goncalves J, Gabuzda D. Phosphorylation of Vif and its role in HIV-1 replication. J Biol Chem 1996, 271:10121-10129. 10.1074/jbc.271.17.10121, 8626571.
9. Gary JD, Clarke S. RNA and protein interactions modulated by protein arginine methylation. Prog Nucleic Acid Res Mol Biol 1998, 61:65-131.
10. Bedford MT, Clarke SG. Protein arginine methylation in mammals: who, what, and why. Mol Cell 2009, 33:1-13. 10.1016/j.molcel.2008.12.013, 3372459, 19150423.
11. Miranda TB, Miranda M, Frankel A, Clarke S. PRMT7 is a member of the protein arginine methyltransferase family with a distinct substrate specificity. J Biol Chem 2004, 279:22902-22907. 10.1074/jbc.M312904200, 15044439.
12. Bedford MT, Richard S. Arginine methylation an emerging regulator of protein function. Mol Cell 2005, 18:263-272. 10.1016/j.molcel.2005.04.003, 15866169.
13. Bedford MT. Arginine methylation at a glance. J Cell Sci 2007, 120:4243-4246. 10.1242/jcs.019885, 18057026.
14. Lakowski TM, Frankel A. A kinetic study of human protein arginine N-methyltransferase 6 reveals a distributive mechanism. J Biol Chem 2008, 283:10015-10025. 10.1074/jbc.M710176200, 18263580.
15. Lee YH, Stallcup MR. Minireview: protein arginine methylation of nonhistone proteins in transcriptional regulation. Mol Endocrinol 2009, 23:425-433. 10.1210/me.2008-0380, 2667706, 19164444.
16. Boisvert FM, Cote J, Boulanger MC, Richard S. A proteomic analysis of arginine-methylated protein complexes. Mol Cell Proteomics 2003, 2:1319-1330. 10.1074/mcp.M300088-MCP200, 14534352.
17. Frankel A, Yadav N, Lee J, Branscombe TL, Clarke S, Bedford MT. The novel human protein arginine N-methyltransferase PRMT6 is a nuclear enzyme displaying unique substrate specificity. J Biol Chem 2002, 277:3537-3543. 10.1074/jbc.M108786200, 11724789.
18. Michaud-Levesque J, Richard S. Thrombospondin-1 is a transcriptional repression target of PRMT6. J Biol Chem 2009, 284:21338-21346. 10.1074/jbc.M109.005322, 2755858, 19509293.
19. Hyllus D, Stein C, Schnabel K, Schiltz E, Imhof A, Dou Y, Hsieh J, Bauer UM. PRMT6-mediated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes Dev 2007, 21:3369-3380. 10.1101/gad.447007, 2113036, 18079182.
20. Waldmann T, Izzo A, Kamieniarz K, Richter F, Vogler C, Sarg B, Lindner H, Young NL, Mittler G, Garcia BA, Schneider R. Methylation of H2AR29 is a novel repressive PRMT6 target. Epigenetics Chromatin 2011, 4:11. 10.1186/1756-8935-4-11, 3164600, 21774791.
21. Xie B, Invernizzi CF, Richard S, Wainberg MA. Arginine methylation of the human immunodeficiency virus type 1 Tat protein by PRMT6 negatively affects Tat Interactions with both cyclin T1 and the Tat transactivation region. J Virol 2007, 81:4226-4234. 10.1128/JVI.01888-06, 1866113, 17267505.
22. Boulanger MC, Liang C, Russell RS, Lin R, Bedford MT, Wainberg MA, Richard S. Methylation of Tat by PRMT6 regulates human immunodeficiency virus type 1 gene expression. J Virol 2005, 79:124-131. 10.1128/JVI.79.1.124-131.2005, 538702, 15596808.
23. Invernizzi CF, Xie B, Richard S, Wainberg MA. PRMT6 diminishes HIV-1 Rev binding to and export of viral RNA. Retrovirology 2006, 3:93. 10.1186/1742-4690-3-93, 1779295, 17176473.
24. Invernizzi CF, Xie B, Frankel FA, Feldhammer M, Roy BB, Richard S, Wainberg MA. Arginine methylation of the HIV-1 nucleocapsid protein results in its diminished function. AIDS 2007, 21:795-805. 10.1097/QAD.0b013e32803277ae, 17415034.
25. Suhasini M, Reddy TR. Cellular proteins and HIV-1 Rev function. Curr HIV Res 2009, 7:91-100. 10.2174/157016209787048474, 19149558.
26. Tange TO, Jensen TH, Kjems J. In vitro interaction between human immunodeficiency virus type 1 Rev protein and splicing factor ASF/SF2-associated protein, p32. J Biol Chem 1996, 271:10066-10072. 10.1074/jbc.271.17.10066, 8626563.
27. Thomas D, Lakowski TM, Pak ML, Kim JJ, Frankel A. Forster resonance energy transfer measurements of cofactor-dependent effects on protein arginine N-methyltransferase homodimerization. Protein Sci 2010, 19:2141-2151. 10.1002/pro.492, 3005785, 20812326.
28. Kuhn P, Chumanov R, Wang Y, Ge Y, Burgess RR, Xu W. Automethylation of CARM1 allows coupling of transcription and mRNA splicing. Nucleic Acids Res 2011, 39:2717-2726. 10.1093/nar/gkq1246, 3074151, 21138967.
29. Sivakumaran H, van der Horst A, Fulcher AJ, Apolloni A, Lin MH, Jans DA, Harrich D. Arginine methylation increases the stability of human immunodeficiency virus type 1 Tat. J Virol 2009, 83:11694-11703. 10.1128/JVI.00499-09, 2772670, 19726520.
30. Cha B, Kim W, Kim YK, Hwang BN, Park SY, Yoon JW, Park WS, Cho JW, Bedford MT, Jho EH. Methylation by protein arginine methyltransferase 1 increases stability of Axin, a negative regulator of Wnt signaling. Oncogene 2011, 30:2379-2389. 10.1038/onc.2010.610, 21242974.
31. Willemsen NM, Hitchen EM, Bodetti TJ, Apolloni A, Warrilow D, Piller SC, Harrich D. Protein methylation is required to maintain optimal HIV-1 infectivity. Retrovirology 2006, 3:92. 10.1186/1742-4690-3-92, 1766367, 17169163.
32. Shirakawa K, Takaori-Kondo A, Yokoyama M, Izumi T, Matsui M, Io K, Sato T, Sato H, Uchiyama T. Phosphorylation of APOBEC3G by protein kinase A regulates its interaction with HIV-1 Vif. Nat Struct Mol Biol 2008, 15:1184-1191. 10.1038/nsmb.1497, 18836454.
33. Dussart S, Douaisi M, Courcoul M, Bessou G, Vigne R, Decroly E. APOBEC3G ubiquitination by Nedd4-1 favors its packaging into HIV-1 particles. J Mol Biol 2005, 345:547-558. 10.1016/j.jmb.2004.10.067, 15581898.
34. Douaisi M, Dussart S, Courcoul M, Bessou G, Lerner EC, Decroly E, Vigne R. The tyrosine kinases Fyn and Hck favor the recruitment of tyrosine-phosphorylated APOBEC3G into vif-defective HIV-1 particles. Biochem Biophys Res Commun 2005, 329:917-924. 10.1016/j.bbrc.2005.02.057, 15752743.
35. Sayegh J, Webb K, Cheng D, Bedford MT, Clarke SG. Regulation of protein arginine methyltransferase 8 (PRMT8) activity by its N-terminal domain. J Biol Chem 2007, 282:36444-36453. 10.1074/jbc.M704650200, 17925405.
36. Lakowski TM, t Hart P, Ahern CA, Martin NI, Frankel A. Neta-substituted arginyl peptide inhibitors of protein arginine N-methyltransferases. ACS Chem Biol 2010, 5:1053-1063. 10.1021/cb100161u, 20701328.
37. Choi S, Jung CR, Kim JY, Im DS. PRMT3 inhibits ubiquitination of ribosomal protein S2 and together forms an active enzyme complex. Biochim Biophys Acta 2008, 1780:1062-1069. 10.1016/j.bbagen.2008.05.010, 18573314.
38. Jarmalavicius S, Trefzer U, Walden P. Differential arginine methylation of the G-protein pathway suppressor GPS-2 recognized by tumor-specific T cells in melanoma. FASEB J 2010, 24:937-946. 10.1096/fj.09-136283, 19917673.
39. Yamamoto N, Tanaka C, Wu Y, Chang MO, Inagaki Y, Saito Y, Naito T, Ogasawara H, Sekigawa I, Hayashida Y. Analysis of human immunodeficiency virus type 1 integration by using a specific, sensitive and quantitative assay based on real-time polymerase chain reaction. Virus Genes 2006, 32:105-113. 10.1007/s11262-005-5851-2, 16525741.
40. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol 1986, 59:284-291. 253077, 3016298.
41. Rasband WS. ImageJ 1997-2011, Bethesda, Maryland, USA: Health NIo ed.
42. Donahue DA, Sloan RD, Kuhl BD, Bar-Magen T, Schader SM, Wainberg MA. Stage-dependent inhibition of HIV-1 replication by antiretroviral drugs in cell culture. Antimicrob Agents Chemother 2010, 54:1047-1054. 10.1128/AAC.01537-09, 2826010, 20038621.
43. Schader SM, Oliveira M, Ibanescu RI, Moisi D, Colby-Germinario SP, Wainberg MA. In vitro resistance profile of the candidate HIV-1 microbicide drug dapivirine. Antimicrob Agents Chemother 2012, 56:751-756. 10.1128/AAC.05821-11, 3264246, 22123692.