Arginine methylation of the HIV-1 nucleocapsid protein results in its diminished function

AIDS

Volumn 21, Issue 7, 2007, Pages 795-805

  Invernizzi, Cédric F ^a,b   Xie, Baode ^a   Frankel, Fernando A ^a,b   Feldhammer, Matthew ^a   Roy, Bibhuti B ^a   Richard, Stéphane ^a,b   Wainberg, Mark A ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Arginine methylation; Arginine methyltransferase inhibitor; HIV 1; Nucleocapsid; Protein arginine methyltransferase 6

Indexed keywords

ARGININE; ARGININE METHYLTRANSFERASE INHIBITOR 3.4; ENZYME INHIBITOR; NUCLEOCAPSID PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 6; RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; IN VIVO STUDY; METHYLATION; MONONUCLEAR CELL; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; REVERSE TRANSCRIPTION; UMBILICAL CORD BLOOD; VIRUS INFECTIVITY; VIRUS REPLICATION;

ARGININE; CELLS, CULTURED; ENZYME INHIBITORS; HIV-1; HUMANS; METHYLATION; METHYLTRANSFERASES; NUCLEAR PROTEINS; NUCLEOCAPSID PROTEINS; PROTEIN-ARGININE N-METHYLTRANSFERASE; RNA, TRANSFER, LYS; RNA, VIRAL; VIRUS REPLICATION;

EID: 34147223386     PISSN: 02699370     EISSN: None     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32803277ae     Document Type: Article

References (48)

1. Sakaguchi K, Zambrano N, Baldwin ET, Shapiro BA, Erickson JW, Omichinski JG, et al. Identification of a binding site for the human immunodeficiency virus type 1 nucleocapsid protein. Proc Natl Acad Sci U S A 1993; 90:5219-5223.
2. Amarasinghe GK, De Guzman RN, Turner RB, Chancellor KJ, Wu ZR, Summers MF. NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the psi-RNA packaging signal. Implications for genome recognition. J Mol Biol 2000; 301:491-511.
3. Shubsda MF, Paoletti AC, Hudson BS, Borer PN. Affinities of packaging domain loops in HIV-1 RNA for the nucleocapsid protein. Biochemistry 2002; 41:5276-5282.
4. Maki AH, Ozarowski A, Misra A, Urbaneja MA, Casas-Finet JR. Phosphorescence and optically detected magnetic resonance of HIV-1 nucleocapsid protein complexes with stem-loop sequences of the genomic Psi-recognition element. Biochemistry 2001; 40:1403-1412.
5. Guo J, Wu T, Anderson J, Kane BF, Johnson DG, Gorelick RJ, et al. Zinc finger structures in the human immunodeficiency virus type 1 nucleocapsid protein facilitate efficient minus- and plus-strand transfer. J Virol 2000; 74:8980-8988.
6. Cen S, Khorchid A, Gabor J, Rong L, Wainberg MA, Kleiman L. Roles of Pr55(gag) and NCp7 in tRNA(3)(Lys) genomic placement and the initiation step of reverse transcription in human immunodeficiency virus type 1. J Virol 2000; 74:10796-10800.
7. De Rocquigny H, Gabus C, Vincent A, Fournie-Zaluski MC, Roques B, Darlix JL. Viral RNA annealing activities of human immunodeficiency virus type 1 nucleocapsid protein require only peptide domains outside the zinc fingers. Proc Natl Acad Sci U S A 1992; 89:6472-6476.
8. Roldan A, Warren OU, Russell RS, Liang C, Wainberg MA. A HIV-1 minimal gag protein is superior to nucleocapsid at in vitro annealing and exhibits multimerization-induced inhibition of reverse transcription. J Biol Chem 2005; 280:17488-17496.
9. Lingappa JR, Dooher JE, Newman MA, Kiser PK, Klein KC. Basic residues in the nucleocapsid domain of gag are required for interaction of HIV-1 gag with ABCE1 (HP68), a cellular protein important for HIV-1 capsid assembly. J Biol Chem 2006; 281:3773-3784.
10. Gottwein E, Krausslich HG. Analysis of human immunodeficiency virus type 1 Gag ubiquitination. J Virol 2005; 79:9134-9144.
11. Bedford MT, Richard S. Arginine methylation an emerging regulator of protein function. Mol Cell 2005; 18:263-272.
12. Gary JD, Clarke S. RNA and protein interactions modulated by protein arginine methylation. Prog Nucl Acid Res Mol Biol 1998; 61:65-131.
13. McBride AE, Silver PA. State of the arg: protein methylation at arginine comes of age. Cell 2001; 106:5-8.
14. Boisvert FM, Cote J, Boulanger MC, Richard S. A proteomic analysis of arginine-methylated protein complexes. Mol Cell Proteom 2003; 2:1319-1330.
15. 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.
16. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000; 403:41-45.
17. Zhang Y, Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 2001; 15:2343-2360.
18. Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell 2004; 116:259-272.
19. Lee DY, Teyssier C, Strahl BD, Stallcup MR. Role of protein methylation in regulation of transcription. Endocr Rev 2005; 26:147-170.
20. Cote J, Boisvert FM, Boulanger MC, Bedford MT, Richard S. Sam68 RNA binding protein is an in vivo substrate for protein arginine N-methyltransferase 1. Mol Biol Cell 2003; 14:274-287.
21. 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.
22. Lin WJ, Gary JD, Yang MC, Clarke S, Herschman HR. The mammalian immediate-early TIS21 protein and the leukemia-associated BTG1 protein interact with a protein-arginine N-methyltransferase. J Biol Chem 1996; 271:15034-15044.
23. Scott HS, Antonarakis SE, Lalioti MD, Rossier C, Silver PA, Henry MF. Identification and characterization of two putative human arginine methyltransferases (HRMT1L1 and HRMT1L2). Genomics 1998; 48:330-340.
24. Tang J, Gary JD, Clarke S, Herschman HR. PRMT 3, a type I protein arginine N-methyltransferase that differs from PRMT1 in its oligomerization, subcellular localization, substrate specificity, and regulation. J Biol Chem 1998; 273:16935-16945.
25. Zhang X, Zhou L, Cheng X. Crystal structure of the conserved core of protein arginine methyltransferase PRMT3. EMBO J 2000; 19:3509-3519.
26. Chen D, Ma H, Hong H, Koh SS, Huang SM, Schurter BT, et al. Regulation of transcription by a protein methyltransferase. Science 1999; 284:2174-2177.
27. Lee J, Sayegh J, Daniel J, Clarke S, Bedford MT. PRMT8, a new membrane-bound tissue-specific member of the protein arginine methyltransferase family. J Biol Chem 2005; 280:32890-32896.
28. Pollack BP, Kotenko SV, He W, Izotova LS, Barnoski BL, Pestka S. The human homologue of the yeast proteins Skb1 and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J Biol Chem 1999; 274:31531-31542.
29. Branscombe TL, Frankel A, Lee JH, Cook JR, Yang Z, Pestka S, et al. PRMT5 (Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J Biol Chem 2001; 276:32971-32976.
30. Lee JH, Cook JR, Yang ZH, Mirochnitchenko O, Gunderson SI, Felix AM, et al. PRMT7, a new protein arginine methyltransferase that synthesizes symmetric dimethylarginine. J Biol Chem 2005; 280:3656-3664.
31. Cook JR, Lee JH, Yang ZH, Krause CD, Herth N, Hoffmann R, Pestka S. FBXO11/PRMT9, a new protein arginine methyltransferase, symmetrically dimethylates arginine residues. Biochem Biophys Res Commun 2006; 342:472-481.
32. Kzhyshkowska J, Schutt H, Liss M, Kremmer E, Stauber R, Wolf H, et al. Heterogeneous nuclear ribonucleoprotein E1B-AP5 is methylated in its Arg-Gly-Gly (RGG) box and interacts with human arginine methyltransferase HRMT1L1. Biochem J 2001; 358:305-314.
33. Miranda TB, Webb KJ, Edberg DD, Reeves R, Clarke S. Protein arginine methyltransferase 6 specifically methylates the non-histone chromatin protein HMGA1a. Biochem Biophys Res Commun 2005; 336:831-835.
34. Sgarra R, Lee J, Tessari MA, Altamura S, Spolaore B, Giancotti V, et al. The AT-hook of the chromatin architectural transcription factor high mobility group A1a is arginine-methylated by protein arginine methyltransferase 6. J Biol Chem 2006; 281:3764-3772.
35. Andaloussi N, Valovka T, Toveille M, Steinacher R, Focke F, Gehrig P, et al. Arginine methylation regulates DNA polymerase β. Mol Cell 2006; 22:51-62.
36. Bannister AJ, Schneider R, Kouzarides T. Histone methylation: dynamic or static? Cell 2002; 109:801-806.
37. Cuthbert GL, Daujat S, Snowden AW, Erdjument-Bromage H, Hagiwara T, Yamada M, et al. Histone deimination antagonizes arginine methylation. Cell 2004; 118:545-553.
38. Wang Y, Wysocka J, Sayegh J, Lee YH, Perlin JR, Leonelli L, et al. Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 2004; 306:279-283.
39. Li YJ, Stallcup MR, Lai MM. Hepatitis delta virus antigen is methylated at arginine residues, and methylation regulates subcellular localization and RNA replication. J Virol 2004; 78:13325- 13334.
40. Duong FH, Christen V, Berke JM, Penna SH, Moradpour D, Heim MH. Upregulation of protein phosphatase 2Ac by hepatitis C virus modulates NS3 helicase activity through inhibition of protein arginine methyltransferase 1. J Virol 2005; 79:15342-15350.
41. Boulanger MC, Liang C, Russell RS, Lin R, Bedford MT, Wainberg MA, et al. Methylation of Tat by PRMT6 regulates human immunodeficiency virus type 1 gene expression. J Virol 2005; 79:124-131.
42. Kwak YT, Guo J, Prajapati S, Park KJ, Surabhi RM, Miller B, et al. Methylation of SPT5 regulates its interaction with RNA polymerase II and transcriptional elongation properties. Mol Cell 2003; 11:1055-1066.
43. Kameoka M, Rong L, Gotte M, Liang C, Russell RS, Wainberg MA. Role for human immunodeficiency virus type 1 Tat protein in suppression of viral reverse transcriptase activity during late stages of viral replication. J Virol 2001; 75:2675-2683.
44. Frankel FA, Marchand B, Turner D, Gotte M, Wainberg MA. Impaired rescue of chain-terminated DNA synthesis associated with the L74V mutation in human immunodeficiency virus type 1 reverse transcriptase. Antimicrob Agents Chemother 2005; 49:2657-2664.
45. Liang C, Rong L, Gotte M, Li X, Quan Y, Kleiman L, et al. Mechanistic studies of early pausing events during initiation of HIV-1 reverse transcription. J Biol Chem 1998; 273:21309-21315.
46. Salomon H, Belmonte A, Nguyen K, Gu Z, Gelfand M, Wainberg MA. Comparison of cord blood and peripheral blood mononuclear cells as targets for viral isolation and drug sensitivity studies involving human immunodeficiency virus type 1. J Clin Microbiol 1994; 32:2000-2002.
47. Wei X, Liang C, Gotte M, Wainberg MA. Negative effect of the M184V mutation in HIV-1 reverse transcriptase on initiation of viral DNA synthesis. Virology 2003; 311:202-212.
48. Li X, Quan Y, Arts EJ, Li Z, Preston BD, De Rocquigny H, et al. Human immunodeficiency virus type 1 nucleocapsid protein (NCp7) directs specific initiation of minus-strand DNA synthesis primed by human tRNA(Lys3) in vitro: studies of viral RNA molecules mutated in regions that flank the primer binding site. J Virol 1996; 70:4996-5004.