Direct evidence that RNA inhibits APOBEC3G ssDNA cytidine deaminase activity

Biochemical and Biophysical Research Communications

Volumn 412, Issue 4, 2011, Pages 612-617

  McDougall, William M ^a   Smith, Harold C ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

APOBEC; Deaminase; HIV; Ribonucleotprotein; RNA; SsDNA

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; VIRUS RNA;

ARTICLE; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RNA SEQUENCE;

CYTIDINE DEAMINASE; DNA, SINGLE-STRANDED; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HUMANS; RIBONUCLEOPROTEINS; RNA; SUBSTRATE SPECIFICITY;

EID: 80052614833     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2011.08.009     Document Type: Article

References (41)

1. Harris R.S., Petersen-Mahrt S.K., Neuberger M.S. RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol. Cell 2002, 10:1247-1253.
2. Jarmuz A., Chester A., Bayliss J., Gisbourne J., Dunham I., Scott J., Navaratnam N. An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 2002, 79:285-296.
3. Wedekind J.E., Dance G.S., Sowden M.P., Smith H.C. Messenger RNA editing in mammals: new members of the APOBEC family seeking roles in the family business. Trends in Genetics: TIG 2003, 19:207-216.
4. Newman E.N., Holmes R.K., Craig H.M., Klein K.C., Lingappa J.R., Malim M.H., Sheehy A.M. Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr. Biol. 2005, 15:166-170.
5. Hache G., Liddament M.T., Harris R.S. The retroviral hypermutation specificity of APOBEC3F and APOBEC3G is governed by the C-terminal DNA cytosine deaminase domain. J. Biol. Chem. 2005, 280:10920-10924.
6. Bishop K.N., Holmes R.K., Sheehy A.M., Davidson N.O., Cho S.J., Malim M.H. Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr. Biol. 2004, 14:1392-1396.
7. Sheehy A.M., Gaddis N.C., Choi J.D., Malim M.H. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002, 418:646-650.
8. Yu Q., Konig R., Pillai S., Chiles K., Kearney M., Palmer S., Richman D., Coffin J.M., Landau N.R. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 2004, 11:435-442.
9. Suspene R., Sommer P., Henry M., Ferris S., Guetard D., Pochet S., Chester A., Navaratnam N., Wain-Hobson S., Vartanian J.P. APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase. Nucleic Acids Res. 2004, 32:2421-2429.
10. Schrofelbauer B., Yu Q., Zeitlin S.G., Landau N.R. Human immunodeficiency virus type 1 Vpr induces the degradation of the UNG and SMUG uracil-DNA glycosylases. J. Virol. 2005, 79:10978-10987.
11. Mangeat B., Turelli P., Caron G., Friedli M., Perrin L., Trono D. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 2003, 424:99-103.
12. Zhang H., Yang B., Pomerantz R.J., Zhang C., Arunachalam S.C., Gao L. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 2003, 424:94-98.
13. Lecossier D., Bouchonnet F., Clavel F., Hance A.J. Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 2003, 300:1112.
14. Mariani R., Chen D., Schrofelbauer B., Navarro F., Konig R., Bollman B., Munk C., Nymark-McMahon H., Landau N.R. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 2003, 114:21-31.
15. Stopak K., De Noronha C., Yonemoto W., Greene W.C. HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol. Cell 2003, 12:591-601.
16. Bishop K.N., Verma M., Kim E.Y., Wolinsky S.M., Malim M.H. APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog. 2008, 4:e1000231.
17. Guo F., Cen S., Niu M., Yang Y., Gorelick R.J., Kleiman L. The interaction of APOBEC3G with human immunodeficiency virus type 1 nucleocapsid inhibits tRNA3Lys annealing to viral RNA. J. Virol. 2007, 81:11322-11331.
18. Goila-Gaur R., Khan M.A., Miyagi E., Strebel K. Differential sensitivity of Old Versus " new" APOBEC3G to human immunodeficiency virus type 1 vif. J. Virol. 2009, 83:1156-1160.
19. Soros V.B., Yonemoto W., Greene W.C. Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA, and subsequently activated by RNase H. PLoS Pathog. 2007, 3:e15.
20. Svarovskaia E.S., Xu H., Mbisa J.L., Barr R., Gorelick R.J., Ono A., Freed E.O., Hu W.S., Pathak V.K. Human APOBEC3G is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J. Biol. Chem. 2004.
21. Friew Y.N., Boyko V., Hu W.S., Pathak V.K. Intracellular interactions between APOBEC3G, RNA, and HIV-1 Gag: APOBEC3G multimerization is dependent on its association with RNA. Retrovirology 2009, 6:56.
22. Gallois-Montbrun S., Kramer B., Swanson C.M., Byers H., Lynham S., Ward M., Malim M.H. Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J. Virol. 2007, 81:2165-2178.
23. Kreisberg J.F., Yonemoto W., Greene W.C. Endogenous factors enhance HIV infection of tissue naive CD4 T cells by stimulating high molecular mass APOBEC3G complex formation. J. Exp. Med. 2006, 203:865-870.
24. Wichroski M.J., Robb G.B., Rana T.M. Human retroviral host restriction factors APOBEC3G and APOBEC3F localize to mRNA processing bodies. PLoS Pathog. 2006, 2:e41.
25. Chiu Y.L., Greene W.C. Multifaceted antiviral actions of APOBEC3 cytidine deaminases. Trends Immunol. 2006, 27:291-297.
26. Salter J.D., Krucinska J., Raina J., Smith H.C., Wedekind J.E. A hydrodynamic analysis of APOBEC3G reveals a monomer-dimer-tetramer self-association that has implications for anti-HIV function. Biochemistry 2009, 48:10685-10687.
27. Wedekind J.E., Gillilan R., Janda A., Krucinska J., Salter J.D., Bennett R.P., Raina J., Smith H.C. Nanostructures of APOBEC3G support a hierarchical assembly model of high molecular mass ribonucleoprotein particles from dimeric subunits. J. Biol. Chem. 2006, 281:38122-38126.
28. Smith H.C. APOBEC3G: a double agent in defense. Trends Biochem. Sci. 2011, 36:239-244.
29. Smith H.C. Analysis of protein complexes assembled on apolipoprotein B mRNA for mooring sequence-dependent RNA editing. Methods 1998, 15:27-39.
30. Iwatani Y., Takeuchi H., Strebel K., Levin J.G. Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect. J. Virol. 2006, 80:5992-6002.
31. McDougall W.M., Okany C., Smith H.C. Deaminase activity on ssDNA occurred in vitro when APOBEC3G forms homotetramers and higher-order complexes. J. Biol. Chem. 2011.
32. Navarro F., Bollman B., Chen H., Konig R., Yu Q., Chiles K., Landau N.R. Complementary function of the two catalytic domains of APOBEC3G. Virology 2005, 333:374-386.
33. Wang T., Tian C., Zhang W., Luo K., Sarkis P.T., Yu L., Liu B., Yu Y., Yu X.F. 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J. Virol. 2007, 81:13112-13124.
34. Bennett R.P., Salter J.D., Liu X., Wedekind J.E., Smith H.C. APOBEC3G subunits self-associate via the C-terminal deaminase domain. J. Biol. Chem. 2008, 283:33329-33336.
35. Huthoff H., Autore F., Gallois-Montbrun S., Fraternali F., Malim M.H. RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog. 2009, 5:e1000330.
36. Chelico L., Prochnow C., Erie D.A., Chen X.S., Goodman M.F. Structural model for deoxycytidine deamination mechanisms of the HIV-1 inactivation enzyme APOBEC3G. J. Biol. Chem. 2010, 285:16195-16205.
37. Shlyakhtenko L.S., Lushnikov A.Y., Li M., Lackey L., Harris R.S., Lyubchenko Y.L. Atomic force microscopy studies provide direct evidence for dimerization of the HIV restriction factor APOBEC3G. J. Biol. Chem. 2011, 286:3387-3395.
38. Bennett R.P., Salter J.D., Liu X., Wedekind J.E., Smith H.C. APOBEC3G subunits self-associate via the C-terminal deaminase domain. J. Biol. Chem. 2008, 283:33329-33336.
39. Stopak K.S., Chiu Y.L., Kropp J., Grant R.M., Greene W.C. Distinct patterns of cytokine regulation of APOBEC3G expression and activity in primary lymphocytes, macrophages, and dendritic cells. J. Biol. Chem. 2007, 282:3539-3546.
40. Douaisi M., Dussart S., Courcoul M., Bessou G., Lerner E.C., 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.
41. Demorest Z.L., Li M., Harris R.S. Phosphorylation directly regulates the intrinsic DNA cytidine deaminase activity of aid and APOBEC3G. J. Biol. Chem. 2011.