Comparison of the replication and persistence of simian-human immunodeficiency viruses expressing Vif proteins with mutation of the SLQYLA or HCCH domains in macaques

Virology

Volumn 404, Issue 2, 2010, Pages 187-203

  Schmitt, Kimberly ^a   Hill, M Sarah ^a   Liu, Zhenqian ^a   Ruiz, Autumn ^a   Culley, Nathan ^b   Pinson, David M ^a   Stephens, Edward B ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

APOBEC3F; APOBEC3G; BC box; Replication; Rhesus macaques; SHIV; Simian human immunodeficiency virus; Vif; Zn binding motif

Indexed keywords

ALANINE; CD4 ANTIGEN; GLYCINE; NEF PROTEIN; VIF PROTEIN; VPU PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; GENE MUTATION; GENE SEQUENCE; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VIVO STUDY; MACACA; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL GENETICS; VIRUS LOAD; VIRUS REPLICATION; VIRUS VIRULENCE;

ANIMALS; ANTIBODIES, VIRAL; CELL LINE; GENE PRODUCTS, VIF; HIV-1; HUMANS; LYMPHOCYTES; MACACA MULATTA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN STRUCTURE, TERTIARY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIRAL LOAD; VIRUS REPLICATION;

EID: 77954535463     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.04.017     Document Type: Article

References (55)

1. Baba T.W., Jeong Y.S., Pennick D., Bronson R., Greene M.F., Ruprecht R.M. Pathogenicity of live, attenuated SIV after mucosal infection of neonatal macaques. Science 1995, 267:1820-1825.
2. Baba T.W., Liska V., Khimani A.H., Ray N.B., Dailey P.J., Penninck D., Bronson R., Greene M.F., McClure H.M., Martin L.N., Ruprecht R.M. Live attenuated, multiply deleted simian immunodeficiency virus causes AIDS in infant and adult macaques. Nat. Med. 1999, 5:194-203.
3. Borman A.M., Quillent C., Charneau P., Dauguet C., Clavel F. Human immunodeficiency virus type 1 Vif-mutant particles from restrictive cells: role of Vif in correct particle assembly and infectivity. J. Virol. 1995, 69:2058-2067.
4. Blanc D., Patience C., Schulz T.F., Weiss R., Spire B. Transcomplementation of VIF-HIV-1 mutants in CEM cells suggests that VIF affects late steps of the viral life cycle. Virology 1993, 193:186-192.
5. Chen G., He Z., Wang T., Xu R., Yu X.F. A patch of positively charged amino acids surrounding the human immunodeficiency virus type 1 Vif SLVx4Yx9Y motif influences its interaction with APOBEC3G. J. Virol. 2009, 83:8674-8682.
6. Dang Y., Wang X., Zhou T., York I.A., Zheng Y.H. Identification of a novel WxSLVK motif in the N terminus of human immunodeficiency virus and simian immunodeficiency virus Vif that is critical for APOBEC3G and APOBEC3F neutralization. J. Virol. 2009, 83:8544-8552.
7. Dang Y., Wang X., Esselman W.J., Zheng Y.-H. Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. J. Virol. 2006, 80:10522-10533.
8. Dang Y., Siew L.M., Wang X., Han Y., Lampen R., Zheng Y.H. Human cytidine deaminase APOBEC3H restricts HIV-1 replication. J. Biol. Chem. 2008, 283:11606-11614.
9. Derdeyn C.A., Decker J.M., Sfakianos J.N., Wu X., O'Brien W.A., Ratner L., Kappes J.C., Shaw G.M., Hunter E. Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J. Virol. 2000, 74:8358-8367.
10. Desrosiers R.C., Lifson J.D., Gibbs J.S., Czajak S.C., Howe A.Y., Arthur L.O., Johnson R.P. Identification of highly attenuated mutants of simian immunodeficiency virus. J. Virol. 1998, 72:1431-1437.
11. Doehle B.P., Schafer A., Cullen B.R. Human APOBEC3B is a potent inhibitor of HIV-1 infectivity and is resistant to Vif. Virology 2005, 339:281-288.
12. Fan L., Peden K. Cell-free transmission of Vif mutants of HIV-1. Virology 1992, 190:19-29.
13. Gabuzda D.H., Lawrence K., Langhoff E., Terwilliger E., Dorfman T., Haseltine W.A., Sodroski J. Role of vif in replication of human immunodeficiency virus type 1 in CD4+ T lymphocytes. J. Virol. 1992, 66:6489-6495.
14. Harris R.S., Bishop K.N., Sheehy A.M., Craig H.M., Petersen-Mahrt S.K., Watt I.N., Neuberger M.S., Malim M.H. DNA deamination mediates innate immunity to retroviral infection. Cell 2003, 113:803-809.
15. Hill M.S., Mulcahy E.R., Gomez L.M., Miller J.M., Berman N.E., Stephens E.B. APOBEC3G expression is restricted to neurons in the brains of macaques. AIDS Res. Hum. Retroviruses 2006, 22:541-550.
16. Hill M.S., Ruiz A., Gomez L.M., Miller J.M., Berman N.E., Stephens E.B. APOBEC3G expression is restricted to epithelial cells of the proximal convoluted tubules and is not expressed in the glomeruli of macaques. J. Histochem. Cytochem. 2007, 55:63-70.
17. Hill M.S., Ruiz A., Pacyniak E., Pinson D.M., Culley N., Yen B., Wong S.W., Stephens E.B. Modulation of the severe CD4+ T-cell los caused by a pathogenic simian-human immunodeficiency virus by replacement of the subtype B vpu from a subtype C HIV-1 clinical isolate. Virology 2008, 371(1):86-97.
18. Hofmann-Lehmann R., Swenerton R.K., Liska V., Leutenegger C.M., Lutz H., McClure H.M., Ruprecht R.M. Sensitive and robust one-tube real-time reverse transcriptase-polymerase chain reaction to quantify SIV RNA load: comparison of one- versus two-enzyme systems. AIDS Res. Hum. Retroviruses 2000, 16:1247-1257.
19. TM) that is less pathogenic for pig-tailed macaques. Virology 2005, 339:56-69.
20. KU1bMC33) with that of M2 of influenza A results in a virus that is sensitive to inhibitors of the M2 ion channel and is pathogenic for pig-tailed macaques. Virology 2006, 344:541-559.
21. 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.
22. Joag S.V., Li Z., Wang C., Jia F., Foresman L., Adany I., Pinson D.M., Stephens E.B., Narayan O. Chimeric SHIV that causes CD4+ T cell loss and AIDS in rhesus macaques. J. Med. Primatol. 1998, 27(2-3):59-64.
23. Kim E.Y., Busch M., Abel K., Fritts L., Bustamante P., Stanton J., Lu D., Wu S., Glowczwskie J., Rourke T., Bogdan D., Piatak M., Lifson J.D., Desrosiers R.C., Wolinsky S., Miller C.J. Retroviral recombination in vivo: viral replication patterns and genetic structure of simian immunodeficiency virus (SIV) populations in rhesus macaques after simultaneous or sequential intravaginal inoculation with SIVmac239Deltavpx/Deltavpr and SIVmac239Deltanef. J. Virol. 2005, 79:4886-4895.
24. Koff W.C., Johnson P.R., Watkins D.I., Burton D.R., Lifson J.D., Hasenkrug K.J., McDermott A.B., Schultz A., Zamb T.J., Boyle R., Desrosiers R.C. HIV vaccine design: insights from live attenuated SIV vaccines. Nat. Immunol. 2006, 7:19-23.
25. Luo K., Xiao Z., Ehrlich E., Yu Y., Liu B., Zheng S., Yu X.F. Primate lentiviral virion infectivity factors are substrate receptors that assemble with cullin 5-E3 ligase through a HCCH motif to suppress APOBEC3G. Proc. Natl Acad. Sci. USA 2005, 102:11444-11449.
26. 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.
27. Marcario J.K., Riazi M., Adany R.I., Kenjale H., Fleming K., Marquis J., Nemon O., Mayo S., Yankee T., Narayan O., Cheney P.D. Effect of morphine on the neuropathogenesis of SIVmac infection in Indian rhesus macaques. J. Neuroimmune Pharmacol. 2008, 3(12):12-25.
28. 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.
29. Mehle A., Goncalves J., Santa-Marta M., McPike M., Gabuzda D. Phosphorylation of a novel SOCS-box and upstream cysteines. Genes Dev. 2004, 18:2867-2872.
30. Mehle A., Strack B., Ancuta P., Zhang C., McPike M., Gabuzda D. Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J. Biol. Chem. 2004, 279:7792-7798.
31. Mehle A., Thomas E.R., Rajendran K.S., Gabuzda D. A zinc-binding region in Vif binds Cul5 and determines cullin selection. J. Biol. Chem. 2006, 281:17259-17265.
32. Mehle A., Wilson H., Zhang C., Brazier A.J., McPike M., Pery E., Gabuzda D. Identification of an APOBEC3G binding site in human immunodeficiency virus type1 Vif and inhibitors of Vif-APOBEC3G binding. J. Virol. 2007, 81:13235-13241.
33. Pery E., Rajendran K.S., Brazier A.J., Gabuzda D. Regulation of APOBEC3 proteins by a novel YXXL motif in human immunodeficiency virus type 1 Vif and simian immunodeficiency virus SIVagm Vif 2009.
34. Russell R.A., Pathak V.K. Identification of two distinct human immunodeficiency virus type 1 Vif determinants critical for interactions with human APOBEC3G and APOBEC3F. J. Virol. 2007, 81:8201-8210.
35. Sakai H., Shibata R., Sakuragi J., Sakuragi S., Kawamura M., Adachi A. Cell-dependent requirement of human immunodeficiency virus type 1 Vif protein for maturation of virus particles. J. Virol. 1993, 67:1663-1666.
36. Schmitt K., Hill M.S., Ruiz A., Culley N., Pinson D.M., Wong S.W., Stephens E.B. Mutations in the highly conserved SLQYLA motif of Vif in a simian-human immunodeficiency virus result in a less pathogenic virus and are associated with G-to-A mutations in the viral genome. Virology 2009, 383:362-372.
37. Sheehy A.M., Gaddis N.C., Malim M.H. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat. Med. 2003, 9:1404-1407.
38. Shindo K., Takaori-Kondo A., Kobayashi M., Abudu A., Fukunaga K., Uchiyama T. The enzymatic activity of CEM15/Apobec-3G is essential for the regulation of the infectivity of HIV-1 virion but not a sole determinant of its antiviral activity. J. Biol. Chem. 2003, 278:44412-44416.
39. KU-lbMC33 in pig-tailed macaques. Virology 2003, 313:435-451.
40. Sparger E.E., Dubie R.A., Shacklett B.L., Cole K.S., Chang W.L., Luciw P.A. Vaccination of rhesus macaques with a vif-deleted simian human immunodeficiency virus proviral DNA vaccine. Virology 2008, 374:261-272.
41. Stephens E.B., McCormick C., Pacyniak E., Griffin D., Pinson D.M., Sun F., Nothnick W., Wong S.W., Gunderson R., Berman N.E., Singh D.K. Deletion of the vpu sequences prior to the env in a simian-human immunodeficiency virus results in enhanced Env precursor synthesis but is less pathogenic for pig-tailed macaques. Virology 2002, 293:252-261.
42. 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.
43. von Schwedler U., Song J., Aiken C., Trono D. Vif is crucial for human immunodeficiency virus type 1 proviral DNA synthesis in infected cells. J. Virol. 1993, 67:4945-4955.
44. Virgen C.A., Hatziioannou T. Antiretroviral activity and Vif sensitivity of rhesus macaque APOBEC3 proteins. J. Virol. 2007, 81:13932-13937.
45. Wei X., Decker J.M., Liu H., Zhang Z., Arani R.B., Kilby J.M., Saag M.S., Wu X., Shaw G.M., Kappes J.C. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 2000, 46:1896-1905.
46. Wiegand H.L., Doehle B.P., Bogerd H.P., Cullen B.R. A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J. 2004, 23:2451-2488.
47. Xiao Z., Xiong Y., Zhang W., Tan L., Ehrlich E., Guo D., Yu X.F. Characterization of a novel Cullin5 binding domain in HIV-1 Vif. J. Mol. Biol. 2007, 373:541-550.
48. Yang Y., Guo F., Cen S., Kleiman L. Inhibition of initiation of reverse transcription in HIV-1 by human APOBEC3F. Virology 2007, 365:92-100.
49. 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.
50. Yu Q., Chen D., Konig R., Mariani R., Unutmaz D., Landau N.R. APOBEC3B and APOBEC3C are potent inhibitors of simian immunodeficiency virus replication. J. Biol. Chem. 2004, 279:53379-53386.
51. Yu X., Yu Y., Liu B., Luo K., Kong W., Mao P., Yu X.F. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 2003, 302:1056-1060.
52. Yu Y., Xiao Z., Ehrlich E.S., Yu X., Yu X.F. Selective assembly of HIV-1 Vif-Cul5-ElonginB-ElonginC E3 ubiquitin ligase complex through a novel SOCS box and upstream cysteines. Genes Dev. 2004, 18:2867-2872.
53. Zennou V., Bieniasz P.D. Comparative analysis of the antiretroviral activity of APOBEC3G and APOBEC3F from primates. Virology 2006, 349:31-40.
54. 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.
55. Zheng Y.H., Irwin D., Kurosu T., Tokunaga K., Sata T., Peterlin B.M. Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication. J. Virol. 2004, 78:6072-6076.