Emerging complexities of APOBEC3G action on immunity and viral fitness during HIV infection and treatment

Retrovirology

Volumn 9, Issue , 2012, Pages

  Monajemi, Mahdis ^a   Woodworth, Claire F ^a   Benkaroun, Jessica ^a   Grant, Michael ^a   Larijani, Mani ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABACAVIR; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; DELAVIRDINE; DIDANOSINE; EFAVIRENZ; LAMIVUDINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEVIRAPINE; VIF PROTEIN;

ADAPTIVE IMMUNITY; ANTIGEN EXPRESSION; ANTIVIRAL RESISTANCE; APOBEC3G GENE; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL DIFFERENTIATION; CYTOTOXIC T LYMPHOCYTE; GENE ACTIVITY; GENE MUTATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNITY; INNATE IMMUNITY; MACROPHAGE; MONOCYTE; NONHUMAN; PATHOGENESIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; VIRUS GENE; VIRUS GENOME; VIRUS REPLICATION;

ADAPTATION, BIOLOGICAL; ADAPTIVE IMMUNITY; ANIMALS; ANTI-HIV AGENTS; CYTOSINE DEAMINASE; DRUG RESISTANCE, VIRAL; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, VIRAL; GENOME, VIRAL; HIV; HIV INFECTIONS; HUMANS; IMMUNE EVASION; MUTATION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84862171038     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-9-35     Document Type: Article

References (164)

1. Sheehy AM, Gaddis NC, Choi JD, Malim MH. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 2002, 418:646-650. 10.1038/nature00939, 12167863.
2. Chiu YL, Soros VB, Kreisberg JF, Stopak K, Yonemoto W, Greene WC. Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells. Nature 2005, 435:108-114. 10.1038/nature03493, 15829920.
3. Conticello SG, Thomas CJ, Petersen-Mahrt SK, Neuberger MS. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol Biol Evol 2005, 22:367-377.
4. 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. 10.1006/geno.2002.6718, 11863358.
5. Conticello SG. The AID/APOBEC family of nucleic acid mutators. Genome Biol 2008, 9:229. 2530864, 18671835.
6. Beale RC, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS. Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J Mol Biol 2004, 337:585-596. 10.1016/j.jmb.2004.01.046, 15019779.
7. Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN, Neuberger MS, Malim MH. DNA deamination mediates innate immunity to retroviral infection. Cell 2003, 113:803-809. 10.1016/S0092-8674(03)00423-9, 12809610.
8. Simon JH, Gaddis NC, Fouchier RA, Malim MH. Evidence for a newly discovered cellular anti-HIV-1 phenotype. Nat Med 1998, 4:1397-1400. 10.1038/3987, 9846577.
9. Madani N, Kabat D. An endogenous inhibitor of human immunodeficiency virus in human lymphocytes is overcome by the viral Vif protein. J Virol 1998, 72:10251-10255. 110608, 9811770.
10. Peng G, Greenwell-Wild T, Nares S, Jin W, Lei KJ, Rangel ZG, Munson PJ, Wahl SM. Myeloid differentiation and susceptibility to HIV-1 are linked to APOBEC3 expression. Blood 2007, 110:393-400. 10.1182/blood-2006-10-051763, 1896122, 17371941.
11. Pido-Lopez J, Whittall T, Wang Y, Bergmeier LA, Babaahmady K, Singh M, Lehner T. Stimulation of cell surface CCR5 and CD40 molecules by their ligands or by HSP70 up-regulates APOBEC3G expression in CD4(+) T cells and dendritic cells. J Immunol 2007, 178:1671-1679.
12. Stopak KS, Chiu YL, Kropp J, Grant RM, Greene WC. Distinct patterns of cytokine regulation of APOBEC3G expression and activity in primary lymphocytes, macrophages, and dendritic cells. J Biol Chem 2007, 282:3539-3546.
13. Koning FA, Newman EN, Kim EY, Kunstman KJ, Wolinsky SM, Malim MH. Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J Virol 2009, 83:9474-9485. 10.1128/JVI.01089-09, 2738220, 19587057.
14. Pion M, Granelli-Piperno A, Mangeat B, Stalder R, Correa R, Steinman RM, Piguet V. APOBEC3G/3 F mediates intrinsic resistance of monocyte-derived dendritic cells to HIV-1 infection. J Exp Med 2006, 203:2887-2893. 10.1084/jem.20061519, 2118170, 17145955.
15. Bonvin M, Achermann F, Greeve I, Stroka D, Keogh A, Inderbitzin D, Candinas D, Sommer P, Wain-Hobson S, Vartanian JP, Greeve J. Interferon-inducible expression of APOBEC3 editing enzymes in human hepatocytes and inhibition of hepatitis B virus replication. Hepatology 2006, 43:1364-1374. 10.1002/hep.21187, 16729314.
16. Komohara Y, Suekane S, Noguchi M, Matsuoka K, Yamada A, Itoh K. Expression of APOBEC3G in kidney cells. Tissue Antigens 2007, 69:95-98. 10.1111/j.1399-0039.2006.00725.x, 17212712.
17. Peng G, Lei KJ, Jin W, Greenwell-Wild T, Wahl SM. Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J Exp Med 2006, 203:41-46. 10.1084/jem.20051512, 2118075, 16418394.
18. Tanaka Y, Marusawa H, Seno H, Matsumoto Y, Ueda Y, Kodama Y, Endo Y, Yamauchi J, Matsumoto T, Takaori-Kondo A, et al. Anti-viral protein APOBEC3G is induced by interferon-alpha stimulation in human hepatocytes. Biochem Biophys Res Commun 2006, 341:314-319. 10.1016/j.bbrc.2005.12.192, 16426578.
19. Yu Q, Konig R, Pillai S, Chiles K, Kearney M, Palmer S, Richman D, Coffin JM, Landau NR. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat Struct Mol Biol 2004, 11:435-442. 10.1038/nsmb758, 15098018.
20. Lecossier D, Bouchonnet F, Clavel F, Hance AJ. Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 2003, 300:1112. 10.1126/science.1083338, 12750511.
21. 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. 10.1038/nature01709, 12808466.
22. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, Gao L. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 2003, 424:94-98. 10.1038/nature01707, 1350966, 12808465.
23. Klarmann GJ, Chen X, North TW, Preston BD. Incorporation of uracil into minus strand DNA affects the specificity of plus strand synthesis initiation during lentiviral reverse transcription. J Biol Chem 2003, 278:7902-7909. 10.1074/jbc.M207223200, 12458216.
24. Mbisa JL, Barr R, Thomas JA, Vandegraaff N, Dorweiler IJ, Svarovskaia ES, Brown WL, Mansky LM, Gorelick RJ, Harris RS, et al. Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plus-strand DNA transfer and integration. J Virol 2007, 81:7099-7110. 10.1128/JVI.00272-07, 1933301, 17428871.
25. Simon V, Zennou V, Murray D, Huang Y, Ho DD, Bieniasz PD. Natural variation in Vif: differential impact on APOBEC3G/3 F and a potential role in HIV-1 diversification. PLoS Pathog 2005, 1:e6. 10.1371/journal.ppat.0010006, 1238741, 16201018.
26. Newman EN, Holmes RK, Craig HM, Klein KC, Lingappa JR, Malim MH, Sheehy AM. Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol 2005, 15:166-170. 10.1016/j.cub.2004.12.068, 15668174.
27. Anderson JL, Hope TJ. APOBEC3G restricts early HIV-1 replication in the cytoplasm of target cells. Virology 2008, 375:1-12. 10.1016/j.virol.2008.01.042, 2679893, 18308358.
28. Li XY, Guo F, Zhang L, Kleiman L, Cen S. APOBEC3G inhibits DNA strand transfer during HIV-1 reverse transcription. J Biol Chem 2007, 282:32065-32074. 10.1074/jbc.M703423200, 17855362.
29. Navarro F, Bollman B, Chen H, Konig R, Yu Q, Chiles K, Landau NR. Complementary function of the two catalytic domains of APOBEC3G. Virology 2005, 333:374-386. 10.1016/j.virol.2005.01.011, 15721369.
30. Luo K, Wang T, Liu B, Tian C, Xiao Z, Kappes J, Yu XF. Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. J Virol 2007, 81:7238-7248. 10.1128/JVI.02584-06, 1933265, 17428847.
31. Mbisa JL, Bu W, Pathak VK. APOBEC3F and APOBEC3G inhibit HIV-1 DNA integration by different mechanisms. J Virol 2010, 84:5250-5259. 10.1128/JVI.02358-09, 2863843, 20219927.
32. Guo F, Cen S, Niu M, Yang Y, Gorelick RJ, 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. 10.1128/JVI.00162-07, 2045548, 17670826.
33. Wang X, Ao Z, Chen L, Kobinger G, Peng J, Yao X. The Cellular Antiviral Protein APOBEC3G Interacts with HIV-1 Reverse Transcriptase and Inhibits Its Function during Viral Replication. J Virol 2012, 86:3777-3786. 10.1128/JVI.06594-11, 22301159.
34. Browne EP, Allers C, Landau NR. Restriction of HIV-1 by APOBEC3G is cytidine deaminase-dependent. Virology 2009, 387:313-321. 10.1016/j.virol.2009.02.026, 19304304.
35. Smith HC. APOBEC3G: a double agent in defense. Trends Biochem Sci 2011, 36:239-244. 10.1016/j.tibs.2010.12.003, 3086942, 21239176.
36. Miyagi E, Opi S, Takeuchi H, Khan M, Goila-Gaur R, Kao S, Strebel K. Enzymatically active APOBEC3G is required for efficient inhibition of human immunodeficiency virus type 1. J Virol 2007, 81:13346-13353. 10.1128/JVI.01361-07, 2168852, 17928335.
37. Schumacher AJ, Nissley DV, Harris RS. APOBEC3G hypermutates genomic DNA and inhibits Ty1 retrotransposition in yeast. Proc Natl Acad Sci U S A 2005, 102:9854-9859. 10.1073/pnas.0501694102, 1172225, 16000409.
38. Schumacher AJ, Hache G, Macduff DA, Brown WL, Harris RS. The DNA deaminase activity of human APOBEC3G is required for Ty1, MusD, and human immunodeficiency virus type 1 restriction. J Virol 2008, 82:2652-2660. 10.1128/JVI.02391-07, 2259018, 18184715.
39. Holmes RK, Koning FA, Bishop KN, Malim MH. APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G. J Biol Chem 2007, 282(4):2587-2595. Epub 2006 Nov 22.
40. Stenglein MD, Harris RS. APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J Biol Chem 2006, 281:16837-16841. 10.1074/jbc.M602367200, 16648136.
41. Muckenfuss H, Hamdorf M, Held U, Perkovic M, Lower J, Cichutek K, Flory E, Schumann GG, Munk C. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 2006, 281:22161-22172. 10.1074/jbc.M601716200, 16735504.
42. Turelli P, Mangeat B, Jost S, Vianin S, Trono D. Inhibition of hepatitis B virus replication by APOBEC3G. Science 1829, 2004:303.
43. Bogerd HP, Wiegand HL, Hulme AE, Garcia-Perez JL, O'Shea KS, Moran JV, Cullen BR. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc Natl Acad Sci U S A 2006, 103:8780-8785. 10.1073/pnas.0603313103, 1482655, 16728505.
44. Esnault C, Heidmann O, Delebecque F, Dewannieux M, Ribet D, Hance AJ, Heidmann T, Schwartz O. APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 2005, 433:430-433. 10.1038/nature03238, 15674295.
45. Esnault C, Millet J, Schwartz O, Heidmann T. Dual inhibitory effects of APOBEC family proteins on retrotransposition of mammalian endogenous retroviruses. Nucleic Acids Res 2006, 34:1522-1531. 10.1093/nar/gkl054, 1401513, 16537839.
46. Chiu YL, Witkowska HE, Hall SC, Santiago M, Soros VB, Esnault C, Heidmann T, Greene WC. High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition. Proc Natl Acad Sci U S A 2006, 103:15588-15593. 10.1073/pnas.0604524103, 1592537, 17030807.
47. Zhang J, Webb DM. Rapid evolution of primate antiviral enzyme APOBEC3G. Hum Mol Genet 2004, 13:1785-1791. 10.1093/hmg/ddh183, 15198990.
48. Wedekind JE, Dance GS, Sowden MP, Smith HC. Messenger RNA editing in mammals: new members of the APOBEC family seeking roles in the family business. Trends Genet 2003, 19:207-216. 10.1016/S0168-9525(03)00054-4, 12683974.
49. Do H, Vasilescu A, Diop G, Hirtzig T, Heath SC, Coulonges C, Rappaport J, Therwath A, Lathrop M, Matsuda F, Zagury JF. Exhaustive genotyping of the CEM15 (APOBEC3G) gene and absence of association with AIDS progression in a French cohort. J Infect Dis 2005, 191:159-163. 10.1086/426826, 15609224.
50. Sawyer SL, Emerman M, Malik HS. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2004, 2:E275. 10.1371/journal.pbio.0020275, 479043, 15269786.
51. Bizinoto MC, Leal E, Diaz RS, Janini LM. Loci polymorphisms of the APOBEC3G gene in HIV type 1-infected Brazilians. AIDS Res Hum Retroviruses 2011, 27:137-141. 10.1089/aid.2010.0146, 20874421.
52. An P, Bleiber G, Duggal P, Nelson G, May M, Mangeat B, Alobwede I, Trono D, Vlahov D, Donfield S, et al. APOBEC3G genetic variants and their influence on the progression to AIDS. J Virol 2004, 78:11070-11076. 10.1128/JVI.78.20.11070-11076.2004, 521814, 15452227.
53. Kieffer TL, Kwon P, Nettles RE, Han Y, Ray SC, Siliciano RF. G-A hypermutation in protease and reverse transcriptase regions of human immunodeficiency virus type 1 residing in resting CD4+ T cells in vivo. J Virol 2005, 79:1975-1980. 10.1128/JVI.79.3.1975-1980.2005, 544145, 15650227.
54. Pace C, Keller J, Nolan D, James I, Gaudieri S, Moore C, Mallal S. Population level analysis of human immunodeficiency virus type 1 hypermutation and its relationship with APOBEC3G and vif genetic variation. J Virol 2006, 80:9259-9269. 10.1128/JVI.00888-06, 1563905, 16940537.
55. Piantadosi A, Humes D, Chohan B, McClelland RS, Overbaugh J. Analysis of the percentage of human immunodeficiency virus type 1 sequences that are hypermutated and markers of disease progression in a longitudinal cohort, including one individual with a partially defective Vif. J Virol 2009, 83:7805-7814. 10.1128/JVI.00280-09, 2715790, 19494014.
56. Land AM, Ball TB, Luo M, Pilon R, Sandstrom P, Embree JE, Wachihi C, Kimani J, Plummer FA. Human immunodeficiency virus (HIV) type 1 proviral hypermutation correlates with CD4 count in HIV-infected women from Kenya. J Virol 2008, 82:8172-8182. 10.1128/JVI.01115-08, 2519552, 18550667.
57. Gandhi SK, Siliciano JD, Bailey JR, Siliciano RF, Blankson JN. Role of APOBEC3G/F-mediated hypermutation in the control of human immunodeficiency virus type 1 in elite suppressors. J Virol 2008, 82:3125-3130. 10.1128/JVI.01533-07, 2259015, 18077705.
58. Preston BD, Poiesz BJ, Loeb LA. Fidelity of HIV-1 reverse transcriptase. Science 1988, 242:1168-1171. 10.1126/science.2460924, 2460924.
59. Yu X, Yu Y, Liu B, Luo K, Kong W, Mao P, Yu XF. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 2003, 302:1056-1060. 10.1126/science.1089591, 14564014.
60. Santa-Marta M, da Silva FA, Fonseca AM, Goncalves J. HIV-1 Vif can directly inhibit apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3 G-mediated cytidine deamination by using a single amino acid interaction and without protein degradation. J Biol Chem 2005, 280:8765-8775.
61. Khan MA, Aberham C, Kao S, Akari H, Gorelick R, Bour S, Strebel K. Human immunodeficiency virus type 1 Vif protein is packaged into the nucleoprotein complex through an interaction with viral genomic RNA. J Virol 2001, 75:7252-7265. 10.1128/JVI.75.16.7252-7265.2001, 114961, 11461998.
62. Goncalves J, Santa-Marta M. HIV-1 Vif and APOBEC3G: multiple roads to one goal. Retrovirology 2004, 1:28. 10.1186/1742-4690-1-28, 521195, 15383144.
63. Sheehy AM, Gaddis NC, Malim MH. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med 2003, 9:1404-1407. 10.1038/nm945, 14528300.
64. 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.
65. Goila-Gaur R, Strebel K. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 2008, 5:51. 10.1186/1742-4690-5-51, 2443170, 18577210.
66. Stopak K, de Noronha C, Yonemoto W, Greene WC. HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol Cell 2003, 12:591-601. 10.1016/S1097-2765(03)00353-8, 14527406.
67. Strebel K, Luban J, Jeang KT. Human cellular restriction factors that target HIV-1 replication. BMC Med 2009, 7:48. 10.1186/1741-7015-7-48, 2759957, 19758442.
68. Conticello SG, Harris RS, Neuberger MS. The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr Biol 2003, 13:2009-2013. 10.1016/j.cub.2003.10.034, 14614829.
69. Kao S, Akari H, Khan MA, Dettenhofer M, Yu XF, Strebel K. Human immunodeficiency virus type 1 Vif is efficiently packaged into virions during productive but not chronic infection. J Virol 2003, 77:1131-1140. 10.1128/JVI.77.2.1131-1140.2003, 140813, 12502829.
70. Soros VB, Greene WC. APOBEC3G and HIV-1: strike and counterstrike. Curr Infect Dis Rep 2006, 8:317-323. 10.1007/s11908-006-0077-6, 16822376.
71. Svarovskaia ES, Xu H, Mbisa JL, Barr R, Gorelick RJ, Ono A, Freed EO, Hu WS, Pathak VK. Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3 G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J Biol Chem 2004, 279:35822-35828. 10.1074/jbc.M405761200, 15210704.
72. Alce TM, Popik W. APOBEC3G is incorporated into virus-like particles by a direct interaction with HIV-1 Gag nucleocapsid protein. J Biol Chem 2004, 279:34083-34086. 10.1074/jbc.C400235200, 15215254.
73. Ma J, Li X, Xu J, Zhang Q, Liu Z, Jia P, Zhou J, Guo F, You X, Yu L, et al. The cellular source for APOBEC3G's incorporation into HIV-1. Retrovirology 2011, 8:2. 10.1186/1742-4690-8-2, 3024284, 21211018.
74. Mariani R, Chen D, Schrofelbauer B, Navarro F, Konig R, Bollman B, Munk C, Nymark-McMahon H, Landau NR. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 2003, 114:21-31. 10.1016/S0092-8674(03)00515-4, 12859895.
75. Wissing S, Galloway NL, Greene WC. HIV-1 Vif versus the APOBEC3 cytidine deaminases: an intracellular duel between pathogen and host restriction factors. Mol Aspects Med 2010, 31:383-397. 10.1016/j.mam.2010.06.001, 2967609, 20538015.
76. Xu H, Chertova E, Chen J, Ott DE, Roser JD, Hu WS, Pathak VK. Stoichiometry of the antiviral protein APOBEC3G in HIV-1 virions. Virology 2007, 360:247-256. 10.1016/j.virol.2006.10.036, 17126871.
77. Mercenne G, Bernacchi S, Richer D, Bec G, Henriet S, Paillart JC, Marquet R. HIV-1 Vif binds to APOBEC3G mRNA and inhibits its translation. Nucleic Acids Res 2010, 38:633-646. 10.1093/nar/gkp1009, 2810999, 19910370.
78. Kao S, Khan MA, Miyagi E, Plishka R, Buckler-White A, Strebel K. The human immunodeficiency virus type 1 Vif protein reduces intracellular expression and inhibits packaging of APOBEC3G (CEM15), a cellular inhibitor of virus infectivity. J Virol 2003, 77:11398-11407. 10.1128/JVI.77.21.11398-11407.2003, 229358, 14557625.
79. Opi S, Kao S, Goila-Gaur R, Khan MA, Miyagi E, Takeuchi H, Strebel K. Human immunodeficiency virus type 1 Vif inhibits packaging and antiviral activity of a degradation-resistant APOBEC3G variant. J Virol 2007, 81:8236-8246. 10.1128/JVI.02694-06, 1951302, 17522211.
80. Kao S, Goila-Gaur R, Miyagi E, Khan MA, Opi S, Takeuchi H, Strebel K. Production of infectious virus and degradation of APOBEC3G are separable functional properties of human immunodeficiency virus type 1 Vif. Virology 2007, 369:329-339. 10.1016/j.virol.2007.08.005, 2129170, 17825339.
81. Jager S, Kim DY, Hultquist JF, Shindo K, LaRue RS, Kwon E, Li M, Anderson BD, Yen L, Stanley D, et al. Vif hijacks CBF-beta to degrade APOBEC3G and promote HIV-1 infection. Nature 2011, 481:371-375.
82. Zhang W, Du J, Evans SL, Yu Y, Yu XF. T-cell differentiation factor CBF-beta regulates HIV-1 Vif-mediated evasion of host restriction. Nature 2011, 481:376-379.
83. Hamilton CE, Papavasiliou FN, Rosenberg BR. Diverse functions for DNA and RNA editing in the immune system. RNA Biol 2010, 7:220-228. 10.4161/rna.7.2.11344, 20220309.
84. Sadler HA, Stenglein MD, Harris RS, Mansky LM. APOBEC3G contributes to HIV-1 variation through sublethal mutagenesis. J Virol 2010, 84:7396-7404. 10.1128/JVI.00056-10, 2898230, 20463080.
85. Goila-Gaur R, Khan MA, Miyagi E, Strebel K. Differential sensitivity of "old" versus "new" APOBEC3G to human immunodeficiency virus type 1 vif. J Virol 2009, 83:1156-1160. 10.1128/JVI.01734-08, 2612393, 19004939.
86. Sakai K, Dimas J, Lenardo MJ. The Vif and Vpr accessory proteins independently cause HIV-1-induced T cell cytopathicity and cell cycle arrest. Proc Natl Acad Sci U S A 2006, 103:3369-3374. 10.1073/pnas.0509417103, 1413893, 16492778.
87. Wang J, Shackelford JM, Casella CR, Shivers DK, Rapaport EL, Liu B, Yu XF, Finkel TH. The Vif accessory protein alters the cell cycle of human immunodeficiency virus type 1 infected cells. Virology 2007, 359:243-252. 10.1016/j.virol.2006.09.026, 1934563, 17056089.
88. Wang J, Shackelford JM, Selliah N, Shivers DK, O'Neill E, Garcia JV, Muthumani K, Weiner D, Yu XF, Gabuzda D, Finkel TH. The HIV-1 Vif protein mediates degradation of Vpr and reduces Vpr-induced cell cycle arrest. DNA Cell Biol 2008, 27:267-277. 10.1089/dna.2007.0707, 18462066.
89. DeHart JL, Bosque A, Harris RS, Planelles V. Human immunodeficiency virus type 1 Vif induces cell cycle delay via recruitment of the same E3 ubiquitin ligase complex that targets APOBEC3 proteins for degradation. J Virol 2008, 82:9265-9272. 10.1128/JVI.00377-08, 2546900, 18596088.
90. Chiu YL, Greene WC. APOBEC3G: an intracellular centurion. Philos Trans R Soc Lond B Biol Sci 2009, 364:689-703. 10.1098/rstb.2008.0193, 2660915, 19008196.
91. Kreisberg JF, Yonemoto W, Greene WC. 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. 10.1084/jem.20051856, 2118295, 16606671.
92. Chiu YL, Greene WC. The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu Rev Immunol 2008, 26:317-353. 10.1146/annurev.immunol.26.021607.090350, 18304004.
93. Wichroski MJ, Robb GB, Rana TM. Human retroviral host restriction factors APOBEC3G and APOBEC3F localize to mRNA processing bodies. PLoS Pathog 2006, 2:e41. 10.1371/journal.ppat.0020041, 1458959, 16699599.
94. Kozak SL, Marin M, Rose KM, Bystrom C, Kabat D. The anti-HIV-1 editing enzyme APOBEC3G binds HIV-1 RNA and messenger RNAs that shuttle between polysomes and stress granules. J Biol Chem 2006, 281:29105-29119. 10.1074/jbc.M601901200, 16887808.
95. Chiu YL. Biochemical fractionation and purification of high-molecular-mass APOBEC3G complexes. Methods Mol Biol 2011, 718:185-206. 10.1007/978-1-61779-018-8_12, 21370050.
96. Gallois-Montbrun S, Kramer B, Swanson CM, Byers H, Lynham S, Ward M, Malim MH. Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J Virol 2007, 81:2165-2178. 10.1128/JVI.02287-06, 1865933, 17166910.
97. Strebel K, Khan MA. APOBEC3G encapsidation into HIV-1 virions: which RNA is it?. Retrovirology 2008, 5:55. 10.1186/1742-4690-5-55, 2491656, 18597677.
98. Khan MA, Goila-Gaur R, Opi S, Miyagi E, Takeuchi H, Kao S, Strebel K. Analysis of the contribution of cellular and viral RNA to the packaging of APOBEC3G into HIV-1 virions. Retrovirology 2007, 4:48. 10.1186/1742-4690-4-48, 1948019, 17631688.
99. Khan MA, Kao S, Miyagi E, Takeuchi H, Goila-Gaur R, Opi S, Gipson CL, Parslow TG, Ly H, Strebel K. Viral RNA is required for the association of APOBEC3G with human immunodeficiency virus type 1 nucleoprotein complexes. J Virol 2005, 79:5870-5874. 10.1128/JVI.79.9.5870-5874.2005, 1082784, 15827203.
100. Wang T, Tian C, Zhang W, Luo K, Sarkis PT, Yu L, Liu B, Yu Y, Yu XF. 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J Virol 2007, 81:13112-13124. 10.1128/JVI.00892-07, 2169093, 17881443.
101. Onafuwa-Nuga AA, Telesnitsky A, King SR. 7SL RNA, but not the 54-kd signal recognition particle protein, is an abundant component of both infectious HIV-1 and minimal virus-like particles. RNA 2006, 12:542-546. 10.1261/rna.2306306, 1421090, 16489186.
102. Shandilya SM, Nalam MN, Nalivaika EA, Gross PJ, Valesano JC, Shindo K, Li M, Munson M, Royer WE, Harjes E, et al. Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 2010, 18:28-38. 10.1016/j.str.2009.10.016, 2913127, 20152150.
103. Chen KM, Harjes E, Gross PJ, Fahmy A, Lu Y, Shindo K, Harris RS, Matsuo H. Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 2008, 452:116-119. 10.1038/nature06638, 18288108.
104. Holden LG, Prochnow C, Chang YP, Bransteitter R, Chelico L, Sen U, Stevens RC, Goodman MF, Chen XS. Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 2008, 456:121-124. 10.1038/nature07357, 2714533, 18849968.
105. Huthoff H, Autore F, Gallois-Montbrun S, Fraternali F, Malim MH. RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog 2009, 5:e1000330. 10.1371/journal.ppat.1000330, 2646141, 19266078.
106. Wang X, Dolan PT, Dang Y, Zheng YH. Biochemical differentiation of APOBEC3F and APOBEC3G proteins associated with HIV-1 life cycle. J Biol Chem 2007, 282:1585-1594. 1880894, 17142455.
107. Kamata M, Nagaoka Y, Chen IS. Reassessing the role of APOBEC3G in human immunodeficiency virus type 1 infection of quiescent CD4+ T-cells. PLoS Pathog 2009, 5:e1000342. 10.1371/journal.ppat.1000342, 2652112, 19300495.
108. de Sio FR S, Trono D. APOBEC3G-depleted resting CD4+ T cells remain refractory to HIV1 infection. PLoS One 2009, 4:6571.
109. Goila-Gaur R, Khan MA, Miyagi E, Kao S, Opi S, Takeuchi H, Strebel K. HIV-1 Vif promotes the formation of high molecular mass APOBEC3G complexes. Virology 2008, 372:136-146. 10.1016/j.virol.2007.10.017, 2396953, 18023836.
110. Johnson VA, Calvez V, Gunthard HF, Paredes R, Pillay D, Shafer R, Wensing AM, Richman DD. 2011 update of the drug resistance mutations in HIV-1. Top Antivir Med 2011, 19:156-164.
111. Berkhout B, de Ronde A. APOBEC3G versus reverse transcriptase in the generation of HIV-1 drug-resistance mutations. AIDS 2004, 18:1861-1863. 10.1097/00002030-200409030-00022, 15316354.
112. Jern P, Russell RA, Pathak VK, Coffin JM. Likely role of APOBEC3G-mediated G-to-A mutations in HIV-1 evolution and drug resistance. PLoS Pathog 2009, 5:e1000367. 10.1371/journal.ppat.1000367, 2659435, 19343218.
113. Suspene R, Rusniok C, Vartanian JP, Wain-Hobson S. Twin gradients in APOBEC3 edited HIV-1 DNA reflect the dynamics of lentiviral replication. Nucleic Acids Res 2006, 34:4677-4684. 10.1093/nar/gkl555, 1635257, 16963778.
114. Mulder LC, Harari A, Simon V. Cytidine deamination induced HIV-1 drug resistance. Proc Natl Acad Sci U S A 2008, 105:5501-5506. 10.1073/pnas.0710190105, 2291111, 18391217.
115. Dang Y, Wang X, Zhou T, York IA, Zheng YH. 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. 10.1128/JVI.00651-09, 2738151, 19535447.
116. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 1994, 68:6103-6110. 237022, 8057491.
117. Rinaldo C, Huang XL, Fan ZF, Ding M, Beltz L, Logar A, Panicali D, Mazzara G, Liebmann J, Cottrill M, et al. High levels of anti-human immunodeficiency virus type 1 (HIV-1) memory cytotoxic T-lymphocyte activity and low viral load are associated with lack of disease in HIV-1-infected long-term nonprogressors. J Virol 1995, 69:5838-5842. 189455, 7637030.
118. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, Borkowsky W, Farthing C, Ho DD. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 1994, 68:4650-4655. 236393, 8207839.
119. Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 2008, 9:267-276.
120. Domingo E, Holland JJ. RNA virus mutations and fitness for survival. Annu Rev Microbiol 1997, 51:151-178. 10.1146/annurev.micro.51.1.151, 9343347.
121. Frost SD, Nijhuis M, Schuurman R, Boucher CA, Brown AJ. Evolution of lamivudine resistance in human immunodeficiency virus type 1-infected individuals: the relative roles of drift and selection. J Virol 2000, 74:6262-6268. 10.1128/JVI.74.14.6262-6268.2000, 112131, 10864635.
122. Moya A, Holmes EC, Gonzalez-Candelas F. The population genetics and evolutionary epidemiology of RNA viruses. Nat Rev Microbiol 2004, 2:279-288. 10.1038/nrmicro863, 15031727.
123. Kim EY, Bhattacharya T, Kunstman K, Swantek P, Koning FA, Malim MH, Wolinsky SM. Human APOBEC3G-mediated editing can promote HIV-1 sequence diversification and accelerate adaptation to selective pressure. J Virol 2010, 84:10402-10405. 10.1128/JVI.01223-10, 2937764, 20660203.
124. Yebra G, Holguin A. Mutation Vif-22 H, which allows HIV-1 to use the APOBEC3G hypermutation to develop resistance, could appear more quickly in certain non-B variants. J Antimicrob Chemother 2011, 66:941-942. 10.1093/jac/dkr012, 21393191.
125. Fourati S, Malet I, Binka M, Boukobza S, Wirden M, Sayon S, Simon A, Katlama C, Simon V, Calvez V, Marcelin AG. Partially active HIV-1 Vif alleles facilitate viral escape from specific antiretrovirals. AIDS 2010, 24:2313-2321.
126. Harrer T, Harrer E, Kalams SA, Elbeik T, Staprans SI, Feinberg MB, Cao Y, Ho DD, Yilma T, Caliendo AM, et al. Strong cytotoxic T cell and weak neutralizing antibody responses in a subset of persons with stable nonprogressing HIV type 1 infection. AIDS Res Hum Retroviruses 1996, 12:585-592. 10.1089/aid.1996.12.585, 8743084.
127. Shankar P, Russo M, Harnisch B, Patterson M, Skolnik P, Lieberman J. Impaired function of circulating HIV-specific CD8(+) T cells in chronic human immunodeficiency virus infection. Blood 2000, 96:3094-3101.
128. Heintel T, Sester M, Rodriguez MM, Krieg C, Sester U, Wagner R, Pees HW, Gartner B, Maier R, Meyerhans A. The fraction of perforin-expressing HIV-specific CD8 T cells is a marker for disease progression in HIV infection. AIDS 2002, 16:1497-1501. 10.1097/00002030-200207260-00006, 12131187.
129. Ogg GS, Jin X, Bonhoeffer S, Dunbar PR, Nowak MA, Monard S, Segal JP, Cao Y, Rowland-Jones SL, Cerundolo V, et al. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 1998, 279:2103-2106. 10.1126/science.279.5359.2103, 9516110.
130. Yusim K, Kesmir C, Gaschen B, Addo MM, Altfeld M, Brunak S, Chigaev A, Detours V, Korber BT. Clustering patterns of cytotoxic T-lymphocyte epitopes in human immunodeficiency virus type 1 (HIV-1) proteins reveal imprints of immune evasion on HIV-1 global variation. J Virol 2002, 76:8757-8768. 10.1128/JVI.76.17.8757-8768.2002, 136996, 12163596.
131. Jones NA, Wei X, Flower DR, Wong M, Michor F, Saag MS, Hahn BH, Nowak MA, Shaw GM, Borrow P. Determinants of human immunodeficiency virus type 1 escape from the primary CD8+ cytotoxic T lymphocyte response. J Exp Med 2004, 200:1243-1256. 10.1084/jem.20040511, 2211924, 15545352.
132. Tomiyama H, Fujiwara M, Oka S, Takiguchi M. Cutting Edge: Epitope-dependent effect of Nef-mediated HLA class I down-regulation on ability of HIV-1-specific CTLs to suppress HIV-1 replication. J Immunol 2005, 174:36-40.
133. Barouch DH, Letvin NL. Viral evolution and challenges in the development of HIV vaccines. Vaccine 2002, 20(Suppl 4):A66-A68.
134. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, Meyers H, Nelson JA, Gairin JE, Hahn BH, Oldstone MB, Shaw GM. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med 1997, 3:205-211. 10.1038/nm0297-205, 9018240.
135. Geels MJ, Cornelissen M, Schuitemaker H, Anderson K, Kwa D, Maas J, Dekker JT, Baan E, Zorgdrager F, van den Burg R, et al. Identification of sequential viral escape mutants associated with altered T-cell responses in a human immunodeficiency virus type 1-infected individual. J Virol 2003, 77:12430-12440. 10.1128/JVI.77.23.12430-12440.2003, 262568, 14610167.
136. Wood N, Bhattacharya T, Keele BF, Giorgi E, Liu M, Gaschen B, Daniels M, Ferrari G, Haynes BF, McMichael A, et al. HIV evolution in early infection: selection pressures, patterns of insertion and deletion, and the impact of APOBEC. PLoS Pathog 2009, 5:e1000414. 10.1371/journal.ppat.1000414, 2671846, 19424423.
137. Casartelli N, Guivel-Benhassine F, Bouziat R, Brandler S, Schwartz O, Moris A. The antiviral factor APOBEC3G improves CTL recognition of cultured HIV-infected T cells. J Exp Med 2010, 207:39-49. 10.1084/jem.20091933, 2812543, 20038599.
138. Sakuma R, Noser JA, Ohmine S, Ikeda Y. Inhibition of HIV-1 replication by simian restriction factors, TRIM5alpha and APOBEC3G. Gene Ther 2007, 14:185-189.
139. Cen S, Peng ZG, Li XY, Li ZR, Ma J, Wang YM, Fan B, You XF, Wang YP, Liu F, et al. Small molecular compounds inhibit HIV-1 replication through specifically stabilizing APOBEC3G. J Biol Chem 2010, 285:16546-16552. 10.1074/jbc.M109.085308, 2878088, 20363737.
140. Chen H, Wang LW, Huang YQ, Gong ZJ. Interferon-alpha Induces High Expression of APOBEC3G and STAT-1 in Vitro and in Vivo. Int J Mol Sci 2010, 11:3501-3512. 10.3390/ijms11093501, 2956108, 20957108.
141. Pillai SK, Wong JK, Barbour JD. Turning up the volume on mutational pressure: is more of a good thing always better? (A case study of HIV-1 Vif and APOBEC3). Retrovirology 2008, 5:26. 10.1186/1742-4690-5-26, 2323022, 18339206.
142. Vazquez-Perez JA, Ormsby CE, Hernandez-Juan R, Torres KJ, Reyes-Teran G. APOBEC3G mRNA expression in exposed seronegative and early stage HIV infected individuals decreases with removal of exposure and with disease progression. Retrovirology 2009, 6:23. 10.1186/1742-4690-6-23, 2661038, 19254362.
143. Jin X, Brooks A, Chen H, Bennett R, Reichman R, Smith H. APOBEC3G/CEM15 (hA3G) mRNA levels associate inversely with human immunodeficiency virus viremia. J Virol 2005, 79:11513-11516. 10.1128/JVI.79.17.11513-11516.2005, 1193574, 16103203.
144. Cho SJ, Drechsler H, Burke RC, Arens MQ, Powderly W, Davidson NO. APOBEC3F and APOBEC3G mRNA levels do not correlate with human immunodeficiency virus type 1 plasma viremia or CD4+ T-cell count. J Virol 2006, 80:2069-2072. 10.1128/JVI.80.4.2069-2072.2006, 1367163, 16439564.
145. Mussil B, Sauermann U, Motzkus D, Stahl-Hennig C, Sopper S. Increased APOBEC3G and APOBEC3F expression is associated with low viral load and prolonged survival in simian immunodeficiency virus infected rhesus monkeys. Retrovirology 2011, 8:77. 10.1186/1742-4690-8-77, 3192745, 21955401.
146. Russell RA, Moore MD, Hu WS, Pathak VK. APOBEC3G induces a hypermutation gradient: purifying selection at multiple steps during HIV-1 replication results in levels of G-to-A mutations that are high in DNA, intermediate in cellular viral RNA, and low in virion RNA. Retrovirology 2009, 6:16. 10.1186/1742-4690-6-16, 2657108, 19216784.
147. Hu WS, Temin HM. Retroviral recombination and reverse transcription. Science 1990, 250:1227-1233. 10.1126/science.1700865, 1700865.
148. Zhang J, Temin HM. Rate and mechanism of nonhomologous recombination during a single cycle of retroviral replication. Science 1993, 259:234-238. 10.1126/science.8421784, 8421784.
149. Temin HM. Mixed infection with two types of Rous sarcoma virus. Virology 1961, 13:158-163. 10.1016/0042-6822(61)90049-6, 13775833.
150. Holland JJ, De La Torre JC, Steinhauer DA. RNA virus populations as quasispecies. Curr Top Microbiol Immunol 1992, 176:1-20. 10.1007/978-3-642-77011-1_1, 1600748.
151. Mansky LM, Temin HM. Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol 1995, 69:5087-5094. 189326, 7541846.
152. Coffin JM. Genetic diversity and evolution of retroviruses. Curr Top Microbiol Immunol 1992, 176:143-164. 10.1007/978-3-642-77011-1_10, 1600751.
153. Katz RA, Skalka AM. Generation of diversity in retroviruses. Annu Rev Genet 1990, 24:409-445. 10.1146/annurev.ge.24.120190.002205, 1708222.
154. Jetzt AE, Yu H, Klarmann GJ, Ron Y, Preston BD, Dougherty JP. High rate of recombination throughout the human immunodeficiency virus type 1 genome. J Virol 2000, 74:1234-1240. 10.1128/JVI.74.3.1234-1240.2000, 111457, 10627533.
155. Charpentier C, Nora T, Tenaillon O, Clavel F, Hance AJ. Extensive recombination among human immunodeficiency virus type 1 quasispecies makes an important contribution to viral diversity in individual patients. J Virol 2006, 80:2472-2482. 10.1128/JVI.80.5.2472-2482.2006, 1395372, 16474154.
156. Chen J, Powell D, Hu WS. High frequency of genetic recombination is a common feature of primate lentivirus replication. J Virol 2006, 80:9651-9658. 10.1128/JVI.00936-06, 1617242, 16973569.
157. Onafuwa-Nuga A, Telesnitsky A. The remarkable frequency of human immunodeficiency virus type 1 genetic recombination. Microbiol Mol Biol Rev 2009, 73:451-480. Table of Contents, 10.1128/MMBR.00012-09, 2738136, 19721086.
158. Jung A, Maier R, Vartanian JP, Bocharov G, Jung V, Fischer U, Meese E, Wain-Hobson S, Meyerhans A. Recombination: Multiply infected spleen cells in HIV patients. Nature 2002, 418:144. 10.1038/418144a, 12110879.
159. Nikolenko GN, Svarovskaia ES, Delviks KA, Pathak VK. Antiretroviral drug resistance mutations in human immunodeficiency virus type 1 reverse transcriptase increase template-switching frequency. J Virol 2004, 78:8761-8770. 10.1128/JVI.78.16.8761-8770.2004, 479068, 15280484.
160. Malim MH, Emerman M. HIV-1 sequence variation: drift, shift, and attenuation. Cell 2001, 104:469-472. 10.1016/S0092-8674(01)00234-3, 11239404.
161. van Hemert FJ, Berkhout B. The tendency of lentiviral open reading frames to become A-rich: constraints imposed by viral genome organization and cellular tRNA availability. J Mol Evol 1995, 41:132-140.
162. Berkhout B, van Hemert FJ. The unusual nucleotide content of the HIV RNA genome results in a biased amino acid composition of HIV proteins. Nucleic Acids Res 1994, 22:1705-1711. 10.1093/nar/22.9.1705, 308053, 8202375.
163. Berkhout B, Das AT, Beerens N. HIV-1 RNA editing, hypermutation, and error-prone reverse transcription. Science 2001, 292:7. 10.1126/science.292.5514.7a, 11292864.
164. Chelico L, Pham P, Goodman MF. Mechanisms of APOBEC3G-catalyzed processive deamination of deoxycytidine on single-stranded DNA. Nat Struct Mol Biol 2009, 16:454-455. author reply 455-456, 10.1038/nsmb0509-454, 2764237, 19421154.