The HDAC6/APOBEC3G complex regulates HIV-1 infectiveness by inducing Vif autophagic degradation

Retrovirology

Volumn 12, Issue 1, 2015, Pages

  Valera, María Soledad ^a   de Armas Rillo, Laura ^a   Barroso González, Jonathan ^a   Ziglio, Serena ^a   Batisse, Julien ^b   Dubois, Noé ^b   Marrero Hernández, Sara ^a   Borel, Sophie ^c   García Expósito, Laura ^a   Biard Piechaczyk, Martine ^c   Paillart, Jean Christophe ^b   Valenzuela Fernández, Agustín ^a  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c University of Montpellier I and II   (France)

Author keywords

Anti HIV 1 restriction complex; APOBEC3G; Autophagic clearance; CBF ; HDAC6; HIV 1; Vif

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; CORE BINDING FACTOR BETA; HISTONE DEACETYLASE 6; VIF PROTEIN; APOBEC3G PROTEIN, HUMAN; CYTIDINE DEAMINASE; HDAC6 PROTEIN, HUMAN; HISTONE DEACETYLASE; PROTEIN BINDING; VIF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTIVIRAL ACTIVITY; APOBEC3G GENE; ARTICLE; AUTOPHAGIC DEGRADATION; AUTOPHAGY; BIODEGRADATION; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; COMPETITIVE INHIBITION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ENZYME REGULATION; HDAC6 GENE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFECTION CONTROL; MICROTUBULE; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; STEADY STATE; UBIQUITINATION; VIRAL CLEARANCE; VIRION; VIRUS CELL INTERACTION; VIRUS INFECTIVITY; VIRUS PARTICLE; VIRUS PATHOGENESIS; VIRUS VIRULENCE; CELL LINE; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN DEGRADATION; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

APOBEC-3G DEAMINASE; AUTOPHAGY; CELL LINE; CYTIDINE DEAMINASE; EPITHELIAL CELLS; HISTONE DEACETYLASES; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEOLYSIS; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84935037656     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-015-0181-5     Document Type: Article

References (95)

1. Jarmuz A, Chester A, Bayliss J, Gisbourne J, Dunham I, Scott J et al (2002) An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 79:285-296
2. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, Trono D (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424:99-103
3. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, Gao L (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424:94-98
4. Shindo K, Takaori-Kondo A, Kobayashi M, Abudu A, Fukunaga K, Uchiyama T (2003) 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 278:44412-44416
5. Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN et al (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113:803-809
6. Simon JH, Malim MH (1996) The human immunodeficiency virus type 1 Vif protein modulates the postpenetration stability of viral nucleoprotein complexes. J Virol 70:5297-5305
7. Gaddis NC, Chertova E, Sheehy AM, Henderson LE, Malim MH (2003) Comprehensive investigation of the molecular defect in vif-deficient human immunodeficiency virus type 1 virions. J Virol 77:5810-5820
8. Newman EN, Holmes RK, Craig HM, Klein KC, Lingappa JR, Malim MH et al (2005) Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr Biol 15:166-170
9. Lecossier D, Bouchonnet F, Clavel F, Hance AJ (2003) Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300:1112
10. Klarmann GJ, Chen X, North TW, Preston BD (2003) Incorporation of uracil into minus strand DNA affects the specificity of plus strand synthesis initiation during lentiviral reverse transcription. J Biol Chem 278:7902-7909
11. Mbisa JL, Barr R, Thomas JA, Vandegraaff N, Dorweiler IJ, Svarovskaia ES et al (2007) Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plus-strand DNA transfer and integration. J Virol 81:7099-7110
12. Monajemi M, Woodworth CF, Benkaroun J, Grant M, Larijani M (2012) Emerging complexities of APOBEC3G action on immunity and viral fitness during HIV infection and treatment. Retrovirology 9:35
13. Li J, Potash MJ, Volsky DJ (2004) Functional domains of APOBEC3G required for antiviral activity. J Cell Biochem 92:560-572
14. Chiu YL, Soros VB, Kreisberg JF, Stopak K, Yonemoto W, Greene WC (2005) Cellular APOBEC3G restricts HIV-1 infection in resting CD4+T cells. Nature 435:108-114
15. Li XY, Guo F, Zhang L, Kleiman L, Cen S (2007) APOBEC3G inhibits DNA strand transfer during HIV-1 reverse transcription. J Biol Chem 282:32065-32074
16. Luo K, Wang T, Liu B, Tian C, Xiao Z, Kappes J et al (2007) Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. J Virol 81:7238-7248
17. Mbisa JL, Bu W, Pathak VK (2010) APOBEC3F and APOBEC3G inhibit HIV-1 DNA integration by different mechanisms. J Virol 84:5250-5259
18. Svarovskaia ES, Xu H, Mbisa JL, Barr R, Gorelick RJ, Ono A et al (2004) Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J Biol Chem 279:35822-35828
19. Wichroski MJ, Robb GB, Rana TM (2006) Human retroviral host restriction factors APOBEC3G and APOBEC3F localize to mRNA processing bodies. PLoS Pathog 2:e41
20. Gallois-Montbrun S, Kramer B, Swanson CM, Byers H, Lynham S, Ward M et al (2007) Antiviral protein APOBEC3G localizes to ribonucleoprotein complexes found in P bodies and stress granules. J Virol 81:2165-2178
21. Berkhout B, de Ronde A (2004) APOBEC3G versus reverse transcriptase in the generation of HIV-1 drug-resistance mutations. AIDS 18:1861-1863
22. Mulder LC, Harari A, Simon V (2008) Cytidine deamination induced HIV-1 drug resistance. Proc Natl Acad Sci USA 105:5501-5506
23. Kim EY, Bhattacharya T, Kunstman K, Swantek P, Koning FA, Malim MH et al (2010) Human APOBEC3G-mediated editing can promote HIV-1 sequence diversification and accelerate adaptation to selective pressure. J Virol 84:10402-10405
24. Sadler HA, Stenglein MD, Harris RS, Mansky LM (2010) APOBEC3G contributes to HIV-1 variation through sublethal mutagenesis. J Virol 84:7396-7404
25. Chiu YL, Greene WC (2006) Multifaceted antiviral actions of APOBEC3 cytidine deaminases. Trends Immunol 27:291-297
26. Smith HC (2011) APOBEC3G: a double agent in defense. Trends Biochem Sci 36:239-244
27. Malim MH, Emerman M (2008) HIV-1 accessory proteins-ensuring viral survival in a hostile environment. Cell Host Microbe 3:388-398
28. Harris RS, Hultquist JF, Evans DT (2012) The restriction factors of human immunodeficiency virus. J Biol Chem 287:40875-40883
29. Simon JH, Miller DL, Fouchier RA, Soares MA, Peden KW, Malim MH (1998) The regulation of primate immunodeficiency virus infectivity by Vif is cell species restricted: a role for Vif in determining virus host range and cross-species transmission. EMBO J 17:1259-1267
30. Henriet S, Mercenne G, Bernacchi S, Paillart JC, Marquet R (2009) Tumultuous relationship between the human immunodeficiency virus type 1 viral infectivity factor (Vif) and the human APOBEC-3G and APOBEC-3F restriction factors. Microbiol Mol Biol Rev 73:211-232
31. Sheehy AM, Gaddis NC, Choi JD, Malim MH (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650
32. Marin M, Rose KM, Kozak SL, Kabat D (2003) HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 9:1398-1403
33. Yu X, Yu Y, Liu B, Luo K, Kong W, Mao P et al (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302:1056-1060
34. Mehle A, Goncalves J, Santa-Marta M, McPike M, Gabuzda D (2004) Phosphorylation of a novel SOCS-box regulates assembly of the HIV-1 Vif-Cul5 complex that promotes APOBEC3G degradation. Genes Dev 18:2861-2866
35. Yu Y, Xiao Z, Ehrlich ES, Yu X, Yu XF (2004) Selective assembly of HIV-1 Vif-Cul5-ElonginB-ElonginC E3 ubiquitin ligase complex through a novel SOCS box and upstream cysteines. Genes Dev 18:2867-2872
36. Guo Y, Dong L, Qiu X, Wang Y, Zhang B, Liu H et al (2014) Structural basis for hijacking CBF-beta and CUL5 E3 ligase complex by HIV-1 Vif. Nature 505:229-233
37. Jager S, Kim DY, Hultquist JF, Shindo K, LaRue RS, Kwon E et al (2011) Vif hijacks CBF-beta to degrade APOBEC3G and promote HIV-1 infection. Nature 481:371-375
38. Wang X, Zhang H, Lv M, Zuo T, Wu H, Wang J et al (2013) Interactions between HIV-1 Vif and human ElonginB-ElonginC are important for CBF-beta binding to Vif. Retrovirology 10:94
39. Mariani R, Chen D, Schrofelbauer B, Navarro F, Konig R, Bollman B et al (2003) Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114:21-31
40. Stopak K, de Noronha C, Yonemoto W, Greene WC (2003) HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol Cell 12:591-601
41. Sheehy AM, Gaddis NC, Malim MH (2003) The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med 9:1404-1407
42. Mercenne G, Bernacchi S, Richer D, Bec G, Henriet S, Paillart JC et al (2010) HIV-1 Vif binds to APOBEC3G mRNA and inhibits its translation. Nucleic Acids Res 38:633-646
43. Kao S, Khan MA, Miyagi E, Plishka R, Buckler-White A, Strebel K (2003) 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 77:11398-11407
44. Valenzuela-Fernandez A, Alvarez S, Gordon-Alonso M, Barrero M, Ursa A, Cabrero JR et al (2005) Histone deacetylase 6 regulates human immunodeficiency virus type 1 infection. Mol Biol Cell 16:5445-5454
45. Valenzuela-Fernandez A, Cabrero JR, Serrador JM, Sanchez-Madrid F (2008) HDAC6: a key regulator of cytoskeleton, cell migration and cell-cell interactions. Trends Cell Biol 18:291-297
46. Malinowsky K, Luksza J, Dittmar MT (2008) Susceptibility to virus-cell fusion at the plasma membrane is reduced through expression of HIV gp41 cytoplasmic domains. Virology 376:69-78
47. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115:727-738
48. Iwata A, Riley BE, Johnston JA, Kopito RR (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J Biol Chem 280:40282-40292
49. Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, Nedelsky NB et al (2007) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447:859-863
50. Lee JY, Koga H, Kawaguchi Y, Tang W, Wong E, Gao YS et al (2010) HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J 29:969-980
51. Ouyang H, Ali YO, Ravichandran M, Dong A, Qiu W, MacKenzie F et al (2012) Protein aggregates are recruited to aggresome by histone deacetylase 6 via unanchored ubiquitin C termini. J Biol Chem 287:2317-2327
52. Pai MT, Tzeng SR, Kovacs JJ, Keaton MA, Li SS, Yao TP et al (2007) Solution structure of the Ubp-M BUZ domain, a highly specific protein module that recognizes the C-terminal tail of free ubiquitin. J Mol Biol 370:290-302
53. Hao R, Nanduri P, Rao Y, Panichelli RS, Ito A, Yoshida M et al (2013) Proteasomes activate aggresome disassembly and clearance by producing unanchored ubiquitin chains. Mol Cell 51:819-828
54. Verdel A, Khochbin S (1999) Identification of a new family of higher eukaryotic histone deacetylases. Coordinate expression of differentiation-dependent chromatin modifiers. J Biol Chem 274:2440-2445
55. Grozinger CM, Hassig CA, Schreiber SL (1999) Three proteins define a class of human histone deacetylases related to yeast Hda1p. Proc Natl Acad Sci USA 96:4868-4873
56. Bertos NR, Gilquin B, Chan GK, Yen TJ, Khochbin S, Yang XJ (2004) Role of the tetradecapeptide repeat domain of human histone deacetylase 6 in cytoplasmic retention. J Biol Chem 279:48246-48254
57. Seigneurin-Berny D, Verdel A, Curtet S, Lemercier C, Garin J, Rousseaux S et al (2001) Identification of components of the murine histone deacetylase 6 complex: link between acetylation and ubiquitination signaling pathways. Mol Cell Biol 21:8035-8044
58. Hook SS, Orian A, Cowley SM, Eisenman RN (2002) Histone deacetylase 6 binds polyubiquitin through its zinc finger (PAZ domain) and copurifies with deubiquitinating enzymes. Proc Natl Acad Sci USA 99:13425-13430
59. Kovacs JJ, Hubbert C, Yao TP (2004) The HDAC complex and cytoskeleton. Novartis Found Symp 259:170-177 discussion 178-181, 223-175
60. Amerik AY, Li SJ, Hochstrasser M (2000) Analysis of the deubiquitinating enzymes of the yeast Saccharomyces cerevisiae. Biol Chem 381:981-992
61. Bertos NR, Wang AH, Yang XJ (2001) Class II histone deacetylases: structure, function, and regulation. Biochem Cell Biol 79:243-252
62. Dussart S, Courcoul M, Bessou G, Douaisi M, Duverger Y, Vigne R et al (2004) The Vif protein of human immunodeficiency virus type 1 is posttranslationally modified by ubiquitin. Biochem Biophys Res Commun 315:66-72
63. Mehle A, Strack B, Ancuta P, Zhang C, McPike M, Gabuzda D (2004) Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J Biol Chem 279:7792-7798
64. Hultquist JF, Binka M, LaRue RS, Simon V, Harris RS (2011) Vif proteins of human and simian immunodeficiency viruses require cellular CBFbeta to degrade APOBEC3 restriction factors. J Virol 86:2874-2877
65. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A et al (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417:455-458
66. Matsuyama A, Shimazu T, Sumida Y, Saito A, Yoshimatsu Y, Seigneurin-Berny D et al (2002) In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J 21:6820-6831
67. Opi S, Kao S, Goila-Gaur R, Khan MA, Miyagi E, Takeuchi H et al (2007) Human immunodeficiency virus type 1 Vif inhibits packaging and antiviral activity of a degradation-resistant APOBEC3G variant. J Virol 81:8236-8246
68. Bogerd HP, Doehle BP, Wiegand HL, Cullen BR (2004) A single amino acid difference in the host APOBEC3G protein controls the primate species specificity of HIV type 1 virion infectivity factor. Proc Natl Acad Sci USA 101:3770-3774
69. Mangeat B, Turelli P, Liao S, Trono D (2004) A single amino acid determinant governs the species-specific sensitivity of APOBEC3G to Vif action. J Biol Chem 279:14481-14483
70. Xu H, Svarovskaia ES, Barr R, Zhang Y, Khan MA, Strebel K et al (2004) A single amino acid substitution in human APOBEC3G antiretroviral enzyme confers resistance to HIV-1 virion infectivity factor-induced depletion. Proc Natl Acad Sci USA 101:5652-5657
71. Batisse J, Guerrero SX, Bernacchi S, Richert L, Godet J, Goldschmidt V et al (2013) APOBEC3G impairs the multimerization of the HIV-1 Vif protein in living cells. J Virol 87:6492-6506
72. Dompierre JP, Godin JD, Charrin BC, Cordelieres FP, King SJ, Humbert S et al (2007) Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J Neurosci 27:3571-3583
73. Zhou T, Han Y, Dang Y, Wang X, Zheng YH (2009) A novel HIV-1 restriction factor that is biologically distinct from APOBEC3 cytidine deaminases in a human T cell line CEM.NKR. Retrovirology 6:31
74. Zhou T, Dang Y, Baker JJ, Zhou J, Zheng YH (2012) Evidence for Vpr-dependent HIV-1 replication in human CD4+CEM.NKR T-cells. Retrovirology 9:93
75. Seglen PO, Gordon PB (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci USA 79:1889-1892
76. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H et al (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402:672-676
77. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS et al (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4:151-175
78. Bjorkoy G, Lamark T, Johansen T (2006) p62/SQSTM1: a missing link between protein aggregates and the autophagy machinery. Autophagy 2:138-139
79. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H et al (2007) p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282:24131-24145
80. Barrero-Villar M, Barroso-Gonzalez J, Cabrero JR, Gordon-Alonso M, Alvarez-Losada S, Munoz-Fernandez MA et al (2008) PI4P5-kinase Ialpha is required for efficient HIV-1 entry and infection of T cells. J Immunol 181:6882-6888
81. Barrero-Villar M, Cabrero JR, Gordon-Alonso M, Barroso-Gonzalez J, Alvarez-Losada S, Munoz-Fernandez MA et al (2009) Moesin is required for HIV-1-induced CD4-CXCR4 interaction, F-actin redistribution, membrane fusion and viral infection in lymphocytes. J Cell Sci 122:103-113
82. Barroso-Gonzalez J, El Jaber-Vazdekis N, Garcia-Exposito L, Machado JD, Zarate R, Ravelo AG et al (2009) The lupane-type triterpene 30-oxo-calenduladiol is a CCR5 antagonist with anti-HIV-1 and anti-chemotactic activities. J Biol Chem 284:16609-16620
83. Garcia-Exposito L, Barroso-Gonzalez J, Puigdomenech I, Machado JD, Blanco J, Valenzuela-Fernandez A (2011) HIV-1 requires Arf6-mediated membrane dynamics to efficiently enter and infect T lymphocytes. Mol Biol Cell 22:1148-1166
84. Miyakawa K, Matsunaga S, Kanou K, Matsuzawa A, Morishita R, Kudoh A et al (2015) ASK1 restores the antiviral activity of APOBEC3G by disrupting HIV-1 Vif-mediated counteraction. Nat Commun 6:6945
85. Pillai SK, Wong JK, Barbour JD (2008) 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 5:26
86. Chiu YL, Greene WC (2008) The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu Rev Immunol 26:317-353
87. Roberts SA, Lawrence MS, Klimczak LJ, Grimm SA, Fargo D, Stojanov P et al (2013) An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat Genet 45:970-976
88. Kovacs AL, Rez G, Palfia Z, Kovacs J (2000) Autophagy in the epithelial cells of murine seminal vesicle in vitro. Formation of large sheets of nascent isolation membranes, sequestration of the nucleus and inhibition by wortmannin and 3-ethyladenine. Cell Tissue Res 302:253-261
89. Wang Y, Kinlock BL, Shao Q, Turner TM, Liu B (2014) HIV-1 Vif inhibits G to A hypermutations catalyzed by virus-encapsidated APOBEC3G to maintain HIV-1 infectivity. Retrovirology 11:89
90. Sabo Y, Walsh D, Barry DS, Tinaztepe S, de Los Santos K, Goff SP (2013) HIV-1 induces the formation of stable microtubules to enhance early infection. Cell Host Microbe 14:535-546
91. Huo L, Li D, Sun X, Shi X, Karna P, Yang W et al (2011) Regulation of tat acetylation and transactivation activity by the microtubule-associated deacetylase HDAC6. J Biol Chem 286:9280-9286
92. Garcia-Exposito L, Ziglio S, Barroso-Gonzalez J, de Armas-Rillo L, Valera MS, Zipeto D et al (2013) Gelsolin activity controls efficient early HIV-1 infection. Retrovirology 10:39
93. Akari H, Fujita M, Kao S, Khan MA, Shehu-Xhilaga M, Adachi A et al (2004) High level expression of human immunodeficiency virus type-1 Vif inhibits viral infectivity by modulating proteolytic processing of the Gag precursor at the p2/nucleocapsid processing site. J Biol Chem 279:12355-12362
94. Izumi T, Takaori-Kondo A, Shirakawa K, Higashitsuji H, Itoh K, Io K et al (2009) MDM2 is a novel E3 ligase for HIV-1 Vif. Retrovirology 6:1
95. Mehle A, Wilson H, Zhang C, Brazier AJ, McPike M, Pery E et al (2007) Identification of an APOBEC3G binding site in human immunodeficiency virus type 1 Vif and inhibitors of Vif-APOBEC3G binding. J Virol 81:13235-13241