The dimerization domain of HIV-1 viral infectivity factor Vif is required to block virion incorporation of APOBEC3G

Retrovirology

Volumn 4, Issue , 2007, Pages

  Miller, James H ^a   Presnyak, Vlad ^b   Smith, Harold C ^a,b  

^a OyaGen Inc   (United States)

^b Department of Biochemistry and Biophysics ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; HYBRID PROTEIN; PEPTIDE; THREONINE; VIF PROTEIN; APOBEC3G PROTEIN, HUMAN; CYTIDINE DEAMINASE; UNCLASSIFIED DRUG;

ARTICLE; CELL TRANSPORT; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; ENZYME REPRESSION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ASSEMBLY; PROTEIN CONTENT; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; VIRION; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS PARTICLE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; METABOLISM; PATHOGENICITY; PHYSIOLOGY; VIROLOGY; VIRULENCE; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

CYTIDINE DEAMINASE; DIMERIZATION; HIV INFECTIONS; HIV-1; HUMANS; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; VIRULENCE; VIRUS REPLICATION;

EID: 38949106531     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-4-81     Document Type: Article

References (66)

1. Gaddis NC Chertova E Sheehy AM Henderson LE Malim MH Comprehensive investigation of the molecular defect in vif-deficient human immunodeficiency virus type 1 virions J Virol 2003 77 10 5810 5820 154025 12719574 10.1128/JVI.77.10.5810-5820.2003
2. Goncalves J Santa-Marta M HIV-1 Vif and APOBEC3G: Multiple roads to one goal Retrovirology 2004, 1:28 521195 15383144 10.1186/1742-4690-1-28
3. 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(12):10251-10255 110608 9811770
4. Conticello SG Harris RS Neuberger MS The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G Curr Biol 2003, 13(22):2009-2013 10.1016/j.cub.2003.10.034 14614829
5. Kobayashi M Takaori-Kondo A Miyauchi Y Iwai K Uchiyama T Ubiquitination of APOBEC3G by an HIV-1 Vif-Cullin5-Elongin B-Elongin C complex is essential for Vif function J Biol Chem 2005, 280(19):18573-18578 10.1074/ jbc.C500082200 15781449
6. 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(1):21-31 10.1016/ S0092-8674(03)00515-4 12859895
7. Mehle A Goncalves J Santa-Marta M McPike M Gabuzda D Phosphorylation of a novel SOCS-box regulates assembly of the HIV-1 Vif-Cul5 complex that promotes APOBEC3G degradation Genes Dev 2004, 18(23):2861-2866 534646 15574592 10.1101/gad.1249904
8. 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(9):7792-7798 10.1074/jbc.M313093200 14672928
9. 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(3):591-601 10.1016/ S1097-2765(03)00353-8 14527406
10. Wichroski MJ Ichiyama K Rana TM Analysis of HIV-1 viral infectivity factor-mediated proteasome-dependent depletion of APOBEC3G: Correlating function and subcellular localization J Biol Chem 2005, 280(9):8387-8396 10.1074/jbc.M408048200 15537645
11. 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(5647):1056-1060 10.1126/science.1089591 14564014
12. 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 1948019 17631688 10.1186/1742-4690-4-48
13. Liu B Yu X Luo K Yu Y Yu XF Influence of primate lentiviral Vif and proteasome inhibitors on human immunodeficiency virus type 1 virion packaging of APOBEC3G J Virol 2004, 78(4):2072-2081 369424 14747572 10.1128/JVI.78.4.2072-2081.2004
14. Mangeat B Turelli P Liao S Trono D A single amino acid determinant governs the species-specific sensitivity of APOBEC3G to Vif action J Biol Chem 2004, 279(15):14481-14483 10.1074/jbc.C400060200 14966139
15. 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(6898):646-650 10.1038/nature00939 12167863
16. 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(2):247-256 10.1016/j.virol.2006.10.036 17126871
17. Xu H Svarovskaia ES Barr R Zhang Y Khan MA Strebel K Pathak VK A single amino acid substitution in human APOBEC3G antiretroviral enzyme confers resistance to HIV-1 virion infectivity factor-induced depletion Proc Natl Acad Sci U S A 2004, 101(15):5652-5657 397464 15054139 10.1073/ pnas.0400830101
18. Zennou V Perez-Caballero D Gottlinger H Bieniasz PD APOBEC3G incorporation into human immunodeficiency virus type 1 particles J Virol 2004, 78(21):12058-12061 523273 15479846 10.1128/ JVI.78.21.12058-12061.2004
19. Bishop KN Holmes RK Malim MH Antiviral potency of APOBEC proteins does not correlate with cytidine deamination J Virol 2006, 80(17):8450-8458 1563846 16912295 10.1128/JVI.00839-06
20. Guo F Cen S Niu M Saadatmand J Kleiman L Inhibition of formula-primed reverse transcription by human APOBEC3G during human immunodeficiency virus type 1 replication J Virol 2006, 80(23):11710-11722 1642613 16971427 10.1128/JVI.01038-06
21. 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
22. Chelico L Pham P Calabrese P Goodman MF APOBEC3G DNA deaminase acts processively 3′ - > 5′ on single-stranded DNA Nat Struct Mol Biol 2006, 13(5):392-399 10.1038/nsmb1086 16622407
23. 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(6):803-809 10.1016/ S0092-8674(03)00423-9 12809610
24. Iwatani Y Takeuchi H Strebel K Levin JG Biochemical activities of highly purified, catalytically active human APOBEC3G: Correlation with antiviral effect J Virol 2006, 80(12):5992-6002 1472592 16731938 10.1128/ JVI.02680-05
25. 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(6944):99-103 10.1038/ nature01709 12808466
26. 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(2):374-386 10.1016/j.virol.2005.01.011 15721369
27. 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
28. 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(6944):94-98 1350966 12808465 10.1038/nature01707
29. Yang B Gao L Li L Lu Z Fan X Patel CA Pomerantz RJ DuBois GC Zhang H Potent suppression of viral infectivity by the peptides that inhibit multimerization of human immunodeficiency virus type 1 (HIV-1) Vif proteins J Biol Chem 2003, 278(8):6596-6602 1350967 2480936 10.1074/ jbc.M210164200
30. Yang S Sun Y Zhang H The multimerization of human immunodeficiency virus type I Vif protein: A requirement for Vif function in the viral life cycle J Biol Chem 2001, 276(7):4889-4893 1350968 11071884 10.1074/ jbc.M004895200
31. Auclair JR Green KM Shandilya S Evans JE Somasundaran M Schiffer CA Mass spectrometry analysis of HIV-1 Vif reveals an increase in ordered structure upon oligomerization in regions necessary for viral infectivity Proteins 2007 17598142
32. Marin M Rose KM Kozak SL Kabat D HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation Nat Med 2003, 9(11):1398-1403 10.1038/nm946 14528301
33. Tian C Yu X Zhang W Wang T Xu R Yu XF Differential requirement for conserved tryptophans in human immunodeficiency virus type 1 Vif for the selective suppression of APOBEC3G and APOBEC3F J Virol 2006, 80(6):3112-3115 1395459 16501124 10.1128/JVI.80.6.3112-3115.2006
34. Balaji S Kalpana R Shapshak P Paradigm development: Comparative and predictive 3D modeling of HIV-1 Virion Infectivity Factor (vif) Bioinformation 2006, 1(8):290-309 1891711 17597910
35. Lv W Liu Z Jin H Yu X Zhang L Zhang L Three-dimensional structure of HIV-1 VIF constructed by comparative modeling and the function characterization analyzed by molecular dynamics simulation Org Biomol Chem 2007, 5(4):617-626 10.1039/b612050d 17285170
36. Chiu YL Greene WC APOBEC3 cytidine deaminases: Distinct antiviral actions along the retroviral life cycle J Biol Chem 2006, 281(13):8309-8312 10.1074/jbc.R500021200 16407183
37. Chiu YL Greene WC Multifaceted antiviral actions of APOBEC3 cytidine deaminases Trends Immunol 2006, 27(6):291-297 10.1016/j.it.2006.04.003 16678488
38. 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(7038):108-114 10.1038/nature03493 15829920
39. 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(4):865-870 10.1084/ jem.20051856 16606671
40. Cen S Guo F Niu M Saadatmand J Deflassieux J Kleiman L The interaction between HIV-1 Gag and APOBEC3G J Biol Chem 2004, 279(32):33177-33184 10.1074/jbc.M402062200 15159405
41. Schafer A Bogerd HP Cullen BR Specific packaging of APOBEC3G into HIV-1 virions is mediated by the nucleocapsid domain of the gag polyprotein precursor Virology 2004, 328(2):163-168 10.1016/j.virol.2004.08.006 15464836
42. 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 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs J Biol Chem 2004, 279(34):35822-35828 10.1074/jbc.M405761200 15210704
43. Cullen BR Role and mechanism of action of the APOBEC3 family of antiretroviral resistance factors J Virol 2006, 80(3):1067-1076 1346961 16414984 10.1128/JVI.80.3.1067-1076.2006
44. Malim MH Natural resistance to HIV infection: The Vif-APOBEC interaction C R Biol 2006, 329(11):871-875 10.1016/j.crvi.2006.01.012 17067930
45. Richman D Rosenthal AS Skoog M Eckner RJ Chou TC Sabo JP Merluzzi VJ BI-RG-587 is active against zidovudine-resistant human immunodeficiency virus type 1 and synergistic with zidovudine Antimicrob Agents Chemother 1991, 35(2):305-308 244996 1708976
46. http://www.niaid.nih.gov/daids/dtpdb/000001.asp
47. Goncalves J Jallepalli P Gabuzda DH Subcellular localization of the Vif protein of human immunodeficiency virus type 1 J Virol 1994, 68(2):704-712 236506 8289374
48. Wichroski MJ Robb GB Rana TM Human retroviral host restriction factors APOBEC3G and APOBEC3F localize to mRNA processing bodies PLoS Pathog 2006, 2(5):e41 1458959 16699599 10.1371/journal.ppat.0020041
49. Ford KG Souberbielle BE Darling D Farzaneh F Protein transduction: An alternative to genetic intervention? Gene Ther 2001, 8(1):1-4 10.1038/ sj.gt.3301383 11402295
50. Bennett RP Diner E Sowden MP Lees JA Wedekind JE Smith HC APOBEC-1 and AID are nucleo-cytoplasmic trafficking proteins but APOBEC3G cannot traffic Biochem Biophys Res Commun 2006, 350(1):214-219 1847397 16999936 10.1016/j.bbrc.2006.09.032
51. Kao S Miyagi E Khan MA Takeuchi H Opi S Goila-Gaur R Strebel K Production of infectious human immunodeficiency virus type 1 does not require depletion of APOBEC3G from virus-producing cells Retrovirology 2004, 1(27):520834-15373943 10.1186/1742-4690-1-27
52. Khan MA Akari H Kao S Aberham C Davis D Buckler-White A Strebel K Intravirion processing of the human immunodeficiency virus type 1 Vif protein by the viral protease may be correlated with Vif function J Virol 2002, 76(18):9112-9123 136454 12186895 10.1128/ JVI.76.18.9112-9123.2002
53. Soros VB Yonemoto W Greene WC Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA, and subsequently activated by RNase H PLoS Pathog 2007, 3(2):e15 1796622 17291161 10.1371/ journal.ppat.0030015
54. Santa-Marta M da Silva FA Fonseca AM Goncalves J HIV-1 Vif can directly inhibit apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3G-mediated cytidine deamination by using a single amino acid interaction and without protein degradation J Biol Chem 2005, 280(10):8765-8775 10.1074/jbc.M409309200 15611076
55. Dettenhofer M Cen S Carlson BA Kleiman L Yu XF Association of human immunodeficiency virus type 1 Vif with RNA and its role in reverse transcription J Virol 2000, 74(19):8938-8945 102089 10982337 10.1128/ JVI.74.19.8938-8945.2000
56. Simon JH Malim MH The human immunodeficiency virus type 1 Vif protein modulates the postpenetration stability of viral nucleoprotein complexes J Virol 1996, 70(8):5297-5305 190487 8764040
57. 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(20):11322-11331 10.1128/ JVI.00162-07 17670826
58. 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(16):7252-7265 114961 11461998 10.1128/ JVI.75.16.7252-7265.2001
59. Ohagen A Gabuzda D Role of Vif in stability of the human immunodeficiency virus type 1 core J Virol 2000, 74(23):11055-11066 113185 11070000 10.1128/JVI.74.23.11055-11066.2000
60. Zhang H Pomerantz RJ Dornadula G Sun Y Human immunodeficiency virus type 1 Vif protein is an integral component of an mRNP complex of viral RNA and could be involved in the viral RNA folding and packaging process J Virol 2000, 74(18):8252-8261 116333 10954522 10.1128/ JVI.74.18.8252-8261.2000
61. Feng F Davis A Lake JA Carr J Xia W Burrell C Li P Ring finger protein ZIN interacts with human immunodeficiency virus type 1 Vif J Virol 2004, 78(19):10574-10581 516435 15367624 10.1128/JVI.78.19.10574-10581.2004
62. Hassaine G Courcoul M Bessou G Barthalay Y Picard C Olive D Collette Y Vigne R Decroly E The tyrosine kinase Hck is an inhibitor of HIV-1 replication counteracted by the viral vif protein J Biol Chem 2001, 276(20):16885-16893 10.1074/jbc.M009076200 11278465
63. 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(9):3369-3374 1413893 16492778 10.1073/pnas.0509417103
64. Yang X Gabuzda D Mitogen-activated protein kinase phosphorylates and regulates the HIV-1 Vif protein J Biol Chem 1998, 273(45):29879-29887 10.1074/jbc.273.45.29879 9792705
65. Robertson JR Drug abuse and HIV infection: General practice treatment and research agendas Br J Gen Pract 1992, 42(364):451-452 1372264 1472388
66. Toohey K Wehrly K Nishio J Perryman S Chesebro B Human immunodeficiency virus envelope V1 and V2 regions influence replication efficiency in macrophages by affecting virus spread Virology 1995, 213(1):70-79 10.1006/viro.1995.1547 7483281