Insight into the HIV-1 Vif SOCS-box-ElonginBC interaction

Open Biology

Volumn 3, Issue NOV, 2013, Pages

  Lu, Zhisheng ^a,b   Bergeron, Julien R C ^a,b,e   Atkinson, R Andrew ^a   Schaller, Torsten ^b   Veselkov, Dennis A ^a   Oregioni, Alain ^d   Yang, Yi ^c   Matthews, Stephen J ^c   Malim, Michael H ^b   Sanderson, Mark R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b GUY S HOSPITAL   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

ElonginBC; HIV 1 viral infectivity factor; NMR; SOCS box domain; Solution structure

Indexed keywords

CULLIN; ELONGIN; PROLINE; SUPPRESSOR OF CYTOKINE SIGNALING; TRANSCRIPTION FACTOR; VIF PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ELONGINBC; GENETICS; HIV-1 VIRAL INFECTIVITY FACTOR; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SOCS-BOX DOMAIN; SOLUTION STRUCTURE;

ELONGINBC; HIV-1 VIRAL INFECTIVITY FACTOR; NMR; SOCS-BOX DOMAIN; SOLUTION STRUCTURE;

AMINO ACID SEQUENCE; BINDING SITES; CULLIN PROTEINS; HIV-1; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROLINE; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSCRIPTION FACTORS; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84896297234     PISSN: None     EISSN: 20462441     Source Type: Journal    
DOI: 10.1098/rsob.130100     Document Type: Article

References (67)

1. LaRue RS et al. 2009 Guidelines for naming nonprimate APOBEC3 genes and proteins. J. Virol. 83, 494-497. (doi:10.1128/JVI.01976-08)
2. Conticello SG, Thomas CJ, Petersen-Mahrt SK, Neuberger MS. 2005 Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol. Biol. Evol. 22, 367-377. (doi:10. 1093/molbev/msi026) (Pubitemid 40130201)
3. Petersen-Mahrt SK, Harris RS, Neuberger MS. 2002 AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418, 99-103. (doi:10.1038/nature00862) (Pubitemid 34742579)
4. Pham P, Bransteitter R, Petruska J, Goodman MF. 2003 Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature 424, 103-107. (doi:10. 1038/nature01760) (Pubitemid 36834850)
5. Wissing S, Galloway NL, Greene WC. 2010 HIV-1 Vif versus the APOBEC3 cytidine deaminases: an intracellular duel between pathogen and host restriction factors. Mol. Aspects Med. 31, 383-397. (doi:10.1016/j.mam.2010.06.001)
6. Albin JS, Harris RS. 2010 Interactions of host APOBEC3 restriction factors with HIV-1 in vivo: implications for therapeutics. Expert Rev. Mol. Med. 12, e4. (doi:10.1017/S1462399409001343)
7. Kirchhoff F. 2010 Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 8, 55-67. (doi:10.1016/j.chom.2010.06.004)
8. Imahashi M, Nakashima M, Iwatani Y. 2012 Antiviral mechanism and biochemical basis of the human APOBEC3 family. Front Microbiol. 3, 250. (doi:10. 3389/fmicb.2012.00250)
9. Dang Y, Wang X, Esselman WJ, Zheng YH. 2006 Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. J. Virol. 80, 10 522-10 533. (doi:10.1128/JVI.01123-06) (Pubitemid 44628899)
10. Wiegand HL, Doehle BP, Bogerd HP, Cullen BR. 2004 A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J. 23, 2451-2458. (doi:10.1038/sj. emboj.7600246) (Pubitemid 38954852)
11. Zheng YH, Irwin D, Kurosu T, Tokunaga K, Sata T, Peterlin BM. 2004 Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication. J. Virol. 78, 6073-6076. (doi:10. 1128/JVI.78.11.6073-6076.2004) (Pubitemid 38661697)
12. Bishop KN, Holmes RK, Sheehy AM, Davidson NO, Cho SJ, Malim MH. 2004 Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr. Biol. 14, 1392-1396. (doi:10.1016/j.cub.2004.06.057) (Pubitemid 39081643)
13. Yu X, Yu Y, Liu B, Luo K, Kong W, Mao P, Yu XF. 2003 Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302, 1056-1060. (doi:10.1126/science. 1089591) (Pubitemid 37386201)
14. 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. (doi:10.1074/jbc.M313093200) (Pubitemid 38294663)
15. 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. (doi:10.1038/nature00939)
16. Lecossier D, Bouchonnet F, Clavel F, Hance AJ. 2003 Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300, 1112. (doi:10.1126/science. 1083338) (Pubitemid 36583087)
17. 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. (doi:10.1038/nm945) (Pubitemid 37466190)
18. OhAinle M, Kerns JA, Li MM, Malik HS, Emerman M. 2008 Antiretroelement activity of APOBEC3H was lost twice in recent human evolution. Cell Host Microbe 4, 249-259. (doi:10.1016/j.chom.2008.07.005)
19. Tan L, Sarkis PT, Wang T, Tian C, Yu XF. 2009 Sole copy of Z2-type human cytidine deaminase APOBEC3H has inhibitory activity against retrotransposons and HIV-1. FASEB J. 23, 279-287. (doi:10.1096/fj.07-088781)
20. Zhao K, Ishida Y, Oleksyk TK, Winkler CA, Roca AL. 2012 Evidence for selection at HIV host susceptibility genes in a West Central African human population. BMC Evol. Biol. 12, 237. (doi:10.1186/1471-2148-12-237)
21. Mahrour N et al. 2008 Characterization of Cullin-box sequences that direct recruitment of Cul2-Rbx1 and Cul5-Rbx2 modules to Elongin BC-based ubiquitin ligases. J. Biol. Chem. 283, 8005-8013. (doi:10. 1074/jbc.M706987200)
22. 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. (doi:10.1101/gad.1250204) (Pubitemid 39602305)
23. Duda DM, Borg LA, Scott DC, Hunt HW, Hammel M, Schulman BA. 2008 Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation. Cell 134, 995-1006. (doi:10.1016/j.cell.2008.07.022)
24. Zheng N et al. 2002 Structure of the Cul1-Rbx1- Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416, 703-709. (doi:10.1038/416703a) (Pubitemid 34429140)
25. Kamura T, Maenaka K, Kotoshiba S, Matsumoto M, Kohda D, Conaway RC, Conaway JW, Nakayama KI. 2004 VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes Dev. 18, 3055-3065. (doi:10.1101/gad.1252404) (Pubitemid 39658174)
26. Zhou X, Evans SL, Han X, Liu Y, Yu XF. 2012 Characterization of the interaction of full-length HIV-1 Vif protein with its key regulator CBFbeta and CRL5 E3 ubiquitin ligase components. PLoS ONE 7, e33495. (doi:10.1371/journal. pone.0033495)
27. Jager S et al. 2012 Vif hijacks CBF-beta to degrade APOBEC3G and promote HIV-1 infection. Nature 481, 371-375
28. Kim DY, Kwon E, Hartley PD, Crosby DC, Mann S, Krogan NJ, Gross JD. 2013 CBFbeta stabilizes HIV Vif to counteract APOBEC3 at the expense of RUNX1 target gene expression. Mol. Cell 49, 632-644. (doi:10.1016/j.molcel.2012.12.012)
29. Zhang W, Du J, Evans SL, Yu Y, Yu XF. 2012 T-cell differentiation factor CBF-beta regulates HIV-1 Vifmediated evasion of host restriction. Nature 481, 376-379.
30. Du J, Zhao K, Rui Y, Li P, Zhou X, Zhang W, Yu XF. 2013 Differential requirements for HIV-1 Vifmediated APOBEC3G degradation and RUNX1- mediated transcription by core binding factor beta. J. Virol. 87, 1906-1911. (doi:10.1128/JVI.02199-12)
31. He Z, Zhang W, Chen G, Xu R, Yu XF. 2008 Characterization of conserved motifs in HIV-1 Vif required for APOBEC3G and APOBEC3F interaction. J. Mol. Biol. 381, 1000-1011. (doi:10.1016/j.jmb. 2008.06.061)
32. Russell RA, Pathak VK. 2007 Identification of two distinct human immunodeficiency virus type 1 Vif determinants critical for interactions with human APOBEC3G and APOBEC3F. J. Virol. 81, 8201-8210. (doi:10.1128/JVI.00395-07) (Pubitemid 47101506)
33. Paul I, Cui J, Maynard EL. 2006 Zinc binding to the HCCH motif of HIV-1 virion infectivity factor induces a conformational change that mediates proteinprotein interactions. Proc. Natl Acad. Sci. USA 103, 18 475-18 480. (doi:10.1073/pnas.0604150103) (Pubitemid 44913435)
34. Xiao Z, Xiong Y, Zhang W, Tan L, Ehrlich E, Guo D, Yu XF. 2007 Characterization of a novel Cullin5 binding domain in HIV-1 Vif. J. Mol. Biol. 373, 541-550. (doi:10.1016/j.jmb.2007.07.029) (Pubitemid 47488386)
35. Mehle A, Thomas ER, Rajendran KS, Gabuzda D. 2006 A zinc-binding region in Vif binds Cul5 and determines cullin selection. J. Biol. Chem. 281, 17 259-17 265. (doi:10.1074/jbc.M602413200)
36. Kobayashi M, Takaori-Kondo A, Miyauchi Y, Iwai K, Uchiyama T. 2005 Ubiquitination of APOBEC3G by an HIV-1 Vif-Cullin5-Elongin B-Elongin C complex is essential for Vif function. J. Biol. Chem. 280, 18 573-18 578. (doi:10.1073/pnas.0604150103) (Pubitemid 41379555)
37. Bergeron JR, Huthoff H, Veselkov DA, Beavil RL, Simpson PJ, Matthews SJ, Malim MH, Sanderson MR. 2010 The SOCS-box of HIV-1 Vif interacts with ElonginBC by induced-folding to recruit its Cul5- containing ubiquitin ligase complex. PLoS Pathog. 6, e1000925. (doi:10.1371/journal.ppat.1000925)
38. Stanley BJ, Ehrlich ES, Short L, Yu Y, Xiao Z, Yu XF, Xiong Y. 2008 Structural insight into the human immunodeficiency virus Vif SOCS box and its role in human E3 ubiquitin ligase assembly. J. Virol. 82, 8656-8663. (doi:10.1128/JVI.00767-08)
39. 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. (doi:10.1101/gad.1249904) (Pubitemid 39602304)
40. Simon JH, Sheehy AM, Carpenter EA, Fouchier RA, Malim MH. 1999 Mutational analysis of the human immunodeficiency virus type 1 Vif protein. J. Virol. 73, 2675-2681. (Pubitemid 29135652)
41. Donahue JP, Vetter ML, Mukhtar NA, D'Aquila RT. 2008 The HIV-1 Vif PPLP motif is necessary for human APOBEC3G binding and degradation. Virology 377, 49-53. (doi:10.1016/j.virol.2008.04.017)
42. Walker Jr RC, Khan MA, Kao S, Goila-Gaur R, Miyagi E, Strebel K. 2010 Identification of dominant negative human immunodeficiency virus type 1 Vif mutants that interfere with the functional inactivation of APOBEC3G by virus-encoded Vif. J. Virol. 84, 5201-5211. (doi:10.1128/JVI.02318-09)
43. Yang B, Gao L, Li L, Lu Z, Fan X, Patel CA, Pomerantz RJ, DuBois GC, Zhang H. 2003 Potent suppression of viral infectivity by the peptides that inhibit multimerization of human immunodeficiency virus type 1 (HIV-1) Vif proteins. J. Biol. Chem. 278, 6596-6602. (doi:10.1074/jbc.M210164200) (Pubitemid 36800923)
44. Techtmann SM, Ghirlando R, Kao S, Strebel K, Maynard EL. 2012 Hydrodynamic and functional analysis of HIV-1 Vif oligomerization. Biochemistry 51, 2078-2086. (doi:10.1021/bi201738a)
45. Engelman A, Cherepanov P. 2012 The structural biology of HIV-1: mechanistic and therapeutic insights. Nat. Rev. Microbiol. 10, 279-290. (doi:10. 1038/nrmicro2747)
46. Barraud P, Paillart JC, Marquet R, Tisne C. 2008 Advances in the structural understanding of Vif proteins. Curr. HIV Res. 6, 91-99. (doi:10.2174/ 157016208783885056) (Pubitemid 351479788)
47. Babon JJ, Sabo JK, Soetopo A, Yao S, Bailey MF, Zhang JG, Nicola NA, Norton RS. 2008 The SOCS box domain of SOCS3: structure and interaction with the elonginBC-cullin5 ubiquitin ligase. J. Mol. Biol. 381, 928-940. (doi:10.1016/j.jmb.2008.06.038)
48. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A. 1995 NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293. (doi:10.1007/BF00197809)
49. Vranken WF et al. 2005 The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687-696. (doi:10.1002/ prot.20449) (Pubitemid 40695845)
50. Fogh RH, Boucher W, Vranken WF, Pajon A, Stevens TJ, Bhat TN, Westbrook J, Ionides JM, Laue ED. 2005 A framework for scientific data modeling and automated software development. Bioinformatics 21, 1678-1684. (doi:10.1093/bioinformatics/bti234) (Pubitemid 40542728)
51. Korotkova N et al. 2008 Binding of Dr adhesins of Escherichia coli to carcinoembryonic antigen triggers receptor dissociation. Mol. Microbiol. 67, 420-434. (doi:10.1111/j.1365-2958.2007.06054.x) (Pubitemid 350295843)
52. Battiste JL, Wagner G. 2000 Utilization of sitedirected spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data. Biochemistry 39, 5355-5365. (doi:10.1021/bi000060h) (Pubitemid 30257075)
53. Shen Y, Vernon R, Baker D, Bax A. 2009 De novo protein structure generation from incomplete chemical shift assignments. J. Biomol. NMR 43, 63-78. (doi:10.1007/s10858-008-9288-5)
54. Ramelot TA et al. 2009 Improving NMR protein structure quality by Rosetta refinement: a molecular replacement study. Proteins 75, 147-167. (doi:10. 1002/prot.22229)
55. Dominguez C, Boelens R, Bonvin AM. 2003 HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 125, 1731-1737. (doi:10.1021/ ja026939x) (Pubitemid 36232568)
56. de Vries SJ, van Dijk M, Bonvin AM. 2010 The HADDOCK web server for data-driven biomolecular docking. Nat. Protocol 5, 883-897. (doi:10.1038/ nprot.2010.32)
57. Zhou P, Lugovskoy AA, Wagner G. 2001 A solubilityenhancement tag (SET) for NMR studies of poorly behaving proteins. J. Biomol. NMR 20, 11-14. (doi:10.1023/A:1011258906244) (Pubitemid 32519649)
58. Schreiber G. 2002 Kinetic studies of protein-protein interactions. Curr. Opin. Struct. Biol. 12, 41-47. (doi:10.1016/S0959-440X(02)00287-7) (Pubitemid 34142719)
59. Wolfe LS, Stanley BJ, Liu C, Eliason WK, Xiong Y. 2010 Dissection of the HIVVif interaction with human E3 ubiquitin ligase. J. Virol. 84, 7135-7139. (doi:10.1128/JVI.00031-10)
60. Tzeng SR, Kalodimos CG. 2012 Protein activity regulation by conformational entropy. Nature 488, 236-240. (doi:10.1038/nature11271)
61. Bullock AN, Debreczeni JE, Edwards AM, Sundstrom M, Knapp S. 2006 Crystal structure of the SOCS2- elongin C-elongin B complex defines a prototypical SOCS box ubiquitin ligase. Proc. Natl Acad. Sci. USA 103, 7637-7642. (doi:10.1073/pnas.0601638103)
62. Wang X et al. 2013 Interactions between HIV-1 Vif and human ElonginB-ElonginC are important for CBF-beta binding to Vif. Retrovirology 10, 94. (doi:10.1186/1742-4690-10-94)
63. Garvey KJ, Oberste MS, Elser JE, Braun MJ, Gonda MA. 1990 Nucleotide sequence and genome organization of biologically active proviruses of the bovine immunodeficiency-like virus. Virology 175, 391-409. (doi:10.1016/0042-6822(90) 90424-P) (Pubitemid 20133441)
64. Bullock AN, Rodriguez MC, Debreczeni JE, Songyang Z, Knapp S. 2007 Structure of the SOCS4-ElonginB/C complex reveals a distinct SOCS box interface and the molecular basis for SOCS-dependent EGFR degradation. Structure 15, 1493-1504. (doi:10. 1016/j.str.2007.09.016) (Pubitemid 350051927)
65. Zadjali F et al. 2011 Structural basis for c-KIT inhibition by the suppressor of cytokine signaling 6 (SOCS6) ubiquitin ligase. J. Biol. Chem. 286, 480-490. (doi:10.1074/jbc.M110.173526)
66. Ribeiro AC, Maia e Silva A, Santa-Marta M, Pombo A, Moniz-Pereira J, Goncalves J, Barahona I. 2005 Functional analysis of Vif protein shows less restriction of human immunodeficiency virus type 2 by APOBEC3G. J. Virol. 79, 823-833. (doi:10.1128/ JVI.79.2.823-833.2005) (Pubitemid 40053865)
67. Oberste MS, Gonda MA. 1992 Conservation of amino-acid sequence motifs in lentivirus Vif proteins. Virus Genes 6, 95-102. (doi:10.1007/ BF01703760)