Cellular requirements for bovine immunodeficiency virus Vif-mediated inactivation of bovine APOBEC3 proteins

Journal of Virology

Volumn 88, Issue 21, 2014, Pages 12528-12540

  Zhang, Wenyan ^a,b   Wang, Hong ^a   Li, Zhaolong ^a   Liu, Xin ^a   Liu, Guanchen ^a   Harris, Reuben S ^c   Yu, Xiao Fang ^a,b,d  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d TIANJIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3F; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; CARRIER PROTEINS AND BINDING PROTEINS; CORE BINDING FACTOR BETA; CULLIN; CULLIN 5; ELONGIN B; ELONGIN C; RBX1 PROTEIN; RBX2 PROTEIN; UNCLASSIFIED DRUG; VIF PROTEIN; CARRIER PROTEIN; CYTOSINE DEAMINASE; PROTEIN BINDING; UBIQUITIN PROTEIN LIGASE;

ARTICLE; BOVINE IMMUNODEFICIENCY LIKE VIRUS; CONTROLLED STUDY; HUMAN; NONHUMAN; PROTEIN DEGRADATION; RNA INTERFERENCE; VIRUS ASSEMBLY; VIRUS INACTIVATION; VIRUS INHIBITION; VIRUS MUTATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BOVINE; HOST PATHOGEN INTERACTION; IMMUNE EVASION; IMMUNOLOGICAL TOLERANCE; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS;

ANIMALS; CARRIER PROTEINS; CATTLE; CULLIN PROTEINS; CYTOSINE DEAMINASE; GENE PRODUCTS, VIF; HOST-PATHOGEN INTERACTIONS; IMMUNE EVASION; IMMUNE TOLERANCE; IMMUNODEFICIENCY VIRUS, BOVINE; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEOLYSIS; UBIQUITIN-PROTEIN LIGASES;

EID: 84907997112     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02072-14     Document Type: Article

References (42)

1. Jones D, Crowe E, Stevens TA, Candido EP. 2002. Functional and phylogenetic analysis of the ubiquitylation system in Caenorhabditis elegans: ubiquitin-conjugating enzymes, ubiquitin-activating enzymes, and ubiquitin-like proteins. Genome Biol. 3:RESEARCH0002. http://dx.doi.org/10.1186/gb-2001-3-1-research0002.
2. Petroski MD, Deshaies RJ. 2005. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6:9-20. http://dx.doi.org/10.1038/nrm1547.
3. 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. http://dx.doi.org/10.1126 /science.1089591.
4. Conticello SG, Harris RS, Neuberger MS. 2003. The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr. Biol. 13:2009-2013. http://dx.doi.org/10.1016/j.cub.2003.10.034.
5. 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. http://dx.doi.org/10.1038/nm946.
6. Mehle A, Strack B, Ancuta P, Zhang C, McPike M, Gabuzda D. 2004. Vif overcomes the innate antiviral activity ofAPOBEC3Gby promoting its degradation in the ubiquitin-proteasome pathway. J. Biol. Chem. 279: 7792-7798. http://dx.doi.org/10.1074/jbc.M313093200.
7. 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. http://dx.doi.org/10.1038/nm945.
8. 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. http://dx.doi.org/10.1016/S1097-2765(03)00353-8.
9. 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. http://dx.doi.org/10.1101/gad.1249904.
10. 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. http://dx.doi.org/10.1101/gad.1250204.
11. Hultquist JF, Binka M, LaRue RS, Simon V, Harris RS. 2012. Vif proteins of human and simian immunodeficiency viruses require cellular CBFbeta to degrade APOBEC3 restriction factors. J. Virol. 86:2874-2877. http://dx.doi.org/10.1128/JVI.06950-11.
12. Jonsson SR, Hache G, Stenglein MD, Fahrenkrug SC, Andresdottir V, Harris RS. 2006. Evolutionarily conserved and non-conserved retrovirus restriction activities of artiodactyl APOBEC3F proteins. Nucleic Acids Res. 34:5683-5694. http://dx.doi.org/10.1093/nar/gkl721.
13. Chackerian B, Long EM, Luciw PA, Overbaugh J. 1997. Human immunodeficiency virus type 1 coreceptors participate in postentry stages in the virus replication cycle and function in simian immunodeficiency virus infection. J. Virol. 71:3932-3939.
14. Larue RS, Lengyel J, Jonsson SR, Andresdottir V, Harris RS. 2010. Lentiviral Vif degrades the APOBEC3Z3/APOBEC3H protein of its mammalian host and is capable of cross-species activity. J. Virol. 84:8193-8201. http://dx.doi.org/10.1128/JVI.00685-10.
15. Han X, Liang W, Hua D, Zhou X, Du J, Evans SL, Gao Q, Wang H, Viqueira R, Wei W, Zhang W, Yu XF. 2014. Evolutionarily conserved requirement for core binding factor beta in the assembly of the human immunodeficiency virus/simian immunodeficiency virus Vif-Cullin 5-RING E3 ubiquitin ligase. J. Virol. 88:3320-3328. http://dx.doi.org/10.1128/JVI.03833-13.
16. Zhang W, Chen G, Niewiadomska AM, Xu R, Yu XF. 2008. Distinct determinants in HIV-1 Vif and human APOBEC3 proteins are required for the suppression of diverse host anti-viral proteins. PLoS One 3:e3963. http://dx.doi.org/10.1371/journal.pone.0003963.
17. 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. http://dx.doi.org/10.1016/j.jmb.2008.06.061.
18. Chen G, He Z, Wang T, Xu R, Yu XF. 2009. A patch of positively charged amino acids surrounding the human immunodeficiency virus type 1 Vif SLVx4Yx9Y motif influences its interaction with APOBEC3G. J. Virol. 83:8674-8682. http://dx.doi.org/10.1128/JVI.00653-09.
19. Guo Y, Dong L, Qiu X, Wang Y, Zhang B, Liu H, Yu Y, Zang Y, Yang M, Huang Z. 2014. Structural basis for hijacking CBF-beta and CUL5 E3 ligase complex by HIV-1 Vif. Nature 505:229-233. http://dx.doi.org/10.1038/nature12884.
20. Fribourgh JL, Nguyen HC, Wolfe LS, Dewitt DC, Zhang W, Yu XF, Rhoades E, Xiong Y. 2014. Core binding factor beta plays a critical role by facilitating the assembly of the Vif-cullin 5 E3 ubiquitin ligase. J. Virol. 88:3309-3319. http://dx.doi.org/10.1128/JVI.03824-13.
21. Zhou X, Han X, Zhao K, Du J, Evans SL, Wang H, Li P, Zheng W, Rui Y, Kang J, Yu XF. 2014. Dispersed and conserved hydrophobic residues of HIV-1 Vif are essential for CBFβ recruitment and A3G suppression. J. Virol. 88:2555-2563. http://dx.doi.org/10.1128/JVI.03604-13.
22. Matsui Y, Shindo K, Nagata K, Io K, Tada K, Iwai F, Kobayashi M, Kadowaki N, Harris RS, Takaori-Kondo A. 2014. Defining HIV-1 Vif residues that interact with CBFbeta by site-directed mutagenesis. Virology 449:82-87. http://dx.doi.org/10.1016/j.virol.2013.11.004.
23. 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. http://dx.doi.org /10.1101/gad.1252404.
24. Gonda MA, Oberste MS, Garvey KJ, Pallansch LA, Battles JK, Pifat DY, Bess JW, Jr, Nagashima K. 1990. Development of the bovine immunodeficiency-like virus as a model of lentivirus disease. Dev. Biol. Stand. 72:97-110.
25. Mahrour N, Redwine WB, Florens L, Swanson SK, Martin-Brown S, Bradford WD, Staehling-Hampton K, Washburn MP, Conaway RC, Conaway JW. 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. http://dx.doi.org/10.1074/jbc.M706987200.
26. Querido E, Blanchette P, Yan Q, Kamura T, Morrison M, Boivin D, Kaelin WG, Conaway RC, Conaway JW, Branton PE. 2001. Degradation of p53 by adenovirus E4orf6 and E1B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 15:3104-3117 http://dx.doi.org/10.1101/gad.926401.
27. Iwai K, Yamanaka K, Kamura T, Minato N, Conaway RC, Conaway JW, Klausner RD, Pause A. 1999. Identification of the von Hippel-Lindau tumor-suppressor protein as part of an active E3 ubiquitin ligase complex. Proc. Natl. Acad. Sci. U. S. A. 96:12436-12441. http://dx.doi.org/10.1073 /pnas.96.22.12436.
28. Zhang W, Huang M, Wang T, Tan L, Tian C, Yu X, Kong W, Yu XF. 2008 Conserved and non-conserved features of HIV-1 and SIVagm Vif mediated suppression of APOBEC3 cytidine deaminases. Cell. Microbiol. 10:1662-1675. http://dx.doi.org/10.1111/j.1462-5822.2008.01157.x.
29. Evans SL, Schon A, Gao Q, Han X, Zhou X, Freire E, Yu XF. 2014. HIV-1 Vif N-terminal motif is required for recruitment of Cul5 to suppress APOBEC3. Retrovirology 11:4. http://dx.doi.org/10.1186/1742-4690-11-4.
30. Pickart CM. 2004. Back to the future with ubiquitin. Cell 116:181-190. http://dx.doi.org/10.1016/S0092-8674(03)01074-2.
31. 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: 18573-18578. http://dx.doi.org/10.1074/jbc.C500082200.
32. Jager S, Kim DY, Hultquist JF, Shindo K, LaRue RS, Kwon E, Li M, Anderson BD, Yen L, Stanley D, Mahon C, Kane J, Franks-Skiba K, Cimermancic P, Burlingame A, Sali A, Craik CS, Harris RS, Gross JD, Krogan NJ. 2012. Vif hijacks CBF-beta to degrade APOBEC3G and promote HIV-1 infection. Nature 481:371-375. http://dx.doi.org/10.1038 /nature10693.
33. Zhang W, Du J, Evans SL, Yu Y, Yu XF. 2012. T-cell differentiation factor CBF-beta regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481:376-379. http://dx.doi.org/10.1038/nature10718.
34. Luo K, Xiao Z, Ehrlich E, Yu Y, Liu B, Zheng S, Yu XF. 2005. 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. U. S. A. 102:11444-11449. http://dx.doi.org/10.1073 /pnas.0502440102.
35. Wada H, Yeh ET, Kamitani T. 2000. A dominant-negative UBC12 mutant sequesters NEDD8 and inhibits NEDD8 conjugation in vivo. J. Biol. Chem. 275:17008-17015. http://dx.doi.org/10.1074/jbc.275.22.17008.
36. Huang DT, Ayrault O, Hunt HW, Taherbhoy AM, Duda DM, Scott DC, Borg LA, Neale G, Murray PJ, Roussel MF, Schulman BA. 2009. E2-RING expansion of the NEDD8 cascade confers specificity to cullin modification. Mol. Cell 33:483-495. http://dx.doi.org/10.1016/j.molcel.2009.01.011.
37. Soucy TA, Smith PG, Milhollen MA, Berger AJ, Gavin JM, Adhikari S, Brownell JE, Burke KE, Cardin DP, Critchley S, Cullis CA, Doucette A, Garnsey JJ, Gaulin JL, Gershman RE, Lublinsky AR, McDonald A, Mizutani H, Narayanan U, Olhava EJ, Peluso S, Rezaei M, Sintchak MD, Talreja T, Thomas MP, Traore T, Vyskocil S, Weatherhead GS, Yu J, Zhang J, Dick LR, Claiborne CF, Rolfe M, Bolen JB, Langston SP. 2009. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458:732-736. http://dx.doi.org/10.1038/nature07884.
38. Liu J, Furukawa M, Matsumoto T, Xiong Y. 2002. NEDD8 modification of CUL1 dissociates p120(CAND1), an inhibitor of CUL1-SKP1 binding and SCF ligases. Mol. Cell 10:1511-1518. http://dx.doi.org/10.1016/S1097-2765(02)00783-9.
39. Morimoto M, Nishida T, Honda R, Yasuda H. 2000. Modification of cullin-1 by ubiquitin-like protein Nedd8 enhances the activity of SCF (skp2) toward p27(kip1). Biochem. Biophys. Res. Commun. 270:1093-1096 http://dx.doi.org/10.1006/bbrc.2000.2576.
40. Stanley DJ, Bartholomeeusen K, Crosby DC, Kim DY, Kwon E, Yen L, Cartozo NC, Li M, Jager S, Mason-Herr J, Hayashi F, Yokoyama S, Krogan NJ, Harris RS, Peterlin BM, Gross JD. 2012. Inhibition of a NEDD8 cascade restores restriction of HIV by APOBEC3G. PLoS Pathog. 8:e1003085. http://dx.doi.org/10.1371/journal.ppat.1003085.
41. Kamura T, Koepp DM, Conrad MN, Skowyra D, Moreland RJ, Iliopoulos O, Lane WS, Kaelin WG, Jr, Elledge SJ, Conaway RC, Harper JW, Conaway JW. 1999. Rbx1, a component of the VHL tumor suppressor complex and SCF ubiquitin ligase. Science 284:657-661. http://dx.doi.org/10.1126/science.284.5414.657.
42. Kibel A, Iliopoulos O, DeCaprio JA, Kaelin WG, Jr. 1995. Binding of the von Hippel-Lindau tumor suppressor protein to Elongin B and C. Science 269:1444-1446. http://dx.doi.org/10.1126/science.7660130.