Long-term restriction by APOBEC3F selects human immunodeficiency virus type 1 variants with restored vif function

Journal of Virology

Volumn 84, Issue 19, 2010, Pages 10209-10219

  Albin, John S ^a   Haché, Guylaine ^a,b   Hultquist, Judd F ^a   Brown, William L ^a   Harris, Reuben S ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

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; LYSINE; VIF PROTEIN; APOBEC3F PROTEIN, HUMAN; APOBEC3G PROTEIN, HUMAN; CYTIDINE DEAMINASE; CYTOSINE DEAMINASE; PRIMER DNA; VIF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; VIRUS DNA;

ALLELE; ARTICLE; HERITABILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN VARIANT; VIRUS ISOLATION; VIRUS NEUTRALIZATION; VIRUS REPLICATION; WILD TYPE; CELL LINE; GENETIC SELECTION; GENETICS; HOST PATHOGEN INTERACTION; MUTATION; PATHOGENICITY; PHYSIOLOGY; REGULATOR GENE; SITE DIRECTED MUTAGENESIS; T LYMPHOCYTE; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ALLELES; BASE SEQUENCE; CELL LINE; CYTIDINE DEAMINASE; CYTOSINE DEAMINASE; DNA PRIMERS; DNA, VIRAL; GENES, VIF; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MUTAGENESIS, SITE-DIRECTED; MUTATION; SELECTION, GENETIC; T-LYMPHOCYTES; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

EID: 77956848635     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00632-10     Document Type: Article

References (62)

1. Abudu, A., A. Takaori-Kondo, T. Izumi, K. Shirakawa, M. Kobayashi, A. Sasada, K. Fukunaga, and T. Uchiyama. 2006. Murine retrovirus escapes from murine APOBEC3 via two distinct novel mechanisms. Curr. Biol. 16:1565-1570.
2. Albin, J. S., and R. S. Harris. 2010. Interactions of host APOBEC3 restriction factors with HIV-1 in vivo: implications for therapeutics. Expert Rev. Mol. Med. 12:1-26.
3. Bishop, K. N., R. K. Holmes, and M. H. Malim. 2006. Antiviral potency of APOBEC proteins does not correlate with cytidine deamination. J. Virol. 80:8450-8458.
4. Bishop, K. N., R. K. Holmes, A. M. Sheehy, N. O. Davidson, S. J. Cho, and M. H. Malim. 2004. Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr. Biol. 14:1392-1396.
5. Bishop, K. N., M. Verma, E. Y. Kim, S. M. Wolinsky, and M. H. Malim. 2008. APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog. 4:e1000231.
6. Bogerd, H. P., R. L. Tallmadge, J. L. Oaks, S. Carpenter, and B. R. Cullen. 2008. Equine infectious anemia virus resists the antiretroviral activity of equine APOBEC3 proteins through a packaging-independent mechanism. J. Virol. 82:11889-11901.
7. Chen, G., Z. He, T. Wang, R. Xu, and X. F. Yu. 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.
8. Chiu, Y. L., and W. C. Greene. 2008. The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu. Rev. Immunol. 26:317-353.
9. Conticello, S. G., R. S. Harris, and M. S. Neuberger. 2003. The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr. Biol. 13:2009-2013.
10. Dang, Y., X. Wang, T. Zhou, I. A. York, and Y. H. Zheng. 2009. 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. 83:8544-8552.
11. Derse, D., S. A. Hill, G. Princler, P. Lloyd, and G. Heidecker. 2007. Resistance of human T cell leukemia virus type 1 to APOBEC3G restriction is mediated by elements in nucleocapsid. Proc. Natl. Acad. Sci. U. S. A. 104: 2915-2920.
12. Doehle, B. P., H. P. Bogerd, H. L. Wiegand, N. Jouvenet, P. D. Bieniasz, E. Hunter, and B. R. Cullen. 2006. The betaretrovirus Mason-Pfizer monkey virus selectively excludes simian APOBEC3G from virion particles. J. Virol. 80:12102-12108.
13. Doehle, B. P., A. Schafer, H. L. Wiegand, H. P. Bogerd, and B. R. Cullen. 2005. Differential sensitivity of murine leukemia virus to APOBEC3-mediated inhibition is governed by virion exclusion. J. Virol. 79:8201-8207.
14. Gervaix, A., D. West, L. M. Leoni, D. D. Richman, F. Wong-Staal, and J. Corbeil. 1997. A new reporter cell line to monitor HIV infection and drug susceptibility in vitro. Proc. Natl. Acad. Sci. U. S. A. 94:4653-4658.
15. Gifford, R. J., A. Katzourakis, M. Tristem, O. G. Pybus, M. Winters, and R. W. Shafer. 2008. A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution. Proc. Natl. Acad. Sci. U. S. A. 105:20362-20367.
16. Guo, F., S. Cen, M. Niu, J. Saadatmand, and L. Kleiman. 2006. Inhibition of formula-primed reverse transcription by human APOBEC3G during human immunodeficiency virus type 1 replication. J. Virol. 80:11710-11722. (Pubitemid 44788884)
17. Haché, G., T. E. Abbink, B. Berkhout, and R. S. Harris. 2009. Optimal translation initiation enables Vif-deficient human immunodeficiency virus type 1 to escape restriction by APOBEC3G. J. Virol. 83:5956-5960.
18. Haché, G., K. Shindo, J. S. Albin, and R. S. Harris. 2008. Evolution of HIV-1 isolates that use a novel Vif-independent mechanism to resist restriction by human APOBEC3G. Curr. Biol. 18:819-824.
19. Hassaine, G., I. Agostini, D. Candotti, G. Bessou, M. Caballero, H. Agut, B. Autran, Y. Barthalay, and R. Vigne. 2000. Characterization of human immunodeficiency virus type 1 vif gene in long-term asymptomatic individuals. Virology 276:169-180.
20. Holmes, R. K., F. A. Koning, K. N. Bishop, and M. H. Malim. 2007. APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G. J. Biol. Chem. 282:2587-2595.
21. Iwatani, Y., D. S. Chan, F. Wang, K. S. Maynard, W. Sugiura, A. M. Gronenborn, I. Rouzina, M. C. Williams, K. Musier-Forsyth, and J. G. Levin. 2007. Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res. 35:7096-7108.
22. Kao, S., M. A. Khan, E. Miyagi, R. Plishka, A. Buckler-White, and K. Strebel. 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.
23. Komoto, S., S. Tsuji, B. J. Lee, Y. Iwabu, Y. Kojima, T. Otake, K. Taniguchi, and K. Ikuta. 2005. Higher frequency of premature stop codon mutations at vpu gene of human immunodeficiency virus type 1 CRF01-AE compared with those of other subtypes. Microbes Infect. 7:139-147.
24. Koning, F. A., E. N. Newman, E. Y. Kim, K. J. Kunstman, S. M. Wolinsky, and M. H. Malim. 2009. Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J. Virol. 83:9474-9485.
25. Li, X. Y., F. Guo, L. Zhang, L. Kleiman, and S. Cen. 2007. APOBEC3G inhibits DNA strand transfer during HIV-1 reverse transcription. J. Biol. Chem. 282:32065-32074.
26. Liddament, M. T., W. L. Brown, A. J. Schumacher, and R. S. Harris. 2004. APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr. Biol. 14:1385-1391.
27. Löchelt, M., F. Romen, P. Bastone, H. Muckenfuss, N. Kirchner, Y. B. Kim, U. Truyen, U. Rösler, M. Battenberg, A. Saib, E. Flory, K. Cichutek, and C. Münk. 2005. The antiretroviral activity of APOBEC3 is inhibited by the foamy virus accessory Bet protein. Proc. Natl. Acad. Sci. U. S. A. 102:7982-7987.
28. Luo, K., T. Wang, B. Liu, C. Tian, Z. Xiao, J. Kappes, and X. F. Yu. 2007. Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. J. Virol. 81:7238-7248.
29. Mariani, R., D. Chen, B. Schröfelbauer, F. Navarro, R. König, B. Bollman, C. Münk, H. Nymark-McMahon, and N. R. Landau. 2003. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114:21-31.
30. Marin, M., S. Golem, K. M. Rose, S. L. Kozak, and D. Kabat. 2008. Human immunodeficiency virus type 1 Vif functionally interacts with diverse APOBEC3 cytidine deaminases and moves with them between cytoplasmic sites of mRNA metabolism. J. Virol. 82:987-998.
31. Marin, M., K. M. Rose, S. L. Kozak, and D. Kabat. 2003. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 9:1398-1403.
32. Mbisa, J. L., R. Barr, J. A. Thomas, N. Vandegraaff, I. J. Dorweiler, E. S. Svarovskaia, W. L. Brown, L. M. Mansky, R. J. Gorelick, R. S. Harris, A. Engelman, and V. K. Pathak. 2007. Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plusstr-and DNA transfer and integration. J. Virol. 81:7099-7110.
33. Mbisa, J. L., W. Bu, and V. K. Pathak. 2010. APOBEC3F and APOBEC3G inhibit HIV-1 DNA integration by different mechanisms. J. Virol. 84:5250-5259.
34. Mehle, A., J. Goncalves, M. Santa-Marta, M. McPike, and D. Gabuzda. 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. (Pubitemid 39602304)
35. Mehle, A., B. Strack, P. Ancuta, C. Zhang, M. McPike, and D. Gabuzda. 2004. Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J. Biol. Chem. 279:7792-7798.
36. Mercenne, G., S. Bernacchi, D. Richer, G. Bec, S. Henriet, J. C. Paillart, and R. Marquet. 2010. HIV-1 Vif binds to APOBEC3G mRNA and inhibits its translation. Nucleic Acids Res. 38:633-646.
37. Peng, G., K. J. Lei, W. Jin, T. Greenwell-Wild, and S. M. Wahl. 2006. Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J. Exp. Med. 203:41-46.
38. Rangel, H. R., D. Garzaro, A. K. Rodriguez, A. H. Ramirez, G. Ameli, C. Del Rosario Gutierrez, and F. H. Pujol. 2009. Deletion, insertion and stop codon mutations in vif genes of HIV-1 infecting slow progressor patients. J. Infect. Dev. Ctries 3:531-538.
39. Refsland, E. W., M. D. Stenglein, K. Shindo, J. S. Albin, W. L. Brown, and R. S. Harris. 2010. Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues: implications for HIV-1 restriction. Nucleic Acids Res. 38:4274-4284.
40. Russell, R. A., H. L. Wiegand, M. D. Moore, A. Schafer, M. O. McClure, and B. R. Cullen. 2005. Foamy virus Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors. J. Virol. 79: 8724-8731.
41. Sadler, H. A., M. D. Stenglein, R. S. Harris, and L. M. Mansky. 2010. APOBEC3G contributes to HIV-1 variation through sublethal mutagenesis. J. Virol. 84:7396-7404.
42. Santa-Marta, M., F. A. da Silva, A. M. Fonseca, and J. Goncalves. 2005. 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. 280:8765-8775.
43. Sheehy, A. M., N. C. Gaddis, J. D. Choi, and M. H. Malim. 2002. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650.
44. Sheehy, A. M., N. C. Gaddis, and M. H. Malim. 2003. The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat. Med. 9:1404-1407.
45. Simon, V., V. Zennou, D. Murray, Y. Huang, D. D. Ho, and P. D. Bieniasz. 2005. Natural variation in Vif: differential impact on APOBEC3G/3F and a potential role in HIV-1 diversification. PLoS Pathog. 1:e6.
46. Smith, J. L., W. Bu, R. C. Burdick, and V. K. Pathak. 2009. Multiple ways of targeting APOBEC3-virion infectivity factor interactions for anti-HIV-1 drug development. Trends Pharmacol. Sci. 30:638-646.
47. Sova, P., M. van Ranst, P. Gupta, R. Balachandran, W. Chao, S. Itescu, G. McKinley, and D. J. Volsky. 1995. Conservation of an intact human immunodeficiency virus type 1 vif gene in vitro and in vivo. J. Virol. 69:2557-2564.
48. Stenglein, M. D., and R. S. Harris. 2006. APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J. Biol. Chem. 281:16837-16841.
49. Stopak, K., C. de Noronha, W. Yonemoto, and W. C. Greene. 2003. HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol. Cell 12:591-601.
50. Tominaga, K., S. Kato, M. Negishi, and T. Takano. 1996. A high frequency of defective vif genes in peripheral blood mononuclear cells from HIV type 1-infected individuals. AIDS Res. Hum. Retroviruses 12:1543-1549.
51. Wiegand, H. L., B. P. Doehle, H. P. Bogerd, and B. R. Cullen. 2004. A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J. 23:2451-2458.
52. Wieland, U., J. Hartmann, H. Suhr, B. Salzberger, H. J. Eggers, and J. E. Kuhn. 1994. In vivo genetic variability of the HIV-1 vif gene. Virology 203:43-51.
53. Wieland, U., A. Seelhoff, A. Hofmann, J. E. Kuhn, H. J. Eggers, P. Mugyenyi, and S. Schwander. 1997. Diversity of the vif gene of human immunodeficiency virus type 1 in Uganda. J. Gen. Virol. 78:393-400.
54. Worobey, M., M. Gemmel, D. E. Teuwen, T. Haselkorn, K. Kunstman, M. Bunce, J. J. Muyembe, J. M. Kabongo, R. M. Kalengayi, E. Van Marck, M. T. Gilbert, and S. M. Wolinsky. 2008. Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature 455:661-664.
55. Yang, Y., F. Guo, S. Cen, and L. Kleiman. 2007. Inhibition of initiation of reverse transcription in HIV-1 by human APOBEC3F. Virology 365:92-100. (Pubitemid 46907232)
56. Yedavalli, V. R., and N. Ahmad. 2001. Low conservation of functional domains of HIV type 1 vif and vpr genes in infected mothers correlates with lack of vertical transmission. AIDS Res. Hum. Retroviruses 17:911-923.
57. Yedavalli, V. R., C. Chappey, E. Matala, and N. Ahmad. 1998. Conservation of an intact vif gene of human immunodeficiency virus type 1 during maternal- fetal transmission. J. Virol. 72:1092-1102.
58. Yu, X., Y. Yu, B. Liu, K. Luo, W. Kong, P. Mao, and X. F. Yu. 2003. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302:1056-1060.
59. Yu, Y., Z. Xiao, E. S. Ehrlich, X. Yu, and X. F. Yu. 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.
60. Zhang, L., Y. Huang, H. Yuan, S. Tuttleton, and D. D. Ho. 1997. Genetic characterization of vif, vpr, and vpu sequences from long-term survivors of human immunodeficiency virus type 1 infection. Virology 228:340-349.
61. Zheng, Y. H., D. Irwin, T. Kurosu, K. Tokunaga, T. Sata, and B. M. Peterlin. 2004. Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication. J. Virol. 78:6073-6076.
62. Zielonka, J., I. G. Bravo, D. Marino, E. Conrad, M. Perkovic, M. Battenberg, K. Cichutek, and C. Münk. 2009. Restriction of equine infectious anemia virus by equine APOBEC3 cytidine deaminases. J. Virol. 83:7547-7559.