Association of potent human antiviral cytidine deaminases with 7SL RNA and viral RNP in HIV-1 virions

Journal of Virology

Volumn 84, Issue 24, 2010, Pages 12903-12913

  Zhang, Wenyan ^a   Du, Juan ^a   Yu, Kevin ^b   Wang, Tao ^b   Yong, Xiong ^c   Yu, Xiao Fang ^a,b  

^a JILIN UNIVERSITY   (China)

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

^c YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7SL RNA; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; CYTIDINE DEAMINASE; GAG PROTEIN; GENOMIC RNA; RIBONUCLEOPROTEIN; TRANSFER RNA; UNCLASSIFIED DRUG; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; CHIMERA; ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN RNA BINDING; PROTEIN TARGETING; VIRION; VIRUS INHIBITION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANTIVIRAL AGENTS; BLOTTING, WESTERN; CELLS, CULTURED; CYTIDINE DEAMINASE; DNA PRIMERS; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOPRECIPITATION; KIDNEY; MOLECULAR SEQUENCE DATA; PLASMIDS; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEOPROTEINS; RNA, MESSENGER; RNA, SMALL CYTOPLASMIC; RNA, VIRAL; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL RECOGNITION PARTICLE; VIRION; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 78649395474     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01632-10     Document Type: Article

References (67)

1. Aguiar, R. S., N. Lovsin, A. Tanuri, and B. M. Peterlin. 2008. Vpr.A3A chimera inhibits HIV replication. J. Biol. Chem. 283:2518-2525.
2. Alce, T. M., and W. Popik. 2004. APOBEC3G is incorporated into virus-like particles by a direct interaction with HIV-1 Gag nucleocapsid protein. J. Biol. Chem. 279:34083-34086.
3. Bach, D., S. Peddi, B. Mangeat, A. Lakkaraju, K. Strub, and D. Trono. 2008. Characterization of APOBEC3G binding to 7SL RNA. Retrovirology 5:54.
4. Bogerd, H. P., and B. R. Cullen. 2008. Single-stranded RNA facilitates nucleocapsid: APOBEC3G complex formation. RNA 14:1228-1236.
5. Bulliard, Y., P. Turelli, U. F. Rohrig, V. Zoete, B. Mangeat, O. Michielin, and D. Trono. 2009. Functional analysis and structural modeling of human APOBEC3G reveal the role of evolutionarily conserved elements in the inhibition of human immunodeficiency virus type 1 infection and Alu transposition. J. Virol. 83:12611-12621.
6. Burnett, A., and P. Spearman. 2007. APOBEC3G multimers are recruited to the plasma membrane for packaging into human immunodeficiency virus type 1 virus-like particles in an RNA-dependent process requiring the NC basic linker. J. Virol. 81:5000-5013. (Pubitemid 46744412)
7. Cen, S., F. Guo, M. Niu, J. Saadatmand, J. Deflassieux, and L. Kleiman. 2004. The interaction between HIV-1 Gag and APOBEC3G. J. Biol. Chem. 279:33177-33184.
8. Chen, K. M., E. Harjes, P. J. Gross, A. Fahmy, Y. Lu, K. Shindo, R. S. Harris, and H. Matsuo. 2008. Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452:116-119.
9. 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.
10. Chiu, Y. L., H. E. Witkowska, S. C. Hall, M. Santiago, V. B. Soros, C. Esnault, T. Heidmann, and W. C. Greene. 2006. High-molecular-mass APOBEC3G complexes restrict Alu retrotransposition. Proc. Natl. Acad. Sci. U. S. A. 103:15588-15593.
11. 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.
12. Conticello, S. G., M. A. Langlois, and M. S. Neuberger. 2007. Insights into DNA deaminases. Nat. Struct. Mol. Biol. 14:7-9.
13. Conticello, S. G., M. A. Langlois, Z. Yang, and M. S. Neuberger. 2007. DNA deamination in immunity: AID in the context of its APOBEC relatives. Adv. Immunol. 94:37-73.
14. Cullen, B. R. 2006. Role and mechanism of action of the APOBEC3 family of antiretroviral resistance factors. J. Virol. 80:1067-1076.
15. Douaisi, M., S. Dussart, M. Courcoul, G. Bessou, R. Vigne, and E. Decroly. 2004. HIV-1 and MLV Gag proteins are sufficient to recruit APOBEC3G into virus-like particles. Biochem. Biophys. Res. Commun. 321:566-573.
16. Goila-Gaur, R., M. A. Khan, E. Miyagi, S. Kao, and K. Strebel. 2007. Targeting APOBEC3A to the viral nucleoprotein complex confers antiviral activity. Retrovirology 4:61.
17. Goila-Gaur, R., and K. Strebel. 2008. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 5:51.
18. Haché, G., L. M. Mansky, and R. S. Harris. 2006. Human APOBEC3 proteins, retrovirus restriction, and HIV drug resistance. AIDS Rev. 8:148-157.
19. Harris, R. S., K. N. Bishop, A. M. Sheehy, H. M. Craig, S. K. Petersen- Mahrt, I. N. Watt, M. S. Neuberger, and M. H. Malim. 2003. DNA deamination mediates innate immunity to retroviral infection. Cell 113:803-809.
20. Harris, R. S., S. K. Petersen-Mahrt, and M. S. Neuberger. 2002. RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol. Cell 10:1247-1253.
21. Holden, L. G., C. Prochnow, Y. P. Chang, R. Bransteitter, L. Chelico, U. Sen, R. C. Stevens, M. F. Goodman, and X. S. Chen. 2008. Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456:121-124.
22. Houzet, L., J. C. Paillart, F. Smagulova, S. Maurel, Z. Morichaud, R. Marquet, and M. Mougel. 2007. HIV controls the selective packaging of genomic, spliced viral and cellular RNAs into virions through different mechanisms. Nucleic Acids Res. 35:2695-2704. (Pubitemid 47073682)
23. Huthoff, H., F. Autore, S. Gallois-Montbrun, F. Fraternali, and M. H. Malim. 2009. RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog. 5:e1000330.
24. Huthoff, H., and M. H. Malim. 2007. Identification of amino acid residues in APOBEC3G required for regulation by human immunodeficiency virus type 1 Vif and virion encapsidation. J. Virol. 81:3807-3815.
25. Iwatani, Y., H. Takeuchi, K. Strebel, and J. G. Levin. 2006. Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect. J. Virol. 80:5992-6002.
26. Jarmuz, A., A. Chester, J. Bayliss, J. Gisbourne, I. Dunham, J. Scott, and N. Navaratnam. 2002. An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 79:285-296. (Pubitemid 34211936)
27. Keene, S. E., S. R. King, and A. Telesnitsky. 2010. 7SL RNA is retained in HIV-1 minimal virus-like particles as an S-domain fragment. J. Virol. 84: 9070-9077.
28. Khan, M. A., S. Kao, E. Miyagi, H. Takeuchi, R. Goila-Gaur, S. Opi, C. L. Gipson, T. G. Parslow, H. Ly, and K. Strebel. 2005. Viral RNA is required for the association of APOBEC3G with human immunodeficiency virus type 1 nucleoprotein complexes. J. Virol. 79:5870-5874.
29. Langlois, M. A., R. C. Beale, S. G. Conticello, and M. S. Neuberger. 2005. Mutational comparison of the single-domained APOBEC3C and double-domained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities. Nucleic Acids Res. 33:1913-1923.
30. Lecossier, D., F. Bouchonnet, F. Clavel, and A. J. Hance. 2003. Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300:1112.
31. Liu, B., P. T. Sarkis, K. Luo, Y. Yu, and X. F. Yu. 2005. Regulation of Apobec3F and human immunodeficiency virus type 1 Vif by Vif-Cul5- ElonB/C E3 ubiquitin ligase. J. Virol. 79:9579-9587.
32. Liu, B., X. Yu, K. Luo, Y. Yu, and X. F. Yu. 2004. Influence of primate lentiviral Vif and proteasome inhibitors on human immunodeficiency virus type 1 virion packaging of APOBEC3G. J. Virol. 78:2072-2081.
33. Losey, H. C., A. J. Ruthenburg, and G. L. Verdine. 2006. Crystal structure of Staphylococcus aureus tRNA adenosine deaminase TadA in complex with RNA. Nat. Struct. Mol. Biol. 13:153-159.
34. Luo, K., B. Liu, Z. Xiao, Y. Yu, X. Yu, R. Gorelick, and X. F. Yu. 2004. Amino-terminal region of the human immunodeficiency virus type 1 nucleo- capsid is required for human APOBEC3G packaging. J. Virol. 78:11841-11852.
35. Luo, K., Z. Xiao, E. Ehrlich, Y. Yu, B. Liu, S. Zheng, and X. F. Yu. 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.
36. Malim, M. H., and M. Emerman. 2008. HIV-1 accessory proteins - ensuring viral survival in a hostile environment. Cell Host Microbe 3:388-398.
37. Mangeat, B., P. Turelli, G. Caron, M. Friedli, L. Perrin, and D. Trono. 2003. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424:99-103. (Pubitemid 36834849)
38. Mariani, R., D. Chen, B. Schrofelbauer, F. Navarro, R. Konig, B. Bollman, C. Munk, H. Nymark-McMahon, and N. R. Landau. 2003. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114:21-31.
39. 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.
40. 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)
41. Mehle, A., E. R. Thomas, K. S. Rajendran, and D. Gabuzda. 2006. A zincbinding region in Vif binds Cul5 and determines cullin selection. J. Biol. Chem. 281:17259-17265.
42. Navaratnam, N., S. Bhattacharya, T. Fujino, D. Patel, A. L. Jarmuz, and J. Scott. 1995. Evolutionary origins of apoB mRNA editing: catalysis by a cytidine deaminase that has acquired a novel RNA-binding motif at its active site. Cell 81:187-195.
43. Navarro, F., B. Bollman, H. Chen, R. Konig, Q. Yu, K. Chiles, and N. R. Landau. 2005. Complementary function of the two catalytic domains of APOBEC3G. Virology 333:374-386.
44. Newman, E. N., R. K. Holmes, H. M. Craig, K. C. Klein, J. R. Lingappa, M. H. Malim, and A. M. Sheehy. 2005. Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr. Biol. 15:166-170.
45. Niewiadomska, A. M., C. Tian, L. Tan, T. Wang, P. T. Sarkis, and X. F. Yu. 2007. Differential inhibition of long interspersed element 1 by APOBEC3 does not correlate with high-molecular-mass-complex formation or P-body association. J. Virol. 81:9577-9583.
46. Niewiadomska, A. M., and X. F. Yu. 2009. Host restriction of HIV-1 by APOBEC3 and viral evasion through Vif. Curr. Top. Microbiol. Immunol. 339:1-25.
47. Onafuwa-Nuga, A. A., A. Telesnitsky, and S. R. King. 2006. 7SL RNA, but not the 54-kd signal recognition particle protein, is an abundant component of both infectious HIV-1 and minimal virus-like particles. RNA 12:542-546.
48. Prochnow, C., R. Bransteitter, M. G. Klein, M. F. Goodman, and X. S. Chen. 2007. The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 445:447-451.
49. Schäfer, A., H. P. Bogerd, and B. R. Cullen. 2004. Specific packaging of APOBEC3G into HIV-1 virions is mediated by the nucleocapsid domain of the gag polyprotein precursor. Virology 328:163-168.
50. 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.
51. 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.
52. Soros, V. B., W. Yonemoto, and W. C. Greene. 2007. Newly synthesized APOBEC3G is incorporated into HIV virions, inhibited by HIV RNA, and subsequently activated by RNase H. PLoS Pathog. 3:e15.
53. 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.
54. Suspène, R., P. Sommer, M. Henry, S. Ferris, D. Guetard, S. Pochet, A. Chester, N. Navaratnam, S. Wain-Hobson, and J. P. Vartanian. 2004. APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase. Nucleic Acids Res. 32:2421-2429.
55. Svarovskaia, E. S., H. Xu, J. L. Mbisa, R. Barr, R. J. Gorelick, A. Ono, E. O. Freed, W. S. Hu, and V. K. Pathak. 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.
56. Tian, C., T. Wang, W. Zhang, and X. F. Yu. 2007. Virion packaging determinants and reverse transcription of SRP RNA in HIV-1 particles. Nucleic Acids Res. 35:7288-7302.
57. Wang, T., C. Tian, W. Zhang, K. Luo, P. T. Sarkis, L. Yu, B. Liu, Y. Yu, and X. F. Yu. 2007. 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J. Virol. 81:13112-13124.
58. Wang, T., W. Zhang, C. Tian, B. Liu, Y. Yu, L. Ding, P. Spearman, and X. F. Yu. 2008. Distinct viral determinants for the packaging of human cytidine deaminases APOBEC3G and APOBEC3C. Virology 377:71-79.
59. Xiao, Z., E. Ehrlich, Y. Yu, K. Luo, T. Wang, C. Tian, and X. F. Yu. 2006. Assembly of HIV-1 Vif-Cul5 E3 ubiquitin ligase through a novel zinc-binding domain-stabilized hydrophobic interface in Vif. Virology 349:290-299.
60. Xiao, Z., Y. Xiong, W. Zhang, L. Tan, E. Ehrlich, D. Guo, and X. F. Yu. 2007. Characterization of a novel cullin5 binding domain in HIV-1 Vif. J. Mol. Biol. 373:541-550.
61. Yu, Q., D. Chen, R. Konig, R. Mariani, D. Unutmaz, and N. R. Landau. 2004. APOBEC3B and APOBEC3C are potent inhibitors of simian immunodeficiency virus replication. J. Biol. Chem. 279:53379-53386.
62. Yu, Q., R. Konig, S. Pillai, K. Chiles, M. Kearney, S. Palmer, D. Richman, J. M. Coffin, and N. R. Landau. 2004. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 11:435-442.
63. 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.
64. 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.
65. Zennou, V., D. Perez-Caballero, H. Gottlinger, and P. D. Bieniasz. 2004. APOBEC3G incorporation into human immunodeficiency virus type 1 particles. J. Virol. 78:12058-12061.
66. Zhang, H., B. Yang, R. J. Pomerantz, C. Zhang, S. C. Arunachalam, and L. Gao. 2003. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424:94-98. (Pubitemid 36834848)
67. Zhang, K. L., B. Mangeat, M. Ortiz, V. Zoete, D. Trono, A. Telenti, and O. Michielin. 2007. Model structure of human APOBEC3G. PLoS One 2:e378.