Deamination-independent inhibition of hepatitis B virus reverse transcription by APOBEC3G

Journal of Virology

Volumn 81, Issue 9, 2007, Pages 4465-4472

  Nguyen, David H ^a   Gummuluru, Suryaram ^b   Hu, Jianming ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (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; CYTIDINE DEAMINASE; SINGLE STRANDED DNA; VIRUS DNA;

ANTIVIRAL ACTIVITY; ARTICLE; CELL LINE; CONTROLLED STUDY; DEAMINATION; DNA DEGRADATION; DNA RNA HYBRIDIZATION; DNA SYNTHESIS INHIBITION; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RETROVIRUS; REVERSE TRANSCRIPTION; RNA PACKAGING; VIROGENESIS; VIRUS INHIBITION; VIRUS REPLICATION;

BLOTTING, SOUTHERN; BLOTTING, WESTERN; CELL LINE, TUMOR; DNA, VIRAL; HEPATITIS B VIRUS; HUMANS; NUCLEOCAPSID; NUCLEOSIDE DEAMINASES; REPRESSOR PROTEINS; REVERSE TRANSCRIPTION; VIRUS ASSEMBLY;

HEPATITIS B VIRUS; MAMMALIA;

EID: 34247635482     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02510-06     Document Type: Article

References (59)

1. 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.
2. 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.
3. Bonvin, M., F. Achermann, I. Greeve, D. Stroka, A. Keogh, D. Inderbitzin, D. Candinas, P. Sommer, S. Wain-Hobson, J. P. Vartanian, and J. Greeve. 2006. Interferon-inducible expression of APOBEC3 editing enzymes in human hepatocytes and inhibition of hepatitis B virus replication. Hepatology 43:1364-1374.
4. Chelico, L., P. Pham, P. Calabrese, and M. F. Goodman. 2006. APOBEC3G DNA deaminase acts processively 3′→5′ on single-stranded DNA. Nat. Struct. Mol. Biol. 13:392-399.
5. Chen, H., C. E. Lilley, Q. Yu, D. V. Lee, J. Chou, I. Narvaiza, N. R. Landau, and M. D. Weitzman. 2006. APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr. Biol. 16:480-485.
6. Chen, Y., and P. L. Marion. 1996. Amino acids essential for RNase H activity of hepadnaviruses are also required for efficient elongation of minus-strand viral DNA. J. Virol. 70:6151-6156.
7. Chiu, Y. L., V. B. Soros, J. F. Kreisberg, K. Stopak, W. Yonemoto, and W. C. Greene. 2005. Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells. Nature 435:108-114.
8. Cullen, B. R. 2006. Role and mechanism of action of the APOBEC3 family of antiretroviral resistance factors. J. Virol. 80:1067-1076.
9. Delebecque, F., R. Suspene, S. Calattini, N. Casartelli, A. Saib, A. Froment, S. Wain-Hobson, A. Gessain, J. P. Vartanian, and O. Schwartz. 2006. Restriction of foamy viruses by APOBEC cytidine deaminases. J. Virol. 80:605-614.
10. Di Noia, J., and M. S. Neuberger. 2002. Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature 419: 43-48.
11. Fallows, D. A., and S. P. Goff. 1995. Mutations in the epsilon sequences of human hepatitis B virus affect both RNA encapsidation and reverse transcription. J. Virol. 69:3067-3073.
12. Ganem, D., and A. M. Prince. 2004. Hepatitis B virus infection - natural history and clinical consequences. N. Engl. J. Med. 350:1118- 1129.
13. Ganem, D., and R. J. Schneider. 2001. Hepadnaviridae, p. 2923-2969. In D. M. Knipe and P. M. Howley (ed.), Fields virology. Lippincott Williams & Wilkins, Philadelphia, PA.
14. Gerelsaikhan, T., J. Tavis, and V. Bruss. 1996. Hepatitis B virus nucleocapsid envelopment does not occur without genomic DNA synthesis. J. Virol. 70:4269-4274.
15. Guo, J. T., M. Pryce, X. Wang, M. I. Barrasa, J. Hu, and C. Seeger. 2003. Conditional replication of duck hepatitis B virus in hepatoma cells. J. Virol. 77:1885-1893.
16. 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.
17. Harris, R. S., and M. T. Liddament. 2004. Retroviral restriction by APOBEC proteins. Nat. Rev. Immunol. 4:868-877.
18. Hu, J., D. Flores, D. Toft, X. Wang, and D. Nguyen. 2004. Requirement of heat shock protein 90 for human hepatitis B virus reverse transcriptase function. J. Virol. 78:13122-13131.
19. Hu, J., and C. Seeger. 1996. Hsp90 is required for the activity of a hepatitis B virus reverse transcriptase. Proc. Natl. Acad. Sci. USA 93:1060-1064.
20. Hu, J., and C. Seeger. 1997. RNA signals that control DNA replication in hepadnaviruses. Semin. Virol. 8:205-211.
21. Hu, J., D. O. Toft, and C. Seeger. 1997. Hepadnavirus assembly and reverse transcription require a multi-component chaperone complex which is incorporated into nucleocapsids. EMBO J. 16:59-68.
22. Huthoff, H., and M. H. Malim. 2005. Cytidine deamination and resistance to retroviral infection: towards a structural understanding of the APOBEC proteins. Virology 334:147-153.
23. 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.
24. 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.
25. Junker-Niepmann, M., R. Bartenschlager, and H. Schaller. 1990. A short cis-acting sequence is required for hepatitis B virus pregenome encapsidation and sufficient for packaging of foreign RNA. EMBO J. 9:3389-3396.
26. Kaiser, S. M., and M. Emerman. 2006. Uracil DNA glycosylase is dispensable for human immunodeficiency virus type 1 replication and does not contribute to the antiviral effects of the cytidine deaminase Apobec3G. J. Virol. 80:875-882.
27. 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.
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. Lanford, R. E., L. Notvall, and B. Beames. 1995. Nucleotide priming and reverse transcriptase activity of hepatitis B virus polymerase expressed in insect cells. J. Virol. 69:4431-4439.
30. Lanford, R. E., L. Notvall, H. Lee, and B. Beames. 1997. Transcomplementation of nucleotide priming and reverse transcription between independently expressed TP and RT domains of the hepatitis B virus reverse transcriptase. J. Virol. 71:2996-3004.
31. Lecossier, D., F. Bouchonnet, F. Gavel, and A. J. Hance. 2003. Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300:1112.
32. MacGinnitie, A. J., S. Anant, and N. O. Davidson. 1995. Mutagenesis of apobcc-1, the catalytic subunit of the mammalian apolipoprotein B mRNA editing enzyme, reveals distinct domains that mediate cytosine nucleoside deaminase, RNA binding, and RNA editing activity. J. Biol. Chem. 270: 14768-14775.
33. 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.
34. 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.
35. 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.
36. 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.
37. Noguchi, C., H. Ishino, M. Tsuge, Y. Fujimoto, M. Imamura, S. Takahashi, and K. Chayama. 2005. G to A hypermutation of hepatitis B virus. Hepatology 41:626-633.
38. Prochnow, C., R. Bransteitter, M. G. Klein, M. K. Goodman, and X. S. Chen. 2007. The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 445:447-451.
39. Radziwill, G., W. Tucker, and H. Schaller. 1990. Mutational analysis of the hepatitis B virus P gene product: domain structure and RNase H activity. J. Virol. 64:613-620.
40. Rieger, A., and M. Nassal. 1996. Specific hepatitis B virus minus-strand DNA synthesis requires only the 5′ encapsidation signal and the 3′-proximal direct repeat DR1. J. Virol. 70:585-589.
41. Rosler, C., J. Kock, M. Kann, M. H. Malim, H. E. Blum, T. F. Baumert, and F. von Weizsacker. 2005. APOBEC-mediated interference with hepadnavirus production. Hepatology 42:301-309.
42. Seeger, C., and W. S. Mason. 2000. Hepatitis B virus biology. Microbiol. Mol. Biol. Rev. 64:51-68.
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. 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.
46. 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.
47. Summers, J., and W. S. Mason. 1982. Replication of the genome of a hepatitis B-like virus by reverse transcription of an RNA intermediate. Cell 29:403-415.
48. Suspene, R., D. Guetard, M. Henry, P. Sommer, S. Wain-Hobson, and J. P. Vartanian. 2005. Extensive editing of both hepatitis B virus DNA strands by APOBEC3 cytidine deaminases in vitro and in vivo. Proc. Natl. Acad. Sci. USA 102:8321-8326.
49. Suspene, 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.
50. 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.
51. Tanaka, Y., H. Marusawa, H. Seno, Y. Matsumoto, Y. Ueda, Y. Kodama, Y. Endo, J. Yamauchi, T. Matsumoto, A. Takaori-Kondo, I. Ikai, and T. Chiba. 2006. Anti-viral protein APOBEC3G is induced by interferon-alpha stimulation in human hepatocytes. Biochem. Biophys. Res. Commun. 341:314-319.
52. Turelli, P., B. Mangeat, S. Jost, S. Vianin, and D. Trono. 2004. Inhibition of hepatitis B virus replication by APOBEC3G. Science 303:1829.
53. Wang, G. H., and C. Seeger. 1993. Novel mechanism for reverse transcription in hepatitis B viruses. J. Virol. 67:6507-6512.
54. Wang, G. H., and C. Seeger. 1992. The reverse transcriptase of hepatitis B virus acts as a protein primer for viral DNA synthesis. Cell 71:663-670.
55. Wang, X., N. Grammatikakis, and J. Hu. 2002. Role of p50/CDC37 in hepadnavirus assembly and replication. J. Biol. Chem. 277:24361-24367.
56. Yu, M., and J. Summers. 1994. Multiple functions of capsid protein phosphorylation in duck hepatitis B virus replication. J. Virol. 68:4341-4348.
57. 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.
58. 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.
59. 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.