The human immunodeficiency virus type 1 Gag polyprotein has nucleic acid chaperone activity: Possible role in dimerization of genomic RNA and placement of tRNA on the primer binding site

Journal of Virology

Volumn 73, Issue 5, 1999, Pages 4251-4256

  Feng, Ya Xiong ^a   Campbell, Stephen ^a   Harvin, Demetria ^a   Ehresmann, Bernard ^b   Ehresmann, Chantal ^b   Rein, Alan ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b INST DE BIOL MOLEC ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GAG PROTEIN; NUCLEIC ACID; RECOMBINANT PROTEIN; TRANSFER RNA; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; BINDING SITE; CATALYSIS; DIMERIZATION; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; RETROVIRUS; VIRUS ASSEMBLY; VIRUS GENOME; VIRUS PARTICLE;

EID: 0032928073     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.5.4251-4256.1999     Document Type: Article

References (36)

1. Adachi, A., H. E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M. A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
2. Aiyar, A., D. Cobrinik, Z. Ge, H. J. Kung, and J. Leis. 1992. Interaction between retroviral U5 RNA and the T psi C loop of the tRNA(Trp) primer is required for efficient initiation of reverse transcription. J. Virol. 66:2464-2472.
3. Allen, P., B. Collins, D. Brown, Z. Hostomsky, and L. Gold. 1996. A specific RNA structural motif mediates high affinity binding by the HIV-1 nucleo-capsid protein (NCp7). Virology 225:306-315.
4. Berglund, J. A., B. Charpentier, and M. Rosbash. 1997. A high affinity binding site for the HIV-1 nucleocapsid protein. Nucleic Acids Res. 25:1042-1049.
5. Berkowitz, R., J. Fisher, and S. P. Goff. 1996. RNA packaging. Curr. Top. Microbiol. Immunol. 214:177-218.
6. Busch, L. K. 1994. Production of HIV-1 (MN) nucleocapsid protein (p7) by recombinant DNA technology. M.S. thesis. Hood College, Frederick, Md.
7. Campbell, S., and A. Rein. 1999. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol. 73:2270-2279.
8. Campbell, S., and V. M. Vogt. 1997. In vitro assembly of virus-like particles with Rous sarcoma virus Gag deletion mutants: identification of the p10 domain as a morphological determinant in the formation of spherical particles. J. Virol. 71:4425-4435.
9. Canaani, E., K. V. Helm, and P. Duesberg. 1973. Evidence for 30-40S RNA as precursor of the 60-70S RNA of Rous sarcoma virus. Proc. Natl. Acad. Sci. USA 70:401-405.
10. Coffin, J. M., S. H. Hughes, and H. E. Varnius. 1997. Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
11. Crawford, S., and S. P. Goff. 1985. A deletion mutation in the 5′ part of the pol gene of Moloney murine leukemia virus blocks proteolytic processing of the gag and pol polyproteins. J. Virol. 53:899-907.
12. Darlix, J. L., M. Lapadat-Tapolsky, H. de Rocquigny, and B. P. Roques. 1995. First glimpses at structure-function relationships of the nucleocapsid protein of retroviruses. J. Mol. Biol. 254:523-537.
13. Feng, Y. X., T. D. Copeland, L. E. Henderson, R. J. Gorelick, W. J. Bosche, J. G. Levin, and A. Rein. 1996. HIV-1 nucleocapsid protein induces "maturation" of dimeric retroviral RNA in vitro. Proc. Natl. Acad. Sci. USA 93:7577-7581.
14. Feng, Y. X., W. Fu, A. J. Winter, J. G. Levin, and A. Rein. 1995. Multiple regions of Harvey sarcoma virus RNA can dimerize in vitro. J. Virol. 69: 2486-2490.
15. Fisher, R. J., A. Rein, M. Fivash, M. A. Urbaneja, J. R. Casas-Finet, M. Medaglia, and L. E. Henderson. 1998. Sequence-specific binding of human immunodeficiency virus type 1 nucleocapsid protein to short oligonucleotides. J. Virol. 72:1902-1909.
16. Fu, W., R. J. Gorelick, and A. Rein. 1994. Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and protease-defective virions. J. Virol. 68:5013-5018.
17. Fu, W., B. A. Ortiz-Conde, R. J. Gorelick, S. H. Hughes, and A. Rein. 1997. Placement of tRNA primer on the primer-binding site requires pol gene expression in avian but not murine retroviruses. J. Virol. 71:6940-6946.
18. Fu, W., and A. Rein. 1993. Maturation of dimeric viral RNA of Moloney murine leukemia virus. J. Virol. 67:5443-5449.
19. Gross, H. J., G. Krupp, H. Domdey, M. Raba, P. Jank, C. Lossow, H. Alberty, K. Ramm, and H. L. Sanger. 1982. Nucleotide sequence and secondary structure of citrus exocortis and chrysanthemum stunt viroid. Eur. J. Biochem. 121:249-257.
20. Guo, J., L. E. Henderson, J. Bess, B. Kane, and J. G. Levin. 1997. Human immunodeficiency virus type 1 nucleocapsid protein promotes efficient strand transfer and specific viral DNA synthesis by inhibiting TAR-dependent self-priming from minus-strand strong-stop DNA. J. Virol. 71:5178-5188.
21. Herschlag, D. 1995. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270:20871-20874.
22. Huang, Y., A. Khorchid, J. Gabor, J. Wang, X. Li, J. L. Darlix, M. A. Wainberg, and L. Kleiman. 1998. The role of nucleocapsid and U5 stem/A-rich loop sequences in tRNA(3Lys) genomic placement and initiation of reverse transcription in human immunodeficiency virus type 1. J. Virol. 72:3907-3915.
23. Huang, Y., J. Wang, A. Shalom, Z. Li, A. Khorchid, M. A. Wainberg, and L. Kleiman. 1997. Primer tRNA3Lys on the viral genome exists in unextended and two-base extended forms within mature human immunodeficiency virus type 1. J. Virol. 71:726-728.
24. Isel, C., C. Ehresmann, G. Keith, B. Ehresmann, and R. Marquet. 1995. Initiation of reverse transcription of HIV-1: secondary structure of the HIV-1 RNA/tRNA(3Lys) (template/primer). J. Mol. Biol. 247:236-250.
25. Isel, C., R. Marquet, G. Keith, C. Ehresmann, and B. Ehresmann. 1993. Modified nucleotides of tRNA(3Lys) modulate primer/template loop-loop interaction in the initiatior complex of HIV-1 reverse transcription. J. Biol. Chem. 268:25269-25272.
26. Keith, G. Personal communication.
27. Lapadat-Tapolsky, M., C. Gabus, M. Rau, and J. L. Darlix. 1997. Possible roles of HIV-1 nucleocarsid protein in the specificity of proviral DNA synthesis and in its variabi ity. J. Mol. Biol. 268:250-260.
28. Liang, C., X. Li, L. Rong, P. Inouye, Y. Quan, L. Kleiman, and M. A. Wainberg. 1997. The importance of the A-rich loop in human immunodeficiency virus type 1 reverse transcription and infectivity. J. Virol. 71:5750-5757.
29. Liang, C., L. Rong, N. Morin, E. Cherry, Y. Huang, L. Kleiman, and M. A. Wainberg. 1997. The roles of the human immunodeficiency virus type 1 Pol protein and the primer binding site in the placement of primer tRNA(3Lys) onto viral genomic RNA. J. Virol. 71:9075-9086.
30. Prats, A.-C., C. Roy, P. Wang, M. Erard, V. Housset, C. Gabus, C. Paoletti, and J.-L. Darlix. 1990. cis elements and trans-acting factors involved in dimer formation of murine leukemia virus RNA. J. Virol. 64:774-783.
31. Prats, A. C., L. Sarih, C. Gabus, S. Litvak, G. Keith, and J. L. Darlix. 1988. Small finger protein of av an and murine retroviruses has nucleic acid annealing activity and positions the replication primer tRNA onto genomic RNA. EMBO J. 7:1777-1783.
32. Rein, A., L. E. Henderson, and J. G. Levin. 1998. Nucleic acid chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem. Sci. 23:297-301.
33. Stewart, L., G. Schatz, and V. M. Vogt. 1990. Properties of avian retrovirus particles defective in viral protease. J. Virol. 64:5076-5092.
34. Stoltzfus, C. M., and P. N. Snyder. 1975. Structure of B77 sarcoma virus RNA: stabilization of RNA after packaging. J. Virol. 16:1161-1170.
35. Tsuchihashi, Z., and P. O. Brown. 1994. DNA strand exchange and selective DNA annealing promoted by the human immunodeficiency virus type 1 nucleocapsid protein. J. Virol. 68:5863-5870.
36. Wu, W., L. E. Henderson, T. D. Copeland, R. J. Gorelick, W. J. Bosche, A. Rein, and J. G. Levin. 1996. Human immunodeficiency virus type 1 nucleocapsid protein reduces reverse transcriptase pausing at a secondary structure near the murine leukemia virus polypurine tract. J. Virol. 70:7132-7142.