Rescue of multiple viral functions by a second-site suppressor of a human immunodeficiency virus type 1 nucleocapsid mutation

Journal of Virology

Volumn 74, Issue 9, 2000, Pages 4273-4283

  Cimarelli, Andrea ^a   Sandin, Sara ^b   Höglund, Stefan ^b   Luban, Jeremy ^a  

^a Columbia Univ Coll of Phys/Surgs ^*  (United States)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA; VIRUS RNA;

ARTICLE; DNA SYNTHESIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; PACKAGING; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VIRION; VIRUS GENOME; VIRUS ISOLATION; VIRUS MUTATION; VIRUS NUCLEOCAPSID; VIRUS REPLICATION;

AMINO ACID SEQUENCE; CELL LINE, TRANSFORMED; DNA, VIRAL; HELA CELLS; HIV-1; HUMANS; JURKAT CELLS; KINETICS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; NUCLEOCAPSID PROTEINS; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN CONFORMATION; RNA, VIRAL; TRANSCRIPTION, GENETIC; VIRION; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 0034003379     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.9.4273-4283.2000     Document Type: Article

References (72)

1. Allain, B., M. Lapadat-Tapolsky, C. Berlioz, and J. L. Darlix. 1994. Transactivation of the minus-strand DNA transfer by nucleocapsid protein during reverse transcription of the retroviral genome. EMBO J. 13:973-981.
2. Allain, B., J. B. Rascle, H. de Rocquigny, B. Roques, and J. L. Darlix. 1998. CIS elements and trans-acting factors required for minus strand DNA transfer during reverse transcription of the genomic RNA of murine leukemia virus. J. Mol. Biol. 277:225-235.
3. Ansari-Lari, M. A., L. A. Donehower, and R. A. Gibbs. 1995. Analysis of human immunodeficiency virus type 1 integrase mutants. Virology 213:680.
4. Bennett, R. P., T. D. Nelle, and J. W. Wills. 1993. Functional chimeras of the Rous sarcoma virus and human immunodeficiency virus Gag proteins. J. Virol. 67:6487-6498.
5. Berkowitz, R., J. Fisher, and S. P. Goff. 1996. RNA packaging. Curr. Top. Microbiol. Immunol. 214:177-218.
6. Berthoux, L., C. Pechoux, M. Ottmann, G. Morel, and J. L. Darlix. 1997. Mutations in the N-terminal domain of human immunodeficiency virus type 1 nucleocapsid protein affect virion core structure and proviral DNA synthesis. J. Virol. 71:6973-6981.
7. Bor, Y. C., F. D. Bushman, and L. E. Orgel. 1995. In vitro integration of human immunodeficiency virus type 1 cDNA into targets containing protein-induced bends. Proc. Natl. Acad. Sci. USA 92:10334-10338.
8. Borroto-Esoda, K., and L. R. Boone. 1991. Equine infectious anemia virus and human immunodeficiency virus DNA synthesis in vitro: characterization of the endogenous reverse transcriptase reaction. J. Virol. 65:1952-1959.
9. Braaten, D., E. K. Franke, and J. Luban. 1996. Cyclophilin A is required for an early step in the life cycle of human immunodeficiency virus type 1 prior to the initiation of reverse transcription. J. Virol. 70:3551-3560.
10. Brown, P. O., B. Bowerman, H. E. Varmus, and J. M. Bishop. 1987. Correct integration of retroviral DNA in vitro. Cell 49:347-356.
11. Burniston, M. T., A. Cimarelli, J. Colgan, S. P. Curtis, and J. Luban. 1999. Human immunodeficiency virus type 1 Gag polyprotein multimerization requires the nucleocapsid domain and RNA and is promoted by the capsiddimer interface and the basic region of matrix protein. J. Virol. 73:8527-8540.
12. Bushman, F. D., and R. Craigie. 1992. Integration of human immunodeficiency virus DNA: adduct interference analysis of required DNA sites. Proc. Natl. Acad. Sci. USA 89:3458-3462.
13. 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.
14. Carriere, C., B. Gay, N. Chazal, N. Morin, and P. Boulanger. 1995. Sequence requirements for encapsidation of deletion mutants and chimeras of human immunodeficiency virus type 1 Gag precursor into retrovirus-like particles. J. Virol. 69:2366-2377.
15. 2+-dependent DNA integration in vitro. J. Virol. 71:6225-6229.
16. Carteau, S., R. J. Gorelick, and F. D. Bushman. 1999. Coupled integration of human immunodeficiency virus type 1 cDNA ends by purified integrase in vitro: stimulation by the viral nucleocapsid protein. J. Virol. 73:6670-6679.
17. Cimarelli, A., and J. Luban. 1999. Translation elongation factor 1-alpha interacts specifically with the human immunodeficiency virus type 1 Gag polyprotein. J. Virol. 73:5388-5401.
18. Cimarelli, A., S. Sandin, S. Höglund, and J. Luban. 2000. Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA. J. Virol. 74:3046-3057.
19. Craigie, R., T. Fujiwara, and F. Bushman. 1990. The IN protein of Moloney murine leukemia virus processes the viral DNA ends and accomplishes their integration in vitro. Cell 62:829-837.
20. 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. 1. Mol. Biol. 254:523-537.
21. Dawson, L., and X. F. Yu. 1998. The role of nucleocapsid of HIV-1 in virus assembly. Virology 251:141-157.
22. De Guzman, R. N., Z. R. Wu, C. C. Stalling, L. Pappalardo, P. N. Borer, and M. F. Summers. 1998. Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science 279:384-388.
23. Dorfman, T., J. Luban, S. P. Goff, W. A. Haseltine, and H. G. Gottlinger. 1993. Mapping of functionally important residues of a cysteine-histidine box in the human immunodeficiency virus type 1 nucleocapsid protein. J. Virol. 67:6159-6169.
24. Ellis, J., and A. Bernstein. 1989. Retrovirus vectors containing an internal attachment site: evidence that circles are not intermediates to murine retrovirus integration. J. Virol. 63:2844-2846.
25. Engelman, A., G. Englund, J. M. Orenstein, M. A. Martin, and R. Craigie. 1995. Multiple effects of mutations in human immunodeficiency virus type 1 integrase on viral replication. J. Virol. 69:2729-2736.
26. Farnet, C. M., and F. D. Bushman. 1997. HIV-1 cDNA integration: requirement of HMG I(Y) protein for function of preintegration complexes in vitro. Cell 88:483-492.
27. Feng, Y. X., S. Campbell, D. Harvin, B. Ehresmann, C. Ehresmann, and A. Rein. 1999. The human immunodeficiency virus type I Gag polyprotein has nucleic acid chaperone activity: possible role in dimerization of genomic RNA and placement of tRNA on the primer binding site. J. Virol. 73:4251-4256.
28. 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.
29. Franke, E. K., H. E. H. Yuan, K. L. Bossolt, S. P. Goff, and J. Luban. 1994. Specificity and sequence requirements for interactions between various retroviral Gag proteins. J. Virol. 68:5300-5305.
30. Freed, E. O. 1998. HIV-1 gag proteins: diverse functions in the virus life cycle. Virology 251:1-15.
31. 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.
32. Fu, W., and A. Rein. 1993. Maturation of dimeric viral RNA of Moloney murine leukemia virus. J. Virol. 67:5443-5449.
33. Gallay, P., S. Swingler, J. Song, F. Bushman, and D. Trono. 1995. HIV nuclear import is governed by the phosphotyrosine-mediated binding of matrix to the core domain of integrase. Cell 83:569-576.
34. Ganser, B. K., S. Li, V. Y. Klishko, J. T. Finch, and W. I. Sundquist. 1999. Assembly and analysis of conical models for the HIV-1 core. Science 283: 80-83.
35. Gheysen, D., E. Jacobs, F. de Foresta, C. Thiriart, M. Francotte, D. Thines, and M. DeWilde. 1989. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells. Cell 59:103-112.
36. Goncalves, J., Y. Korin, J. Zack, and D. Gabuzda. 1996. Role of Vif in human immunodeficiency virus type 1 reverse transcription. J. Virol. 70: 8701-8709.
37. Gorelick, R. J., W. Fu, T. D. Gagliardi, W. J. Busche, A. Rein, L. E. Henderson, and L. O. Arthur. 1999. Characterization of the block in replication of nucleocapsid protein zinc finger mutants from Moloney murine leukemia virus. J. Virol. 73:8185-8195.
38. Gorelick, R. J., T. D. Gagliardi, W. J. Bosche, T. A. Wiltrout, L. V. Coren, D. J. Chabot, J. D. Lifson, L. E. Henderson, and L. O. Arthur. 1999. Strict conservation of the retroviral nucleocapsid protein zinc finger is strongly influenced by its role in viral infection processes: characterization of HIV-1 particles containing mutant nucleocapsid zinc-coordinating sequences. Virology 256:92-104.
39. Gross, I., H. Hohenberg, and H. G. Krausslich. 1997. In vitro assembly properties of purified bacterially expressed capsid proteins of human immunodeficiency virus. Eur. J. Biochem. 249:592-600.
40. 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.
41. Hirt, B. 1967. Selective extraction of polyomavirus DNA from infected mouse cell cultures. J. Mol. Biol. 26:365-369.
42. Housset, V., H. De Rocquigny, B. P. Roques, and J. L. Darlix. 1993. Basic amino acids flanking the zinc finger of Moloney murine leukemia virus nucleocapsid protein NCp10 are critical for virus infectivity. J. Virol. 67: 2537-2545.
43. Jowett, J. B., D. J. Hockley, M. V. Nermut, and I. M. Jones. 1992. Distinct signals in human immunodeficiency virus type 1 Pr55 necessary for RNA binding and particle formation. J. Gen. Virol. 73:3079-3086.
44. Katz, R. A., G. Merkel, J. Kulkosky, J. Leis, and A. M. Skalka. 1990. The avian retroviral IN protein is both necessary and sufficient for integrative recombination in vitro. Cell 63:87-95.
45. Kiernan, R. E., A. Ono, G. Englund, and E. O. Freed. 1998. Role of matrix in an early postentry step in the human immunodeficiency virus type 1 life cycle. J. Virol. 72:4116-4126.
46. Kimpton, J., and M. Emerman. 1992. Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated β-galactosidase gene. J. Virol. 66: 2232-2239.
47. Kostrikis, L. G., S. Tyagi, M. M. Mhlanga, D. D. Ho, and F. R. Kramer. 1998. Spectral genotyping of human alleles. Science 279:1228-1229.
48. Krausslich, H. G., and R. Welker. 1996. Intracellular transport of retroviral capsid components. Curr. Top. Microbiol. Immunol. 214:25-63.
49. Lapadat-Tapolsky, M., H. De Rocquigny, D. Van Gent, B. Roques, R. Plasterk, and J. L. Darlix. 1993. Interactions between HIV-1 nucleocapsid protein and viral DNA may have important functions in the viral life cycle. Nucleic Acids Res. 21:831-839.
50. Lener, D., V. Tanchou, B. P. Roques, S. F. Le Grice, and J. L. Darlix. 1998. Involvement of HIV-1 nucleocapsid protein in the recruitment of reverse transcriptase into nucleoprotein complexes formed in vitro. J. Biol. Chem. 273:33781-33786.
51. Lewin, S. R., M. Vesanen, L. Kostrikis, A. Hurley, M. Duran, L. Zhang, D. D. Ho, and M. Markowitz. 1999. Use of real-time PCR and molecular beacons to detect virus replication in human immunodeficiency virus type 1-infected individuals on prolonged effective antiretroviral therapy. J. Virol. 73:6099-6103.
52. Lobel, L. I., J. E. Murphy, and S. P. Goff. 1989. The palindromic LTR-LTR junction of Moloney murine leukemia virus is not an efficient substrate for proviral integration. J. Virol. 63:2629-2637.
53. Lys into human immunodeficiency virus type 1 particles. J. Virol. 68:2065-2072.
54. Mak, J., A. Khorchid, Q. Cao, Y. Huang, I. Lowy, M. A. Parniak. V. R. Prasad, M. A. Wainberg, and L. Kleiman. 1997. Effects of mutations in Pr160gag-pol upon tRNA(Lys3) and Pr160gag-pol incorporation into HIV-1. J. Mol. Biol. 265:419-431
55. McDermott, J., L. Farrell, R. Ross, and E. Barklis. 1996. Structural analysis of human immunodeficiency virus type 1 Gag protein interactions, using cysteine-specific reagents. J. Virol. 70:5106-5114.
56. Miller, M. D., C. M. Farnet, and F. D. Bushman. 1997. Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J. Virol. 71:5382-5390.
57. Muller, H. P., and H. E. Varmus. 1994. DNA bending creates favored sites for retroviral integration: an explanation for preferred insertion sites in nucleosomes. EMBO J. 13:4704-4714.
58. Myers, G., B. Korber, S. Wain-Hobson, K.-T. Jeang, L. E. Henderson, and G. N. Pavlakis. 1994. Human retroviruses and AIDS. Los Alamos National Laboratory, Los Alamos, N. Mex.
59. Ottmann, M., C. Gabus, and J. L. Darlix. 1995. The central globular domain of the nucleocapsid protein of human immunodeficiency virus type 1 is critical for virion structure and infectivity. J. Virol. 69:1778-1784.
60. Peliska, J. A., S. Balasubramanian, D. P. Giedroc, and S. J. Benkovc. 1994. Recombinant HIV-1 nucleocapsid protein accelerates HIV-1 reverse transcriptase catalyzed DNA strand transfer reactions and modulates RNase H activity. Biochemistry 33:13817-13823.
61. Poon, D. T., J. Wu, and A. Aldovini. 1996. Charged amino acid residues of human immunodeficiency virus type 1 nucleocapsid p7 protein involved in RNA packaging and infectivity. J. Virol. 70:6607-6616.
62. Pruss, D., F. D. Bushman, and A. P. Wolffe. 1994. Human immunodeficiency virus integrate directs integration to sites of severe DNA distortion within the nucleosome core. Proc. Natl. Acad. Sci. USA 91:5913-5917.
63. Rascle, J. B., D. Ficheux, and J. L. Darlix. 1998. Possible roles of nucleocapsid protein of MoMuLV in the specificity of proviral DNA synthesis and in the genetic variability of the virus. J. Mol. Biol. 280:215-225.
64. Rein, A. 1994. Retroviral RNA packaging: a review. Arch. Virol. Suppl. 9:513-522.
65. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
66. Shank, P. R., and H. E. Varmus. 1978. Virus-specific DNA in the cytoplasm of avian sarcoma virus-infected cells is a precursor to covalently closed circular viral DNA in the nucleus. J. Virol. 25:104-114.
67. Swanstrom, R., W. J. DeLorbe, J. M. Bishop, and H. E. Varmus. 1981. Nucleotide sequence of cloned unintegrated avian sarcoma virus DNA: viral DNA contains direct and inverted repeats similar to those in transposable elements. Proc. Natl. Acad. Sci. USA 78:124-128.
68. Tanchou, V., C. Gabus, V. Rogemond, and J. L. Darlix. 1995. Formation of stable and functional HIV-1 nucleoprotein complexes in vitro. J. Mol. Biol. 252:563-571.
69. 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.
70. Weiss, A., R. Wiskocil, and J. Stobo. 1984. The role of T3 surface molecules in the activation of human T cells: a two stimulus requirement for IL-2 production reflects events occurring at a pretranslational level. J. Immunol. 133:123-128.
71. Wiskerchen, M., and M. A. Muesing. 1995. Human immunodeficiency virus type 1 integrase: effects of mutations on viral ability to integrate, direct viral gene expression from unintegrated viral DNA templates, and sustain viral propagation in primary cells. J. Virol. 69:376-386.
72. You, J. C., and C. S. McHenry. 1994. Human immunodeficiency virus nucleocapsid protein accelerates strand transfer of the terminally redundant sequences involved in reverse transcription. J. Biol. Chem. 269:31491-31495.