Coupled integration of human immunodeficiency virus type 1 cDNA ends by purifed integrase in vitro: Stimulation by the viral nucleocapsid protein

Journal of Virology

Volumn 73, Issue 8, 1999, Pages 6670-6679

  Carteau, Sandrine ^a   Gorelick, Robert J ^b   Bushman, Frederic D ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; INTEGRASE; NUCLEOCAPSID PROTEIN; VIRUS DNA;

ARTICLE; DNA INTEGRATION; DNA SEQUENCE; ENZYME ACTIVITY; GENETIC RECOMBINATION; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; VIRUS REPLICATION;

EID: 0032776165     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.8.6670-6679.1999     Document Type: Article

References (61)

1. Alyar, A., P. Hindmarsh, A. M. Skalka, and J. Leis. 1996. Concerted integration of linear retroviral DNA by the avian sarcoma virus integrase in vitro: dependence on both long terminal repeat termini. J. Virol. 70:3571-3580.
2. Allen, P., S. Worland, and L. Gold. 1995. Isolation of high-affinity RNA ligands to HIV-1 integrase from a random pool. Virology 209:327-336.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1987. Current protocols in molecular biology. John Wiley and Sons, Inc., New York, N.Y.
4. Bess, J. W., P. J. Powell, H. J. Issaq, L. J. Schumack, M. K. Grimes, L. E. Henderson, and L. O. Arthur. 1992. Tightly bound zinc in human immunodeficiency virus type 1, human T-cell leukemia virus type I, and other retroviruses. J. Virol. 66:840-847.
5. Bor, Y.-C., F. Bushman, and L. 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.
6. Brown, P. O., B. Bowerman, H. E. Varmus, and J. M. Bishop. 1987. Correct integration of retroviral DNA in vitro. Cell 49:347-356.
7. Bukrinsky, M. I., N. Sharova, T. L. McDonald, T. Pushkarskaya, G. W. Tarpley, and M. Stevenson. 1993. Association of integrase, matrix, and reverse transcriptase antigens of human immunodeficiency virus type 1 with viral nucleic acids following acute infection. Proc. Natl. Acad. Sci. USA 90:6125-6129.
8. Burke, C. J., G. Sanyal, M. W. Bruner, J. A. Ryan, R. L. LaFemina, H. L. Robbins, A. S. Zeft, C. R. Middaugh, and M. G. Cordingley. 1992. Structural implications of spectroscopic characterization of a putative zinc finger peptide from HIV-1 integrase. J. Biol. Chem. 267:9639-9644.
9. Bushman, F. D., and R. Craigie. 1990. Sequence requirements for integration of Moloney murine leukemia virus DNA in vitro. J. Virol. 64:5645-5648.
10. Bushman, F. D., and R. Craigie. 1991. Activities of human immunodeficiency virus (HIV) integration protein in vitro: specific cleavage and integration of HIV DNA. Proc. Natl. Acad. Sci. USA 88:1339-1343.
11. 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.
12. Bushman, F. D., T. Fujiwara, and R. Craigie. 1990. Retroviral DNA integration directed by HIV integration protein in vitro. Science 249:1555-1558.
13. Camaur, D., and D. Trono. 1996. Characterization of human immunodeficiency virus type 1 Vif particle incorporation. J. Virol. 70:6106-6111.
14. 2+-dependent DNA integration in vitro. J. Virol. 71:6225-6229.
15. Chen, H., and A. Engelman. 1998. The barrier-to-autointegration protein is a host factor for HIV type 1 integration. Proc. Natl. Acad. Sci. USA 95: 15270-15274.
16. Coffin, J. M., S. H. Hughes, and H. E. Varmus. 1997. Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
17. Colicelli, J., and S. P. Goff. 1985. Mutants and pseudorevertants of Moloney murine leukemia virus with alterations at the integration site. Cell 42:573-580.
18. Colicelli, J., and S. P. Goff. 1988. Sequence and spacing requirements of a retrovirus integration site. J. Mol. Biol. 199:47-59.
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. Ellison, V. H., H. Abrams, T. Roe, J. Lifson, and P. O. Brown. 1990. Human immunodeficiency virus integration in a cell-free system. J. Virol. 64:2711-2715.
21. Farnet, C., and F. D. Bushman. 1997. HIV-1 cDNA integration: requirement of HMG I(Y) protein for function of preintegration complexes in vitro. Cell 88:1-20.
22. Farnet, C. M., and W. A. Haseltine. 1990. Integration of human immunodeficiency virus type 1 DNA in vitro. Proc. Natl. Acad. Sci. USA 87:4164-4168.
23. Farnet, C. M., and W. A. Haseltine. 1991. Determination of viral proteins present in the human immunodeficiency virus type 1 preintegration complex. J. Virol. 65:1910-1915.
24. 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.
25. Fitzgerald, M. L., A. C. Vora, W. G. Zeh, and D. P. Grandgenett. 1992. Concerted integration of viral DNA termini by purified avian myeloblastosis virus integrase. J. Virol. 66:6257-6263.
26. Gallay, P., T. Hope, D. Chin, and D. Trono. 1997. HIV-1 infection of nondividing cells through the recognition of integrase by the importin/karyopherin pathway. Proc. Natl. Acad. Sci. USA 94:9825-9830.
27. 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 17:569-576.
28. Goodarzi, G., R. Chiu, K. Brackmann, K. Kohn, Y. Pommler, and D. P. Grandgenett. 1997. Host site selection for concerted integration by human immunodeficiency virus type-1 virions in vitro. Virology 231:210-217.
29. Goodarzi, G., G.-J. Im, K. Brackmann, and D. Grandgenett. 1995. Concerted integration of retrovirus-like DNA by human immunodeficiency virus type 1 integrase. J. Virol. 69:6090-6097.
30. Gorelick, R. J., D. J. Chabot, A. Rein, L. E. Henderson, and L. O. Arthur. 1993. The two zinc fingers in the human immunodeficiency virus type 1 nucleocapsid protein are not functionally equivalent. J. Virol. 67:4027-4036.
31. 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. Strict conservation of the retroviral nucleocapsid (NC) protein zinc-finger is strongly influenced by its role in viral infection processes: characterization of HIV-1 particles containing mutant NC zinc-coordinating sequences. Virology 256:92-104.
32. Hansen, M., and F. D. Bushman. 1997. HIV-2 preintegration complexes: activities in vitro and response to inhibitors. J. Virol. 71:3351-3356.
33. Hansen, M. S. T., S. Carteau, C. Hoffmann, L. Li, and F. Bushman. 1998. Retroviral cDNA integration: mechanism, applications and inhibition, p. 41-62. In J. K. Setlow (ed.), Genetic engineering: principles and methods. Plenum Press, New York, N.Y.
34. Hendersen, L. E., M. A. Bowers, R. C. Sowder, S. A. Serabyn, D. G. Johnson, J. W. Bess, L. O. Arthur, D. K. Bryant, and C. Fenselau. 1992. Gag proteins of the highly replicative MN strain of human immunodeficiency virus type 1: posttranslational modifications, proteolytic processings, and complete amino acid sequences. J. Virol. 66:1856-1865.
35. Mne). J. Virol. 62:2587-2595.
36. Henderson, L. E., R. Sowder, T. D. Copeland, G. Smythers, and S. Oroszlan. 1984. Quantitative separation of murine leukemia virus proteins by reversed-phase high-pressure liquid chromatography reveals newly described gag and env cleavage products. J. Virol. 52:492-500.
37. Jenkins, T. M., A. Engelman, R. Ghirlando, and R. Craigie. 1996. A soluble active mutant of HIV-1 integrase: involvement of both the core and carboxyl-terminal domains in multimerization. J. Biol. Chem. 271:7712-7718.
38. Kalpana, G. V., S. Marmon, W. Wang, G. R. Crabtree, and S. P. Goff. 1994. Binding and stimulation of HIV-1 integrase by a human homolog of yeast transcription factor SNF5. Science 266:2002-2006.
39. Katz, R. A., K. Gravuer, and A. M. Skalka. 1998. A preferred target DNA structure for retroviral integrase in vitro. J. Biol. Chem. 273:24190-24195.
40. 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.
41. 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.
42. Lee, M. S., and R. Craigie. 1998. A previously unidentified host protein protects retroviral DNA from autointegration. Proc. Natl. Acad. Sci. USA 95:1528-1533.
43. Li, L., C. M. Farnet, W. F. Anderson, and F. D. Bushman. 1998. Modulation of activity of Moloney murine leukemia virus preintegration complexes by several host factors in vitro. J. Virol. 72:2125-2131.
44. Miller, M., Y.-C. Bor, and F. D. Bushman. 1995. Target DNA capture by HIV-1 integration complexes. Curr. Biol. 5:1047-1056.
45. 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.
46. 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.
47. Murphy, J. E., and S. P. Goff. 1992. A mutation at one end of Moloney murine leukemia virus DNA blocks cleavage of both ends by the viral integrase in vivo. J. Virol. 66:5092-5095.
48. Myrik, K., and C. Farnet. Unpublished data.
49. Patel, P. H., and B. D. Preston. 1994. Marked infidelity of human immunodeficiency virus type 1 reverse transcriptase at RNA and DNA template ends. Proc. Natl. Acad. Sci. USA 91:549-553.
50. Pruss, D., F. D. Bushman, and A. P. Wolffe. 1994. Human immunodeficiency virus integrase directs integration to sites of severe DNA distortion within the nucleosome core. Proc. Natl. Acad. Sci. USA 91:5913-5917.
51. 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.
52. Scottoline, B. P., S. Chow, V. Ellison, and P. O. Brown. 1997. Disruption of the terminal base pairs of retroviral DNA during integration. Genes Dev. 11:371-382.
53. Sherman, P. A., and J. A. Fyfe. 1990. Human immunodeficiency virus integration protein expressed in Escherichia coli possesses selective DNA cleaving activity. Proc. Natl. Acad. Sci. USA 87:5119-5123.
54. Swingler, S., P. Gallay, D. Camaur, J. Song, A. Abo, and D. Trono. 1997. The Nef protein of human immunodeficiency virus type 1 enhances serine phosphorylation of the viral matrix. J. Virol. 71:4372-4377.
55. Tanchou, V., D. Decimo, C. Pechoux, D. Lener, V. Rogemond, L. Berthoux, M. Ottmann, and J.-L. Darlix. 1998. Role of the N-terminal zinc finger of human immunodeficiency virus type 1 nucleocapsid protein in virus structure and replication. J. Virol. 72:4442-4447.
56. 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.
57. Vora, A. C., R. Chin, M. McCord, G. Goodarzi, S. J. Stahl, T. C. Mueser, C. C. Hyde, and D. P. Grandgenett. 1997. Avian retrovirus U3 and U5 DNA inverted repeats. Role of nonsymmetrical nucleotides in promoting full-site integration by purified virion and bacterial recombinant integrases. J. Biol. Chem. 272:23938-23945.
58. Vora, A. C., and D. P. Grandgenett. 1995. Assembly and catalytic properties of retrovirus integrase-DNA complexes capable of efficiently performing concerted integration. J. Virol. 69:7483-7488.
59. Wei, S.-Q., K. Mizuuchi, and R. Craigie. 1998. Footprints of the viral DNA ends in Moloney murine leukemia virus preintegration complexes reflect a specific association with integrase. Proc. Natl. Acad. Sci. USA 95:10535-10540.
60. 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. 70:132-142.
61. Zheng, R., T. M. Jenkins, and R. Craigie. 1996. Zinc folds the N-terminal domain of HIV-1 integrase, promotes multimerization, and enhances catalytic activity. Proc. Natl. Acad. Sci. USA 93:13659-13664.