Reversion of a human immunodeficiency virus type 1 integrase mutant at a second site restores enzyme function and virus infectivity

Journal of Virology

Volumn 70, Issue 12, 1996, Pages 8277-8284

  Taddeo, Brunella ^a   Carlini, Francesca ^a   Verani, Paola ^a   Engelman, Alan ^b  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRASE;

AMINO ACID SUBSTITUTION; ARTICLE; CRYSTAL STRUCTURE; DNA STRAND; ENZYME ACTIVITY; GENETIC TRANSFECTION; GENOME; GENOTYPE; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVERTANT; SITE DIRECTED MUTAGENESIS; STRUCTURAL GENE; VIRION; VIRUS INFECTIVITY; VIRUS REPLICATION;

EID: 0029861757     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.12.8277-8284.1996     Document Type: Article

References (71)

1. Ansari-Lari, M. L., L. A. Donehower, and R. A. Gibbs. 1995 Analysis of human immunodeficiency virus type I inlegrase mutants. Virology 211:332-335.
2. Brown, P. O., B. Bowerman, H. E. Varmus, and J. M. Bishop. 1989. Retro-viral integration: structure of the initial covalent product and its precursor, and a role for the viral IN protein. Proc. Natl. Acad. Sci. USA 86:2525-2529.
3. Bujacz, G., M. Jaskolski, J. Alexandratos, A. Wlodower, G. Merkel, R. A. Katz, and A. M. Skalka. 1995. High-resolution structure of the catalytic domain of avian sarcoma virus integrase. J. Mol. Biol. 253:336-346.
4. 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.
5. Bushman, F. D., A. Engelman, I. Palmer, P. Wingfteld, and R. Craigie. 1993. Domains of the integrase protein of human immunodeficiency virus type 1 responsible for polynucleotidyl transfer and zinc binding. Proc. Natl. Acad. Sci. USA 90:3428-3432.
6. Cannon, P. M., W. Wilson, E. Byles, S. M. Kingsman, and A. J. Kingsman. 1994. Human immunodeficiency virus type 1 integrase: effect on viral replication of mutations at highly conserved residues. J. Virol. 68:4768-4775.
7. Carlini, F., and B. Taddeo. Unpublished observation.
8. Chow, S. A., and P. O. Brown. 1994. Juxtaposition of two viral ends in a bimolecular disintegration reaction mediated by multimers of human immunodeficiency virus type I or murine leukemia virus integrase. J. Virol. 68: 7869-7878.
9. Chow, S. A., K. A. Vincent, V. Ellison, and P. O. Brown. 1992. Reversal of integration and DNA splicing mediated by integrase of human immunodeficiency virus. Science 255:723-726.
10. Colicelli, J., and S. P. Goff. 1988. Sequence and spacing requirements of a retrovirus integration site. J. Mol. Biol. 199:47-59.
11. 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.
12. Craigie, R., A. B. Hickman, and A. Engelman. 1995. Integrase, p. 53-71. In J. Karn (ed.), HIV, vol. II. A practical approach. Oxford University Press, Oxford.
13. Dayton, A. I., E. F. Terwilliger, J. Potz, M. Kowalski, J. G. Sodroski, and W. A. Haseltine. 1988. cis-acting sequences responsive to the rev gene product of the human immunodeficiency virus. J. Acquired Immune Defic. Syndr. 1:441-452.
14. Donehower, L. A., and H. E. Varmus. 1984. A mutant murine leukemia virus with a single missense codon in pol is defective in a function affecting integration. Proc. Natl. Acad. Sci. USA 81:6461-6465.
15. Drelich, M., M. Haenggi, and J. Mous. 1993. Conserved residues Pro-109 and Asp-116 are required for interaction of the human immunodeficiency virus type 1 integrase protein with its viral DNA substrate. J. Virol. 67:5041-5044.
16. Drelich, M., R. Wilhelm, and J. Mous. 1992. Identification of amino acid residues critical for endonuclease and integration activities of HIV-1 IN protein in vitro. Virology 188:459-468.
17. Dyda, F., A. B. Hickman, T. M. Jenkins, A. Engelman, R. Craigie, and D. R. Davies. 1994. Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266:1981-1986.
18. Eijkelenboom, A. P. A. M., R. A. P. Lutzke, R. Boelens, R. H. A. Plasterk, R. Kaptein, and K. Hard. 1995. The DNA binding domain of HIV-1 integrase has an SH3-like fold. Nature (London) Struct. Biol. 2:807-810.
19. Engelman, A., F. D. Bushman, and R. Craigie. 1993. Identification of discrete functional domains of HIV-1 integrase and their organization within an active multimeric complex. EMBO J. 12:3269-3275.
20. Engelman, A., and R. Craigie. 1992. Identification of conserved amino acid residues critical for human immunodeficiency virus type 1 integrase function in vitro. J. Virol. 66:6361-6369.
21. Engelman, A., and R. Craigie. 1995. Efficient magnesium-dependent human immunodeficiency virus type 1 integrase activity. J. Virol. 69:5908-5911.
22. 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.
23. Engelman, A., A. B. Hickman, and R. Craigie. 1994. The core and carboxyl terminal domains of the integrase protein of human immunodeficiency virus type I each contribute to nonspecific DNA binding. J. Virol. 68:5911-5917.
24. Englund, G., T. S. Theodore, E. Freed, A. Engelman, and M. A. Martin. 1995. Integration is required for productive infection of monocyte-derived macrophages by human immunodeficiency virus type 1. J. Virol. 69:3216-3219.
25. Fujiwara, T., and K. Mizuuchi. 1988. Retroviral DNA integration: structure of an integration intermediate. Cell 54:497-504.
26. Goulaouic, H., and S. A. Chow. 1996. Directed integration of viral DNA mediated by fusion proteins consisting of human immunodeficiency virus type 1 integrase and Escherichia coil LexA protein. J. Virol. 70:37-46.
27. Grandgenett, D. P., and G. Goodarzi. 1994. Folding of the multidomain human immunodeficiency virus type 1 integrase. Protein Sci. 3:888-897.
28. Hazuda, D. J., A. L. Wolfe, J. C. Hastings, H. L. Robbins. P. L. Graham, R. L. LaFemina, and E. A. Emini. 1994. Viral long terminal repeat substrate binding characteristics of human immunodeficiency virus type 1 integrase. J. Biol. Chem. 269:3999-4004.
29. Higuchi, R., B. Krummel, and R. K. Saiki. 1988. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 16:7351-7367.
30. 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 C-terminal domains in multimerization. J. Biol. Chem. 271:7712-7718.
31. Jenkins, T. M., A. B. Hickman, F. Dyda, R. Ghirlando, D. R. Davies, and R. Craigie. 1995. Catalytic domain of human immunodeficiency virus type 1 integrase: identification of a soluble mutant by systematic replacement of hydrophobic residues. Proc. Natl. Acad. Sci. USA 92:6057-6061.
32. Johnson, M. S., M. A. McClure, D.-F. Feng, J. Gray, and R. F. Doolittle. 1986. Computer analysis of retroviral pol genes: assignment of enzymatic functions to specific sequences and homologies with non viral enzymes. Proc. Nail. Acad. Sci. USA 83:7648-7652.
33. Kalpana, G. V., and S. P. Goff. 1993. Genetic analysis of homomeric interactions of human immunodeficiency virus type 1 integrase using the yeast two-hybrid system. Proc. Natl. Acad. Sci. USA 90:10593-10597.
34. 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.
35. Katz, R. A., and A. M. Skalka. 1994. The retroviral enzymes. Annu. Rev. Biochem. 63:133-173.
36. Katzman, M., R. A. Katz, A. M. Skalka, and J. Leis. 1989. The avian retroviral integration protein cleaves the terminal sequences of linear viral DNA at the in vivo sites of integration. J. Virol. 63:5319-5327.
37. Khan, E., J. P. G. Mack, R. A. Katz, J. Kulkosky, and A. M. Skalka. 1991. Retroviral integrase domains: DNA binding and the recognition of LTR sequences. Nucleic Acids Res. 19:851-860.
38. Kraulis, P. J. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24:946-950.
39. Kulkosky, J., K. S. Jones, R. A. Katz, J. P. G. Mack, and A. M. Skalka. 1992. Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposascs. Mol. Cell. Biol. 12:2331-2338.
40. LaFemina, R. L., C. L. Schneider, H. L. Robbins, P. L. Callahan, K. LeGrow, E. Roth, W. A. Schleif, and E. A. Emini. 1992. Requirement of active human immunodeficiency virus type 1 integrase enzyme for productive infection of human T-lymphoid cells. J. Virol. 66:7414-7419.
41. Leavitt, A. D., G. Robles, N. Alesandro, and H. E. Varmus. 1996. Human immunodeficiency virus type 1 integrase mutants retain in vitro integrase activity yet fail to integrate DNA efficiently during infection. J. Virol. 70: 721-728.
42. Leavitt, A. D., L. Shiue, and H. E. Varmus. 1993. Site-directed mutagenesis of HIV-1 integrase demonstrates differential effects on integrase function in vitro. J. Biol. Chem. 268:2113-2119.
43. Lodi, P. J., J. A. Ernst, J. Kuszewski, A. B. Hickman, A. Engelman, R. Craigie, G. M. Clore, and A. M. Gronenborn. 1995. Solution structure of the DNA binding domain of HIV-1 integrase. Biochemistry 34:9826-9833.
44. Masuda, T., V. Planelles, P. Krogstad, and I. S. Y. Chen. 1995. Genetic analysis of human immunodeficiency virus type 1 integrase and the U3 att site: unusual phenotype of mutants in the zinc finger-like domain. J. Virol. 69:6687-6696.
45. Mazumder, A., A. Engelman, R. Craigie, M. Fresen, and Y. Pommier. 1994. Intermolecular disintegration and intramolecular strand transfer activities of wild-type and mutant HIV-1 integrase. Nucleic Acids Res. 22:1037-1043.
46. Meyers, G., S. Wain-Hobson, B. Korber, R. F. Smith, and G. N. Pavlakis. 1993. Human retroviruses and AIDS. A compilation and analysis of nucleic acid and amino acid sequences. Theoretical biology and biophysics group T-10. Los Alamos National Laboratory, Los Alamos. N.Mex.
47. Murphy, J. E., and S. P. Goff. 1992. A mutation at one end of Moloney murine leukemia virus DNA blocks cleavage at both ends by the viral integrase in vivo. J. Virol. 66:5092-5095.
48. Nakamoto, R. K., M. K. Alshawi, and M. Futai. 1995. The ATP synthetase gamma subunit-suppressor mutagenesis reveals three helical regions involved in energy coupling. J. Biol. Chem. 270:14042-140146.
49. Panganiban, A. T., and H. M. Temin. 1983. The terminal nucleotides of retroviral DNA are required for integration hut not virus production. Nature (London) 306:155-160.
50. Panganiban, A. T., and H. M. Temin. 1984. The retrovirus pol gene encodes a product required for DNA integration: identification of a retrovirus int locus. Proc. Natl. Acad. Sci. USA 81:7885-7889.
51. Puras-Lutzke, R. A., C. Vink, and R. H. A. Plasterk. 1994. Characterization of the minimal DNA-hinding domain of the HIV integrase protein. Nucleic Acids Res. 22:4125-4131.
52. Quinn, T. P., and D. P. Grandgenett. 1988. Genetic evidence that the avian retrovirus DNA endonuclease domain of Pol is necessary for viral integration. J. Virol. 62:2307-2312.
53. Rice, P. A., and K. Mizuuchi. 1995. Structure of the bacteriophage Mu transposase core: a common structural motif for DNA transposition and retroviral integration. Cell 82:209-220.
54. Roth, M. J., P. L. Schwartzberg, and S. P. Goff. 1989. Structure of the termini of DNA intermediates in the integration of retroviral DNA: dependence on IN function and terminal DNA sequence. Cell 58:47-54.
55. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
56. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
57. Schwartzberg, P., J. Colicelli, and S. P. Goff. 1984. Construction and analysis of deletion mutants in the pol gene of Moloney murine leukemia virus: a new viral function required for productive infection. Cell 37:1043-1052.
58. 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.
59. Shin, C., B. Taddeo, W. A. Haseltine, and C. M. Farnet. 1994. Genetic analysis of the human immunodeficiency virus type 1 integrase protein. J. Virol. 68:1633-1642.
60. Studier, F. W., and B. A. Moffatt. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130.
61. Taddeo, B., W. A. Haseltine, and C. M. Farnet. 1994. Integrase mutants of human immunodeficiency virus type 1 with a specific defect in integration. J. Virol. 68:8401-8405.
62. van Dyke, M. W., M. Sirilo, and M. Sawadogo. 1992. Single-step purification of bacterially expressed polypeptides containing an oligo-histidine domain. Gene 111:99-104.
63. van Gent, D. C., Y. Elgersma, M. W. J. Bolk, C. Vink, and R. H. A. Plasterk. 1991. DNA binding of the integrase proteins of human immunodeficiency viruses types 1 and 2. Nucleic Acids Res. 19:3821-3827.
64. van Gent, D. C., A. A. M. Oude Groeneger, and R. H. A. Plasterk. 1992. Mutational analysis of the integrase protein of human immunodeficiency virus type 2. Proc. Natl. Acad. Sci. USA 89:9598-9602.
65. van Gent, D. C., C. Vink, A. A. M. Oude Groeneger, and R. H. A. Plasterk. 1993. Complementation between HIV integrase proteins mutated in different domains. EMBO J. 12:3261-3267.
66. Vincent, K. A., V. Ellison, S. A. Chow, and P. O. Brown. 1993. Characterization of human immunodeficiency virus type 1 integrase expressed in Escherichia coli and analysis of variants with amino-terminal mutations. J. Virol. 67:425-437.
67. Vink, C., A. A. M. Oude Groeneger, and R. H. A. Plasterk. 1993. Identification of the catalytic and DNA-binding region of human immunodeficiency virus type 1 integrase protein. Nucleic Acids Res. 21:1419-1425.
68. Vora, A. C., M. L. Fitzgerald, and D. P. Grandgenett. 1990. Removal of 3́-OH-terminal nucleotides from blunt-ended long terminal repeat termini by the avian retrovirus integration protein. J. Virol. 64:5656-5659.
69. Wiskerchen, M., and M. A. Muesing. 1995. Human immunodeficiency virus type 1 integrase: effects of mutations on viral ability to integrate, direct gene expression from unintegrated viral DNA templates, and sustain propagation in primary cells. J. Virol. 69:376-386.
70. Woerner, A. M., M. Klutch, J. G. Levin, and C. J. Marcus-Sekura. 1992. Localization of DNA binding activity of HIV-1 integrase to the C-terminal half of the protein. AIDS Res. Hum. Retroviruses 8:297-304.
71. Yamaguchi, A., Y. Inagaki, and T. Sawai. 1995. Second site suppressor mutations for the Asp-66→Cys mutant of the transposon Tn10-encoded metal-tetracycline/H+ antiporter of Escherichia coli. Biochemistry 34:11800-11806.