Complementation of integrase function in HIV-1 virions

EMBO Journal

Volumn 16, Issue 16, 1997, Pages 5123-5138

  Fletcher III, Thomas M ^a   Soares, Marcelo A ^a   McPhearson, Silvia ^b   Hui, Huxiong ^a   Wiskerchen, MaryAnn ^c   Muesing, Mark A ^d   Shaw, George M ^a,b   Leavitt, Andrew D ^e   Boeke, Jef D ^f   Hahn, Beatrice H ^a,b  

^a Center for Palliative Care   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c PROMEGA CORPORATION   (United States)

^d AARON DIAMOND AIDS RESEARCH CENTER   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Functional IN subdomains; HIV 1 integrase; IN multimerization; trans complementation; Vpr

Indexed keywords

ANTIVIRUS AGENT; GAG PROTEIN; HYBRID PROTEIN; INTEGRASE; POL PROTEIN; PROTEINASE; SYNTHETIC DNA; VIRUS DNA; VPR PROTEIN; ZINC FINGER PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DRUG DESIGN; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; VIRION; VIRUS ASSEMBLY; VIRUS DNA CELL DNA INTERACTION; VIRUS INFECTION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; BLOTTING, WESTERN; CELL LINE; GENE PRODUCTS, VPR; GENETIC COMPLEMENTATION TEST; HIV INTEGRASE; HIV PROTEASE; HIV-1; MOLECULAR SEQUENCE DATA; MUTATION; RECOMBINANT FUSION PROTEINS; RETROVIRIDAE PROTEINS; RNA-DIRECTED DNA POLYMERASE; TRANSFECTION; VIRUS ASSEMBLY; VIRUS INTEGRATION; ZINC FINGERS;

DNA VIRUSES; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0030792182     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.16.5123     Document Type: Article

References (78)

1. Bowerman, B., Brown, P.O., Bishop, J.M. and Varmus, H.E. (1989) A nucleoprotein complex mediates the integration of retroviral DNA. Genes Dev., 3, 469-478.
2. Bukovsky, A. and Göttlinger, H. (1996) Lack of integrase can markedly affect human immunodeficiency virus type 1 particle production in the presence of an active viral protease. J. Virol., 70, 6820-6825.
3. Bukrinskaya, A.G., Ghorpade, A., Heinzinger, N.K., Smithgall, T.E., Lewis, R.E. and Stevenson, M. (1996) Phosphorylation-dependent human immunodeficiency virus type 1 infection and nuclear targeting of viral DNA. Proc. Natl Acad. Sci. USA, 93, 367-371.
4. Bukrinsky, M.I., Haggerty, S., Dempsey, M.P., Sharova, N., Adzhubei, A., Spitz, L., Lewis, P., Goldfarb, D., Emerman, M. and Stevenson, M. (1993a) A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature, 365, 666-669.
5. Bukrinsky, M.I., Sharova, N., McDonald, T.L., Pushkarskaya, T., Tarpley, W.G. and Stevenson, M. (1993b) 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.
6. Burke, C. J., Sanyal, G., Bruner, M.W., Ryan, J.A., LaFemina, R.L., Robbins, H.L., Zeft, A.S., Middaugh, C.R. and Cordingley, M.G. (1992) Structural implications of spectroscopic characterization of a putative zinc-finger peptide from HIV-1 integrase. J. Biol. Chem., 267, 9639-9644.
7. Bushman, F.D. (1994) Tethering human immunodeficiency virus 1 integrase to a DNA site directs integration to nearby sequences. Proc. Natl Acad. Sci. USA, 91, 9233-9237.
8. Bushman, F.D. (1995) Targeting retroviral integration. Science, 267, 1443-1444.
9. Bushman, F.D. and Craigie, R. (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.
10. Bushman, F.D., Fujiwara, T. and Craigie, R. (1990) Retroviral DNA integration directed by HIV integration protein in vitro. Science, 249, 1555-1558.
11. Bushman, F.D., Engelman, A., Palmer, I., Wingfield, P. and Craigie, R. (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.
12. Cannon, P.M., Wilson, W., Byles, E., Kingsman, S.M. and Kingsman, A.J. (1994) Human immunodeficiency virus type 1 integrase: effect on viral replication of mutations at highly conserved residues. J. Virol., 68, 4768-4775.
13. Cannon, P.M., Byles, E.D., Kingsman, S.M. and Kingsman, A.J. (1996) Conserved sequences in the carboxyl terminus of integrase that are essential for human immunodeficiency virus type 1 replication. J. Virol., 70, 651-657.
14. Chow, S.A., Vincent, K.A., Ellison, V. and Brown, P.O. (1992) Reversal of integration and DNA splicing mediated by integrase of human immunodeficiency virus. Science, 255, 723-726.
15. Corbeau, P., Kraus, G. and Wong-Staal, F. (1996) Efficient gene transfer by a human immunodeficiency virus type 1 (HIV-1) derived vector utilizing a stable HIV packaging cell line. Proc. Natl Acad. Sci. USA, 93, 14070-14075.
16. Doak, T.G., Doerder, F.P., Jahn, C.L. and Herrick, G. (1994) A proposed super-family of transposase genes: transposon-like elements in ciliated protozoa and a common 'D35E' motif. Proc. Natl Acad. Sci. USA, 91, 942-946.
17. Drelich, M., Wilheim, R. and Mous, J. (1992) Identification of amino acid residues critical for endonuclease and integration activities of HIV-1 IN protein in vitro. Virology, 188, 459-468.
18. Ellison, V. and Brown, P.O. (1994) A stable complex between integrase and viral DNA ends mediates human immunodeficiency virus integration in vitro. Proc. Natl Acad. Sci. USA, 91, 7316-7320.
19. Ellison, V., Gerton, J., Vincent, K.A. and Brown, P.O. (1995) An essential interaction between distinct domains of HIV-1 integrase mediates assembly of the active multimer. J. Biol. Chem., 270, 3320-3326.
20. Emerman, M. (1996) HIV-1, Vpr and the cell cycle. Curr. Biol., 6, 1096-1103.
21. Engelman, A. and Craigie, R. (1992) Identification of conserved amino acid residues critical for human immunodeficiency virus type 1 integrase function in vitro. J. Virol., 66, 6361-6369.
22. Engelman, A., Mizuuchi, K. and Craigie, R. (1991) HIV-1 DNA integration: mechanism of viral DNA cleavage and DNA strand transfer. Cell, 67, 1211-1221.
23. Engelman, A., Bushman, F.D. and Craigie, R. (1993) Identification of discrete functional domains of HIV-1 integrase and their organization within an active multimeric complex. EMBO J., 12, 3269-3275.
24. Engelman, A., Hickman, A.B. and Craigie, R. (1994) The core and carboxyl-terminal domains of the integrase protein of human immunodeficiency virus type 1 each contribute to nonspecific DNA binding. J. Virol., 68, 5911-5917.
25. Engelman, A., Englund, G., Orenstein, J.M., Martin, M.A. and Craigie, R. (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 Bushman, F.D. (1996) HIV cDNA integration: molecular biology and inhibitor development. AIDS, 10, S3-S11.
27. Farnet, C.M. and Bushman, F.D. (1997) HIV-1 cDNA integration: requirement of HMG I(Y) protein for function of preintegration complexes in vitro. Cell, 88, 483-492.
28. Feinberg, M.B., Baltimore, D. and Frankel, A.D. (1991) The role of Tat in the HIV life cycle indicates a primary effect on transcriptional elongation. Proc. Natl Acad. Sci. USA, 88, 4045-4050.
29. Fletcher, T.M., III, Wu, X., Liu, S., McPherson, S., Shaw, G.M., Boeke, J.D., Muesing, M.A., Kappes, J.C., Stevenson, M. and Hahn, B.H. (1995) Virion associated accessory proteins: new targets for antiviral therapy. In Girard, M. and Dodet, B. (eds), Retroviruses of Human AIDS and Related Animal Diseases. Dixeme Colloque des Cent Gardes, pp. 99-106
30. Fletcher, T.M., III, Brichacek, B., Sharova, M., Newman, M.A., Stivatis, G., Sharp, P.M., Emerman, M., Hahn, B.H. and Stevenson, M. (1996) Nuclear import and cell cycle arrest functions of the HIV-1 Vpr protein are encoded by two separate genes in HIV-1/SIVsm. EMBO J., 15, 6155-6165.
31. Gallay, P., Swingler, S., Aiken, C. and Trono, D. (1995a) HIV-1 infection of nondividing cells: C-terminal tyrosine phosphorylation of the viral matrix protein is a key regulator. Cell, 80, 379-388.
32. Gallay, P., Swingler, S., Song, J., Bushman, F.D. and Trono, D. (1995b) HIV nuclear import is governed by the phosphotyrosine-mediated binding of matrix to the core domain of integrase. Cell, 83, 569-576.
33. Goff, S.P. (1992) Genetics of retroviral integration. Annu. Rev. Genet., 26, 527-544.
34. Goulaouic, H. and Chow, S.A. (1996) Directed integration of viral DNA mediate by fusion proteins consisting of human immunodeficiency virus type 1 integrase and Escherichia coli LexA protein. J. Virol., 70, 37-46.
35. Grandgenett, D.P. and Goodarzi, G. (1994) Folding of the multidomain human immunodeficiency virus type I integrase. Protein Sci., 3, 888-897.
36. Hahn, B.H., Shaw, G.M., Arya, S.K., Popovic, M., Gallo, R.C. and Wong-Staal, F. (1984) Molecular cloning and characterization of the HTLV-III virus associated with AIDS. Nature, 312, 166-169.
37. Hazuda, D.J., Wolfe, A.L., Hastings, J.C., Robbins, H.L., Graham, P.L., LaFemina, R.L. and Emini, E.A. (1994) Viral long terminal repeat substrate binding characteristics of the human immunodeficiency virus type 1 integrase. J. Biol. Chem., 269, 3999-4004.
38. Heinzinger, N.K., Bukrinsky, M.I., Haggerty, S.A., Ragland, A.M., Kewalramani, V., Lee, M.-A., Gendelman, H.E., Ratner, L., Stevenson, M. and Emerman, M. (1994) The Vpr protein of human immunodeficiency virus type 1 influences nuclear localization of viral nucleic acids in nondividing host cells. Proc. Natl Acad. Sci. USA, 91, 7311-7315.
39. Katz, R.A., Merkel, G. and Skalka, A.M. (1996) Targeting of retroviral integrase by fusion to a heterologous DNA binding domain: In vitro activities and incorporation of a fusion protein into viral particles. Virology, 217, 178-190.
40. Kewalramani, V.N. and Emerman, M. (1996) Vpx association with mature core structures of HIV-2. Virology, 218, 159-168.
41. Kimpton, J. and Emerman, M. (1992) Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated b-galactosidase gene. J. Virol., 66, 2232-2239.
42. Kulkosky, J., Jones, K.S., Katz, R.A., Mack, J.P.G. and Skalka, A.M. (1992) Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases. Mol. Cell. Biol., 12, 2331-2338.
43. Kulkosky, J. and Skalka, A.M. (1994) Molecular mechanism of retroviral DNA integration. Pharmac. Ther., 61, 185-203.
44. Landau, N.R., Page, K.A. and Littman, D.R. (1991) Pseudotyping with human T-cell leukemia virus type 1 broadens the human immunodeficiency virus host range. J. Virol., 65, 162-169.
45. Leavitt, A.D., Shiue, L. and Varmus, H.E. (1993) Site-directed mutagenesis of HIV-1 integrase demonstrates differential effects on integrase function in vitro. J. Biol. Chem., 268, 2113-2119.
46. Leavitt, A.D., Robles, G., Alesandro, N. and Varmus, H.E. (1996) Human immunodeficiency virus type 1 integrase mutants retain in vitro integrase activity yet fail to integrate viral DNA efficiently during infection. J. Virol., 70, 721-728.
47. Li, Y., Kappes, J.C., Conway, J.A., Price, R.W., Shaw, G.M. and Hahn, B.H. (1991) Molecular characterization of human immunodeficiency virus type 1 cloned directly from uncultured human brain tissue: identification of replication-competent and -defective viral genomes. J. Virol., 65, 3973-3985.
48. Lu, Y.-L., Spearman, P. and Ratner, L. (1993) Human immunodeficiency virus type 1 viral protein R localization in infected cells and virions. J. Virol., 67, 6542-6550.
49. Maniatis, T., Fritsch, E.F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 269-295.
50. Masuda, T., Planelles, V., Krogstad, P. and Chen, I.S.Y. (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.
51. McEuen, A.R., Edwards, B., Koepke, K.A., Ball, A.E., Jennings, B.A., Wolstenholme, A.J., Danson, M.J. and Hough, D.W. (1992) Zinc binding by retroviral integrase. Biochem. Biophys. Res. Commun., 189, 813-818.
52. Miller, M.D., Warmerdam, M.T., Gaston, I., Greene, W.C. and Feinberg, M.B. (1994) The human immunodeficiency virus-1 nef gene product: a positive factor for viral infection and replication in primary lymphocytes and macrophages. J. Exp. Med., 179, 101-113.
53. Miller, M.D., Bor, Y.-C. and Bushman, F.D. (1995) Target DNA capture by HIV-1 integration complexes. Curr. Biol., 5, 1047-1056.
54. Minassian, A.A., Kalyanaraman, V.S., Gallo, R.C. and Popovic, M. (1988) Monoclonal antibodies against human immunodeficiency virus (HIV) type 2 core proteins: Cross-reactivity with HIV type 1 and simian immunodeficiency virus. Proc. Natl Acad. Sci. USA, 85, 6939-6943.
55. Muesing, M. A., Smith, D.H., Cabradilla, C.D., Benton, C.V., Lasky, L.A. and Capon, D.J. (1985) Nucleic acid structure and expression of the human AIDS/lymphadenopathy retrovirus. Nature, 313, 450-458.
56. Naldini, L., Blomer, U., Gallay, P. Ory, D., Mulligan, R., Gage, F.H., Verma, I.M. and Trono, D. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science, 272, 263-267.
57. Parolin, C., Dorfman, T., Palu, G., Göttlinger, H. and Sodroski, J. (1994) Analysis in human immunodeficiency virus type 1 vectors of cis-acting sequences that affect gene transfer into human lymphocytes. J. Virol., 68, 3888-3895.
58. Paxton, W., Connor, R.I. and Landau, N.R. (1993) Incorporation of Vpr into human immunodeficiency virus type 1 virions: requirement for the p6 region of gag and mutational analysis. J. Virol., 67, 7229-7237.
59. Pettit, S.C., Simsic, J., Loeb, D.D., Everitt, L., Hutchison, C.A., III and Swanstrom, R. (1991) Analysis of retroviral protease cleavage sites reveals two types of cleavage sites and the structural requirements of the P1 amino acid. J. Biol. Chem., 266, 14539-14547.
60. Plasterk, R.H.A. (1995) The HIV integrase catalytic core. Struct. Biol., 2, 87-90.
61. Rice, P. and Mizuuchi, K. (1995) Structure of the bacteriophage Mu transposase core: a common structural motif for DNA transposition and retroviral integration. Cell, 82, 209-220.
62. Sato, A., Yoshimoto, J., Isaka, Y., Miki, S., Suyama, A., Adachi, A., Hayami, M., Fujiwara, T. and Yoshie, O. (1996) Evidence for direct association of Vpr and matrix protein p17 within the HIV-1 virion. Virology, 220, 208-212.
63. Schauer, M. and Billich, A. (1992) The N-terminal region of HIV-1 integrase is required for integration activity, but not for DNA-binding. Biochem. Biophys. Res. Commun., 185, 874-880.
64. Taddeo, B., Carlini, F., Verani, P. and Engelman, A. (1996) Reversion of a human immunodeficiency virus type 1 integrase mutant at a second site restores enzyme function and virus infectivity. J. Virol. 70, 8277-8284.
65. Trono, D. (1995) HIV accessory proteins: Leading roles for the supporting cast. Cell, 82, 189-192.
66. van Gent, D.C., Oude Groeneger, A.A.M and Plasterk, R.H.A. (1992) Mutational analysis of the integrase protein of human immunodeficiency virus type 2. Proc. Natl Acad. Sci. USA, 89, 9598-9602.
67. van Gent, D.C., Vink, C., Oude Groeneger, A.A.M. and Plasterk, R.H.A. (1993) Complementation between HIV integrase proteins mutated in different domains. EMBO J., 12, 3261-3267.
68. von Schwedler, U., Kornbluth, R.S. and Trono, D. (1994) The nuclear localization signal of the matrix protein of human immunodeficiency virus type 1 allows the establishment of infection in macrophages and quiescent T lymphocytes. Proc. Natl Acad. Sci. USA, 91, 6992-6996.
69. Vile, R.G. and Russell, S.J. (1995) Retroviruses as vectors. Br. Med. Bull., 51, 12-30.
70. Vincent, K.A., Ellison, V., Chow, S.A. and Brown, P.O. (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.
71. Vink, C., Groenink, M., Elgersma, Y., Fouchier, R.A.M., Tersmette, M. and Plasterk, R.H.A. (1990) Analysis of the junctions between human immunodeficiency virus type 1 proviral DNA and human DNA. J. Virol., 64, 5626-5627.
72. Vink, C., Oude Groeneger, A.A.M. and Plasterk, R.H.A. (1993) Identification of the catalytic and DNA-binding region of the human immunodeficiency virus type 1 integrase protein. Nucleic Acids Res., 21, 1419-1425.
73. Wiskerchen, M. and Muesing, M.A. (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.
74. Wei, X., Ghosh, S.K., Taylor, M.E., Johnson, V.A., Emini, E.A., Deutsch, P., Lifson, J.D., Bonhoeffer, S., Nowak, M.A., Hahn, B.H., Saag, M.S. and Shaw, G.M. (1995) Viral dynamics in human immunodeficiency virus type 1 infection. Nature, 373, 117-122.
75. Woerner, A.M. and Marcus-Sekura, C.J. (1993) Characterization of a DNA binding domain in the C-terminus of HIV-1 integrase by deletion mutagenesis. Nucleic Acids Res., 21, 3507-3511.
76. Wu, X., Liu, H., Xiao, H., Kim, J., Seshaiah, P., Natsoulis, G., Boeke, J.D., Hahn, B.H. and Kappes, J.C. (1995) Targeting foreign proteins to human immunodeficiency virus particles via fusion with Vpr and Vpx. J. Virol., 69, 3389-98.
77. Wu, X., Liu, H.M. and Kappes, J.C. (1997) Virion incorporation of Vpr-RT fusion protein rescues replication of RT-defective HIV-1. 4th Conference on Retroviruses and Opportunistic Infections, Washington, D.C.
78. Yu, X., Matsuda, F.M., Yu, Q.-C., Lee, T.-H. and Essex, M. (1993) Vpx of Simian Immunodeficiency virus is located primarily outside the virus core in mature virions. J. Virol., 67, 4386-4390.