Evaluation of the functional involvement of human immunodeficiency virus type 1 integrase in nuclear import of viral cDNA during acute infection

Journal of Virology

Volumn 78, Issue 21, 2004, Pages 11563-11573

  Ikeda, Tamako ^a   Nishitsuji, Hironori ^a   Zhou, Xin ^a   Nara, Nobuo ^a   Ohashi, Takashi ^a   Kannagi, Mari ^a   Masuda, Takao ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; INTEGRASE; VIRUS DNA; VIRUS ENZYME;

ANIMAL CELL; ARTICLE; CELL STRAIN COS7; CONTROLLED STUDY; DNA BINDING; DNA SYNTHESIS; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENE MUTATION; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; NUCLEAR IMPORT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VIRUS GENE; VIRUS REPLICATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; COS CELLS; DNA, COMPLEMENTARY; DNA, VIRAL; HIV INTEGRASE;

EID: 6344219975     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.21.11563-11573.2004     Document Type: Article

References (68)

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 retroviras in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
2. Bouyac-Bertoia, M., J. D. Dvorin, R. A. Fouchier, Y. Jenkins, B. E. Meyer, L. I. Wu, M. Emerman, and M. H. Malim. 2001. HIV-1 infection requires a functional integrase NLS. Mol. Cell 7:1025-1035.
3. Bukrinsky, M. I., and O. K. Haffar. 1997. HIV-1 nuclear import: in search of a leader. Front. Biosci. 2:d578-d587.
4. Bukrinsky, M. I., S. Haggerty, M. P. Dempsey, N. Sharova, A. Adzhubel, L. Spitz, P. Lewis, D. Goldfarb, M. Emerman, and M. Stevenson. 1993. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature 365:666-669.
5. Bukrinsky, M. I., N. Sharova, T. L. McDonald, T. Pushkarskaya, W. G. 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.
6. Burke, C. J., G. Sanyal, M. W. Bruner, J. A. Ryan, R. L. LaFemina, H. L. Rabbins, 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.
7. Bushman, F. D., A. Engelman, I. Palmer, P. Wingfield, 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.
8. Cai, M., R. Zheng, M. Caffrey, R. Craigie, G. M. Clore, and A. M. Gronenborn. 1997. Solution structure of the N-terminal zinc binding domain of HIV-1 integrase. Nat. Struct. Biol. 4:567-577.
9. 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.
10. Chameau, P., and F. Clavel. 1991. A single-stranded gap in human immunodeficiency virus unintegrated linear DNA defined by a central copy of the polypurine tract. J. Virol. 65:2415-2421.
11. Chen, J. C., J. Krucinski, L. J. Miercke, J. S. Finer-Moore, A. H. Tang, A. D. Leavitt, and R. M. Stroud. 2000. Crystal structure of the HIV-1 integrase catalytic core and C-terminal domains: a model for viral DNA binding. Proc. Natl. Acad. Sci. USA 97:8233-8238.
12. 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.
13. Cullen, B. R. 2001. Journey to the center of the cell. Cell 105:697-700.
14. Depienne, C., A. Mousnier, H. Leh, E. Le Rouzic, D. Dormont, S. Benichou, and C. Dargemont. 2001. Characterization of the nuclear import pathway for HIV-1 integrase. J. Biol. Chem. 276:18102-18107.
15. Devroe, E., A. Engelman, and P. A. Silver. 2003. Intracellular transport of human immunodeficiency virus type 1 integrase. J. Cell Sci. 116:4401-4408.
16. Dirac, A. M., and J. Kjems. 2001. Mapping DNA-binding sites of HIV-1 integrase by protein footprinting. Eur. J. Biochem. 268:743-751.
17. Dvorin, J. D., P. Bell, G. G. Maul, M. Yamashita, M. Emerman, and M. H. Malim. 2002. Reassessment of the roles of integrase and the central DNA flap in human immunodeficiency virus type 1 nuclear import. J. Virol. 76: 12087-12096.
18. 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.
19. Eijkelenboom, A. P., R. A. Lutzke, R. Boelens, R. H. Plasterk, R. Kaptein. and K. Hard. 1995. The DNA-binding domain of HIV-1 integrase has an SH3-like fold. Nat. Struct. Biol. 2:807-810.
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., G. England, 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.
22. Esposito, D., and R. Craigie. 1998. Sequence specificity of viral end DNA binding by HIV-1 integrase reveals critical regions for protein-DNA interaction. EMBO J. 17:5832-5843.
23. Fassati, A., D. Gorlich, I. Harrison, L. Zaylseva, and J. M. Mingot. 2003. Nuclear import of HIV-1 intracellular reverse transcription complexes is mediated by importin 7. EMBO J. 22:3675-3685.
24. Fouchier, R. A., B. E. Meyer, J. H. Simon, U. Fischer, A. V. Albright, F. Gonzalez-Scarano, and M. H. Malim. 1998. Interaction of the human immunodeficiency virus type 1 Vpr protein with the nuclear pore complex. J. Virol. 72:6004-6013.
25. Freed, E. O., G. Englund, F. Maldarelli, and M. A. Martin. 1997. Phosphorylation of residue 131 of HIV-1 matrix is not required for macrophage infection. Cell 88:171-173.
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 83:569-576.
28. Gerton, J. L., S. Ohgi, M. Olsen, J. DeRisi, and P. O. Brown. 1998. Effects of mutations in residues near the active site of human immunodeficiency virus type 1 integrase on specific enzyme-substrate interactions. J. Virol. 72:5046-5055.
29. Goff, S. P. 2001. Intracellular trafficking of retroviral genomes during the early phase of infection: viral exploitation of cellular pathways. J. Gene Med. 3:517-528.
30. Goldgur, Y., F. Dyda, A. B. Hickman, T. M. Jenkins, R. Craigie, and D. R. Davies. 1998. Three new structures of the core domain of HIV-1 integrase: an active site that binds magnesium. Proc. Natl. Acad. Sci. USA 95:9150-9154.
31. Hansen, M. S., G. J. Smith III, T. Kafri, V. Molteni, J. S. Siegel, and F. D. Bushman. 1999. Integration complexes derived from HIV vectors for rapid assays in vitro. Nat. Biotechnol. 17:578-582.
32. Heinzinger, N. K., M. I. Bukinsky, S. A. Haggerry, A. M. Ragland, V. Kewalramani, M. A. Lee, H. E. Gendelman, L. Ratner, M. Stevenson, and M. Emerman. 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.
33. Heuer, T. S., and P. O. Brown. 1997. Mapping features of HIV-1 integrase near selected sites on viral and target DNA molecules in an active enzymeDNA complex by photo-cross-linking. Biochemistry 36:10655-10665.
34. Heuer, T. S., and P. O. Brown. 1998. Photo-cross-linking studies suggest a model for the architecture of an active human immunodeficiency virus type 1 integrase-DNA complex. Biochemistry 37:6667-6678.
35. Hindmarsh, P., and J. Leis. 1999. Retroviral DNA integration. Microbiol. Mol. Biol. Rev. 63:836-843.
36. Jenkins, T. M., D. Esposito, A. Engelman, and R. Craigie. 1997. Critical contacts between HIV-1 integrase and viral DNA identified by structure-based analysis and photo-crosslinking. EMBO J. 16:6849-6859.
37. Jenkins, Y., M. McEntee, K. Weis, and W. C. Greene. 1998. Characterization of HIV-1 vpr nuclear import: analysis of signals and pathways. J. Cell Biol. 143:875-885.
38. Katz, R. A., and A. M. Skalka. 1994. The retroviral enzymes. Annu. Rev. Biochem. 63:133-173.
39. Katzman, M., and M. Sudol. 1996. Influence of subterminal viral DNA nucleotides on differential susceptibility to cleavage by human immunodeficiency virus type 1 and visna virus integrases. J. Virol. 70:9069-9073.
40. Katzman, M., and M. Sudol. 1998. Mapping viral DNA specificity to the central region of integrase by using functional human immunodeficiency virus type 1/visna virus chimeric proteins. J. Virol. 72:1744-1753.
41. Lewis, P., M. Hensel, and M. Emerman. 1992. Human immunodeficiency virus infection of cells arrested in the cell cycle. EMBO J. 11:3053-3058.
42. Lewis, P. F., and M. Emerman. 1994. Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. J. Virol. 68:510-516.
43. Limon, A., E. Devroe, R. Lu, H. Z. Ghory, P. A. Silver, and A. Engelman. 2002. Nuclear localization of human immunodeficiency virus type 1 preintegration complexes (PICs): V165A and R166A are pleiotropic integrase mutants primarily defective for integration, not PIC nuclear import. J. Virol. 76:10598-10607.
44. Limon, A., N. Nakajima, R. Lu, H. Z. Ghory, and A. Engelman. 2002. Wild-type levels of nuclear localization and human immunodeficiency virus type 1 replication in the absence of the central DNA flap. J. Virol. 76:12078-12086.
45. Lins, R. D., A. Adesokan, T. A. Scares, and J. M. Briggs. 2000. Investigations on human immunodeficiency virus type 1 integrase/DNA binding interactions via molecular dynamics and electrostatics calculations. Pharmacol. Ther. 85:123-131.
46. 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.
47. Maertens, G., P. Cherepanov, W. Pluymers, K. Busschots, E. De Clercq, Z. Debyser, and Y. Engelborghs. 2003. LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. J. Biol. Chem. 278:33528-33539.
48. Masuda, T., M. J. Kuroda, and S. Harada. 1998. Specific and independent recognition of U3 and U5 att sites by human immunodeficiency virus type 1 integrase in vivo. J. Virol. 72:8396-8402.
49. Masuda, T., V. Flanelles, P. Krogstad, and I. S. 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.
50. 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.
51. Murakami, T., T. Hagiwara, K. Yamamoto, J. Hattori, M. Kasami, M. Utsumi, and T. Kaneda. 2001. A novel method for detecting HIV-1 by non-radioactive in situ hybridization: application of a peptide nucleic acid probe and catalysed signal amplification. J. Pathol. 194:130-135.
52. Nakamura, T., T. Masuda, T. Goto, K. Sano, M. Nakai, and S. Harada. 1997. Lack of infectivity of HIV-1 integrase zinc finger-like domain mutant with morphologically normal maturation. Biochem. Biophys. Res. Commun. 239: 715-722.
53. Petit, C., O. Schwartz, and F. Mammano. 2000. The karyophilic properties of human immunodeficiency virus type 1 integrase are not required for nuclear import of proviral DNA. J. Virol. 74:7119-7126.
54. Pluymers, W., P. Cherepanov, D. Schols, E. De Clercq, and Z. Debyser. 1999. Nuclear localization of human immunodeficiency virus type 1 integrase expressed as a fusion protein with green fluorescent protein. Virology 258:327-332.
55. Reil, H., A. A. Bukovskv, H. R. Gelderblom, and H. G. Gottlinger. 1998. Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J. 17:2699-2708.
56. Roe, T., T. C. Reynolds, G. Yu, and P. O. Brown. 1993. Integration of murine leukemia virus DNA depends on mitosis. EMBO J. 12:2099-2108.
57. Sayasith, K., G. Sauve, and J. Yelle. 2000. Characterization of mutant HIV-1 integrase carrying amino acid changes in the catalytic domain. Mol. Cells 10:525-532.
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. Suzuki, Y., N. Misawa, C. Sato, H. Ebina, T. Masuda, N. Yamamoto, and Y. Koyanagi. 2003. Quantitative analysis of human immunodeficiency virus type 1 DNA dynamics by real-time PCR: integration efficiency in stimulated and unstimulated peripheral blood mononuclear cells. Virus Genes 27:177-188.
60. Tsurutani, N., M. Kubo, Y. Maeda, T. Ohashi, N. Yamamoto, M. Kannagi, and T. Masuda. 2000. Identification of critical amino acid residues in human immunodeficiency virus type 1 integrase required for efficient proviral DNA formation at steps prior to integration in dividing and nondividing cells. J. Virol. 74:4795-4806.
61. Vink, C., D. C. van Gent, Y. Elgersma, and R. H. Plasterk. 1991. Human immunodeficiency virus integrase protein requires a subterminal position of its vira] DNA recognition sequence for efficient cleavage. J. Virol. 65:4636-4644.
62. Vora, A., and D. P. Grandgenett. 2001. DNase protection analysis of retro-virus integrase at the viral DNA ends for full-site integration in vitro. J. Virol. 75:3556-3567.
63. Wang, J. Y., H. Ling, W. Yang, and R. Craigie. 2001. Structure of a two-domain fragment of HIV-1 integrase: implications for domain organization in the intact protein. EMBO J. 20:7333-7343.
64. Weinberg, J. B., T. J. Matthews, B. R. Cullen, and M. H. Malim. 1991. Productive human immunodeficiency virus type 1 (HIV-1) infection of non-proliferating human monocytes. J. Exp Med. 174:1477-1482.
65. 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.
66. Zack, J. A., S. J. Arrigo, S. R. Weitsman, A. S. Go, A. Haislip, and I. S. Chen. 1990. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61:213-222.
67. Zargarian, L., M. S. Benleumi, J. G. Renisio, H. Merad, R. G. Maroun, F. Wieber, O. Mauffret, H. Porumb, F. Troalen, and S. Fermandjian. 2003. Strategy to discriminate between high and low affinity bindings of human immunodeficiency virus, type 1 integrase to viral DNA. J. Biol. Chem. 278: 19966-19973.
68. Zennou, V., C. Petit, D. Guetard, U. Nerhbass, L. Montagnier, and P. Charneau. 2000. HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 101:173-185.