The requirement for cellular transportin 3 (TNPO3 or TRN-SR2) during infection maps to human immunodeficiency virus type 1 capsid and not integrase

Journal of Virology

Volumn 84, Issue 1, 2010, Pages 397-406

  Krishnan, Lavanya ^a   Matreyek, Kenneth A ^a   Oztop, Ilker ^a   Lee, Kyeongeun ^b   Tipper, Christopher H ^a   Li, Xiang ^a   Dar, Mohd J ^a,c   KewalRamani, Vineet N ^b   Engelman, Alan ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CAPSID PROTEIN; INTEGRASE; TRANSPORTIN 3; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; BINDING AFFINITY; BOVINE IMMUNODEFICIENCY LIKE VIRUS; CHIMERA; CONTROLLED STUDY; EQUINE INFECTIOUS ANEMIA VIRUS; FELINE IMMUNODEFICIENCY VIRUS; FEMALE; HELA CELL; HEREDITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IN VITRO STUDY; LENTIVIRINAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; RETROVIRUS; ROUS SARCOMA ONCOVIRUS; SENSITIZATION; SIMIAN IMMUNODEFICIENCY VIRUS; SURFACE PLASMON RESONANCE; VIRUS CAPSID;

ANIMALS; BETA KARYOPHERINS; CAPSID; CELL LINE; HIV INFECTIONS; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; INTEGRASES; KARYOPHERINS; LENTIVIRUS; LEUKEMIA VIRUS, MURINE; PROTEIN BINDING;

BOVINE IMMUNODEFICIENCY VIRUS; EQUINE INFECTIOUS ANEMIA VIRUS; FELINE IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE; MOLONEY MURINE LEUKEMIA VIRUS; RICE STRIPE VIRUS; ROUS SARCOMA VIRUS; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 72849130164     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01899-09     Document Type: Article

References (55)

1. Alexander, L., R. S. Veazey, S. Czajak, M. DeMaria, M. Rosenzweig, A. A. Lackner, R. C. Desrosiers, and V. G. Sasseville. 1999. Recombinant simian immunodeficiency virus expressing green fluorescent protein identifies infected cells in rhesus monkeys. AIDS Res. Hum. Retroviruses 15:11-21.
2. Ao, Z., G. Huang, H. Yao, Z. Xu, M. Labine, A. W. Cochrane, and X. Yao. 2007. Interaction of human immunodeficiency virus type 1 integrase with cellular nuclear import receptor importin 7 and its impact on viral replication. J. Biol. Chem. 282:13456-13467.
3. Berkowitz, R., H. Ilves, W. Y. Lin, K. Eckert, A. Coward, S. Tamaki, G. Veres, and I. Plavec. 2001. Construction and molecular analysis of gene transfer systems derived from bovine immunodeficiency virus. J. Virol. 75:3371-3382. (Pubitemid 32225900)
4. Bowerman, B., P. O. Brown, J. M. Bishop, and H. E. Varmus. 1989. A nucleoprotein complex mediates the integration of retroviral DNA. Genes Dev. 3:469-478.
5. Brass, A. L., D. M. Dykxhoorn, Y. Benita, N. Yan, A. Engelman, R. J. Xavier, J. Lieberman, and S. J. Elledge. 2008. Identification of host proteins required for HIV infection through a functional genomic screen. Science 319:921-926.
6. Bukrinsky, M., N. Sharova, M. Dempsey, T. Stanwick, A. Bukrinskaya, S. Haggerty, and M. Stevenson. 1992. Active nuclear import of human immunodeficiency virus type 1 preintegration complexes. Proc. Natl. Acad. Sci. U. S. A. 89:6580-6584.
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. U. S. A. 90:3428-3432.
8. Busschots, K., J. Vercammen, S. Emiliani, R. Benarous, Y. Engelborghs, F. Christ, and Z. Debyser. 2005. The interaction of LEDGF/p75 with integrase is lentivirus-specific and promotes DNA binding. J. Biol. Chem. 280:17841-17847.
9. Cannon, P. M., E. D. Byles, S. M. Kingsman, and A. J. Kingsman. 1996. Conserved sequences in the carboxyl terminus of integrase that are essential for human immunodeficiency virus type 1 replication. J. Virol. 70:651-657.
10. Chen, C. M., D. M. Smith, M. A. Peters, M. E. Samson, J. Zitz, C. J. Tabin, and C. L. Cepko. 1999. Production and design of more effective avian replication-incompetent retroviral vectors. Dev. Biol. 214:370-384.
11. Cherepanov, P. 2007. LEDGF/p75 interacts with divergent lentiviral integrases and modulates their enzymatic activity in vitro. Nucleic Acids Res. 35:113-124. (Pubitemid 46189836)
12. Cherepanov, P., E. Devroe, P. A. Silver, and A. Engelman. 2004. Identification of an evolutionarily-conserved domain in LEDGF/p75 that binds HIV-1 integrase. J. Biol. Chem. 279:48883-48892.
13. Christ, F., W. Thys, J. De Rijck, R. Gijsbers, A. Albanese, D. Arosio, S. Emiliani, J. C. Rain, R. Benarous, A. Cereseto, and Z. Debyser. 2008. Transportin-SR2 imports HIV into the nucleus. Curr. Biol. 18:1192-1202.
14. Craigie, R., A. B. Hickman, and A. Engelman. 1995. Integrase, p. 53-71. In J. Karn (ed.), HIV volume2: biochemistry, molecular biology, and drug discovery. IRL Press, New York, NY.
15. De Rijck, J., L. Vandekerckhove, F. Christ, and Z. Debyser. 2007. Lentiviral nuclear import: a complex interplay between virus and host. Bioessays 29:441-451. (Pubitemid 46750736)
16. Engelman, A. 1996. Biochemical characterization of recombinant equine infectious anemia virus integrase. Protein Expr. Purif. 8:299-304.
17. Engelman, A., and P. Cherepanov. 2008. The lentiviral integrase binding protein LEDGF/p75 and HIV-1 replication. PLoS Pathog. 4:e1000046.
18. 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.
19. Fassati, A. 2006. HIV infection of non-dividing cells: a divisive problem. Retrovirology 3:74. (Pubitemid 44742670)
20. Fassati, A., and S. P. Goff. 2001. Characterization of intracellular reverse transcription complexes of human immunodeficiency virus type 1. J. Virol. 75:3626-3635. (Pubitemid 32246372)
21. Fassati, A., and S. P. Goff. 1999. Characterization of intracellular reverse transcription complexes of Moloney murine leukemia virus. J. Virol. 73:8919-8925. (Pubitemid 29487043)
22. Fassati, A., D. Gorlich, I. Harrison, L. Zaytseva, and J. M. Mingot. 2003. Nuclear import of HIV-1 intracellular reverse transcription complexes is mediated by importin 7. EMBO J. 22:3675-3685. (Pubitemid 36898344)
23. 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. U. S. A. 94:9825-9830.
24. He, J., Y. Chen, M. Farzan, H. Choe, A. Ohagen, S. Gartner, J. Busciglio, X. Yang, W. Hofmann, W. Newman, C. R. Mackay, J. Sodroski, and D. Gabuzda. 1997. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 385:645-649. (Pubitemid 27087579)
25. Hearps, A. C., and D. A. Jans. 2006. HIV-1 integrase is capable of targeting DNA to the nucleus via an importin alpha/beta-dependent mechanism. Biochem. J. 398:475-484.
26. Jonsson, C. B., G. A. Donzella, and M. J. Roth. 1993. Characterization of the forward and reverse integration reactions of the Moloney murine leukemia virus integrase protein purified from Escherichia coli. J. Biol. Chem. 268:1462-1469.
27. Kataoka, N., J. L. Bachorik, and G. Dreyfuss. 1999. Transportin-SR, a nuclear import receptor for SR proteins. J. Cell Biol. 145:1145-1152. (Pubitemid 29293627)
28. Katz, R. A., C. A. Omer, J. H. Weis, S. A. Mitsialis, A. J. Faras, and R. V. Guntaka. 1982. Restriction endonuclease and nucleotide sequence analyses of molecularly cloned unintegrated avian tumor virus DNA: structure of large terminal repeats in circle junctions. J. Virol. 42:346-351.
29. Khare, P. D., N. Loewen, W. Teo, R. A. Barraza, D. T. Saenz, D. H. Johnson, and E. M. Poeschla. 2008. Durable, safe, multi-gene lentiviral vector expression in feline trabecular meshwork. Mol. Ther. 16:97-106.
30. Konig, R., Y. Zhou, D. Elleder, T. L. Diamond, G. M. Bonamy, J. T. Irelan, C. Y. Chiang, B. P. Tu, P. D. De Jesus, C. E. Lilley, S. Seidel, A. M. Opaluch, J. S. Caldwell, M. D. Weitzman, K. L. Kuhen, S. Bandyopadhyay, T. Ideker, A. P. Orth, L. J. Miraglia, F. D. Bushman, J. A. Young, and S. K. Chanda. 2008. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 135:49-60.
31. Lewis, P., M. Hensel, and M. Emerman. 1992. Human immunodeficiency virus infection of cells arrested in the cell cycle. EMBO J. 11:3053-3058.
32. 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. (Pubitemid 24974657)
33. Loewen, N., R. Barraza, T. Whitwam, D. T. Saenz, I. Kemler, and E. M. Poeschla. 2003. FIV vectors. Methods Mol. Biol. 229:251-271.
34. Mattaj, I. W., and L. Englmeier. 1998. Nucleocytoplasmic transport: the soluble phase. Annu. Rev. Biochem. 67:265-306.
35. Miller, D. G., M. A. Adam, and A. D. Miller. 1990. Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection. Mol. Cell. Biol. 10:4239-4242.
36. Miller, M., C. Farnet, and F. Bushman. 1997. Human immunodeficiency virus type 1 preintegration complexes: studies of organization and composition. J. Virol. 71:5382-5390. (Pubitemid 27258214)
37. Naldini, L., U. Blömer, P. Gallay, D. Ory, R. Mulligan, F. H. Gage, I. M. Verma, and D. Trono. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263-267.
38. Olsen, J. C. 1998. Gene transfer vectors derived from equine infectious anemia virus. Gene Ther. 5:1481-1487. (Pubitemid 28517375)
39. O'Rourke, J. P., G. C. Newbound, D. B. Kohn, J. C. Olsen, and B. A. Bunnell. 2002. Comparison of gene transfer efficiencies and gene expression levels achieved with equine infectious anemia virus- and human immunodeficiency virus type 1-derived lentivirus vectors. J. Virol. 76:1510-1515.
40. Perron, M. J., M. Stremlau, B. Song, W. Ulm, R. C. Mulligan, and J. Sodroski. 2004. TRIM5alpha mediates the postentry block to N-tropic murine leukemia viruses in human cells. Proc. Natl. Acad. Sci. U. S. A. 101:11827-11832.
41. Poeschla, E. M. 2008. Integrase, LEDGF/p75 and HIV replication. Cell. Mol. Life Sci. 65:1403-1424.
42. 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. (Pubitemid 23157725)
43. Schwartz, R. M., and M. O. Dayhoff. 1978. Matrices for detecting distance relationships, p. 353-358. In M. O. Dayhoff (ed.), Atlas of protein sequence and structure, vol.5, suppl. 3. National Biochemical Research Foundation, Washington, DC.
44. Shibagaki, Y., M. L. Holmes, R. S. Appa, and S. A. Chow. 1997. Characterization of feline immunodeficiency virus integrase and analysis of functional domains. Virology 230:1-10. (Pubitemid 27243517)
45. Shun, M. C., J. E. Daigle, N. Vandegraaff, and A. Engelman. 2007. Wild-type levels of human immunodeficiency virus type 1 infectivity in the absence of cellular emerin protein. J. Virol. 81:166-172. (Pubitemid 44975157)
46. Ulm, J. W., M. Perron, J. Sodroski, and R. C. Mulligan. 2007. Complex determinants within the Moloney murine leukemia virus capsid modulate susceptibility of the virus to Fv1 and Ref1-mediated restriction. Virology 363:245-255.
47. Vandegraaff, N., E. Devroe, F. Turlure, P. A. Silver, and A. Engelman. 2006. Biochemical and genetic analyses of integrase-interacting proteins lens epithelium- derived growth factor (LEDGF)/p75 and hepatoma-derived growth factor related protein 2 (HRP2) in preintegration complex function and HIV-1 replication. Virology 346:415-426. (Pubitemid 43357885)
48. 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.
49. Woodward, C. L., S. Prakobwanakit, S. Mosessian, and S. A. Chow. 2009. Integrase interacts with nucleoporin NUP153 to mediate the nuclear import of human immunodeficiency virus type 1. J. Virol. 83:6522-6533.
50. Yamashita, M., and M. Emerman. 2004. Capsid is a dominant determinant of retrovirus infectivity in nondividing cells. J. Virol. 78:5670-5678. (Pubitemid 38661654)
51. Yamashita, M., and M. Emerman. 2006. Retroviral infection of non-dividing cells: old and new perspectives. Virology 344:88-93. (Pubitemid 41814454)
52. Yamashita, M., and M. Emerman. 2005. The cell cycle independence of HIV infections is not determined by known karyophilic viral elements. PLoS Pathog. 1:e18.
53. Yamashita, M., O. Perez, T. J. Hope, and M. Emerman. 2007. Evidence for direct involvement of the capsid protein in HIV infection of nondividing cells. PLoS Pathog. 3:1502-1510. (Pubitemid 350085614)
54. Zaitseva, L., P. Cherepanov, L. Leyens, S. J. Wilson, J. Rasaiyaah, and A. Fassati. 2009. HIV-1 exploits importin 7 to maximize nuclear import of its DNA genome. Retrovirology 6:11.
55. Zufferey, R., J. E. Donello, D. Trono, and T. J. Hope. 1999. Woodchuck hepatitis virus posttranscriptional regulatory element enhances expression of transgenes delivered by retroviral vectors. J. Virol. 73:2886-2892. (Pubitemid 29135675)