Nuclear import of HIV-1 intracellular reverse transcription complexes is mediated by importin 7

EMBO Journal

Volumn 22, Issue 14, 2003, Pages 3675-3685

  Fassati, Ariberto ^a   Görlich, Dirk ^b   Harrison, Ian ^a   Zaytseva, Lyubov ^a   Mingot, José Manuel ^b  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

HIV 1; Importins; Nuclear import; Reverse transcription complex; Small interfering RNA

Indexed keywords

HISTONE H1; IMPORTIN 7; KARYOPHERIN; RIBOSOME PROTEIN; RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ACTIVE TRANSPORT; ANIMAL CELL; ARTICLE; CELL DIVISION; COMPLEX FORMATION; DNA HISTONE INTERACTION; ENERGY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTRACELLULAR TRANSPORT; LENTIVIRINAE; MACROPHAGE; MEMBRANE COMPONENT; MOLECULAR MECHANICS; NONHUMAN; NUCLEAR IMPORT; PRIORITY JOURNAL; PROCESS MODEL; PROTEIN ANALYSIS; PROTEIN PURIFICATION; PROTEIN TARGETING; RECEPTOR BINDING; REVERSE TRANSCRIPTION COMPLEX; RIBOSOME; TRANSCRIPTION REGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANTIGENS, CD4; CELL NUCLEOLUS; CELL NUCLEUS; CELLS, CULTURED; DNA, VIRAL; HELA CELLS; HIV INFECTIONS; HIV-1; HIV-1 REVERSE TRANSCRIPTASE; HUMANS; KARYOPHERINS; MACROPHAGES; MUTATION; NUCLEAR ENVELOPE; RAN GTP-BINDING PROTEIN; RECEPTORS, CCR5; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRUS; RNA VIRUSES;

EID: 0041312658     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg357     Document Type: Article

References (55)

1. Adam, S.A. and Gerace, L. (1991) Cytosolic proteins that specifically bind nuclear location signals are receptors for nuclear import. Cell, 66, 837-847.
2. Adam, S.A., Sterne Marr R. and Gerace, L. (1990) Nuclear import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol., 111, 807-816.
3. Bischoff, F.R., Scheffzek, K. and Postingl, H. (2002) How Ran is regulated. In Weis, K. (ed.), Nuclear Transport. Springer-Verlag, Berlin, Germany, pp. 49-66.
4. Bukrinsky, M.I., Sharova, N., Dempsey, M.P., Stanwick, T.L., Bukrinkaya, A.G., Haggerty, S. and Stevenson, M. (1992) Active nuclear import of human immunodeficiency virus type 1 preintegration complexes. Proc. Natl Acad. Sci. USA, 89, 6580-6584.
5. Bukrinsky, M.I., Sharova, N., McDonald, T.L., Pushkarskaya, T., Tarpley, W.G. and Stevenson M. (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. Clapham, P.R., McKnight, A. and Weiss, R.A. (1992) Human immunodeficiency virus type-2 infection and fusion of CD4-negative human cell lines: induction and enhancement by soluble CD4. J. Virol., 66, 3531-3537.
7. Cohen, O.J. and Fauci, A.S. (2001) Pathogenesis and medical aspects of HIV-1 infection. In Knipe, D.M. and Howley, P.M. (eds), Fields Virology. Lippincot Williams & Wilkins, Philadelphia, PA, pp. 2043-2094.
8. Cullen, B.R. (2002) Using retroviruses to study the nuclear export of mRNA. In Weis, K. (ed.), Nuclear Transport. Springer-Verlag, Berlin, Germany, pp. 151-168.
9. Demiason, C., Parsley, K., Brouns, G., Scherr, M., Battmer, K., Kinnon, C., Grez, M. and Thrasher, A.J. (2002) High-level transduction and gene expression in hematopoietic repopulating cells using a HIV-1 based lentiviral vector containing an internal spleen focus forming virus promoter. Hum. Gene Ther., 13, 803-813.
10. Deng, H. et al. (1996) Identification of a major co-receptor for primary isolates of HIV-1. Nature, 381, 661-666.
11. deNoronha, C.M., Sherman, M.P., Lin, H.W., Cavrois, M.V., Moir, R.D., Goldman, R.D. and Greene, W.C. (2001) Dynamic disruptions in nuclear envelope architecture and integrity induced by HIV-1 Vpr. Science, 294, 1105-1108.
12. Dvorin, J.D., Bell, P., Maul, G.G., Yamashita, M., Emerman, M. and Malim, M.H. (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.
13. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001) Duplexes of 21-nucleotide RNAs mediate interference in cultured mammalian cells. Nature, 411, 494-498.
14. 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.
15. Farnet, C.M. and Haseltine, W.A. (1991) Determination of viral proteins present in the human immunodeficiency virus type 1 preintegration complex. J. Virol., 65, 1910-1915.
16. Fassati, A. and Goff, S.P. (1999) Characterization of intracellular reverse transcription complexes of Moloney murine leukemia virus. J. Virol., 73, 8919-8925.
17. Fassati, A. and Goff, S.P. (2001) Characterization of intracellular reverse transcription complexes of human immunodeficiency type-1. J. Virol., 75, 3626-3635.
18. Freed, E.O. and Martin, M.A. (2001) HIVs and their replication. In Knipe, D.M. and Howley, P.M. (eds). Fields Virology. Lippincot Williams & Wilkins, Philadelphia, PA, pp. 1971-2041.
19. Gallay, P., Hope, T., Chin, D., Trono, D. (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.
20. 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.
21. Görlich, D. and Kutay, U. (1999) Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell. Dev. Biol., 15, 607-660.
22. Görlich, D., Prehn, S., Laskey, R A. and Hartmann, E. (1994) Isolation of a protein that is essential for the first step of nuclear protein import. Cell, 79, 767-778.
23. Görlich, D., Henklein, P., Laskey, R.A. and Hartmann, E. (1996) A 41 amino acid motif in importin α confers binding to importin β and hence transit into the nucleus. EMBO J., 15, 1810-1817.
24. Görlich, D., Dabrowski, M., Bischoff, F.R., Kutay, U., Bork, P., Hartmann, E., Prehn, S. and Izaurralde, E. (1997) A novel class of RanGTP binding proteins. J. Cell Biol., 138, 65-80.
25. Gottlieb, M.S., Schroff R., Schanker H.M., Weisman, J.D., Fan, P.T, Wolf, R.A. and Saxon A. (1981) Pneumocystis carinii pneumonia and mucosal candidiasis in previously healthy homosexual men: evidence of a new acquired cellular immunodeficiency. N. Engl. J. Med., 305, 1425-1431.
26. Henderson, B.R. and Percipalle, P. (1997) Interactions between Rev and nuclear import and export factors: the rev nuclear localisation signal mediates specific binding to human importin B. J. Mol. Biol., 274, 693-707.
27. Hirt, B. (1967) Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol., 26, 365-369.
28. Izaurralde, E. (2002) Nuclear export of messenger RNA. In Weis, K. (ed.) Nuclear Transport. Springer-Verlag, Berlin, Germany, pp. 133-150.
29. Izaurralde, E., Kutay, U., von Kobbe, C., Mattaj, I.W. and Görlich, D. (1997) The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J., 16, 6535-6547.
30. Jäkel, S. and Görlich, D. (1998) Importin β, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J., 17, 4491-4502.
31. Jäkel, S., Albig, W., Kutay, U., Bischoff, F.R., Schwamborn, K., Doenecke, D. and Görlich, D. (1999) The importin β/importin 7 heterodimer is a functional nuclear import receptor for histone H1. EMBO J., 18, 2411-2423.
32. Jäkel, S., Mingot J-M., Schwarzmaier, P., Hartmann, E., and Görlich, D. (2002) Importins fulfil a dual function as nuclear import receptors and cytoplasmic chaperones for exposed basic domains. EMBO J., 21, 377-386.
33. Kalderon, D., Roberts, B.L., Richardson, W.D. and Smith, A.E. (1984) A short amino acid sequence able to specify nuclear location. Cell, 39, 499-509.
34. Kann, M., Sodeik, B., Vlachou, A., Gerlich, W.H. and Helenius, A. (1999) Phosphorylation dependent binding of hepatitis B virus core particles to the nuclear pore complex. J. Cell Biol., 145, 45-55.
35. Kutay, U., Izaurralde, E., Bischoff, F.R., Mattaj, I. and Görlich, D. (1997) Dominant-negative mutants of importinβ block multiple pathways of import and export through the nuclear pore complex. EMBO J., 16, 1153-1163.
36. Limon, A., Nakajima, N., Lu, R., Ghory, H.Z. and Engelman, A. (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.
37. Malim, M.H. and Cullen, B.R. (1991) HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency. Cell, 65, 241-248.
38. McEwen, C.R. (1967) Tables for estimating sedimentation through linear concentration gradients of sucrose solution. Anal. Biochem., 20, 114-149.
39. Miller, M.D., Farnet, C.M. and Bushman, F.D. (1997) Human immunodeficiency virus type-1 preintegration complexes: studies of organization and composition. J. Virol., 71, 5382-5390.
40. Mingot, J.-M., Kostka, S., Kraft, R., Hartmann, E. and Görlich, D. (2001) Importin 13: a novel mediator of nuclear import and export. EMBO J., 20, 3685-3694.
41. 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.
42. Neil, S., Martin, F., Ikeda, Y. and Collins, M. (2001) Postentry restriction to human immunodeficiency virus-based vector transduction in human monocytes. J. Virol., 75, 5448-5456.
43. O'Neill, R., Jaskunas, R., Blobel, G., Palese, P. and Moroianu, J. (1995) Nuclear import of influenza virus RNA can be mediated by viral nucleoprotein and transport factors required for protein import. J. Biol. Chem., 270, 22701-22704.
44. Rexach, M. and Blobel, G. (1995) Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors and nucleoporins. Cell, 83, 683-692.
45. Ribbeck, K. and Görlich, D. (2002) The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J., 21, 2664-2671.
46. Ribbeck, K. Lipowsky, G., Kent, H.M., Stewart, M. and Görlich, D. (1998) NTF2 mediates nuclear import of Ran. EMBO J., 17, 6587-6598.
47. Roe, T., Reynolds, G., Yu, G. and Brown, P.O. (1993) Integration of murine leukemia virus DNA depends on mitosis. EMBO J., 12, 2099-2108.
48. Rout, M.P., Aitchinson, J.D., Suprapto, A., Hjertaas, K., Zhao, Y. and Chait, B.T. (2000) The yeast nuclear pore complex: composition, architecture and transport mechanism. J. Cell Biol., 148, 635-651.
49. Sapphire, A.C.S., Guan, T., Schirmer, E.C., Nemerow, G.R. and Gerace, L. (2000) Nuclear import of adenovirus DNA in vitro involves the nuclear protein import pathway and hsc70. J. Biol. Chem., 275, 4298-4304.
50. Siomi, M.C., Eder, P.S., Kataoka, N., Wan, L., Liu, Q. and Dreyfuss, G. (1997) Transportin-mediated nuclear import of heterogeneous nuclear RNP proteins. J. Cell Biol., 138, 1181-1192.
51. Soda, Y., Shimizu, N., Jinno, A., Liu, H.Y., Kanabe, K., Kitamura, T. and Hoshino,H. (1999) Establishment of a new system for determination of coreceptor usages of HIV based on the human glioma NP-2 cell line. Biochem. Biophys. Res. Commun., 258, 313-321.
52. Trotman, L.C., Mosberger, N., Fornerod, M., Stidwill, R.P. and Greber, U.F. (2001) Import of adenovirus DNA involves the nuclear pore complex receptor CAN/Nup214 and histone H1. Nature Cell Biol., 3, 1092-1100.
53. UNAIDS (2002) Report on the global HIV/AIDS epidemic. http://www.unaids.org/epidemic_update/report_july02/english/embargo.htm
54. Zennou, V., Petit, C., Guetard, U., Nerhbass, U., Montagnier, L. and Charneau, P. (2000) HIV-1 genome nuclear import is mediated by a central DNA flap. Cell, 101, 173-185.
55. Zufferey, R., Nagy, D., Mandel, R.J., Naldini, L. and Trono, D. (1997) Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol., 15, 871-875.