The C-terminal proline-rich tail of human immunodeficiency virus type 2 Vpx is necessary for nuclear localization of the viral preintegration complex in nondividing cells

Journal of Virology

Volumn 74, Issue 13, 2000, Pages 6162-6167

  Pancio, Heather A ^a   Vander Heyden, Nancy ^a   Ratner, Lee ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; KARYOPHERIN; PROLINE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VPR PROTEIN; VPX PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 2; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROVIRUS; VIRUS DNA CELL DNA INTERACTION;

CELL DIVISION; CELL LINE, TRANSFORMED; CELL NUCLEUS; CELLS, CULTURED; DNA, VIRAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HIV-2; HUMANS; LUMINESCENT PROTEINS; MACROPHAGES; NUCLEAR LOCALIZATION SIGNALS; PROLINE; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; U937 CELLS; VIRAL REGULATORY PROTEINS; VIRUS INTEGRATION;

EID: 0034125942     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.13.6162-6167.2000     Document Type: Article

References (49)

1. agm. J. Virol. 73:9992-9999.
2. Bedford, M. T., D. C. Chan, and P. Leder. 1997. FBP WW domains and the Abl SH3 domain bind to a specific class of proline-rich ligands. EMBO J. 16:2376-2383.
3. Bukrinsky, M. I., S. Haggerty, M. P. Dempsey, N. Sharova, A. Adzhubei, 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.
4. Chen, H. I., and M. Sudol. 1995. The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc. Natl. Acad. Sci. USA 92:7819-7823.
5. Di Marzio, P., S. Choe, M. Ebright, R. Knoblauch, and N. R. Landau. 1993. Mutational analysis of cell cycle arrest, nuclear localization, and virion packaging of human immunodeficiency virus type 1 Vpr. J. Virol. 69:7909-7916.
6. Dobrosotskaya, I., R. K. Guy, and G. L. James. 1997. MAGI-1, a membrane-associated guanylate kinase with a unique arrangement of protein-protein interaction domains. J. Biol. Chem. 272:31589-31597.
7. Emerman, M. 1996. HIV-1, Vpr and the cell cycle. Curr. Biol. 6:1096-1103.
8. Farnet, C. N., and W. A. Haseltine. 1990. Integration of human immunodeficiency virus type 1 DNA in vitro. Proc. Natl. Acad. Sci. USA 87:4164-4168.
9. Fletcher, T. M., B. Brichacek, N. Sharova, M. A. Newman, G. Stivahtis, P. M. Sharp, M. Emerman, B. H. Hahn, and M. Stevenson. 1996. Nuclear import and cell cycle arrest of the HIV-1 vpr protein are encoded by two separate genes in HIV-2/SIVsm. EMBO J. 15:6155-6165.
10. Fouchier, R. A. M., B. E. Meyer, J. H. M. Simon, U. Fischer, and M. H. Malim. 1997. HIV-1 infection of non-dividing cells: evidence that the amino-terminal basic region of the viral matrix protein is important for gag processing but not for post-entry nuclear import. EMBO J. 16:4531-4539.
11. Franchini, G., J. R. Rusche, T. J. O'Keeffe, and F. Wong-Staal. 1988. The human immunodeficiency virus type 2 (HIV-2) contains a novel gene encoding a 16 kD protein associated with mature virions AIDS Res. Hum. Retrovir. 4:243-250.
12. 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.
13. Gallay, P., V. Stitt, C. Mundy, M. Oettinger, and D. Trono. 1996. Role of the karyopherin pathway in human immunodeficiency virus type 1 nuclear import. J. Virol. 70:1027-1032.
14. Gorlich, D., H. Kostka, R. Kraft, C. Dingwall, R. A. Laskey, E. Hartmann, and S. Prehn. 1995. Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr. Biol. 5:383-392.
15. Gorlich, D., S. Prehn, R. A. Laskey, and E. Hartmann. 1994. Isolation of a protein that is essential for the first step of nuclear protein import. Cell 79:767-778.
16. Heinzinger, N. K., M. I. Bukrinsky, S. A. Haggerty, 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.
17. Hirsch, V. M., M. E. Sharkey, C. R. Brown, B. Brichacek, S. Goldstein, J. Wakefield, R. Byrum, W. R. Elkins, B. H. Hahn, J. D. Lifson, and M. Stevenson. 1998. Vpx is required for dissemination and pathogenesis of SIVsmPBj: evidence of macrophage-dependent viral amplification. Nat. Med. 4:1401-1408.
18. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
19. Horton, R., P. Spearman, and L. Ratner. 1994. HIV-2 viral protein X association with the gag p27 capsid protein. Virology 199:453-457.
20. Hu, W., N. Vander Heyden, and L. Ratner. 1989. Analysis of the function of viral protein X (VPX) of HIV-2. Virology 173:624-630.
21. Hung, C.-S., N. Vander Heyden, and L. Ratner. 1999. Analysis of the critical domain in the V3 loop of human immunodeficiency virus type 1 gp120 involved in CCR5 utilization. J. Virol. 73:8216-8226.
22. Imamoto, N., T. Tachibana, M. Matsube, and V. Yoneda. 1995. A karyophilic protein forms a stable complex with cytoplasmic components prior to nuclear pore binding. J. Biol. Chem. 270:8559-8565.
23. 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.
24. gag is important for Vpr incorporation into human immunodeficiency virus type 1 particles. J. Virol. 69: 6873-6879.
25. Lu, Y.-L., P. Spearman, and L. Ratner. 1993. Human immunodeficiency virus type 1 viral protein R localization in infected cells and virions. J. Virol. 67:6542-6550.
26. Mahalingham, S., V. Ayyavoo, M. Patel, T. Kieber-Emmons, and D. B. Weiner. 1997. Nuclear import, virion incorporation, and cell cycle arrest/ differentiation are mediated by distinct functional domains of human immunodeficiency virus type 1 Vpr. J. Virol. 71:6339-6347.
27. Mahalingham, S., S. A. Khan, M. A. Jabbar, C. E. Monken, R. G. Collman, and A. Srinivasan. 1995. Identification of residues in the N-terminal acidic domain of HIV-1 vpr essential for virion incorporation. Virology 207:297-302.
28. Maleszka, R. A., A. Lupas, S. D. Hanes, and G. L. G. Miklos. 1997. The Dodo gene family encodes a novel protein involved in signal transduction and protein folding. Gene 203:89-93.
29. Moore, M. S., and G. Blobel. 1993. The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature 365:661-663.
30. Moore, M. S., and G. Blobel. 1994. Purification of a Ran-interacting protein that is required for protein import into the nucleus. Proc. Natl. Acad. Sci. USA 91:10212-10216.
31. Mosca, P. J., P. A. Dijkwel, and J. L. Hamlin. 1992. The plant amino acid mimosine may inhibit initiation at origins of replication in Chinese hamster cells. Mol. Cell. Biol. 12:4375-4383.
32. Musacchia, A., M. Wilmanns, and M. Saraste. 1994. Structure and function of the SH3 domain. Progress Biophys. Mol. Biol. 61:283-297.
33. Nakielny, S., and G. Dreyfuss. 1999. Transport of proteins and RNAs in and out of the nucleus. Cell 99:677-680.
34. Pancio, H. A., and L. Ratner. 1998. Human immunodeficiency virus type 2 Vpx-Gag interaction. J. Virol. 72:5271-5275.
35. Park, I.-W., and J. Sodroski. 1995. Amino acid sequence requirements for the incorporation of the vpx protein of simian immunodeficiency virus into virion particles. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 10:506-510.
36. Pirounaki, M., N. Vander Heyden, M. Arens, and L. Ratner. 2000. Rapid phenotypic drug susceptibility assay for HIV-1 with a CCR5 expressing indicator cell line. J. Virol. Methods 85:151-161.
37. Poiesz, B. J., F. W. Ruscetti, A. F. Gazdar, P. A. Burns, J. D. Minna, and R. C. Gallo. 1980. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc. Natl. Acad. Sci. USA 77:7415-7419.
38. Popov, S., M. Rexach, L. Ratner, G. Blobel, and M. Bukrinsky. 1998. Viral protein R regulates docking of the HIV-1 preintegration complex to the nucleus pore complex. J. Biol. Chem. 273:13347-13352.
39. Popov, S., M. Rexach, G. Zybarth, N. Reiling, M.-A. Lee, L. Ratner, C. M. Lane, M. S. Moore, G. Blobel, and M. Bukrinsky. 1998. Viral protein R regulates nuclear import of the HIV-1 preintegration complex. EMBO J. 17:909-917.
40. Radu, A., M. S. Moore, and G. Blobel. 1995. The peptide repeat domain of Nup98 functions as a docking site in transport across the nuclear pore complex. Cell 81:215-222.
41. Rexach, M., and G. Blobel. 1995. Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83:683-692.
42. Sharp, P. M., E. Bailes, M. Stevenson, M. Emerman, and B. Hahn. 1996. Gene acquisition in HIV and SIV. Nature 383:586-587.
43. Shoya, Y., T. Kobayashi, T. Koda, K. Ikuta, M. Kakinuma, and M. Kishi. 1998. Two proline-rich nuclear localization signals in the amino-and carboxyl-terminal regions of the Borna disease virus phosphoprotein. J. Virol. 72:9755-9762.
44. Tristem, M., C. Marshall, A. Karpas, and F. Hill. 1992. Evolution of the primate lentiviruses: evidence from vpx and vpr. EMBO J. 11:3405-3412.
45. Vodicka, M. A., D. M. Koepp, P. A. Silver, and M. Emerman. 1998. HIV-1 vpr interacts with the nuclear transport pathway to promote macrophage infection. Genes Dev. 12:175-185.
46. Weis, K., I. W. Mattaj, and A. I. Lamond. 1995. Identification of hSRP1 alpha as a functional receptor for nuclear localization sequences. Science 268:1049-1053.
47. Wu, X., J. A. Conway, J. Kim, and J. C. Kappes. 1994. Localization of the Vpx packaging signal within the C terminus of the human immunodeficiency virus type 2 Gag precursor protein. J. Virol. 68:6161-6169.
48. Yao, X.-J., R. A. Subbramanian, N. Rougeau, F. Boisvert, D. Bergeron, and E. A. Cohen. 1995. Mutagenic analysis of human immunodeficiency virus type 1 Vpr: role of a predicted N-terminal alpha-helical structure in Vpr nuclear localization and virion incorporation. J. Virol. 69:7032-7044.
49. Zhou, Y., Y.-L. Lu, and L. Ratner. 1998. Arginine residues in the C-terminus of HIV-I vpr are important for nuclear localization and cell cycle arrest. Virology 242:414-424.