The Vpu protein of human immunodeficiency virus type 1 plays a protective role against virus-induced apoptosis in primary CD4+ T lymphocytes

Journal of Virology

Volumn 77, Issue 19, 2003, Pages 10304-10313

  Komoto, Satoshi ^a,b   Tsuji, Shoutaro ^a   Ibrahim, Madiha S ^a   Li, Yong Gang ^a   Warachit, Jiranan ^a   Taniguchi, Koki ^b   Ikuta, Kazuyoshi ^a  

^a OSAKA UNIVERSITY   (Japan)

^b FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

VPU PROTEIN;

APOPTOSIS; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; CULTURE MEDIUM; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; T LYMPHOCYTE; VIRUS ISOLATION;

AMINO ACID SEQUENCE; APOPTOSIS; BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; GENE PRODUCTS, VPU; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; VIRUS REPLICATION;

EID: 0141521644     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.19.10304-10313.2003     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 retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
2. Akari, H., S. Bour, S. Kao, A. Adachi, and K. Strebel. 2001. The human immunodeficiency virus type 1 accessory protein Vpu induces apoptosis by suppressing the nuclear factor κB-dependent expression of antiapoptotic factors. J. Exp. Med. 194:1299-1311.
3. Auwanit, W., T. Mukai, P. I. N. Ayuthaya, T. Kurata, and K. Ikuta. 2001. Full-length sequences of two subtype E HIV-1 isolates from 1995 samples of patients with sexually transmitted diseases in Thailand. AIDS Res. Hum. Retrovir. 17:867-871.
4. Badley, A. D., A. A. Pilon, A. Landay, and D. H. Lynch. 2000. Mechanisms of HIV-associated lymphocyte apoptosis. Blood 96:2951-2964.
5. Banda, N. K., J. Bernier, D. K. Kurahara, R. Kurrle, N. Haiwood, R. P. Sekaly, and T. H. Finkel. 1992. Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J. Exp. Med. 176:1099-1106.
6. Bartz, S. R., and M. Emerman. 1999. Human immunodeficiency virus type 1 Tat induces apoptosis and increases sensitivity to apoptotic signals by upregulating ELICE/caspase-8. J. Virol. 73:1956-1963.
7. Biard-Piechaczyk, M., V. Robert-Hebmann, V. Richard, J. Ronald, R. A. Hipskind, and C. Devaux. 2000. Caspase-dependent apoptosis of cells expressing the chemokine receptor CXCR4 is induced by cell membrane-associated human immunodeficiency virus type 1 envelope glycoprotein (gp120). Virology 268:329-344.
8. + T-cell lines caused by human immunodeficiency virus type 1 does not depend on caspase or apoptosis. J. Virol. 76:5094-5107.
9. Bour, S., U. Schubert, and K. Strebel. 1995. The human immunodeficiency virus type 1 Vpu protein specifically binds to the cytoplasmic domain of CD4: implication for the mechanism of degradation. J. Virol. 69:1510-1520.
10. Casélla, C. R., E. L. Rapaport, and T. H. Finkel. 1999. Vpu increases susceptibility of human immunodeficiency virus type 1-infected cells to Fas killing. J. Virol. 73:92-100.
11. Conti, L., P. Matarrese, B. Varano, M. C. Gauzzi, A. Sato, W. Malorni, F. Belardelli, and S. Gessani. 2000. Dual role of the HIV-1 vpr protein in the modulation of the apoptotic response of T cells. J. Immunol. 165:3293-3300.
12. Ewart, G. D., T. Sutherland, P. W. Gage, and G. B. Cox. 1996. The Vpu protein of human immunodeficiency virus type 1 forms cation-selective ion channels. J. Virol. 70:7108-7115.
13. Fauci, A. S. 1988. The human immunodeficiency virus: infectivity and mechanisms of pathogenesis. Science 239:617-622.
14. Genini, D., D. Sheeter, S. Rought, J. J. Zaunders, S. A. Susin, G. Kroemer, D. D. Richman, D. A. Carson, J. Corbell, and J. M. Leoni. 2001. HIV induces lymphocyte apoptosis by a p53-initiated, mitochondrial-mediated mechanism. FASEB J. 15:5-6.
15. Gibellini, D., A. Caputo, C. Celeghini, A. Bassini, M. La Placa, S. Capitani, and G. Zauli. 1995. Tat-expressing Jurkat cells show an increased resistance to different apoptotic stimuli, including acute human immunodeficiency virus-type 1 (HIV-1) infection. Br. J. Haematol. 89:24-33.
16. Göttlinger, H. G., T. Dorfman, E. A. Cohen, and W. A. Haseltine. 1993. Vpu protein of human immunodeficiency virus type 1 enhances the release of capsids produced by gag gene constructs of widely divergent retroviruses. Proc. Natl. Acad. Sci. USA 90:7381-7385.
17. Gummuluru, S., C. M. Kinsey, and M. Emerman. 2000. An in vitro rapid-turnover assay for human immunodeficiency virus type 1 replication selects for cell-to-cell spread of virus. J. Virol. 74:10882-10891.
18. + T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature 395:189-194.
19. Ho, D. D., A. U. Neumann, A. S. Perelson, W. Chen, J. M. Leonard, and M. Markowitz. 1995. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373:123-126.
20. + produce interleukin-4 which contributes to enhanced replication of T-tropic human immunodeficiency virus type 1. Virology 293:94-102.
21. Huet, T., R. Cheynier, A. Meyerhans, G. Roelants, and S. Wain-Hobson. 1990. Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature 345:356-359.
22. Ikuta, K., M. Kameoka, and R. B. Luftig. 1997. AIDS pathogenesis: the role of accessory gene mutations, leading to formation of long-lived persistently infected cells and/or apoptosis-inducing HIV-1 particles. Virus Res. 52:145-156.
23. Ikuta, K., S. Suzuki, H. Horikoshi, T. Mukai, and R. B. Luftig. 2000. Positive and negative aspects of the human immunodeficiency virus protease: development of inhibitors versus its role in AIDS pathogenesis. Microbiol. Mol. Biol. Rev. 64:725-745.
24. Kameoka, M., T. Kimura, Y. H. Zheng, S. Suzuki, K. Fujinaga, R. B. Luftig, and K. Ikuta. 1997. Protease-defective, gp120-containing human immunodeficiency virus type 1 particles induce apoptosis more efficiently than does wild-type virus or recombinant gp120 protein in healthy donor-derived peripheral blood T cells. J. Clin. Microbiol. 35:41-47.
25. Kishi, M., Y. Nishino, M. Sumiya, K. Ohki, T. Kimura, T. Goto, M. Nakai, M. Kakinuma, and K. Ikuta. 1992. Cells surviving infection by human immunodeficiency virus type 1: vif and vpu mutants produce non-infectious or markedly less cytopathic viruses. J. Gen. Virol. 73:77-87.
26. Klimkait, T., K. Strebel, M. D. Hoggan, M. A. Martin, and J. M. Orenstein. 1990. The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. J. Virol. 64:621-629.
27. + T cells is variable among primary isolates of human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 18:435-446.
28. Lamb, R. A., and L. H. Pinto. 1997. Do Vpu and Vpr of human immunodeficiency virus type 1 and NB of influenza B virus have ion channel activities in the virus life cycles? Virology 229:1-11.
29. + T lymphocytes by human immunodeficiency virus type 1 appears necrotic rather than apoptotic and does not require env. J. Virol. 76:5082-5093.
30. Li, C. J., D. J. Friedman, C. Wang, V. Metelev, and A. B. Pardee. 1995, Induction of apoptosis in uninfected lymphocytes by HIV-1 Tat protein. Science 268:429-431.
31. Li, J. T., M. Halloran, C. I. Lord, A. Watson, J. Ranchalis, M. Fung, N. L. Letvin, and J. G. Sodroski. 1995. Persistent infection of macaques with simian-human immunodeficiency viruses. J. Virol. 69:7061-7071.
32. + cells expressing gp160 of human immunodeficiency virus type 1. J. Virol. 68:390-399.
33. Mackay, G. A., Y. Niu, Z. Q. Liu, S. Mukherjee, Z. Li, I. Adany, S. Buch, W. Zhuge, H. M. McClure, O. Narayan, and M. S. Smith. 2002. Presence of intact vpu and nef genes in nonpathogenic SHIV is essential for acquisition of pathogenicity of this virus by serial passage in macaques. Virology 295:133-146.
34. Maddarelli, F., M.-Y. Chen, R. L. Wiley, and K. Strebel. 1993. Human immunodeficiency virus type 1 Vpu protein is an oligomeric type 1 integral membrane protein. J. Virol. 67:5056-5061.
35. McCloskey, T. W., M. Ott, E. Tribble, S. A. Khan, S. Teichberg, M. O. Paul, S. Pahwa, E. Verdin, and N. Chirmule. 1997. Dual role of HIV Tat in regulation of apoptosis in T cells. J. Immunol. 158:1014-1019.
36. + T cell loss and neuro-AIDS in pig-tailed macaques. Virology 272:112-126.
37. McCormick-Davis, C., L.-J. Zhao, S. Mukherjee, K. Leung, D. Sheffer, S. V. Joag, O. Narayan, and E. B. Stephens. 1998. Chronology of genetic changes in the vpu, env, and nef genes in chimeric simian-human immunodeficiency virus (strain HXB2) during acquisition of virulence for pig-tailed macaques. Virology 248:275-283.
38. Oyaizu, N., T. W. McCloskey, S. Than, R. Hu, V. S. Kalyanaraman, and S. Pahwa. 1994. Cross-linking of CD4 molecules upregulates Fas antigen expression in lymphocytes by inducing interferon-γ and tumor necrosis factor-α secretion. Blood 84:2622-2631.
39. Patki, A. H., and M. N. Lederman. 1996. HIV-1 Tat protein and its inhibitor Ro 24-7429 inhibit lymphocyte proliferation and induce apoptosis in peripheral blood mononuclear cells from healthy donors. Cell. Immunol. 169:40-46.
40. Paul, M., S. Mazumder, N. Raja, and M. A. Jabbar. 1998. Mutational analysis of the human immunodeficiency virus type 1 Vpu transmembrane domain that promotes the enhanced release of virus-like particles from the plasma membrane of mammalian cells. J. Virol. 72:1270-1279.
41. Perelson, A. S., A. U. Neumann, M. Markowitz, J. M. Leopard, and D. D. Ho. 1996. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271:1582-1586.
42. Purvis, S. F., J. W. Jacobberger, R. M. Sramkoski, A. H. Patki, and M. M. Lederman. 1995. HIV type 1 Tat protein induces apoptosis and death in Jurkat cells. AIDS Res. Hum. Retrovir. 11:443-450.
43. Raja, N. U., and M. A. Jabbar. 1996. The human immunodeficiency virus type 1 Vpu protein tethered to the CD4 extracellular domain is localized to the plasma membrane and is biologically active in the secretory pathway of mammalian cells: implications for the mechanisms of Vpu function. Virology 220:141-151.
44. Rapaport, E., C. R. Casella, D. Iklé, F. Mustafa, D. Isaak, and T. H. Finkel. 1998. Mapping of HIV-1 determinants of apoptosis in infected cells. Virology 252:407-417.
45. Rasola, A., D. Gramaglia, C. Boccaccio, and P. M. Comoglio. 2001. Apoptosis enhancement by the HIV-1 Nef protein. J. Immunol. 166:81-88.
46. Roggero, R., V. Robert-Hebmann, S. Harrington, J. Ronald, L. Vergne, S. Jaleco, C. Devaux, and M. Biard-Piechaczyk. 2001. Binding of human immunodeficiency virus type 1 gp120 to CXCR4 induces mitochondrial transmembrane depolarization and cytochrome c-mediated apoptosis independently of Fas signaling. J. Virol. 75:7637-7650.
47. + cells expressing gp160 of HIV. Virology 224:18-24.
48. Sastry, K. J., M. C. Marin, P. N. Nehete, K. McConnell, A. K. el-Naggar, and T. J. McDonnell. 1996. Expression of human immunodeficiency virus type 1 tat results in down-regulation of bcl-2 and induction of apoptosis in hematopoietic cells. Oncogene 13:487-493.
49. Schubert, U., and K. Strebel. 1994. Differential activities of the human immunodeficiency virus type 1-encoded Vpu protein are regulated by phosphorylation and occur in different cellular compartments. J. Virol. 68:2260-2271.
50. Schubert, U., S. Bour, A. V. Ferrer-Montiel, M. Montal, F. Maldarell, and K. Strebel, 1996. The two biological activities of human immunodeficiency virus type 1 Vpu protein involve two separable structural domains. J. Virol. 70:809-819.
51. Schubert, U., K. A. Clouse, and K. Strebel. 1995. Augmentation of virus secretion by the human immunodeficiency virus type 1 Vpu protein is cell type independent and occurs in cultured human primary macrophages and lymphocytes. J. Virol. 69:7699-7711.
52. Schubert, U., A. V. Ferrer-Montiel, M. Oblatt-Montal, P. Henklein, K. Strebel, and M. Montal. 1996. Identification of an ion channel activity of the Vpu transmembrane domain and its involvement in the regulation of virus release from HV-1-infected cells. FEBS Lett. 398:12-18.
53. Schubert, U., P. Henklein, B. Boldyreff, E. Wingender, K. Strebel, and T. Porstmann. 1994. The human immunodeficiency virus type 1 encoded Vpu protein is phosphorylated by casein kinase-2 (CK-2) at positions Ser52 and Ser56 within a predicted alpha-helix-turn-alpha-helix-motif. J. Mol. Biol. 236:16-25.
54. Schubert, U., T. Schneider, P. Henklein, K. Hoffmann, E. Berthold, H. Hauser, G. Pauli, and T. Porstmann. 1992. Human-immunodeficiency-virus-type-1-encoded Vpu protein is phosphorylated by casein kinase II. Eur. J. Biochem. 204:875-883.
55. Schwartz, M. D., R. J. Geraghty, and A. T. Panganiban. 1996. HIV-1 particle release mediated by Vpu is distinct from that mediated by p6. Virology 224:302-309.
56. Stewart, S. A., B. Poon, J. B. Jowett, and I. S. Chen. 1997. Human immunodeficiency virus type 1 Vpr induces apoptosis following cell cycle arrest. J. Virol. 71:5579-5592.
57. Stewart, S. A., B. Poon, J. B. Jowett, Y. Xie, and I. S. Chen. 1999. Lentiviral delivery of HIV-1 Vpr protein induces apoptosis in transformed cells. Proc. Natl. Acad. Sci. USA 96:12039-12043.
58. Stewart, S. A., B. Poon, J. Y. Song, and I. S. Chen. 2000. Human immunodeficiency virus type 1 vpr induces apoptosis through caspase activation. J. Virol. 74:3105-3111.
59. Strebel, K., T. Klimkait, F. Maldarelli, and M. A. Martin. 1989. Molecular and biochemical analyses of human immunodeficiency virus type 1 Vpu protein. J. Virol. 63:3784-3791.
60. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
61. Venkat, R. K. Y., M. Husain, A. Horodner, and N. Ahmad. 2001. Molecular characterization of HIV type 1 vpu genes from mothers and infants after perinatal transmission. AIDS Res. Hum. Retrovir. 17:1089-1098.
62. Vincent, M. J., and M. A. Jabbar. 1995. The human immunodeficiency virus type 1 Vpu protein: a potential regulator of proteolysis and protein transport in the mammalian secretory pathway. Virology 213:639-649.
63. Wei, X., S. K. Ghosh, V. A. Johnson, E. A. Emini, P. Deutsch, J. D. Lifson, S. Bonhoeffer, M. A. Nowak, B. H. Hahn, M. S. Saag, and G. M. Shaw. 1995. Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373:117-122.
64. Westendorp, M. O., R. Frank, C. Ochsenbauer, K. Stricker, J. Dhein, H. Walczak, K. M. Debatin, and P. H. Krammer. 1995. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375:497-500.
65. Willey, R. L., F. Maldarelli, M. A. Martin, and K. Strebel. 1992. Human immunodeficiency virus type Vpu protein regulates the formation of intracellular gp160-CD4 complexes. J. Virol. 66:226-234.
66. Willey, R. L., F. Maldarelli, M. A. Martin, and K. Strebel. 1992. Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J. Virol. 66:7193-7200.
67. Yao, X. J., H. Göttlinger, W. A. Haseltine, and E. A. Cohen. 1992. Envelope glycoprotein and CD4 independence of vpu-facilitated human immunodeficiency virus type 1 capsid export. J. Virol. 66:5119-5126.
68. Zauli, G., D. Gibellini, P. Secchiero, H. Dutartre, D. Olive, S. Capitani, and Y. Collette. 1999. Human immunodeficiency virus type 1 Nef protein sensitizes CD4 (+) T lymphoid cells to apoptosis via functional upregulation of the CD95/CD95 ligand pathway. Blood 93:1000-1010.