Site-directed mutagenesis of HIV-1 vpu gene demonstrates two clusters of replication-defective mutants with distinct ability to down-modulate cell surface CD4 and tetherin

Frontiers in Microbiology

Volumn 1, Issue NOV, 2010, Pages

  Nomaguchi, Masako ^a   Doi, Naoya ^a   Fujiwara, Sachi ^a   Fujita, Mikako ^b   Adachi, Akio ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

CD4; HIV 1; Replication; Tetherin; Vpu

Indexed keywords

EID: 84875337927     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2010.00116     Document Type: Article

References (43)

1. Adachi, A., Gendelman, H. E., Koenig, S., Folks, T., Willey, R., Rabson, A., and Martin, M. A. (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. Bour, S., Schubert, U., and Strebel, K. (1995). The human immunodeficiency virus type 1 Vpu protein specifically binds to the cytoplasmic domain of CD4: implications for the mechanism of degradation. J. Virol. 69, 1510-1520.
3. Bour, S., and Strebel K. (2003). The HIV-1 Vpu protein: a multifunctional enhancer of viral particle release. Microbes Infect. 5, 1029-1039.
4. Casartelli, N., Sourisseau, M., Feldmann, J., Guivel-Benhassine, F., Mallet, A., Marcelin, A. G., Guatelli, J., and Schwartz, O. (2010). Tetherin restricts productive HIV-1 cell-tocell transmission. PLoS Pathog. 6, e1000955. doi: 10.1371/journal. ppat.1000955.
5. Desrosiers, R. C. (2007). "Nonhuman Lentiviruses," in Fields Virology, 5th Edn, eds D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (Philadelphia: Lippincott Williams and Wilkins), 2215-2243.
6. Douglas, J. L., Gustin, J. K., Viswanathan, K., Mansouri, M., Moses, A. V., and Früh, K. (2010). The great escape: viral strategies to counter BST-2/ tetherin. PLoS Pathog. 6, e1000913. doi: 10.1371/journal.ppat.1000913.
7. Douglas, J. L., Viswanathan, K., McCarroll, M. N., Gustin, J. K., Früh, K., and Moses, A. V. (2009). Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a βTrCP-dependent mechanism. J. Virol. 83, 7931-7947.
8. Dubé, M., Roy, B. B., Guiot-Guillain, P., Binette, J., Mercier, J., Chiasson, A., and Cohen, E. A. (2010). Antagonism of tetherin restriction of HIV-1 release by Vpu involves binding and sequestration of the restriction factor in a perinuclear compartment. PLoS Pathog. 6, e1000856. doi: 10.1371/journal. ppat.1000856.
9. Dubé, M., Roy, B. B., Guiot-Guillain, P., Mercier, J., Binette, J., Leung, G., and Cohen, E. A. (2009). Suppression of tetherin-restricting activity upon human immunodeficiency virus type 1 particle release correlates with localization of Vpu in the trans-Golgi network. J. Virol. 83, 4574-4590.
10. Goffinet, C., Allespach, I., Homann, S., Tervo, H. M., Habermann, A., Rupp, D., Oberbremer, L., Kern, C., Tibroni, N., Welsch, S., Krijnse-Locker, J., Banting, G., Kräusslich, H. G., Fackler, O. T., and Keppler, O. T. (2009). HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor. Cell Host Microbe 5, 285-297.
11. Gummuluru, S., Kinsey, C. M., and Emerman, M. (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.
12. Iida, S., Fukumori, T., Oshima, Y., Koyama, A. H., and Adachi, A. (1999). Growth characteristics of T-cell tropic HIV-1 vpu gene mutants in human peripheral blood mononuclear cells. J. Med. Invest. 46, 43-47.
13. Iwabu, Y., Fujita, H., Kinomoto, M., Kaneko, K., Ishizaka, Y., Tanaka, Y., Sata, T., and Tokunaga, K. (2009). HIV-1 accessory protein Vpu internalizes cell-surface BST-2/tetherin through transmembrane interactions leading to lysosomes. J. Biol. Chem. 284, 35060-35072.
14. Kimpton, J., and Emerman, M. (1992). Detection of replication-competent and pseudotyped human immuno-deficiency virus with a sensitive cell line on the basis of activation of an integrated beta-galactosidase gene. J. Virol. 66, 2232-2239.
15. Kirchhoff, F. (2009). Is the high virulence of HIV-1 an unfortunate coincidence of primate lentiviral evolution? Nat. Rev. Microbiol. 7, 467-476.
16. Lebkowski, J. S., Clancy, S., and Calos, M. P. (1985). Simian virus 40 replication in adenovirus-transformed human cells antagonizes gene expression. Nature 317, 169-171.
17. Lenburg, M. E., and Landau, N. R. (1993). Vpu-induced degradation of CD4: requirement for specific amino acid residues in the cytoplasmic domain of CD4. J. Virol. 67, 7238-7245.
18. Levesque, K., Zhao, Y. S., and Cohen, E. A. (2003). Vpu exerts a positive effect on HIV-1 infectivity by down-modulating CD4 receptor molecules at the surface of HIV-1-producing cells. J. Biol. Chem. 278, 28346-28353.
19. Magadán, J. G., Pérez-Victoria, F. J., Sougrat, R., Ye, Y., Strebel, K., and Bonifacino, J. S. (2010). Multilayered mechanism of CD4 downregulation by HIV-1 Vpu involving distinct ER retention and ERAD targeting steps. PLoS Pathog. 6, e1000869. doi: 10.1371/journal.ppat.1000869.
20. Mangeat, B., Gers-Huber, G., Lehmann, M., Zufferey, M., Luban, J., and Piguet, V. (2009). HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its beta-TrCP2-dependent degradation. PLoS Pathog. 5, e1000574. doi: 10.1371/ journal.ppat.1000574.
21. + cell line H9. AIDS Res. Hum. Retroviruses 5, 253-255.
22. Margottin, F., Bour, S. P., Durand, H., Selig, L., Benichou, S., Richard, V., Thomas, D., Strebel, K., and Benarous, R. (1998). A novel human WD protein, h-beta TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1, 565-574.
23. Mitchell, R. S., Katsura, C., Skasko, M. A., Fitzpatrick, K., Lau, D., Ruiz, A., Stephens, E. B., Margottin-Goguet, F., Benarous, R., and Guatelli, J. C. (2009). Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking. PLoS Pathog. 5, e1000450. doi: 10.1371/journal.ppat.1000450.
24. Miyagi, E., Andrew, A. J., Kao, S., and Strebel, K. (2009). Vpu enhances HIV-1 virus release in the absence of Bst-2 cell surface down-modulation and intracellular depletion. Proc. Natl. Acad. Sci. U.S.A. 106, 2868-2873.
25. Neil, S. J., Sandrin, V., Sundquist, W. I., and Bieniasz, P. D. (2007). An interferon-alpha-induced tethering mechanism inhibits HIV-1 and Ebola virus particle release but is counteracted by the HIV-1 Vpu protein. Cell Host Microbe 2, 193-203.
26. Neil, S. J., Zang, T., and Bieniasz, P. D. (2008). Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425-430.
27. Nomaguchi, M., Fujita, M., and Adachi, A. (2008). Role of HIV-1 Vpu protein for virus spread and pathogenesis. Microbes Infect. 10, 960-967.
28. Paul, M., and Jabbar, M. A. (1997). Phosphorylation of both phosphoacceptor sites in the HIV-1 Vpu cytoplasmic domain is essential for Vpu-mediated ER degradation of CD4. Virology 232, 207-216.
29. Ruiz, A., Hill, M. S., Schmitt, K., Guatelli, J., and Stephens, E. B. (2008). Requirements of the membrane proximal tyrosine and dileucine-based sorting signals for efficient transport of the subtype C Vpu protein to the plasma membrane and in virus release. Virology 378, 58-68.
30. Sakai, H., Tokunaga, K., Kawamura, M., and Adachi, A. (1995). Function of human immunodeficiency virus type 1 Vpu protein in various cell types. J. Gen. Virol. 76, 2717-2722.
31. Sauter, D., Specht, A., and Kirchhoff, F. (2010). Tetherin: holding on and letting go. Cell 141, 392-398.
32. Schindler, M., Rajan, D., Banning, C., Wimmer, P., Koppensteiner, H., Iwanski, A., Specht, A., Sauter, D., Dobner, T., and Kirchhoff, F. (2010). Vpu serine 52 dependent counteraction of tetherin is required for HIV-1 replication in macrophages, but not in ex vivo human lymphoid tissue. Retrovirology 7, 1.
33. Schubert, U., Bour, S., Ferrer-Montiel, A. V., Montal, M., Maldarell, F., and Strebel, K. (1996). The two biological activities of human immunodeficiency virus type 1 Vpu protein involve two separable structural domains. J. Virol. 70, 809-819.
34. Schubert, U., and Strebel, K. (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.
35. Strebel, K., Klimkait, T., Maldarelli, F., and Martin, M. A. (1989). Molecular and biochemical analyses of human immunodeficiency virus type 1 vpu protein. J. Virol. 63, 3784-3791.
36. Tanaka, M., Ueno, T., Nakahara, T., Sasaki, K., Ishimoto, A., and Sakai, H. (2003). Downregulation of CD4 is required for maintenance of viral infectivity of HIV-1. Virology 311, 316-325.
37. Terwilliger, E. F., Cohen, E. A., Lu, Y. C., Sodroski, J. G., and Haseltine, W. A. (1989). Functional role of human immunodeficiency virus type 1 vpu. Proc. Natl. Acad. Sci. U.S.A. 86, 5163-5167.
38. Tiganos, E., Friborg, J., Allain, B., Daniel, N. G., Yao, X. J., and Cohen, E. A. (1998). Structural and functional analysis of the membrane-spanning domain of the human immunodeficiency virus type 1 Vpu protein. Virology 251, 96-107.
39. Tokarev, A., Skasko, M., Fitzpatrick, K., and Guatelli, J. (2009). Antiviral activity of the interferon-induced cellular protein BST-2/tetherin. AIDS Res. Hum. Retroviruses 25, 1197-1210.
40. Van Damme, N., Goff, D., Katsura, C., Jorgenson, R. L., Mitchell, R., Johnson, M. C., Stephens, E. B., and Guatelli, J. (2008). The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3, 245-252.
41. Wang, H., Sakurai, A., Khamsri, B., Uchiyama, T., Gu, H., Adachi, A., and Fujita M. (2005). Unique characteristics of HIV-1 Vif expression. Microbes Infect. 7, 385-390.
42. Willey, R. L., Smith, D. H., Lasky, L. A., Theodore, T. S., Earl, P. L., Moss, B., Capon, D. J., and Martin, M.A. (1988). In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J. Virol. 62, 139-147.
43. Yamashita, T., Kamada, K., Hatcho, K., Adachi, A., and Nomaguchi, M. (2008). Identification of amino acid residues in HIV-1 Vif critical for binding and exclusion of APOBEC3G/F. Microbes Infect. 10, 1142-1149.