HIV-1 Vpu accessory protein induces caspase-mediated cleavage of IRF3 transcription factor

Journal of Biological Chemistry

Volumn 289, Issue 51, 2014, Pages 35102-35110

  Park, Sang Yoon ^a   Waheed, Abdul A ^b   Zhang, Zai Rong ^a   Freed, Eric O ^b   Bonifacino, Juan S ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL DEATH; CELLS; CYTOLOGY; DISEASES; GLYCOPROTEINS; PROTEINS; T-CELLS; TRANSCRIPTION; TRANSCRIPTION FACTORS; VIRUSES;

ANTIVIRAL RESPONSE; C-TERMINAL FRAGMENTS; DNA BINDING DOMAIN; INTERFERON REGULATORY FACTOR 3; PROTEOLYTIC CLEAVAGE; TRANSACTIVATION DOMAIN; TRANSCRIPTIONAL ACTIVITY; VESICULAR STOMATITIS VIRUS;

MOLECULAR BIOLOGY;

CASPASE; INTERFERON REGULATORY FACTOR 3; VIF PROTEIN; VPR PROTEIN; VPU PROTEIN; G PROTEIN, VESICULAR STOMATITIS VIRUS; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; IRF3 PROTEIN, HUMAN; MEMBRANE PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; VIF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; VIRAL PROTEIN; VIRUS ENVELOPE PROTEIN; VPR PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; VPU PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTIVIRAL SUSCEPTIBILITY; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; DNA BINDING MOTIF; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE INACTIVATION; HOST CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; VIRUS STRAIN; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; IMMUNOBLOTTING; JURKAT CELL LINE; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN DEGRADATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; VESICULAR STOMATITIS VIRUS;

APOPTOSIS; CASPASES; HEK293 CELLS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; IMMUNOBLOTTING; INTERFERON REGULATORY FACTOR-3; JURKAT CELLS; MEMBRANE GLYCOPROTEINS; MUTATION; POLY(ADP-RIBOSE) POLYMERASES; PROTEOLYSIS; TRANSFECTION; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; VIRAL ENVELOPE PROTEINS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84919388383     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.597062     Document Type: Article

References (43)

1. Dubé, M., Bego, M. G., Paquay, C., and Cohen, É. A. (2010) Modulation of HIV-1-host interaction: role of the Vpu accessory protein. Retrovirology 7, 114
2. Willey, R. L., Maldarelli, F., Martin, M. A., and Strebel, K. (1992) Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4. J. Virol. 66, 7193-7200
3. 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
4. Zhang, Z. R., Bonifacino, J. S., and Hegde, R. S. (2013) Deubiquitinases sharpen substrate discrimination during membrane protein degradation from the ER. Cell 154, 609-622
5. 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
6. 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
7. Galão, R. P., Le Tortorec, A., Pickering, S., Kueck, T., and Neil, S. J. (2012) Innate sensing of HIV-1 assembly by Tetherin induces NFκB-dependent proinflammatory responses. Cell Host Microbe 12, 633-644
8. 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 β-TrCP and endo-lysosomal trafficking. PLoS Pathog. 5, e1000450
9. 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
10. Shah, A. H., Sowrirajan, B., Davis, Z. B., Ward, J. P., Campbell, E. M., Planelles, V., and Barker, E. (2010) Degranulation of natural killer cells following interaction with HIV-1-infected cells is hindered by downmodulation of NTB-A by Vpu. Cell Host Microbe 8, 397-409
11. Matusali, G., Potestà, M., Santoni, A., Cerboni, C., and Doria, M. (2012) The human immunodeficiency virus type 1 Nef and Vpu proteins downregulate the natural killer cell-activating ligand PVR. J. Virol. 86, 4496-4504
12. Moll, M., Andersson, S. K., Smed-Sörensen, A., and Sandberg, J. K. (2010) Inhibition of lipid antigen presentation in dendritic cells by HIV-1 Vpu interference with CD1d recycling from endosomal compartments. Blood 116, 1876-1884
13. Taniguchi, T., Ogasawara, K., Takaoka, A., and Tanaka, N. (2001) IRF family of transcription factors as regulators of host defense. Annu. Rev. Immunol. 19, 623-655
14. Ockenhouse, C. F., Bernstein, W. B., Wang, Z., and Vahey, M. T. (2005) Functional genomic relationships in HIV-1 disease revealed by gene-expression profiling of primary human peripheral blood mononuclear cells. J. Infect. Dis. 191, 2064-2074
15. Harman, A. N., Lai, J., Turville, S., Samarajiwa, S., Gray, L., Marsden, V., Mercier, S. K., Jones, K., Nasr, N., Rustagi, A., Cumming, H., Donaghy, H., Mak, J., Gale, M., Jr., Churchill, M., Hertzog, P., and Cunningham, A. L. (2011) HIV infection of dendritic cells subverts the IFN induction pathway via IRF-1 and inhibits type 1 IFN production. Blood 118, 298-308
16. Okumura, A., Alce, T., Lubyova, B., Ezelle, H., Strebel, K., and Pitha, P. M. (2008) HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation. Virology 373, 85-97
17. Doehle, B. P., Chang, K., Rustagi, A., McNevin, J., McElrath, M. J., and Gale, M., Jr. (2012) Vpu mediates depletion of interferon regulatory factor 3 during HIV infection by a lysosome-dependent mechanism. J. Virol. 86, 8367-8374
18. Hotter, D., Kirchhoff, F., and Sauter, D. (2013) HIV-1 Vpu does not degrade interferon regulatory factor 3. J. Virol. 87, 7160-7165
19. Nguyen, K. L., llano, M., Akari, H., Miyagi, E., Poeschla, E. M., Strebel, K., and Bour, S. (2004) Codon optimization of the HIV-1 vpu and vif genes stabilizes their mRNA and allows for highly efficient Rev-independent expression. Virology 319, 163-175
20. Schaeffer, E., Geleziunas, R., and Greene, W. C. (2001) Human immunodeficiency virus type 1 Nef functions at the level of virus entry by enhancing cytoplasmic delivery of virions. J. Virol. 75, 2993-3000
21. 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
22. Klimkait, T., Strebel, K., Hoggan, M. D., Martin, M. A., and Orenstein, J. M. (1990) The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. J. Virol. 64, 621-629
23. Freed, E. O., Englund, G., and Martin, M. A. (1995) Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection. J. Virol. 69, 3949-3954
24. + T cells and macrophages. J. Virol. 87, 444-453
25. Yee, J. K., Friedmann, T., and Burns, J. C. (1994) Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol. 43, 99-112
26. 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-β TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1, 565-574
27. Magadán, J. G., and Bonifacino, J. S. (2012) Transmembrane domain determinants of CD4 downregulation by HIV-1 Vpu. J. Virol. 86, 757-772
28. Sears, N., Sen, G. C., Stark, G. R., and Chattopadhyay, S. (2011) Caspase-8-mediated cleavage inhibits IRF-3 protein by facilitating its proteasome-mediated degradation. J. Biol. Chem. 286, 33037-33044
29. Akari, H., Bour, S., Kao, S., Adachi, A., and Strebel, K. (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
30. Verma, S., Ali, A., Arora, S., and Banerjea, A. C. (2011) Inhibition of β-TrcP-dependent ubiquitination of p53 by HIV-1 Vpu promotes p53-mediated apoptosis in human T cells. Blood 117, 6600-6607
31. Casella, C. R., Rapaport, E. L., and Finkel, T. H. (1999) Vpu increases susceptibility of human immunodeficiency virus type 1-infected cells to Fas killing. J. Virol. 73, 92-100
32. Yoneyama, M., Suhara, W., Fukuhara, Y., Sato, M., Ozato, K., and Fujita, T. (1996) Autocrine amplification of type I interferon gene expression mediated by interferon stimulated gene factor 3 (ISGF3). J. Biochem. 120, 160-169
33. Hiscott, J. (2007) Triggering the innate antiviral response through IRF-3 activation. J. Biol. Chem. 282, 15325-15329
34. Li, Y., Hu, X., Song, Y., Lu, Z., Ning, T., Cai, H., and Ke, Y. (2011) Identification of novel alternative splicing variants of interferon regulatory factor 3. Biochim. Biophys. Acta 1809, 166-175
35. Bour, S., Perrin, C., Akari, H., and Strebel, K. (2001) The human immunodeficiency virus type 1 Vpu protein inhibits NF-κB activation by interfering with βTrCP-mediated degradation of IκB. J. Biol. Chem. 276, 15920-15928
36. Gougeon, M. L. (2003) Apoptosis as an HIV strategy to escape immune attack. Nat. Rev. Immunol. 3, 392-404
37. Sastry, K. J., Marin, M. C., Nehete, P. N., McConnell, K., el-Naggar, A. K., and McDonnell, T. J. (1996) Expression of human immunodeficiency virus type I tat results in down-regulation of bcl-2 and induction of apoptosis in hematopoietic cells. Oncogene 13, 487-493
38. Jacotot, E., Ravagnan, L., Loeffler, M., Ferri, K. F., Vieira, H. L., Zamzami, N., Costantini, P., Druillennec, S., Hoebeke, J., Briand, J. P., Irinopoulou, T., Daugas, E., Susin, S. A., Cointe, D., Xie, Z. H., Reed, J. C., Roques, B. P., and Kroemer, G. (2000) The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J. Exp. Med. 191, 33-46
39. Best, S. M., and Bloom, M. E. (2004) Caspase activation during virus infection: more than just the kiss of death? Virology 320, 191-194
40. Barral, P. M., Morrison, J. M., Drahos, J., Gupta, P., Sarkar, D., Fisher, P. B., and Racaniello, V. R. (2007) MDA-5 is cleaved in poliovirus-infected cells. J. Virol. 81, 3677-3684
41. McCune, J. M. (2001) The dynamics of CD4+ T-cell depletion in HIV disease. Nature 410, 974-979
42. + T cells. Nature 417, 95-98
43. Garcia, S., Fevrier, M., Dadaglio, G., Lecoeur, H., Riviere, Y., and Gougeon, M. L. (1997) Potential deleterious effect of anti-viral cytotoxic lymphocyte through the CD95 (FAS/APO-1)-mediated pathway during chronic HIV infection. Immunol. Lett. 57, 53-58