Interaction between Ebola virus glycoprotein and host Toll-like receptor 4 leads to induction of proinflammatory cytokines and SOCS1

Journal of Virology

Volumn 84, Issue 1, 2010, Pages 27-33

  Atsushi, Okumura ^a   Pitha, Paula M ^b   Yoshimura, Akihiko ^c,d   Harty, Ronald N ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c KEIO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; VIRUS GLYCOPROTEIN;

ARTICLE; CELL STIMULATION; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOKINE PRODUCTION; EBOLA VIRUS; EMBRYO; HOST; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IMMUNOPRECIPITATION; INNATE IMMUNITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; VIRUS INFECTION; VIRUS PARTICLE; WESTERN BLOTTING;

CELL LINE; CYTOKINES; EBOLAVIRUS; GLYCOPROTEINS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; MONOCYTES; NF-KAPPA B; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TOLL-LIKE RECEPTOR 4; TRANSCRIPTIONAL ACTIVATION; VIRAL PROTEINS; VIRION;

EBOLA VIRUS;

EID: 72849134026     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01462-09     Document Type: Article

References (34)

1. Basler, C. F., A. Mikulasova, L. Martinez-Sobrido, J. Paragas, E. Muhlberger, M. Bray, H. D. Klenk, P. Palese, and A. Garcia-Sastre. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956.
2. Bosio, C. M., B. D. Moore, K. L. Warfield, G. Ruthel, M. Mohamadzadeh, M. J. Aman, and S. Bavari. 2004. Ebola and Marburg virus-like particles activate human myeloid dendritic cells. Virology 326:280-287. (Pubitemid 39078259)
3. Bray, M., and T. W. Geisbert. 2005. Ebola virus: the role of macrophages and dendritic cells in the pathogenesis of Ebola hemorrhagic fever. Int. J. Biochem. Cell Biol. 37:1560-1566.
4. Burzyn, D., J. C. Rassa, D. Kim, I. Nepomnaschy, S. R. Ross, and I. Piazzon. 2004. Toll-like receptor 4-dependent activation of dendritic cells by a retrovirus. J. Virol. 78:576-584. (Pubitemid 38067579)
5. Cardenas, W. B., Y. M. Loo, M. Gale, Jr., A. L. Hartman, C. R. Kimberlin, L. Martinez-Sobrido, E. O. Saphire, and C. F. Basler. 2006. Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J. Virol. 80:5168-5178.
6. Divanovic, S., A. Trompette, S. F. Atabani, R. Madan, D. T. Golenbock, A. Visintin, R. W. Finberg, A. Tarakhovsky, S. N. Vogel, Y. Belkaid, E. A. Kurt-Jones, and C. L. Karp. 2005. Negative regulation of Toll-like receptor 4 signaling by the Toll-like receptor homolog RP105. Nat. Immunol. 6:571-578.
7. Feldmann, H., H. Bugany, F. Mahner, H. D. Klenk, D. Drenckhahn, and H. J. Schnittler. 1996. Filovirus-induced endothelial leakage triggered by infected monocytes/macrophages. J. Virol. 70:2208-2214. (Pubitemid 26087581)
8. Georgel, P., Z. Jiang, S. Kunz, E. Janssen, J. Mols, K. Hoebe, S. Bahram, M. B. Oldstone, and B. Beutler. 2007. Vesicular stomatitis virus glycoprotein G activates a specific antiviral Toll-like receptor 4-dependent pathway. Virology 362:304-313. (Pubitemid 46678142)
9. Harty, R. N., M. E. Brown, G. Wang, J. Huibregtse, and F. P. Hayes. 2000. A PPxY motif within the VP40 protein of Ebola virus interacts physically and functionally with a ubiquitin ligase: implications for filovirus budding. Proc. Natl. Acad. Sci. U.S.A. 97:13871-13876.
10. Haynes, L. M., D. D. Moore, E. A. Kurt-Jones, R. W. Finberg, L. J. Anderson, and R. A. Tripp. 2001. Involvement of Toll-like receptor 4 in innate immunity to respiratory syncytial virus. J. Virol. 75:10730-10737.
11. Johnston, J. A. 2004. Are SOCS suppressors, regulators, and degraders? J. Leukoc. Biol. 75:743-748.
12. Kaletsky, R. L., J. R. Francica, C. Agrawal-Gamse, and P. Bates. 2009. Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 106:2886-2891.
13. Kawai, T., O. Takeuchi, T. Fujita, J. Inoue, P. F. Muhlradt, S. Sato, K. Hoshino, and S. Akira. 2001. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J. Immunol. 167:5887-5894. (Pubitemid 33062783)
14. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. J. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1:398-401.
15. Licata, J. M., R. F. Johnson, Z. Han, and R. N. Harty. 2004. Contribution of Ebola virus glycoprotein, nucleoprotein, and VP24 to budding of VP40 virus-like particles. J. Virol. 78:7344-7351.
16. Licata, J. M., M. Simpson-Holley, N. T. Wright, Z. Han, J. Paragas, and R. N. Harty. 2003. Overlapping motifs (PTAP and PPEY) within the Ebola virus VP40 protein function independently as late budding domains: involvement of host proteins TSG101 and VPS-4. J. Virol. 77:1812-1819.
17. Lizundia, R., K. S. Sauter, G. Taylor, and D. Werling. 2008. Host species-specific usage of the TLR4-LPS receptor complex. Innate Immun. 14:223-231.
18. Martinez, O., C. Valmas, and C. F. Basler. 2007. Ebola virus-like particle-induced activation of NF-kappaB and Erk signaling in human dendritic cells requires the glycoprotein mucin domain. Virology 364:342-354. (Pubitemid 46873712)
19. Muzio, M., N. Polentarutti, D. Bosisio, M. K. Prahladan, and A. Mantovani. 2000. Toll-like receptors: a growing family of immune receptors that are differentially expressed and regulated by different leukocytes. J. Leukoc. Biol. 67:450-456.
20. Nishi, M., A. Ryo, N. Tsurutani, K. Ohba, T. Sawasaki, R. Morishita, K. Perrem, I. Aoki, Y. Morikawa, and N. Yamamoto. 2009. Requirement for microtubule integrity in the SOCS1-mediated intracellular dynamics of HIV-1 Gag. FEBS Lett. 583:1243-1250.
21. Okumura, A., P. M. Pitha, and R. N. Harty. 2008. ISG15 inhibits Ebola VP40 VLP budding in an L-domain-dependent manner by blocking Nedd4 ligase activity. Proc. Natl. Acad. Sci. U.S.A. 105:3974-3979.
22. Rassa, J. C., J. L. Meyers, Y. Zhang, R. Kudaravalli, and S. R. Ross. 2002. Murine retroviruses activate B cells via interaction with Toll-like receptor 4. Proc. Natl. Acad. Sci. U.S.A. 99:2281-2286.
23. Reid, S. P., L. W. Leung, A. L. Hartman, O. Martinez, M. L. Shaw, C. Carbonnelle, V. E. Volchkov, S. T. Nichol, and C. F. Basler. 2006. Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation. J. Virol. 80:5156-5167.
24. Rothlin, C. V., S. Ghosh, E. I. Zuniga, M. B. Oldstone, and G. Lemke. 2007. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 131:1124-1136. (Pubitemid 350235020)
25. Ryo, A., N. Tsurutani, K. Ohba, R. Kimura, J. Komano, M. Nishi, H. Soeda, S. Hattori, K. Perrem, M. Yamamoto, J. Chiba, J. Mimaya, K. Yoshimura, S. Matsushita, M. Honda, A. Yoshimura, T. Sawasaki, I. Aoki, Y. Morikawa, and N. Yamamoto. 2008. SOCS1 is an inducible host factor during HIV-1 infection and regulates the intracellular trafficking and stability of HIV-1 Gag. Proc. Natl. Acad. Sci. U.S.A. 105:294-299.
26. Shimojima, M., A. Takada, H. Ebihara, G. Neumann, K. Fujioka, T. Irimura, S. Jones, H. Feldmann, and Y. Kawaoka. 2006. Tyro3 family-mediated cell entry of Ebola and Marburg viruses. J. Virol. 80:10109-10116. (Pubitemid 44522604)
27. Simmons, G., A. J. Rennekamp, N. Chai, L. H. Vandenberghe, J. L. Riley, and P. Bates. 2003. Folate receptor alpha and caveolae are not required for Ebola virus glycoprotein-mediated viral infection. J. Virol. 77:13433-13438. (Pubitemid 37494340)
28. Strong, J. E., G. Wong, S. E. Jones, A. Grolla, S. Theriault, G. P. Kobinger, and H. Feldmann. 2008. Stimulation of Ebola virus production from persistent infection through activation of the Ras/MAPK pathway. Proc. Natl. Acad. Sci. U.S.A. 105:17982-17987.
29. Takada, A., C. Robison, H. Goto, A. Sanchez, K. G. Murti, M. A. Whitt, and Y. Kawaoka. 1997. A system for functional analysis of Ebola virus glycoprotein. Proc. Natl. Acad. Sci. U.S.A. 94:14764-14769.
30. Takada, A., S. Watanabe, H. Ito, K. Okazaki, H. Kida, and Y. Kawaoka. 2000. Downregulation of beta1 integrins by Ebola virus glycoprotein: implication for virus entry. Virology 278:20-26. (Pubitemid 32002589)
31. Wahl-Jensen, V., S. K. Kurz, P. R. Hazelton, H. J. Schnittler, U. Stroher, D. R. Burton, and H. Feldmann. 2005. Role of Ebola virus secreted glycoproteins and virus-like particles in activation of human macrophages. J. Virol. 79:2413-2419. (Pubitemid 40204596)
32. Warfield, K. L., C. M. Bosio, B. C. Welcher, E. M. Deal, M. Mohamadzadeh, A. Schmaljohn, M. J. Aman, and S. Bavari. 2003. Ebola virus-like particles protect from lethal Ebola virus infection. Proc. Natl. Acad. Sci. U.S.A. 100:15889-15894.
33. Wool-Lewis, R. J., and P. Bates. 1998. Characterization of Ebola virus entry by using pseudotyped viruses: identification of receptor-deficient cell lines. J. Virol. 72:3155-3160.
34. Yoshimura, A., T. Naka, and M. Kubo. 2007. SOCS proteins, cytokine signalling and immune regulation. Nat. Rev. Immunol. 7:454-465.