Viral cell death inhibitor MC159 enhances innate immunity against vaccinia virus infection

Journal of Virology

Volumn 84, Issue 20, 2010, Pages 10467-10476

  Challa, Sreerupa ^a   Woelfel, Melissa ^a   Guildford, Melissa ^a   Moquin, David ^a   Chan, Francis Ka Ming ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLICE INHIBITORY PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN MC 159; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL DEATH; INFLAMMATION; INNATE IMMUNITY; MOLLUSCIPOXVIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIATION CHIMERA; T LYMPHOCYTE; VACCINIA VIRUS; VIRUS INFECTION; VIRUS REPLICATION;

ANIMALS; APOPTOSIS; BASE SEQUENCE; DNA PRIMERS; GENE EXPRESSION; GENES, VIRAL; GTPASE-ACTIVATING PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; LIPOPOLYSACCHARIDES; LIVER; MICE; MICE, TRANSGENIC; MOLLUSCUM CONTAGIOSUM VIRUS; NF-KAPPA B; T-LYMPHOCYTE SUBSETS; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA; VACCINIA; VACCINIA VIRUS; VIRAL PROTEINS; VIRUS REPLICATION;

MOLLUSCUM CONTAGIOSUM VIRUS; MUS; MUS MUSCULUS; VACCINIA VIRUS;

EID: 77957194670     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00983-10     Document Type: Article

References (58)

1. Bahl, K., A. Huebner, R. J. Davis, and R. M. Welsh. 2010. Analysis of apoptosis of memory T cells and dendritic cells during the early stages of viral infection or exposure to toll-like receptor agonists. J. Virol. 84:4866-4877.
2. Balachandran, S., T. Venkataraman, P. B. Fisher, and G. N. Barber. 2007. Fas-associated death domain-containing protein-mediated antiviral innate immune signaling involves the regulation of Irf7. J. Immunol. 178:2429-2439.
3. Benedict, C. A., P. S. Norris, and C. F. Ware. 2002. To kill or be killed: viral evasion of apoptosis. Nat. Immunol. 3:1013-1018.
4. Bertin, J., R. C. Armstrong, S. Ottilie, D. A. Martin, Y. Wang, S. Banks, G. H. Wang, T. G. Senkevich, E. S. Alnemri, B. Moss, M. J. Lenardo, K. J. Tomaselli, and J. I. Cohen. 1997. Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis. Proc. Natl. Acad. Sci. U. S. A. 94:1172-1176.
5. Bukowski, J. F., B. A. Woda, S. Habu, K. Okumura, and R. M. Welsh. 1983. Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J. Immunol. 131:1531-1538.
6. Challa, S., and F. K. Chan. 8 June 2010, posting date. Going up in flames: necrotic cell injury and inflammatory diseases. Cell. Mol. Life Sci. doi: 10.1007/s00018-010-0413-8.
7. Chan, F. K., and M. J. Lenardo. 2000. A crucial role for p80 TNF-R2 in amplifying p60 TNF-R1 apoptosis signals in T lymphocytes. Eur. J. Immunol. 30:652-660.
8. Chan, F. K., J. Shisler, J. G. Bixby, M. Felices, L. Zheng, M. Appel, J. Orenstein, B. Moss, and M. J. Lenardo. 2003. A role for tumor necrosis factor receptor-2 and receptor-interacting protein in programmed necrosis and antiviral responses. J. Biol. Chem. 278:51613-51621.
9. Chen, N. J., I. I. Chio, W. J. Lin, G. Duncan, H. Chau, D. Katz, H. L. Huang, K. A. Pike, Z. Hao, Y. W. Su, K. Yamamoto, R. F. de Pooter, J. C. Zuniga-Pflucker, A. Wakeham, W. C. Yeh, and T. W. Mak. 2008. Beyond tumor necrosis factor receptor: TRADD signaling in toll-like receptors. Proc. Natl. Acad. Sci. U. S. A. 105:12429-12434.
10. Cheong, R., A. Hoffmann, and A. Levchenko. 2008. Understanding NF-kappaB signaling via mathematical modeling. Mol. Syst. Biol. 4:192.
11. Cho, Y. S., S. Challa, D. Moquin, R. Genga, T. D. Ray, M. Guildford, and F. K. Chan. 2009. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137:1112-1123.
12. Chugh, P., H. Matta, S. Schamus, S. Zachariah, A. Kumar, J. A. Richardson, A. L. Smith, and P. M. Chaudhary. 2005. Constitutive NF-kappaB activation, normal Fas-induced apoptosis, and increased incidence of lymphoma in human herpes virus 8 K13 transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 102:12885-12890.
13. Costa, M. F., R. de Souza-Martins, M. C. de Souza, C. F. Benjamim, B. Piva, B. L. Diaz, M. Peters-Golden, M. G. Henriques, C. Canetti, and C. Penido. 2010. Leukotriene B4 mediates gammadelta T lymphocyte migration in response to diverse stimuli. J. Leukoc. Biol. 87:323-332.
14. Cusson-Hermance, N., S. Khurana, T. H. Lee, K. A. Fitzgerald, and M. A. Kelliher. 2005. Rip1 mediates the Trif-dependent toll-like receptor 3- and 4-induced NF-κB activation but does not contribute to interferon regulatory factor 3 activation. J. Biol. Chem. 280:36560-36566.
15. Diehl, G. E., H. H. Yue, K. Hsieh, A. A. Kuang, M. Ho, L. A. Morici, L. L. Lenz, D. Cado, L. W. Riley, and A. Winoto. 2004. TRAIL-R as a negative regulator of innate immune cell responses. Immunity 21:877-889.
16. Erickson, S. L., F. J. de Sauvage, K. Kikly, K. Carver-Moore, S. Pitts-Meek, N. Gillett, K. C. Sheehan, R. D. Schreiber, D. V. Goeddel, and M. W. Moore. 1994. Decreased sensitivity to tumour-necrosis factor but normal T-cell development in TNF receptor-2-deficient mice. Nature 372:560-563.
17. Ermolaeva, M. A., M. C. Michallet, N. Papadopoulou, O. Utermohlen, K. Kranidioti, G. Kollias, J. Tschopp, and M. Pasparakis. 2008. Function of TRADD in tumor necrosis factor receptor 1 signaling and in TRIF-dependent inflammatory responses. Nat. Immunol. 9:1037-1046.
18. Garvey, T., J. Bertin, R. Siegel, M. Lenardo, and J. Cohen. 2002. The death effector domains (DEDs) of the molluscum contagiosum virus MC159 v-FLIP protein are not functionally interchangeable with each other or with the DEDs of caspase-8. Virology 300:217-225.
19. Garvey, T. L., J. Bertin, R. M. Siegel, G. H. Wang, M. J. Lenardo, and J. I. Cohen. 2002. Binding of FADD and caspase-8 to molluscum contagiosum virus MC159 v-FLIP is not sufficient for its antiapoptotic function. J. Virol. 76:697-706.
20. Gil, J., J. Rullas, J. Alcami, and M. Esteban. 2001. MC159L protein from the poxvirus molluscum contagiosum virus inhibits NF-kappaB activation and apoptosis induced by PKR. J. Gen. Virol. 82:3027-3034.
21. Giraud, S. N., C. M. Caron, D. Pham-Dinh, P. Kitabgi, and A. B. Nicot. 2010. Estradiol inhibits ongoing autoimmune neuroinflammation and NFkappaB-dependent CCL2 expression in reactive astrocytes. Proc. Natl. Acad. Sci. U. S. A. 107:8416-8421.
22. Hanson, D., and D. G. Diven. 2003. Molluscum contagiosum. Dermatol. Online J. 9:2.
23. Hsu, H., J. Huang, H. B. Shu, V. Baichwal, and D. V. Goeddel. 1996. TNF-dependent recruitment of the protein kinase RIP to the TNF receptor-1 signaling complex. Immunity 4:387-396.
24. Hu, S., C. Vincenz, M. Buller, and V. M. Dixit. 1997. A novel family of viral death effector domain-containing molecules that inhibit both CD-95- and tumor necrosis factor receptor-1-induced apoptosis. J. Biol. Chem. 272: 9621-9624.
25. Hutchens, M. A., K. E. Luker, J. Sonstein, G. Nunez, J. L. Curtis, and G. D. Luker. 2008. Protective effect of Toll-like receptor 4 in pulmonary vaccinia infection. PLoS Pathog. 4:e1000153.
26. Izquierdo, M., A. Grandien, L. M. Criado, S. Robles, E. Leonardo, J. P. Albar, G. G. de Buitrago, and A. C. Martinez. 1999. Blocked negative selection of developing T cells in mice expressing the baculovirus p35 caspase inhibitor. EMBO J. 18:156-166.
27. Karin, M., and Y. Ben-Neriah. 2000. Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol. 18:621-663.
28. Lens, S. M., T. Kataoka, K. A. Fortner, A. Tinel, I. Ferrero, R. H. MacDonald, M. Hahne, F. Beermann, A. Attinger, H. A. Orbea, R. C. Budd, and J. Tschopp. 2002. The caspase 8 inhibitor c-FLIP(L) modulates T-cell receptor-induced proliferation but not activation-induced cell death of lymphocytes. Mol. Cell. Biol. 22:5419-5433.
29. Matta, H., L. Mazzacurati, S. Schamus, T. Yang, Q. Sun, and P. M. Chaudhary. 2007. Kaposi's sarcoma-associated herpesvirus (KSHV) oncoprotein K13 bypasses TRAFs and directly interacts with the IkappaB kinase complex to selectively activate NF-kappaB without JNK activation. J. Biol. Chem. 282:24858-24865.
30. Meylan, E., K. Burns, K. Hofmann, V. Blancheteau, F. Martinon, M. Kelliher, and J. Tschopp. 2004. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-kappa B activation. Nat. Immunol. 5:503-507.
31. Moquin, D., and F. K. Chan. 2010. The molecular regulation of programmed necrotic cell injury. Trends Biochem. Sci. 35:434-441.
32. Moutaftsi, M., B. Peters, V. Pasquetto, D. C. Tscharke, J. Sidney, H. H. Bui, H. Grey, and A. Sette. 2006. A consensus epitope prediction approach identifies the breadth of murine T(CD8+)-cell responses to vaccinia virus. Nat. Biotechnol. 24:817-819.
33. Murao, L. E., and J. L. Shisler. 2005. The MCV MC159 protein inhibits late, but not early, events of TNF-alpha-induced NF-kappaB activation. Virology 340:255-264.
34. Newton, K., A. W. Harris, M. L. Bath, K. G. Smith, and A. Strasser. 1998. A dominant interfering mutant of FADD/MORT1 enhances deletion of autoreactive thymocytes and inhibits proliferation of mature T lymphocytes. EMBO J. 17:706-718. (Pubitemid 28062050)
35. Nussbaum, A. K., and J. L. Whitton. 2004. The contraction phase of virus-specific CD8+ T cells is unaffected by a pan-caspase inhibitor. J. Immunol. 173:6611-6618.
36. Penido, C., A. Vieira-de-Abreu, M. T. Bozza, H. C. Castro-Faria-Neto, and R. T. Bozza. 2003. Role of monocyte chemotactic protein-1/CC chemokine ligand 2 on gamma delta T lymphocyte trafficking during inflammation induced by lipopolysaccharide or Mycobacterium bovis bacille Calmette-Guerin. J. Immunol. 171:6788-6794.
37. Pfeffer, K., T. Matsuyama, T. M. Kundig, A. Wakeham, K. Kishihara, A. Shahinian, K. Wiegmann, P. S. Ohashi, M. Kronke, and T. W. Mak. 1993. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 73:457-467.
38. Pobezinskaya, Y. L., Y. S. Kim, S. Choksi, M. J. Morgan, T. Li, C. Liu, and Z. Liu. 2008. The function of TRADD in signaling through tumor necrosis factor receptor 1 and TRIF-dependent Toll-like receptors. Nat. Immunol. 9:1047-1054.
39. Ramshaw, I. A., A. J. Ramsay, G. Karupiah, M. S. Rolph, S. Mahalingam, and J. C. Ruby. 1997. Cytokines and immunity to viral infections. Immunol. Rev. 159:119-135.
40. Rode, M., S. Balkow, V. Sobek, R. Brehm, P. Martin, A. Kersten, T. Dumrese, T. Stehle, A. Mullbacher, R. Wallich, and M. M. Simon. 2004. Perforin and Fas act together in the induction of apoptosis, and both are critical in the clearance of lymphocytic choriomeningitis virus infection. J. Virol. 78:12395-12405.
41. Rothe, J., W. Lesslauer, H. Lotscher, Y. Lang, P. Koebel, F. Kontgen, A. Althage, R. Zinkernagel, M. Steinmetz, and H. Bluethmann. 1993. Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 364:798-802. (Pubitemid 23261759)
42. Ruby, J., H. Bluethmann, and J. J. Peschon. 1997. Antiviral activity of tumor necrosis factor (TNF) is mediated via p55 and p75 TNF receptors. J. Exp. Med. 186:1591-1596.
43. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179:1109-1118.
44. Schmid, D., and C. Munz. 2007. Innate and adaptive immunity through autophagy. Immunity 27:11-21. (Pubitemid 47089030)
45. Selin, L. K., P. A. Santolucito, A. K. Pinto, E. Szomolanyi-Tsuda, and R. M. Welsh. 2001. Innate immunity to viruses: control of vaccinia virus infection by gamma delta T cells. J. Immunol. 166:6784-6794.
46. Smith, K. G., A. Strasser, and D. L. Vaux. 1996. CrmA expression in T lymphocytes of transgenic mice inhibits CD95 (Fas/APO-1)-transduced apoptosis, but does not cause lymphadenopathy or autoimmune disease. EMBO J. 15:5167-5176.
47. Stitz, L., J. Baenziger, H. Pircher, H. Hengartner, and R. M. Zinkernagel. 1986. Effect of rabbit anti-asialo GM1 treatment in vivo or with anti-asialo GM1 plus complement in vitro on cytotoxic T cell activities. J. Immunol. 136:4674-4680.
48. Thome, M., P. Schneider, K. Hofmann, H. Fickenscher, E. Meinl, F. Neipel, C. Mattmann, K. Burns, J. L. Bodmer, M. Schroter, C. Scaffidi, P. H. Krammer, M. E. Peter, and J. Tschopp. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386:517-521.
49. Thurau, M., H. Everett, M. Tapernoux, J. Tschopp, and M. Thome. 2006. The TRAF3-binding site of human molluscipox virus FLIP molecule MC159 is critical for its capacity to inhibit Fas-induced apoptosis. Cell Death Differ. 13:1577-1585. (Pubitemid 44210360)
50. Varfolomeev, E. E., M. Schuchmann, V. Luria, N. Chiannilkulchai, J. S. Beckmann, I. L. Mett, D. Rebrikov, V. M. Brodianski, O. C. Kemper, O. Kollet, T. Lapidot, D. Soffer, T. Sobe, K. B. Avraham, T. Goncharov, H. Holtmann, P. Lonai, and D. Wallach. 1998. Targeted disruption of the mouse Caspase 8 gene ablates cell death induction by the TNF receptors, Fas/Apo1, and DR3 and is lethal prenatally. Immunity 9:267-276.
51. Walsh, C. M., B. G. Wen, A. M. Chinnaiyan, K. O'Rourke, V. M. Dixit, and S. M. Hedrick. 1998. A role for FADD in T cell activation and development. Immunity 8:439-449.
52. Wang, W., S. Faubel, D. Ljubanovic, A. Mitra, S. A. Falk, J. Kim, Y. Tao, A. Soloviev, L. L. Reznikov, C. A. Dinarello, R. W. Schrier, and C. L. Edelstein. 2005. Endotoxemic acute renal failure is attenuated in caspase-1-deficient mice. Am. J. Physiol. Renal Physiol. 288:F997-1004.
53. Woelfel, M., J. Bixby, M. A. Brehm, and F. K. Chan. 2006. Transgenic expression of the viral FLIP MC159 causes lpr/gld-like lymphoproliferation and autoimmunity. J. Immunol. 177:3814-3820.
54. Wu, Z., M. Roberts, M. Porter, F. Walker, E. J. Wherry, J. Kelly, M. Gadina, E. M. Silva, G. A. DosReis, M. F. Lopes, J. O'Shea, W. J. Leonard, R. Ahmed, and R. M. Siegel. 2004. Viral FLIP impairs survival of activated T cells and generation of CD8 T cell memory. J. Immunol. 172:6313-6323.
55. Yeh, W. C., J. L. Pompa, M. E. McCurrach, H. B. Shu, A. J. Elia, A. Shahinian, M. Ng, A. Wakeham, W. Khoo, K. Mitchell, W. S. El-Deiry, S. W. Lowe, D. V. Goeddel, and T. W. Mak. 1998. FADD: essential for embryo development and signaling from some, but not all, inducers of apoptosis. Science 279:1954-1958.
56. Yuwen, H., J. H. Cox, J. W. Yewdell, J. R. Bennink, and B. Moss. 1993. Nuclear localization of a double-stranded RNA-binding protein encoded by the vaccinia virus E3L gene. Virology 195:732-744.
57. Zhang, J., D. Cado, A. Chen, N. H. Kabra, and A. Winoto. 1998. Fas-mediated apoptosis and activation-induced T-cell proliferation are defective in mice lacking FADD/Mort1. Nature 392:296-300.
58. Zornig, M., A. O. Hueber, and G. Evan. 1998. p53-dependent impairment of T-cell proliferation in FADD dominant-negative transgenic mice. Curr. Biol. 8:467-470.