Poxvirus MCI60 protein utilizes multiple mechanisms to inhibit NF-κB activation mediated via components of the tumor necrosis factor receptor 1 signal transduction pathway

Journal of Virology

Volumn 83, Issue 7, 2009, Pages 3162-3174

  Nichols, Daniel Brian ^a   Shisler, Joanna L ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b B103 Chemical and Life Sciences Building ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 90; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; POXVIRUS MC160 PROTEIN; PROCASPASE 8; PROTEIN PRECURSOR; TUMOR NECROSIS FACTOR RECEPTOR 1; UNCLASSIFIED DRUG; VIRUS PROTEIN; CASPASE 8; CHUK PROTEIN, HUMAN; I KAPPA B KINASE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR;

APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVATION; ENZYME INHIBITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOPRECIPITATION; INFECTION; MOLLUSCIPOXVIRUS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; CELL LINE; DRUG ANTAGONISM; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROTEIN ANALYSIS; PROTEIN BINDING;

IPS; MOLLUSCUM CONTAGIOSUM VIRUS; POXVIRIDAE;

CASPASE 8; CELL LINE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; I-KAPPA B KINASE; IMMUNOPRECIPITATION; MOLLUSCUM CONTAGIOSUM VIRUS; NF-KAPPA B; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; VIRAL PROTEINS;

EID: 63149089887     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02009-08     Document Type: Article

References (60)

1. Anest, V., J. L. Hanson, P. C. Cogswell, K. A. Steinbrecher, B. D. Strahl, and A. S. Baldwin. 2003. A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 423:659-663.
2. Antoniou, C., M. G. Kosmadaki, A. J. Stratigos, and A. D. Katsambas. 2008. Genital HPV lesions and molluscum contagiosum occurring in patients receiving anti-TNF-alpha therapy. Dermatology 216:364-365.
3. Baldi, L., K. Brown, G. Franzoso, and U. Siebenlist. 1996. Critical role for lysines 21 and 22 in signal-induced, ubiquitin-mediated proteolysis of I kappa B-alpha. J. Biol. Chem. 271:376-379.
4. Bonizzi, G., and M. Karin. 2004. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25:280-288.
5. Bowie, A., E. Kiss-Toth, J. A. Symons, G. L. Smith, S. K. Dower, and L. A. O'Neill. 2000. A46R and A52R from vaccinia vims are antagonists of host IL-1 and toll-like receptor signaling. Proc. Natl. Acad. Sci. USA 97:10162-10167.
6. Broemer, M., D. Krappmann, and C. Scheidereit. 2004. Requirement of Hsp90 activity for IkappaB kinase (IKK) biosynthesis and for constitutive and inducible IKK and NF-kappaB activation. Oncogene 23:5378-5386.
7. Chaudhary, P. M., M. T. Eby, A, Jasmin, A, Kumar, L. Liu, and L. Hood. 2000. Activation of the NF-kappaB pathway by caspase 8 and its homologs. Oncogene 19:4451-4460.
8. Chaudhary, P. M., A, Jasmin, M. T. Eby, and L. Hood. 1999. Modulation of the NF-kappa B pathway by virally encoded death effector domains-containing proteins. Oncogene 18:5738-5746.
9. Chen, G., P. Cao, and D. V. Goeddel. 2002. TNF-induced recruitment and activation of the IKK complex require Cdc37 and Hsp90. Mol. Cell 9:401-410.
10. Chen, G., and D. V. Goeddel. 2002. TNF-R1 signaling: a beautiful pathway. Science 296:1634-1635.
11. Chen, R. A., G. Ryzhakov, S. Cooray, F. Randow, and G. L. Smith. 2008. Inhibition of IkappaB kinase by vaccinia virus virulence factor B14. PLoS Pathog. 4:e22.
12. Chen, Z., J. Hagler, V. J. Palombella, F. Melandri, D. Scherer, D. Ballard, and T. Maniatis. 1995. Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-1597.
13. Choi, Y. H., K. B. Kim, H. H. Kim, G. S. Hong, Y. K. Kwon, C. W. Chung, Y. M. Park, Z. J. Shen, B. J. Kim, S. Y. Lee, and Y. K. Jung. 2001. FLASH coordinates NF-kappa B activity via TRAF2. J. Biol. Chem. 276:25073-25077.
14. Cursiefen, C., M. Grunke, C. Dechant, C. Antoni, A. Junemann, and L. M. Holbach. 2002. Multiple bilateral eyelid molluscum contagiosum lesions associated with TNFalpha-antibody and methotrexate therapy. Am. J. Oph-thalmol. 134:270-271.
15. Damon, I., P. M. Murphy, and B. Moss. 1998. Broad spectrum chemokine antagonistic activity of a human poxvirus chemokine homolog. Proc. Natl. Acad. Sci. USA 95:6403-6407.
16. Damon, I. K. 2007. Poxviruses, p. 2947-2976. In D. Knipe and P. Howley (ed.), Fields virology, 5th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
17. DiDonato, J. A., M. Hayakawa, D. M. Rothwarf, E. Zandi, and M. Karin. 1997. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388:548-554.
18. DiPerna, G., J. Stack, A. G. Bowie, A. Boyd, G. Kotwal, Z. Zhang, S. Arvikar, E. Latz, K. A. Fitzgerald, and W. L. Marshall. 2004. Poxviras protein NIL targets the I-kappaB kinase complex, inhibits signaling to NF-kappaB by the tumor necrosis factor superfamily of receptors, and inhibits NF-kappaB and IRF3 signaling by Toll-like receptors. J. Biol. Chem. 279:36570- 36578.
19. Field, N., W. Low, M. Daniels, S. Howell, L. Daviet, C. Bos holt, and M. Collins. 2003. KSHV νFLIP binds to IKK-gamma to activate IKK. J. Cell Sci. 116:3721-3728.
20. Gedey, R., X. L. Jin, O. Hinthong, and J. L. Shisler. 2006. Poxviral regulation of the host NF-kappaB response: the vaccinia virus M2L protein inhibits induction of NF-kappaB activation via an ERK2 pathway in virus-infected human embryonic kidney cells. J. Virol. 80:8676-8685.
21. Golks, A., D. Brenner, P. H. Krammer, and I. N. Lavrik. 2006. The c-FLIP-NH2 terminus (p22-FLIP) induces NF-kappaB activation. J. Exp. Med. 203: 1295-1305.
22. Hinz, M., M. Broemer, S. C. Arslan, A. Otto, E. C. Mueller, R. Dettmer, and C. Scheidereit. 2007. Signal responsiveness of IkappaB kinases is determined by Cdc37-assisted transient interaction with Hsp90. J. Biol. Chem. 282: 32311-32319.
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 recep-tor-1 signaling complex. Immunity 4:387-396.
24. Hsu, H., J. Xiong, and D. V. Goeddel. 1995. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81:495-504.
25. Hu, W. H., H. Johnson, and H. B. Shu. 2000. Activation of NF-kappaB by FADD, Casper, and caspase-8. J. Biol. Chem. 275:10838-10844.
26. Hu, Y., V. Baud, M. Delhase, P. Zhang, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science 284:316-320.
27. Hu, Y., V. Baud, T. Oga, K. I. Kim, K. Yoshida, and M. Karin. 2001. IKKalpha controls formation of the epidermis independently of NF-kappaB. Nature 410:710-714.
28. Jun, J. I., C. W. Chung, H. J. Lee, J. O. Pyo, K. N. Lee, N. S. Kim, Y. S. Kim, H. S. Yoo, T. H. Lee, E. Kim, and Y. K. Jung. 2005. Role of FLASH in caspase-8-mediated activation of NF-kappaB: dominant-negative function of FLASH mutant in NF-kappaB signaling pathway. Oncogene 24:688-696.
29. Ku, J. K., H. J. Kwon, M. Y. Kim, H. Kang, P. I. Song, C. A. Armstrong, J. C. Ansel, H. O. Kim, and Y. M. Park. 2008. Expression of Toll-like receptors in verruca and molluscum contagiosum. J. Korean Med. Sci. 23:307-314.
30. Lemmers, B., L. Salmena, N. Bidere, H. Su, E. Matysiak-Zablocki, K. Murakami, P. S. Ohashi, A. Jurisicova, M. Lenardo, R. Hakem, and A. Hakem. 2007. Essential role for caspase-8 in Toll-like receptors and NFkappaB signaling. J. Biol. Chem. 282:7416-7423.
31. Li, H., and X. Lin. 2008. Positive and negative signaling components involved in TNFalpha-induced NF-kappaB activation. Cytokine 41:1-8.
32. Li, Q., Q. Lu, J. Y. Hwang, D. Buscher, K. F. Lee, J. C. Izpisua-Belmonte, and I. M. Verma. 1999. IKK1-deficient mice exhibit abnormal development of skin and skeleton. Genes Dev. 13:1322-1328.
33. Li, X., Y. Yang, and J. D. Ashwell. 2002. TNF-RII and c-IAPl mediate ubiquitination and degradation of TRAF2. Nature 416:345-347.
34. Maeda, G., T. Chiba, S. Kawashiri, T. Satoh, and K. Imai. 2007. Epigenetic inactivation of IkappaB kinase-alpha in oral carcinomas and tumor progression. Clin. Cancer Res. 13:5041-5047.
35. Matta, H., Q. Sun, G. Moses, and P. M. Chaudhary. 2003. Molecular genetic analysis of human herpes virus 8-encoded viral FLICE inhibitory protein-induced NF-kappaB activation. J. Biol. Chem. 278:52406-52411.
36. Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. Li, D. B. Young, M. Barbosa, M. Mann, A, Manning, and A, Rao. 1997. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278:860-866.
37. Moss, B., J. L. Shisler, Y. Xiang, and T. G. Senkevich. 2000. Immune-defense molecules of molluscum contagiosum virus, a human poxviras. Trends Mi-crobiol. 8:473-477.
38. Muller, J. R., and U. Siebenlist. 2003. Lymphotoxin beta receptor induces sequential activation of distinct NF-kappa B factors via separate signaling pathways. J. Biol. Chem. 278:12006-12012.
39. 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.
40. Muzio, M., A, M. Chinnaiyan, K. C. Kischkel, K. O'Rourke, A, Shevchenko, J. Ni, C. Scaffidi, J. D. Bretz, M. Zhang, R. Gentz, M. Mann, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85:817-827.
41. Nichols, D. B., and J. L. Shisler. 2006. The MCI60 protein expressed by the dermatotropic poxviras molluscum contagiosum virus prevents tumor necrosis factor alpha-induced NF-κB activation via inhibition of I kappa kinase complex formation. J. Virol. 80:578-586.
42. Oie, K. L., and D. J. Pickup. 2001. Cowpox virus and other members of the orthopoxviras genus interfere with the regulation of NF-kappaB activation. Virology 288:175-187.
43. Perkins, N. D. 2006. Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway. Oncogene 25:6717-6730.
44. Sakurai, H., H. Chiba, H. Miyoshi, T. Sugita, and W. Toriumi. 1999. IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J. Biol. Chem. 274:30353-30356.
45. Scheidereit, C. 2006. IkappaB kinase complexes: gateways to NF-kappaB activation and transcription. Oncogene 25:6685-6705.
46. Scherer, D. C., J. A. Brockman, Z. Chen, T. Maniatis, and D. W. Ballard. 1995. Signal-induced degradation of I kappa B alpha requires site-specific ubiquitination. Proc. Natl. Acad. Sci. USA 92:11259-11263.
47. Senkevich, T. G., J. J. Bugert, J. R. Sisler, E. V. Koonin, G. Darai, and B. Moss. 1996. Genome sequence of a human tumorigenic poxviras: prediction of specific host response-evasion genes. Science 273:813-816.
48. Senkevich, T. G., E. V. Koonin, J. J. Bugert, G. Darai, and B. Moss. 1997. The genome of molluscum contagiosum virus: analysis and comparison with other poxviruses. Virology 233:19-42.
49. Shikama, Y., M. Yamada, and T. Miyashita. 2003. Caspase-8 and caspase-10 activate NF-kappaB through RIP, NIK and IKKalpha kinases. Eur. J. Immunol. 33:1998-2006.
50. Shisler, J. L., and X.-L. Jin. 2004. The vaccinia virus K1L gene product inhibits host NF-κB activation by preventing IκBα degradation. J. Virol. 78:3553-3560.
51. Shisler, J. L., and B. Moss. 2001. Molluscum contagiosum virus inhibitors of apoptosis: the MC159 v-FLIP protein blocks Fas-induced activation of pro-caspases and degradation of the related MC160 protein. Virology 282:14-25.
52. Shisler, J. L., T. G. Senkevich, M. J. Berry, and B. Moss. 1998. Ultraviolet-induced cell death blocked by a selenoprotein from a human dermatotropic poxviras. Science 279:102-105.
53. Sizemore, N., N. Lerner, N. Dombrowski, H. Sakurai, and G. R. Stark. 2002. Distinct roles of the Ikappa B kinase alpha and beta subunits in liberating nuclear factor kappa B (NF-kappa B) from Ikappa B and in phosphorylating the p65 subunit of NF-kappa B. J. Biol. Chem. 277:3863-3869.
54. Stebbins, C. E., A. A. Russo, C. Schneider, N. Rosen, F. U. Hartl, and N. P. Pavletich. 1997. Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89:239-250.
55. Sun, Q., S. Zachariah, and P. M. Chaudhary. 2003. The human herpes virus 8-encoded viral FLICE-inhibitory protein induces cellular transformation via NF-kappaB activation. J. Biol. Chem. 278:52437-52445.
56. Takeda, K., O. Takeuchi, T. Tsujimura, S. Itami, O. Adachi, T. Kawai, H. Sanjo, K. Yoshikawa, N. Terada, and S. Akira. 1999. Limb and skin abnormalities in mice lacking IKKalpha. Science 284:313-316.
57. Whitesell, L., E. G. Mimnaugh, B. De Costa, C. E. Myers, and L. M. Neckers. 1994. Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. USA 91:8324-8328.
58. Xiang, Y., and B. Moss. 1999. IL-18 binding and inhibition of interferon gamma induction by human poxvirus-encoded proteins. Proc. Natl. Acad. Sci. USA 96:11537-11542.
59. Yamamoto, Y., U. N. Verma, S. Prajapati, Y. T. Kwak, and R. B. Gaynor. 2003. Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 423:655-659.
60. Yang, K., H. Shi, R. Qi, S. Sun, Y. Tang, B. Zhang, and C. Wang. 2006. Hsp90 regulates activation of interferon regulatory factor 3 and TBK-1 stabilization in Sendai virus-infected cells. Mol. Biol. Cell 17:1461-1471.