NF-κB-mediated inhibition of apoptosis is required for encephalomyocarditis virus virulence: A mechanism of resistance in p50 knockout mice

Journal of Virology

Volumn 72, Issue 7, 1998, Pages 5654-5660

  Schwarz, Edward M ^a,c   Badorff, Cornel ^b   Hiura, Timothy S ^b   Wessely, Rainer ^b   Badorff, Annette ^b   Verma, Inder M ^a   Knowlton, Kirk U ^b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON RECEPTOR;

ANIMAL MODEL; APOPTOSIS; ARTICLE; CYTOLYSIS; CYTOTOXICITY; ENCEPHALOMYOCARDITIS VIRUS; HOST RESISTANCE; KNOCKOUT MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS REPLICATION; VIRUS VIRULENCE; ANIMAL; IMMUNOLOGY; MOUSE; MOUSE MUTANT; PATHOGENICITY; PHYSIOLOGY; VIRULENCE; VIRUS INFECTION;

ANIMALS; APOPTOSIS; CARDIOVIRUS INFECTIONS; ENCEPHALOMYOCARDITIS VIRUS; MICE; MICE, KNOCKOUT; NF-KAPPA B; RECEPTORS, INTERFERON; VIRULENCE; VIRUS REPLICATION;

EID: 0031596337     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.7.5654-5660.1998     Document Type: Article

References (57)

1. Ankarcrona, M., J. M. Dypbukt, E. Bonfoco, B. Zhivotovsky, S. Orrenius, S. A. Lipton, and P. Nicotera. 1995. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973.
2. Armstrong, R. C., T. Aja, J. Xiang, S. Gaur, J. F. Krebs, K. Hoang, X. Bai, S. J. Korsmeyer, D. S. Karanewsky, L. C. Fritz, and K. J. Tomaselli. 1996. Fas-induced activation of the cell death-related protease CPP32 Is Inhibited by Bcl-2 and by ICE family protease inhibitors. J. Biol. Chem. 271:16850-16855.
3. Baeuerle, P. A., and T. Henkel. 1994. Function and activation of NF-kappa B in the immune system. Annu. Rev. Immunol. 12:141-179.
4. Baldwin, A. S., Jr. 1996. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649-683.
5. Barroga, C. F., J. K. Stevenson, E. M. Schwarz, and I. M. Verma. 1995. Constitutive phosphorylation of I kappa B alpha by casein kinase II. Proc. Natl. Acad. Sci. USA 92:7637-7641.
6. Beg, A. A., and D. Baltimore. 1996. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274:782-784.
7. Beg, A. A., W. C. Sha, R. T. Bronson, S. Ghosh, and D. Baltimore. 1995. Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B. Nature 376:167-170.
8. 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 herpes-virus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis. Proc. Natl. Acad. Sci. USA 94:1172-1176.
9. Boulakia, C. A., G. Chen, F. W. Ng, J. G. Teodoro, P. E. Branton, D. W. Nicholson, G. G. Poirier, and G. C. Shore. 1996. Bcl-2 and adenovirus E1B 19 kDa protein prevent E1A-induced processing of CPP32 and cleavage of poly(ADP-ribose)-polymerase. Oncogene 12:529-535.
10. Boyd, J. M., S. Malstrom, T. Subramanian, L. K. Venkatesh, U. Schaepe, B. Elangovan, C. D'Sa-Eipper, and G. Chinnadurai. 1994. Adenovirus E1B 19 kDa and Bcl-2 proteins interact with a common set of cellular proteins. Cell 79:341-351.
11. Brooks, M. A., A. N. Ali, P. C. Turner, and R. W. Moyer. 1995. A rabbitpox virus serpin gene controls host range by inhibiting apoptosis in restrictive cells. J. Virol. 69:7688-7698.
12. Brown, K., S. Gerstberger, L. Carlson, G. Franzoso, and U. Siebenlist. 1995. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267:1485-1488.
13. Bump, N. J., M. Hackett, M. Hugunin, S. Seshagiri, K. Brady, P. Chen, C. Ferenz, S. Franklin, T. Ghayur, P. Li, et al. 1995. Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269:1885-1888.
14. Chinnaiyan, A. M., K. Orth, O. R. K. H. Duan, G. G. Poirier, and V. M. Dixit. 1996. Molecular ordering of the cell death pathway. Bcl-2 and Bcl-xL function upstream of the CED-3-like apoptotic proteases. J. Biol. Chem. 271: 4573-4576.
15. Cohen, J. J., R. C. Duke, V. A. Fadok, and K. S. Sellins. 1992. Apoptosis and programmed cell death in immunity. Annu. Rev. Immunol. 10:267-293.
16. Darzynkiewicz, Z., G. Juan, X. Li, W. Gorczyca, T. Murakami, and F. Traganos. 1997. Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 27:1-20.
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. Duque, H., and A. C. Palmenberg. 1996. Epitope mapping of monoclonal antibodies raised to recombinant mengo 3D polymerase. Virus Genes 13: 159-168.
19. Duvall, E., A. H. Wyllie, and R. G. Morris. 1985. Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology 56:351-358.
20. Fadok, V. A., J. S. Savill, C. Haslett, D. L. Bratton, D. E. Doherty, P. A. Campbell, and P. M. Henson. 1992. Different populations of macrophages use either the vitrionectin reseptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J. Immunol. 149:4029-4035.
21. Fadok, V. A., D. R. Voelker, P. A. Campbell, J. J. Cohen, D. L. Bratton, and P. M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207-2216.
22. Gregory, C. D., C. Dive, S. Henderson, C. A. Smith, G. T. Williams, J. Gordon, and A. B. Rickinson. 1991. Activation of Epstein-Barr virus latent genes protects human B cells from death by apoptosis. Nature 349:612-614.
23. Hershberger, P. A., J. A. Dickson, and P. D. Friesen. 1992. Site-specific mutagenesis of the 35-kilodalton protein gene encoded by Autographa californica nuclear polyhedrosis virus: cell line-specific effects on virus replication. J. Virol. 66:5525-5533.
24. Huber, S. A. 1994. VCAM-1 is a receptor for encephalomyocarditis virus on murine vascular endothelial cells. J. Virol. 68:3453-3458.
25. Jeon, E.-S., Z. Sheng, and K. U. Knowlton. 1996. Coxsackievirus induces myocyte apoptosis. Circulation 94(Suppl. I):I-356.
26. Levine, B., Q. Huang, J. T. Isaacs, J. C. Reed, D. E. Griffin, and J. M. Hardwick. 1993. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature 361:739-742.
27. Liou, H. C., and D. Baltimore. 1993. Regulation of the NF-kappa B/rel transcription factor and I kappa B inhibitor system. Curr. Opin. Cell Biol. 5:477-487.
28. Liu, Z. G., H. Hsu, D. V. Goeddel, and M. Karin. 1996. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87:565-576.
29. Martin, S. J., C. P. Reutelingsperger, A. J. McGahon, J. A. Rader, R. C. van Schie, D. M. LaFace, and D. R. Green. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182:1545-1556.
30. Muller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921.
31. Newman, S. L., J. E. Henson, and P. M. Henson. 1982. Phagocytosis of senescent neutrophils by human monocyte derived macrophages and rabbit inflammatory macrophages. J. Exp. Med. 156:430-442.
32. Perry, S. W., L. G. Epstein, and H. A. Gelbard. 1997. Simultaneous in situ detection of apoptosis and necrosis in monolayer cultures by TUNEL and trypan blue staining. BioTechniques 22:1102-1106.
33. Pilder, S., J. Logan, and T. Shenk. 1984. Deletion of the gene encoding the adenovirus 5 early region 1b 21,000-molecular-weight polypeptide leads to degradation of viral and host cell DNA. J. Virol. 52:664-671.
34. Raff, M. C. 1992. Social controls on cell survival and cell death. Nature 356:397-400.
35. Rao, L., M. Debbas, P. Sabbatini, D. Hockenbery, S. Korsmeyer, and E. White. 1992. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc. Natl. Acad. Sci. USA 89:7742-7746.
36. Ray, C. A., R. A. Black, S. R. Kronheim, T. A. Greenstreet, P. R. Sleath, G. S. Salvesen, and D. J. Pickup. 1992. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme. Cell 69:597-604.
37. Razvi, E. S., and R. M. Welsh. 1995. Apoptosis in viral infections. Adv. Virus Res. 45:1-60.
38. Regnier, C. H., H. Y. Song, X. Gao, D. V. Goeddel, Z. Cao, and M. Rothe. 1997. Identification and characterization of an IkappaB kinase. Cell 90:373-383.
39. Rousseau, V., I. Cremer, E. Lauret, I. Riviere, M. Aguet, and E. De Maeyer. 1995. Antiviral activity of autocrine interferon-beta requires the presence of a functional interferon type I receptor. J. Interferon Cytokine Res. 15:785-789.
40. Rueckert, R. R. 1996. Picornaviridae: the viruses and their replication, p. 609-654. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
41. Schwarz, E. M., P. Krimpenfort, A. Berns, and I. M. Verma. 1997. Immunological defects in mice with a targeted disruption in Bcl-3. Genes Dev. 11:187-197.
42. Schwarz, E. M., D. Van Antwerp, and I. M. Verma. 1996. Constitutive phosphorylation of IκBα by casein kinase II occurs preferentially at serine 293: requirement for degradation of free IκBα. Mol. Cell. Biol. 16:3554-3559.
43. Sha, W. C., H. C. Liou, E. I. Tuomanen, and D. Baltimore. 1995. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell 80:321-330.
44. Shen, Y., and T. E. Shenk. 1995. Viruses and apoptosis. Curr. Opm. Genet. Dev. 5:105-11.
45. Siebenlist, U., G. Franzoso, and K. Brown. 1994. Structure, regulation and function of NF-kappa B. Annu. Rev. Cell Biol. 10:405-455.
46. Teodoro, J. G., and P. E. Branton. 1997. Regulation of apoptosis by viral gene products. J. Virol. 71:1739-1746.
47. 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.
48. Tolskaya, E. A., L. I. Romanova, M. S. Kolesnikova, T. A. Ivannikova, E. A. Smirnova, N. T. Raikhlin, and V. I. Agol. 1995. Apoptosis-inducing and apoptosis-preventing functions of poliovirus. J. Virol. 69:1181-1189.
49. Traenckner, E. B., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J. 14:2876-2883.
50. Van Antwerp, D. J., S. J. Martin, T. Kafri, D. R. Green, and I. M. Verma. 1996. Suppression of TNF-alpha-induced apoptosis hy NF-kappaB. Science 274:787-789.
51. Verma, I. M., J. K. Stevenson, E. M. Schwarz, D. Van Antwerp, and S. Miyamoto. 1995. Rel/NF-kappa B/I kappa B family: intimate tales of association and dissociation. Genes Dev. 9:2723-2735.
52. Wang, C. Y., M. W. Mayo, and A. S. Baldwin, Jr. 1996. TNF- and cancer therapy-induced apoptosis: potentiation hy inhibition of NF-kappaB. Science 274:784-787.
53. Wang W. Z., A. Matsumori, T. Yamada, T. Shioi, I. Okada, S. Matsui, Y. Sato, H. Suzuki, K. Shiota, and S. Sasayama. 1997. Beneficial effects of amlodipine in a murine model of congestive heart failure induced by viral myocarditis. A possible mechanism through inhibition of nitric oxide production. Circulation 95:245-251.
54. White, E., and B. Stillman. 1987. Expression of adenovirus E1B mutant phenotypes is dependent on the host cell and on synthesis of E1A proteins. J. Virol. 61:426-435.
55. Xue, D., and H. R. Horvitz. 1995. Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377:248-251.
56. Zhu, Z., W. Tang, A. Ray, Y. Wu, O. Einarsson, M. L. Landry, J. Gwaltney, Jr., and J. A. Elias. 1996. Rhinovirus stimulation of interleukin-b in vivo and in vitro. Evidence for nuclear factor kappa B-dependent transcriptional activation. J. Clin. Invest. 97:421-430.
57. Zinkernagel, R. M. 1996. Immunology taught by viruses. Science 271:173-178.