Human cytomegalovirus inhibits IFN-α-stimulated antiviral and immunoregulatory responses by blocking multiple levels of IFN-α signal transduction

Journal of Immunology

Volumn 162, Issue 10, 1999, Pages 6107-6113

  Miller, Daniel M ^a   Zhang, Yingxue ^a   Rahill, Brian M ^a   Waldman, W James ^a   Sedmak, Daniel D ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b 139 Hamilton Hall ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; ALPHA INTERFERON; INTERFERON REGULATORY FACTOR 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN KINASE; TRANSCRIPTION FACTOR;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FIBROBLAST; GENE EXPRESSION; HERPES VIRUS; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IMMUNOREGULATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANTIVIRAL AGENTS; CYTOMEGALOVIRUS; DNA-BINDING PROTEINS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HUMANS; INTERFERON-ALPHA; INTERFERON-STIMULATED GENE FACTOR 3; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; JANUS KINASE 1; MODELS, IMMUNOLOGICAL; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STAT2 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 0033563134     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. Alford, C. A., S. Stagno, R. F. Pass, and W. J. Britt. 1990. Congenital and perinatal cytomegalovirus infections. Rev. Infect. Dis. 12:745.
2. Rubin, R. H. 1990. Impact of cytomegalovirus infection on organ transplant recipients. Rev. Infect. Dis. 12:754.
3. Winston, D. J., W. G. Ho, and R. E. Champlin. 1990. Cytomegalovirus infections after allogenic bone marrow transplantation. Rev. Infect. Dis. 12:776.
4. Sedmak, D. D. 1995. The role of cytomegalovirus in transplant vascular sclerosis. In Transplant Vascular Sclerosis, Chapter 17. R. G. Landes Company, Austin, p. 185.
5. Simmons, P., K. Kaushansky, and B. Torok-Storb. 1990. Mechanisms of cytomegalovirus-mediated myelosuppression: perturbation of stromal cell function versus direct infection of myeloid cells. Proc. Natl. Acad. Sci. USA 87:1386.
6. Klatt, E. C., and D. Shibata. 1988. Cytomegalovirus infection in the acquired immunodeficiency syndrome. Arch. Pathol. Lab. Med. 112:540.
7. Jacobson, M. A. 1997. Treatment of cytomegalovirus retinitis in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 337:105.
8. Muller, U., U. Steinhoff, L. F. L. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type 1 and type II interferons in antiviral defense. Science 264:1918.
9. Darnell, J. E., I. M. Kerr, and G. R. Stark. 1994. Jak-Stat pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415.
10. Orange, J. S., and C. A. Biron. 1996. Characterization of early IL-12, IFN-αβ, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. J. Immunol. 156:4746.
11. Cheeseman, S. H., R. H. Rubin, J. A. Stewart, N. E. Tolkoff-Rubin, A. B. Cosimi, K. Cantell, J. Gilbert, S. Winkle, J. T. Herrin, P. H. Black, P. S. Russell, and M. S. Hirsch. 1979. Controlled clinical trial of prophylactic human-leukocyte interferon in renal transplantation. N. Engl. J. Med. 300:1345.
12. Yeow, W.-S., C. M. Lawson, and M. W. Beilharz. 1998. Antiviral activities of individual murine IFN-a subtypes in vivo: intramuscular injection of IFN expression constructs reduces Cytomegalovirus replication. J. Immunol 160:2932.
13. Presti, R. M., J. L. Pollock, A. J. Dal Canto, A. K. O'Guin, and H. W. Virgin. 1998. Interferon-γ regulation of acute, chronic, and latent murine cytomegalovirus infection and disease of the great vessels. J. Exp. Med. 188:577.
14. Levy, D. E., D. S. Kessler, R. Pine, and J. E. Darnell, Jr. 1989. Cytoplasmic activation of ISGF3, the positive regulator of interferon-a-stimulated transcription, reconstituted in vitro. Genes Dev. 3:1362.
15. Lew, D. J., T. Decker, and J. E. Darnell. 1992. α interferon and γ interferon stimulate transcription of a single gene through different signal transduction pathways. Mol. Cell. Biol. 9:5404.
16. Schindler, C., X. Y. Fu, T. Improta, R. Aebersold, and J. E. Darnell. 1992. Proteins of transcription factor ISGF-3: one gene encodes the 91-and 84-kDa ISGF-3 proteins that are activated by interferon α. Proc. Natl. Acad. Sci. USA 89:7836.
17. Ghislain, J. J., and E. N. Fish. 1996. Application of genomic DNA affinity chromatography identifies multiple interferon-α-regulated Stat2 complexes. J. Biol. Chem. 271:12408.
18. Li. X., S. Leung, I. M. Kerr, and G. R. Stark. 1997. Functional subdomains of STAT2 required for preassodation with the α interferon receptor and for signaling. Mol. Cell. Biol. 17:2048.
19. Haque, S. J., and B. R. G. Williams. 1994. Identification and characterization of an interferon (IFN)-stimulated response element-IFN-stimulated gene factor 3-independent signaling pathway for IFN-α. J. Biol. Chem. 269:19523.
20. Li, X., S. Leung, S. Qureshi, J. E. Darnell, and G. R. Stark. 1996. Formation of Stat1 -Stat2 heterodimers and their role in the activation of IRF-1 gene transcription by interferon-α. J. Biol. Chem. 271:5790.
21. Miller, D. M., B. M. Rahill, J. M. Boss, M. D. Lairmore, J. E. Durbin, W. J. Waldman, and D. D. Sedmak. 1998. Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway. J. Exp. Med. 187:675.
22. Zhu, H., J. P. Cong, and T. Shenk. 1997. Use of differential display analysis to assess the effect of human cytomegalovirus infection on the accumulation of cellular RNAs: induction of interferon-responsive RNAs. Proc. Natl. Acad. Sci. USA 94:13985.
23. Leonard, G. T., and G. C. Sen. 1996. Effects of adenovirus E1A protein on interferon-signaling. Virology 224:25.
24. Kalvakolanu, D. V. R., S. K. Bandyopadhyay, M. L. Harter, and G. C. Sen. 1991. Inhibition of the interferon inducible gene expression by adenovirus E1A proteins: block in transcriptional complex formation. Proc. Natl. Acad. Sci. USA 88:7459.
25. Leonard, G. T., and G. C. Sen. 1997. Restoration of interferon responses of adenovirus E1A-expressing HT1080 cell lines by overexpression of p48 protein. J. Virol. 71:5095.
26. Ploegh, H. L. 1998. Viral strategies of immune evasion. Science 280:248.
27. Sedmak, D. D., A. M. Guglielmo, D. A. Knight, D. J. Birmingham, E. H. Huang, and W. J. Waldman. 1994. Cytomegalovirus inhibits major histocompatibility class II expression on infected endothelial cells. Am. J. Pathol. 144:683.
28. Waldman, W. J., W. H. Roberts, D. H. Davis, M. V. Williams, D. D. Sedmak, and R. E. Stephens. 1991. Preservation of natural endothelial cytopathogenicity of cytomegalovirus by propagation in endothelial cells. Arch. Virol. 117:143.
29. Huang, E. S. 1975. Human cytomegalovirus III: virus-induced DNA polymerase. J. Virol. 16:298.
30. Lehtonen, A., S. Matikainen, and I. Julkunen. 1997. Interferons up-regulate Stat1, Stat2, and IRF family transcription factor gene expression in human peripheral blood mononuclear cells and macrophages. J. Immunol. 159:794.
31. Dignam. J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475.
32. Heise, M. T., M. Connick, and H. W. Virgin. 1998. Murine cytomegalovirus inhibits interferon-γ-induced antigen presentation to CD4 T cells by macrophages via regulation of expression of major histocompatibility complex class II-associated genes. J. Exp. Med. 187:1.
33. Sinzger, C., and G. Jahn. 1996. Human cytomegalovirus cell tropism and pathogenesis. Intervirology 39:302.
34. Sinzger, C., A. Grefte, B. Plachter, A. S. H. Gouw, T. H. The, and G. Jahn. 1995. Fibroblasts, epithelial cells, endothelial cells and smooth muscle cells are major target of human cytomegalovirus infection in lung and gastrointestinal tissues. J. Gen. Virol. 76:741.
35. 2-microglobulin genes in vivo. J. Immunol. 150:2805.
36. Martin, B., K. Chin, J. Olsen, C. Skinner, A. Dey, K. Ozato, and J. Ting. 1997. Induction of MHC class I expression by the MHC class II transactivator CIITA. Immunity 6:591.
37. Hobart, M., V. Ramassar, N. Goes, J. Urmsori, and P. F. Halloran. 1997. IFN regulatory factor-1 plays a central role in the regulation of the expression of class I and II MHC genes in vivo. J. Immunol 158:4260.
38. Gobin, S., A. Peijnenburg, V. Keijsers, and P. van den Elsen. 1997. Site α is crucial for two routes of IFN-γ-induced MHC class I transactivation: the ISRE-mediated route and a novel pathway involving CIITA. Immunity 6:601.
39. Kimura, T., K. Nakayama, J. Penninger, M. Kitagawa, H. Harada, T. Matsuyama, N. Tanaka, R. Kamijo, J. Vilcek, T. W. Mak, and T. Taniguchi. 1994. Involvement of the IRF-1 transcription factor in antiviral responses to interferons. Science 264:1921.
40. Staeheli, P., O. Haller, W. Boll, J. Lindenmann, and C. Weissmann. 1986. Mx protein: constitutive expression in 3T3 cells transformed with cloned Mx cDNA confers selective resistance to influenza virus. Cell 44:147.
41. Weihua, X., V. Kolla, and D. V. Kalvakolanu. 1997. Interferon γ-induced transcription of the murine ISGFSγ (p48) gene is mediated by novel factors. Proc. Natl. Acad. Sci. USA 94:103.
42. Martinez-Moczygemba, M., M. J. Gutch, D. L. French, and N. C. Reich. 1997. Distinct Stat structure promotes interaction of Stat2 with the p48 subunit of the interferon-α-slimulated transcription factor ISGF3. J. Biol. Chem. 272:20070.
43. Veals, S. A., C. Schindler, D. Leonard, F. Xin-Yuan, R. Aebersold, J. E. Darnell, and D. E. Levy. 1992. Subunit of an α-interferon-responsive transcription factor is related to interferon regulatory factor and Myb families of DNA-binding proteins. Mol. Cell. Biol. 12:3315.
44. Gao, P.-Q., S. H. Sims, D. C. Chang, and A. B. Deisseroth. 1993. Interferon-γ priming effects in the activation and deactivation of ISGF in K562 cells. J. Biol. Chem. 268:12380.
45. Kimura, T., Y. Kadokawa, H. Harada, M. Matsumoto, M. Saw, Y. Kashiwazaki, M. Tarutani, R. S.-P. Tan, T. Takasugi, T. Matsuyama, et al. 1996. Essential and nonredundant roles of p48 (ISGF3-γ) and IRF-1 in both type I and type II interferon responses, as revealed by gene targeting studies. Genes Cells 1:115.
46. Kanda, K., T. Decker, P. Aman, M. Wahlstrom, A. von Gabain, and B. Kallin. 1992. The EBNA2-related resistance towards α interferon in Burkitt's lymphoma cells effects induction of IFN-induced genes but not the activation of transcription factor ISGF3. Mol. Cell. Biol. 12:4930.
47. Navarro, L., K. Mowen, S. Rodems, B. Weaver, N. Reich, D Spector, and M. David. 1998. Cytomegalovirus activates interferon immediate-early response gene expression and an interferon regulatory factor 3-containing interferon-stimulated response element-binding complex. Mol. Cell. Biol. 18:3796.
48. Waldman, W. J., D. A. Knight, E. H. Huang, and D. D. Sedmak. 1995. Bidirectional transmission of infectious cytomegalovirus between monocytes and vascular endothelial cells: an in vitro model. J. Infect. Dis. 171:263.
49. Fish, K. N., S. G. Stenglein, C. Ibanez, and J. A. Nelson. 1995. Cytomegalovirus persistence in macrophages and endothelial cells. Stand. J. Infect. Dis. 99:34.
50. Koffron, A. J., M. Hummel, B. K. Patterson, S. Yan, D. B. Kaufman, J. P. Fryer, F. P. Stuart, and M. I. Abecassis. 1998. Cellular localization of latent murine cytomegalovirus. J. Virol. 72:95.
51. Pober, J. S., and R. S Cotran 1990. The role of endothelial cells in inflammation. Transplantation 50:537.
52. Epperson, D. E., and J. S. Pober. 1994. Antigen-presenting function of human endothelial cells: direct activation of resting CD8 T cells. J. Immunol. 153:5402.