Human rhinovirus attenuates the type I interferon response by disrupting activation of interferon regulatory factor 3

Journal of Virology

Volumn 80, Issue 10, 2006, Pages 5021-5031

  Peng, Tao ^a   Kotla, Swathi ^b   Bumgarner, Roger E ^a   Gustin, Kurt E ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; BETA INTERFERON; DOUBLE STRANDED RNA; GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; JANUS KINASE; MESSENGER RNA; STAT PROTEIN;

ARTICLE; CELL NUCLEUS; COMMON COLD; CONTROLLED STUDY; DIMERIZATION; FLUORESCENCE MICROSCOPY; HELA CELL; HOST RESISTANCE; HUMAN; HUMAN CELL; HUMAN RHINOVIRUS; HUMAN RHINOVIRUS TYPE 14; IMMUNE RESPONSE; INNATE IMMUNITY; LUNG ALVEOLUS EPITHELIUM; MICROARRAY ANALYSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS INFECTION;

ACTIVATING TRANSCRIPTION FACTOR 2; CELL LINE; DIMERIZATION; HELA CELLS; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; INTERFERON-BETA; JANUS KINASE 1; NF-KAPPA B; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RHINOVIRUS; RNA, MESSENGER; STAT TRANSCRIPTION FACTORS;

HUMAN RHINOVIRUS SP.; RHINOVIRUS;

EID: 33646450399     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.10.5021-5031.2006     Document Type: Article

References (64)

1. Abzug, M. J., A. C. Beam, E. A. Gyorkos, and M. J. Levin. 1990. Viral pneumonia in the first month of life. Pediatr. Infect. Dis. J. 9:881-885.
2. Baigent, S. J., G. Zhang, M. D. Fray, H. Flick-Smith, S. Goodbourn, and J. W. McCauley. 2002. Inhibition of beta interferon transcription by non-cytopathogenic bovine viral diarrhea virus is through an interferon regulatory factor 3-dependent mechanism. J. Virol. 76:8979-8988.
3. Barro, M., and J. T. Patton. 2005. Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc. Natl. Acad. Sci. USA 102:4114-4119.
4. 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.
5. Bertino, J. S. 2002. Cost burden of viral respiratory infections: issues for formulary decision makers. Am. J. Med. 112(Suppl. 6A):42S-49S.
6. Biron, A. B., and G. C. Sen. 2001. Interferons and other cytokines, p. 321-351. In B. N. Fields and D. M. Knipe (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
7. Bossert, B., S. Marozin, and K. K. Conzelmann. 2003. Nonstructural proteins NS1 and NS2 of bovine respiratory syncytial virus block activation of interferon regulatory factor 3. J. Virol. 77:8661-8668.
8. Browne, E. P., B. Wing, D. Coleman, and T. Shenk. 2001. Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J. Virol. 75:12319-12330.
9. Chen, Y., E. Hamati, P. K. Lee, W. M. Lee, S. Wachi, D. Schnurr, S. Yagi, G. Dolganov, H. Boushey, P. Avila, and R. Wu. 2005. Rhinovirus induces airway epithelial gene expression through dsRNA and interferon-dependent pathways. Am. J. Respir. Cell Mol. Biol. 34:192-203.
10. Couch, R. B. 2001. Rhinoviruses, p. 777-798. In B. N. Fields and D. M. Knipe (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
11. Dodd, D. A. 2002. Effects of poliovirus infection and picornaviral 3A proteins on the cellular response to viral infection. Ph.D. thesis. Stanford University, Stanford, Calif.
12. Einarsson, O., G. P. Geba, Z. Zhu, M. Landry, and J. A. Elias. 1996. Interleukin-11: stimulation in vivo and in vitro by respiratory viruses and induction of airways hyperresponsiveness. J. Clin. Investig. 97:915-924.
13. Foy, E., K. Li, C. Wang, R. Sumpter, Jr., M. Ikeda, S. M. Lemon, and M. Gale, Jr. 2003. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300:1145-1148.
14. Garofalo, R., F. Mei, R. Espejo, G. Ye, H. Haeberle, S. Baron, P. L. Ogra, and V. E. Reyes. 1996. Respiratory syncytial virus infection of human respiratory epithelial cells up-regulates class I MHC expression through the induction of IFN-beta and IL-1 alpha. J. Immunol. 157:2506-2513.
15. Geiss, G. K., V. S. Carter, Y. He, B. K. Kwieciszewski, T. Holzman, M. J. Korth, C. A. Lazaro, N. Fausto, R. E. Bumgarner, and M. G. Katze. 2003. Gene expression profiling of the cellular transcriptional network regulated by alpha/beta interferon and its partial attenuation by the hepatitis C virus nonstructural 5A protein. J. Virol. 77:6367-6375.
16. Ghosh, S., R. Champlin, R. Couch, J. Englund, I. Raad, S. Malik, M. Luna, and E. Whimbey. 1999. Rhinovirus infections in myelosuppressed adult blood and marrow transplant recipients. Clin. Infect. Dis. 29:528-532.
17. Gustin, K. E., and P. Sarnow. 2002. Inhibition of nuclear import and alteration of nuclear pore complex composition by rhinovirus. J. Virol. 76:8787-8796.
18. Hall, D. J., M. E. Bates, L. Guar, M. Cronan, N. Korpi, and P. J. Bertics. 2005. The role of p38 MAPK in rhinovirus-induced monocyte chemoattractant protein-1 production by monocytic-lineage cells. J. Immunol. 174:8056-8063.
19. Iwamura, T., M. Yoneyama, K. Yamaguchi, W. Suhara, W. Mori, K. Shiota, Y. Okabe, H. Namiki, and T. Fujita. 2001. Induction of IRF-3/-7 kinase and NF-κB in response to double-stranded RNA and virus infection: common and unique pathways. Genes Cells 6:375-388.
20. Jamaluddin, M., S. Wang, R. P. Garofalo, T. Elliott, A. Casola, S. Baron, and A. R. Brasier. 2001. IFN-β mediates coordinate expression of antigen-processing genes in RSV-infected pulmonary epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 280:L248-L257.
21. Johnston, S. L., P. K. Pattemore, G. Sanderson, S. Smith, F. Lampe, L. Josephs, P. Symington, S. O'Toole, S. H. Myint, D. A. Tyrrell, et al. 1995. Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. BMJ 310:1225-1229.
22. Kim, J., S. P. Sanders, E. S. Siekierski, V. Casolaro, and D. Proud. 2000. Role of NF-kappa B in cytokine production induced from human airway epithelial cells by rhinovirus infection. J. Immunol. 165:3384-3392.
23. Kohl, A., R. F. Clayton, F. Weber, A. Bridgen, R. E. Randall, and R. M. Elliott. 2003. Bunyamwera virus nonstructural protein NSs counteracts interferon regulatory factor 3-mediated induction of early cell death. J. Virol. 77:7999-8008.
24. Kumar, K. P., K. M. McBride, B. K. Weaver, C. Dingwall, and N. C. Reich. 2000. Regulated nuclear-cytoplasmic localization of interferon regulatory factor 3, a subunit of double-stranded RNA-activated factor 1. Mol. Cell. Biol. 20:4159-4168.
25. Lin, R., C. Heylbroeck, P. M. Pitha, and J. Hiscott. 1998. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 18:2986-2996.
26. Lin, R., R. S. Noyce, S. E. Collins, R. D. Everett, and K. L. Mossman. 2004. The herpes simplex virus ICP0 RING finger domain inhibits IRF3- and IRF7-mediated activation of interferon-stimulated genes. J. Virol. 78:1675-1684.
27. Loveys, D. A., S. Kulkarni, and P. L. Atreya. 2000. Role of type I IFNs in the in vitro attenuation of live, temperature-sensitive vaccine strains of human respiratory syncytial virus. Virology 271:390-400.
28. McMillan, J. A., L. B. Weiner, A. M. Higgins, and K. Macknight. 1993. Rhinovirus infection associated with serious illness among pediatric patients. Pediatr. Infect. Dis. J. 12:321-325.
29. Monto, A. S., A. M. Fendrick, and M. W. Sarnes. 2001. Respiratory illness caused by picornavirus infection: a review of clinical outcomes. Clin. Ther. 23:1615-1627.
30. Mori, M., M. Yoneyama, T. Ito, K. Takahashi, F. Inagaki, and T. Fujita. 2004. Identification of Ser-386 of interferon regulatory factor 3 as critical target for inducible phosphorylation that determines activation. J. Biol. Chem. 279:9698-9702.
31. Neznanov, N., K. M. Chumakov, L. Neznanova, A. Almasan, A. K. Banerjee, and A. V. Gudkov. 2005. Proteolytic cleavage of the p65-RelA subunit of NF-κB during poliovirus infection. J. Biol. Chem. 280:24153-24158.
32. Olson, M. O., K. Guetzow, and H. Busch. 1981. Localization of phosphoprotein C23 in nucleoli by immunological methods. Exp. Cell Res. 135:259-265.
33. Pahl, H. L. 1999. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18:6853-6866.
34. Papi, A., and S. L. Johnston. 1999. Respiratory epithelial cell expression of vascular cell adhesion molecule-1 and its up-regulation by rhinovirus infection via NF-κB and GATA transcription factors. J. Biol. Chem. 274:30041-30051.
35. Papi, A., and S. L. Johnston. 1999. Rhinovirus infection induces expression of its own receptor intercellular adhesion molecule 1 (ICAM-1) via increased NF-κB-mediated transcription. J. Biol. Chem. 274:9707-9720.
36. Peng, T., T. R, Golub, and D. M. Sabatini. 2002. The immunosuppressant rapamycin mimics a starvation-like signal distinct from amino acid and glucose deprivation. Mol. Cell. Biol. 22:5575-5584.
37. Raj, N. B., and P. M. Pitha. 1980. The messenger RNA sequences in human fibroblast cells induced with poly rI.rC to produce interferon. Nucleic Acids Res. 8:3427-3437.
38. Richtsteiger, R., C. Henke-Gendo, M. Schmidtke, G. Harste, and A. Heim. 2003. Quantitative multiplex real-time PCR for the sensitive detection of interferon beta gene induction and viral suppression of interferon beta expression. Cytokine 24:190-200.
39. Ronco, L. V., A. Y. Karpova, M. Vidal, and P. M. Howley. 1998. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev. 12:2061-2072.
40. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809.
41. Schroth, M. K., E. Grimm, P. Frindt, D. M. Galagan, S. I. Konno, R. Love, and J. E. Gern. 1999. Rhinovirus replication causes RANTES production in primary bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 20:1220-1228.
42. Schweizer, M., and E. Peterhans. 2001. Noncytopathic bovine viral diarrhea virus inhibits double-stranded RNA-induced apoptosis and interferon synthesis. J. Virol. 75:4692-4698.
43. Servant, M. J., N. Grandvaux, B. R. tenOever, D. Duguay, R. Lin, and J. Hiscott. 2003. Identification of the minimal phosphoacceptor site required for in vivo activation of interferon regulatory factor 3 in response to virus and double-stranded RNA. J. Biol. Chem. 278:9441-9447.
44. Servant, M. J., B. ten Oever, C. LePage, L. Conti, S. Gessani, I. Julkunen, R. Lin, and J. Hiscott. 2001. Identification of distinct signaling pathways leading to the phosphorylation of interferon regulatory factor 3. J. Biol. Chem. 276:355-363.
45. Spiegel, M., A. Pichlmair, L. Martinez-Sobrido, J. Cros, A. Garcia-Sastre, O. Haller, and F. Weber. 2005. Inhibition of beta interferon induction by severe acute respiratory syndrome coronavirus suggests a two-step model for activation of interferon regulatory factor 3. J. Virol. 79:2079-2086.
46. Stoker, D., J. Kiernat, and C. Gauntt. 1973. Interferon induction by rhinoviruses and effect of interferon on rhinovirus yields in human cell lines. Proc. Soc. Exp. Biol. Med. 143:23-27.
47. Subauste, M. C., D. B. Jacoby, S. M. Richards, and D. Proud. 1995. Infection of a human respiratory epithelial cell line with rhinovirus. Induction of cytokine release and modulation of susceptibility to infection by cytokine exposure. J. Clin. Investig. 96:549-557.
48. Suhara, W., M. Yoneyama, I. Kitabayashi, and T. Fujita. 2002. Direct involvement of CREB-binding protein/p300 in sequence-specific DNA binding of virus-activated interferon regulatory factor-3 holocomplex. J. Biol. Chem. 277:22304-22313.
49. Suzuki, T., M. Yamaya, M. Kamanaka, Y. X. Jia, K. Nakayama, M. Hosoda, N. Yamada, H. Nishimura, K. Sekizawa, and H. Sasaki. 2001. Type 2 rhinovirus infection of cultured human tracheal epithelial cells: role of LDL receptor. Am. J. Physiol. Lung Cell. Mol. Physiol. 280:L409-L420.
50. Talon, J., C. M. Horvath, R. Polley, C. F. Basler, T. Muster, P. Palese, and A. Garcia-Sastre. 2000. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J. Virol. 74:7989-7996.
51. Terajima, M., M. Yamaya, K. Sekizawa, S. Okinaga, T. Suzuki, N. Yamada, K. Nakayama, T. Ohrui, T. Oshima, Y. Numazaki, and H. Sasaki. 1997. Rhinovirus infection of primary cultures of human tracheal epithelium: role of ICAM-1 and IL-1beta. Am. J. Physiol. 273:L749-L759.
52. Thomas, D., G. Blakqori, V. Wagner, M. Banholzer, N. Kessler, R. M. Elliott, O. Haller, and F. Weber. 2004. Inhibition of RNA polymerase II phosphorylation by a viral interferon antagonist. J. Biol. Chem. 279:31471-31477.
53. Turner, R. B. 2001. The treatment of rhinovirus infections: progress and potential. Antivir. Res. 49:1-14.
54. Unterstab, G., S. Ludwig, A. Anton, O. Planz, B. Dauber, D. Krappmann, G. Heins, C. Ehrhardt, and T. Wolff. 2005. Viral targeting of the interferon-β-inducing Traf family member-associated NF-κB activator (TANK)-binding kinase-1. Proc. Natl. Acad. Sci. USA 102:13640-13645.
55. van Dam, H., D. Wilhelm, I. Herr, A. Steffen, P. Herrlich, and P. Angel. 1995. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J. 14:1798-1811.
56. Wark, P. A., S. L. Johnston, F. Bucchieri, R. Powell, S. Puddicombe, V. Laza-Stanca, S. T. Holgate, and D. E. Davies. 2005. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J. Exp. Med. 201:937-947.
57. Weaver, B. K., K. P. Kumar, and N. C. Reich. 1998. Interferon regulatory factor 3 and CREB-binding protein/p300 are subunits of double-stranded RNA-activated transcription factor DRAF1. Mol. Cell. Biol. 18:1359-1368.
58. Weber, F., A. Bridgen, J. K. Fazakerley, H. Streitenfeld, N. Kessler, R. E. Randall, and R. M. Elliott. 2002. Bunyamwera bunyavirus nonstructural protein NSs counteracts the induction of alpha/beta interferon. J. Virol. 76:7949-7955.
59. Yang, H., C. H. Lin, G. Ma, M. Orr, M. O. Baffi, and M. G. Wathelet. 2002. Transcriptional activity of interferon regulatory factor (IRF)-3 depends on multiple protein-protein interactions. Eur. J. Biochem. 269:6142-6151.
60. Yoneyama, M., W. Suhara, and T. Fujita. 2002. Control of IRF-3 activation by phosphorylation. J. Interferon Cytokine Res. 22:73-76.
61. Yoneyama, M., W. Suhara, Y. Fukuhara, M. Fukuda, E. Nishida, and T. Fujita. 1998. Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J. 17:1087-1095.
62. Zhang, Y., B. A. Luxon, A. Casola, R. P. Garofalo, M. Jamaluddin, and A. R. Brasier. 2001. Expression of respiratory syncytial virus-induced chemokine gene networks in lower airway epithelial cells revealed by cDNA microarrays. J. Virol. 75:9044-9058.
63. Zhu, Z., W. Tang, J. M. Gwaltney, Jr., Y. Wu, and J. A. Elias. 1997. Rhinovirus stimulation of interleukin-8 in vivo and in vitro: role of NF-kappaB. Am. J. Physiol. 273:L814-L824.
64. 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-6 in vivo and in vitro. Evidence for nuclear factor kappa B-dependent transcriptional activation. J. Clin. Investig. 97:421-430.