Persistent activation of RelA by respiratory syncytial virus involves protein kinase C, underphosphorylated IκBβ, and sequestration of protein phosphatase 2A by the viral phosphoprotein

Journal of Virology

Volumn 72, Issue 7, 1998, Pages 5610-5618

  Bitko, Vira ^a   Barik, Sailen ^a  

^a UNIVERSITY OF SOUTH ALABAMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN INHIBITOR; PROTEIN KINASE C; REACTIVE OXYGEN METABOLITE;

ARTICLE; DNA BINDING; GENE ACTIVATION; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SIGNAL TRANSDUCTION; TRANSACTIVATION;

EID: 0031800762     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.7.5610-5618.1998     Document Type: Article

References (57)

1. Amtmann, E. 1996. The antiviral, antitumoural xanthate D609 is a competitive inhibitor of phosphatidylcholine-specific phospholipase C. Drugs Exp. Clin. Res. 22:287-294.
2. Ananaba, G. A., and L. J. Anderson. 1991. Antibody enhancement of respiratory syncytial virus stimulation of leukotriene production by a macrophage-like cell line. J. Virol. 65:5052-5060.
3. Anderson, L. J., and C. A. Heilman. 1995. Protective and disease-enhancing immune responses to respiratory syncytial virus. J. Infect. Dis. 171:1-7.
4. Ansai, T., L. C. Dupuy, and S. Barik. 1996. Interactions between a minimal protein serine/threonine phosphatase and its phosphopeptide substrate sequence. J. Biol. Chem. 271:24401-24407.
5. Arnold, R., B. Humbert, H. Werchau, H. Gallati, and W. Konig. 1994. Interleukin-8, interleukin-6, and soluble tumour necrosis factor receptor type I release from a human pulmonary epithelial cell line (A549) exposed to respiratory syncytial virus. Immunology 82:126-133.
6. Banerjee, A., S. Barik, and B. P. De. 1991. Gene expression of nonsegmented negative strand RNA viruses. Pharmacol. Ther. 51:47-70.
7. Barik, S. 1992. Transcription of human respiratory syncytial virus genome RNA in vitro: requirement of cellular factor(s). J. Virol. 66:6813-6818.
8. Barik, S. 1993. Expression and biochemical properties of a protein serine/ threonine phosphatase encoded by bacteriophage λ. Proc. Natl. Acad. Sci. USA 15:10633-10637.
9. 237 may play an accessory role. Virology 213:405-412.
10. Baeuerle, P. A., and T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12:141-180.
11. Becker, S., H. S. Koren, and D. C. Henke. 1993. Interleukin-8 expression in normal nasal epithelium and its modulation by infection with respiratory syncytial virus and cytokines tumor necrosis factor, interleukin-1, and interleukin-6. Am. J. Respir. Cell Mol. Biol. 8:20-27.
12. Becker, S., J. Quay, and J. Soukup. 1991. Cytokine (tumor necrosis factor, IL-6, and IL-8) production by respiratory syncytial virus-infected human alveolar macrophages. J. Immunol. 147:4307-4312.
13. Bitko, V., A. Velazquez, L. Yang, Y. C. Yang, and S. Barik. 1997. Transcriptional induction of multiple cytokines by human respiratory syncytial virus requires activation of NF-κB and is inhibited by sodium salicylate and aspirin. Virology 232:369-378.
14. Bruder, J. T., and I. Kovesdi. 1997. Adenovirus infection stimulates the Raf/MAPK signaling pathway and induces expression of interleukin-8 expression. J. Virol. 71:398-404.
15. Chen, Z., J. Hagler, V. J. Palombella, F. Melandri, D. Scherer, D. Ballard, and T. Maniatis. 1995. Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-1597.
16. Cobb, R. R., K. A. Felts, G. C. Parry, and N. Mackman. 1996. D609, a phosphatidylcholine-specific phospholipase C inhibitor, blocks interleukin-1 β-induced vascular cell adhesion molecule 1 gene expression in human endothelial cells. Mol. Pharmacol. 49:998-1004.
17. Collins, P. L. 1991. The molecular biology of human respiratory syncytial virus (RSV) of the genus Pneumovirus, p. 103-162. In D. W. Kingsbury (ed.), The paramyxoviruses. Plenum Publishing Corp., New York, N.Y.
18. Courtois, G., S. T. Whiteside, C. H. Sibley, and A. Israel. 1997. Characterization of a mutant cell line that does not activate NF-κB in response to multiple stimuli. Mol. Cell. Biol. 17:1441-1449.
19. 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. 11:1475-1489.
20. 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. I. Clin. Invest. 97:915-924.
21. Elias, J. A., T. Zheng, O. Einarsson, M. Landry, T. Trow, N. Rebert, and J. Panuska. 1994. Epithelial interleukin-11. Regulation by cytokines, respiratory syncytial virus, and retinoic acid. J. Biol. Chem. 269:22261-22268.
22. Fiedler, M. A., K. Wernke-Dollries, and J. M. Stark. 1996. Inhibition of viral replication reverses respiratory syncytial virus-induced NF-kappa B activation and interleukin-8 gene expression in A549 cells. J. Virol. 70:9079-9082.
23. Fiedler, M. A., K. Wernke-Dollries, and J. M. Stark. 1996. Mechanism of RSV-induced IL-8 gene expression in A549 cells before viral replication. Am. J. Physiol. 271:L963-L971.
24. Folgueira, L., J. A. McElhinney, G. D. Bren, W. F. MacMorran, M. T. Diaz-Meco, J. Moscat, and C. Paya. 1996. Protein kinase C-ζ mediates NF-κB activation in human immunodeficiency virus-infected monocytes. J. Virol. 70:223-231.
25. 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-β and IL-1 α. J. Immunol. 157:2506-2513.
26. Garofalo, R., M. Sabry, M. Jamaluddin, R. K. Yu, A. Casola, P. L. Ogra, and A. R. Brasier. 1996. Transcriptional activation of the interleukin-8 gene by respiratory syncytial virus infection in alveolar epithelial cells: nuclear translocation of the RelA transcription factor as a mechanism producing airway mucosal inflammation. J. Virol. 70:8773-8781.
27. Ghoda, L., X. Lin, and W. C. Greene. 1997. The 90-kDa ribosomal S6 kinase (pp90rsk) phosphorylates the N-terminal regulatory domain of IκBα and stimulates its degradation in vitro. J. Biol. Chem. 272:21281-21288.
28. Guan, K. L., and J. E. Dixon. 1991. Evidence for protein-tyrosine-phosphatase catalysis proceeding via a cysteine-phosphate intermediate. J. Biol. Chem. 266:17026-17030.
29. Hall, C. B. 1994. Prospects for a respiratory syncytial virus vaccine. Science 265:1393-1394.
30. Harhaj, E. W., and S. C. Sun. 1997. The serine/threonine phosphatase inhibitor calyculin A induces rapid degradation of IκBβ. Requirement of both the N- and C-terminal sequences. J. Biol. Chem. 272:5409-5412.
31. Heriche, J. K., F. Lebrin, T. Rabilloud, D. Leroy, E. M. Chambaz, and Y. Goldberg. 1997. Regulation of protein phosphatase 2A by direct association with casein kinase 2a. Science 276:952-955.
32. Kiss, Z., and M. Tomono. 1995. Compound D609 inhibits phorbol esterstimulated phospholipase D activity and phospholipase C-mediated phosphatidylethanolamine hydrolysis. Biochim. Biophys. Acta 1259:105-108.
33. Kopp, E., and S. Ghosh. 1994. Inhibition of NF-κB by sodium salicylate and aspirin. Science 265:956-959.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Lee, F. S., J. Hagler, Z. J. Chen, and T. Maniatis. 1997. Activation of the IκB α kinase complex by MEKK1, a kinase of the JNK pathway. Cell 88:213-222.
36. Lindholm, P. F., M. Tamami, J. Makowski, and J. N. Brady. 1996. Human T-cell lymphotropic virus type 1 Tax1 activation of NF-κB: involvement of the protein kinase C pathway. J. Virol. 70:2525-2532.
37. Maniatis, T. 1997. Catalysis by a multiprotein IκB kinase complex. Science 278:818-819.
38. Mastronarde, J. G., B. He, M. M. Monick, N. Mukaida, K. Matsushima, and G. W. Hunninghake. 1996. Induction of IL-8 gene expression by respiratory syncytial virus involves activation of NF-κB and NF-IL-6. J. Infect. Dis. 174:262-267.
39. 237 as the site of phosphorylation by cellular casein kinase II. Virology 205:93-103.
40. McKinsey, T. A., J. A. Brockman, D. C. Scherer, S. W. Al-Murrani, P. L. Green, and D. W. Ballard. 1996. Inactivation of IκBβ by the tax protein of human T-cell leukemia virus type 1: a potential mechanism for constitutive induction of NF-κB. Mol. Cell. Biol. 16:2083-2090.
41. Muller-Decker, K., E. Amtmann, and G. Sauer. 1987. Inhibition of the phosphorylation of the regulatory non-structural protein of vesicular stomatitis virus by an antiviral xanthate compound. J. Gen. Virol. 68:3045-3056.
42. Panuska, J. R., R. Merolla, N. A. Rebert, S. P. Hoffmann, P. Tsivitse, N. M. Cirino, R. H. Silverman, and J. A. Rankin. 1995. Respiratory syncytial virus induces interleukin-10 by human alveolar macrophages. Suppression of early cytokine production and implications for incomplete immunity. J. Clin. Invest. 96:2445-2453.
43. Patel, J. A., M. Kunimoto, T. C. Sim, R. Garofalo, T. Eliott, S. Baron, O. Ruuskanen, T. Chonmaitree, P. L. Ogra, and F. Schmalstieg. 1995. Interleukin-1α mediates the enhanced expression of intercellular adhesion molecule-1 in pulmonary epithelial cells infected with respiratory syncytial virus. Am. J. Respir. Cell Mol. Biol. 13:602-609.
44. Phillips, R. J., and S. Ghosh. 1997. Regulation of IκBβin WEHI 231 mature B cells. Mol. Cell. Biol. 17:4390-4396.
45. Saito, T., R. W. Deskin, A. Casola, H. Haeberle, B. Olszewska, P. B. Ernst, R. Alam, P. L. Ogra, and R. Garofalo. 1997. Respiratory syncytial virus induces selective production of the chemokine RANTES by upper airway epithelial cells. J. Infect. Dis. 175:497-504.
46. Sanchez-Seco, M. P., J. Navarro, R. Martinez, and N. Villanueva. 1995. C-terminal phosphorylation of human respiratory syncytial virus P protein occurs mainly at serine residue 232. J. Gen. Virol. 76:425-430.
47. Schutze, S., K. Potthoff, T. Machleidt, D. Berkovic, K. Wiegmann, and M. Kronke. 1992. TNF activates NF-κB by phosphatidylcholine-specific phospholipase C-induced "acidic" sphingomyelin breakdown. Cell 71:765-776.
48. Siebenlist, U., G. Franzoso, and K. Brown. 1994. Structure, regulation, and function of NF-κB. Annu. Rev. Cell Biol. 10:405-455.
49. Sontag, E., J. M. Sontag, and A. Garcia. 1997. Protein Phosphatase 2A is a critical regulator of protein kinase C ζ signaling targeted by SV40 small t to promote cell growth and NF-κB activation. EMBO J. 16:5662-5671.
50. Stankovski, I., and D. Baltimore. 1997. NF-κB activation: the IκB kinase revealed? Cell 91:299-302.
51. Stark, J. M., V. Godding, J. B. Sedgwick, W. W. Busse. 1996. Respiratory syncytial virus infection enhances neutrophil and eosinophil adhesion to cultured respiratory epithelial cells. Roles of CD18 and intercellular adhesion molecule-1. J. Immunol. 156:4774-4782.
52. Sun, S. C., S. B. Maggirwar, and E. Harhaj. 1995. Activation of NF-κB by phosphatase inhibitors involves the phosphorylation of IκBα at phosphatase 2A-sensitive sites. J. Biol. Chem. 270:18347-18351.
53. Sung, S. J., J. A. Walters, and S. M. Fu. 1992. Stimulation of tumor necrosis factor α production in human monocytes by inhibitors of protein phosphatase 1 and 2A. J. Exp. Med. 176:897-901.
54. Suyang, H., R. Phillips, I. Douglas, and S. Ghosh. 1996. Role of unphosphorylated, newly synthesized IκB β in persistent activation of NF-κB. Mol. Cell. Biol. 16:5444-5449.
55. Villanueva, N., J. Navarro, and E. Cubero. 1991. Antiviral effects of xanthate D609 on the human respiratory syncytial virus growth cycle. Virology 181: 101-108.
56. Walter, G., and M. Mumby. 1993. Protein serine/threonine phosphatases and cell transformation. Biochim. Biophys. Acta 1155:207-226.
57. Weil, R., C. Laurent-Winter, and A. Israel. 1997. Regulation of IκBβ degradation. Similarities to and differences from IκBα. J. Biol. Chem. 272:9942-9949.