The Major Component of Ikappa Balpha  Proteolysis Occurs Independently of the Proteasome Pathway in Respiratory Syncytial Virus-Infected Pulmonary Epithelial Cells

This Article

	Full Text
	Full Text (PDF)
	Alert me when this article is cited
	Alert me if a correction is posted

Services

	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new issues of the journal
	Download to citation manager
	Reprints and Permissions
	Copyright Information
	Books from ASM Press
	MicrobeWorld

Citing Articles

	Citing Articles via HighWire
	Citing Articles via Google Scholar

Google Scholar

	Articles by Jamaluddin, M.
	Articles by Brasier, A. R.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Jamaluddin, M.
	Articles by Brasier, A. R.

Previous Article | Next Article

J Virol, June 1998, p. 4849-4857, Vol. 72, No. 6
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

The Major Component of I $kappa$ B $alpha$ Proteolysis Occurs Independently of the Proteasome Pathway in Respiratory Syncytial Virus-Infected Pulmonary Epithelial Cells

Mohammad Jamaluddin,¹ Antonella Casola,² Roberto P. Garofalo,² Youqi Han,¹ Todd Elliott,² Pearay L. Ogra,² and Allan R. Brasier¹^,^*

Department of Medicine and Sealy Center for Molecular Science¹ and Department of Pediatrics,² University of Texas Medical Branch, Galveston, Texas 77555-1060

Received 8 October 1997/Accepted 24 February 1998

Previously we showed that infection of human type II airway epithelial (A549) cells with purified respiratory syncytial virus(pRSV) induced interleukin-8 transcription by a mechanism involvingcytokine-inducible cytoplasmic-nuclear translocation of the RelAtranscription factor. In unstimulated cells, RelA is tetheredin the cytoplasm by association with the I $kappa$ B inhibitor and canbe released only following I $kappa$ B degradation. In this study, weexamined the spectrum of I $kappa$ B isoform expression and kinetics ofproteolysis of the isoforms in A549 cells following pRSV infection.In contrast to the rapid and robust activation of RelA DNA bindingthat peaked within 15 min of treatment produced by the prototypicactivator tumor necrosis factor alpha (TNF- $alpha$ ), pRSV produced aweaker increase in RelA binding that began at 3 h and did notpeak until 24 h after infection. A549 cells expressed the I $kappa$ Binhibitory subunits I $kappa$ B $alpha$ , I $kappa$ B $beta$ , and p105; however, following eitherstimulus, only the I $kappa$ B $alpha$ and I $kappa$ B $beta$ steady-state levels declinedin parallel with the increase in RelA DNA-binding activity. The>120-min half-life of I $kappa$ B $alpha$ in control cells was shortened to 5min in TNF- $alpha$ -stimulated cells and to 90 min in pRSV-infected cells.Although I $kappa$ B $alpha$ was resynthesized within 30 min following recombinanthuman TNF $alpha$ treatment due to a robust 25-fold increase of I $kappa$ B $alpha$ mRNA expression (the RelA:I $kappa$ B $alpha$ positive feedback loop), followingpRSV infection, there was no reaccumulation of I $kappa$ B $alpha$ protein, asinfected cells produced only a 3-fold increase in I $kappa$ B $alpha$ mRNA at24 h, indicating the RelA:I $kappa$ B $alpha$ positive feedback loop was insufficientto restore control I $kappa$ B $alpha$ levels. I $kappa$ B $alpha$ proteolysis induced by TNF- $alpha$ occurred through the 26S proteasome, as both 26S proteasome activityand I $kappa$ B $alpha$ proteolysis were blocked by specific inhibitors lactacystin,MG-132, and ZLLF-CHO. Although total proteasome activity in 24-hpRSV-infected lysates increased twofold, its activity was >90%inhibited by the proteasome inhibitors; surprisingly, however,I $kappa$ B $alpha$ proteolysis was not. We conclude that RSV infection producesI $kappa$ B $alpha$ proteolysis through a mechanism primarily independent ofthe proteasome pathway.

^* Corresponding author. Mailing address: Division of Endocrinology, University of Texas Medical Branch, 301 University Blvd.,MRB 8.138, Galveston, TX 77555-1060. Phone: (409) 772-2824. Fax:(409) 772-8709. E-mail: arbrasie{at}utmb.edu.

J Virol, June 1998, p. 4849-4857, Vol. 72, No. 6
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

This article has been cited by other articles:

Liu, P., Li, K., Garofalo, R. P., Brasier, A. R. (2008). Respiratory Syncytial Virus Induces RelA Release from Cytoplasmic 100-kDa NF-{kappa}B2 Complexes via a Novel Retinoic Acid-inducible Gene-I{middle dot}NF-{kappa}B-inducing Kinase Signaling Pathway. J. Biol. Chem. 283: 23169-23178 [Abstract] [Full Text]
Fink, K., Duval, A., Martel, A., Soucy-Faulkner, A., Grandvaux, N. (2008). Dual Role of NOX2 in Respiratory Syncytial Virus- and Sendai Virus-Induced Activation of NF-{kappa}B in Airway Epithelial Cells. J. Immunol. 180: 6911-6922 [Abstract] [Full Text]
Liu, P., Jamaluddin, M., Li, K., Garofalo, R. P., Casola, A., Brasier, A. R. (2007). Retinoic Acid-Inducible Gene I Mediates Early Antiviral Response and Toll-Like Receptor 3 Expression in Respiratory Syncytial Virus-Infected Airway Epithelial Cells. J. Virol. 81: 1401-1411 [Abstract] [Full Text]
Jamaluddin, M., Choudhary, S., Wang, S., Casola, A., Huda, R., Garofalo, R. P., Ray, S., Brasier, A. R. (2005). Respiratory Syncytial Virus-Inducible BCL-3 Expression Antagonizes the STAT/IRF and NF-{kappa}B Signaling Pathways by Inducing Histone Deacetylase 1 Recruitment to the Interleukin-8 Promoter. J. Virol. 79: 15302-15313 [Abstract] [Full Text]
Choudhary, S., Boldogh, S., Garofalo, R., Jamaluddin, M., Brasier, A. R. (2005). Respiratory Syncytial Virus Influences NF-{kappa}B-Dependent Gene Expression through a Novel Pathway Involving MAP3K14/NIK Expression and Nuclear Complex Formation with NF-{kappa}B2. J. Virol. 79: 8948-8959 [Abstract] [Full Text]
Tian, B., Nowak, D. E., Jamaluddin, M., Wang, S., Brasier, A. R. (2005). Identification of Direct Genomic Targets Downstream of the Nuclear Factor-{kappa}B Transcription Factor Mediating Tumor Necrosis Factor Signaling. J. Biol. Chem. 280: 17435-17448 [Abstract] [Full Text]
Clifton, D. R., Rydkina, E., Freeman, R. S., Sahni, S. K. (2005). NF-{kappa}B Activation during Rickettsia rickettsii Infection of Endothelial Cells Involves the Activation of Catalytic I{kappa}B Kinases IKK{alpha} and IKK{beta} and Phosphorylation-Proteolysis of the Inhibitor Protein I{kappa}B{alpha}. Infect. Immun. 73: 155-165 [Abstract] [Full Text]
Brasier, A. R., Spratt, H., Wu, Z., Boldogh, I., Zhang, Y., Garofalo, R. P., Casola, A., Pashmi, J., Haag, A., Luxon, B., Kurosky, A. (2004). Nuclear Heat Shock Response and Novel Nuclear Domain 10 Reorganization in Respiratory Syncytial Virus-Infected A549 Cells Identified by High-Resolution Two-Dimensional Gel Electrophoresis. J. Virol. 78: 11461-11476 [Abstract] [Full Text]
Haeberle, H. A., Casola, A., Gatalica, Z., Petronella, S., Dieterich, H.-J., Ernst, P. B., Brasier, A. R., Garofalo, R. P. (2004). I{kappa}B Kinase Is a Critical Regulator of Chemokine Expression and Lung Inflammation in Respiratory Syncytial Virus Infection. J. Virol. 78: 2232-2241 [Abstract] [Full Text]
Zhang, Y., Jamaluddin, M., Wang, S., Tian, B., Garofalo, R. P., Casola, A., Brasier, A. R. (2003). Ribavirin Treatment Up-Regulates Antiviral Gene Expression via the Interferon-Stimulated Response Element in Respiratory Syncytial Virus-Infected Epithelial Cells. J. Virol. 77: 5933-5947 [Abstract] [Full Text]
Tian, B., Brasier, A. R. (2003). Identification of a Nuclear Factor Kappa B-dependent Gene Network. Recent Prog Horm Res 58: 95-130 [Abstract] [Full Text]
Luo, H., Zhang, J., Dastvan, F., Yanagawa, B., Reidy, M. A., Zhang, H. M., Yang, D., Wilson, J. E., McManus, B. M. (2002). Ubiquitin-Dependent Proteolysis of Cyclin D1 Is Associated with Coxsackievirus-Induced Cell Growth Arrest. J. Virol. 77: 1-9 [Abstract] [Full Text]
Tian, B., Zhang, Y., Luxon, B. A., Garofalo, R. P., Casola, A., Sinha, M., Brasier, A. R. (2002). Identification of NF-{kappa}B-Dependent Gene Networks in Respiratory Syncytial Virus-Infected Cells. J. Virol. 76: 6800-6814 [Abstract] [Full Text]
Haeberle, H. A., Nesti, F., Dieterich, H.-J., Gatalica, Z., Garofalo, R. P. (2002). Perflubron Reduces Lung Inflammation in Respiratory Syncytial Virus Infection by Inhibiting Chemokine Expression and Nuclear Factor-{kappa}B Activation. Am. J. Respir. Crit. Care Med. 165: 1433-1438 [Abstract] [Full Text]
Zhang, Y., Luxon, B. A., Casola, A., Garofalo, R. P., Jamaluddin, M., Brasier, A. R. (2001). Expression of Respiratory Syncytial Virus-Induced Chemokine Gene Networks in Lower Airway Epithelial Cells Revealed by cDNA Microarrays. J. Virol. 75: 9044-9058 [Abstract] [Full Text]
Casola, A., Garofalo, R. P., Haeberle, H., Elliott, T. F., Lin, R., Jamaluddin, M., Brasier, A. R. (2001). Multiple cis Regulatory Elements Control RANTES Promoter Activity in Alveolar Epithelial Cells Infected with Respiratory Syncytial Virus. J. Virol. 75: 6428-6439 [Abstract] [Full Text]
Jamaluddin, M., Wang, S., Garofalo, R. P., Elliott, T., Casola, A., Baron, S., Brasier, A. R. (2001). IFN-{beta} mediates coordinate expression of antigen-processing genes in RSV-infected pulmonary epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 280: L248-L257 [Abstract] [Full Text]
Lee, C. G., Yoon, H. J., Zhu, Z., Link, H., Wang, Z., Gwaltney, J. M. Jr., Landry, M., Elias, J. A. (2000). Respiratory Syncytial Virus Stimulation of Vascular Endothelial Cell Growth Factor/Vascular Permeability Factor. Am. J. Respir. Cell Mol. Bio. 23: 662-669 [Abstract] [Full Text]
Thomas, L. H., Wickremasinghe, M. I. Y., Sharland, M., Friedland, J. S. (2000). Synergistic Upregulation of Interleukin-8 Secretion from Pulmonary Epithelial Cells by Direct and Monocyte-Dependent Effects of Respiratory Syncytial Virus Infection. J. Virol. 74: 8425-8433 [Abstract] [Full Text]
Herbein, G., O'brien, W. A. (2000). Tumor Necrosis Factor (TNF)-{alpha} and TNF Receptors in Viral Pathogenesis. Exp. Biol. Med. 223: 241-257 [Abstract] [Full Text]
Jamaluddin, M., Meng, T., Sun, J., Boldogh, I., Han, Y., Brasier, A. R. (2000). Angiotensin II Induces Nuclear Factor (NF)-{kappa}B1 Isoforms to Bind the Angiotensinogen Gene Acute-Phase Response Element: A Stimulus-Specific Pathway for NF-{kappa}B Activation. Mol. Endocrinol. 14: 99-113 [Abstract] [Full Text]
Vlahopoulos, S., Boldogh, I., Casola, A., Brasier, A. R. (1999). Nuclear Factor-kappa B-Dependent Induction of Interleukin-8 Gene Expression by Tumor Necrosis Factor alpha : Evidence for an Antioxidant Sensitive Activating Pathway Distinct From Nuclear Translocation. Blood 94: 1878-1889 [Abstract] [Full Text]
Fiedler, M. A., Wernke-Dollries, K. (1999). Incomplete Regulation of NF-kappa B by Ikappa Balpha during Respiratory Syncytial Virus Infection in A549 Cells. J. Virol. 73: 4502-4507 [Abstract] [Full Text]
Han, Y., Weinman, S., Boldogh, I., Walker, R. K., Brasier, A. R. (1999). Tumor Necrosis Factor-alpha -inducible Ikappa Balpha Proteolysis Mediated by Cytosolic m-Calpain. A MECHANISM PARALLEL TO THE UBIQUITIN-PROTEASOME PATHWAY FOR NUCLEAR FACTOR-kappa B ACTIVATION. J. Biol. Chem. 274: 787-794 [Abstract] [Full Text]
Han, Y., Meng, T., Murray, N. R., Fields, A. P., Brasier, A. R. (1999). Interleukin-1-induced Nuclear Factor-kappa B-Ikappa Balpha Autoregulatory Feedback Loop in Hepatocytes. A ROLE FOR PROTEIN KINASE Calpha IN POST-TRANSCRIPTIONAL REGULATION OF Ikappa Balpha RESYNTHESIS. J. Biol. Chem. 274: 939-947 [Abstract] [Full Text]
Kouba, D. J., Nakano, H., Nishiyama, T., Kang, J., Uitto, J., Mauviel, A. (2001). Tumor Necrosis Factor-alpha Induces Distinctive NF-kappa B Signaling within Human Dermal Fibroblasts. J. Biol. Chem. 276: 6214-6224 [Abstract] [Full Text]

J. Bacteriol.	Mol. Cell. Biol.	Microbiol. Mol. Biol. Rev.

Clin. Vaccine Immunol.	ALL ASM JOURNALS

The Major Component of IB Proteolysis Occurs Independently of the Proteasome Pathway in Respiratory Syncytial Virus-Infected Pulmonary Epithelial Cells

The Major Component of I $kappa$ B $alpha$ Proteolysis Occurs Independently of the Proteasome Pathway in Respiratory Syncytial Virus-Infected Pulmonary Epithelial Cells