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A Potential Respiratory Syncytial Virus (RSV) Infection Respiratory Syncytial Virus (RSV) Infection Induces Cyclooxygenase 2: A Potential Target for RSV Therapy This information is current as Joann Y. Richardson, Martin G. Ottolini, Lioubov Pletneva, of September 27, 2021. Marina Boukhvalova, Shuling Zhang, Stefanie N. Vogel, Gregory A. Prince and Jorge C. G. Blanco J Immunol 2005; 174:4356-4364; ; doi: 10.4049/jimmunol.174.7.4356 http://www.jimmunol.org/content/174/7/4356 Downloaded from References This article cites 70 articles, 27 of which you can access for free at: http://www.jimmunol.org/content/174/7/4356.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 27, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2005 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Respiratory Syncytial Virus (RSV) Infection Induces Cyclooxygenase 2: A Potential Target for RSV Therapy1 Joann Y. Richardson,* Martin G. Ottolini,* Lioubov Pletneva,§ Marina Boukhvalova,§ Shuling Zhang,† Stefanie N. Vogel,‡ Gregory A. Prince,§ and Jorge C. G. Blanco2§ Cyclooxygenases (COXs) are rate-limiting enzymes that initiate the conversion of arachidonic acid to prostanoids. COX-2 is the inducible isoform that is up-regulated by proinflammatory agents, initiating many prostanoid-mediated pathological aspects of inflammation. The roles of cyclooxygenases and their products, PGs, have not been evaluated during respiratory syncytial virus (RSV) infection. In this study we demonstrate that COX-2 is induced by RSV infection of human lung alveolar epithelial cells with the concomitant production of PGs. COX-2 induction was dependent on the dose of virus and the time postinfection. PG pro- duction was inhibited preferentially by NS-398, a COX-2-specific inhibitor, and indomethacin, a pan-COX inhibitor, but not by SC-560, a COX-1-specific inhibitor. In vivo, COX-2 mRNA expression and protein production were strongly induced in the lungs Downloaded from and cells derived from bronchioalveolar lavage of cotton rats infected with RSV. The pattern of COX-2 expression in vivo in lungs is cyclical, with a final peak on day 5 that correlates with maximal histopathology. Treatment of cotton rats with indomethacin significantly mitigated lung histopathology produced by RSV. The studies described in this study provide the first evidence that COX-2 is a potential therapeutic target in RSV-induced disease. The Journal of Immunology, 2005, 174: 4356–4364. 3 espiratory syncytial virus (RSV) is the leading viral 10). Many inflammatory mediators induced in the lung by RSV are http://www.jimmunol.org/ cause of death in children under 1 year of age and is an effective inducers of the cyclooxygenase 2 (COX-2) in lung epithelial R increasing cause of morbidity and mortality in transplant and inflammatory cells (11–15). The expressions of COX-2 and its patients and the elderly (1–3). RSV causes upper and lower respi- products, PGs and thromboxanes (TBx), have been correlated with ratory tract infections, occasionally leading to severe bronchiolitis the development of many inflammatory processes (16, 17), some of and pneumonia. In addition, RSV bronchiolitis has been associated which occur during viral infection (e.g., regulatory effects on the with the development of recurrent episodes of bronchiolar obstruc- immune response, vascular tone, platelets aggregation, airway remod- tion, specific IgE production, and establishment of asthma (4–6). eling, allergic processes, etc.). Moreover, RSV induces the production It is unclear why children, the elderly, and the immunosuppressed of PGE2 in cultures of human monocytes and dendritic cells (18). The are at much higher risk for severe disease; however, an RSV- potent physiologic effects of PGs and TBx and their possible role in by guest on September 27, 2021 induced immune pathological mechanism has long been suspected. RSV infection suggest that these mediators should be considered as Yet there is no safe and effective vaccine against RSV. Passive potential important factors in the RSV disease process. The animal anti-RSV Ab, although effective in prophylactic settings, does not model of choice for RSV studies is the cotton rat (Sigmodon hispidus), provide any clinically beneficial outcome when applied therapeu- because it most closely resembles disease in humans (19). Preclinical tically, indicating that RSV-induced pathology is primarily the re- data from cotton rats have resulted in a successful prophylactic sult of the inflammatory response to infection, rather than a direct approach in humans (20–24). viral effect. Therefore, a combined antiviral and anti-inflammatory In this work we present data demonstrating the induction of therapy might represent the most safe and efficient treatment COX-2 expression during RSV infection in vitro, in human lung against RSV infection. alveolar epithelial cells and cotton rat macrophages, and in vivo, in During RSV infection, proinflammatory cytokines and chemo- the lungs of cotton rats infected with RSV. We present additional kines are detectable in isolates from bronchioalveolar lavage evidence that indicates the potential of nonsteroidal anti- (BAL) fluids of patients with lower respiratory tract infection (7– inflammatory drugs in the treatment of RSV-induced bronchiolitis. Materials and Methods Departments of *Pediatrics and †Microbiology and Immunology, Uniformed Services Animals ‡ University of the Health Sciences, Bethesda, MD 20814; Department of Microbiol- Inbred cotton rats (S. hispidus) were obtained from a colony maintained at ogy and Immunology, University of Maryland, Baltimore, MD 21201; and §Virion Systems, Rockville, MD 20850 Virion Systems. Cotton rats were housed in large polycarbonate rat cages with a bedding of pine shavings (Harlan Teklad) and were fed a diet of Received for publication October 9, 2003. Accepted for publication January 20, 2005. rodent chow and water. The cotton rat colony was monitored for Abs to The costs of publication of this article were defrayed in part by the payment of page paramyxoviruses, RSV, and rodent viruses; no such Abs were found. The charges. This article must therefore be hereby marked advertisement in accordance animals used for infection experiments were, on the average, 8–12 wk old with 18 U.S.C. Section 1734 solely to indicate this fact. and weighed 100 g at the time they were used. All animal experimentation 1 This work was supported by National Institutes of Health Grants RR13161-03 (to procedures were performed following National Institutes of Health and G.A.P.) and RO1AI057575-01 (to J.C.G.B. and S.N.V.). U.S. Department of Agriculture guidelines with institutional animal care 2 Address correspondence and reprint requests to Dr. Jorge C. G. Blanco, Virion and use committee approval. Systems, 9610 Medical Center Drive, Suite 100, Rockville, MD 20850. E-mail ad- Virus and tissue culture cells dress: [email protected] 3 Abbreviations used in this paper: RSV, respiratory syncytial virus; BAL, bronchoal- The Long strain (group A) of RSV was obtained from American Type veolar lavage; COX-2, cyclooxygenase 2; LT, leukotriene; m.o.i., multiplicity of in- Culture Collection. Virus stocks were prepared in HEp-2 cells and con- fection; rh, recombinant human; TBx, thromboxane. tained 1 ϫ 107.5 PFU/ml. Viral titers in stocks and lung homogenates were Copyright © 2005 by The American Association of Immunologists, Inc. 0022-1767/05/$02.00 The Journal of Immunology 4357 determined by plaque assay on HEp-2 cells (19). A549 cells were obtained the RSV F protein gene was amplified using the following primers: forward from American Type Culture Collection and were grown in DMEM sup- primer, AATCCTCAAAGCAAATGCAATTACC; and reverse primer, AT- plemented with 2 mM L-glutamine, 100 IU/ml penicillin, 100 ␮g/ml strep- GGCTCCTAGAGATGTGATAACGGAGC, using 32 (macrophages) or 25 tomycin, and 10% FBS in a humidified 37°C incubator with 5% CO2. For (A549 cells) amplification cycles and 55°C for the annealing temperature. The RSV infection, cells were seeded in a six-well plate at a density of 4 ϫ 105 product of the reaction (a 1.2-kb band) was visualized by direct ethidium cells/well 1 day before infection. The cells were generally 70–80% con- bromide staining of agarose gel after electrophoresis. fluent on the day after seeding. Purified stocks of RSV were diluted in DMEM to yield multiplicities of infection (m.o.i.) of 1, 0.5, and 0.1. The COX-2 Western blot and immunoprecipitation medium was removed from the cells and replaced with medium containing virus dilutions for 1 h, then replaced with complete DMEM. Uninfected A549 cells were homogenized in lysis buffer containing 20 mM Tris-HCl HEp-2 cell culture supernatant served as the control (mock inoculum). (pH 8), 100 mM NaCl, 1% Nonidet P-40, 4 mM DTT, 0.5 mM PMSF, 7.5 Cells were harvested at various times postinfection, and the supernatants mM sodium fluoride, 2 mM EDTA, and a mixture of protease inhibitors were stored at Ϫ70°C for quantification of PGE by ELISA (Cayman (Complete; Roche). Cell lysates were normalized by protein concentration, 2 ␮ Chemicals). For inhibition experiments of COX enzymes in A549 cells, and 40 g/lane was subjected to electrophoresis in 10% SDS-PAGE gels. infected cells were incubated with different concentrations of indomethacin Western blot analysis was used to detect COX-2 protein using a polyclonal (in saline), Indocin, a pan-COX inhibitor (Merck); NS-398 (in DMSO), a rabbit Ab (catalogue no.
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