Respiratory syncytial virus-induced activation of nuclear factor-kB in the lung involves alveolar macrophages and toll-like receptor 4-dependent pathways

Journal of Infectious Diseases

Volumn 186, Issue 9, 2002, Pages 1199-1206

  Haeberle, Helene A ^a,d   Takizawa, Ryuta ^a   Casola, Antonella ^a   Brasier, Allan R ^b   Dieterich, Hans Juergen ^d   Van Rooijen, Nico ^c   Gatalica, Zoran ^b   Garofalo, Roberto P ^a  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

^d UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P50; PROTEIN SUBUNIT; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; EPITHELIUM CELL; GENE ACTIVATION; GENE EXPRESSION REGULATION; IMMUNOMODULATION; IN VIVO STUDY; INFLAMMATION; INFLAMMATORY CELL; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SIGNAL TRANSDUCTION;

ANIMALS; DROSOPHILA PROTEINS; HUMANS; LUNG; MACROPHAGES, ALVEOLAR; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; NF-KAPPA B; PROTEIN SUBUNITS; RECEPTORS, CELL SURFACE; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

EID: 0036838764     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/344644     Document Type: Article

References (50)

1. Hall CB. Respiratory syncytial virus and parainfluenza virus. N Engl J Med 2001;344:1917-28.
2. Garofalo RP, Welliver RC, Ogra PL. Clinical aspects of bronchial reactivity and cell-virus interaction. In: Ogra PL, Lamm ME, Bienenstock J, Mestecky J, Strober W, McGhee JR, eds. Mucosal Immunology. 2nd Ed. San Diego: Academic Press, 1999:1223-37.
3. Graham BS, Johnson TR, Peebles RS. Immune-mediated disease pathogenesis in respiratory syncytial virus infection. Immunopharmacology 2000; 48:237-47.
4. Zhang Y, Luxon B, Casola A, Garofalo RP, Jamaluddin M, Brasier AR. Expression of RSV-induced chemokine gene networks in lower airway epithelial cells revealed by cDNA microarrays. J Virol 2001;75:9044-58.
5. Patel JA, Kunimoto M, Sim TC, et al. Interteukin-1 alpha mediates the enhanced expression of intercellular adhesion molecule-1 in pulmonary epithelial cells infected with respiratory syncytial virus. Am J Respir Cell Mol Biol 1995;13:602-9.
6. Becker S, Quay J, Soukup J. Cytokine (tumor necrosis factor, IL-6, and IL-8) production by respiratory syncytial virus-infected human alveolar macrophages. J Immunol 1991;147:4307-12.
7. Panuska JR, Merolla R, Rebert NA, et al. Respiratory syncytial virus induces interleukin-10 by human alveolar macrophages: Suppression of early cytokine production and implications for incomplete immunity. J Clin Invest 1995;96:2445-53.
8. Mastronarde JG, Monick MM, Hunninghake GW. Oxidant tone regulates 1L-8 production in epithelium infected with respiratory syncytial virus. Am J Respir Cell Mol Biol 1995;13:237-44.
9. Saito T, Deskin RW, Casola A. et al. Respiratory syncytial virus induces selective production of the chemokine RANTES by upper airway epithelial cells. J Infect Dis 1997;175:497-504.
10. Olszewska-Pazdrak B, Casola A, Saito T, et al. Cell-specific expression of RANTES, MCP-1, and MIP-1 alpha by lower airway epithelial cells and eosinophils infected with respiratory syncytial virus. J Virol 1998; 72:4756-64.
11. Garofalo R, Mei F, Espejo R, et al. Respiratory syncytial virus infection of human respiratory epithelial cells up-regulates class I MHC expression through the induction of IFN-β and IL-1α. J Immunol 1997;157:2506-13.
12. Matsuzaki Z, Okamoto Y, Sarashina N, Ito E, Togawa K, Saito I. Induction of intercellular adhesion molecule-1 in human nasal epithelial cells during respiratory syncytial virus infection. Immunology 1996;88:565-8.
13. Jamaluddin M, Wang S, Garofalo RP, et al. IFN-beta mediates coordinate expression of antigen-processing genes in RSV-infected pulmonary epithelial cells. Am J Physiol Lung Cell Mol Physiol 2001;280:L248-57.
14. Haeberle HA, Kuziel WA, Dieterich HJ, Casola A, Gatalica Z, Garofalo RP. Inducible expression of inflammatory chemokines in respiratory syncytial virus-infected mice: Role of MIP-1α in lung pathology. J Virol 2000;75: 878-90.
15. Tripp RA, Jones L, Anderson LJ. Respiratory syncytial virus G and/or SH glycoproteins modify CC and CXC chemokine mRNA expression in the BALB/c mouse. J Virol 2000;74:6227-9.
16. Hussell T, Pennycook A, Openshaw PJ. Inhibition of tumor necrosis factor reduces the severity of virus-specific lung immunopathology. Eur J Immunol 2001;31:2566-73.
17. Garofalo RP, Patti J, Hintz KA, Hill V, Ogra PL, Welliver RC. Macrophage inflammatory protein-1α, and not T-helper type 2 cytokines, is associated with severe forms of bronchiolitis. J Infect Dis 2001;184:393-9.
18. Harrison AM, Bonville CA, Rosenberg HF, Domachowske JB. Respiratory syncytial virus-induced chemokine expression in the lower airways: Eosinophil recruitment and degranulation. Am J Respir Crit Care Med 1999; 159:1918-24.
19. Barnes PJ, Karin M. Nuclear factor-κB: A pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 1997;336:1066-71.
20. Beg AA, Baldwin ASJ. The I kappa B proteins: Multifunctional regulators of Rel/NF-kappa B transcription factors. Genes Dev 1993;7:2064-70.
21. Karin M, Delhase M. The I kappa B kinase (IKK) and NF-kappa B: Key elements of proinflammatory signalling. Semin Immunol 2000;12:85-98.
22. Garofalo RP, Sabry M, Jamaluddin M, et al. 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 1996;70:8773-81.
23. Mastronarde JG, He B, Monick MM, Mukaida N, Matsushima K, Hunninghake GW. Induction of interleukin (IL)-8 gene expression by respiratory syncytial virus involves activation of nuclear factor (NF)-κB and NF-IL-6. J Infect Dis 1996;174:262-7.
24. Bitko V, Velazquez A, Yank L, Yang Y-C, Barik S. Transcriptional induction of multiple cytokines by human respiratory syncytial virus requires activation of NF-κB and is inhibited by sodium salicylate and aspirin. Virology 1997;232:369-78.
25. Jamaluddin M, Casola A, Garofalo RP. et al. The major component of IkBα proteolysis occurs independently of the proteasome pathway in respiratory syncytial virus-infected pulmonary epithelial cells. J Virol 1998;72:4849-57.
26. Fiedler MA, Wernke-Dollries K, Stark JM. Inhibition of viral replication reverses respiratory syncytial virus-induced NF-κB activation and interleukin-8 gene expression in A549 cells. J Virol 1996;70:9079-82.
27. Thomas H, Friedland JS, Sharland M, Becker S. Respiratory syncytial virus-induced RANTES production from human bronchial epithelial cells is dependent on nuclear factor-κB nuclear binding and is inhibited by adenovirus-mediated expression of inhibitor of κBα. J Immunol 1998;161: 1007-16.
28. Casola A, Garofalo RP, Haeberle H, et al. Multiple cis regulatory elements control RANTES promoter activity in alveolar epithelial cells infected with respiratory syncytial virus. J Virol 2001;75:6428-39.
29. Kisch AL, Johnson KM. A plaque assay for respiratory syncytial virus. Proc Soc Exp Biol Med 1963;112:583.
30. Jamaluddin M, Garofalo RP, Ogra PL, Brasier AR. Inducible translational regulation of the NF-IL6 transcription factor by respiratory syncytial virus infection in pulmonary epithelial cells. J Virol 1996;70:1554-63.
31. Graham BS, Perkins MD, Wright PF, Karzon DT. Primary respiratory syncytial virus infection in mice. J Med Virol 1988;26:153-62.
32. Bohrer H, Qiu F, Zimmermann T, et al. Role of NF-κB in the mortality of sepsis. J Clin Invest 1997;100:972-85.
33. Thepen T, McMenamin C, Oliver J, Kraal G, Holt PG. Regulation of immune response to inhaled antigen by alveolar macrophages: Differential effects of in vivo alveolar macrophage elimination on the induction of tolerance vs. immunity. Eur J Immunol 1991;21:2845-50.
34. Berg JT, Lee ST, Thepen T, Lee CY, Tsan MF. Depletion or alveolar macrophages by liposome-encapsulated dichloromethylene diphosphonate. J Appl Physiol 1993;74:2812-19.
35. van Rooijen N, Sanders A. Liposome mediated depletion of macrophages: Mechanism of action, preparation of liposomes and applications. J Immunol Methods 1994;174:83-93.
36. Stadnyk AW, Gillan TL, Anderson R. Respiratory syncytial virus triggers synthesis of IL-6 in BALB/c mouse alveolar macrophages in the absence of virus replication. Cell Immunol 1997;176:122-6.
37. Leemans JC, Juffermans NP, Florquin S, et al. Depletion of alveolar macrophages exerts protective effects in pulmonary tuberculosis in mice. J Immunol 2001;166:4604-11.
38. Kurt-Jones EA, Popova L, Kwinn L, et al. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat Immunol 2000;1:398-401.
39. Haynes LM, Moore DD, Kurt-Jones EA, Finberg RW, Anderson LJ, Tripp RA. Involvement of toll-like receptor 4 in innate immunity to respiratory syncytial virus. J Virol 2001;75:10730-7.
40. Poltorak A, He X, Smirnova I, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 1998;282:2085-8.
41. Ruuskanen O, Ogra PL. Respiratory syncytial virus. Curr Probl Pediatr 1993;23:50-79.
42. Tian B, Zhang Y, Luxon B, et al. Identification of NF-κB-dependent gene networks in respiratory syncytial virus-infected cells. J Virol 2002;76: 6800-14.
43. Taylor G, Stott EJ, Hughes M, Collins AP. Respiratory syncytial virus infection in mice. Infect Immun 1984;43:649-55.
44. Lentsch AB, Shanley TP, Sarma V, Ward PA. In vivo suppression of NF-κB and preservation of IkBα by interleukin-10 and interleukin-13. J Clin Invest 1997;100:2443-8.
45. Lentsch AB, Czermak BJ, Bless NM, Ward PA. NF-kappaB activation during IgG immune complex-induced lung injury: Requirements for TNF-alpha and IL-1beta but not complement. Am J Pathol 1998;152:1327-36.
46. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature 2000;406:782-7.
47. Hoshino K, Takeuchi O, Kawai T, et al. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: Evidence for TLR4 as the Lps gene product. J Immunol 1999;162:3749-52.
48. Muzio M, Bosisio D, Polentarutti N, et al. Differential expression and regtilation of toll-like receptors (TLR) in human leukocytes: Selective expression of TLR3 in dendritic cells. J Immunol 2000;164:5998-6004.
49. Akira S, Takeda K, Kaisho T. Toll-like receptors: Critical proteins linking innate and acquired immunity. Nat Immunol 2001;2:675-80.
50. Garofalo RP, Haeberle H. Epithelial regulation of innate immunity to respiratory syncytial virus. Am J Respir Cell Mol Biol 2000;23:581-5.