Respiratory syncytial virus activates innate immunity through toll-like receptor 2

Journal of Virology

Volumn 83, Issue 3, 2009, Pages 1492-1500

  Murawski, Matthew R ^a   Bowen, Glennice N ^a   Cerny, Anna M ^a   Anderson, Larry J ^b   Haynes, Lia M ^b   Tripp, Ralph A ^c   Kurt Jones, Evelyn A ^a   Finberg, Robert W ^a,d  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d Department of Medicine ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL MIGRATION; CONTROLLED STUDY; FEMALE; INNATE IMMUNITY; KNOCKOUT MOUSE; LEUKOCYTE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; VIRUS REPLICATION;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; DENDRITIC CELLS; HUMANS; IMMUNITY, INNATE; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; RESPIRATORY SYNCYTIAL VIRUSES; TOLL-LIKE RECEPTOR 2;

MUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 59749092826     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00671-08     Document Type: Article

References (56)

1. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124:783-801.
2. Applequist, S. E., R. P. Wallin, and H. G. Ljunggren. 2002. Variable expression of Toll-like receptor in murine innate and adaptive immune cell lines. Int. Immunol. 14:1065-1074.
3. Awomoyi, A. A., P. Rallabhandi, T. I. Pollin, E. Lorenz, M. B. Sztein, M. S. Boukhvalova, V. G. Hemming, J. C. Blanco, and S. N. Vogel. 2007. Association of TLR4 polymorphisms with symptomatic respiratory syncytial virus infection in high-risk infants and young children. J. Immunol. 179:3171-3177.
4. Bataki, E. L., G. S. Evans, and M. L. Everard. 2005. Respiratory syncytial virus and neutrophil activation. Clin. Exp. Immunol. 140:470-477.
5. 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.
6. Becker, Y. 2006. Respiratory syncytial virus (RSV) evades the human adaptive immune system by skewing the Th1/Th2 cytokine balance toward increased levels of Th2 cytokines and IgE, markers of allergy - a review. Virus Genes 33:235-252.
7. Boukhvalova, M. S., G. A. Prince, L. Soroush, D. C. Harrigan, S. N. Vogel, and J. C. Blanco. 2006. The TLR4 agonist, monophosphoryl lipid A, attenuates the cytokine storm associated with respiratory syncytial virus vaccine-enhanced disease. Vaccine 24:5027-5035.
8. Chang, S., A. Dolganiuc, and G. Szabo. 2007. Toll-like receptors 1 and 6 are involved in TLR2-mediated macrophage activation by hepatitis C virus core and NS3 proteins. J. Leukoc. Biol. 82:479-487.
9. Compton, T., E. A. Kurt-Jones, K. W. Boehme, J. Belko, E. Latz, D. T. Golenbock, and R. W. Finberg. 2003. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J. Virol. 77:4588-4596.
10. Culley, F. J., A. M. Pennycook, J. S. Tregoning, T. Hussell, and P. J. Openshaw. 2006. Differential chemokine expression following respiratory virus infection reflects Th1- or Th2-biased immunopathology. J. Virol. 80:4521-4527.
11. Cyr, S. L., T. Jones, I. Stoica-Popescu, D. Burt, and B. J. Ward. 2007. C57Bl/6 mice are protected from respiratory syncytial virus (RSV) challenge and IL-5 associated pulmonary eosinophilic infiltrates following intranasal immunization with Protollin-eRSV vaccine. Vaccine 25:3228-3232.
12. Demedts, I. K., K. R. Bracke, T. Maes, G. F. Joos, and G. G. Brusselle. 2006. Different roles for human lung dendritic cell subsets in pulmonary immune defense mechanisms. Am. J. Respir. Cell Mol. Biol. 35:387-393.
13. Ehl, S., R. Bischoff, T. Ostler, S. Vallbracht, J. Schulte-Monting, A. Poltorak, and M. Freudenberg. 2004. The role of Toll-like receptor 4 versus interleukin-12 in immunity to respiratory syncytial virus. Eur. J. Immunol. 34:1146-1153.
14. Faisca, P., D. B. Tran Anh, A. Thomas, and D. Desmecht. 2006. Suppression of pattern-recognition receptor TLR4 sensing does not alter lung responses to pneumovirus infection. Microbes Infect. 8:621-627.
15. Fan, J., R. S. Frey, and A. B. Malik. 2003. TLR4 signaling induces TLR2 expression in endothelial cells via neutrophil NADPH oxidase. J. Clin. Investig. 112:1234-1243.
16. Fuentes, S., K. C. Tran, P. Luthra, M. N. Teng, and B. He. 2007. Function of the respiratory syncytial virus small hydrophobic protein. J. Virol. 81:8361-8366.
17. Gias, E., S. U. Nielsen, L. A. Morgan, and G. L. Toms. 2008. Purification of human respiratory syncytial virus by ultracentrifugation in iodixanol density gradient. J. Virol. Methods 147:328-332.
18. Gu, L., S. Tseng, R. M. Horner, C. Tam, M. Loda, and B. J. Rollins. 2000. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature 404:407-411.
19. Haeberle, H. A., R. Takizawa, A. Casola, A. R. Brasier, H. J. Dieterich, N. Van Rooijen, Z. Gatalica, and R. P. Garofalo. 2002. Respiratory syncytial virus-induced activation of nuclear factor-κB in the lung involves alveolar macrophages and toll-like receptor 4-dependent pathways. J. Infect. Dis. 186:1199-1206.
20. Hancock, G. E., K. M. Heers, K. S. Pryharski, J. D. Smith, and L. Tiberio. 2003. Adjuvants recognized by toll-like receptors inhibit the induction of polarized type 2 T cell responses by natural attachment (G) protein of respiratory syncytial virus. Vaccine 21:4348-4358.
21. Haynes, L. M., D. D. Moore, E. A. Kurt-Jones, R. W. Finberg, L. J. Anderson, and R. A. Tripp. 2001. Involvement of toll-like receptor 4 in innate immunity to respiratory syncytial virus. J. Virol. 75:10730-10737.
22. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5:987-995.
23. Janssen, R., J. Pennings, H. Hodemaekers, A. Buisman, M. van Oosten, L. de Rond, K. Ozturk, J. Dormans, T. Kimman, and B. Hoebee. 2007. Host transcription profiles upon primary respiratory syncytial virus infection. J. Virol. 81:5958-5967.
24. Jones, A., J. M. Qui, E. Bataki, H. Elphick, S. Ritson, G. S. Evans, and M. L. Everard. 2002. Neutrophil survival is prolonged in the airways of healthy infants and infants with RSV bronchiolitis. Eur. Respir. J. 20:651-657.
25. Kawai, T., and S. Akira. 2007. TLR signaling. Semin. Immunol. 19:24-32.
26. Kong, X., H. San Juan, M. Kumar, A. K. Behera, A. Mohapatra, G. R. Hellermann, S. Mane, R. F. Lockey, and S. S. Mohapatra. 2003. Respiratory syncytial virus infection activates STAT signaling in human epithelial cells. Biochem. Biophys. Res. Commun. 306:616-622.
27. Kurt-Jones, E. A., M. Chan, S. Zhou, J. Wang, G. Reed, R. Bronson, M. M. Arnold, D. M. Knipe, and R. W. Finberg. 2004. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc. Natl. Acad. Sci. USA 101:1315-1320.
28. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. J. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1:398-401.
29. Lee, A. H., J. H. Hong, and Y. S. Seo. 2000. Tumour necrosis factor-alpha and interferon-gamma synergistically activate the RANTES promoter through nuclear factor κB and interferon regulatory factor 1 (IRF-1) transcription factors. Biochem. J. 350:131-138.
30. Liu, P., M. Jamaluddin, K. Li, R. P. Garofalo, A. Casola, and A. R. Brasier. 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.
31. Matsuda, K., H. Tsutsumi, S. Sone, Y. Yoto, K. Oya, Y. Okamoto, P. L. Ogra, and S. Chiba. 1996. Characteristics of IL-6 and TNF-alpha production by respiratory syncytial virus-infected macrophages in the neonate. J. Med. Virol. 48:199-203.
32. Matsukawa, A., C. M. Hogaboam, N. W. Lukacs, P. M. Lincoln, R. M. Strieter, and S. L. Kunkel. 1999. Endogenous monocyte chemoattractant protein-1 (MCP-1) protects mice in a model of acute septic peritonitis: cross-talk between MCP-1 and leukotriene B4. J. Immunol. 163:6148-6154.
33. Mayer, A. K., M. Muehmer, J. Mages, K. Gueinzius, C. Hess, K. Heeg, R. Bals, R. Lang, and A. H. Dalpke. 2007. Differential recognition of TLR-dependent microbial ligands in human bronchial epithelial cells. J. Immunol. 178:3134-3142.
34. Megiovanni, A. M., F. Sanchez, M. Robledo-Sarmiento, C. Morel, J. C. Gluckman, and S. Boudaly. 2006. Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J. Leukoc. Biol. 79:977-988.
35. Ogra, P. L. 2004. Respiratory syncytial virus: the virus, the disease and the immune response. Paediatr Respir. Rev. 5(Suppl. A):S119-S126.
36. Openshaw, P. J., F. J. Culley, and W. Olszewska. 2001. Immunopathogenesis of vaccine-enhanced RSV disease. Vaccine 20(Suppl. 1):S27-S31.
37. Openshaw, P. J., G. S. Dean, and F. J. Culley. 2003. Links between respiratory syncytial virus bronchiolitis and childhood asthma: clinical and research approaches. Pediatr. Infect. Dis. J. 22:S58-S64.
38. Rassa, J. C., J. L. Meyers, Y. Zhang, R. Kudaravalli, and S. R. Ross. 2002. Murine retroviruses activate B cells via interaction with toll-like receptor 4. Proc. Natl. Acad. Sci. USA 99:2281-2286.
39. Rudd, B. D., M. A. Schaller, J. J. Smit, S. L. Kunkel, R. Neupane, L. Kelley, A. A. Berlin, and N. W. Lukacs. 2007. MyD88-mediated instructive signals in dendritic cells regulate pulmonary immune responses during respiratory virus infection. J. Immunol. 178:5820-5827.
40. Rudd, B. D., J. J. Smit, R. A. Flavell, L. Alexopoulou, M. A. Schaller, A. Gruber, A. A. Berlin, and N. W. Lukacs. 2006. Deletion of TLR3 alters the pulmonary immune environment and mucus production during respiratory syncytial virus infection. J. Immunol. 176:1937-1942.
41. Schlender, J., V. Hornung, S. Finke, M. Gunthner-Biller, S. Marozin, K. Brzozka, S. Moghim, S. Endres, G. Hartmann, and K. K. Conzelmann. 2005. Inhibition of toll-like receptor 7- and 9-mediated α/β interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. J. Virol. 79:5507-5515.
42. Stark, J. M., V. Godding, J. B. Sedgwick, and 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.
43. Stark, J. M., S. A. McDowell, V. Koenigsknecht, D. R. Prows, J. E. Leikauf, A. M. Le Vine, and G. D. Leikauf. 2002. Genetic susceptibility to respiratory syncytial virus infection in inbred mice. J. Med. Virol. 67:92-100.
44. Sukkar, M. B., S. Xie, N. M. Khorasani, O. M. Kon, R. Stanbridge, R. Issa, and K. F. Chung. 2006. Toll-like receptor 2, 3, and 4 expression and function in human airway smooth muscle. J. Allergy Clin. Immunol. 118:641-648.
45. Suzuki, K., T. Suda, T. Naito, K. Ide, K. Chida, and H. Nakamura. 2005. Impaired toll-like receptor 9 expression in alveolar macrophages with no sensitivity to CpG DNA. Am. J. Respir. Crit. Care Med. 171:707-713.
46. Syed, M. M., N. K. Phulwani, and T. Kielian. 2007. Tumor necrosis factor-alpha (TNF-alpha) regulates Toll-like receptor 2 (TLR2) expression in microglia. J. Neurochem. 103:1461-1471.
47. Taylor, G., E. J. Stott, M. Hughes, and A. P. Collins. 1984. Respiratory syncytial virus infection in mice. Infect. Immun. 43:649-655.
48. Tekkanat, K. K., H. Maassab, A. Miller, A. A. Berlin, S. L. Kunkel, and N. W. Lukacs. 2002. RANTES (CCL5) production during primary respiratory syncytial virus infection exacerbates airway disease. Eur. J. Immunol. 32:3276-3284.
49. Tripp, R. A., C. Oshansky, and R. Alvarez. 2005. Cytokines and respiratory syncytial virus infection. Proc. Am. Thorac. Soc. 2:147-149.
50. Tulic, M. K., R. J. Hurrelbrink, C. M. Prele, I. A. Laing, J. W. Upham, P. Le Souef, P. D. Sly, and P. G. Holt. 2007. TLR4 polymorphisms mediate impaired responses to respiratory syncytial virus and lipopolysaccharide. J. Immunol. 179:132-140.
51. van der Sluijs, K. F., L. van Elden, M. Nijhuis, R. Schuurman, S. Florquin, H. M. Jansen, R. Lutter, and T. van der Poll. 2003. Toll-like receptor 4 is not involved in host defense against respiratory tract infection with Sendai virus. Immunol. Lett. 89:201-206.
52. Wang, S. Z., and K. D. Forsyth. 2000. The interaction of neutrophils with respiratory epithelial cells in viral infection. Respirology 5:1-10.
53. Wang, S. Z., H. Xu, A. Wraith, J. J. Bowden, J. H. Alpers, and K. D. Forsyth. 1998. Neutrophils induce damage to respiratory epithelial cells infected with respiratory syncytial virus. Eur. Respir. J. 12:612-618.
54. Wu, Q., R. J. Martin, S. Lafasto, B. J. Efaw, J. G. Rino, R. J. Harbeck, and H. W. Chu. 2008. Toll-like receptor 2 down-regulation in mouse allergic lungs decreases mycoplasma clearance. Am. J. Respir. Crit. Care Med. 177:720-729
55. Yamamoto, M., S. Sato, K. Mori, K. Hoshino, O. Takeuchi, K. Takeda, and S. Akira. 2002. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J. Immunol. 169:6668-6672.
56. Zhou, S., E. A. Kurt-Jones, L. Mandell, A. Cerny, M. Chan, D. T. Golenbock, and R. W. Finberg. 2005. MyD88 is critical for the development of innate and adaptive immunity during acute lymphocytic choriomeningitis virus infection. Eur. J. Immunol. 35:822-830.