The role Of TLR2 and bacterial lipoprotein in enhancing airway inflammation and immunity

Frontiers in Immunology

Volumn 2, Issue APR, 2011, Pages

  Lugade, Amit A ^a   Bogner, Paul N ^a   Murphy, Timothy F ^b   Thanavala, Yasmin ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

B cells; Inflammation,T cells; NTHI; P6

Indexed keywords

EID: 84860857395     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2011.000     Document Type: Article

References (39)

1. Abe, Y., Murphy, T. F., Sethi, S., Faden, H. S., Dmochowski, J., Harabuchi, Y., and Thanavala, Y. M. (2002). Lymphocyte proliferative response to P6 of Haemophilus influenzae is associated with relative protection from exacerbations of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 165, 967-971.
2. Alexopoulou, L., and Kontoyiannis, D. (2005). Contribution of microbialassociated molecules in innate mucosal responses. Cell.Mol.Life Sci. 62, 1349-1358.
3. Badr, W. H., Loghmanee, D., Karalus, R. J., Murphy, T. F., and Thanavala, Y. (1999). Immunization of mice with P6 of nontypeable Haemophilus influenzae: kinetics of the antibody response and IgG subclasses. Vaccine 18, 29-37.
4. Bagaitkar, J., Demuth, D. R., Daep, C. A., Renaud, D. E., Pierce, D. L., and Scott, D. A. (2010). Tobacco upregulates P. gingivalis fimbrial proteins which induce TLR2 hyposensitivity. PLoS ONE 5, e9323. doi: 10.1371/journal.pone.0009323
5. Berenson,C. S.,Murphy,T. F.,Wrona,C. T., and Sethi, S. (2005). Outer membrane protein P6 of nontypeable Haemophilus influenzae is a potent and selective inducer of human macrophage proinflammatory cytokines. Infect. Immun. 73, 2728-2735.
6. Bertot, G. M., Becker, P. D., Guzmán, C. A., and Grinstein, S. (2004). Intranasal vaccination with recombinant P6 protein and adamantylamide dipeptide as mucosal adjuvant confers efficient protection against otitis media and lung infection by nontypeable Haemophilus influenzae. J. Infect. Dis. 189, 1304- 1312.
7. Caramori, G., Casolari, P., Di Gregorio, C., Saetta, M., Baraldo, S., Boschetto, P., Ito, K., Fabbri, L. M., Barnes, P. J., Adcock, I. M., Cavallesco, G., Chung, K. F., and Papi, A. (2009). MUC5AC expression is increased in bronchial submucosal glands of stable COPD patients. Histopathology 55, 321-331.
8. Chen, R., Lim, J. H., Jono, H., Gu, X. X., Kim, Y. S., Basbaum, C. B., Murphy, T. F., and Li, J. D. (2004). Nontypeable Haemophilus influenzae lipoprotein P6 induces MUC5AC mucin transcription via TLR2TAK1-dependent p38 MAPK-AP1 and IKKbeta-IkappaBalphaNF-kappaB signaling pathways. Biochem. Biophys. Res. Commun. 324, 1087-1094.
9. Cyr, S. L., Angers, I., Guillot, L., Stoica Popescu, I., Lussier, M., Qureshi, S., Burt, D. S., and Ward, B. J. (2009). TLR4 and MyD88 control protection and pulmonary granulocytic recruitment in a murine intranasal RSV immunization and challenge model. Vaccine 27, 421-430.
10. Dhillon, N. K., Murphy, W. J., Filla, M. B., Crespo, A. J., Latham, H. A., and O'Brien-Ladner, A. (2009). Down modulation of IFN-gamma signaling in alveolar macrophages isolated from smokers. Toxicol. Appl. Pharmacol. 237, 22-28.
11. Domagala-Kulawik, J. (2008). Effects of cigarette smoke on the lung and systemic immunity. J. Physiol. Pharmacol. 59(Suppl. 6), 19-34.
12. Droemann, D., Goldmann, T., Tiedje, T., Zabel, P., Dalhoff, K., and Schaaf, B. (2005). Toll-like receptor 2 expression is decreased on alveolar macrophages in cigarette smokers and COPD patients. Respir. Res. 6, 68.
13. Gaschler, G. J., Skrtic, M., Zavitz, C. C., Lindahl, M., Onnervik, P. O., Murphy, T. F., Sethi, S., and Stämpfli, M. R. (2009). Bacteria challenge in smoke-exposed mice exacerbates inflammation and skews the inflammatory profile. Am. J. Respir. Crit. Care Med. 179, 666-675.
14. Harrison, O. J., Foley, J., Bolognese, B. J., Long E, III, Podolin, P. L., and Walsh, P. T. (2008). Airway infiltration of CD4+ CCR6+ Th17 type cells associated with chronic cigarette smoke induced airspace enlargement. Immunol. Lett. 121, 13-21.
15. Heimesaat, M. M., Fischer, A., Jahn, H. K., Niebergall, J., Freudenberg, M., Blaut, M., Liesenfeld, O., Schumann, R. R., Göbel, U. B., and Bereswill, S. (2007). Exacerbation of murine ileitis by Tolllike receptor 4 mediated sensing of lipopolysaccharide from commensal Escherichia coli. Gut 56, 941-948.
16. Hotomi, M., Saito, T., and Yamanaka, N. (1998). Specific mucosal immunity and enhanced nasopharyngeal clearance of nontypeable Haemophilus influenzae after intranasal immunization with outer membrane protein P6 and cholera toxin.Vaccine 16, 1950-1956.
17. Ishida, Y., Abe, Y., Yanai, M., Kobayashi, H., and Harabuchi, Y. (2006). Identification of human T-cell epitopes and highly immunogenic analog peptides on the non-typeable Haemophilus influenzae P6 outer membrane protein. Clin. Immunol. 121, 90-99.
18. Knowles, M. R., and Boucher, R. C. (2002). Mucus clearance as a primary innate defense mechanism for mammalian airways. J. Clin. Invest. 109, 571-577.
19. Kraft, M., Adler, K. B., Ingram, J. L., Crews, A. L., Atkinson, T. P., Cairns, C. B., Krause, D. C., and Chu, H. W. (2008). Mycoplasma pneumoniae induces airway epithelial cell expression of MUC5AC in asthma. Eur. Respir. J. 31, 43-46.
20. Layland, L. E., Rad, R., Wagner, H., and da Costa, C. U. (2007). Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur. J. Immunol. 37, 2174-2184.
21. Li, J. D. (2003). Exploitation of host epithelial signaling networks by respiratory bacterial pathogens. J. Pharmacol. Sci. 91, 1-7.
22. Lugade, A. A., Vethanayagam, R. R., Nasirikenari, M., Bogner, P., Segal, B. H., and Thanavala, Y. (2011). Nrf2 regulates chronic lung inflammation and B cell responses to non-typeable Haemophilus influenzae. Am. J. Respir. Cell Mol. Biol. doi: 10.1165/rcmb.2010-0321OC [Epub ahead of print].
23. Manicassamy, S., and Pulendran, B. (2009). Modulation of adaptive immunity with Toll-like receptors. Semin. Immunol. 21, 185-193.
24. Martí-Lliteras, P., Regueiro, V., Morey, P., Hood, D. W., Saus, C., Sauleda, J., Agustí, A. G., Bengoechea, J. A., and Garmendia, J. (2009). Nontypeable Haemophilus influenzae clearance by alveolar macrophages is impaired by exposure to cigarette smoke. Infect. Immun. 77, 4232-4242.
25. McMahon, M., Murphy, T. F., Kyd, J., and Thanavala, Y. (2005). Role of an immunodominant T cell epitope of the P6 protein of nontypeable Haemophilus influenzae in murine protective immunity. Vaccine 23, 3590-3596.
26. Mehta, H., Nazzal, K., and Sadikot, R. T. (2008). Cigarette smoking and innate immunity. Inflamm. Res. 57, 497-503.
27. Moghaddam, S. J., Clement, C. G., De la Garza, M. M., Zou, X., Travis, E. L., Young, H. W., Evans, C. M., Tuvim, M. J., and Dickey, B. F. (2008). Haemophilus influenzae lysate induces aspects of the chronic obstructive pulmonary disease phenotype. Am. J. Respir. Cell Mol. Biol. 38, 629-638.
28. Munson, R. S., Jr., and Granoff, D. M. (1985). Purification and partial characterization of outer membrane proteins P5 and P6 from Haemophilus influenzae type b. Infect. Immun. 49, 544-549.
29. Murawski, M. R., Bowen, G. N., Cerny, A. M., Anderson, L. J., Haynes, L. M., Tripp, R. A., Kurt-Jones, E. A., and Finberg, R. W. (2009). Respiratory syncytial virus activates innate immunity through Toll-like receptor 2. J. Virol. 83, 1492-1500.
30. Murphy, T. F., Kirkham, C., and Lesse, A. J. (2006). Construction of a mutant and characterization of the role of the vaccine antigen P6 in outer membrane integrity of nontypeable Haemophilus influenzae. Infect. Immun. 74, 5169-5176.
31. Noda, K., Kodama, S., Umemoto, S., Abe, N., Hirano, T., and Suzuki, M. (2010). Nasal vaccination with P6 outer membrane protein and alpha-galactosylceramide induces nontypeable Haemophilus influenzae-specific protective immunity associated with NKT cell activation and dendritic cell expansion in nasopharynx. Vaccine 28, 5068-5074.
32. Nomura, Y., Abe, Y., Ishida, Y., Kobayashi, H., and Harabuchi, Y. (2008). Promiscuous peptides on the nontypeable Haemophilus influenzae P6 outer membrane protein. J. Clin. Immunol. 28, 361-369.
33. Phaybouth, V., Wang, S. Z., Hutt, J. A., McDonald, J. D., Harrod, K. S., and Barrett, E. G. (2006). Cigarette smoke suppresses Th1 cytokine production and increases RSV expression in a neonatal model. Am. J. Physiol. Lung Cell Mol. Physiol. 290, L222-31.
34. Sayi, A., Kohler, E., Toller, I. M., Flavell, R. A., Müller, W., Roers, A., and Müller, A. (2011). TLR2-activated B cells suppress Helicobacter-induced preneoplastic gastric immunopathology by inducing T regulatory-1 cells. J. Immunol. 186, 878-890.
35. Sethi, S., and Murphy, T. F. (2001). Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review. Clin. Microbiol. Rev. 14, 336-363.
36. Shuto, T., Xu, H., Wang, B., Han, J., Kai, H., Gu, X. X., Murphy, T. F., Lim, D. J., and Li, J. D. (2001). Activation of NF-kappa B by nontypeable Haemophilus influenzae is mediated by toll-like receptor 2-TAK1-dependent NIK-IKK alpha/beta-I kappa B alpha and MKK3/6-p38 MAP kinase signaling pathways in epithelial cells. Proc. Natl. Acad. Sci. U.S.A. 98, 8774-8779.
37. Stämpfli, M. R., and Anderson, G. P. (2009). How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat. Rev. Immunol. 9, 377-384.
38. Wu, T., Chen, J., Murphy, T. F., Green, B. A., and Gu, X. X. (2005). Investigation of non-typeable Haemophilus influenzae outer membrane protein P6 as a new carrier for lipooligosaccharide conjugate vaccines. Vaccine 23, 5177-5185.
39. Yarovinsky, F., Hieny, S., and Sher, A. (2008). Recognition of Toxoplasma gondii by TLR11 prevents parasiteinduced immunopathology. J. Immunol. 181, 8478-8484.