Dysregulation in lung immunity - The protective and pathologic Th17 response in infection

European Journal of Immunology

Volumn 43, Issue 12, 2013, Pages 3116-3124

  Way, Emily E ^a   Chen, Kong ^a   Kolls, Jay K ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

Author keywords

Animal models; CD4 T cells; Cellular immunology; Cytokines; Lung inflammation

Indexed keywords

CYTOKINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; BACTERIAL PNEUMONIA; CELL FUNCTION; CHRONIC GRANULOMATOUS DISEASE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CYSTIC FIBROSIS; EFFECTOR CELL; EPITHELIUM CELL; HUMAN; IMMUNE RESPONSE; INFLAMMATION; ION TRANSPORT; LUNG FUNCTION; LUNG INFECTION; LUNG MYCOSIS; NEUTROPHIL; NONHUMAN; PATHOLOGY; PRIORITY JOURNAL; TH17 CELL; VIRUS PNEUMONIA; ANIMAL; ANIMAL MODELS; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; IMMUNOLOGY; INFECTION; LUNG; METABOLISM; PNEUMONIA; REVIEW;

ANIMAL MODELS; CD4 T CELLS; CELLULAR IMMUNOLOGY; CYTOKINES; LUNG INFLAMMATION;

ANIMALS; CYSTIC FIBROSIS; GRANULOMATOUS DISEASE, CHRONIC; HUMANS; INFECTION; LUNG; TH17 CELLS;

EID: 84896998364     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343713     Document Type: Article

References (67)

1. McGeachy, M. J. and Cua, D. J., Th17 cell differentiaxstion: the long and winding road. Immunity 2008. 28: 445-453.
2. McGeachy, M. J., Chen, Y., Tato, C. M., Laurence, A., Joyce-Shaikh, B., Blumenschein, W. M. and McClanahan, T. K., The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat. Immunol. 2009. 10: 314-324.
3. Ouyang, W., Kolls, J. K. and Zheng, Y., The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008. 28: 454-467.
4. Bordon, J., Aliberti, S., Fernandez-Botran, R., Uriarte, S. M., Rane, M. J., Duvvuri, P. and Peyrani, P., Understanding the roles of cytokines and neutrophil activity and neutrophil apoptosis in the protective versus deleterious inflammatory response in pneumonia. Int. J. Infect. Dis. 2013. 17: e76-e83.
5. Ye, P., Rodriguez, F. H., Kanaly, S., Stocking, K. L., Schurr, J., Schwarzenberger, P. and Oliver, P., Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 2001. 194: 519-527.
6. Sutton, C. E., Mielke, L. A. and Mills, K. H., IL-17-producing gammadelta T cells and innate lymphoid cells. Eur. J. Immunol. 2012. 42: 2221-2231.
7. Curtis, M. M. and Way, S. S., Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 2009. 126: 177-185.
8. Khader, S. A., Gaffen, S. L. and Kolls, J. K., Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol. 2009. 2: 403-411.
9. Paulson, M. L., Freeman, A. F. and Holland, S. M., Hyper IgE syndrome: an update on clinical aspects and the role of signal transducer and activator of transcription 3. Curr. Opin. Allergy Clin. Immunol. 2008. 8: 527-533.
10. Milner, J. D., Sandler, N. G. and Douek, D. C., Th17 cells, Job's syndrome and HIV: opportunities for bacterial and fungal infections. Curr. Opin. HIV AIDS 2010. 5: 179-183.
11. Conti, H. R., Shen, F., Nayyar, N., Stocum, E., Sun, J. N., Lindemann, M. J. and Ho, A. W., Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J. Exp. Med. 2009. 206: 299-311.
12. Puel, A., Cypowyj, S., Marodi, L., Abel, L., Picard, C. and Casanova, J. L., Inborn errors of human IL-17 immunity underlie chronic mucocutaneous candidiasis. Curr. Opin. Allergy Clin. Immunol. 2012. 12: 616-622.
13. Cypowyj, S., Picard, C., Marodi, L., Casanova, J. L. and Puel, A., Immunity to infection in IL-17-deficient mice and humans. Eur. J. Immunol. 2012. 42: 2246-2254.
14. Kudva, A., Scheller, E. V., Robinson, K. M., Crowe, C. R., Choi, S. M., Slight, S. R. and Khader, S. A., Influenza A inhibits Th17-mediated host defense against bacterial pneumonia in mice. J. Immunol. 2011. 186: 1666-1674.
15. Cheng, P., Liu, T., Zhou, W. Y., Zhuang, Y., Peng, L. S., Zhang, J. Y. and Yin, Z. N., Role of gamma-delta T cells in host response against Staphylococcus aureus-induced pneumonia. BMC Immunol. 2012. 13: 38.
16. Vantourout, P. and Hayday, A., Six-of-the-best: unique contributions of gammadelta T cells to immunology. Nat. Rev. Immunol. 2013. 13: 88-100.
17. Happel, K. I., Dubin, P. J., Zheng, M., Ghilardi, N., Lockhart, C., Quinton, L. J. and Odden, A. R., Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 2005. 202: 761-769.
18. Cooper, A. M., Kipnis, A., Turner, J., Magram, J., Ferrante, J. and Orme, I. M., Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 p40 subunit is present. J. Immunol. 2002. 168: 1322-1327.
19. Holscher, C., Atkinson, R. A., Arendse, B., Brown, N., Myburgh, E., Alber, G. and Brombacher, F., A protective and agonistic function of IL-12p40 in mycobacterial infection. J. Immunol. 2001. 167: 6957-6966.
20. Khader, S. A., Pearl, J. E., Sakamoto, K., Gilmartin, L., Bell, G. K., Jelley-Gibbs, D. M. and Ghilardi, N., IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J. Immunol. 2005. 175: 788-795.
21. Umemura, M., Yahagi, A., Hamada, S., Begum, M. D., Watanabe, H., Kawakami, K. and Suda, T., IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 2007. 178: 3786-3796.
22. Khader, S. A., Bell, G. K., Pearl, J. E., Fountain, J. J., Rangel-Moreno, J., Cilley, G. E. and Shen, F., IL-23 and IL-17 in the establishment of protective pulmonary CD4 +T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 2007. 8: 369-377.
23. Okamoto Yoshida, Y., Umemura, M., Yahagi, A., O'Brien, R. L., Ikuta, K., Kishihara, K. and Hara, H., Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung. J. Immunol. 2010. 184: 4414-4422.
24. Lockhart, E., Green, A. M. and Flynn, J. L., IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J. Immunol. 2006. 177: 4662-4669.
25. Mahon, B. P., Brady, M. T. and Mills, K. H., Protection against Bordetella pertussis in mice in the absence of detectable circulating antibody: implications for long-term immunity in children. J. Infect. Dis. 2000. 181: 2087-2091.
26. Higgins, S. C., Jarnicki, A. G., Lavelle, E. C. and Mills, K. H., TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J. Immunol. 2006. 177: 7980-7989.
27. Dunne, A., Ross, P. J., Pospisilova, E., Masin, J., Meaney, A., Sutton, C. E. and Iwakura, Y., Inflammasome activation by adenylate cyclase toxin directs Th17 responses and protection against Bordetella pertussis. J. Immunol. 2010. 185: 1711-1719.
28. Warfel, J. M. and Merkel, T. J., Bordetella pertussis infection induces a mucosal IL-17 response and long-lived Th17 and Th1 immune memory cells in nonhuman primates. Mucosal Immunol. 2012. 6: 787-796.
29. Wu, Q., Martin, R. J., Rino, J. G., Breed, R., Torres, R. M. and Chu, H. W., IL-23-dependent IL-17 production is essential in neutrophil recruitment and activity in mouse lung defense against respiratory Mycoplasma pneumoniae infection. Microbes Infect. 2007. 9: 78-86.
30. Sieve, A. N., Meeks, K. D., Bodhankar, S., Lee, S., Kolls, J. K., Simecka, J. W. and Berg, R. E., A novel IL-17-dependent mechanism of cross protection: respiratory infection with mycoplasma protects against a secondary listeria infection. Eur. J. Immunol. 2009. 39: 426-438.
31. Lu, Y. J., Gross, J., Bogaert, D., Finn, A., Bagrade, L., Zhang, Q. and Kolls, J. K., Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog. 2008. 4: e1000159.
32. Moffitt, K. L., Gierahn, T. M., Lu, Y. J., Gouveia, P., Alderson, M., Flechtner, J. B. and Higgins, D. E., T(H)17-based vaccine design for prevention of Streptococcus pneumoniae colonization. Cell Host Microbe 2011. 9: 158-165.
33. Garvy, B. A., Wiley, J. A., Gigliotti, F. and Harmsen, A. G., Protection against Pneumocystis carinii pneumonia by antibodies generated from either T helper 1 or T helper 2 responses. Infect. Immun. 1997. 65: 5052-5056.
34. Rudner, X. L., Happel, K. I., Young, E. A. and Shellito, J. E., Interleukin-23 (IL-23)-IL-17 cytokine axis in murine Pneumocystis carinii infection. Infect. Immun. 2007. 75: 3055-3061.
35. Deepe, G. S., Jr. and Gibbons, R. S., Interleukins 17 and 23 influence the host response to Histoplasma capsulatum. J. Infect. Dis. 2009. 200: 142-151.
36. Wozniak, K. L., Hardison, S. E., Kolls, J. K. and Wormley, F. L., Role of IL-17A on resolution of pulmonary C. neoformans infection. PLoS One 2011. 6: e17204.
37. Zhang, Y., Wang, F., Tompkins, K. C., McNamara, A., Jain, A. V., Moore, B. B. and Toews, G. B., Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dissemination of highly virulent Cryptococcus neoformans H99. Am. J. Pathol. 2009. 175: 2489-2500.
38. Downey, D. G., Bell, S. C. and Elborn, J. S., Neutrophils in cystic fibrosis. Thorax 2009. 64: 81-88.
39. Tan, H. L., Regamey, N., Brown, S., Bush, A., Lloyd, C. M. and Davies, J. C., The Th17 pathway in cystic fibrosis lung disease. Am. J. Respir. Crit. Care Med. 2011. 184: 252-258.
40. McAllister, F., Henry, A., Kreindler, J. L., Dubin, P. J., Ulrich, L., Steele, C. and Finder, J. D., Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J. Immunol. 2005. 175: 404-412.
41. Chan, Y. R., Chen, K., Duncan, S. R., Lathrop, K. L., Latoche, J. D., Logar, A. J. and Pociask, D. A., Patients with cystic fibrosis have inducible IL-17(+)IL-22(+) memory cells in lung draining lymph nodes. J. Allergy Clin. Immunol. 2013. 131: 1117-1129.e1115.
42. Dubin, P. J. and Kolls, J. K., IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 2007. 292: L519-L528.
43. Liu, J., Feng, Y., Yang, K., Li, Q., Ye, L., Han, L. and Wan, H., Early production of IL-17 protects against acute pulmonary Pseudomonas aeruginosa infection in mice. FEMS Immunol. Med. Microbiol. 2011. 61: 179-188.
44. Rieber, N., Hector, A., Kuijpers, T., Roos, D. and Hartl, D., Current concepts of hyperinflammation in chronic granulomatous disease. Clin. Dev. Immunol. 2012. 2012: 252460.
45. Horvath, R., Rozkova, D., Lastovicka, J., Polouckova, A., Sedlacek, P., Sediva, A. and Spisek, R., Expansion of T helper type 17 lymphocytes in patients with chronic granulomatous disease. Clin. Exp. Immunol. 2011. 166: 26-33.
46. Werner, J. L., Metz, A. E., Horn, D., Schoeb, T. R., Hewitt, M. M., Schwiebert, L. M. and Faro-Trindade, I., Requisite role for the dectin-1 beta-glucan receptor in pulmonary defense against Aspergillus fumigatus. J. Immunol. 2009. 182: 4938-4946.
47. Romani, L., Fallarino, F., de Luca, A., Montagnoli, C., D'Angelo, C., Zelante, T. and Vacca, C., Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 2008. 451: 211-215.
48. di Stefano, A., Caramori, G., Gnemmi, I., Contoli, M., Vicari, C., Capelli, A. and Magno, F., T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin. Exp. Immunol. 2009. 157: 316-324.
49. Vargas-Rojas, M. I., Ramirez-Venegas, A., Limon-Camacho, L., Ochoa, L., Hernandez-Zenteno, R. and Sansores, R. H., Increase of Th17 cells in peripheral blood of patients with chronic obstructive pulmonary disease. Respir. Med. 2011. 105: 1648-1654.
50. Chen, K., Pociask, D. A., McAleer, J. P., Chan, Y. R., Alcorn, J. F., Kreindler, J. L. and Keyser, M. R., IL-17RA is required for CCL2 expression, macrophage recruitment, and emphysema in response to cigarette smoke. PLoS One 2011. 6: e20333.
51. Zelante, T., de Luca, A., Bonifazi, P., Montagnoli, C., Bozza, S., Moretti, S. and Belladonna, M. L., IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur. J. Immunol. 2007. 37: 2695-2706.
52. Gessner, M. A., Werner, J. L., Lilly, L. M., Nelson, M. P., Metz, A. E., Dunaway, C. W. and Chan, Y. R., Dectin-1-dependent interleukin-22 contributes to early innate lung defense against Aspergillus fumigatus. Infect. Immun. 2012. 80: 410-417.
53. Lilly, L. M., Gessner, M. A., Dunaway, C. W., Metz, A. E., Schwiebert, L., Weaver, C. T. and Brown, G. D., The beta-glucan receptor dectin-1 promotes lung immunopathology during fungal allergy via IL-22. J. Immunol. 2012. 189: 3653-3660.
54. Murdock, B. J., Falkowski, N. R., Shreiner, A. B., Sadighi Akha, A. A., McDonald, R. A., White, E. S. and Toews, G. B., Interleukin-17 drives pulmonary eosinophilia following repeated exposure to Aspergillus fumigatus conidia. Infect. Immun. 2012. 80: 1424-1436.
55. Hashimoto, K., Durbin, J. E., Zhou, W., Collins, R. D., Ho, S. B., Kolls, J. K. and Dubin, P. J., Respiratory syncytial virus infection in the absence of STAT 1 results in airway dysfunction, airway mucus, and augmented IL-17 levels. J. Allergy Clin. Immunol. 2005. 116: 550-557.
56. Lukacs, N. W., Smit, J. J., Mukherjee, S., Morris, S. B., Nunez, G. and Lindell, D. M., Respiratory virus-induced TLR7 activation controls IL-17-associated increased mucus via IL-23 regulation. J. Immunol. 2010. 185: 2231-2239.
57. Bera, M. M., Lu, B., Martin, T. R., Cui, S., Rhein, L. M., Gerard, C. and Gerard, N. P., Th17 cytokines are critical for respiratory syncytial virus-associated airway hyperreponsiveness through regulation by complement C3a and tachykinins. J. Immunol. 2011. 187: 4245-4255.
58. Mukherjee, S., Lindell, D. M., Berlin, A. A., Morris, S. B., Shanley, T. P., Hershenson, M. B. and Lukacs, N. W., IL-17-induced pulmonary pathogenesis during respiratory viral infection and exacerbation of allergic disease. Am. J. Pathol. 2011. 179: 248-258.
59. Li, C., Yang, P., Sun, Y., Li, T., Wang, C., Wang, Z. and Zou, Z., IL-17 response mediates acute lung injury induced by the 2009 pandemic influenza A (H1N1) virus. Cell Res. 2012. 22: 528-538.
60. Bermejo-Martin, J. F., Ortiz de Lejarazu, R., Pumarola, T., Rello, J., Almansa, R., Ramirez, P. and Martin-Loeches, I., Th1 and Th17 hypercytokinemia as early host response signature in severe pandemic influenza. Crit. Care 2009. 13: R201.
61. Crowe, C. R., Chen, K., Pociask, D. A., Alcorn, J. F., Krivich, C., Enelow, R. I. and Ross, T. M., Critical role of IL-17RA in immunopathology of influenza infection. J. Immunol. 2009. 183: 5301-5310.
62. Pociask, D. A., Scheller, E. V., Mandalapu, S., McHugh, K. J., Enelow, R. I., Fattman, C. L. and Kolls, J. K., IL-22 is essential for lung epithelial repair following influenza infection. Am. J. Pathol. 2013. 182: 1286-1296.
63. Ivanov, S., Renneson, J., Fontaine, J., Barthelemy, A., Paget, C., Macho Fernandez, E. and Blanc, F., Interleukin-22 reduces lung inflammation during influenza A virus infection and protects against secondary bacterial infection. J. Virol. 2013. 87: 6911-6924.
64. Ghoreschi, K., Laurence, A., Yang, X. P., Tato, C. M., McGeachy, M. J., Konkel, J. E. and Ramos, H. L., Generation of pathogenic T(H)17 cells in the absence of TGF-beta signalling. Nature 2010. 467: 967-971.
65. Lee, Y., Awasthi, A., Yosef, N., Quintana, F. J., Xiao, S., Peters, A. and Wu, C., Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 2012. 13: 991-999.
66. Peters, A., Lee, Y. and Kuchroo, V. K., The many faces of Th17 cells. Curr. Opin. Immunol. 2011. 23: 702-706.
67. Wu, C., Yosef, N., Thalhamer, T., Zhu, C., Xiao, S., Kishi, Y. and Regev, A., Induction of pathogenic TH17 cells by inducible salt-sensing kinase SGK1. Nature 2013. 496: 513-517.