Selective ablation of lung epithelial IKK2 impairs pulmonary Th17 responses and delays the clearance of pneumocystis

Journal of Immunology

Volumn 191, Issue 9, 2013, Pages 4720-4730

  Perez Nazario, Nelissa ^a   Rangel Moreno, Javier ^b   O'Reilly, Michael A ^b   Pasparakis, Manolis ^c   Gigliotti, Francis ^a,b   Wright, Terry W ^a,b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CXCL2 CHEMOKINE; GAMMA INTERFERON; I KAPPA B KINASE; I KAPPA B KINASE 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 4; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; IKBKB PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE ACTIVATION; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CELL PHAGOCYTOSIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; FUNGAL CLEARANCE; HOST PATHOGEN INTERACTION; HOST RESISTANCE; IMMUNE RESPONSE; IN VIVO STUDY; INFECTION CONTROL; INTRACELLULAR SIGNALING; LUNG ALVEOLUS EPITHELIUM; LUNG COMPLIANCE; LUNG RESISTANCE; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; PATHOGEN CLEARANCE; PATHOGEN LOAD; PNEUMOCYSTIS; PNEUMOCYSTOSIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; TH17 CELL; TH2 CELL; ANIMAL; B LYMPHOCYTE; C57BL MOUSE; CYTOLOGY; DEFICIENCY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; LUNG ALVEOLUS MACROPHAGE; LYMPHOCYTE ACTIVATION; METABOLISM; PNEUMOCYSTIS PNEUMONIA; RESPIRATORY TRACT MUCOSA;

ANIMALS; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; I-KAPPA B KINASE; LUNG; LYMPHOCYTE ACTIVATION; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; PNEUMOCYSTIS; PNEUMONIA, PNEUMOCYSTIS; RESPIRATORY MUCOSA; TH17 CELLS;

EID: 84885974098     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301679     Document Type: Article

References (52)

1. Gigliotti, F., P. J. Haidaris, C. G. Haidaris, T. W. Wright, and K. R. Van der Meid. 1993. Further evidence of host species-specific variation in antigens of Pneumocystis carinii using the polymerase chain reaction. J. Infect. Dis. 168: 191-194.
2. Gigliotti, F., A. G. Harmsen, C. G. Haidaris, and P. J. Haidaris. 1993. Pneumocystis carinii is not universally transmissible between mammalian species. Infect. Immun. 61: 2886-2890.
3. Durand-Joly, I., el M. Aliouat, C. Recourt, K. Guyot, N. Francois, M. Wauquier, D. Camus, and E. Dei-Cas. 2002. Pneumocystis carinii f. sp. hominis is not infectious for SCID mice. J. Clin. Microbiol. 40: 1862-1865.
4. Ponce, C. A., M. Gallo, R. Bustamante, and S. L. Vargas. 2010. Pneumocystis colonization is highly prevalent in the autopsied lungs of the general population. Clin. Infect. Dis. 50: 347-353.
5. Vargas, S. L., C. A. Ponce, F. Gigliotti, A. V. Ulloa, S. Prieto, M. P. Muñoz, and W. T. Hughes. 2000. Transmission of Pneumocystis carinii DNA from a patient with P. carinii pneumonia to immunocompetent contact health care workers. J. Clin. Microbiol. 38: 1536-1538.
6. Vargas, S. L., W. T. Hughes, M. E. Santolaya, A. V. Ulloa, C. A. Ponce, C. E. Cabrera, F. Cumsille, and F. Gigliotti. 2001. Search for primary infection by Pneumocystis carinii in a cohort of normal, healthy infants. Clin. Infect. Dis. 32: 855-861.
7. Gigliotti, F., and T. W. Wright. 2012. Pneumocystis: where does it live? PLoS Pathog. 8: e1003025.
8. An, C. L., F. Gigliotti, and A. G. Harmsen. 2003. Exposure of immunocompetent adult mice to Pneumocystis carinii f. sp. muris by cohousing: growth of P. carinii f. sp. muris and host immune response. Infect. Immun. 71: 2065-2070.
9. Djawe, K., K. R. Daly, S. L. Vargas, M. E. Santolaya, C. A. Ponce, R. Bustamante, J. Koch, L. Levin, and P. D. Walzer. 2010. Seroepidemiological study of Pneumocystis jirovecii infection in healthy infants in Chile using recombinant fragments of the P. jirovecii major surface glycoprotein. Int. J. Infect. Dis. 14: e1060-e1066.
10. + percent as risk markers for Pneumocystis carinii pneumonia (PCP): implications for primary PCP prophylaxis. Scand. J. Infect. Dis. 24: 157-160.
11. + lymphocytes. Chest 103(2, Suppl.): 116S-118S.
12. Roths, J. B., J. D. Marshall, R. D. Allen, G. A. Carlson, and C. L. Sidman. 1990. Spontaneous Pneumocystis carinii pneumonia in immunodeficient mutant scid mice. Natural history and pathobiology. Am. J. Pathol. 136: 1173-1186.
13. Shellito, J., V. V. Suzara, W. Blumenfeld, J. M. Beck, H. J. Steger, and T. H. Ermak. 1990. A new model of Pneumocystis carinii infection in mice selectively depleted of helper T lymphocytes. J. Clin. Invest. 85: 1686-1693.
14. Wang, J., F. Gigliotti, S. P. Bhagwat, T. C. George, and T. W. Wright. 2010. Immune modulation with sulfasalazine attenuates immunopathogenesis but enhances macrophage-mediated fungal clearance during Pneumocystis pneumonia. PLoS Pathog. 6: e1001058.
15. Wang, J., F. Gigliotti, S. Maggirwar, C. Johnston, J. N. Finkelstein, and T. W. Wright. 2005. Pneumocystis carinii activates the NF-κB signaling pathway in alveolar epithelial cells. Infect. Immun. 73: 2766-2777.
16. Evans, S. E., P. Y. Hahn, F. McCann, T. J. Kottom, Z. V. Pavlovic', and A. H. Limper. 2005. Pneumocystis cell wall b-glucans stimulate alveolar epithelial cell chemokine generation through nuclear factor-κB-dependent mechanisms. Am. J. Respir. Cell Mol. Biol. 32: 490-497.
17. Bello-Irizarry, S. N., J. Wang, K. Olsen, F. Gigliotti, and T. W. Wright. 2012. The alveolar epithelial cell chemokine response to Pneumocystis requires adaptor molecule MyD88 and interleukin-1 receptor but not Toll-like receptor 2 or 4. Infect. Immun. 80: 3912-3920.
18. Wang, J., F. Gigliotti, S. P. Bhagwat, S. B. Maggirwar, and T. W. Wright. 2007. Pneumocystis stimulates MCP-1 production by alveolar epithelial cells through a JNK-dependent mechanism. Am. J. Physiol. Lung Cell. Mol. Physiol. 292: L1495-L1505.
19. Wright, T. W., C. J. Johnston, A. G. Harmsen, and J. N. Finkelstein. 1999. Chemokine gene expression during Pneumocystis carinii-driven pulmonary inflammation. Infect. Immun. 67: 3452-3460.
20. Li, Z. W., W. Chu, Y. Hu, M. Delhase, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. The IKKb subunit of IkB kinase (IKK) is essential for nuclear factor kB activation and prevention of apoptosis. J. Exp. Med. 189: 1839-1845.
21. Pasparakis, M., G. Courtois, M. Hafner, M. Schmidt-Supprian, A. Nenci, A. Toksoy, M. Krampert, M. Goebeler, R. Gillitzer, A. Israel, et al 2002. TNFmediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2. Nature 417: 861-866.
22. Okubo, T., and B. L. Hogan. 2004. Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J. Biol. 3: 11.
23. Okubo, T., P. S. Knoepfler, R. N. Eisenman, and B. L. Hogan. 2005. Nmyc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development 132: 1363-1374.
24. Chen, W., E. A. Havell, F. Gigliotti, and A. G. Harmsen. 1993. Interleukin-6 production in a murine model of Pneumocystis carinii pneumonia: relation to resistance and inflammatory response. Infect. Immun. 61: 97-102.
25. L increases sensitivity to oxygen without disrupting lung development. Am. J. Respir. Cell Mol. Biol. 43: 376-385.
26. + cells in resistance to Pneumocystis carinii pneumonia in mice. J. Exp. Med. 172: 937-945.
27. Lund, F. E., K. Schuer, M. Hollifield, T. D. Randall, and B. A. Garvy. 2003. Clearance of Pneumocystis carinii in mice is dependent on B cells but not on P carinii-specific antibody. J. Immunol. 171: 1423-1430.
28. Marcotte, H., D. Levesque, K. Delanay, A. Bourgeault, R. de la Durantaye, S. Brochu, and M. C. Lavoie. 1996. Pneumocystis carinii infection in transgenic B cell-deficient mice. J. Infect. Dis. 173: 1034-1037.
29. Harmsen, A. G., and M. Stankiewicz. 1991. T cells are not sufficient for resistance to Pneumocystis carinii pneumonia in mice. J. Protozool. 38: 44S-45S.
30. Limper, A. H., J. S. Hoyte, and J. E. Standing. 1997. The role of alveolar macrophages in Pneumocystis carinii degradation and clearance from the lung. J. Clin. Invest. 99: 2110-2117.
31. Lalor, S. J., L. S. Dungan, C. E. Sutton, S. A. Basdeo, J. M. Fletcher, and K. H. Mills. 2011. Caspase-1-processed cytokines IL-1b and IL-18 promote IL17 production by gd and CD4 T cells that mediate autoimmunity. J. Immunol. 186: 5738-5748.
32. van de Veerdonk, F. L., L. A. Joosten, P. J. Shaw, S. P. Smeekens, R. K. Malireddi, J. W. van der Meer, B. J. Kullberg, M. G. Netea, and T. D. Kanneganti. 2011. The inflammasome drives protective Th1 and Th17 cellular responses in disseminated candidiasis. Eur. J. Immunol. 41: 2260-2268.
33. Rudner, X. L., K. I. Happel, E. A. Young, and J. E. Shellito. 2007. Interleukin-23 (IL-23)-IL-17 cytokine axis in murine Pneumocystis carinii infection. Infect. Immun. 75: 3055-3061.
34. Beg, A. A., and D. Baltimore. 1996. An essential role for NF-κB in preventing TNF-a-induced cell death. Science 274: 782-784.
35. Zelante, T., A. De Luca, C. D'Angelo, S. Moretti, and L. Romani. 2009. IL-17/ Th17 in anti-fungal immunity: what's new? Eur. J. Immunol. 39: 645-648.
36. Carmona, E. M., T. J. Kottom, D. M. Hebrink, T. Moua, R. D. Singh, R. E. Pagano, and A. H. Limper. 2012. Glycosphingolipids mediate pneumocystis cell wall b-glucan activation of the IL-23/IL-17 axis in human dendritic cells. Am. J. Respir. Cell Mol. Biol. 47: 50-59.
37. Eddens, T., and J. K. Kolls. 2012. Host defenses against bacterial lower respiratory tract infection. Curr. Opin. Immunol. 24: 424-430.
38. Werner, J. L., M. A. Gessner, L. M. Lilly, M. P. Nelson, A. E. Metz, D. Horn, C. W. Dunaway, J. Deshane, D. D. Chaplin, C. T. Weaver, et al 2011. Neutrophils produce interleukin 17A (IL-17A) in a dectin-1- and IL-23-dependent manner during invasive fungal infection. Infect. Immun. 79: 3966-3977.
39. Gigliotti, F., C. G. Haidaris, T. W. Wright, and A. G. Harmsen. 2002. Passive intranasal monoclonal antibody prophylaxis against murine Pneumocystis carinii pneumonia. Infect. Immun. 70: 1069-1074.
40. Lund, F. E. 2008. Cytokine-producing B lymphocytes-key regulators of immunity. Curr. Opin. Immunol. 20: 332-338.
41. Fleury-Feith, J., J. T. Van Nhieu, C. Picard, E. Escudier, and J. F. Bernaudin. 1989. Bronchoalveolar lavage eosinophilia associated with Pneumocystis carinii pneumonitis in AIDS patients. Comparative study with non-AIDS patients. Chest 95: 1198-1201.
42. Swain, S. D., N. N. Meissner, and A. G. Harmsen. 2006. CD8 T cells modulate CD4 T-cell and eosinophil-mediated pulmonary pathology in Pneumocystis pneumonia in B-cell-deficient mice. Am. J. Pathol. 168: 466-475.
43. Swain, S. D., S. Han, A. Harmsen, K. Shampeny, and A. G. Harmsen. 2007. Pulmonary hypertension can be a sequela of prior Pneumocystis pneumonia. Am. J. Pathol. 171: 790-799.
44. + T lymphocyte subsets and host defense against Pneumocystis carinii. J. Infect. Dis. 181: 2011-2017.
45. Garvy, B. A., J. A. Wiley, F. Gigliotti, and A. G. Harmsen. 1997. Protection against Pneumocystis carinii pneumonia by antibodies generated from either T helper 1 or T helper 2 responses. Infect. Immun. 65: 5052-5056.
46. Garvy, B. A., R. A. Ezekowitz, and A. G. Harmsen. 1997. Role of g interferon in the host immune and inflammatory responses to Pneumocystis carinii infection. Infect. Immun. 65: 373-379.
47. Wang, J., T. W. Wright, and F. Gigliotti. 2011. Immune modulation as adjunctive therapy for Pneumocystis pneumonia. Interdiscip. Perspect. Infect. Dis. 2011: 918038.
48. Nelson, M. P., B. S. Christmann, J. L. Werner, A. E. Metz, J. L. Trevor, C. A. Lowell, and C. Steele. 2011. IL-33 and M2a alveolar macrophages promote lung defense against the atypical fungal pathogen Pneumocystis murina. J. Immunol. 186: 2372-2381.
49. Qureshi, M. H., A. G. Harmsen, and B. A. Garvy. 2003. IL-10 modulates host responses and lung damage induced by Pneumocystis carinii infection. J. Immunol. 170: 1002-1009.
50. Martinez, F. O., A. Sica, A. Mantovani, and M. Locati. 2008. Macrophage activation and polarization. Front. Biosci. 13: 453-461.
51. Kobayashi, M., M. G. Jeschke, K. Shigematsu, A. Asai, S. Yoshida, D. N. Herndon, and F. Suzuki. 2010. M2b monocytes predominated in peripheral blood of severely burned patients. J. Immunol. 185: 7174-7179.
52. Rastrick, J. M., C. S. Stevenson, S. Eltom, M. Grace, M. Davies, I. Kilty, S. M. Evans, M. Pasparakis, M. C. Catley, T. Lawrence, et al. 2013. Cigarette smoke induced airway inflammation is independent of NF-κB signalling. PLoS ONE 8: e54128.