Original Article

Requirement of Interleukin 17 Receptor Signaling for Lung CXC Chemokine and Granulocyte Colony-stimulating Factor Expression, Neutrophil Recruitment, and Host Defense

Correspondence to: Jay K. Kolls, LSUHSC Gene Therapy Program, CSRB 601, 533 Bolivar St., New Orleans, LA 70112. Tel:504-568-6152 Fax:504-568-8500 E-mail:jkolls{at}lshsc.edu.

Bacterial pneumonia is an increasing complication of HIV infection and inversely correlates with the CD4⁺ lymphocyte count. Interleukin (IL)-17 is a cytokine produced principally by CD4⁺ T cells, which induces granulopoiesis via granulocyte colony-stimulating factor (G-CSF) production and induces CXC chemokines. We hypothesized that IL-17 receptor (IL-17R) signaling is critical for G-CSF and CXC chemokine production and lung host defenses. To test this, we used a model of Klebsiella pneumoniae lung infection in mice genetically deficient in IL-17R or in mice overexpressing a soluble IL-17R. IL-17R–deficient mice were exquisitely sensitive to intranasal K. pneumoniae with 100% mortality after 48 h compared with only 40% mortality in controls. IL-17R knockout (KO) mice displayed a significant delay in neutrophil recruitment into the alveolar space, and had greater dissemination of K. pneumoniae compared with control mice. This defect was associated with a significant reduction in steady-state levels of G-CSF and macrophage inflammatory protein (MIP)-2 mRNA and protein in the lung in response to the K. pneumoniae challenge in IL-17R KO mice. Thus, IL-17R signaling is critical for optimal production of G-CSF and MIP-2 and local control of pulmonary K. pneumoniae infection. These data support impaired IL-17R signaling as a potential mechanism by which deficiency of CD4 lymphocytes predisposes to bacterial pneumonia.

Key Words: IL-17, T lymphocyte, granulocyte-colony stimulating factor, Klebsiella pneumoniae, chemokine

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• Warnatz, K., Bossaller, L., Salzer, U., Skrabl-Baumgartner, A., Schwinger, W., van der Burg, M., van Dongen, J. J. M., Orlowska-Volk, M., Knoth, R., Durandy, A., Draeger, R., Schlesier, M., Peter, H. H., Grimbacher, B. (2006). Human ICOS deficiency abrogates the germinal center reaction and provides a monogenic model for common variable immunodeficiency. Blood 107: 3045-3052 [Abstract] [Full Text]  
• Malley, R., Srivastava, A., Lipsitch, M., Thompson, C. M., Watkins, C., Tzianabos, A., Anderson, P. W. (2006). Antibody-Independent, Interleukin-17A-Mediated, Cross-Serotype Immunity to Pneumococci in Mice Immunized Intranasally with the Cell Wall Polysaccharide. Infect. Immun. 74: 2187-2195 [Abstract] [Full Text]  
• Ingersoll, M. A., Zychlinsky, A. (2006). ShiA Abrogates the Innate T-Cell Response to Shigella flexneri Infection. Infect. Immun. 74: 2317-2327 [Abstract] [Full Text]  
• Kramer, J. M., Yi, L., Shen, F., Maitra, A., Jiao, X., Jin, T., Gaffen, S. L. (2006). Cutting Edge: Evidence for Ligand-Independent Multimerization of the IL-17 Receptor. J. Immunol. 176: 711-715 [Abstract] [Full Text]  
• Kleinschek, M. A., Muller, U., Brodie, S. J., Stenzel, W., Kohler, G., Blumenschein, W. M., Straubinger, R. K., McClanahan, T., Kastelein, R. A., Alber, G. (2006). IL-23 Enhances the Inflammatory Cell Response in Cryptococcus neoformans Infection and Induces a Cytokine Pattern Distinct from IL-12. J. Immunol. 176: 1098-1106 [Abstract] [Full Text]  
• Happel, K. I., Nelson, S. (2005). Alcohol, Immunosuppression, and the Lung. Proc Am Thorac Soc 2: 428-432 [Abstract] [Full Text]  
• Jones, M. R., Simms, B. T., Lupa, M. M., Kogan, M. S., Mizgerd, J. P. (2005). Lung NF-{kappa}B Activation and Neutrophil Recruitment Require IL-1 and TNF Receptor Signaling during Pneumococcal Pneumonia. J. Immunol. 175: 7530-7535 [Abstract] [Full Text]  
• Kao, C.-Y., Huang, F., Chen, Y., Thai, P., Wachi, S., Kim, C., Tam, L., Wu, R. (2005). Up-Regulation of CC Chemokine Ligand 20 Expression in Human Airway Epithelium by IL-17 through a JAK-Independent but MEK/NF-{kappa}B-Dependent Signaling Pathway. J. Immunol. 175: 6676-6685 [Abstract] [Full Text]  
• Kielian, T., Haney, A., Mayes, P. M., Garg, S., Esen, N. (2005). Toll-Like Receptor 2 Modulates the Proinflammatory Milieu in Staphylococcus aureus-Induced Brain Abscess. Infect. Immun. 73: 7428-7435 [Abstract] [Full Text]  
• Happel, K. I., Dubin, P. J., Zheng, M., Ghilardi, N., Lockhart, C., Quinton, L. J., Odden, A. R., Shellito, J. E., Bagby, G. J., Nelson, S., Kolls, J. K. (2005). Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. JEM 202: 761-769 [Abstract] [Full Text]  
• Lubberts, E., Schwarzenberger, P., Huang, W., Schurr, J. R., Peschon, J. J., van den Berg, W. B., Kolls, J. K. (2005). Requirement of IL-17 Receptor Signaling in Radiation-Resistant Cells in the Joint for Full Progression of Destructive Synovitis. J. Immunol. 175: 3360-3368 [Abstract] [Full Text]  
• Sugimoto, Y., Fukada, Y., Mori, D., Tanaka, S., Yamane, H., Okuno, Y., Deai, K., Tsuchiya, S., Tsujimoto, G., Ichikawa, A. (2005). Prostaglandin E2 Stimulates Granulocyte Colony-Stimulating Factor Production via the Prostanoid EP2 Receptor in Mouse Peritoneal Neutrophils. J. Immunol. 175: 2606-2612 [Abstract] [Full Text]  
• Ning, W., Choi, A. M. K., Li, C. (2005). Carbon monoxide inhibits IL-17-induced IL-6 production through the MAPK pathway in human pulmonary epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 289: L268-L273 [Abstract] [Full Text]  

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