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The Journal of Immunology, 2007, 178: 3786-3796.
Copyright © 2007 by The American Association of Immunologists, Inc.

IL-17-Mediated Regulation of Innate and Acquired Immune Response against Pulmonary Mycobacterium bovis Bacille Calmette-Guérin Infection1

Masayuki Umemura2,*,{ddagger}, Ayano Yahagi*,{ddagger}, Satoru Hamada*,§, Mst Dilara Begum*,{ddagger}, Hisami Watanabe{dagger}, Kazuyoshi Kawakami, Takashi Suda||, Katsuko Sudo#, Susumu Nakae#, Yoichiro Iwakura# and Goro Matsuzaki*,{ddagger}

* Molecular Microbiology Group, and {dagger} Immunobiology Group, Center of Molecular Biosciences, University of the Ryukyus, Okinawa, Japan; {ddagger} Division of Host Defense and Vaccinology, Department of Microbiology, and § Division of Child Health and Welfare, Department of Investigative Medicine, Graduate School of Medicine, University of the Ryukyus, Okinawa, Japan; Division of Microbiology and Immunobiology, Department of Medical Technology, School of Health Sciences, Tohoku University and Infection Control Research Center, Tohoku University Hospital, Miyagi, Japan; || Division of Immunology and Molecular Biology, Cancer Research Institute, Kanazawa University, Ishikawa, Japan; and # Center for Experimental Medicine, Institute of Medical Science, University of Tokyo, Tokyo, Japan

IL-17 is a cytokine that induces neutrophil-mediated inflammation, but its role in protective immunity against intracellular bacterial infection remains unclear. In the present study, we demonstrate that IL-17 is an important cytokine not only in the early neutrophil-mediated inflammatory response, but also in T cell-mediated IFN-{gamma} production and granuloma formation in response to pulmonary infection by Mycobacterium bovis bacille Calmette-Guérin (BCG). IL-17 expression in the BCG-infected lung was detected from the first day after infection and the expression depended on IL-23. Our observations indicated that {gamma}{delta} T cells are a primary source of IL-17. Lung-infiltrating T cells of IL-17-deficient mice produced less IFN-{gamma} in comparison to those from wild-type mice 4 wk after BCG infection. Impaired granuloma formation was also observed in the infected lungs of IL-17-deficient mice, which is consistent with the decreased delayed-type hypersensitivity response of the infected mice against mycobacterial Ag. These data suggest that IL-17 is an important cytokine in the induction of optimal Th1 response and protective immunity against mycobacterial infection.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

1 This work was supported by grants from the Ministry of Education, Culture, Sports, Science and Technology of Japan, The Naito Foundation, and Takeda Science Foundation.

2 Address correspondence and reprint requests to Dr. Masayuki Umemura, Molecular Microbiology Group, Center of Molecular Biosciences, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan. E-mail address: umemura{at}comb.u-ryukyu.ac.jp

3 Abbreviations used in this paper: KO, knockout; i.t., intratracheally; DTH, delayed-type hypersensitivity; PPD, purified protein derivative; LN, lymph node; PIF, pulmonary infiltrated; BAL, bronchoalveolar lavage fluid; FCM, flow cytometry; Ct, cycle threshold.




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