The Journal of Experimental Medicine
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Published online
doi:10.1084/jem.20091436
The Journal of Experimental Medicine, Vol. 206, No. 11, 2351-2364
The Rockefeller University Press, 0022-1007 $30.00
© Nagatake et al.
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Article

 Id2-, ROR{gamma}t-, and LTβR-independent initiation of lymphoid organogenesis in ocular immunity

Takahiro Nagatake1,5, Satoshi Fukuyama1, Dong-Young Kim1,6, Kaoru Goda1, Osamu Igarashi1, Shintaro Sato1, Tomonori Nochi1, Hiroshi Sagara2, Yoshifumi Yokota7, Anton M. Jetten8, Tsuneyasu Kaisho9, Shizuo Akira10, Hitomi Mimuro3, Chihiro Sasakawa3, Yoshinori Fukui11, Kohtaro Fujihashi12, Taishin Akiyama4, Jun-ichiro Inoue4, Josef M. Penninger13, Jun Kunisawa1,14, and Hiroshi Kiyono1,5,12,14

1 Division of Mucosal Immunology, Department of Microbiology and Immunology, 2 Medical Proteomics Laboratory, 3 Division of Bacterial Infection, Department of Microbiology and Immunology, and 4 Division of Cellular and Molecular Biology, The Institute of Medical Science, The University of Tokyo, Minato-ku, Tokyo 108-8639, Japan
5 Graduate School of Medicine and Faculty of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan
6 Department of Otorhinolaryngology, Seoul National University College of Medicine, Chongno-gu, Seoul 110-744, Korea
7 Department of Molecular Genetics, School of Medicine, University of Fukui, Eiheiji-cho, Yoshida-gun, Fukui 910-1193, Japan
8 Cell Biology Section, Laboratory of Respiratory Biology, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, NC 27709
9 Laboratory for Host Defense, Research Center for Allergy and Immunology, Institute of Physical and Chemical Research, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan
10 Laboratory of Host Defense, World Premier International Research Center–Immunology Frontier Research Center, Osaka University, Suita, Osaka 565-0871, Japan
11 Division of Immunogenetics, Department of Immunobiology and Neuroscience, Medical Institute of Bioregulation, Kyushu University, Fukuoka 812-8582, Japan
12 Immunobiology Vaccine Center, Department of Pediatric Dentistry, The University of Alabama at Birmingham, Birmingham, AL 35294
13 Institute of Molecular Biotechnology of the Austrian Academy of Sciences, 1030 Vienna, Austria
14 Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba 277-8561, Japan

CORRESPONDENCE Hiroshi Kiyono: kiyono{at}ims.u-tokyo.ac.jp

The eye is protected by the ocular immunosurveillance system. We show that tear duct–associated lymphoid tissue (TALT) is located in the mouse lacrimal sac and shares immunological characteristics with mucosa-associated lymphoid tissues (MALTs), including the presence of M cells and immunocompetent cells for antigen uptake and subsequent generation of mucosal immune responses against ocularly encountered antigens and bacteria such as Pseudomonas aeruginosa. Initiation of TALT genesis began postnatally; it occurred even in germ-free conditions and was independent of signaling through organogenesis regulators, including inhibitor of DNA binding/differentiation 2, retinoic acid–related orphan receptor {gamma}t, lymphotoxin (LT) {alpha}1β2–LTβR, and lymphoid chemokines (CCL19, CCL21, and CXCL13). Thus, TALT shares immunological features with MALT but has a distinct tissue genesis mechanism and plays a key role in ocular immunity.

Abbreviations used: AID, activation-induced cytidine deaminase; CALT, conjunctiva-associated lymphoid tissue; CT, cholera toxin; FAE, follicle-associated epithelium; FDC, follicular DC; GC, germinal center; HE, hematoxylin and eosin; HEV, high endothelial venule; Id2, inhibitor of DNA binding/differentiation 2; ILF, isolated lymphoid follicle; LT, lymphotoxin; LTi, lymphoid tissue inducer; MAdCAM-1, mucosal addressin cell adhesion molecule 1; MALT, mucosa-associated lymphoid tissue; NALT, nasopharynx-associated lymphoid tissue; NIK, NF-{kappa}B–inducing kinase; NP, nasal passage; pLN, peripheral LN; PNA, peanut agglutinin; PNAd, pLN addressin; PP, Peyer's patch; ROR, retinoic acid–related orphan receptor; TALT, tear duct–associated lymphoid tissue; TLR, Toll-like receptor; TRAF, TNF receptor–associated factor; TRANCE, TNF-related activation-induced cytokine; UEA, Ulex europaeus agglutinin; VCAM-1, vascular cell adhesion molecule 1.

© 2009 Nagatake et al.
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.jem.org/misc/terms.shtml). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).


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