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* Department of Microbiology and Immunology, Hokkaido University Graduate School of Medicine, Sapporo, Japan;
Department of Integrated Biosciences, University of Tokyo, Chiba, Japan; and
Faculty of Fisheries Sciences, Hokkaido University, Hakodate, Japan
TLR22 occurs exclusively in aquatic animals and its role is unknown. Herein we show that the fugu (Takifugu rubripes) (fg)TLR3 and fgTLR22 link the IFN-inducing pathway via the fg Toll-IL-1R homology domain-containing adaptor protein 1(fgTICAM-1, or TRIF) adaptor in fish cells. fgTLR3 resides in endoplasmic reticulum and recognizes relatively short-sized dsRNA, whereas fgTLR22 recognizes long-sized dsRNA on the cell surface. On poly(I:C)-stimulated fish cells, both recruit fgTICAM-1, which in turn moves from the TLR to a cytoplasmic signalosome region. Thus, fgTICAM-1 acts as a shuttling platform for IFN signaling. When fish cells expressing fgTLR22 are exposed to dsRNA or aquatic dsRNA viruses, cells induce IFN responses to acquire resistance to virus infection. Thus, fish have a novel TICAM-1-coupling TLR that is distinct from the mammalian TLR3 in cellular localization, ligand selection, and tissue distribution. TLR22 may be a functional substitute of human cell-surface TLR3 and serve as a surveillant for infection with dsRNA virus to alert the immune system for antiviral protection in fish.
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1 This work was supported in part by CREST-JST (Japan Science and Technology Corporation), by Grants-in-Aid from the Ministry of Education, Science, and Culture (Specified Project for Advanced Research) and the Ministry of Health, Labor, and Welfare of Japan, and by the Takeda Science Foundation, Uehara Memorial Foundation, Northtec Foundation, Akiyama Foundation, and Mitsubishi Foundation. Financial support by the Sapporo Biocluster "Bio-S", the Knowledge Cluster Initiative of the MEXT, and the Program of Founding Research Centers for Emerging and Reemerging Infectious Diseases, MEXT, are gratefully acknowledged.
2 A.Y. and H.O. contributed equally to this paper.
3 Current address: Exploratory Research for Advanced Technology/Japan Science and Technology Center, Laboratory of Molecular and Developmental Biology, University of Tsukuba, Tennoudai 1-1-1, Tsukuba 305-8577, Japan.
4 Address correspondence and reprint requests to Dr. Tsukasa Seya, Department of Microbiology and Immunology, Graduate School of Medicine, Hokkaido University, Kita-ku, Sapporo 060-8638, Japan. E-mail address: seya-tu{at}pop.med.hokudai.ac.jp
5 Abbreviations used in this paper: RIG-I, retinoic acid-inducible gene I; BLAST, basic local alignment search tool; CPE, cytopathic effect; ER, endoplasmic reticulum; fg, Takifugu rubripes; HA, hemagglutinin; IPNV, infectious pancreatic necrosis virus; IRF-3, IFN regulatory factor 3; ISRE, IFN-stimulated regulatory element; LRR, leucine-rich repeat; MAVS, mitochondrial antiviral signaling protein; MDA5, melanoma differentiation-associated gene 5; moi, multiplicity of infection; NAP1, NAK-associated protein 1; PGN, peptidoglycan; rt, rainbow trout; polyC, polycytidylic acid; polyU, polyuridylic acid; TCID50, 50% tissue culture-infective dose; TICAM-1, Toll-IL-1R homology domain-containing adaptor protein 1; TIR, Toll-IL-1 receptor; YFP, yellow fluorescent protein; zf, zebrafish.
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