Adaptor Molecule TRIF in Teleost
Journal: Journal of Clinical Medicine Research DOI: 10.32629/jcmr.v1i2.189
Abstract
The immune defense mechanism mainly depends on the recognition and response of innate immune signaling receptors PRRs to PAMPs or DAMPs. TLRs family is an important category in PRRs, stimulatory cytokines and interferon type I (IFN) are produced through TRIF-or MyD88-dependent after TLRs recognition PAMPs or DAMPs, which regulate innate and adaptive immunity responses. TLR3 only relies on the TRIF-dependent pathway for downstream signaling, TLR4 can conduct downstream signaling through both TRIF- and MyD88-dependent pathways. Teleosts TLR3 detects viral and additionally bacterial PAMPs, while TLR3-mediated activation of mammalian immune responses only depends on viral double-stranded RNA intermediates. Teleost TLR4 is suggested to down-regulate TLR signaling and/or to interact with alternative receptors such as b2-integrins, whereas mammalian TLR4 associates with CD14 and MD2 in order to sense LPS. In this review, we will further study the structure of TRIF, the TRIF-dependent signaling pathway, and its function in fish, with emphasis on the TRIF-dependent signaling pathway and different biological activities. The study of TRIF and its role in innate immunity has potential significance for the prevention and treatment of fish diseases.
Keywords
TRIF, TRIF-dependent pathway, signal transduction, TLR3＆4, teleost
Funding
The Fundamental Research Funds for the Central Universities (201822025, 201762003) and Shandong Provincial Natural Science Foundation (ZR2019MC051)
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[2] Kvarnhammar AM, Cardell LO. Pattern-recognition receptors in human eosinophils. Immunology. 2012; 136(1): 11-20.
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[4] Bruce B. Inferences, questions and possibilities in Toll-like receptor signalling. Nature. 2004; 430(6996): 257-263.
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[6] Kumeta H, Sakakibara H, Enokizono Y, Ogura K, Horiuchi M, Matsumoto M, et al. The N-terminal domain of TIR domain-containing adaptor molecule-1, TICAM-1. J Biomol NMR. 2014; 58(3): 227-230.
[7] O'Neill LAJ, Golenbock D, Bowie AG. The history of Toll-like receptors — Redefining innate immunity. Nature Reviews Immunology. 2013; 13(6): 453-460.
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[9] Joseph S Nelson. Fishes of the World. Fourth Edition. New Jersey: Wiley; 2006.
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[11] Horng T, Barton GM, Medzhitov R. TIRAP: an adapter molecule in the Toll signaling pathway. Nat Immunol. 2001; 2(9): 835-841.
[12] Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol. 2003; 4(2): 161-167.
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[15] Sato S, Sugiyama M, Yamamoto M, Watanabe Y, Kawai T, Takeda K, et al. Toll/IL-1 Receptor Domain-Containing Adaptor Inducing IFN-β (TRIF) Associates with TNF Receptor-Associated Factor 6 and TANK-Binding Kinase 1, and Activates Two Distinct Transcription Factors, NF-κB and IFN-Regulatory Factor-3, in the Toll-Like Receptor Signaling. J Immunol. 2003; 171(8): 4304-4310.
[16] Sasai M, Tatematsu M, Oshiumi H, Funami K, Matsumoto M, Hatakeyama S, et al. Direct binding of TRAF2 and TRAF6 to TICAM-1/TRIF daptor participates in activation of the Toll-like receptor 3/4 pathway. Mol Immunol. 2010; 47(6): 1283-1291.
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[21] Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010; 11(5): 373-384.
[22] Chang M, Jin W, Sun SC. Peli1 facilitates TRIF-dependent Toll-like receptor signaling and proinflammatory cytokine production. Nat Immunol. 2009; 10(10): 1089-1095.
[23] Kawasaki T, Takemura N, Standley DM, Akira S, Kawai T. The second messenger phosphatidylinositol-5-phosphate facilitates antiviral innate immune signaling. Cell Host Microbe. 2013; 14(2): 148-158.
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[26] Da SC, J., Ulevitch RJ. MD-2 and TLR4 N-Linked Glycosylations Are Important for a Functional Lipopolysaccharide Receptor. J Biol Chem. 2002; 277(3): 1845-1854.
[27] Visintin A, Mazzoni A, Spitzer JA, Segal DM. Secreted MD-2 is a large polymeric protein that efficiently confers lipopolysaccharide sensitivity to Toll-like receptor 4. Proceedings of the National Academy of ences. 2001; 98(21): 12156-12161.
[28] Lek M, Karczewski K, Minikel E, et al. Analysis of protein-coding genetic variation in 60,706 humans. Nature. 2016; 536(7616): 285-291.
[29] Arbour NC, Lorenz E, Schutte BC, Zabner J, Kline JN, Jones M, et al. TLR4 mutations are associated with endotoxin hyporesponsiveness in humans. Nat Genet. 2000; 25(2):187-191.
[30] Sebastiani G, Leveque G, Larivière L, Laroche L, Malo D. Cloning and Characterization of the Murine Toll-like Receptor 5 (Tlr5) Gene: Sequence and mRNA Expression Studies in Salmonella-Susceptible MOLF/Ei Mice. Genomics. 2000; 64(3): 230-240.
[31] Volff JN. Genome evolution and biodiversity in teleost fish. Heredity (Edinb). 2005; 94(3): 280-294.
[32] Wittbrodt J, Meyer A, Schartl M. More genes in fish? Bioessays. 1998; 20(6): 511-515.
[33] Baoprasertkul P, Peatman E, Somridhivej B, Liu Z. Toll-like receptor 3 and TICAM genes in catfish: species-specific expression profiles following infection with Edwardsiella ictaluri. Immunogenetics. 2006; 58(10): 817-830.
[34] Fan S, Chen S, Liu Y, Lin Y, Liu H, Guo L, et al. Zebrafish TRIF, a Golgi-localized protein, participates in IFN induction and NF-κB activation. J Immunol. 2008; 180(8): 5373-5383.
[35] Yang C, Li Q, Su J, Chen X, Wang Y, Peng L. Identification and functional characterizations of a novel TRIF gene from grass carp (Ctenopharyngodon idella). Dev Comp Immunol. 2013; 41(2): 222-229.
[36] Wei J, Zhang X, Zang S, Qin Q. Expression and functional characterization of TRIF in orange-spotted grouper (Epinephelus coioides). Fish Shellfish Immunol. 2017; 71: 295-304.
[37] Zou PF, Shen JJ, Li Y, Yan Q, Zou ZH, Zhang ZP, et al. Molecular cloning and functional characterization of TRIF in large yellow croaker Larimichthys crocea. Fish Shellfish Immunol. 2019; 91: 108-121.
[38] Chiou PP, Lin CM, Bols NC, Chen TT. Characterization of virus/double-stranded RNA-dependent induction of antimicrobial peptide hepcidin in trout macrophages. Dev Comp Immunol. 2007; 31(12): 1297-1309.
[39] Hu GB, Li XP, Liu DH, Liu QM, Zhang SC. A toll-like receptor 3 homologue that is up-regulated by poly I:C and DNA virus in turbot Scophthalmus maximus. J Fish Biol. 2015; 86(2): 431-447.
[40] Bilodeau AL, Peterson BC, Bosworth BG. Response of toll-like receptors, lysozyme, and IGF-I in back-cross hybrid (F1 male (blue x channel) x female channel) catfish challenged with virulent Edwardsiella ictaluri. Fish Shellfish Immunol. 2006; 20(1): 29-39.
[41] Bilodeau AL, Waldbieser GC. Activation of TLR3 and TLR5 in channel catfish exposed to virulent Edwardsiella ictaluri. Dev Comp Immunol. 2005; 29(8): 713-721.
[42] Chau TL, Gioia R, Gatot JS, Patrascu F, Carpentier I, Chapelle JP, et al. Are the IKKs and IKK-related kinases TBK1 and IKK-epsilon similarly activated? Trends Biochem Sci. 2008; 33(4): 171-180.
[43] Zou PF, Shen JJ, Li Y, Zhang ZP, Wang YL. TRAF3 enhances TRIF-mediated signaling via NF-kappaB and IRF3 activation in large yellow croaker Larimichthys crocea. Fish Shellfish Immunol. 2020; 97: 114-124.
[44] Nayak SK, Swain P, Nanda PK, Dash S, Shukla S, Meher PK, et al. Effect of endotoxin on the immunity of Indian major carp, Labeo rohita. Fish Shellfish Immunol. 2008; 24(4): 394-399.
[45] Purcell MK, Smith KD, Hood L, Winton JR, Roach JC. Conservation of Toll-Like Receptor Signaling Pathways in Teleost Fish. Comparative biochemistry and physiology Part D, Genomics & proteomics. 2006; 1(1): 77-88.
[46] Meijer AH, Gabby Krens SF, Medina Rodriguez IA, He S, Bitter W, Ewa Snaar-Jagalska B, et al. Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol Immunol. 2004; 40(11): 773-783.
[47] Su J, Yang C, Xiong F, Wang Y, Zhu Z. Toll-like receptor 4 signaling pathway can be triggered by grass carp reovirus and Aeromonas hydrophila infection in rare minnow Gobiocypris rarus. Fish Shellfish Immunol. 2009; 27(1): 33-39.
[48] Sepulcre MP, Alcaraz-Perez F, Lopez-Munoz A, Roca FJ, Meseguer J, Cayuela ML, et al. Evolution of lipopolysaccharide (LPS) recognition and signaling: fish TLR4 does not recognize LPS and negatively regulates NF-kappaB activation. J Immunol. 2009; 182(4): 1836-1845.
[2] Kvarnhammar AM, Cardell LO. Pattern-recognition receptors in human eosinophils. Immunology. 2012; 136(1): 11-20.
[3] Roach JC, Gustavo G, Lee R, Amardeep K, Purcell MK, Smith KD, et al. The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci U S A. 2005; 102(27): 9577-9582.
[4] Bruce B. Inferences, questions and possibilities in Toll-like receptor signalling. Nature. 2004; 430(6996): 257-263.
[5] Boudinot P, Zou J, Ota T, Buonocore F, Scapigliati G, Canapa A, et al. A tetrapod-like repertoire of innate immune receptors and effectors for coelacanths. J Exp Zool B Mol Dev Evol. 2014; 322(6): 415-437.
[6] Kumeta H, Sakakibara H, Enokizono Y, Ogura K, Horiuchi M, Matsumoto M, et al. The N-terminal domain of TIR domain-containing adaptor molecule-1, TICAM-1. J Biomol NMR. 2014; 58(3): 227-230.
[7] O'Neill LAJ, Golenbock D, Bowie AG. The history of Toll-like receptors — Redefining innate immunity. Nature Reviews Immunology. 2013; 13(6): 453-460.
[8] Saavedra V, Moghaddas F, Latz E, Masters SL. Pattern Recognition Receptors in Autoinflammation//Philip J. H, Ronald M. L, Simon A. Textbook of Autoinflammation. 2019.
[9] Joseph S Nelson. Fishes of the World. Fourth Edition. New Jersey: Wiley; 2006.
[10] Tanekhy M. The role of Toll-like Receptors in innate immunity and infectious diseases of teleost. Aquacult Res. 2016; 47(5): 1369-1391.
[11] Horng T, Barton GM, Medzhitov R. TIRAP: an adapter molecule in the Toll signaling pathway. Nat Immunol. 2001; 2(9): 835-841.
[12] Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol. 2003; 4(2): 161-167.
[13] Ullah MO, Ve T, Mangan M, et al. The TLR signalling adaptor TRIF/TICAM-1 has an N-terminal helical domain with structural similarity to IFIT proteins. Acta Crystallogr D Biol Crystallogr. 2013; 69(Pt 12): 2420-2430.
[14] Tatematsu M, Ishii A, Oshiumi H, et al. A molecular mechanism for Toll-IL-1 receptor domain-containing adaptor molecule-1-mediated IRF-3 activation. J Biol Chem. 2010; 285(26): 20128-20136.
[15] Sato S, Sugiyama M, Yamamoto M, Watanabe Y, Kawai T, Takeda K, et al. Toll/IL-1 Receptor Domain-Containing Adaptor Inducing IFN-β (TRIF) Associates with TNF Receptor-Associated Factor 6 and TANK-Binding Kinase 1, and Activates Two Distinct Transcription Factors, NF-κB and IFN-Regulatory Factor-3, in the Toll-Like Receptor Signaling. J Immunol. 2003; 171(8): 4304-4310.
[16] Sasai M, Tatematsu M, Oshiumi H, Funami K, Matsumoto M, Hatakeyama S, et al. Direct binding of TRAF2 and TRAF6 to TICAM-1/TRIF daptor participates in activation of the Toll-like receptor 3/4 pathway. Mol Immunol. 2010; 47(6): 1283-1291.
[17] Meylan E, Burns K, Hofmann K, Blancheteau V, Martinon F, Kelliher M, et al. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-κB activation. Nat Immunol. 2004; 5(5): 503-507.
[18] Vercammen E, Staal J, Beyaert R. Sensing of viral infection and activation of innate immunity by toll-like receptor 3. Clin Microbiol Rev. 2008; 21(1): 13-25.
[19] Dauphinee SM, Karsan A. Lipopolysaccharide signaling in endothelial cells. Lab Invest. 2006; 86(1): 9-22.
[20] Takeda K, Akira S. TLR signaling pathways. Semin Immunol. 2004; 16(1): 3-9.
[21] Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010; 11(5): 373-384.
[22] Chang M, Jin W, Sun SC. Peli1 facilitates TRIF-dependent Toll-like receptor signaling and proinflammatory cytokine production. Nat Immunol. 2009; 10(10): 1089-1095.
[23] Kawasaki T, Takemura N, Standley DM, Akira S, Kawai T. The second messenger phosphatidylinositol-5-phosphate facilitates antiviral innate immune signaling. Cell Host Microbe. 2013; 14(2): 148-158.
[24] Kawasaki T, Kawai T. Toll-like receptor signaling pathways. Front Immunol. 2014; 5: 461.
[25] Wright, S. D. Toll, A New Piece in the Puzzle of Innate Immunity. The Journal of experimental medicine. 1999; 189(4): 605-609.
[26] Da SC, J., Ulevitch RJ. MD-2 and TLR4 N-Linked Glycosylations Are Important for a Functional Lipopolysaccharide Receptor. J Biol Chem. 2002; 277(3): 1845-1854.
[27] Visintin A, Mazzoni A, Spitzer JA, Segal DM. Secreted MD-2 is a large polymeric protein that efficiently confers lipopolysaccharide sensitivity to Toll-like receptor 4. Proceedings of the National Academy of ences. 2001; 98(21): 12156-12161.
[28] Lek M, Karczewski K, Minikel E, et al. Analysis of protein-coding genetic variation in 60,706 humans. Nature. 2016; 536(7616): 285-291.
[29] Arbour NC, Lorenz E, Schutte BC, Zabner J, Kline JN, Jones M, et al. TLR4 mutations are associated with endotoxin hyporesponsiveness in humans. Nat Genet. 2000; 25(2):187-191.
[30] Sebastiani G, Leveque G, Larivière L, Laroche L, Malo D. Cloning and Characterization of the Murine Toll-like Receptor 5 (Tlr5) Gene: Sequence and mRNA Expression Studies in Salmonella-Susceptible MOLF/Ei Mice. Genomics. 2000; 64(3): 230-240.
[31] Volff JN. Genome evolution and biodiversity in teleost fish. Heredity (Edinb). 2005; 94(3): 280-294.
[32] Wittbrodt J, Meyer A, Schartl M. More genes in fish? Bioessays. 1998; 20(6): 511-515.
[33] Baoprasertkul P, Peatman E, Somridhivej B, Liu Z. Toll-like receptor 3 and TICAM genes in catfish: species-specific expression profiles following infection with Edwardsiella ictaluri. Immunogenetics. 2006; 58(10): 817-830.
[34] Fan S, Chen S, Liu Y, Lin Y, Liu H, Guo L, et al. Zebrafish TRIF, a Golgi-localized protein, participates in IFN induction and NF-κB activation. J Immunol. 2008; 180(8): 5373-5383.
[35] Yang C, Li Q, Su J, Chen X, Wang Y, Peng L. Identification and functional characterizations of a novel TRIF gene from grass carp (Ctenopharyngodon idella). Dev Comp Immunol. 2013; 41(2): 222-229.
[36] Wei J, Zhang X, Zang S, Qin Q. Expression and functional characterization of TRIF in orange-spotted grouper (Epinephelus coioides). Fish Shellfish Immunol. 2017; 71: 295-304.
[37] Zou PF, Shen JJ, Li Y, Yan Q, Zou ZH, Zhang ZP, et al. Molecular cloning and functional characterization of TRIF in large yellow croaker Larimichthys crocea. Fish Shellfish Immunol. 2019; 91: 108-121.
[38] Chiou PP, Lin CM, Bols NC, Chen TT. Characterization of virus/double-stranded RNA-dependent induction of antimicrobial peptide hepcidin in trout macrophages. Dev Comp Immunol. 2007; 31(12): 1297-1309.
[39] Hu GB, Li XP, Liu DH, Liu QM, Zhang SC. A toll-like receptor 3 homologue that is up-regulated by poly I:C and DNA virus in turbot Scophthalmus maximus. J Fish Biol. 2015; 86(2): 431-447.
[40] Bilodeau AL, Peterson BC, Bosworth BG. Response of toll-like receptors, lysozyme, and IGF-I in back-cross hybrid (F1 male (blue x channel) x female channel) catfish challenged with virulent Edwardsiella ictaluri. Fish Shellfish Immunol. 2006; 20(1): 29-39.
[41] Bilodeau AL, Waldbieser GC. Activation of TLR3 and TLR5 in channel catfish exposed to virulent Edwardsiella ictaluri. Dev Comp Immunol. 2005; 29(8): 713-721.
[42] Chau TL, Gioia R, Gatot JS, Patrascu F, Carpentier I, Chapelle JP, et al. Are the IKKs and IKK-related kinases TBK1 and IKK-epsilon similarly activated? Trends Biochem Sci. 2008; 33(4): 171-180.
[43] Zou PF, Shen JJ, Li Y, Zhang ZP, Wang YL. TRAF3 enhances TRIF-mediated signaling via NF-kappaB and IRF3 activation in large yellow croaker Larimichthys crocea. Fish Shellfish Immunol. 2020; 97: 114-124.
[44] Nayak SK, Swain P, Nanda PK, Dash S, Shukla S, Meher PK, et al. Effect of endotoxin on the immunity of Indian major carp, Labeo rohita. Fish Shellfish Immunol. 2008; 24(4): 394-399.
[45] Purcell MK, Smith KD, Hood L, Winton JR, Roach JC. Conservation of Toll-Like Receptor Signaling Pathways in Teleost Fish. Comparative biochemistry and physiology Part D, Genomics & proteomics. 2006; 1(1): 77-88.
[46] Meijer AH, Gabby Krens SF, Medina Rodriguez IA, He S, Bitter W, Ewa Snaar-Jagalska B, et al. Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish. Mol Immunol. 2004; 40(11): 773-783.
[47] Su J, Yang C, Xiong F, Wang Y, Zhu Z. Toll-like receptor 4 signaling pathway can be triggered by grass carp reovirus and Aeromonas hydrophila infection in rare minnow Gobiocypris rarus. Fish Shellfish Immunol. 2009; 27(1): 33-39.
[48] Sepulcre MP, Alcaraz-Perez F, Lopez-Munoz A, Roca FJ, Meseguer J, Cayuela ML, et al. Evolution of lipopolysaccharide (LPS) recognition and signaling: fish TLR4 does not recognize LPS and negatively regulates NF-kappaB activation. J Immunol. 2009; 182(4): 1836-1845.
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