Structural and evolutionary characteristics of fish-specific TLR19

Wang, Jinlan; Zheng, Zhen; Fu, Hui; Zhang, Shangli; Liu, Jing; Chang, Fen; Li, Fang; Zhao, Jing; Yin, Deling

doi:10.1016/j.fsi.2015.09.005

Cited by 15 publications

(9 citation statements)

References 55 publications

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“…Both TLR11 and TLR12 are only found in mammals, whereas TLR16 is unique to Xenopus and TLR19, TLR20 and TLR26 have only been found in some species of teleost36. Mouse TLR11 and TLR12 colocalize to similar endosomal compartments and are able to form homo- and hetero-dimers to recognize profilin from Toxoplasma gondii 3738.…”

Section: Resultsmentioning

confidence: 99%

Ectodomain Architecture Affects Sequence and Functional Evolution of Vertebrate Toll-like Receptors

Wang

Zhang

Liu

et al. 2016

Sci Rep

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Toll-like receptors (TLRs) are crucial components of innate immunity that specifically recognize diverse pathogen-associated molecular patterns from pathogens. The continuous hydrogen-bond network (asparagine ladder) formed among the asparagine residues on the concave surfaces of neighboring leucine-rich repeat modules assists in stabilizing the overall shape of TLR ectodomains responsible for ligand recognition. Analysis of 28 types of vertebrate TLRs showed that their ectodomains possessed three types of architectures: a single-domain architecture with an intact asparagine ladder, a three-domain architecture with the ladder interrupted in the middle, and a trans-three-domain architecture with the ladder broken in both termini. Based on a phylogenetic analysis, the three vertebrate TLR architectures arose during early evolution. The 1428 vertebrate TLRs can be divided into eight families based on sequence and structural differences. TLRs ligand specificities are affected by their ectodomain architectures. Three-domain TLRs bind hydrophobic ligands, whereas single-domain and trans-three-domain TLRs mainly recognize hydrophilic ligands. Analysis of 39 vertebrate genomes suggested that the number of single-domain TLR genes in terrestrial vertebrate genomes decreased by half compared to aquatic vertebrate genomes. Single-domain TLR genes underwent stronger purifying selective pressures than three-domain TLR genes in mammals. Overall, ectodomain architecture influences the sequence and functional evolution of vertebrate TLRs.

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Section: Resultsmentioning

confidence: 99%

Ectodomain Architecture Affects Sequence and Functional Evolution of Vertebrate Toll-like Receptors

Wang

Zhang

Liu

et al. 2016

Sci Rep

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“…TLR3 depends on the electrostatic surface potentials of LRRs to recognize dsRNA, and the ascending lateral surface has obviously positively charged regions (47). Similar to TLR3, TLR19 is also strongly charged on the ascending lateral surface of LRRs (30), implying that TLR19 may bind to dsRNA in connection with the electrostatic potential of the ascending lateral surface. In the current study, dsRNA analog poly(I:C) upregulates TLR19 expression, which means that TLR19 responds to poly(I: C).…”

Section: Discussionmentioning

confidence: 99%

“…*p , 0.05, **p , 0.01, ***p , 0.001. TLR20 and TLR23 to TLR28 are considered to be fish-specific TLRs (27)(28)(29)(30)(31). Up to now, TLR19 sequence has been identified in several teleosts such as Danio rerio (32), Ictalurus punctatus (33,34), Salmo salar (35), Megalobrama amblycephala (36), and Ctenopharyngodon idella (31).…”

mentioning

confidence: 99%

Teleost-Specific TLR19 Localizes to Endosome, Recognizes dsRNA, Recruits TRIF, Triggers both IFN and NF-κB Pathways, and Protects Cells from Grass Carp Reovirus Infection

Rao

Wan

et al. 2018

The Journal of Immunology

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TLRs are pivotal pattern recognition receptors in initiating innate immunity and triggering adaptive immunity. TLR pathways have been comprehensively investigated in mammals. However, the teleost-specific TLR19 pathway remains largely unknown. In this study, we identified TLR19 from grass carp (), and explored the ligand, adaptor, and signaling pathways. Pathogen-associated molecular pattern binding and luciferase activity assays indicate that TLR19 recognizes and responds to dsRNA analog (polyinosinic:polycytidylic acid). Confocal fluorescence microscopy demonstrates that TLR19 is synthesized in ribosomes not binding on endoplasmic reticulum, then transfers to early endosome post-polyinosinic:polycytidylic acid stimulation. Fluorescence colocalization and immunoprecipitation experiments confirm TLR19 interacts with adaptor TRIF, not MyD88, TIRAP, or SARM1. TLR19 facilitates protein and phosphorylation levels of IRF3, inhibits phosphorylation of IRF7. TLR19 enhances the promoter activities and mRNA expressions of major IFNs and NF-κBs; in contrast, grass carp TLR3 just significantly motivates IFN1 expression post-grass carp reovirus (GCRV) infection. Further investigations reveal that TLR19 inhibits GCRV replication by overexpression, knockdown, Western blotting techniques and virus titer assays, and protects cells from GCRV infection by flow cytometry and MTT method. Collectively, these results demonstrate that teleost-specific TLR19 recognizes dsRNA, recruits adaptor molecule TRIF, enhances IRF3 protein and phosphorylation levels, triggers both IFN and NF-κB pathways, and prevents viral proliferation. This is the first attempt to systematically clarify the TLR19 signaling pathway, which is the third TLR member recognizing dsRNA. The results will serve the antiviral immune mechanisms in teleost and evolutionary immunology.

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“…Numerous "fish-specific" TLRs have been isolated, including TLR13 ( 224 , 225 ), TLR19 ( 23 , 226 ), TLR20 ( 197 , 203 , 227 ), TLR21 ( 158 , 197 , 203 , 228 ), TLR22 ( 55 , 229 – 231 ), TLR23 ( 158 ), and TLR26 ( 152 ), in such fish as miiuy croaker, punctate-tailed fish, zebrafish, pufferfish, large yellow croaker, Atlantic salmon, Asian sea bass, orange-spotted grouper, grass carp, and barbel chub. Wang and colleagues were the first to report that in Perciformes (particularly Sciaenidae), the teleost TLR13 is highly expressed in such immune defense-related tissues as the spleen, liver, and kidney ( 224 ).…”

Section: Tlrs In Non-mammalian Vertebratesmentioning

confidence: 99%

Toll-Like Receptors, Associated Biological Roles, and Signaling Networks in Non-Mammals

et al. 2018

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The innate immune system is the first line of defense against pathogens, which is initiated by the recognition of pathogen-associated molecular patterns (PAMPs) and endogenous damage-associated molecular patterns (DAMPs) by pattern recognition receptors (PRRs). Among all the PRRs identified, the toll-like receptors (TLRs) are the most ancient class, with the most extensive spectrum of pathogen recognition. Since the first discovery of Toll in Drosophila melanogaster, numerous TLRs have been identified across a wide range of invertebrate and vertebrate species. It seems that TLRs, the signaling pathways that they initiate, or related adaptor proteins are essentially conserved in a wide variety of organisms, from Porifera to mammals. Molecular structure analysis indicates that most TLR homologs share similar domain patterns and that some vital participants of TLR signaling co-evolved with TLRs themselves. However, functional specification and emergence of new signaling pathways, as well as adaptors, did occur during evolution. In addition, ambiguities and gaps in knowledge still exist regarding the TLR network, especially in lower organisms. Hence, a systematic review from the comparative angle regarding this tremendous signaling system and the scenario of evolutionary pattern across Animalia is needed. In the current review, we present overview and possible evolutionary patterns of TLRs in non-mammals, hoping that this will provide clues for further investigations in this field.

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Structural and evolutionary characteristics of fish-specific TLR19

Cited by 15 publications

References 55 publications

Ectodomain Architecture Affects Sequence and Functional Evolution of Vertebrate Toll-like Receptors

Ectodomain Architecture Affects Sequence and Functional Evolution of Vertebrate Toll-like Receptors

Teleost-Specific TLR19 Localizes to Endosome, Recognizes dsRNA, Recruits TRIF, Triggers both IFN and NF-κB Pathways, and Protects Cells from Grass Carp Reovirus Infection

Toll-Like Receptors, Associated Biological Roles, and Signaling Networks in Non-Mammals

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