Molecular and functional characterization of Toll-like receptor (Tlr)1 and Tlr2 in common carp ( Cyprinus carpio )

Fink, I.R.; Pietretti, Danilo; Voogdt, Carlos G.P.; Westphal, Adrie H.; Savelkoul, H.F.J.; Forlenza, Maria; Wiegertjes, G.F.

doi:10.1016/j.fsi.2016.06.049

Cited by 44 publications

(23 citation statements)

References 57 publications

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“…In mammals, TLR1 is involved in the recognition of triacylated lipoproteins and mycobacterial products by binding to TLR2 to form a heterodimer ( 157 ). Teleost TLR1 and TLR2 have been characterized in Tetraodon ( Tetraodon nigroviridis ) ( 157 ), pufferfish ( Takifugu rubripes ) ( 158 ), zebrafish ( Danio rerio ) ( 159 , 160 ), Japanese flounder ( Paralichthys olivaceus ) ( 161 ), channel catfish ( Ictalurus punctatus ) ( 152 , 162 ), rainbow trout ( Oncorhynchus mykiss ) ( 163 , 164 ), orange-spotted grouper ( Epinephelus coioides ) ( 165 ), large yellow croaker ( Pseudosciaena crocea ) ( 166 – 168 ), rohu ( Labeo rohita ) ( 169 ), common carp ( Cyprinus carpio ) ( 170 ), and grass carp ( Ctenopharyngodon idella ) ( 171 ). TLR2 signaling plays an important role in the activation of intestinal immune system in mammals ( 172 ).…”

Section: Tlrs In Non-mammalian Vertebratesmentioning

confidence: 99%

“…Searches for reptilian TLR sequences have identified these in only one species, the green anole lizard Anolis carolinensis , which have been annotated as molecules resembling mammalian TLR2, 3, 4, 5, 6, 7, and 13. Recently, Voogdt and colleagues ( 170 ) reported the cloning, characterization, and functional analysis of TLR5 from A. carolinensis , and found that the receptor (acTLR5) displays a typical TLR protein structure with 22 extracellular LRRs flanked by N- and C-terminal LRR domains, an intracellular TIR domain, and a transmembrane region. Phylogenetically, acTLR5 is most distant from the TLR5 of fish and closest to the avian TLR5.…”

Section: Tlrs In Non-mammalian Vertebratesmentioning

confidence: 99%

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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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Section: Tlrs In Non-mammalian Vertebratesmentioning

confidence: 99%

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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“…Common carp ( Cyprinus carpio L.) is a freshwater fish widespread in Europe and Asia. To date, TLR1 and TLR2 [ 19 , 20 ], TLR3 [ 21 ], TLR4 [ 22 ], TLR9 [ 23 ], TLR18 [ 24 ], TLR20 [ 25 ] and TLR22 [ 26 ] were reported in common carp. Since TLRs play an important role in host anti-pathogen responses, the study of TLRs will be beneficial to the disease control of common carp.…”

Section: Introductionmentioning

confidence: 99%

Molecular characterization and expression patterns of a non-mammalian toll-like receptor gene (TLR21) in larvae ontogeny of common carp (Cyprinus carpio L.) and upon immune stimulation

Guo

et al. 2018

BMC Vet Res

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BackgroundIn the host innate immune system, various pattern recognition receptors (PRRs) recognize conserved pathogen-associated molecular patterns (PAMPs) and represent an efficient first line of defense against invading pathogens. Toll-like receptors (TLRs) are a major class of PRRs, which are able to recognize a wide range of PAMPs and play a central role in initiating innate immune responses. TLR21 is one of the non-mammalian TLRs identified in some bird and fish species.ResultsIn the present study, we reported the cloning and identification of a TLR21 cDNA from the head kidney of common carp (Cyprinus carpio L.), named CcTLR21. The full-length CcTLR21 cDNA was 3557 bp long, including an open reading frame (ORF) of 2895 bp, which encoded a putative protein of 964 amino acids. The putative CcTLR21 protein was found to comprise a signal peptide, 14 LRR domains in the extracellular region and a TIR domain in the cytoplasmic region, which fits with the characteristic TLR domain architecture. The phylogenetic analysis showed that CcTLR21 possessed high amino acid identities with the TLR21s in other freshwater teleosts. A Real-time PCR assay showed that CcTLR21 mRNA was expressed in almost all tissues examined in healthy common carp, while the levels obviously varied among different tissues. During the embryonic and early larval developmental stages of common carp, the CcTLR21 showed two peaks of expression, with the first at 1 dpf and the second at 10 dpf. When challenged with poly(I:C) (a viral model) or Aeromonas hydrophila, the expression level of CcTLR21 was up-regulated in a variety of common carp tissues.ConclusionsOur findings indicate that CcTLR21 plays a significant role in innate immune defense during larvae ontogeny and in responses to viral or bacterial pathogens.Electronic supplementary materialThe online version of this article (10.1186/s12917-018-1474-4) contains supplementary material, which is available to authorized users.

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“…For reasons unknown, TLR10 has been preserved in some mammals (including humans) and has been lost in other vertebrates. Among teleost fish, the common carp ( Cyprinus carpio ) duplicated its TLR2 gene ( 11 ), whereas the Atlantic cod ( Gadus morhua ) lost TLR1, TLR2, TLR6, and TLR10 altogether ( 12 ). In birds, duplications of TLR1 and TLR2 are abundant ( 6 , 13 ) which has left chicken ( Gallus gallus ) with the paralogs TLR2A, TLR2B, TLR1A (also known as TLR16), and TLR1B.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary Regression and Species-Specific Codon Usage of TLR15

et al. 2018

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Toll-like receptors (TLRs) form an ancient family of innate immune receptors that detect microbial structures and activate the host immune response. Most subfamilies of TLRs (including TLR3, TLR5, and TLR7) are highly conserved among vertebrate species. In contrast, TLR15, a member of the TLR1 subfamily, appears to be unique to birds and reptiles. We investigated the functional evolution of TLR15. Phylogenetic and synteny analyses revealed putative TLR15 orthologs in bird species, several reptilian species and also in a shark species, pointing to an unprecedented date of origin of TLR15 as well as large scale reciprocal loss of this TLR in most other vertebrates. Cloning and functional analysis of TLR15 of the green anole lizard (Anolis carolinensis), salt water crocodile (Crocodylus porosus), American alligator (Alligator mississippiensis), and chicken (Gallus gallus) showed for all species TLR15 specific protease-induced activation of NF-κB, despite highly variable TLR15 protein expression levels. The variable TLR15 expression was consistent in both human and reptilian cells and could be attributed to species-specific differences in TLR15 codon usage. The species-specific codon bias was not or barely noted for more evolutionarily conserved TLRs (e.g., TLR3). Overall, our results indicate that TLR15 originates before the divergence of chondrichthyes fish and tetrapods and that TLR15 of both avian and reptilian species has a conserved function as protease activated receptor. The species-specific codon usage and large scale loss of TLR15 in most vertebrates suggest evolutionary regression of this ancient TLR.

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Molecular and functional characterization of Toll-like receptor (Tlr)1 and Tlr2 in common carp ( Cyprinus carpio )

Cited by 44 publications

References 57 publications

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

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

Molecular characterization and expression patterns of a non-mammalian toll-like receptor gene (TLR21) in larvae ontogeny of common carp (Cyprinus carpio L.) and upon immune stimulation

Evolutionary Regression and Species-Specific Codon Usage of TLR15

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