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

Overview

Journal BMC Vet Res

Publisher Biomed Central

Specialty Veterinary Medicine

Date 2018 May 5

PMID 29724212

Citations 11

Authors

Hua Li

Ting Li

Yujie Guo

Yujun Li

Yan Zhang

Na Teng

Fumiao Zhang

Guiwen Yang

Affiliations

Soon will be listed here.

Abstract

Background: In 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.

Results: In 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.

Conclusions: Our findings indicate that CcTLR21 plays a significant role in innate immune defense during larvae ontogeny and in responses to viral or bacterial pathogens.

Citing Articles

In Ovo Vaccination with Recombinant Herpes Virus of the Turkey-Laryngotracheitis Vaccine Adjuvanted with CpG-Oligonucleotide Provides Protection against a Viral Challenge in Broiler Chickens.

Gaghan C, Browning M, Fares A, Abdul-Careem M, Gimeno I, Kulkarni R Viruses. 2023; 15(10).

PMID: 37896880 PMC: 10612038. DOI: 10.3390/v15102103.

Transcriptome Analysis Reveals Molecular Underpinnings of Common Carp () Under Hypoxia Stress.

Suo N, Zhou Z, Xu J, Cao D, Wu B, Zhang H Front Genet. 2022; 13:907944.

PMID: 35669183 PMC: 9163828. DOI: 10.3389/fgene.2022.907944.

Molecular identification and functional characterization of IRF4 from common carp (Cyprinus carpio. L) in immune response: a negative regulator in the IFN and NF-κB signalling pathways.

Zhu Y, Yang G BMC Vet Res. 2022; 18(1):106.

PMID: 35300694 PMC: 8928632. DOI: 10.1186/s12917-022-03205-8.

Spätzle 1b Is Required to Confer Antibacterial Defense Against Gram-Negative Bacteria by Regulation of Antimicrobial Peptides.

Bae Y, Jo Y, Patnaik B, Kim B, Park K, Tesfaye Edosa T Front Physiol. 2021; 12:758859.

PMID: 34867464 PMC: 8637286. DOI: 10.3389/fphys.2021.758859.

Survival Mechanisms to Selective Pressures and Implications.

Xie S, Liu M Open Life Sci. 2021; 13:340-347.

PMID: 33817102 PMC: 7874742. DOI: 10.1515/biol-2018-0042.

References

Zhu Y, Qi C, Shan S, Zhang F, Li H, An L . Characterization of common carp (Cyprinus carpio L.) interferon regulatory factor 5 (IRF5) and its expression in response to viral and bacterial challenges. BMC Vet Res. 2016; 12(1):127. PMC: 4924235. DOI: 10.1186/s12917-016-0750-4. View

Pietretti D, Scheer M, Fink I, Taverne N, Savelkoul H, Spaink H . Identification and functional characterization of nonmammalian Toll-like receptor 20. Immunogenetics. 2013; 66(2):123-41. DOI: 10.1007/s00251-013-0751-4. View

Ribeiro C, Hermsen T, Taverne-Thiele A, Savelkoul H, Wiegertjes G . Evolution of recognition of ligands from Gram-positive bacteria: similarities and differences in the TLR2-mediated response between mammalian vertebrates and teleost fish. J Immunol. 2010; 184(5):2355-68. DOI: 10.4049/jimmunol.0900990. View

Shan S, Qi C, Zhu Y, Li H, An L, Yang G . Expression profile of carp IFN correlate with the up-regulation of interferon regulatory factor-1 (IRF-1) in vivo and in vitro: the pivotal molecules in antiviral defense. Fish Shellfish Immunol. 2016; 52:94-102. DOI: 10.1016/j.fsi.2016.03.019. View

Belvin M, Anderson K . A conserved signaling pathway: the Drosophila toll-dorsal pathway. Annu Rev Cell Dev Biol. 1996; 12:393-416. DOI: 10.1146/annurev.cellbio.12.1.393. View

Medzhitov R . Toll-like receptors and innate immunity. Nat Rev Immunol. 2002; 1(2):135-45. DOI: 10.1038/35100529. View

Li H, Zhang F, Guo H, Zhu Y, Yuan J, Yang G . Molecular characterization of hepcidin gene in common carp (Cyprinus carpio L.) and its expression pattern responding to bacterial challenge. Fish Shellfish Immunol. 2013; 35(3):1030-8. DOI: 10.1016/j.fsi.2013.07.001. View

Akira S . Pathogen recognition by innate immunity and its signaling. Proc Jpn Acad Ser B Phys Biol Sci. 2009; 85(4):143-56. PMC: 3524297. DOI: 10.2183/pjab.85.143. View

Reyes-Becerril M, Ascencio-Valle F, Hirono I, Kondo H, Jirapongpairoj W, Esteban M . TLR21's agonists in combination with Aeromonas antigens synergistically up-regulate functional TLR21 and cytokine gene expression in yellowtail leucocytes. Dev Comp Immunol. 2016; 61:107-15. DOI: 10.1016/j.dci.2016.03.012. View

10.

Priyathilaka T, Elvitigala D, Whang I, Lim B, Jeong H, Yeo S . Molecular characterization and transcriptional analysis of non-mammalian type Toll like receptor (TLR21) from rock bream (Oplegnathus fasciatus). Gene. 2014; 553(2):105-16. DOI: 10.1016/j.gene.2014.10.008. View

11.

Baoprasertkul P, Xu P, Peatman E, Kucuktas H, Liu Z . Divergent Toll-like receptors in catfish (Ictalurus punctatus): TLR5S, TLR20, TLR21. Fish Shellfish Immunol. 2007; 23(6):1218-30. DOI: 10.1016/j.fsi.2007.06.002. View

12.

Hacker H, Redecke V, Blagoev B, Kratchmarova I, Hsu L, Wang G . Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature. 2005; 439(7073):204-7. DOI: 10.1038/nature04369. View

13.

Lee M, Kim Y . Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu Rev Biochem. 2007; 76:447-80. DOI: 10.1146/annurev.biochem.76.060605.122847. View

14.

Pietretti D, Wiegertjes G . Ligand specificities of Toll-like receptors in fish: indications from infection studies. Dev Comp Immunol. 2013; 43(2):205-22. DOI: 10.1016/j.dci.2013.08.010. View

15.

Zhu Y, Xing W, Shan S, Zhang S, Li Y, Li T . Characterization and immune response expression of the Rig-I-like receptor mda5 in common carp Cyprinus carpio. J Fish Biol. 2016; 88(6):2188-202. DOI: 10.1111/jfb.12981. View

16.

Yang G, Guo H, Li H, Shan S, Zhang X, Rombout J . Molecular characterization of LEAP-2 cDNA in common carp (Cyprinus carpio L.) and the differential expression upon a Vibrio anguillarum stimulus; indications for a significant immune role in skin. Fish Shellfish Immunol. 2014; 37(1):22-9. DOI: 10.1016/j.fsi.2014.01.004. View

17.

Kongchum P, Hallerman E, Hulata G, David L, Palti Y . Molecular cloning, characterization and expression analysis of TLR9, MyD88 and TRAF6 genes in common carp (Cyprinus carpio). Fish Shellfish Immunol. 2010; 30(1):361-71. DOI: 10.1016/j.fsi.2010.11.012. View

18.

Shan S, Liu D, Liu R, Zhu Y, Li T, Zhang F . Non-mammalian Toll-like receptor 18 (Tlr18) recognizes bacterial pathogens in common carp (Cyprinus carpio L.): Indications for a role of participation in the NF-κB signaling pathway. Fish Shellfish Immunol. 2017; 72:187-198. DOI: 10.1016/j.fsi.2017.09.081. View

19.

Wang W, Shen Y, Pandit N, Li J . Molecular cloning, characterization and immunological response analysis of Toll-like receptor 21 (TLR21) gene in grass carp, Ctenopharyngodon idella. Dev Comp Immunol. 2013; 40(3-4):227-31. DOI: 10.1016/j.dci.2013.03.003. View

20.

Ishii A, Kawasaki M, Matsumoto M, Tochinai S, Seya T . Phylogenetic and expression analysis of amphibian Xenopus Toll-like receptors. Immunogenetics. 2007; 59(4):281-93. DOI: 10.1007/s00251-007-0193-y. View