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Original Article • Braz. J. Poult. Sci. 24 (03) • 2022 • https://doi.org/10.1590/1806-9061-2020-1431   copy

Identification of Avian Toll-Like Receptor 3 and 7 and Analysis of Gene Variation Sites

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Toll-like receptors 3 and 7 (TLR3 and 7) mediate immune responses through the recognition of viral single-stranded RNA and double-stranded RNA and therefore play important roles in host defense. Differences in TLR3 or 7 may affect host resistance to RNA viral infection. To illuminate these differences, the partial coding sequence (CDS) of TLR3 and 7 genes were cloned and amplified from the Phasianus colchicus and Numida meleagris, total 64 avian species of TLR3 and 7 sequences were later analyzed. Based on the results, 315 non-synonymous mutation sites and 202 synonymous mutation sites were also observed in the avian TLR3, and 227 non-synonymous mutation sites and 174 synonymous mutation sites were observed in the avian TLR7. Among these sites, 44 and 45 sites were observed in functional regions of TLR3 and 7, used common variation of amino acids in most avian species. A number of these different sites appeared to affect the recognition and were also visualized. H59Y, E60K, G64R, E93K, L112S, K117E, N118K, R120H, V123M, L163F, R443Q, R459K, E460D, C485H, and F511L for TLR3, and I432V, M437V, and T732S for TLR7 were considered. It is possible that these sites bind to ligands and play crucial roles in viral recognition. These data indicated that the positive selection has occurred in the avian TLR3 and 7 genes.

Keywords:
Avian, Evolution; Numida Meleagris; Phasianus colchicus; Toll-Like Receptor (TLR)

INTRODUCTION

Toll-like receptors (TLRs) are the most-characterized receptors among the pattern recognition receptors (PRRs). PRRs are recognized as a diverse range of pathogen associated molecular patterns (PAMPs) and play a critical role in antimicrobial host defense (Medzhitov, 2001Medzhitov R. Toll-like receptors and innate immunity. Nature Reviews Immunology 2001;1:135-45.). Toll-like receptors are critical proteins linking innate and acquired immunity (Akira, 2001Akira S. Toll-like receptors and innate immunity. Advances in Immunology 2001;78:1-56.). TLRs are evolutionarily conserved with homologs present in insects, fish, mammals, and birds (Kimbrell & Beutler, 2001Kimbrell DA, Beutler B. The evolution and genetics of innate immunity. Nature Reviews Genetics 2001;2:256-67.; Roach et al., 2005Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, et al. The evolution of vertebrate Toll-like receptors. Proceedings of National Academy Science USA 2005;102:9577-82.; Satake & Sasaki, 2010Satake H, Sasaki N. Comparative overview of toll-like receptors in lower animals. Zoological Science 2010;27:154-61.; Valanne et al., 2011Valanne S, Wang JH and Ramet M. The Drosophila toll signaling pathway. Journal of Immunology 2011;186:649-56.). Ranges of TLR genes have been identified in avian species (Boyd et al., 2001Boyd Y, Goodchild M, Morroll S, Bumstead N. Mapping of the chicken and mouse genes for toll-like receptor 2 (TLR2) to an evolutionarily conserved chromosomal segment. Immunogenetics 2001;52:294-8.; Fukui et al., 2001Fukui A, Inoue N, Matsumoto M, Nomura M, Yamada K, Matsuda Y, et al. Molecular cloning and functional characterization of chicken toll-like receptors A single chicken toll covers multiple molecular patterns. Journal of Biological Chemistry 2001;276:47143-9.; Iqbal et al., 2005Iqbal M, Philbin V J, Withanage GS, Wigley P, Beal RK, Goodchild MJ, et al. Identification and functional characterization of chicken toll-like receptor 5 reveals a fundamental role in the biology of infection with Salmonella enterica serovar typhimurium. Infection and Immunity 2005;73:2344-50.; Philbin et al., 2005Philbin VJ, Iqbal M, Boyd Y, Goodchild MJ, Beal RK, Bumstead N, et al. Identification and characterization of a functional alternatively spliced Toll-like receptor 7 (TLR7) and genomic disruption of TLR8 in chickens. Immunology 2005;114:507- 21.; Yilmaz et al., 2005Yilmaz A, Shen S, Adelson DL, Xavier S, Zhu JJ. Identification and sequence analysis of chicken Toll-like receptors. Immunogenetics 2005;56:743-53.; Brownlie & Allan, 2011Brownlie R, Allan B. Avian toll-like receptors. Cell Tissue Research 2011;343:121-30.; Keestra et al., 2013Keestra AM, Zoete MR de, Bouwman LI, Vaezirad MM, Putten JP van. Unique features of chicken Toll-like receptors. Developmental and Comparative Immunology 2013;41:316-23.). All avian TLR family have 10 members that include TLR1 type 1 and type 2, TLR2 type 1 and type 2, TLR3, TLR4, TLR5, TLR7, TLR15, and TLR21. However, not all birds have exact 10 TLRs. Several species have duplicated TLR7, others not functional TLR5 (Brownlie & Allan, 2011; Velova et al., 2018Velova H, Gutowska-Ding MW, Burt DW, Vinkler M. Toll-like receptor evolution in birds: gene duplication pseudogenisation and diversifying selection. Molecular Biology and Evolution 2018;35(9):2170-84.). TLR1, TLR2, TLR4, and TLR5 have recognized bacterial components, such as peptidoglycans (PGN), lipopolysaccharides (LPS), cell wall lipids, and flagellum (Brownlie & Allan, 2011). TLR15 has recognized yeast-derived components (Boyd et al., 2012). TLR21 has recognized microbial DNA and is homologous with fish (Keestra et al., 2010). The recognition of viral RNA depends on TLR3 and TLR7, which recognize viral double-stranded RNA and single-stranded RNA (Alexopoulou et al., 2001Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001;413:732-8.; Heil et al., 2004Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, Akira S, et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004;303:1526-9.).

Due to the important roles in resistance to pathogen invasion, TLR genes have been conserved throughout evolution. Mutations in TLRs may have a profound influence on the host’s response to pathogens and are also associated with resistance to and susceptibility to diseases (Chen et al., 2009Chen Z, Ma G, Qian Q, Yao Y, Feng Y, Tang C. Toll-like receptor 8 polymorphism and coronary artery disease. Molecular Biology Reports 2009;36:1897-901.; Hawn et al., 2009Hawn T, Scholes RD, Li SS, Wang H, Yang Y, Roberts PL, et al. Toll-like receptor polymorphisms and susceptibility to urinary tract infections in adult women. PloS One 2009;4:e5990.; Al-Qahtani et al., 2012Al-Qahtani A, Al-Ahdal M, Abdo A, Sanai F, Al-Anazi M, Khalaf N, et al. Toll-like receptor 3 polymorphism and its association with hepatitis B virus infection in Saudi Arabian patients. Journal of Medical Virology 2012;84:1353-9.; Goyal et al., 2012Goyal S, Dubey PK,Tripathy K, Mahajan R, Pan S, Dixit SP, et al. Detection of polymorphism and sequence characterization of Toll-like receptor 7 gene of Indian goat revealing close relationship between ruminant species. Animal Biotechnology 2012;23:194-203.; O’Dwyer et al., 2013). There are many studies researching mutations in human TLRs (Misch & Hawn, 2008Misch EA, Hawn TR. Toll-like receptor polymorphisms and susceptibility to human disease. Clinical Science (London) 2008;114:347-60.; Mukherjee et al., 2019Mukherjee S, Huda S and Sinha Babu SP. Toll-like receptor polymorphism in host immune response to infectious diseases: A review. Scandinavian Journal of Immunology 2019;90:e12771.). Several studies have focused on avian TLR gene mutations and polymorphisms (Alcaide & Edwards, 2011Alcaide M, Edwards SV. Molecular evolution of the toll-like receptor multigene family in birds. Molecular Biology and Evolution 2011;28:1703-15.; Ruan et al., 2012Ruan W, Wu Y, Zheng S J. Different genetic patterns in avian Toll-like receptor (TLR)5 genes. Molecular Biology Reports 2012;39:3419-26.; Ruan et al., 2015; Swiderska et al., 2018Swiderska Z, Smidova A, Buchtova L, Bryjova A, Fabianova A, Munclinger P, et al. Avian Toll-like receptor allelic diversity far exceeds human polymorphism: an insight from domestic chicken breeds. Science Report 2018;8:17878.; Velova et al., 2018Velova H, Gutowska-Ding MW, Burt DW, Vinkler M. Toll-like receptor evolution in birds: gene duplication pseudogenisation and diversifying selection. Molecular Biology and Evolution 2018;35(9):2170-84.). In the present study, we explored different genetic patterns of TLR3 and 7 in the Phasianus colchicus, Numida meleagris, and other 62 avian species. The results were helpful to understand the genetic evolution of avian TLR3 and 7.

MATERIALS AND METHODS

Sources of avian breeds

The Numida meleagris and the Phasianus colchicus used in this study were obtained from Beijing Shahe breeder. We arranged four repeats of individuals. All procedures were approved by the Animal Care and Use Committee of Beijing University of Agriculture (Beijing, China).

Molecular cloning of TLR3 and 7 and sequence accession number

The total RNA was obtained from spleens using TRIzol (Invitrogen, USA). The total RNA, a random primer, dNTPs, and M-MLV reverse transcriptase (Promega, USA) were used for cDNA synthesis. PCR was performed to amplify the target gene using three pairs of specific primers for TLR3 and four pairs of specific primers for TLR7 (Table1). PCR reactions were performed with pfu polymerase (Promega, USA). The 25 µl PCR reaction contained 50 pmol of each forward and reverse primers, 2 µl template cDNA, 200 µM each of deoxynucleotide triphosphate mixture and 2.5 U Pfu DNA polymerase (Promega) in 1× Pfu DNA polymerase buffer. Amplification conditions were as follows: initial denaturation at 94°C for 2 min, 35 cycles at 94°C for 30 s, annealing at 56°C for 30 s, and extension at 72°C for 3 min, followed by a final extension at 72°C for 10 min. PCR amplicons were verified by 1% agarose gel electrophoresis, then ligated into a pEASY-Blunt simple cloning vector (TransGen, Beijing, China). Recombinant plasmids were characterized by PCR using gene specific and vector primer pairs. Recombinant plasmids with avian TLR3 and 7 were sequenced from both ends by Sangon Biotech Co., Ltd. Sequences for TLR3 and 7 for Numida meleagris and the Phasianus colchicus were deposited in the GenBank database under accession number MG604328-MG604332. Other sequences of TLR3 and 7 of 62 avian species were acquired from GenBank, the accession numbers are shown in Table 2.

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Table 1
PCR primers used in this study.

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Table 2
Avian names and GenBank accession numbers.

Analysis of variation sites

Nucleotide sequences for avian TLR3 and TLR7 were aligned in MegAlign by the ClustalW method (DNAstar version 8.1.3). The nucleotide homology was showed in a report of MegAlign. The functional regions were detected with the analysis tools provided at the website (http://smart.embl-heidelberg.de and http://split.pmfst.hr). The relative frequency of non-synonymous (dN) and synonymous (dS) substitutions was calculated and constructed using the MEGA7 software (version 7) (Kumar, et al., 2016Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis. Version 70 for Bigger Datasets. Molecular Biology and Evolution 2016;33:1870-4.). Crystal structures and non-synonymous sites in the avian TLR3 and 7 were visualized by PDB (Protein Data Bank, ID:1ZIW and 5GMF) models and PyMOL software (version 2.3, DeLano Scientific LLC).

RESULTS AND DISCUSSION

The full-length open reading frame (ORF) for avian TLR3 was 3036 nucleotides that encoded 1011 amino acids. The ORF for avian TLR7 was 3180 nucleotides and encoded 1059 amino acids. Partial nucleotide sequences were also analyzed for homology. The nucleotide sequence alignment showed that Phasianus colchicus and Numida meleagris share 93.6%-95% homology with chicken TLR3 and 7. The homology between Numida meleagris and the Phasianus colchicus was 92.8%-94.1% for TLR3 and 7.

The extracellular domain of the TLR, especially the leucine-rich repeat domain (LRR), is a region for recognizing pathogens (Jin and Lee, 2008Jin MS, Lee JO. Structures of the toll-like receptor family and its ligand complexes. Immunity 2008;29:182-91.; Werling, et al., 2009Werling D, Jann OC, Offord V, Glass EJ, Coffey TJ. Variation matters: TLR structure and species-specific pathogen recognition. Trends in Immunology 2009;30:124-30.). Cytoplasmic domains of the TLR, especially the Toll/interleukin-1 receptor domain (TIR), is a region for signal transduction (Verstak, et al., 2009Verstak B, Nagpal K, Bottomley SP, Golenbock DT, Hertzog PJ, Mansell A. MyD88 adapter-like (Mal)/TIRAP interaction with TRAF6 is critical for TLR2- and TLR4-mediated NF-kappaB proinflammatory responses. Journal of Biological Chemistry 2009;284:24192-203.). Three hundred and fifteen non-synonymous mutation sites and 202 synonymous mutation sites were observed in the avian TLR3, including 60 sites for Numida meleagris and 44 sites for the Phasianus colchicus. Sixty-two variable sites were located in the extracellular domain, including 34 sites in LRR regions. Eighteen variable sites were also located in the cytoplasmic domain, including 9 sites in the TIR region. Two hundred and twenty-seven non-synonymous mutation sites and 174 synonymous mutation sites were observed in the avian TLR7, including 58 sites for Numida meleagris and 64 sites for the Phasianus colchicus. Eight-two variable sites were located in the extracellular domain, including 34 sites in the LRR domain, and 8 variable sites were located in the cytoplasmic domain, including 2 sites in the TIR domain. Two sites were located in the trans-membrane domain. Among these sites, 44 amino acid sites were observed in LRR and TIR region of TLR3 and used common variation of amino acids in most avian species (Table 3), including G64R, L163F, and H627Y in α-helix structure, V123M, V224R, N381S, and E383Q in β-sheet structure (Figure 1). Forty-five mutation sites were also observed in LRR and TIR region of TLR7 and used common variation of amino acids in most avian species (Table 4), including T175N, F176L, and E341Q sites in α-helix structure, F51S, R56T, V216I, Q664E, I689V, and I739M in β-sheet structure (Figure 1). These sites located in α-helix or β-sheet may affect structure of TLR and recognition function.

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Table 3
Avian TLR3 differences sites at functional region.
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Table 4
Avian TLR7 differences sites at functional region.

Figure 1
Visualization of amino acids corresponding to nonsynonymous single nucleotide variations in the extracellular domain of avian TLR3 (left) and TLR7 (right) based on the protein structure predicted by CPHmodels 3.0. The predicted ligand binding sites were marked with dotted box.

Three-dimensional structures of avian TLR3 and TLR7 were helpful for further speculating on the role of these variable sites (Choe et al., 2005Choe J, Kelker MS, Wilson IA. Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 2005;309:581-5.). The sites that are located at the external and LRR domains may be more important than others (Botos, et al., 2011Botos I, Segal DM, Davies DR. The structural biology of Toll-like receptors. Structure 2011;19:447-59.). Moreover, it reported that two N-terminal half-sites in both dimer subunits of TLR3 are the viral dsRNA binding sites (Alexopoulou et al., 2001Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001;413:732-8.; Leonard et al., 2008Leonard JN, Ghirlando R, Askins J, Bell JK, Margulies DH, Davies DR and Segal DM. The TLR3 signaling complex forms by cooperative receptor dimerization. Proceedings of National Academy Science USA 2008;105:258-63.; Liu et al., 2008Liu L, Botos I, Wang Y, Leonard JN, Shiloach J, Segal D, et al. Structural basis of toll-like receptor 3 signaling with double-stranded RNA. Science 2008;320:379-81.; Zhang et al., 2017Zhang Z, Ohto U, Shimizu T. Toward a structural understanding of nucleic acid-sensing Toll-like receptors in the innate immune system. FEBS Letters 2017;591:3167-81.). In this study, H59Y, E60K, G64R, E93K, L112S, K117E, N118K, R120H, V123M, L163F, R443Q, R459K, E460D, C485H, and F511L for avian TLR3 were considered in all 51 avian species (Figure 1). The sites located at long loop of TLR7, termed ‘Z-loop’, may also be the viral ssRNA binding sites (Zhang et al., 2016; Zhang et al., 2017; Diebold et al., 2004Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004;303:1529-31.). In this study, I432V, M437V, and T732S for avian TLR7 were considered in all 49 avian species (Figure 1). These sites may bind to ligands and play crucial roles in viral recognition. Fully characterizing the functions of these sites would require a large number of experiments.

There is mounting evidence suggesting that there are species-specific components to TLR (Werling et al., 2009Werling D, Jann OC, Offord V, Glass EJ, Coffey TJ. Variation matters: TLR structure and species-specific pathogen recognition. Trends in Immunology 2009;30:124-30.). Differences in avian TLR3 and TLR7 reflect the differences in geography and microbial environments (Liu et al., 2006Liu YP, Wu GS, Yao YG, Miao YW, Luikart G, Baig M, et al. Multiple maternal origins of chickens: out of the Asian jungles. Molecular Phylogenetics and Evolution 2006;38:12-9.; Alcaide & Edwards, 2011Alcaide M, Edwards SV. Molecular evolution of the toll-like receptor multigene family in birds. Molecular Biology and Evolution 2011;28:1703-15.). These variable TLRs recognize the same or similar pathogens and perform the same functions. Different avian TLR3 and TLR7 sequences could also affect the host’s resistance to viruses. These variable sites in the extracellular LRR domain, especially the viral binding sites that have been reported, play a dramatic role in recognizing viruses. Further functional research regarding these differences may clarify the impacts of these variable sites in avian TLR3 and 7.

The dS/dN represents the proportion between the Ka (Synonymous mutation) and the Ks (non-synonymous mutation). This ratio determines whether there was any selective pressure on the TLR3 and 7 genes. This finding indicates positive selection occurred in avian TLR3 and 7 genes because the frequency of synonymous (dS)/frequency of non-synonymous (dN) (dS/dN of TLR3 is 0.64; dS/dN of TLR7 is 0.77). Mutations will be retained in avian TLR3 and 7. This property was highly conserved through gene evolution and the more important function of recognizing viruses (Liu et al., 2006Liu YP, Wu GS, Yao YG, Miao YW, Luikart G, Baig M, et al. Multiple maternal origins of chickens: out of the Asian jungles. Molecular Phylogenetics and Evolution 2006;38:12-9.; Bergman et al., 2010Bergman IM, Rosengren JK, Edman K, Edfors I. European wild boars and domestic pigs display different polymorphic patterns in the Toll-like receptor (TLR) 1 TLR2 and TLR6 genes. Immunogenetics 2010;62:49-58.; Alcaide & Edwards, 2011Alcaide M, Edwards SV. Molecular evolution of the toll-like receptor multigene family in birds. Molecular Biology and Evolution 2011;28:1703-15.).

Based on the TLR3 and 7 polymorphisms and their correlations with human and mouse susceptibility to viral infections, we propose that avian TLR3 and 7 differences may be associated with either resistance or susceptibility to avian infectious diseases (Schott et al., 2007Schott E, Witt H, Neumann K, Taube S, Oh DY, Schreier E, et al. A Toll-like receptor 7 single nucleotide polymorphism protects from advanced inflammation and fibrosis in male patients with chronic HCV-infection. Journal of Hepatology 2007;47:203-11.; Lee et al., 2013Lee SO, Brown RA and Razonable RR. Association between a functional polymorphism in Toll-like receptor 3 and chronic hepatitis C in liver transplant recipients. Transplante Infectious Diseases 2013;15:111-9.; Piaserico et al., 2015Piaserico S, Michelotto A, Frigo AC, Alaibac M. TLR7 Gln11Leu single nucleotide polymorphism and response to treatment with imiquimod in patients with basal cell carcinoma: a pilot study. Pharmacogenomics 2015;16:1913-7.; He et al., 2017He H, Liu S, Liu PP, Li QB, Tan YX, Guo Y, et al. Association of Toll-like receptor 3 gene polymorphism with the severity of enterovirus 71 infection in Chinese children. Archives Virology 2017;162:1717-23.). This study may be helpful to further understand the varied resistance to viral diseases that exist between different avian species.

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  • 1
    Tables 1 to 4 are presented in the pages that follow the references.

Publication Dates

  • Publication in this collection
    26 Aug 2022
  • Date of issue
    2022

History

  • Received
    07 Sept 2021
  • Accepted
    01 Mar 2022
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