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Chicken toll-like receptors and their role in immunity

Published online by Cambridge University Press:  17 December 2010

T.R. KANNAKI*
Affiliation:
Project Directorate on Poultry, Rajendranagar, Hyderabad (A.P.)-500030, India
M.R. REDDY
Affiliation:
Project Directorate on Poultry, Rajendranagar, Hyderabad (A.P.)-500030, India
M. SHANMUGAM
Affiliation:
Project Directorate on Poultry, Rajendranagar, Hyderabad (A.P.)-500030, India
P.C. VERMA
Affiliation:
Indian Veterinary Research Institute, Izatnagar (U.P.)-243122, India
R.P. SHARMA
Affiliation:
Project Directorate on Poultry, Rajendranagar, Hyderabad (A.P.)-500030, India
*
Corresponding author: [email protected]
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Abstract

Toll-like receptors (TLRs) are a group of highly conserved molecules that initiate innate immune responses to pathogens by recognizing structural motifs. In response to pathogen associated molecular patterns (PAMPs), TLRs induce the production of reactive oxygen and nitrogen intermediates (ROI and RNI), inflammatory cytokines and up regulate the expression of co-stimulatory molecules, subsequently initiating adaptive immunity. Ten chicken TLR genes have been identified and their association with various diseases has been ascertained. This review concerns chicken toll-like receptors, their structure, expression, signalling, and their role in innate and adaptive immunity and disease resistance. It is concluded that TLR genes could be used as molecular markers for genetic selection for the improvement of disease resistance and TLR agonists as potential adjuvants in future vaccines.

Type
Review Article
Copyright
Copyright © World's Poultry Science Association 2010

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References

ABASHT, B., KAISER, M.G. and LAMONT, S.J. (2008) Toll like receptor gene expression in cecum and spleen of advanced intercross line chicks infected with Salmonella enteric serovar Enteritidis. Veterinary immunology and immunopathology 123: 314-323.Google Scholar
ABASHT, B., KAISER, M.G., VAN DER POEL, J. and LAMONT, S.J. (2009) Genetic lines differ in Toll-like receptor gene-expression in spleens of chicks inoculated with Salmonella enteric serovar Enteritidis. Poultry Science 88: 744-749.CrossRefGoogle Scholar
ABDUL-CAREEM, M.F., HAQ, K., SHANMUGANATHAN, S., READ, L.R., SCHAT, K.A., HEIDARI, M. and SHARIF S., (2009) Induction of innate host responses in the lungs of chickens following infection with a very virulent strain of Marek's disease virus. Virology 393(2): 250-257.CrossRefGoogle ScholarPubMed
AKIRA, S. (2001) Toll-like receptors and innate immunity. Advances in immunology 781: 1-56.Google Scholar
AKIRA, S. (2004) Toll receptor families: structure and function. Seminars in Immunology 16: 1-2.Google Scholar
ALEXOPOULOU, L., HOLT, A.C., MEDZHITOV, R. and FLAVELL, R.A. (2001) Recognition of double –stranded RNA and activation of NF-KB by Toll-like receptor 3. Nature 413: 732-738.Google Scholar
BALS, R. and WILSON, J.M. (2003) Cathelicidins-a family of multifunctional antimicrobial peptides. Cellular and Molecular Life Science 60(4): 711–720.Google Scholar
BANCHEREAU, J. and STEINMAN, R.M. (1998) Dendritic cells and the control of immunity. Nature 392(6673): 245-252.Google Scholar
BIRCHLER, T., SEIBL, R., BUCHNER, K., LOELIGER, S., SEGER, R. and HOSSLE, J.P. (2001) Human Toll-like receptor 2 mediates induction of the antimicrobial peptide human beta defensin 2 in response to bacterial lipoprotein. European Journal of Immunology 31(11): 3131–3137.Google Scholar
BOYD, Y., GOODCHILD, M., MORROLL, S. and BUMSTEAD, N. (2001) Mapping of the chicken and mouse genes for toll-like receptor 2 (TLR2) to an evolutionarily conserved chromosomal segment. Immunogenetics 52: 294-298.Google Scholar
BROWNLIE, R., ZHU, J., ALLAN, B., MUTWIRI, G.K., BABIUK, L.A., POTTER, A. and GRIEBEL, P. (2009) Chicken TLR21 acts as a functional homologue to mammalian TLR9 in the recognition of CpG oligodeoxynucleotides. Molecular Immunology 46(15): 3163-3170.Google Scholar
CORMICAN, P., MEADE, K.G., CAHALANE, S., NARCIANDI, F., CHAPWANYA, A. and LLOYD, A.T. (2008) Evolution, expression and effectiveness in a cluster of novel bovine betadefensins . Immunogenetics 60(3–4): 147–156.Google Scholar
CORMICAN, P., LLOYD, A.T., DOWNING, T., CONNELL, S.J., BRADLEY, D. and O'FARRELLY, C. (2009) The avian Toll-Like receptor pathway—Subtle differences amidst general conformity. Developmental and Comparative Immunology 33: 967–973.Google Scholar
DAR, A., POTTER, A., TIKOO, S., GERDTS, V., LAI, K., BABIUK, L.A. and MUTWIRI, G. (2009) CpG oligodeoxynucleotides activate innate immune response that suppresses infectious bronchitis virus replication in chicken embryos. Avian Diseases 53(2): 261-267.Google Scholar
DHEDA, K., HUGGET, J.F., CHANG, J.S., KIM, L.U., BUSTIN, S.A., JONHNSON, M.A., ROOK, G.A.W. and ZUMLA, A. (2005) The implication of using an inappropriate reference gene for real-time reverse transcription PCR data normalization. Analytical Biochemistry 344: 141–143.Google Scholar
DIL, N. and QURESHI, M.A. (2002) Differential expression of inducible nitric oxide synthase is associated with differential Toll-like receptor-4 expression in chicken macrophages from different genetic backgrounds. Veterinary Immunology and Immunopathology 84(3-4): 191-207.Google Scholar
FUKUI, A., INOUSE, N., MATSUMOTO, M., NOMURA, M., YAMADA, K., MATSUDA, Y., TOYOSHIMA, K. and SEYA, T. (2001) Molecular cloning and functional characterization of chicken Toll-like receptors. A single chicken Toll covers multiple molecular patterns. The Journal of Biological Chemistry 276: 47143-47149.Google Scholar
HAJJAR, A.M., EARNST, R.K., TSAI, J.H., WILSON, C.B. AND MILLER and S.I., (2002) Human Toll-like receptor 4 recognizes host-specific LPS modifications. Nature Immunology 3: 354-359.Google Scholar
HE, H., MACKINNON, K.M., GENOVESE, K.J. and KOGUT, M.H. (2010) CpG oligodeoxynucleotide and double-stranded RNA synergize to enhance nitric oxide production and mRNA expression of inducible nitric oxide synthase, pro-inflammatory cytokines, and chemokines in chicken monocytes. Innate Immunity: doi:10.1177/1753425909356937.Google Scholar
HIGGS, R., CORMICAN, P., CAHALANE, S., ALLAN, B., LLOYD, A.T. and MEADE, K. (2006) Induction of a novel chicken Toll-like receptor following Salmonella enterica serovar Typhimurium infection. Infection and Immunity 74(3): 1692–1698.Google Scholar
IQBAL, M., PHILBIN, V.J. and SMITH, A.L. (2005a) Expression patterns of chicken Toll-like receptor mRNA in tissues, immune cell subsets and cell lines. Veterinary Immunology and Immunopathology 104(1-2): 117-127.Google Scholar
IQBAL, M., PHILBIN, V.J., WITHANAGE, G.S.K., WIGLEY, P., BEAL, R.K., GOODCHILD, M.J., BARROW, P., MCCONNELL, I., MASKELL, D.J., YOUNG, J., BUMSTEAD, N., BOYD, Y. and SMITH, A.L. (2005b) Identification and functional characterization of chicken Toll-like receptor 5 reveals a fundamental role in biology of infection with Salmonella enteric serovar Typhimurium. Infection and Immunity 73: 2344-2350.Google Scholar
JURK, M., HEIL, F., VOLLMER, J., SCHETTER, C., KREIG, A.M., WANGER, H., LIPFORD, G. AND BAUER and S., (2002) Human TLR7 or TLR8 independently confer responsiveness to antiviral compound R-848. Nature Immunology 3: 499Google Scholar
KARPALA, A.J., LOWENTHAL, J.W. and BEAN, A.G. (2008) Activation of the TLR3 pathway regulates IFN β production in chickens. Development and Comparative Immunology 32(4): 435-444.Google Scholar
KEESTRA, A.M. and VAN PUTTEN, J.P. (2008) Unique properties of the chicken TLR4/MD-2 complex: selective lipopolysaccharide activation of the MyD88-dependent pathway. Journal of Immunology 181(6): 4354-4362.Google Scholar
KEESTRA, A.M., DE ZOETE, M.R., VAN AUBEL, R. and VAN PUTTEN, J. (2007) The central leucine-rich repeat region of chicken TLR16 dictates unique ligand specificity and species specific interaction with TLR2. Journal of Immunology 178(11): 7110–7119.Google Scholar
KOGUT, M.H., IQBAL, M., HE, H., PHILBIN, V., KAISER, P. and SMITH, A. (2005) Expression and function of Toll-like receptors in chicken heterophils. Development and comparative Immunology 29: 791-807.Google Scholar
LEMAITRE, B., NICOLAS, E., MICHAUT, L., REICHHART, J.M. and HOFFMANN, J.A. (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungalresponse in Drosophila adults. Cell 86: 973–983.Google Scholar
LEVEQUE, G., FORGETTA, V., MORROLL, S., SMITH, A.L., BUMSTEAD, N. and BARROW, P. (2003) Allelic variation in TLR4 is linked to susceptibility to Salmonella enteric serovar Typhimurium infection in chickens. Infection and immunity 71: 1116–11124.Google Scholar
LOOTS, K., REVETS, H. and GODDEERIS, B.M. (2008) Attachment of the outer membrane lipoprotein (OprI) of Pseudomonas aeruginosa to the mucosal surfaces of the respiratory and digestive tract of chickens. Vaccine 26: 546–551.Google Scholar
LU, Y., SARSON, A.J., GONG, J., ZHOU, H., ZHU, W., KANG, Z., YU, H., SHARIF, S. and HAN, Y. (2009) Expression profiles of genes in Toll-like receptor-mediated signalling of broilers infected with Clostridium perfringens. Clinical Vaccine Immunology 16(11): 1639-1647.Google Scholar
LYNN, D.J., LLOYD, A.T. and O'FARRELLY, C. (2003) In silico identification of components of the Toll-like receptor (TLR) signalling pathway in clustered chicken expressed sequence tags (ESTs). Veterinary Immunology and Immunopathology 93(3-4): 177-184.Google Scholar
LYNN, D.J., HIGGS, R., GAINES, S., TIERNEY, J., JAMES, T. and LLOYD, A.T. (2004) Bioinformatic discovery and initial characterisation of nine novel antimicrobial peptide genes in the chicken. Immunogenetics 56(3): 170–177.Google Scholar
MACDONALD, M.R., XIA, J., SMITH, A.L. and MAGOR, K.E. (2008) The duck toll like receptor 7: genomic organization, expression and function. Molecular Immunology 45(7): 2055-2061.Google Scholar
MACKINNON, K.M., HE, H., SWAGGERTY, C.L., MCREYNOLDS, J.L., GENOVESE, K.J., DUKE, S.E., NERREN, J.R. and KOGUT, M.H. (2009) In ovo treatment with CpG oligodeoxynucleotides decreases colonization of Salmonella enteritidis in broiler chickens. Veterinary Immunology and Immunopathology 127(3-4): 371-375.Google Scholar
MALEK, M., HASENTEIN, J.R. and LAMONT, S.J. (2004) Analysis of chicken TLR4, CD28, MIF, MD-2 and LITAF genes in a Salmonella enteritidis resource population. Poultry Science 83: 544-549.Google Scholar
MCGUIRE, K., JONES, M., WERLING, D., WILLIAMS, J.L., GASS, E.I. and JANN, O. (2006) Radiation hybrid mapping of all 10 characterized bovine Toll-like receptors. Animal Genetics 37: 47-50.Google Scholar
MEADE, K.G., NARCIANDI, F., CAHALANE, S., REIMAN, C., ALLAN, B. and O'FARRELLY, C. (2009) Comparative in vivo infection models yield insights on early host immune response to Campylobacter in chickens. Immunogenetics 61(2): 101-110.Google Scholar
MEDZHITOV, R. and JANEWAY Jr. C.A., (1997) Innate immunity: the virtues of non-clonal system of recognition. Cell 91: 295-298.Google Scholar
MEDZHITOV, R. and JANEWAY JR. C.A., (2000) How does the immune system distinguish self from nonself. Seminars in Immunology 12: 185-188.Google Scholar
MENZIES, M. and INGHAM, A. (2006) Identification and expression of Toll-like receptors 1-10 in selected bovine and ovine tissues. Veterinary Immunology and Immunopathology 109: 23-30.CrossRefGoogle ScholarPubMed
PHILBIN, V.J., IQBAL, M., BOYD, Y., GOODCHILD, M.J., BEAL, R.K., BUMSTEAD, N., YOUNG, J. and SMITH, A.L. (2005) Identification and characterization of a functional, alternatively spliced Toll-like receptor 7 (TLR7) and genomic disruption of TLR 8 in chickens. Immunology 114: 507-521.Google Scholar
POLTORAK, A., HE, X., SMIRNOVA, I., LIU, M.Y., HUFFEL, C.V., DU, X., BIRDWELL, D., ALEJOS, E., SILVA, M., GALANOS, C., FREUDENBERG, M., RICCIARDI-CASTAGNOLI, P., LAYTON, B. and BEUTLER, B. (1998) Defective LPS signalling in C3H/HeJ and C57BL/10ScCr mice; mutations in TLR4 gene. Science 282: 2085-2088.Google Scholar
RESCIGNO, M., GRANUCCI, F. and RICCIARDI-CASTAGNOLI, P. (2000) Molecular events of bacterial-induced maturation of dendritic cells. Journal of Clinical Immunology 20(3): 161-166.Google Scholar
RESCIGNO, M., GRANUCCI, F., CITTERIO, S., FOTI, M. and RICCIARDI-CASTAGNOLI, P. (1999) Coordinated events during bacteria-induced DC maturation. Immunology Today 20(5): 200-203.Google Scholar
ROACH, J.C., GLUSMAN, G., ROWEN, L., KAUR, A., PURCELL, M.K. and SMITH, K.D. (2005) The evolution of vertebrate Toll-like receptors. Proceedings of National Academy of Science USA 102(27): 9577–9582.CrossRefGoogle Scholar
ROCK, F.L., HARDIMAN, G., TIMANS, J.C., KASTELEIN, R.A. and BAZAN, J.F. (1998) A family of human receptors structurally related to Drosophila Toll. Proceedings of National Academy of Science USA 95: 588-593.Google Scholar
SALLUSTO, F., PALERMO, B., LENIG, D., MIETTINEN, M., MATIKAINEN, S., JULKUNEN, I., FORSTER, R., BURGSTAHLER, R., LIPP, M. and LANZAVECCHIA, A. (1999) Distinct patterns and kinetics of chemokine production regulate dendritic cell function. European Journal of Immunology 29(5): 1617-1625.Google Scholar
SCHMITTGEN, T.D. and ZAKRAJSEK, B.A. (2000) Effects of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. Journal of Biochemical and Biophysical Methods 46: 69-81.Google Scholar
SHAUGHNESSY, R.G., MEADE, K.G., CAHALANE, S., ALLAN, B., REIMAN, C., CALLANAN, J.J. and O'FARRELLY. C., (2009) Innate immune gene expression differentiates the early avian intestinal response between Salmonella and Campylobacter. Veterinary Immunology and Immunopathology 132(2-4): 191-198.Google Scholar
SHINKAI, H., MUNETA, Y., SUZUKI, K., EGUCHIOGAWA, T., AWATA, T. and UENISHI, H. (2006) Porcine Toll-like receptor 1, 6 and 10 genes: complete sequencing of genomic region and expression analysis. Molecular Immunology 43:1474-1480.Google Scholar
SMITH, J., SPEED, D., LAW, A.S., GLASS, E.J. and BURT, D.W. (2004) In-silico identification of chicken immune related genes. Immunogenetics 56(2): 122-133.Google Scholar
STEIN, D., ROTH, S., VOGELSANG, E. and NUSSLEIN-VOLHARD, C. (1991) The polarity of the dorso ventral axis in the Drosophila embryo is defined by an extracellular signal. Cell 65: 725-735.Google Scholar
SWERDLOW, M.P., KENNEDY, D.P., KENNEDY, J.S., WASHABAU, R.J., HENTHORN, P.S., MOORE, P.F., CARDING, S.R. and FELSBURG, P.J. (2006) Expression and function of TLR2, TLR4 AND Nod 2 in primary canine colonic epithelial cells. Veterinary Immunology and Immunopathology 114: 313-319.Google Scholar
TAGHAVI, A., ALLAN, B., MUTWIRI, G., VAN KESSEL, A., WILLSON, P., BABIUK, L., POTTER, A. and GOMIS, S. (2008) Protection of neonatal broiler chicks against Salmonella Typhimurium septicemia by DNA containing CpG motifs. Avian Diseases 52(3): 398-406.Google Scholar
TAKEDA, K. and AKIRA, S. (2004) TLR signalling pathways. Seminars in Immunology 16(1): 3–9.Google Scholar
TAKEDA, K. and AKIRA, S. (2005) Toll-like receptors in innate immunity. International Immunology 17: 1–14.Google Scholar
TEMPERLEY, N.D., BERLIN, S., PATON, I.R., GRIFFIN, D.K. and BURT, D.W. (2008) Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics 9: 62.Google Scholar
THELLIN, O., ZORZI, W., LAKAYE, B., DE BORMAN, B., COUMANS, B., HENNEN, G., GRISAR, T., IGOUT, A. and HEINEN, E. (1999) Housekeeping genes as internal standards: use and limits. Journal of Biotechnology 75: 291– 295.Google Scholar
WATTERS, T.M., KENNY, E.F. and and O'NEILL, L.A. (2007) Structure, function and regulation of the Toll/IL-1 receptor adaptor proteins. Immunology and Cell Biology 85(6): 411–419.Google Scholar
WU, M., MAIER, E., BENZ, R. and HANCOCK, R.E. (1999) Mechanism of interaction of different classes of cationic antimicrobial peptides with planar bilayers and with the cytoplasmic membrane of Escherichia coli. Biochemistry 38(22): 7235–7242.Google Scholar
XING, Z., CARDONA, C.J., LI, J., DAO, N., TRAN, T. and ANDRADA, J. (2008) Modulation of the immune responses in chickens by low-pathogenicity avian influenza virus H9N2. Journal of General Virology 89: 1288-1299.Google Scholar
YANG, D., CHERTOV, O., BYKOVSKAIA, S.N., CHEN, Q., BUFFO, M.J. and SHOGAN, J. (1999) Beta defensins: linking innate and adaptive immunity through dendritic and T cell. Science 286(5439): 525–528.Google Scholar
YILMAZ, A., SHEN, S., ADELSON, D.L., XAVIER, S. and ZHU, J.J. (2005) Identification and sequence analysis of chicken Toll-like receptors. Immunogenetics 56: 743–753.Google Scholar
ZAREMBER, K.A. and GODOWSKI, P.J. (2002) Tissue expression of human TOLL-like receptors and differential regulation of TOLL-like receptor mRNA in leukocytes in response to microbes, their products and cytokines. Journal of Immunology 168: 554-561.Google Scholar
ZEKARIAS, B., TER HUURNE, A.A., LANDMAN, W.J., REBEL, J.M., POL, J.M. and GRUYS, E. (2002) Immunological basis of differences in disease resistance in the chicken. Veterinary Research 33(2):109-125.CrossRefGoogle ScholarPubMed