Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T09:47:45.953Z Has data issue: false hasContentIssue false
  • English
  • Français

Toll like receptors and cytokines as immunostimulatory adjuvants in poultry vaccines: current status and future trends

Published online by Cambridge University Press:  20 August 2019

S. BHADOURIYA ,
B.K. SHARMA ,
N.K. KAKKER  and
R. CHHABRA
S. BHADOURIYA
Affiliation:
Department of Veterinary Microbiology, LUVAS, Hisar, Haryana, India
B.K. SHARMA
Affiliation:
Department of Veterinary Microbiology, LUVAS, Hisar, Haryana, India
N.K. KAKKER
Affiliation:
Department of Veterinary Microbiology, LUVAS, Hisar, Haryana, India
R. CHHABRA*
Affiliation:
College Central Laboratory, College of Veterinary Sciences, LUVAS, Hisar, Haryana, India-125004
*
Corresponding author: rchhabra59@rediffmail.com, rajesh.chhabra@luvas.edu.in
Get access

Abstract

In the face of reducing reliance on in-feed antibiotics, a greater emphasis has been placed on the development of vaccines. Adjuvants play important role in vaccine refinement. Apart from conventional adjuvants, others, like cytokines and toll-like receptors (TLR), have been evaluated experimentally. For example, Pam3CSK4, Polyinosinic-polycytidylic acid are used as immunostimulatory agents which upregulate the expression of type 1 IFNs against avian influenza. The use of TLR4 (lipopolysaccharide; LPS), TLR7 (Loxoribine) and TLR21 (CpG-ODN) agonists have shown good results when used as adjuvants with the avian influenza vaccine. The LPS (TLR4) was used as an adjuvant and liposome as intranasal antigen delivery system for Newcastle's disease (NDV) antigen, which induced significant increases in secretory IgA in tracheal lavage fluid and serum IgG levels. In a challenge study it provided 80% protection against virulent challenge. When resiquimod (TLR7) was used as an adjuvant with inactivated NDV, this potentiated the protective response to 100% against virulent NDV challenge, while protection was only 80% in the vaccine alone group. When 64CpG-plasmids (TLR21) were co-administered with inactivated AIV H5N2 vaccine in chickens, it led to a higher HI titre at two and four weeks of age, and provided 100% protection against virulent challenge of avian influenza. The TLR 3 agonist (poly I:C) showed good results against NDV and avian reovirus. Other TLR agonists and cytokines used against NDV include LPS, loxoribine, CpG-ODN and ChIFN-α, IFN- γ (with an in ovo vaccine). Immunostimulatory adjuvants like LPS, chicken TLR21, have been tried with Marek's disease vaccine, and TLR 5 agonist was used against Salmonella enteritidis and Eimeria tenella. Although the study of cytokines and TLRs in avian species is still in its infancy when compared to that of mammals, huge strides have been made in recent years. In this article, recent studies involving the assessment of immunostimulatory adjuvants in poultry are reviewed.

Keywords

poultryvaccineadjuvantsTLRcytokines
Type
Review
Information
World's Poultry Science Journal , Volume 75 , Issue 3 , September 2019 , pp. 417 - 428
Copyright
Copyright © World's Poultry Science Association 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

AKIRA, S., TAKEDA, K. and KAISHO, T. (2001) Toll-like receptors: critical proteins linking innate and acquired immunity. Nature Immunology 2: 675-680.Google Scholar
ANNAMALAI, A., RAMAKRISHNAN, S., SACHAN, S., KUMAR, B.A., SHARMA, B.K., KUMAR, V., PALANIVELU, M., VARGHESE, B.P., KUMAR, A., SARAVANAN, B.C. and KRISHNASWAMY, N. (2016) Prophylactic potential of resiquimod against very virulent infectious bursal disease virus (vvIBDV) challenge in the chicken. Veterinary Microbiology 187: 21-30.Google Scholar
BLISS, J., MAYLOR, R., STOKES, K., MURRAY, K.S., KETCHUM, M.A. and WOLF, S.F. (1996) Interleukin-12 as Vaccine Adjuvant. Annals of the New York Academy of Sciences 795: 26-35.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: 3163-3170.Google Scholar
CARDENAS-GARCIA, S., DUNWOODY, R.P., MARCANO, V., DIEL, D.G., WILLIAMS, R.J., GOGAL, R.M. (Jr), BROWN, C.C., MILLER, P.J. and AFONSO, C.L. (2016) Effects of chicken interferon Gamma on Newcastle disease virus vaccine immunogenicity. PloS One 11: 0159153.Google Scholar
CHAUNG, H.C., CHENG, L.T., HUNG, L.H., TSAI, P.C., SKOUNTZOU, I., WANG, B., COMPANS, R.W. and LIEN, Y.Y. (2012) Salmonella flagellin enhances mucosal immunity of avian influenza vaccine in chickens. Veterinary Microbiology 157: 69-77.Google Scholar
CHEN, S., CHENG, A. and WANG, M. (2013) Innate sensing of viruses by pattern recognition receptors in birds. Veterinary Research 44: 82.Google Scholar
COX, F.E.G. (1997) Designer vaccines for parasitic diseases. International Journal for Parasitology 27: 1147-1157.Google Scholar
DALLOUL, R.A., LILLEHOJ, H.S., OKAMURA, M., XIE, H., MIN, W., DING, X. and HECKERT, R.A. (2004) In vivo effects of CpG oligodeoxynucleotide on Eimeria infection in chickens. Avian Diseases 48: 783-790.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: 261-267.Google Scholar
DJERABA, A., MUSSET, E., LOWENTHAL, J.W., BOYLE, D.B., CHAUSSÉ, A.M., PÉLOILLE, M. and QUÉRÉ, P. (2002) Protective effect of avian myelomonocytic growth factor in infection with Marek's disease virus. Journal of Virology 76: 1062-1070.Google Scholar
FU, J., LIANG, J., KANG, H., LIN, J., YU, Q. and YANG, Q. (2013) Effects of different CpG oligodeoxynucleotides with inactivated avian H5N1 influenza virus on mucosal immunity of chickens1. Poultry Science 92: 2866-2875.Google Scholar
GOMIS, S., BABIUK, L., GODSON, D.L., ALLAN, B., THRUSH, T., TOWNSEND, H., WILLSON, P., WATERS, E., HECKER, R. and POTTER, A. (2003) Protection of chickens against Escherichia coli infections by DNA containing CpG motifs. Infection and Immunity 71: 857-863.Google Scholar
GORDON, S. (2002) Pattern recognition receptors: doubling up for the innate immune response. Cell 111: 927-930.Google Scholar
HADDADI, S., KIM, D.S., JASMINE, H., VAN DER MEER, F., CZUB, M. and ABDUL-CAREEM, M.F. (2013) Induction of Toll-like receptor 4 signaling in avian macrophages inhibits infectious laryngotracheitis virus replication in a nitric oxide dependent way. Veterinary Immunology and Immunopathology 155: 270-275.Google Scholar
HARTLEY, C., SALISBURY, A.M. and WIGLEY, P. (2012) CpG oligonucleotides and recombinant interferon-γ in combination improve protection in chickens to Salmonella Enterica serovar Enteritidis challenge as an adjuvant component, but have no effect in reducing Salmonella carriage in infected chickens. Avian Pathology 41: 77-82.Google Scholar
HELLER, E.D., LEVY, A.M., VAIMAN, R. and SCHWARTSBURD, B. (1997) Chicken-embryo fibroblasts produce two types of interferon upon stimulation with Newcastle disease virus. Veterinary Immunology and Immunopathology 57: 289-303.Google Scholar
HUANG, J.L., YIN, Y.X., PAN, Z.M., ZHANG, G., ZHU, A.P., LIU, X.F. and JIAO, X.A. (2010) Intranasal immunisation with chitosan/pCAGGS-flaA nanoparticles inhibits Campylobacter jejuni in a White Leghorn model. BioMed Research International: Article ID 589476, http://dx.doi.org/10.1155/2010/589476.Google Scholar
HUNG, L.H., TSAI, P.C., WANG, C.H., LI, S.L., HUANG, C.C., LIEN, Y.Y. and CHAUNG, H.C. (2011) Immunoadjuvant efficacy of plasmids with multiple copies of a CpG motif coadministrated with avian influenza vaccine in chickens. Vaccine 29: 4668-4675.Google Scholar
ICHINOHE, T., WATANABE, I., ITO, S., FUJII, H., MORIYAMA, M., TAMURA, S.I., TAKAHASHI, H., SAWA, H., CHIBA, J., KURATA, T. and SATA, T. (2005) Synthetic double-stranded RNA poly (I: C) combined with mucosal vaccine protects against influenza virus infection. Journal of Virology 79: 2910-2919.Google Scholar
JANEWAY, C.A. (1989) Approaching the asymptote? Evolution and revolution in immunology. In: Cold Spring Harbor symposia on quantitative biology, Vol. 54: pp. 1-13 (Cold Spring Harbor Laboratory Press).Google Scholar
JIN, M.S. and LEE, J.O. (2008) Structures of the Toll-like receptor family and its ligand complexes. Immunity 29: 182-191.Google Scholar
KARACA, K., SHARMA, J.M., WINSLOW, B.J., JUNKER, D.E., REDDY, S., COCHRAN, M. and MCMILLEN, J. (1998) Recombinant fowlpox viruses coexpressing chicken type I IFN and Newcastle disease virus HN and F genes: influence of IFN on protective efficacy and humoral responses of chickens following in ovo or post-hatch administration of recombinant viruses. Vaccine 16: 1496-1503.Google Scholar
KAWAI, T. and AKIRA, S. (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650.Google Scholar
KEESTRA, A.M., DE ZOETE, M.R., BOUWMAN, L.I. and VAN PUTTEN, J.P.M. (2010) Chicken TLR21 is an innate CpG DNA receptor distinct from mammalian TLR9. Journal of Immunology 185: 460-467.Google Scholar
KOGUT, M.H., MOYES, R. and DELOACH, J.R. (1997) Neutralisation of G-CSF inhibits ILK-induced heterophil influx: granulocyte-colony stimulating factor mediates the Salmonella Enteritidis-immune lymphokine potentiation of the acute avian inflammatory response. Inflammation 21: 9-25.Google Scholar
LEUTZ, A., BEUG, H. and GRAF, T. (1984) Purification and characterisation of cMGF, a novel chicken myelomonocytic growth factor. The EMBO journal 3: 3191-3197.Google Scholar
LIANG, J., FU, J., KANG, H., LIN, J., YU, Q. and YANG, Q. (2013) Comparison of 3 kinds of Toll-like receptor ligands for inactivated avian H5N1 influenza virus intranasal immunisation in chicken. Poultry Science 92: 2651-2660.Google Scholar
LINGHUA, Z., XINGSHAN, T. and FENGZHEN, Z. (2007) Vaccination with Newcastle disease vaccine and CpG oligodeoxynucleotides induces specific immunity and protection against Newcastle disease virus in SPF chicken. Veterinary Immunology and Immunopathology 115: 216-222.Google Scholar
LOWENTHAL, J.W., DIGBY, M.R. and YORK, J.J. (1995) Production of interferon-γ by chicken T cells. Journal of Interferon & Cytokine Research 15: 933-938.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 colonisation of Salmonella Enteritidis in broiler chickens. Veterinary Immunology and Immunopathology 127: 371-375.Google Scholar
MALLICK, A.I., PARVIZI, P., READ, L.R., NAGY, E., BEHBOUDI, S. and SHARIF, S. (2011) Enhancement of immunogenicity of a virosome-based avian influenza vaccine in chickens by incorporating CpG-ODN. Vaccine 29: 1657-1665.Google Scholar
MARCUS, P.I. and SEKELLICK, M.J. (2011) Combined sequential treatment with interferon and dsRNA abrogates virus resistance to interferon action. Journal of Interferon & Cytokine Research 21: 423-429.Google Scholar
MEDZHITOV, R., PRESTON-HURLBURT, P. and JANEWAY, C.A. (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.Google Scholar
MIN, W., LILLEHOJ, H.S., BURNSIDE, J., WEINING, K.C., STAEHELI, P. and ZHU, J.J. (2001) Adjuvant effects of IL-1β, IL-2, IL-8, IL-15, IFN-α, IFN-γ TGF-β4 and lymphotactin on DNA vaccination against Eimeria acervulina. Vaccine 20: 267-274.Google Scholar
NUNBERG, J.H., DOYLE, M.V., YORK, S.M. and YORK, C.J. (1989) Interleukin 2 acts as an adjuvant to increase the potency of inactivated rabies virus vaccine. Proceedings of the National Academy of Sciences 86: 4240-4243.Google Scholar
ODEAN, M.J., FRANE, C.M., VAN DERVIEREN, M., TOMAI, M.A. and JOHNSON, A.G. (1990) Involvement of gamma interferon in antibody enhancement by adjuvants. Infection and Immunity 58: 427-432.Google Scholar
OKAMURA, M., MATSUMOTO, W., SEIKE, F., TANAKA, Y., TERATANI, C., TOZUKA, M., KASHIMOTO, T., TAKEHARA, K., NAKAMURA, M. and YOSHIKAWA, Y. (2012) Efficacy of soluble recombinant FliC protein from Salmonella Enterica serovar Enteritidis as a potential vaccine candidate against homologous challenge in chickens. Avian Diseases 56: 354-358.Google Scholar
PALSSON-MCDERMOTT, E.M. and O'NEILL, L.A.J. (2004) Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4 . Immunology 113: 153-162.Google Scholar
PARDOLL, D.M. (1995) Paracrine cytokine adjuvants in cancer immunotherapy. Annual Review of Immunology 13: 399-415.Google Scholar
PARVIZI, P., ABDUL-CAREEM, M.F., MALLICK, A.I., HAQ, K., HAGHIGHI, H.R., OROUJI, S., HEIDARI, M., BEHBOUDI, S. and SHARIF, S. (2014) The effects of administration of ligands for Toll-like receptor 4 and 21 against Marek's disease in chickens. Vaccine 32: 1932-1938.Google Scholar
PARVIZI, P., MALLICK, A.I., HAQ, K., HAGHIGHI, H.R., OROUJI, S., THANTHRIGE-DON, N., ST. PAUL, M., BRISBIN, J.T., READ, L.R., BEHBOUDI, S. and SHARIF, S. (2012) A toll-like receptor 3 ligand enhances protective effects of vaccination against Marek's disease virus and hinders tumor development in chickens. Viral Immunology 25: 394-401.Google Scholar
RAUTENSCHLEIN, S., SUBRAMANIAN, A. and SHARMA, J.M. (1999) Bioactivities of a tumour necrosis-like factor released by chicken macrophages. Developmental & Comparative Immunology 23: 629-640.Google 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 the National Academy of Sciences, U.S.A, 95: pp.588-593.Google Scholar
ROUSE, B.T., MILLER, L.S., TURTINEN, L. and MOORE, R.N. (1985) Augmentation of immunity to herpes simplex virus by in vivo administration of interleukin 2. The Journal of Immunology 134: 926-930.Google Scholar
SACHAN, S., RAMAKRISHNAN, S., ANNAMALAI, A., SHARMA, B.K., MALIK, H., SARAVANAN, B.C., JAIN, L., SAXENA, M., KUMAR, A. and KRISHNASWAMY, N. (2015) Adjuvant potential of resiquimod with inactivated Newcastle disease vaccine and its mechanism of action in chicken. Vaccine 33: 4526-4532.Google Scholar
SCHIJNS, V.E., WEINING, K.C., NUIJTEN, P., RIJKE, E.O. and STAEHELI, P. (2000) Immunoadjuvant activities of E. coli-and plasmid-expressed recombinant chicken IFN-α/β, IFN-γ and IL-1β in 1-day-and 3-week-old chickens. Vaccine 18: 2147-2154.Google Scholar
SHAHROKHI, V., RAD, M. and KALIDARI, G.A. (2013) Treatment of newly hatched chicken with CpG oligodeoxynucleotides decreases liver/spleen colonisation of Salmonella Enteritidis in broiler chickens. Comparative Clinical Pathology 22: 935-939.Google Scholar
SINGH, M., UGOZZOLI, M., BRIONES, M., KAZZAZ, J., SOENAWAN, E. and O'HAGAN, D.T. (2003) The effect of CTAB concentration in cationic PLG microparticles on DNA adsorption and in vivo performance. Pharmaceutical Research 20: 247-251.Google Scholar
SMITH, H.W. (1956) The use of live vaccines in experimental Salmonella Gallinarum infection in chickens with observations on their interference effect. Epidemiology & Infection 54: 419-432.Google Scholar
ST. PAUL, M., BRISBIN, J.T., BARJESTEH, N., VILLANEUEVA, A.I., PARVIZI, P., READ, L.R., NAGY, E. and SHARIF, S. (2014) Avian influenza virus vaccines containing Toll-like receptors 2 and 5 ligand adjuvants promote protective immune responses in chickens. Viral Immunology 27: 160-166.Google Scholar
ST. PAUL, M.S., MALLICK, A.I., READ, L.R., VILLANUEVA, A.I., PARVIZI, P., ABDUL-CAREEM, M.F., NAGY, É. and SHARIF, S. (2012) Prophylactic treatment with Toll-like receptor ligands enhances host immunity to avian influenza virus in chickens. Vaccine 30: 4524-4531.Google Scholar
STEWART, C.R., BAGNAUD-BAULE, A., KARPALA, A.J., LOWTHER, S., MOHR, P.G., WISE, T.G., LOWENTHAL, J.W. and BEAN, A.G. (2012) Toll-like receptor 7 ligands inhibit influenza A infection in chickens. Journal of Interferon & Cytokine Research 32: 46-51.Google Scholar
SUN, A., CHU, C.T., LIU, B.Y., WANG, J.T., LEU, J.S. and CHIANG, C.P. (2000) Expression of interleukin-2 receptor by activated peripheral blood lymphocytes upregulated by the plasma level of interleukin-2 in patients with recurrent aphthous ulcers. Proceedings of the National Science Council, Republic of China. Part B, Life sciences, 24: 116-122.Google Scholar
SUNDICK, R.S. and GILL-DIXON, C. (1997) A cloned chicken lymphokine homologous to both mammalian IL-2 and IL-15. The Journal of Immunology 159: 720-725.Google Scholar
SWAGGERTY, C.L., HE, H., GENOVESE, K.J., DUKE, S.E. and KOGUT, M.H. (2012) Loxoribine pretreatment reduces Salmonella Enteritidis organ invasion in 1-day-old chickens. Poultry Science 91: 1038-1042.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: 398-406.Google Scholar
TAKEUCHI, O. and AKIRA, S. (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.Google Scholar
TEMPERLEY, N., BERLIN, S., PATON, I., GRIFFIN, D. and BURT, D. (2008) Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. BMC genomics 9: 62.Google Scholar
TSENG, L.P., CHIOU, C.J., CHEN, C.C., DENG, M.C., CHUNG, T.W., HUANG, Y.Y. and LIU, D.Z. (2009) Effect of lipopolysaccharide on intranasal administration of liposomal Newcastle disease virus vaccine to SPF chickens. Veterinary Immunology and Immunopathology 131: 285-289.Google Scholar
WANG, X., JIANG, P., DEEN, S., WU, J., LIU, X. and XU, J. (2003) Efficacy of DNA vaccines against infectious bursal disease virus in chickens enhanced by coadministration with CpG oligodeoxynucleotide. Avian Diseases 47: 1305-1312.Google Scholar
WANG, Y., SHAN, C., MING, S., LIU, Y., DU, Y. and JIANG, G. (2009) Immunoadjuvant effects of bacterial genomic DNA and CpG oligodeoxynucleotides on avian influenza virus subtype H5N1 inactivated oil emulsion vaccine in chicken. Research in Veterinary Science 86: 399-405.Google Scholar
WERLING, D. and JUNGI, T. W. (2003) Toll-like receptors linking innate and adaptive immune response. Veterinary Immunology and Immunopathology 91: 1-12.Google Scholar
WIDDERS, P.R., THOMAS, L.M., LONG, K.A., TOKHI, M.A., PANACCIO, M. and APOS, E. (1998) The specificity of antibody in chickens immunised to reduce intestinal colonisation with Campylobacter jejuni. Veterinary Microbiology 64: 39-50.Google Scholar
XIAOWEN, Z., QINGHUA, Y., XIAOFEI, Z. and QIAN, Y. (2009) Co-administration of inactivated avian influenza virus with CpG or rIL-2 strongly enhances the local immune response after intranasal immunisation in chicken. Vaccine 27: 5628-5632.Google Scholar
YIN, G., QIN, M., LIU, X., SUO, J., TANG, X., TAO, G., HAN, Q., SUO, X. and WU, W. (2013) An Eimeria vaccine candidate based on Eimeria tenella immune mapped protein 1 and the TLR-5 agonist Salmonella typhimurium FliC flagellin. Biochemical and Biophysical Research Communications 440: 437-442.Google Scholar
YORK, J.J., STROM, A.D., CONNICK, T.E., MCWATERS, P.G., BOYLE, D.B. and LOWENTHAL, J.W. (1996) In vivo effects of chicken myelomonocytic growth factor: delivery via a viral vector. The Journal of Immunology 156: 2991-2997.Google Scholar
ZHANG, L., ZHANG, M., LI, J., CAO, T., TIAN, X. and ZHOU, F. (2008) Enhancement of mucosal immune responses by intranasal co-delivery of Newcastle disease vaccine plus CpG oligonucleotide in SPF chickens in vivo. Research in Veterinary Science 85: 495-502.Google Scholar