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Ontogeny of gut associated immune competence in the chick

Published online by Cambridge University Press:  18 September 2007

A. Friedman ,
E. Bar-shira  and
D. Sklan
A. Friedman*
Affiliation:
Sections of Immunology
E. Bar-shira
Affiliation:
Sections of Immunology
D. Sklan
Affiliation:
Nutrition, Department of Animal Sciences, Faculty of Agricultural, Nutritional and Environmental Sciences, Hebrew University of Jerusalem, Rehovot, Israel
*
*Corresponding author: e-mail: friedman@agri.huji.ac.il
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Abstract

To accommodate the rapid transition to external nutrients, the chick's gastrointestinal tract undergoes dramatic changes within the first few days of life. These include a rapid increase in mass, villi number and length, enterocyte number, crypt depth and proliferating cells. Concomitant with the development of digestive structures and functions a rapid development of the gut associated lymphoid tissue (GALT) occurs. This lymphoid system works within and in concert with digestive tract parenchyma, however, there is little information describing the normal development and immunological function of the avian GALT in the immediate post-hatch period. The purpose of this review is to summarize current knowledge on the structure and function of the avian GALT during the early post-hatch period. At hatch, the gut is poorly populated by both innate immune leukocytes and lymphocytes. The basal numbers of lymphocytes are the result of early waves migrating from the thymus and bursa of Fabricius. Further waves of lymphocyte migration occur after 4 days of life and continue intermittently with time. In concert with this pattern of lymphocyte population adaptive immunity develops. Hence, the gut of the hatchling is unprotected by adaptive immunity during the first few days of life. Protection during this critical period might be the result of maternal antibody activity or that of the innate immune system. This system appears to be functional at this time, though much work is needed to establish this possibility. Upon maturity of the immune system, most of the immunological activity within the chick GALT is concentrated in the hindgut, and specifically so in the caeca and bursa of Fabricius. Once immune responses have become established the relevant cells disseminate systemically and to other areas of the small intestines. Finally, observations on the beneficial effects of early feeding on development of gut and GALT are discussed with reference to management of hatchlings.

Keywords

gut associated lymphoid tissue (GALT)immune systemmucosal immuneresponsedigestive tractchickontogenypost-hatch
Type
Reviews
Information
World's Poultry Science Journal , Volume 59 , Issue 2 , June 2003 , pp. 209 - 219
Copyright
Copyright © Cambridge University Press 2003

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References

Akiba, Y. and Murakami, H. (1995) Partitioning of energy and protein during early growth of broiler chicks and contribution of vitelline residue. 10th European Symposium on Poultry Nutrition, Anatolia, Turkey.Google Scholar
Arstila, T.P., Toivanen, P. and Lassila, O. (1993) Helper activity of CD4+ alpha beta T cells is required for the avian gamma delta T cell response. Eur: J. Immunol. 23: 2034–2037.Google Scholar
Bar-Shira, E., Sklan, D. and Friedman, A.Establishment of immune competence in the avian GALT during the immediate post-hatch period. Develop. Comp. Immunol. In Press. Available online 10, 2002.Google Scholar
Befus, A.D., Johnston, N., Leslie, G.A. and Bienenstock, J. (1980) Gut associated lymphoid tissue in the chicken. I. morphology, ontogeny, and some functional characteristics of Peyer's patches. J. Immunol. 125: 2626–2632.CrossRefGoogle ScholarPubMed
Berin, M.C., Mckay, D.M. and Perdue, M.H. (1999) Immune-epithelial interactions in host defense. American J. Tropicul Med. Hygiene 60(4 Suppl): 16–25.CrossRefGoogle ScholarPubMed
Berin, M.C., Yang, P.C., Ciok, L., Waserman, S. and Perdue, M.H. (1999) Role for IL-4 in macromolecular transport across human intestinal epithelium. American J. Physio1. 276: C1046–C1052.CrossRefGoogle ScholarPubMed
Bezuidenhout, A.J. and Vanaswegan, G. (1990) A light microscopic and immunocytochemical study of the gastrointestinal tract of the ostrich (Struthio camelus L.). Onderstepoort J. Vet. Res. 57: 37–48.Google ScholarPubMed
Bockman, D.E. and Cooper, M.D. (1973) Pinocytosis by epithelium associated with lymphoid follicles in the bursa of Fabricius, appendix, and Peyer's patches. An electron microscopic study. American J. Anatom. 136: 455–477.CrossRefGoogle ScholarPubMed
Brockus, C.W., Jackwood, M.W. and Harmon, B.G. (1998) Characterization of β-defensin prepropeptide mRNA from chicken and turkey bone marrow. Animal Genet. 29: 283–289.CrossRefGoogle ScholarPubMed
Brummermann, M. and Braun, E.J. (1995) Effect of salt and water balance on colonic motility of White Leghorn roosters. Am. J. Physiol. 268: R690–698.Google ScholarPubMed
Bucy, R.P., Chen, C.L., Cihak, J., Losch, U. and Cooper, M.D. (1988) Avian T cells expressing gamma delta receptors localize in the splenic sinusoids and the intestinal epithelium. J. Immunol. 141: 2200–2205.CrossRefGoogle ScholarPubMed
Burns, R.B. and Maxwell, M.H. (1986) Ultrastructure of Peyer's patches in the domestic fowl and turkey. J. Anat. 147: 235–243.Google ScholarPubMed
Cawthraw, S., Ayling, R., Nuijten, P., Wassenaar, T. and Newell, D.G. (1994) Isotype, specificity, and kinetics of systemic and mucosal antibodies to Campylobacter jejuni antigens, including flagellin, during experimental oral infections of chickens. Avian Dis. 38: 341–349.CrossRefGoogle ScholarPubMed
Clench, M.H. (1999) The Avian Caecum: Update and Motility Review. J. Exp. Zool. 283: 441–447.3.0.CO;2-8>CrossRefGoogle Scholar
Del Cacho, E., Gallego, M., Sanz, A. and Zapata, A. (1993) Characterization of distal lymphoid nodules in the chicken caecum. Anat. Rec. 237: 512–517.CrossRefGoogle ScholarPubMed
Dunon, D., Cooper, M.D. and Imhof, B.A. (1993) Thymic origin of embryonic intestinal gamma/delta T cells. J. Exp. Med. 177: 257–263.CrossRefGoogle ScholarPubMed
Dunon, D., Courtois, D., Vainio, O., Six, A., Chen, C.H., Cooper, M.D., Dangy, J.P. and Imhof, B.A. (1997) Ontogeny of the immune system: gamma/delta and alpha/beta T cells migrate from thymus to the periphery in alternating waves. J. Exp.l Med. 186: 977–988.CrossRefGoogle Scholar
Evans, E.W., Beach, G.G., Wunderlich, J. and Harmon, B.G. (1994) Isolation of antimicrobial peptides from avian heterophils. J. Leukoc. Biol. 56: 661–665.CrossRefGoogle ScholarPubMed
Fagerland, J.A. and Arp, L.H. (1993). Distribution and quantitation of plasma cells, T lymphocyte subsets, and B lymphocytes in bronchus-associated lymphoid tissue of chickens: age-related differences. Reg. Immunol. 5: 28–36.Google Scholar
Friedman, A., Al-Sabbagh, A., Santos, L.M., Fishman-Lobell, J., Polanski, M., Das, M.P., Koury, S.J. and Weiner, H.L. (1994) Oral tolerance: a biologically relevant pathway to generate peripheral tolerance against external and self antigens. Chem. Immunol. 58: 259–290.Google ScholarPubMed
Friedman, A., Arieh, I., Melamed, D. and Nir, I. (1998) Defective immune response and failure to induce oral tolerance following enteral exposure to antigen in broilers afflicted with stunting syndrome. Avian Parhol. 27: 518–525.CrossRefGoogle Scholar
Gallego, M., Cacho, E.D. and Bascuas, J.A. (1995) Antigen-binding cells in the catcall tonsils and Peyer's patches of the chicken after bovine serum albumin administration. Poultry Sci. 74: 472–479.CrossRefGoogle Scholar
Geyra, A., Uni, Z. and Sklan, D. (2001) The effect of fasting at different ages on growth and tissue dynamics in the small intestine of the young chick. Br. J. Nutr. 86: 53–61.CrossRefGoogle ScholarPubMed
Geyra, A., Uni, Z. and Sklan, D. (2001)Enterocyte dynamics and mucosal development in the post hatch chick.Poultry Sci. 80: 776–782.CrossRefGoogle Scholar
Glick, B. and Whatley, S. (1967)The presence of immunoglobulin in the bursa of Fabricius. Poultry Sci. 46: 1587–1589.CrossRefGoogle ScholarPubMed
Gobel, T.W., Kaspers, B. and Stangassinger, M. (2001) NK and T cells constitute two major, functionally distinct intestinal epithelial lymphocyte subsets in the chicken. Int. Immunol. 13: 757–762.CrossRefGoogle Scholar
Henderson, S.C., Bounous, D.I. and Lee, M.D. (1999) Early events in the pathogenesis of avian salmonellosis. Infect. Immun. 67: 3580–3586.CrossRefGoogle ScholarPubMed
Honjo, K., Hagiwara, T., Itoh, K., Hirota, Y. (1993) Immunohistochemical analysis of tissue distribution of B and T cells in germfree and conventional chickens. J. Vet. Med. Sci. 55: 1031–1034.CrossRefGoogle Scholar
Kasahara, Y., Chen, C.H. and Cooper, M.D. (1993) Growth requirements for avian gamma delta T cells include exogenous cytokines, receptor ligation and in vivo priming. Eur. J. Immunol. 23: 2230–2236.CrossRefGoogle ScholarPubMed
Katanbaf, M.N.D. and Siegel, P.B. (1988) Allomorphic relationships from hatching to 56 days in parental lines and FI crosses of chickens selected over 27 generations for high or low body weight. Growth Develop. Ageing 52: 11–22.Google ScholarPubMed
Khan, M.Z. and Hashimoto, Y. (1996) An immunohistochemical analysis of T-cell subsets in the chicken bursa of Fabricius during postnatal stages of development. J. Vet. Med. Sci. 58: 1231–1234.CrossRefGoogle ScholarPubMed
Kitagawa, H., Imagawa, T. and Uehara, M. (1996) The apical catcall diverticulum of the chicken identified as a lymphoid organ. J. Anatomy 189: 667–672.Google Scholar
Klipper, E., Sklan, D. and Friedman, A. (2000) Immune response of chickens to dietary protein antigens. Vet. limmunol. Immunopathol. 74: 209–223.CrossRefGoogle ScholarPubMed
Klipper, E., Sklan, D. and Friedman, A. (2001) Response, tolerance and ignorance following oral exposure to a single protein antigen in gallus domesticus. Vaccine 19: 2890–2897.CrossRefGoogle ScholarPubMed
Lai, H.C. and Duke, G.E. (1978) Colonic motility in domestic turkeys. Am. J. Dig. Dis. 23.: 673–681.CrossRefGoogle ScholarPubMed
Lawrence, E.C., Grayson, J., Koski, I.R., Dooley, N.J., Muchmore, A.V. and Blaese, R.M. (1981) Ontogeny of humord immune function in normal chickens: a comparison of immunoglobulin-aecreting cells in bone marrow, spleen, lungs and intestine. Clin. Exp. Immunol. 43: 450–457.Google Scholar
Lehrer, R.L., Bevins, C.L. and Ganz, T. (1999) Defensins and other antimicrobial peptides.Mucosal Immunology. Ogra, P.L., Mestecky, J., Lammet, M.E. al. London, Academic Press: 89–99.Google Scholar
Lillehoj, H.S. (1993) Avian gut-associated immune system: implication in coccidial vaccine development. Poulrry Sci. 72(7): 1306–1311.CrossRefGoogle Scholar
Lillehoj, H.S. and Chung, K.S. (1992) Postnatal development of T-lymphocyte subpopulations in the intestinal intraepithelium and lamina propria in chickens. Vet. Immunol. Immunopathol. 31: 347–360.CrossRefGoogle ScholarPubMed
Malkinson, M. (1965) The transmission of passive immunity to Escherichia coli from mother to young in the domestic fowl (Gallus domesticus). Imnzunol. 9: 311–317.Google Scholar
Mansikka, A., Veromaa, T., Vainio, O. and Toivanen, P. (1989) B-cell differentiation in the chicken: expression of immunoglobulin genes in the bursal and peripheral lymphocytes. Scand. J. Immunol. 29: 325–331.CrossRefGoogle ScholarPubMed
Masteller, E.L., Pharr, G.T., Funk, P.E. and Thompson, C.B. (1997) Avian B cell development. Int. Rev. Immunol. 15: 185–206.CrossRefGoogle ScholarPubMed
Masteller, E.L. and Thompson, C.B. (1994) B cell development in the chicken. Poultry Sci. 73: 998–1011.CrossRefGoogle ScholarPubMed
Mcghee, J.R., Mestecky, J., Dertzbaugh, M.T., Eldridge, J.H., Hirasawa, M. and Kiyono, H. (1992) The mucosal immune system: from fundamental concepts to vaccine development. Vaccine 10: 75–88.CrossRefGoogle ScholarPubMed
Mestecky, J., Moro, I. and Underdown, B.J. (1999) Mucosal Immunoglobulins. Mucosal Inzmunology. Ogra, P.L., Mestecky, J., Lammet, M.E. al. London, Academic Press: 133–152.Google Scholar
Muir, W.I., Bryden, W.L. and Husband, A.J. (2000) Investigation of the site of precursors for IgA- producing cells in the chicken intestine. Immunol. Cell Biol. 78: 294–296.CrossRefGoogle ScholarPubMed
Naukkarinen, A. and Sorvari, T.E. (1982) Morphological and histochemical characterization of the medullary cells in the bursal follicles of the chicken. Acta. Pathol. Microbiol. Immunol. Scand. [C] 90: 193–199.Google ScholarPubMed
Noy, Y., Geyra, A. and Sklan, D. (2001)The effect of early feeding on growth and small intestinal development in the posthatch poult. Poultry Sci. 80.: 912–919.CrossRefGoogle ScholarPubMed
Noy, Y. and Sklan, D. (1998) Yolk utilisation in the newly hatched poult. Br Poultry Sci. 39: 446–451.CrossRefGoogle ScholarPubMed
Noy, Y. and Sklan, D. (1999) Energy utilization in newly hatched chicks. Poultry Sci. 78: 1750–1756.CrossRefGoogle ScholarPubMed
Noy, Y. and Sklan, D. (1998) Metabolic responses to early nutrition. J. App. Poultry Res. 7: 437–451.CrossRefGoogle Scholar
Popiel, I. and Turnbull, P.C. (1985) Passage of Salmonella enteritidis and Salmonella Thompson through chick ileocecal mucosa. Infect. Immun. 47: 786–792.CrossRefGoogle ScholarPubMed
Sahin, O., Zhang, Q., Meitzler, J.C., Harr, B.S., Morishita, T.Y. and Mohan, R. (2001) Prevalence, antigenic specificity, and bactericidal activity of poultry anti-Campylobacter maternal antibodies.Appl. Environ. Microbiol. 67: 3951–3957.CrossRefGoogle ScholarPubMed
Sanderson, I.R. and Walker, W.A. (1999) Mucosal barrier: an overview. Mucosal Immunology. Ogra, P.L., Mestecky, J., Lammet, M.E. al.London, Academic Press: 5–18.Google Scholar
Scott, T.R., Savage, M.L. and Olah, I. (1993) Plasma cells of the chicken Harderian gland. Poultry Sci. 72: 1273–1219.CrossRefGoogle ScholarPubMed
Sharma, J.M. (1991) Overview of the avian immune system. Vet. Immunol. Immunopathol. 30: 13–17.CrossRefGoogle ScholarPubMed
Short, M.L., Nickel, J., Schmitz, A. and Renkawitz, R. (1996) Lysozyme gene expression and regulation. EXS 75: 243–257.Google ScholarPubMed
Sklan, D. (2001) Development of the digestive tract of poultry. World's Poulty Sci. J. 57: 415–428.CrossRefGoogle Scholar
Sorvari, R., Naukkarinen, A. and Sorvari, T.E. (1977) Anal sucking-like movements in the chicken and chick embryo followed by the transportation of environmental material to the bursa of Fabricius, caeca and catcall tonsils. Poultry Sci. 56: 1426–1429.CrossRefGoogle Scholar
Sorvari, R. and Sorvari, T.E. (1978) Bursa1 fabricii as a peripheral lymphoid organ. Transport of various materials from the anal lips to the bursa1 lymphoid follicles with reference to its immunological importance. Immunol. 32: 499–505.Google Scholar
Sorvari, T., Sorvari, R., Ruotsalainen, P., Toivanen, A. and Toivanen, P. (1975) Uptake of environmental antigens by the bursa of Fabricius. Nature 253: 217–219.CrossRefGoogle ScholarPubMed
Suzuki, K., Oida, T., Hamada, H., Hitotsumatsu, O., Watanabe, M., Hibi, T., Yamamoto, H., Kubota, E., Kaminogawa, S. and Ishikawa, H. (2000) Gut cryptopatches: direct evidence of extrathymic anatomical sites for intestinal T lymphopoiesis. Immunity 13: 691–702.CrossRefGoogle ScholarPubMed
Uni, Z., Noy, Y. and Sklan, D. (1999) Posthatch development of small intestinal function in the poult. Poultry Science 78: 215–222.CrossRefGoogle ScholarPubMed
Uni, Z., Platin, R. and Sklan, D. (1998) Cell proliferation in chicken intestinal epithelium occurs both in the crypt and along the villus. J. Comp. Physiol. 168: 241–247.CrossRefGoogle ScholarPubMed
Uni, Z., Smirnov, A. and Sklan, D. Pre- and posthatch development of goblet cells in the broiler small intestine: effect of delayed access to feed. Poultry Sci. Accepted for publication.Google Scholar
Vervelde, L. and Jeurissen, S.H. (1993) Postnatal development of intra-epithelial leukocytes in the chicken digestive tract: phenotypical characterization in situ. Cell Tis. Res. 274: 295–301.CrossRefGoogle ScholarPubMed
Yamamoto, H., Watanabe, H. and Mikami, T. (1977) Distribution of immunoglobulin and secretory component containing cells in chickens. Am. J. Vet. Res. 38: 1227–1230.Google ScholarPubMed
Zhao, C., Nguyen, T., Liu, L., Sacco, R.E., Brogden, K.A. and Lehrer, R.L. (2001) Gallinacin-3, an inducible epithelial β-defensin in the chicken. Infect. Immun. 69: 2684–2691.CrossRefGoogle ScholarPubMed