Development and adaptations of innate immunity in the gastrointestinal tract of the newly hatched chick
Introduction
The structure and function of the digestive tract reflect the feeding habits of animals. Thus, the gut of predators is structured differently from that that of herbivores and the digestive tracts of herbivores differ structurally depending on the site of cellulose digestion [1], [2]. Another cause for difference in function between digestive systems relates to factors determining the development of digestive function in the gut. Thus, the rate of gut development, both anatomically and functionally, is different between species that immediately proceed to forage an adult-type diet and those that are fed processed foods or milk by parents [1]. Several bird species, including Gallus, proceed to forage immediately at hatch [3]. This intake of an omnivorous diet requires the rapid adaptation of the digestive tract to accommodate breakdown and absorption of complex food stuffs [1], [4], [5]. Concomitant with the exposure to an adult-type diet, the intestinal tract of these birds immediately becomes inhabited by microflora [6], [7], [8], [9], [10]. Interestingly in Gallus sp., the major site for bacterial colonization is the large intestine, particularly the two cecal horns [2], [7], [9], and colonization occurs by rectal as well as by oral routes [7], [9], [10].
Consequent to the rapid colonization of the gut by commensal bacteria, as well as the possible entry of pathogenic bacteria, a parallel rapid development of GALT is expected. However, in spite of rapid gut development, the functional development of lymphocyte functions in the gut of hatchlings was relatively slower [11]. Thus, lymphocyte colonization of the gut occurred in two waves over a period of 14 days, while positive responses to oral and rectal immunogens were detected no earlier than 5 days post-hatch [11]. As adaptive immunity in the chick GALT appeared to mature towards the second week of life, the issue of immune protection during the first week of life was raised.
Immune protection could be provided during the first week of life by two non-mutually exclusive systems: maternal antibodies—active systemically and in the gut cavity [12], [13], [14], and innate effector mechanisms—active along all mucosal surface linings. Numerous studies have investigated the role of maternal antibodies in prevention of early disease in the chick [15], [16], [17], while the maturation of innate functionality in chick GALT has not been investigated to date. In mammalian mucosal surfaces, which are constantly exposed to the external environment, the innate immune system, including the epithelial lining, is the first line of defense against invasive microorganisms [18], [19], [20], [21], [22]. Innate effector mechanisms function to eliminate potential infection by either blocking the entry of microorganisms, or by preventing their spreading prior to induction of adaptive immunity. We hypothesized that in addition to protection provided by maternal antibodies, innate effector mechanisms are active along the hatchling's gut, and enable immune protection during the period required for the functional maturation of adaptive immunity.
To test the protective potential of the innate enteric immune system during the first week of life, we studied expression of functional genes representing different cells and activities of the innate immune system. These genes included pro-inflammatory cytokines and chemokines produced by innate cells and enterocytes, as well as genes encoding for the antibacterial β-defensins Gallinacin 1 and 2 which are produced by heterophils [23], [24], [25].
We show that the intestinal innate immune system is prepared for bacterial encounters at hatch, and for the first time that the preparedness of these innate measures at hatch is probably independent of and additional to bone marrow-hematopoiesis.
Section snippets
Chickens
Newly hatched, unvaccinated Ross broiler chicks were obtained from a local commercial hatchery (Brown and Sons, Hod Hasharon, Israel). Chicks were placed in floor pens on wood-shavings in isolated, disease-free, light and temperature controlled rooms at 32 °C for the first week post-hatch followed by 28 °C during the second week. Feed, was a commercial starter formulated to meet or exceed NRC requirements (Matmor Feed Co., Ashdod, Israel). Pathogen-free feed and water were supplied ad libitum for
Expression of pro-inflammatory cytokine, chemokines and β-defensins in the newly hatched chick gut
To study the development of innate immune cells in the gut we determined the temporal expression of several genes along the gut of newly hatched chicks. The selected genes represent various activities and functions of both innate cells (macrophages and granulocytes) as well as enterocytes. The products of these genes are involved in pro-inflammatory immune responses (chIL-1β and chIL-8), immune cell recruitment and activation (K203, chIL-8 and chIL-1β) and heterophil bactericidal activity
Discussion
The involvement of the innate immune system in defense of the chick gut during the first week life has not been extensively studied with the exception of context with pathogenicity of enteric bacteria [36], [37]. In the present study, we followed the development of the enteric innate immune system in healthy, uninfected newly hatched broiler chicks throughout the first week of life. Initially we focused on studying the temporal expression of three pro-inflammatory cytokine and chemokine
References (57)
Comparative avian nutrition
(1998)- et al.
Comparative physiology of the vertebrate digestive system
(1995) The anatomy of the avian digestive tract as related to feed utilization
Poult Sci
(1982)Development of the digestive tract of poultry
World's Poult Sci J
(2001)- et al.
The effect of fasting at different ages on growth and tissue dynamics in the small intestine of the young chick
Br J Nutr
(2001) - et al.
Poultry digestive microflora biodiversity as indicated by denaturing gradient gel electrophoresis
Poult Sci
(2003) The avian cecum: update and motility review
J Exp Zool
(1999)- et al.
Development of the normal gastrointestinal microflora of specific pathogen-free chickens
J Hyg
(1984) The intestinal microflora of poultry and game birds during life and after storage
J Appl Bacteriol
(1979)Prospects for treatment to control salmonellas and other foodborne pathogens in poultry
Vet J
(2000)
Establishment of immune competence in the avian GALT during the immediate post-hatch period
Develop Comp Immunol
Transfer of maternal anti-rotavirus IgG to the mucosal surfaces and bile of turkey poults
Avian Dis
Transfer of IgA from albumen into the yolk sac during embryonic development in the chicken
Zentral Vet Reihe A
Distribution of immunoglobulins during embryogenesis in the chicken
Zentral Vet Reihe A
Maternal transmission of immunity to Eimeria maxima: western blot analysis of protective antibodies induced by infection
Infect Immun
The transmission of passive immunity to Escherichia coli from mother to young in the domestic fowl (Gallus domesticus)
Immunol
Effect of diffferent levels of maternally derived antibodies on protection against infectious bursal disease virus
Avian Dis
How the gut links innate and adaptive immunity
Ann NY Acad Sci
Mucosal immunity and inflammation. III. The mucosal antigen barrier: cross talk with mucosal cytokines
Am J Physiol
Mucosal immunity and inflammation. V. Innate mechanisms of mucosal defense and repair: the best offense is a good defense
Am J Physiol
Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases
Immunol Lett
Development of the intestinal mucosal barrier
J Pediat Gastroenterol Nutr
Characterization of beta-defensin prepropeptide mRNA from chicken and turkey bone marrow
Anim Genet
Isolation of antimicrobial peptides from avian heterophils
J Leukoc Biol
Gallinacins: cysteine-rich antimicrobial peptides of chicken leukocytes
FEBS Lett
Impaired immune responses in broiler hatchling hindgut following delayed access to feed
Vety Immunol Immunopathol
Monitoring mRNA expression by polymerase chain reaction: the primer-dropping method
Anal Biochem
Avian heterophils in inflammation and disease resistance
Poult Sci
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2022, Animal NutritionCitation Excerpt :A major problem in the poultry industry is that the development of intestinal immune function is slow in neonatal chickens (Alkie et al., 2019; Weström et al., 2020). This immature intestinal immune function could increase the susceptibility to pathogenic microorganisms in the early growing stage of chickens, which might reduce growth performance and eventually lead to heavy financial losses in intensive production (Bar-Shira and Friedman, 2006; Li et al., 2015). Thus, it is of great significance to explore strategies for improving the innate intestinal immune function of chickens.
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A. Friedman is incumbent of the Ron Barabaro Chair in Veterinary Medicine.