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Dynamics of Structural Barriers and Innate Immune Components During Review Article Journal of Innate J Innate Immun 2019;11:111–124 Received: June 25, 2018 DOI: 10.1159/000493719 Accepted after revision: September 9, 2018 Immunity Published online: November 2, 2018 Dynamics of Structural Barriers and Innate Immune Components during Incubation of the Avian Egg: Critical Interplay between Autonomous Embryonic Development and Maternal Anticipation a–d d d d Maxwell T. Hincke Mylène Da Silva Nicolas Guyot Joël Gautron e f d Marc D. McKee Rodrigo Guabiraba-Brito Sophie Réhault-Godbert a b Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, ON, Canada; Department of c Innovation in Medical Education, University of Ottawa, Ottawa, ON, Canada; LE STUDIUM Research Consortium, d Loire Valley Institute for Advanced Studies, Orléans-Tours, Nouzilly, France; BOA, INRA, Val de Loire Centre, e Université de Tours, Nouzilly, France; Department of Anatomy and Cell Biology and Faculty of Dentistry, McGill f University, Montreal, QC, Canada; ISP, INRA, Université de Tours, Nouzilly, France Keywords gressive transformation of egg innate immunity by embryo- Chorioallantoic membrane · Chick embryo · Innate generated structures and mechanisms over the 21-day immunity · Antimicrobial peptides · Avian β-defensins · course of egg incubation, and also discusses the critical in- Toll-like receptors · Eggshell terplay between autonomous development and maternal anticipation. © 2018 The Author(s) Published by S. Karger AG, Basel Abstract The integrated innate immune features of the calcareous egg and its contents are a critical underpinning of the re- Introduction markable evolutionary success of the Aves clade. Beginning at the time of laying, the initial protective structures of the Avian eggs are continuously exposed to microbes. egg, i.e., the biomineralized eggshell, egg-white antimicro- They are challenged with high numbers of potentially bial peptides, and vitelline membrane, are rapidly and dra- pathogenic agents from the laying hen during oviposi- matically altered during embryonic development. The em- tion, through the air and litter, and during natural incu- bryo-generated extra-embryonic tissues (chorioallantoic/ bation. Despite this exposure, most eggs remain viable up amniotic membranes, yolk sac, and associated chambers) to hatching. The foremost reason for this is the highly ef- are all critical to counteract degradation of primary egg de- ficient early defense response of the egg’s innate immune fenses during development. With a focus on the chick em- system. In birds, there are 2 main, complementary types bryo (Gallus gallus domesticus), this review describes the pro- of immune defense: (1) nonspecific mechanisms, which Dr. Maxwell T. Hincke M.T.H. and M.D.S. contributed equally. Faculty of Medicine, University of Ottawa 451 Smyth Road Ottawa, ON K1H 8M5 (Canada) E-Mail mhincke @ uottawa.ca © 2018 The Author(s) Dr. Sophie Réhault-Godbert Published by S. Karger AG, Basel INRA-Centre Val de Loire UMR0083 Biologie des Oiseaux et Aviculture (BOA) E-Mail [email protected] This article is licensed under the Creative Commons Attribution- FR–37380 Nouzilly (France) www.karger.com/jin NonCommercial-NoDerivatives 4.0 International License (CC BY- NC-ND) (http://www.karger.com/Services/OpenAccessLicense). E-Mail sophie.rehault-godbert @ inra.fr Usage and distribution for commercial purposes as well as any dis- tribution of modified material requires written permission. act on pathogens in a nontargeted manner (physical and transfers nutrients and immunoglobulin (Ig)Y from the chemical barriers, and components of innate immunity egg yolk to the developing embryo or the newly hatched including antimicrobial molecules and cellular mecha- chick. Therefore, during the first week after hatching, be- nisms, i.e., heterophils and macrophages), and (2) adap- fore the immune system is mature enough to produce its tive mechanisms, which target specific pathogens (anti- own B lymphocytes, a chick’s humoral immunity depends bodies and lymphocytes). The innate immune responses on maternal antibodies (IgY) received from the egg yolk. can directly control the replication or spread of patho- gens by induction of phagocytosis or antimicrobial prod- ucts. This review covers studies on the well-documented Innate Immune Receptors and Antimicrobial chick embryo (Gallus gallus domesticus), from which Peptides most of our knowledge on avian embryogenesis is de- rived [1]. TLRs recognize microbes by binding to pathogen-as- The first line of defense against pathogenic microor- sociated molecular patterns (PAMPs) such as lipopoly- ganisms is formed by physical barriers such as the skin saccharide (LPS), lipoteichoic acid, bacterial flagellin, li- or, in the egg, the eggshell (ES), as well as by chemical poproteins, peptidoglycans, glycophosphatidylinositol, innate immune protective mechanisms; together, these and bacterial DNA, in addition to single- and double- resist pathogen invasion from a contaminated environ- stranded viral RNA. At this time, 10 TLRs have been iden- ment. Because the development of an avian embryo oc- tified in chickens; most of them still require better char- curs in an egg chamber that is physically separated from acterization on ligand-receptor interactions and the as- the hen, the egg contains all the required elements to sociated downstream signaling pathways involved in nourish and protect the developing embryo during the their immune effector functions [7]. However, it is clear entire cycle of its development prior to hatching. How- that chick embryonic tissues express TLRs from ED3 on- ever, the innate defenses initially present within the egg wards, recognizing viral ligands and responding to them, disappear gradually during incubation; therefore, to pre- thereby exhibiting an innate preparedness [4, 8, 9]. Avian vent the penetration and growth of bacteria in the egg β-defensins (AvBDs) and cathelicidins (CTHLs) are ma- during embryonic development, new defense systems jor classes of antimicrobial peptides with distinctive ex- (not yet fully characterized) are required [2, 3]. Defensive pression patterns during early embryonic development responses also involve the recognition of pathogens by [9]. There are 14 AvBD genes (AvBD1–14) and 4 mem- Toll-like receptors (TLRs) present in blood vessels, and bers of the CTHL gene family (CTHL1, CTHLB1, CTHL2, by leukocytes that develop within the embryo (hetero- and CTHL3) [9]. Antimicrobial peptides such as AvBDs phils and macrophages) [4]. While there are good indica- have a broad spectrum of activity against Gram-negative tors that an innate immune response can be triggered, it and Gram-positive bacteria, as well as fungi [10]. The is not yet clear how an inflammatory response in the em- ovodefensin OvoDA1/gallin is a novel β-defensin-related bryonated egg would be controlled, as the cellular and antimicrobial peptide which appears to be expressed spe- molecular checkpoints in such a process are completely cifically in the avian oviduct and possesses anti-Escherich- unknown. ia coli activity [11–13]. Much less is known about the an- The developing chicken embryo is able to trigger an tibacterial peptide natural killer (NK)-lysin (the chicken immune response to a pathogen just prior to hatching, a ortholog of human granulysin), which is a novel effector characteristic that is routinely exploited in modern, large- of cytotoxic T cells and NK cells [14, 15]. The chicken scale poultry production with the administration of ortholog of liver-expressed antimicrobial peptide-2 in ovo vaccination for multiple pathogens, including (cLEAP-2) is a cationic antimicrobial peptide (CAMP) Marek’s disease (MD) and infectious bursal disease (IBD). that is expressed in chicken epithelial tissues and upregu- Embryonic development takes 21 days, and the first signs lated in response to Salmonella enterica serovar Enteriti- of a developing immune system are observed by the 10th dis infection [16, 17]. NK-lysin and cLEAP-2 have not day (ED10). On ED11 and ED12, T cells and B cells are been detected in the egg or within extra-embryonic struc- developed, respectively, with B cell differentiation occur- tures to date, but are expressed in the chick embryo [14, ring after ED15. By ED18, the chicken embryo is immu- 16]. Maternal stimulation with TLR ligands was observed nocompetent and capable of producing both an innate to modulate oviduct expression of components of innate and an adaptive response to pathogens [5, 6]. During in- immunity such as proinflammatory cytokines, AvBDs, cubation and after hatching, the yolk sac (YS) membrane and CTHLs [18, 19]. 112 J Innate Immun 2019;11:111–124 Hincke et al. DOI: 10.1159/000493719 ED0 Eggshell Physical barrier and Egg white antimicrobial molecules Physicochemical barrier (pH, (OCX36, LYZ, TF) viscosity) and antimicrobial molecules (LYZ, TF, antiproteases) Egg yolk Vitelline membrane Maternal IgY Physical barrier and antimicrobial molecules (AvBD11, VMO1, LYZ) Amniotic sac Physical barrier (membrane) Protection against dehydration and antimicrobial molecules (LYZ, TF, AvBD11, BMSP, ED8 Chorioallantoic membrane etc.) /allantoic sac Physical barrier (membrane) Acid pH (allantoic fluid) Immune cells Toll-like receptors/interferons Yolk sac Antimicrobial molecules Physical barrier/assimilation of IgY Fig. 1. Schema contrasting the basal innate defenses of the egg between ED0 (or unfertilized) and ED8 (developed extra-embryonic membranes). Egg Basic Structures and Innate Immunity tion of the egg microbiome assembly and a
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