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      Fecal antibody levels as a noninvasive method for measuring immunity to gastrointestinal nematodes in ecological studies

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          Abstract

          Among‐individual variation in antibody‐associated immunity to gastrointestinal nematode parasites ( GIN) is known be associated with life‐history traits and vital rates in wild vertebrate systems. To date, measurement of levels of antibodies against GIN antigens in natural populations has exclusively been based on invasive blood sampling techniques. Previous work in laboratory rodents and ruminant livestock suggests that antibody measures from feces may provide a viable noninvasive approach. We measured total and anti‐ GIN antibodies of different isotypes (immunoglobulin (Ig) G, IgA and IgE) from paired samples of plasma and feces from free‐living Soay sheep of different ages and sexes. We tested the correlations among these measures as well as their associations with body mass and Strongyle nematode fecal egg counts ( FEC). Significant positive correlations were present among plasma and fecal anti‐ GIN antibody levels for IgG and IgA. Generally, correlations between total antibody levels in plasma and feces were weaker and not significant. No significant relationships were found between any antibody measures and body mass; however, fecal anti‐ GIN antibody levels were significantly negatively correlated with FEC. Our data clearly demonstrate the feasibility of measuring anti‐ GIN antibodies from fecal samples collected in natural populations. Although associations of fecal antibody levels with their plasma counterparts and FEC were relatively weak, the presence of significant correlations in the predicted direction in a relatively small and heterogeneous sample suggests fecal antibody measures could be a useful, noninvasive addition to current eco‐immunological studies.

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          Intestinal IgA production and its role in host-microbe interaction.

          Complex and diverse communities of bacteria establish mutualistic and symbiotic relationships with the gut after birth. The intestinal immune system responds to bacterial colonization by acquiring a state of hypo-responsiveness against commensals and active readiness against pathogens. The resulting homeostatic balance involves a continuous dialog between the microbiota and lymphocytes with the intermediation of epithelial and dendritic cells. This dialog causes massive production of immunoglobulin A (IgA), a non-inflammatory antibody specialized in mucosal protection. Here, we discuss recent advances on the regulation of intestinal IgA responses and their role in host-microbe interaction. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
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            Secretory IgA: Designed for Anti-Microbial Defense

            Prevention of infections by vaccination remains a compelling goal to improve public health. Mucosal vaccines would make immunization procedures easier, be better suited for mass administration, and most efficiently induce immune exclusion – a term coined for non-inflammatory antibody shielding of internal body surfaces, mediated principally by secretory immunoglobulin A (SIgA). The exported antibodies are polymeric, mainly IgA dimers (pIgA), produced by local plasma cells (PCs) stimulated by antigens that target the mucose. SIgA was early shown to be complexed with an epithelial glycoprotein – the secretory component (SC). A common SC-dependent transport mechanism for pIgA and pentameric IgM was then proposed, implying that membrane SC acts as a receptor, now usually called the polymeric Ig receptor (pIgR). From the basolateral surface, pIg-pIgR complexes are taken up by endocytosis and then extruded into the lumen after apical cleavage of the receptor – bound SC having stabilizing and innate functions in the secretory antibodies. Mice deficient for pIgR show that this is the only receptor responsible for epithelial export of IgA and IgM. These knockout mice show a variety of defects in their mucosal defense and changes in their intestinal microbiota. In the gut, induction of B-cells occurs in gut-associated lymphoid tissue, particularly the Peyer’s patches and isolated lymphoid follicles, but also in mesenteric lymph nodes. PC differentiation is accomplished in the lamina propria to which the activated memory/effector B-cells home. The airways also receive such cells from nasopharynx-associated lymphoid tissue but by different homing receptors. This compartmentalization is a challenge for mucosal vaccination, as are the mechanisms used by the mucosal immune system to discriminate between commensal symbionts (mutualism), pathobionts, and overt pathogens (elimination).
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              Mucosal B cells: phenotypic characteristics, transcriptional regulation, and homing properties.

              Mucosal antibody defense depends on a complex cooperation between local B cells and secretory epithelia. Mucosa-associated lymphoid tissue gives rise to B cells with striking J-chain expression that are seeded to secretory effector sites. Such preferential homing constitutes the biological basis for local production of polymeric immunoglobulin A (pIgA) and pentameric IgM with high affinity to the epithelial pIg receptor that readily can export these antibodies to the mucosal surface. This ultimate functional goal of mucosal B-cell differentiation appears to explain why the J chain is also expressed by IgG- and IgD-producing plasma cells (PCs) occurring at secretory tissue sites; these immunocytes may be considered as 'spin-offs' from early effector clones that through class switch are on their way to pIgA production. Abundant evidence supports the notion that intestinal PCs are largely derived from B cells initially activated in gut-associated lymphoid tissue (GALT). Nevertheless, insufficient knowledge exists concerning the relative importance of M cells, major histocompatibility complex class II-expressing epithelial cells, and professional antigen-presenting cells for the uptake, processing, and presentation of luminal antigens in GALT to accomplish the extensive and sustained priming and expansion of mucosal B cells. Likewise, it is unclear how the germinal center reaction in GALT so strikingly can promote class switch to IgA and expression of J chain. Although B-cell migration from GALT to the intestinal lamina propria is guided by rather well-defined adhesion molecules and chemokines/chemokine receptors, the cues directing preferential homing to different segments of the gut require better definition. This is even more so for the molecules involved in homing of mucosal B cells to secretory effector sites beyond the gut, and in this respect, the role of Waldever's ring (including the palatine tonsils and adenoids) as a regional inductive tissue needs further characterization. Data suggest a remarkable compartmentalization of the mucosal immune system that must be taken into account in the development of effective local vaccines to protect specifically the airways, eyes, oral cavity, small and large intestines, and urogenital tract.
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                Author and article information

                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                08 December 2015
                January 2016
                : 6
                : 1 ( doiID: 10.1002/ece3.2016.6.issue-1 )
                : 56-67
                Affiliations
                [ 1 ] Institutes of Evolutionary Biology and Immunology and Infection Research School of Biological SciencesUniversity of Edinburgh West Mains Road EdinburghUK
                [ 2 ] Moredun Research InstitutePentlands Science Park Bush Loan MidlothianUK
                Author notes
                [*] [* ] Correspondence

                Tom N. McNeilly, Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian, UK.

                Tel.: +(44)131 445 5111; Fax.: +(44)131 445 6111;

                E‐mail: Tom.McNeilly@ 123456moredun.ac.uk

                Article
                ECE31858
                10.1002/ece3.1858
                4716500
                26811774
                43b59ade-8503-4554-a42c-16ba946af56a
                © 2015 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 27 June 2015
                : 22 October 2015
                : 23 October 2015
                Page count
                Pages: 12
                Funding
                Funded by: Scottish Government
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece31858
                January 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.7.5 mode:remove_FC converted:18.01.2016

                Evolutionary Biology
                fecal egg counts,immunoglobulin,ovis aries,soay sheep,strongyle nematode,teladorsagia circumcincta

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