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Mucosal Defence Along the Gastrointestinal Tract of Cats and Dogs Chris Stokes, Nashwa Waly

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Mucosal Defence Along the Gastrointestinal Tract of Cats and Dogs Chris Stokes, Nashwa Waly Mucosal defence along the gastrointestinal tract of cats and dogs Chris Stokes, Nashwa Waly To cite this version: Chris Stokes, Nashwa Waly. Mucosal defence along the gastrointestinal tract of cats and dogs. Vet- erinary Research, BioMed Central, 2006, 37 (3), pp.281-293. 10.1051/vetres:2006015. hal-00903038 HAL Id: hal-00903038 https://hal.archives-ouvertes.fr/hal-00903038 Submitted on 1 Jan 2006 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Vet. Res. 37 (2006) 281–293 281 © INRA, EDP Sciences, 2006 DOI: 10.1051/vetres:2006015 Review article Mucosal defence along the gastrointestinal tract of cats and dogs Chris STOKES*, Nashwa WALY Division of Veterinary Pathology Infection and Immunity, School of Clinical Veterinary Science, University of Bristol, Langford House, Langford, BS40 5DU, United Kingdom (Received 5 July 2005; accepted 9 January 2006) Abstract – Diseases that are associated with infections or allergic reactions in the gastrointestinal and respiratory tracts are major causes of morbidity in both cats and dogs. Future strategies for the control of these conditions require a greater understanding of the cellular and molecular mechanisms involved in the induction and regulation of responses at the mucosal surfaces. Historically, the majority of the fundamental studies have been carried out in rodents or with tissues obtained from man, but the expanding range of reagents available for the study of farm and companion animals provides opportunities for study in a wider range of animals including cats and dogs. To date, these studies have tended to be focussed on characterising the cellular distributions in healthy animals and in groups of cats and dogs identified as having an increased risk of mucosal disturbance. Where species comparisons of mucosal immune systems have been made, the results have tended to be divided between monogastric and ruminant animals. It is then not surprising that the mucosal immune systems of both cats and dogs bear greatest similarity to that documented for man and pigs. For example, IgA is the dominant immunoglobulin in mucosal secretions of cats and dogs and oral tolerance can be induced following the introduction of novel antigens into the diet. Also like several other species, cats become transiently hypersensitive to the newly introduced dietary antigen prior to the establishment of tolerance. In contrast, there are a number of potentially important differences. In particular, there are significant differences between cats and dogs in the expression MHC class II molecules on gut epithelial cells. Similarly, it has been reported that cats have elevated numbers of intraepithelial lymphocytes (IEL) and that a proportion of these express surface IgM. It remains to be determined if these differences reflect the way in which the animals are maintained and if they may have greater biological significance. cat / dog / mucosal / gut / immunology Table of contents 1. Introduction ..................................................................................................................................... 282 2. Enterocytes in mucosal immunity ................................................................................................... 283 3. Inductive and effector sites ............................................................................................................. 284 4. Mucosal immunoglobulins and plasma cells .................................................................................. 286 5. Mucosal cytokines and the response to mucosal infection ............................................................. 287 6. Cell trafficking and homing ............................................................................................................ 288 7. Induction of mucosal immune responses ........................................................................................ 289 * Corresponding author: [email protected] Article published by EDP Sciences and available at http://www.edpsciences.org/vetres or http://dx.doi.org/10.1051/vetres:2006015 282 C. Stokes, N. Waly 1. INTRODUCTION of the diet. In order to control such an exten- sive and diverse challenge, a complex bat- The current state of our collective knowl- tery of responses can be invoked. These edge of mucosal immunology is a reflection include both innate and acquired mecha- of studies carried out on a number of spe- nisms but it can be reasonably argued that cies, most notably man, rodents, ruminants the principal strategy adopted by both is one and pigs. In contrast it could be argued that in which the response is directed toward in terms of contributing “at the cutting preventing the antigen from interacting edge”, studies on the mucosal immune sys- with epithelial cells and thereby closing a tems of both cats and dogs have contributed “potential gateway” into the body. The gut relatively little. Whilst many of the studies epithelial cells and their associated mucus in these companion animals have been layer along with peristalsis and the low aimed at confirming that which has already stomach pH all contribute toward the bar- been reported in other species, there are a rier against the entry of harmful antigens. few notable exceptions. One such pioneer- The gastrointestinal tract is an extremely ing study was that of Cantor and Dumont. complex organ having multiple functions They were the first to highlight the impor- directed toward the digestion and absorp- tant role of the liver in the development of tion of nutrients, and the control of poten- oral tolerance. Using dogs they were able to tially harmful pathogens and commensal demonstrate that portacaval shunting could microflora. It is not surprising therefore that abolish the tolerogenic effect of feeding the a well-developed mucosal immune system contact sensitising agent dinitro-chloro- has evolved to protect it. The mucosal benzene (DNCB) [13]. immune system can be divided into two Whilst overall the strategies adopted by major compartments: that consisting of the most species to control events at mucosal organised lymphoid structures (Peyer’s surfaces are essentially very similar, there patches, mesenteric lymph nodes, etc.) and are significant differences as to how this is that occurring in tissues specialised for accomplished. The most marked differ- other functions (the intestinal lamina propria). ences are found between ruminants and In the conventional model, the organised mono-gastric animals and not surprisingly tissues are “inductive” sites, populated by both cats and dogs fit into the latter pattern. naive cells: following priming the cells migrate The aim of this review is to briefly summa- via the mesenteric lymph node before hom- rise the similarities between what has been ing to the diffuse, “effector” sites such as the established in other species with that intestinal lamina propria. Lymphoid aggre- reported in cats and dogs and to focus upon gates are found throughout the intestine and areas where significant differences have it has been suggested that the numbers may been identified. reflect the bacterial load encountered in dif- The mucosal surface of the gastrointes- ferent areas of the feline large intestine [49]. tinal tract forms a major interface between The large numbers of aggregates in the anal any animal and the environment in which it canal and terminal rectum (“rectal tonsils”) lives. The gut mucosal environment is com- are thought to prevent ascending infection plicated by both the magnitude of challenge from the perianal area. In healthy animals, and the complex array of antigens that are faecal material is present in the post-pelvic presented. The immune system that is asso- region only during defecation and the ciated with the gastrointestinal tract is number of lymphoid aggregates is corre- required to recognise these different groups spondingly low. Faeces are stored in the dis- of antigens and respond “appropriately”. It tal colon proximal to the pelvis, an area must thus be able to respond actively to where there is a greater density of lymphoid potential pathogens whilst at the same time aggregates. Moving away from the pelvis not “over-reacting” to harmless components toward the ileocloic junction, the reduced Feline and canine gut immunology 283 likelihood of faecal stasis may account for villus tip and expression may also be the gradual decline in the number of aggre- induced in the crypt epithelium, secondary gates. Interestingly, a similar pattern is to a range of inflammatory disorders [8]. observed in the distribution of dividing The unique location of gut enterocytes at (proliferating cell nuclear antigen positive the interface between the host and gut envi- - PCNA) epithelial cells with the numbers ronment highlight their pivotal role in gut of PCNA positive cells increased with dis- defence. It is then not surprising that there tance from the anus. is a growing body of literature on their expression of various “accessory mole- cules” that may help facilitate this role. To 2. ENTEROCYTES
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