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The Intestinal Immune System

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The Intestinal Immune System Gut: first published as 10.1136/gut.30.12.1679 on 1 December 1989. Downloaded from Gut, 1989, 30, 1679-1685 The intestinal immune system WILLIAM F DOE (This article is one of a series linked with the Festschrift for Christopher Boot/i. See Gut Festschrift 1989; 30.) The concept of localised intestinal immunity has its contain the largest accumulation of lymphoid tissues origins in Besredka's observation that oral immunisa- in the body' in the form of lymphoid aggregates in tion using killed salmonella organisms provided solid Peyer's patches and in the lamina propria (solitary protection against dysenteric infection irrespective of lymphoid nodules) and as the scattered lymphocyte the titres of serum antibody.' But the clinical benefits populations found in the epithelium and in the lamina were variable and short lived and interest lapsed. propria. Little further progress was made until Heremans' Although nascent Peyer's patches are evident in discovery of IgA and the marked predominance of the newborn, the epithelium and lamina propria are IgA-containing plasma cells in normal intestinal devoid of mononuclear cells. T lymphocytes mi- mucosa.2 The differences between the antigenic grating from the thymus rapidly populate the thymus determinants of serum and secretory IgA led to the - dependent areas of Peyer's patches and the identification of an additional polypeptide chain, the epithelium but exposure to micro-organisms in the secretory component (SC), which is essential to the normal environment is necessary to develop the B secretion and function of IgA antibody at mucosal cell population and their germinal follicles as shown surfaces.' by experiments conducted in germ free animals.6 The importance of the mucosal immune system to the pathogenesis of intestinal disease was swiftly Induction of the secretory immune response recognised by Chris Booth. When I arrived as a houseman at Hammersmith in 1969, several pio- Non-immune and immune mechanisms protect the neering immunological studies of coeliac disease had privileged environment of the lamina propria from been published. The clinical research ethos at challenge by foreign antigens. Gastric acidity, diges- http://gut.bmj.com/ Hammersmith stimulated the study of human disease tive proteases in the gastrointestinal tract, intestinal not only by applying basic scientific knowledge and mobility, the commensal microflora and the mucous techniques but also by recognising that careful study coat or glycocolyx comprise some of the non-specific of human disease can also provide opportunities for protective barriers. The immune mechanisms may advancing our understanding of human biology. I operate within the lumen of the gut, at the mucosal recall the outpatient clinic in 1969 when Chris handed surface or within the lamina propria. The inter- me the referral letter for a new patient he had not epithelial lymphocyte (IEL) population are pre- on September 30, 2021 by guest. Protected copyright. seen: 'Fascinating, sounds like alpha chain disease.' dominantly suppressor lymphocytes (Ts) in contrast Several months later Heremans came to Hammer- with the lamina propria and show evidence of smith to deliver a series of outstanding lectures on the activation whereas most of the lamina propria secretory immune system. Grand rounds that week lymphocytes belong to the helper-inducer subset included the presentation of what was to be one of the (Th). Class II MHC determinants which represent a earliest published cases of alpha chain disease.4 restriction element in T cell dependent immune In the decades since these early discoveries, major responses are expressed on normal small intestinal advances in understanding the physiology of the epithelial cells but not colon epithelial cells unless the intestinal immune response and the advent of mole- colon is inflamed. Expression of class II antigens is cular biology have helped to elucidate the induction modulated by lymphokine products of activated T and regulation of the secretory antibody and cellular cells especially interferon y (IFNy). Bland and responses at mucosal surfaces. Warren7 reported that MHC class Il positive villous epithelial cells can present soluble antigen to primed Gut associated lymphoid tissue (GALT) T cells leading to antigen specific suppression. Although human colonic epithelial cells have been The exposed surface of the intestinal mucosa is under reported to act as stimulators in autologous and constant challenge by ingested foreign antigens in allogeneic responses8 others have been unable to micro-organisms, products of food digestion and stimulate T cells in an allogeneic system using an drugs. It is therefore not surprising that the intestines MHC class II positive colon cancer cell line.' 1679 Gut: first published as 10.1136/gut.30.12.1679 on 1 December 1989. Downloaded from 1680 William F Doe Whether IEL require a second signal from a mucosal surface relates to separation of the T and B accessory cells in the lamina propria remains to be cell zones in Peyer's patches from antigen presenting answered. cells is not known. Mestecky and McGhee'` have Most studies of isolated GALT cells have been speculated that antigen presentation to lymphocytes performed using Peyer's patch cells. Whether these does occur in GALT resulting in an 'initial induction' reflect the function of all organised GALT is un- of immune responses and that the 'terminal inductive known. The dome of Peyer's patches is covered by a stimuli' may occur at distant mucosal sites after these unique epithelium comprising cuboidal epithelial committed lymphocytes have migrated there. cells which express class II MHC antigens, very few The migratory characteristics of IgA-committed goblet cells and specialised antigen-sampling cells lymphoblasts and memory cells are quite distinct. called M (for microfold) cells."' M cells pinocytose Unlike memory lymphocytes, IgA-containing soluble antigens such as ferritin and horse-radish lymphoblasts do not recirculate but 'home' to the peroxidase or phagocytose particulate foreign organ of antigenic stimulation, secrete antibody, antigens including viruses and whole bacteria, and remain associated with the mucosal target tissue and transport them intact across the epithelium to the probably die within a few days.'` In rats primed and underlying lymphoreticular cells in the dome." challenged by intraintestinal injection of cholera Macrophages and dendritic cells are present in the toxin, specific antibody - containing lymphoblasts dome region, and MHC class II positive cells dis- were found three to five days later in the thoracic duct playing dendritic cell morphology are also found in lymph from where they entered the circulation and the T and B cell zones. Dendritic cells found in cell then populated distant mucosal sites. The number of suspensions of Peyer's patches are fully able to lymphoblasts in the thoracic duct greatly diminished present antigen in vitro"' and those present in the after five days but the number of small lymphocytes lamina propria of the small and large intestine in capable of transferring specific immunity to naive mouse and man are also competent to present animals (memory cells) peaked after two weeks and antigens. Whether Peyer's patch macrophages also persisted. The memory cells, which will produce T- function as antigen presenting cells, however, is and B-lymphoblasts when stimulated by specific uncertain, as lamina propria macrophages suppress antigen, enter the circulation from the lymph, 'home' antigen presentation by dendritic cells.'1 to distant mucosal sites and then re-enter the lymph Peyer's patches contain a higher proportion of B to recirculate.'7 Peripheral lymphoid tissues were not cells than nodes. B peripheral While IgM-bearing examined in these experiments but other studies http://gut.bmj.com/ cells predominate, there is significant enrichment for suggest that memory lymphocytes from the thoracic B cells displaying surface lgA and committed to IgA duct also 'home' preferentially to mucosal lymphoid synthesis consistent with the role of GALT as a major tissue. site for the induction of IgA responses. Peyer's Lymphocyte 'homing' is not dependent on the patches are also greatly enriched for T cells of the presence of antigen. IgA lymphoblasts migrate to helper-inducer subset (Th) although suppressor- fetal isografts of small intestine transplanted under- cytotoxic T cells (Ts) and the regulatory contra- neath the kidney capsule of an adult mouse.'` When suppressor T cells (Tcs) which appear to potentiate rats primed by intracolonic injection of cholera toxin on September 30, 2021 by guest. Protected copyright. immune responses to orally presented antigen, are were challenged 14 days later by injecting antigen also found. The high degree of preferential localis- into a surgically isolated loop of jejunum with an ation of B cells and IgA specific Th cells in Peyer's intact blood and lymph supply, blast cells appeared in patches is probably determined by the specificity of comparable numbers in the stimulated intestinal loop binding of these lymphocytes to the high endothelial and in the unstimulated jejunum. By cannulating and venule receptors present in postcapillary venules in draining the thoracic duct, the researchers confirmed Peyer's patches'4 which determine their represen- that antigen stimulation of memory cells in the tation in Peyer's patches and ultimately regulate the isolated jejunal loop resulted in the production of nature of the immune response generated.
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