In the intestine, a balance must be maintained between potentially harmful bacteria and an extensive network of cells that constitute the gut-associated lymphoid tissues (GALT). The mechanisms that govern this homeostasis remain poorly understood. When the homeostasis is compromised, the outcome can range from inflammatory bowel disease to food allergies to inflammation-associated malignancies. In this review, we discuss recent studies that shed light on the organization of immune cells in the intestine and provide clues as to how these interact with luminal microorganisms. We describe the role for an orphan nuclear receptor, RORyt, in the development of lymphoid tissue inducer (LTi) cells during fetal life and of intestinal cryptopatch (CP) cells postnatally, resulting in the genesis of secondary lymphoid organs and tertiary lymphoid follicles, respectively. We also review recent studies showing that dendritic cells (DCs) communicate with the intestinal lumen and transport bacteria from the lumen to the lamina propria (LP). Finally, we propose a model that describes how sensing of microbial content by specialized DCs that extend processes across epithelia can regulate the immune response to the microflora while maintaining the integrity of the intestinal epithelium.
A single layer of intestinal epithelial cells protects the internal organs from more than 700 species of resident gut bacteria totaling approximately 1014 cells [1-4]. The mucosal immune system contains and regulates this permanent "infection," but it also supports it, because of the advantages provided by the microorganisms. The immune system must sense changes in the composition of the microflora. These changes may alert the host to the presence of pathogenic bacteria and activate prompt defense mechanisms. It remains unclear, however, how host defenses can discriminate between commensal and pathogenic bacteria, because they share antigens and express identical Toll-like receptor (TLR) ligands. The intestinal immune system must also have the capacity to recognize and become tolerized against food antigens. Thus the mucosal immune system must handle a number of "nonself" antigens differently—some antigens will induce regulatory or tolerogenic responses, others will be sequestered, and yet others will induce different types of protective immune responses.
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