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      Flagella at the Host-Microbe Interface: Key Functions Intersect With Redundant Responses

      review-article
      ,
      Frontiers in Immunology
      Frontiers Media S.A.
      fliC, goblet cell, IBD, DEFA6, LYPD8, ZG16, TLR5, IgA

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          Abstract

          Many bacteria and other microbes achieve locomotion via flagella, which are organelles that function as a swimming motor. Depending on the environment, flagellar motility can serve a variety of beneficial functions and confer a fitness advantage. For example, within a mammalian host, flagellar motility can provide bacteria the ability to resist clearance by flow, facilitate access to host epithelial cells, and enable travel to nutrient niches. From the host’s perspective, the mobility that flagella impart to bacteria can be associated with harmful activities that can disrupt homeostasis, such as invasion of epithelial cells, translocation across epithelial barriers, and biofilm formation, which ultimately can decrease a host’s reproductive fitness from a perspective of natural selection. Thus, over an evolutionary timescale, the host developed a repertoire of innate and adaptive immune countermeasures that target and mitigate this microbial threat. These countermeasures are wide-ranging and include structural components of the mucosa that maintain spatial segregation of bacteria from the epithelium, mechanisms of molecular recognition and inducible responses to flagellin, and secreted effector molecules of the innate and adaptive immune systems that directly inhibit flagellar motility. While much of our understanding of the dynamics of host-microbe interaction regarding flagella is derived from studies of enteric bacterial pathogens where flagella are a recognized virulence factor, newer studies have delved into host interaction with flagellated members of the commensal microbiota during homeostasis. Even though many aspects of flagellar motility may seem innocuous, the host’s redundant efforts to stop bacteria in their tracks highlights the importance of this host-microbe interaction.

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          Most cited references124

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          The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system.

          The gastrointestinal tract is covered by mucus that has different properties in the stomach, small intestine, and colon. The large highly glycosylated gel-forming mucins MUC2 and MUC5AC are the major components of the mucus in the intestine and stomach, respectively. In the small intestine, mucus limits the number of bacteria that can reach the epithelium and the Peyer's patches. In the large intestine, the inner mucus layer separates the commensal bacteria from the host epithelium. The outer colonic mucus layer is the natural habitat for the commensal bacteria. The intestinal goblet cells secrete not only the MUC2 mucin but also a number of typical mucus components: CLCA1, FCGBP, AGR2, ZG16, and TFF3. The goblet cells have recently been shown to have a novel gate-keeping role for the presentation of oral antigens to the immune system. Goblet cells deliver small intestinal luminal material to the lamina propria dendritic cells of the tolerogenic CD103(+) type. In addition to the gel-forming mucins, the transmembrane mucins MUC3, MUC12, and MUC17 form the enterocyte glycocalyx that can reach about a micrometer out from the brush border. The MUC17 mucin can shuttle from a surface to an intracellular vesicle localization, suggesting that enterocytes might control and report epithelial microbial challenge. There is communication not only from the epithelial cells to the immune system but also in the opposite direction. One example of this is IL10 that can affect and improve the properties of the inner colonic mucus layer. The mucus and epithelial cells of the gastrointestinal tract are the primary gate keepers and controllers of bacterial interactions with the host immune system, but our understanding of this relationship is still in its infancy. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
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            Immunological aspects of intestinal mucus and mucins.

            A number of mechanisms ensure that the intestine is protected from pathogens and also against our own intestinal microbiota. The outermost of these is the secreted mucus, which entraps bacteria and prevents their translocation into the tissue. Mucus contains many immunomodulatory molecules and is largely produced by the goblet cells. These cells are highly responsive to the signals they receive from the immune system and are also able to deliver antigens from the lumen to dendritic cells in the lamina propria. In this Review, we will give a basic overview of mucus, mucins and goblet cells, and explain how each of these contributes to immune regulation in the intestine.
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              Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria.

              Paneth cells in mouse small intestinal crypts secrete granules rich in microbicidal peptides when exposed to bacteria or bacterial antigens. The dose-dependent secretion occurs within minutes and alpha-defensins, or cryptdins, account for 70% of the released bactericidal peptide activity. Gram-negative bacteria, Gram-positive bacteria, lipopolysaccharide, lipoteichoic acid, lipid A and muramyl dipeptide elicit cryptdin secretion. Live fungi and protozoa, however, do not stimulate degranulation. Thus intestinal Paneth cells contribute to innate immunity by sensing bacteria and bacterial antigens, and discharge microbicidal peptides at effective concentrations accordingly.
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                Author and article information

                Contributors
                Journal
                Front Immunol
                Front Immunol
                Front. Immunol.
                Frontiers in Immunology
                Frontiers Media S.A.
                1664-3224
                24 March 2022
                2022
                : 13
                : 828758
                Affiliations
                [1] Department of Microbiology and Immunology, School of Medicine, University of California, Davis , Davis, CA, United States
                Author notes

                Edited by: Wenkai Ren, South China Agricultural University, China

                Reviewed by: Pengpeng Xia, Yangzhou University, China; Mingxu Zhou, Jiangsu Academy of Agricultural Sciences (JAAS), China; Miaomiao Wu, Hunan Agricultural University, China

                *Correspondence: Charles L. Bevins, clbevins@ 123456ucdavis.edu

                This article was submitted to Nutritional Immunology, a section of the journal Frontiers in Immunology

                Article
                10.3389/fimmu.2022.828758
                8987104
                35401545
                99b86544-2dcc-497f-93fa-e087c036c73c
                Copyright © 2022 Akahoshi and Bevins

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 03 December 2021
                : 21 February 2022
                Page count
                Figures: 3, Tables: 1, Equations: 0, References: 124, Pages: 12, Words: 6353
                Categories
                Immunology
                Review

                Immunology
                flic,goblet cell,ibd,defa6,lypd8,zg16,tlr5,iga
                Immunology
                flic, goblet cell, ibd, defa6, lypd8, zg16, tlr5, iga

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