Transepithelial antigen delivery in the small intestine: different paths, different outcomes - PubMed (original) (raw)
Review
Transepithelial antigen delivery in the small intestine: different paths, different outcomes
Kathryn A Knoop et al. Curr Opin Gastroenterol. 2013 Mar.
Abstract
Purpose of review: The intestinal epithelium is a dynamic barrier protecting the body from the multitudes of luminal micro-organisms present in the gut. However, this barrier is not impermeable and mechanisms exist that allow small amounts of antigen to traverse the epithelium in controlled manner to maintain tolerance and to mount immune responses. This review will summarize our current understanding of how luminal antigens traverse the small intestine epithelium without disrupting the epithelial barrier and how these antigen delivery pathways might influence the resulting immune responses.
Recent findings: Recent findings have revealed four pathways for transepithelial antigen delivery in the absence of barrier disruption. We propose that during homeostasis, antigen introduced through microfold cells induces immunoglobulin A responses, antigen delivered by goblet cell-associated antigen passages contributes to peripheral tolerance, and antigen delivered by paracellular leak initiates immune responses in the mesenteric lymph node. In contrast, dendritic cell transepithelial dendrites may play an important role in host protection during pathogen infection, but do not appear to play a role in antigen capture by lamina propria dendritic cells in the steady state.
Summary: These observations indicate that the route by which antigen crosses the epithelium directs the outcome of the subsequent immune response.
Conflict of interest statement
Conflicts of interest:
The authors declare no other conflicts of interest.
Figures
Figure 1
Models for trans-epithelial antigen delivery. The four described pathways of trans-epithelial antigen delivery that do not result in barrier disruption are shown incorporating their different locations, sizes of delivered antigen, cells involved, and proposed physiological outcomes. Not shown is antigen delivery via villous M cells, which is presumed to have similar characteristics to antigen delivery via M cells in the follicle associated epithelium.
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References
- Bockman DE, Cooper MD. Pinocytosis by epithelium associated with lymphoid follicles in the bursa of Fabricius, appendix, and Peyer’s patches. An electron microscopic study. Am J Anat. 1973;136:455–477. - PubMed
- Tyrer PC, Ruth Foxwell A, Kyd JM, Otczyk DC, Cripps AW. Receptor mediated targeting of M-cells. Vaccine. 2007;25:3204–3209. - PubMed
- Hase K, Kawano K, Nochi T, Pontes GS, Fukuda S, Ebisawa M, Kadokura K, Tobe T, Fujimura Y, Kawano S, et al. Uptake through glycoprotein 2 of FimH+ bacteria by M cells initiates mucosal immune response. Nature. 2009;462:226–230. Through the demonstartion that an M cell specific receptor is required for endocytosis and sampling of bacteria, this work clearly describes the importance of M cells in mounting specific responses against enteric bacteria. - PubMed
- Neutra MR, Frey A, Kraehenbuhl JP. Epithelial M cells: gateways for mucosal infection and immunization. Cell. 1996;86:345–348. - PubMed
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