Abstract
The mucosal surfaces of the gastrointestinal and respiratory tracts are lined by epithelial barriers composed of cells joined by tight junctions. These gasket-like junctional structures are generally effective in excluding peptides and macromolecules with antigenic potential (Madara et al. 1990). Mucosal surfaces are also provided with other defenses such as local secretions containing mucins and secretory immunoglobulin A (IgA) antibodies that tend to prevent antigens and pathogens from contacting the epithelium (Neutra et al. 1994). Nevertheless, to obtain samples from the external environment across this barrier, the mucosal immune system depends on a close collaboration between epithelial cells and antigen-presenting and lymphoid cells. These “lympho-epithelial complexes” allow transport of antigen samples across the mucosal barrier without compromising the integrity and protective functions of the epithelium.
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References
Allan CH, Mendrick DL, Trier JS (1993) Rat intestinal M cells contain acidic endosomal-lysosomal compartments and express Class II major histocompatibility complex determinants. Gastroenterology 104:698–708
Amerongen HM, Weltzin, RA, Farnet CM, Michetti P, Haseltine WA, Neutra MR (1991) Transepithelial transport of HIV-1 by intestinal M cells: a mechanism for transmission of AIDS. J Acquir Immune Defic Syndr 4:760–765
Amerongen HM, Wilson GAR, Fields BN, Neutra MR (1994) Proteolytic processing of reovirus is required for adherence to intestinal M cells. J Virol 68:8428–8432
Apodaca G, Katz LA, Mostov KE (1994) Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J Cell Biol 12:67–86
Bass DM, Trier JS, Dambrauskas R, Wolf JL (1988) Reovirus type 1 infection of small intestinal epithelium in suckling mice and its effect on M cells. Lab Invest 55:226–235
Bliska JB, Galan JE, Falkow S (1993) Signal transduction in the mammalian cell during bacterial attachment and entry. Cell 73:903–920
Bockman DE, Cooper MD (1973) Pinocytosis by epithelium associated with lymphoid follicles in the bursa of Fabricius, appendix, and Peyer’s patches. An electron microscopic study. Am J Anat 136:455–478
Borghesi C, Regoli M, Bertelli E, Nicoletti C (1996) Modifications of the follicle-associated epithelium by short-term exposure to a non-intestinal bacterium. J Pathol 180:326–332
Butcher EC (1991) Leukocyte-endothelial cell recognition: three (or more) steps to specificity or diversity. Cell 67:1033–1036
Bye WA, Allan CH, Trier JS (1984) Structure, distribution and origin of M cells in Peyer’s patches of mouse ileum. Gastroenterology 86:789–801
Childers NK, Denys FR, McGhee JF, Michalek SM (1990) Ultrastructural study of liposome uptake by M cells of rat Peyer’s patches: an oral vaccine system for delivery of purified antigen. Regional Immunol 3:8–16
Clark MA, Jepson MA, Simmons NL, Booth TA, Hirst BH (1993) Differential expression of lectin-binding sites defines mouse intestinal M-cells. J Histochem Cytochem 41:1679–1687
Corthesy B, Kaufmann M, Phalipon A, Peitsch M, Neutra MR, Kraehenbuhl JP (1996) A pathogen specific epitope inserted into recombinant secretory immunoglobulin is immunogenic by the oral route. J Biol Chem 52:33670–33677
Cuvelier CA, Quatacker J, Mielants H, de Vos M, Veys E, Roels H (1993) M cells are damaged and increased in number in inflamed human ileal mucosa. Eur J Morphol 31:87–91
Druben DG, Nelson WJ (1996) Origins of cell polarity. Cell 84:335–344
Eckmann L, Kagnoff MF, Fierer J. (1995) Intestinal epithelial cells as watchdogs for the natural immune system. Trends Microbiol 3:118–120
Ermak TH, Owen RL (1987) Phenotype and distribution of T lymphocytes in Peyer’s patches of athymic mice. Histochemistry 87:321–325
Ermak TH, Owen RL (1994) Differential distribution of lymphocytes and accessory cells in mouse Peyer’s patches. Am J Trop Med Hyg 50:14–28
Ermak TH, Steger HJ, Pappo J (1990) Phenotypically distinct subpopulations of T cells in domes and M-cell pockets of rabbit gut-associated lymphoid tissues. Immunology 71:530–537
Ermak TH, Dougherty EP, Bhagat HR, Kabok Z, Pappo J (1995) Uptake and transport of copolymer biodegradable microspheres by rabbit Peyer’s patch M cells. Cell Tissue Res 279:433–436
Falk P, Roth KA, Gordon JI (1994) Lectins are sensitive tools for defining the differentiation programs of epithelial cell lineages in the developing and adult mouse gastrointestinal tract. Am J Physiol 266:G987-G1003
Fantini J, Cook DG, Nathanson N, Spitalnik SL, Gonzalez-Scarano F (1993) Infection of colonic epithelial cell lines by type 1 human immunodeficiency virus (HIV-1) is associated with cell surface expression of galactosyl ceramide, a potential alternative gp 120 receptor. Proc Natl Acad Sei USA 90:2700–2704
Farstad IN, Haistensen TS, Fausa O, Brandtzaeg P (1994) Heterogeneity of M cell-associated B and T cells in human Peyer’s patches. Immunology 83:457–464
Finlay BB, Falkow S (1997) Common themes in microbial pathogenesis revisited. Micrbiol Mol Biol Rev 61:136–139
Finzi G, Cornaggia M, Capeila C, Fiocca R, Bosi F, Solcia E (1993) Cathepsin E in follicle associated epithelium of intestine and tonsils: localization to M cells and possible role in antigen processing. Histochemistry 99:201–211
Frey A, Lencer WI, Weltzin R, Giannasca KT, Giannasca PJ, Neutra MR (1996) Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells: implications for microbial attachment and oral vaccine targeting. J Exp Med 184:1045–1060
Fujimura Y, Kihara T, Mine H (1992) Membranous cells as a portal of Yersinia pseudotuberculosis entry into rabbit ileum. J Clin Electron Microsc 25:35–45
Gebert A, Hach G (1993) Differential binding of lectins to M cells and enterocytes in the rabbit cecum. Gastroenterology 105:1350–1361
Gebert A, Hach G, Bartels H (1992) Co-localization of vimentin and cytokeratins in M-cells of rabbit gut-associated lymphoid tissue (GALT). Cell Tissue Res 269:331–340
Giannasca PJ, Giannasca KT, Falk P, Gordon JI, Neutra MR (1994) Regional differences in glyco- conjugates of intestinal M cells in mice: potential targets for mucosal vaccines. Am J Physiol 267:G1108-G1121
Gordon JI, Hermiston ML (1994) Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr Opin Cell Biol 6:795–803
Griffiths SL, Finkelstein RA, Critchley DR (1986) Characterization of the receptor for cholera toxin and Escherichia coli heat-labile toxin in rabbit intestinal brush borders. Biochem J 238:313–322
Grutzkau A, Hanski C, Hahn H, Riecken EO (1990) Involvement of M cells in the bacterial invasion of Peyer’s patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut 3:1011–1015
Hultgren SJ, Abraham S, Caparon M, Falk P, St. Gerne III JW, Normark S (1993) Pilus and nonpilus adhesins: assembly and function in cell recognition. Cell 73:887–901
Inman LR, Cantey JR (1983) Specific adherence of Escherichia Coli (strain RDEC-1) to membranous (M) cells of the Peyer’s patch in Escherichia Coli diarrhea in the rabbit. J Clin Invest 71:1–8
Ito S (1974) Form and function of the glycocalyx on free cell surfaces. Philos Trans R Soc Lond (Biol) 268:55–66
Jarry A, Robaszkiewicz M, Brousse N, Potet F (1989) Immune cells associated with M cells in the follicle-associated epithelium of Peyer’s patches in the rat. Cell Tissue Res 225:293–298
Jepson MA, Clark MA, Simmons NL, Hirst BH (1993) Epithelial M cells in the rabbit caecal lymphoid patch display distinctive surface characteristics. Histochemistry 100:441–447
Jones BD, Falkow S (1996) Salmonellosis-host immune responses and bacterial virulence determinants. Annu Rev Immunol 14:533–561
Jones BD, Ghori N, Falkow S (1994) Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer’s patches. J Exp Med 180:15–23
Jung HC, Eckmann L, Yang SK, Panja A, Fierer J, Morzycka-Wroblewska E, Kagnoff MF (1995) A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 95:55–65
Kerneis S, Bogdanova A, Colucci-Guyon E, Kraehenbuhl JP, Pringault E (1996) Cytosolic distribution of villin in M cells from mouse Peyer’s patches correlates with the absence of a brush border. Gastroenterology 110:515–521
Kerneis S, Bogdanova A, Kraehenbuhl JP, Pringault E (1997) Conversion by Peyer’s patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277:949–952
Kohbata S, Yokobata H, Yabuuchi E (1986) Cytopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine ileal Peyer’s patches in ligated ileal loops: an ultrastructural study. Microbiol Immunol 30:1225–1237
Madara JL (1994) Migration of neutrophils through epithelial monolayers. Trends Cell Biol 4:4–7
Madara JL, Nash S, Moore R, Atisook K (1990) Structure and function of the intestinal epithelial barrier in health and disease. Monogr Pathol 31:306–324
Matter K, Mellman I (1994) Mechanisms of cell polarity: sorting and transport in epithelial cells. Curr Opin Cell Biol 6:545–554
Maury J, Nicoletti C, Guzzo-Chambraud L, Maroux S (1995) The filamentous brush border glycocalyx, a mucin-like marker of enterocyte hyper-polarization. Eur J Biochem 228:323–331
Mayer L, Panja A, Li Y, Siden E, Pizzimenti A, Gerardi F, Chandswang N (1992) Unique features of antigen presentation in the intestine. Ann N Y Acad Sci 664:39–46
McDaniel RV, Sharp K, Brooks D, McLaughlin AC, Winiski AP, Cafiso D, McLaughlin S (1986) Electrokinetic and electrostatic properties of bilayers containing gangliosides GM1, GD1a or GT1. Comparison with a nonlinear theory. Biophys J 49:741–752
Mendelsohn CL, Wimmer E, Racaniello VR (1989) Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56:855–865
Mooseker M (1985) Organization, chemistry and assembly of the cytoskeletal apparatus of the intestinal brush border. Ann Rev Cell Biol 1:209–241
Morin MJ, Warner A, Fields BN (1994) A pathway for entry of reoviruses into the host through M cells of the respiratory tract. J Exp Med 180:1523–1527
Mostov KE, Cardone MH (1995) Regulation of protein traffic in polarized epithelial cells. Bioessays 17:129–138
Neutra M (1979) Linear arrays of intramembrane particles in microvilli in primate large intestine. Anat Rec 193:367–381
Neutra MR, Kraehenbuhl JP (1996) Antigen uptake by M cells for effective mucosal vaccines. In: Kiyono H, Kagnoff M, McGhee G (eds) Mucosal Vaccines. Academic Press, New York, pp 41–55
Neutra MR, Phillips TL, Mayer EL, Fishkind DJ (1987) Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer’s patch. Cell Tissue Res 247:537–546
Neutra MR, Wilson JM, Weltzin RA, Kraehenbuhl JP (1988) Membrane domains and macromolecular transport in intestinal epithelial cells. Am Rev Respir Dis 138:S10-S16
Neutra MR, Michetti P, Kraehenbuhl JP (1994) Secretory immunoglobulin A: induction, biogenesis and function. In: Johnson LR (ed) Physiology of the Gastrointestinal Tract. Raven Press, New York, pp 685–708
Neutra MR, Giannasca PJ, Giannasca KT, Kraehenbuhl J-P (1995) M cells and microbial pathogens. In: Blaser M, Smith PD, Ravdin JI, Greenberg HB, Guerrant RL (eds) Infections of the Gastrointestinal Tract. Raven Press, New York, pp 163–178
Neutra MR, Pringault E, Kraehenbuhl JP (1996a) Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol 14:275–300
Neutra MR, Frey A, Kraehenbuhl JP (1996b) Epithelial M cells: gateways for mucosal infection and immunization. Cell 86:345–348
Nibert ML, Furlong DB, Fields BN (1991) Mechanisms of viral pathogenesis. J Clin Invest 88:727–734
Orlandi PA, Critchley DR, Fishman PH (1994) The heat-labile enterotoxin of Escherichia coli binds to polytactosaminoglycan-containing receptors in Caco-2 human intestinal epithelial cells. Biochemistry 33:12886–12895
Owen RL (1977) Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer’s patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology 72:440–451
Owen RL, Bhalla DK (1983) Cytochemical analysis of alkaline phosphatase and esterase activities and of lectin-binding and anionic sites in rat and mouse Peyer’s patch M cells. Am J Anat 168:199–212
Owen RL, Pierce NF, Apple RT, Cray WCJ (1986) M cell transport of Vibrio cholerae from the intestinal lumen into Peyer’s patches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis 153:1108–1118
Owen RL, Bass DM, Piazza AJ (1990) Colonic lymphoid patches. A portal of entry in mice for type I reovirus administered anally. Gastroenterology 98:A468
Pappo J, Ermak TH (1989) Uptake and translocation of fluorescent latex particles by rabbit Peyer’s patch follicle epithelium: a quantitative model for M cell uptake. Clin Exp Immunol 76:144–148
Pappo J, Owen RL (1988) Absence of secretory component expression by epithelial cells overlying rabbit gut-associated lymphoid tissue. Gastroenterology 95:1173–1177
Pimplikar SW, Simons K (1993) Role of heterotrimeric G proteins in polarized membrane transport. J Cell Sci Suppl 17:27–32
Rosenshine I, Donnenberg MS, Kaper JB, Finlay BB (1992) Signal transduction between enteropathogenic Escherichia coli (EPEC) and epithelial cells: EPEC induces tyrosine phosphorylation of host cell proteins to initiate cytoskeletal rearrangement and bacterial uptake. EMBO J 11:3551–3560
Roy MJ, Varvayanis M (1987) Development of dome epithelium in gut-associated lymphoid tissues: association of IgA with M cells. Cell Tissue Res 248:645–651
Savidge TC, Smith MW (1995) Evidence that membranous (M) cell genesis is immunoregulated. In: Mestecky J (ed) Advances in Mucosal Immunology. Plenum, New York, pp 239–241
Savidge TC, Smith MW, James PS, Aldred P (1991) Salmonella-induced M-cell formation in germ-free mouse Peyer’s patch tissue. Am J Pathol 139:177–184
Schmidt GH, Wilkinson MM, Ponder BAJ (1985) Cell migration pathway in the intestinal epithelium: an in situ marker system using mouse aggregation chimeras. Cell 40:425–429
Semenza G (1986) Anchoring and biosynthesis of stalked brush border membrane glycoproteins. Annu Rev Cell Biol 2:255–314
Sicinski P, Rowinski J, Warchol JB, Jarzcabek Z, Gut W, Szczygiel B, Bielecki K, Koch G (1990) Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology 98:56–58
Siebers A, Finlay BB (1996) M cells and the pathogenesis of mucosal and systemic infections. Trends Microbiol 4:22–29
Sixma TK, Pronk SE, Kalk KH, Wartna ES, van Zanten BAM, Witholt B, Hoi WGJ (1991) Crystal structure of a cholera toxin-related heat-labile enterotoxin from E. coli. Nature 351:371–377
Smith MW, James PS, Tivey DR (1987) M cell numbers increase after transfer of SPF mice to a normal animal house environment. Am J Pathol 128:385–389
Uchida J (1987) An ultrastructural study on active uptake and transport of bacteria by microfold cells (M cells) to the lymphoid follicles in the rabbit appendix. J Clin Electron Microsc 20:379–394
Wagner N, Lohler J, Kunkel EJ, Ley K, Leung E, Krissansen G, Rajewsky K, Muller W (1996) Critical role for beta-7 integrins in formation of the gut-associated lymphoid tissue. Nature 382:366–370
Walker RI, Schauder-Chock EA, Parker JL (1988) Selective association and transport of Campylobacter jejuni through M cells of rabbit Peyer’s patches. Can J Microbiol 34:1142–1147
Wassef JS, Keren DF, Mailloux JL (1989) Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of Shigellosis. Infect Immun 57:858–863
Weltzin RA, Lucia Jandris P, Michetti P, Fields BN, Kraehenbuhl JP, Neutra MR (1989) Binding and transepithelial transport of immunoglobulins by intestinal M cells: demonstration using monoclonal IgA antibodies against enteric viral proteins. J Cell Biol 108:1673–1685
Winner LS III, Mack J, Weltzin RA, Mekalanos J J, Kraehenbuhl JP, Neutra MR (1991) New model for analysis of mucosal immunity: intestinal secretion of specific monoclonal immunoglobulin A from hybridoma tumors protects against Vibrio cholerae infection. Infect Immun 59:977–982
Wolf JL, Rubin DH, Finberg RS, Kauffman RS, Sharpe AH, Trier JS, Fields BN (1981) Intestinal M cells: a pathway for entry of reovirus into the host. Science 212:471–472
Zhou F, Kraehenbuhl JP, Neutra MR (1995) Mucosal IgA response to rectally administered antigen formulated in IgA-coated liposomes. Vaccine 13: 637–644
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Neutra, M.R. (1999). M Cells in Antigen Sampling in Mucosal Tissues. In: Kraehenbuhl, JP., Neutra, M.R. (eds) Defense of Mucosal Surfaces: Pathogenesis, Immunity and Vaccines. Current Topics in Microbiology and Immunology, vol 236. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-59951-4_2
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