Summary
M cells in Peyer's patch epithelium conduct transepithelial transport of luminal antigens to cells of the mucosal immune system. To determine the distribution of specific lectin-binding sites on luminal membranes of living M cells and to follow the transport route of membranebound molecules, lectin-ferritin conjugates and cationized ferritin were applied to rabbit Peyer's patch mucosa in vivo and in vitro. The degree to which binding enhances transport was estimated by comparing quantitatively the transport of an adherent probe, wheat germ agglutinin-ferritin, to that of a nonadherent BSA-colloidal gold probe. When applied to fixed tissue, the lectins tested bound equally well to M cells and columnar absorptive cells. On living mucosa, however, ferritin conjugates of wheat germ agglutinin and Ricinus communis agglutinins I and II bound more avidly to M cells. Absorptive cells conducted little uptake and no detectable transepithelial transport. Lectins on M cell membranes were endocytosed from coated pits, rapidly transported in a complex system of tubulocisternae and vesicles, and remained adherent to M cell basolateral membranes. Cationized ferritin adhered to anionic sites and was similarly transported, but was released as free clusters at M cell basolateral surfaces. When applied simultaneously to Peyer's patch mucosa, wheat germ agglutinin-ferritin was transported about 50 times more efficiently than was bovine serum albumin-colloidal gold.
Similar content being viewed by others
References
Abrahamson DR, Rodewald R (1981) Evidence for the sorting of endocytic vesicle contents during the receptor mediated transport of IgG across the new born rat intestine. J Cell Biol 91:270–280
Anderson RGW, Kaplan J (1983) Receptor-mediated endocytosis. In: Satir B (ed) Modern Cell Biology. Alan R. Liss, New York, pp 1–52
Bhalla DK, Owen RL (1983) Migration of B and T lymphocytes to M cells in Peyer's patch follicle epithelium: an autoradiographic and immunocytochemical study in mice. Cell Immunol 81:105–117
Bienenstock J (1982) Gut and bronchus-associated lymphoid tissue: An overview. In: Nieuwenhuis P (ed) In Vivo Immunology. Plenum, New York, pp 471–477
Bienenstock J, Befus D (1984) Gut- and bronchus-associated lymphoid tissue. Am J Anat 170:437–445
Bockman DE, Cooper MD (1973) Pinocytosis by epithelium associated with lymphoid follicles in the Bursa of Fabricus, appendix and Peyer's patches. An electron microscopic study. Am J Anat 136:455–478
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
Ducroc R, Heyman M, Beaufrere B, Morgat JL, Desjeux JF (1983) Horseradish peroxidase transport across rabbit jejunum and Peyer's patches in vitro. Am J Physiol 245:G54-G58
Frei PC, Benacerraf B, Thorbecke GJ (1965) Phagocytosis of the antigen, a crucial step in the induction of the primary immune response. Proc Natl Acad Sci USA 53:20–23
Frens G (1973) Controlled nucleation for the regulation of particle size in monodisperse gold solutions. Nature (Physical Science) 241:20–22
Goldstein U, Hayes CE (1978) The lectins: carbohydrate-binding proteins of plants and animals. In: Tipson RS, Horton D (eds) Advances in Carbohydrate Chemistry and Biochemistry. Academic Press, New York, Vol. 35, p 214–224
Goodman SL, Hodges GM, Trjdosiewicz LK, Livingston DC (1981) Colloidal gold markers and probes for routine application in microscopy. J Microsc 123:201–213
Gonnella PG, Neutra MR (1984) Membrane-bound and fluidphase macromolecules enter separate prelysosomal compartments in absorptive cells of suckling rat ileum. J Cell Biol 99:909–917
Gonnella PA, Neutra MR (1985) Glycoconjugate distribution and mobility on absorptive cell apical membranes of suckling rat ileum in vivo. Anat Rec 213:520–528
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
Keljo DJ, Hamilton JR (1983) Quantitative determination of macromolecular transport rate across intestinal Peyer's patches. Am J Physiol 244:G637
Kerjaschki D, Noronha-Blob L, Sacktor B, Farquhar MG (1984) Microdomains of distinctive glycoprotein composition in the kidney proximal tubule brush border. J Cell Biol 98:1505–1513
Kirn YS, Morita A, Miura S, Sioddiqui B (1981) Structure of glycoconjugates of intestinal mucosal membranes: Role in bacterial adherence. In: Boedecker E (ed) Attachment of Microorganisms to the Gut Mucosa. CRC Press, Boca Raton, Vol 2 p 99
King B (1982) The role of coated vesicles in selective transfer across yolk sac epithelium. J Ultrastruct Res 79:273–284
Lefevre ME, Olivo R, Vanderhoff JW, Joel DD (1978) Accumulation of latex in Peyer's patches and its subsequent appearance in villi and mesenteric lymph nodes. Proc Soc Exp Biol Med 159:298
Mayrhofer G (1984) Physiology of the intestinal immune system. In: Newby TRJ, Stokes CR (eds) Local Immune Responses of the Gut. CRC Press, Boca Raton, pp 1–96
Neutra MR, Guerina NG, Hall TL, Nicolson GL (1982) Transport of membrane-bound macromolecules by M cells in rabbit intestine. Gastroenterology 82:1137
Neutra MR, Ceichanover LA, Owen LS, Lodish HF (1985) Intracellular transport of transferrin- and asialoorosomucoid-gold conjugates to lysosomes after receptor-mediated endocytosis. J Histochem Cytochem 33:1134–1144
Ngan J, Kind LS (1978) Suppressor T cells for IgE and IgG in Peyer's patches of mice made tolerant by the oral administration of ovalbumin. J Immunol 120:861–865
Nicolson GL, Singer SJ (1971) Ferritin-conjugated plant agglutinins as specific saccharide stains for electron microscopy: application to saccharides bound to cell membranes. Proc Natl Acad Sci USA 65:942–945
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, Jones AL (1974) Epithelial cell specialization within human Peyer's patches: Ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66:189–203
Owen RL, Apple RT, Bhalla DK (1981) Cytochemical identification and morphometric analysis of lysosomes in “M” cells and adjacent columnar cells of rat Peyer's patches. Gastroenterology [Abstr] 80:1246
Owen RL, Pierce NF, Cray WE Jr (1983) Autoradiographic analysis of M cell uptake and transport of Cholera vibrios into follicles of rabbit Peyer's patches. Gastroenterology [Abstr] 84:1267
Richman LK, Chiller JM, Brown WR, Hanson DG, Vuz NM (1978) Enterically induced immunologic tolerance. 1. Induction of suppressor T lymphocytes by intragastric administration of soluble proteins. J Immunol 121:2429–2434
Richman LK, Graeff AS, Strober W (1981) Antigen presentation by macrophage-enriched cells from the mouse Peyer's patch. Cell Immunol 62:110–118
Richman LK, Graeff AS, Yarchoan R, Strober W (1981) Simultaneous induction of antigen-specific IgA helper T cells and IgG suppressor T cells in the murine Peyer's patch after protein feeding. J Immunol 126:2079–2083
Rodewald R (1980) Distribution of immunoglobulin G receptors in the small intestine of the young rat. J Cell Biol 85:18–32
Shimizu Y, Andrew W (1967) Studies on the rabbit appendix. I. Lymphocytoepithelial relations and the transport of bacteria from lumen to lymphoid nodule. J Morphol 123:231–250
Skutelsky E, Danon D (1976) Redistribution of surface anionic sites on the luminal front of blood vessel endothelium after interaction with polycationic ligand. J Cell Biol 71:232–241
Steinman RM, Mellman IS, Muller WA, Cohn ZA (1983) Endocytosis and the recycling of plasma membrane. J Cell Biol 96:1–28
Stokes CR (1984) Induction and control of intestinal immune responses. In: Newby TJ, Stokes CR (eds) Local Immune Responses of the Gut. CRC Press, Boca Raton pp 97–142
Thomas HC, Parrott DMV (1974) The induction of tolerance to a soluble protein antigen by oral administration. Immunology 27:631–639
Wolf JL, Rubin DH, Finberg R, 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
Wolf JL, Kauffman RS, Finberg R, Dambrauskas R, Fields BN, Trier JS (1983) Determinants of reovirus interaction with the intestinal M cells and absorptive cells of murine intestine. Gastroenterology 85:291–300
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Neutra, M.R., Phillips, T.L., Mayer, E.L. et al. Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer's patch. Cell Tissue Res. 247, 537–546 (1987). https://doi.org/10.1007/BF00215747
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00215747