Transepithelial Transport of Proteins by Intestinal Epithelial Cells

  • Marian R. Neutra
  • Jean-Pierre Kraehenbuhl
Part of the Pharmaceutical Biotechnology book series (PBIO, volume 4)

Abstract

The mucosal surface of the digestive tract is a vast surface area covered by a monolayer of epithelial cells, joined by tight junctions that provide an effective barrier to proteins and peptides. Epithelial cells play important roles in nutrition and mucosal immune defense apart from their simple function as a barrier, however, and some of these functions require transepithelial vesicular transport of intact macromolecules (Neutra and Kraehenbuhl, 1992). For example, a minority population of epithelial cells (the M cells) are highly specialized for import of antigens to the cells of the mucosal immune system, while a major population of diverse epithelial and glandular cells selectively export polymeric immunoglobulins onto mucosal surfaces. In this chapter, we will focus on the basic mechanisms of membrane traffic and the epithelial cell specializations that allow the epithelium in the intestine to function as a gatekeeper. In addition to controlling transepithelial transport of proteins from the lumen to the interstitial tissue of the mucosa, the intestinal epithelium fulfills other roles such as digestion and absorption of nutrients and maintenance of a functional barrier.

Keywords

Fractionation Luminal Macromolecule Microbe Prolactin 

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References

  1. Abrahamson, D. R., and Rodewald, R., 1981, Evidence for the sorting of endocytic vesicle contents during receptor-mediated transport of IgG across newborn rat intestine, J. Cell Biol. 91:270–280.PubMedCrossRefGoogle Scholar
  2. Achler, C., Filmer, D., Merte, C., and Drenckhahn, D., 1989, Role of microtubules in polarized delivery of apical membrane proteins to the brush border of the intestinal epithelium, J. Cell Biol. 109:179–189.PubMedCrossRefGoogle Scholar
  3. Allan, C.H., Meyrick, D. L., and Trier, J. S., 1992, M cells contain acidic compartments and express class II MHC determinants, Gastroenterology 102:A589.Google Scholar
  4. Alpers, D. H., 1975, Protein turnover in intestinal mucosal villus and crypt brush border membranes, Biochem. Biophys. Res. Commun. 75:130–135.CrossRefGoogle Scholar
  5. Amerongen, H. M., Mack, J. A., Wilson, J. M., and Neutra, M. R., 1989, Membrane domains of intestinal epithelial cells: Distribution of Na+,K+-ATPase and the membrane skeleton in adult rat intestine, during fetal development, and after epithelial isolation, J. Cell Biol. 109:2129–2138.PubMedCrossRefGoogle Scholar
  6. Amerongen, H. M., Weltzin, R. A., Farnet, C. M., Michetti, P., Haseltine, W. A., and Neutra, M. R., 1991, Transepithelial transport of HIV-1 by intestinal M cells: A mechanism for transmission of AIDS, J. Acquir. Immune Defic. Syndr. 4:760–765.PubMedGoogle Scholar
  7. Anderson, R. G. W., 1991, Molecular motors that shape endocytic membrane, in: Intracellular Trafficking of Proteins (C. J. Steer and J. A. Hanover, eds.), Cambridge University Press, London, pp. 13–46.Google Scholar
  8. Apodaca, G., Bomsel, M., Arden, J., Breitfeld, P. P., Tang, K. C., and Mostov, K. E., 1991, The polymeric immunoglobulin receptor. A model protein to study transcytosis, J. Clin. Invest. 87:1877–1882.PubMedCrossRefGoogle Scholar
  9. Bacallao, R., Antony, C., Dotti, D., Karsenti, E., Stelzer, E. H., and Simons, K., 1989, The subcellular organization of Madin-Darby canine kidney cells during formation of a polarized epithelium, J. Cell Biol. 109:2817–2832.PubMedCrossRefGoogle Scholar
  10. Bartles, J. R., Feracci, H. M., Steiger, B., and Hubbard, A. L., 1987, Biogenesis of the rat hepatocyte plasma membrane in vivo: Comparison of the pathways taken by apical and basolateral proteins using subcellular fractionation, J. Cell Biol. 105:1241–1251.PubMedCrossRefGoogle Scholar
  11. Bass, D. M., and Greenberg, H. B., 1992, Strategies for the identification of icosahedral virus receptors, J. Clin. Invest. 89:3–9.PubMedCrossRefGoogle Scholar
  12. Bass, D. M., Trier, J. S., Dambrauskas, R., and Wolf, J. L., 1988, Reovirus type I infection of small intestinal epithelium in suckling mice and its effect on M cells, Lab. Invest. 58: 226–235.PubMedGoogle Scholar
  13. Bendayan, M., Ziv, E., Ben-Sasson, R., Bar-On, H., and Kidron, M., 1990, Morphocytochemical and biochemical evidence for insulin absorption by the rat ileal epithelium, Diabetologia 33:197–204.PubMedCrossRefGoogle Scholar
  14. Bland, P. W., and Warren, L. G., 1986, Antigen presentation by epithelial cells of the rat small intestine. II. Selective induction of suppressor T cells, Immunology 58:9–14.PubMedGoogle Scholar
  15. Bomsel, M., Prydz, K., Parton, R. G., Gruenberg, J., and Simons, K., 1989, Endocytosis in filter-grown Madin-Darby canine kidney cells, J. Cell Biol. 109:3243–3258.PubMedCrossRefGoogle Scholar
  16. Bomsel, M., Parton, R., Kuznetsov, S. A., Schroer, T. A., and Gruenberg, J., 1990, Microtubule-and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells, Cell 62:719–731.PubMedCrossRefGoogle Scholar
  17. Brandli, A. W., Parton, R. G., and Simons, K., 1990, Transcytosis in MDCK cells: Identification of glycoproteins transported bidirectionally between both plasma membrane domains, J. Cell Biol. 111:2909–2921.PubMedCrossRefGoogle Scholar
  18. Braun, M., Waheed, A., and von Figura, K., 1989, Lysosomal acid phosphatase is transported to lysosomes via the cell surface, EMBO J. 8:3633–3640.PubMedGoogle Scholar
  19. Breitfeld, P. P., Casanova, J. E., Simister, N. E., Ross, S. A., McKinnon, W. C., and Mostov, K. E., 1989a, Sorting signals, Curr. Opin. Cell Biol. 1:617–623.PubMedCrossRefGoogle Scholar
  20. Breitfeld, P. P., Harris, J. M., and Mostov, K. E., 1989b, Postendocytotic sorting of the ligand for the polymeric immunoglobulin receptor in Madin—Darby canine kidney cells, J. Cell Biol. 109:475–486.PubMedCrossRefGoogle Scholar
  21. Bye, W. A., Allen, C. H., and Trier, J. S., 1984, Structure, distribution and origin of M cells in Peyer’s patches of mouse ileum, Gastroenterology 86:789–801.PubMedGoogle Scholar
  22. Caplan, M. J., Anderson, H. C., Palade, G. E., and Jamieson, J. E., 1986, Intracellular sorting and polarized cell surface delivery of (Na+,K+)ATPase, an endogenous component of MDCK cell basolateral plasma membranes, Cell 46:623–631.PubMedCrossRefGoogle Scholar
  23. Casanova, J. E., Breitfeld, P. P., Ross, S. A., and Mostov, K. E., 1990, Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis, Science 248: 742–745.PubMedCrossRefGoogle Scholar
  24. Courtoy, P. J., 1991, Dissection of endosomes, in: Intracellular Trafficking of Proteins (C. J. Steer and J. A. Hanover, eds.), Cambridge University Press, London, pp. 103–156.Google Scholar
  25. Czerkinsky, C., Russell, M. W., Lycke, N., Lindblad, M., and Holmgren, J., 1989, Oral administration of a streptococcal antigen coupled to cholera toxin B subunit evokes strong antibody responses in salivary glands and extramucosal tissues, Infect. Immun. 57:1072–1077.PubMedGoogle Scholar
  26. DeAizpurua, H. J., and Russell-Jones, G. J., 1988, Oral vaccination: Identification of classes of proteins that provoke an immune response upon oral feeding, J. Exp. Med. 167:440–451.CrossRefGoogle Scholar
  27. Dertzbaugh, M. T., and Elson, C.O., 1991, Cholera toxin as a mucosal adjuvant, in: Topics in Vaccine Adjuvant Research (D. R. Spriggs and W. C. Koff, eds.), CRC Press, Boca Raton, Fla., pp. 119–132.Google Scholar
  28. Diment, S., and Stahl, P., 1985, Macrophage endosomes contain proteases which degrade endocytosed protein ligands, J. Biol. Chem. 260:15311–15317.PubMedGoogle Scholar
  29. Dragsten, P. R., Blumenthal, R., and Handler, J. S., 1981, Membrane asymmetry in epithelia: Is the tight junction a barrier to diffusion in the plasma membrane? Nature 294:718–722.PubMedCrossRefGoogle Scholar
  30. Duroc, R., Heyman, M., Beaufrere, B., Morgat, J. L., and Desjeux, J. F., 1983, Horseradish peroxidase transport across rabbit jejunum and Peyer’s patches in vitro, Am. J. Physiol. 245:G54–G58.Google Scholar
  31. Eilers, U., Klumperman, J., and Hauri, H. P., 1989, Nocodazole, a microtubule-active drug, interferes with apical protein delivery in cultured intestinal epithelial cells (Caco-2), J. Cell Biol. 108:13–22.PubMedCrossRefGoogle Scholar
  32. Ermak, T. H., Steger, H. J., Strober, W., and Owen, L., 1989, M cells and granular mononuclear cells depleted of their lymphocytes by total lymphoid irradiation, Am. J. Pathol. 134:529–537.PubMedGoogle Scholar
  33. Ermak, T. H., Steger, H. J., and 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.PubMedGoogle Scholar
  34. Fujita, M., Reinhart, F., and Neutra, M., 1990, Convergence of apical and basolateral endocytic pathways at apical late endosomes in absorptive cells of suckling rat ileum, J. Cell Sci. 97:385–394.PubMedGoogle Scholar
  35. Geuze, H. J., Slot, J. W., Strous, G. J. A. M., Peppard, J., von Figura, K., Hasilik, A., and Schwartz, A. L., 1984, Intracellular receptor sorting during endocytosis: Comparative immunoelectron microscopy of multiple receptors in rat liver, Cell 37:195–204.PubMedCrossRefGoogle Scholar
  36. Geuze, H. J., Slot, J. W., and Schwartz, A. L., 1987, Membranes of sorting organelles display lateral heterogeneity in receptor distribution, J. Cell Biol. 104:1715–1723.PubMedCrossRefGoogle Scholar
  37. Godefroy, O., Huet, C., Blair, L. A. C., Sahuquillo-Merino, C., and Louvard, D., 1988, Differentiation properties of a clone isolated from the HT29 cell line (a human colon carcinoma): Polarized differentiation of histocompatibility antigens (HLA) and of transferrin receptors, Biol. Cell 63:41–56.PubMedGoogle Scholar
  38. Goldman, I. S., Jones, A. L., Hradek, G. T., and Huling, S., 1983, Hepatocyte handling of immunoglobulin A in the rat: The role of microtubules, Gastroenterology 85:130–140.PubMedGoogle Scholar
  39. Gonnella, P. A., and Neutra, M. R., 1984, Membrane-bound and fluid-phase macromolecules enter separate prelysosomal compartments in absorptive cells of suckling rat ileum, J. Cell Biol. 99:909–917.PubMedCrossRefGoogle Scholar
  40. Gonnella, P. A., and Neutra, M. R., 1985, Glycoconjugate distribution and mobility on apical membranes of absorptive cells of suckling rat ileum in vivo, Anat. Rec. 213:520–528.PubMedCrossRefGoogle Scholar
  41. Gonnella, P. A., Simonski, K., Murphy, R. A., and Neutra, M. R., 1987, Transepithelial transport of epidermal growth factor by absorptive cells of suckling rat, J. Clin. Invest. 80: 22–32.PubMedCrossRefGoogle Scholar
  42. Gonnella, P. A., Harmatz, P., and Walker, W. A., 1989, Prolactin is transported across the epithelium of the jejunum and ileum of the suckling rat ileum, J. Cell Physiol. 140: 138–149.PubMedCrossRefGoogle Scholar
  43. Griffiths, G., Hoflack, B., Simons, K., Mellman, I., and Kornfeld, S., 1988, The mannose 6-phosphate receptor and the biogenesis of lysosomes, Cell 52:329–341.PubMedCrossRefGoogle Scholar
  44. Gruenberg, J., and Howell, K. E., 1989, Membrane traffic in endocytosis: Insights from cell free assays, Annu. Rev. Cell Biol. 5:453–481.PubMedCrossRefGoogle Scholar
  45. Gruenberg, J., Griffiths, G., and Howell, K. E., 1989, Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro, J. Cell Biol. 108:1301–1316.PubMedCrossRefGoogle Scholar
  46. Hansson, H. A., Lange, S., and Lonnvoth, I., 1984, Internalization in vivo of cholera toxin in the small intestine of the rat, Acta Pathol. Microbiol. Scand. 92:15–21.Google Scholar
  47. Heyman, M., Crain-Denoyelle, A. M., Nath, S. K., and Desjeux, J. F., 1990, Quantification of protein transcytosis in the human colon carcinoma cell line Caco-2, J. Cell Physiol. 143: 391–395.PubMedCrossRefGoogle Scholar
  48. Hidalgo, I. J., Raub, T. J., and Borchardt, R. T., 1989, Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability, Gastroenterology 96:736–749.PubMedGoogle Scholar
  49. Ho, N. F. H., Day, J. S., Barsuhn, C. L., Burton, P. S., and Raub, T. J., 1990, Biophysical model approaches to mechanistic transepithelial studies of peptides, J. Controlled Release 11: 3–24.CrossRefGoogle Scholar
  50. Hughson, E. J., and Hopkins, C. R., 1990, Endocytic pathways in polarized Caco-2 cells: Identification of an endosomal compartment accessible from both apical and basolateral surfaces, J. Cell Biol. 110:337–348.PubMedCrossRefGoogle Scholar
  51. Hunziker, W., and Mellman, I., 1989, Expression of macrophage—lymphocyte Fc receptors in Madin—Darby canine kidney cells: Polarity and transcytosis differ for isoforms with or without coated pit localization domains, J. Cell Biol. 109:3291–3302.PubMedCrossRefGoogle Scholar
  52. Hunziker, W., Male, P., and Mellman, I., 1990, Differential microtubule requirements for transcytosis in MDCK cells, EMBO J. 9:3515–3525.PubMedGoogle Scholar
  53. Hunziker, W., Harter, C., Matter, K., and Mellman, I., 1991a, Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant, Cell 66:907–920.PubMedCrossRefGoogle Scholar
  54. Hunziker, W., Whitney, J. A., and Mellman, I., 1991b, Selective inhibition of transcytosis by Brefeldin A in MDCK cells, Cell 67:617–628.PubMedCrossRefGoogle Scholar
  55. Inman, L. R., and Cantey, J. R., 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.PubMedCrossRefGoogle Scholar
  56. Israel, E. J., Simister, N., Freiberg, E., Hendren, R., and Walker, W. A., 1989, Immunoglobulin G binding sites on the human fetal intestine, Pediatr. Res. 25:116a.Google Scholar
  57. Kaiserlain, D., Vidal, K., and Revillard, J. P., 1989, Murine enterocytes can present soluble antigen to specific class II restricted CD4+ T cells, Eur. J. Immunol. 19:1513–1516.CrossRefGoogle Scholar
  58. Keljo, D. J., and Hamilton, J. R., 1983, Quantitative determination of macromolecular transport rate across intestinal Peyer’s patches, Am. J. Physiol. 244:G637–G644.PubMedGoogle Scholar
  59. Kelly, R. B., 1990, Microtubules, membrane traffic, and cell organization, Cell 61:5–7.PubMedCrossRefGoogle Scholar
  60. Kohbata, S., Yokobata, H., and 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.PubMedGoogle Scholar
  61. Kornfeld, S., and Mellman, I., 1989, The biogenesis of lysosomes, Annu. Rev. Cell Biol. 5: 483–525.PubMedCrossRefGoogle Scholar
  62. Kraehenbuhl, J. P., and Neutra, M. R., 1992, Molecular and cellular basis of immune protection of mucosal surfaces, Physiol. Rev. 70:853–879.Google Scholar
  63. Kraehenbuhl, J. P., Bron, C., and Sordat, B., 1979, Transfer of humoral secretory and cellular immunity from mother to offspring, Curr. Top. Pathol. 66:105–157.PubMedCrossRefGoogle Scholar
  64. Kuhn, L. C., and Kraehenbuhl, J. P., 1982, The sacrificial receptor—Translocation of polymeric IgA across epithelia, Trends Biochem. Sci. 7:299–302.CrossRefGoogle Scholar
  65. LeFevre, M. E., Olivo, R., and Joel, D. D., 1978, Accumulation of latex particles in Peyer’s patches and their subsequent appearance in villi and mesenteric lymph nodes, Proc. Soc. Exp. Biol. Med. 159:298–302.PubMedGoogle Scholar
  66. Lencer, W. E., Delp, C., Neutra, M. R., and Madara, J. L., 1992, Mechanism of cholera toxin action on a polarized human intestinal epithelial cell line: Role of vesicular traffic, J. Cell Biol. 117:1197–1210.PubMedCrossRefGoogle Scholar
  67. Levine, J. S., Allen, R. H., Alpers, D. H., and Seetheram, B., 1984, Immunocytochemical location of intrinsic factor—cobalamin receptors in dog ileum, J. Cell Biol. 98:1110–1117.CrossRefGoogle Scholar
  68. Lewis, V., Green, S. A., Marsh, M., Vihko Helenius, A., and Mellman, I., 1985, Glycoproteins of the lysosomal membrane, J. Cell Biol. 100:1839–1847.PubMedCrossRefGoogle Scholar
  69. Lippincott-Schwartz, J., and Fambrough, D. M., 1987, Cycling of the integral glycoprotein LEP 100 between plasma membrane and lysosomes: Kinetic and morphological analysis, Cell 49:669–677.PubMedCrossRefGoogle Scholar
  70. Louvard, D, Godefroy, O., Huet, C., Sahuquillo-Merino, C., Robine, S., and Coudrier, E., 1985, Basolateral membrane proteins are expressed at the surface of immature intestinal cells whereas transport of apical proteins is abortive, in: Current Communications in Molecular Biology, Protein Transport and Secretion (M. J. Gething, ed.), Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., pp. 168–173.Google Scholar
  71. Lycke, N., and Holmgren, J., 1986, Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens, Immunology 59:301–308.PubMedGoogle Scholar
  72. Madara, J. L., 1988, Tight junction dynamics: Is paracellular transport regulated? Cell 53: 497–498.PubMedCrossRefGoogle Scholar
  73. Madara, J. L., and Trier, J. S., 1987, Functional morphology of the mucosa of the small intestine, in: Physiology of the Gastrointestinal Tract (L. R. Johnson, ed.), Raven Press, New York, pp. 1209–1250.Google Scholar
  74. Massey, D., Feracci, H., Gorvel, J. P., Rigal, A., Soulie, J. M., and Maroux, S., 1987, Evidence for the transit of aminopeptidase N through the basolateral membrane before it reaches the brush border of enterocytes, J. Membr. Biol. 9:19–25.Google Scholar
  75. Matlin, K., Bainton, D. F., Pesonen, M., Louvard, D., Gent, N., and Simons, K., 1983, Transepithelial transport of a viral membrane glycoprotein implanted into the apical plasma membrane of MDCK cells. I. Morphological evidence, J. Cell Biol. 97:627–637.PubMedCrossRefGoogle Scholar
  76. Matter, K., Brauchbar, M., Bucher, K., and Hauri, H. P., 1990, Sorting of endogenous plasma membrane proteins occurs from two sites in cultured human intestinal epithelial cells (Caco-2), J. Cell Biol. 60:429–437.Google Scholar
  77. Maxfield, F. R., and Yamashiro, D. J., 1991, Acidification of organelles and the intracellular sorting of proteins during endocytosis, in: Intracellular Trafficking of Proteins (C. J. Steer and J. A. Hanover, eds.), Cambridge University Press, London, pp. 157–182.Google Scholar
  78. Mayer, L., Panja, A., and Li, Y., 1991, Antigen recognition in the gastrointestinal tract: Death to the dogma, Immunol. Res. 10:356–359.PubMedCrossRefGoogle Scholar
  79. Mayrhofer, G., 1984, Physiology of the intestinal immune system, in: Local Immune Responses of the Gut (T. J. Newby and C. R. Stokes, eds.), CRC Press, Boca Raton, Fla., pp. 1–96.Google Scholar
  80. Mooseker, M., 1985, Organization, chemistry and assembly of the cytoskeletal apparatus of the intestinal brush border, Annu. Rev. Cell Biol. 1:209–241.PubMedCrossRefGoogle Scholar
  81. Mostov, K. E., and Simister, N. E., 1985, Transcytosis, Cell 43:389–390.PubMedCrossRefGoogle Scholar
  82. Mostov, K. E., Friedlander, M., and Blobel, G., 1984, The receptor for transepithelial transport of IgA and IgM contains multiple immunoglobulin-like domains, Nature 308:37–43.PubMedCrossRefGoogle Scholar
  83. Moxey, P. C., and Trier, J. S., 1979, Development of villus absorptive cells in the human fetal small intestine: A morphological and morphometric study, Anat. Rec. 195:463–482.PubMedCrossRefGoogle Scholar
  84. Nabi, I. R., LeBivic, A., Fambrough, D., and Rodriguez-Boulan, E., 1991, An endogenous MDCK lysosomal membrane glycoprotein is targeted basolaterally before delivery to lysosomes, J. Cell Biol. 115:1573–1584.PubMedCrossRefGoogle Scholar
  85. Nelson, W. J., and Hammerton, R. W., 1989, A membrane—cytoskeletal complex containing Na+,K+-ATPase, ankyrin, and fodrin in Madin—Darby canine kidney (MDCK) cells: Implications for the biogenesis of epithelial cell polarity, J. Cell Biol. 108:893–902.PubMedCrossRefGoogle Scholar
  86. Neutra, M. R., 1988, The gastrointestinal tract, in: Cell and Tissue Biology (L. Weiss, ed.), Urban & Schwarzenberg, Munich, pp. 641–684.Google Scholar
  87. Neutra, M. R., and Kraehenbuhl, J. P., 1992, Transepithelial transport and mucosal defense, Trends Cell Biol. 2:134–138.PubMedCrossRefGoogle Scholar
  88. Neutra, M. R., and Louvard, D., 1989, Differentiation of intestinal cells in vitro, in: Functional Epithelial Cells in Culture (K. S. Matlin and J. D. Valentich, eds.), Liss, New York, pp. 363–398.Google Scholar
  89. Neutra, M. R., Phillips, T. L., Fishkind, D. J., and Mack, J. A., 1986, Membrane domains of the intestinal M cell, J. Cell Biol. 103:466a.Google Scholar
  90. Neutra, M. R., Phillips, T. L., Mayer, E. L., and Fishkind, D. J., 1987, Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer’s patch, Cell Tissue Res. 247:537–546.PubMedCrossRefGoogle Scholar
  91. Neutra, M. R., Wilson, J. M., Weltzin, R. A., and Kraehenbuhl, J. P., 1988, Membrane domains and macromolecular transport in intestinal epithelial cells, Am. Rev. Respir. Dis. 138:S10–S16.PubMedGoogle Scholar
  92. Nibert, M. L., Furlong, D. B., and Fields, B. N., 1991, Mechanisms of viral pathogenesis. Distinct forms of reoviruses and their roles during replication in cells and host, J. Clin. Invest. 88:727–734.PubMedCrossRefGoogle Scholar
  93. Owen, R. L., 1977, Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer’s patch in the normal unobstructed mouse intestine: An ultrastructural study, Gastroenterology 72:440–451.PubMedGoogle Scholar
  94. Owen, R. L., and Bhalla, D. K., 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.PubMedCrossRefGoogle Scholar
  95. Owen, R. L., Apple, R. T., and Bhalla, D. K., 1986a, Morphometric and cytochemical analysis of lysosomes in rat Peyer’s patch follicle epithelium: Their reduction in volume fraction and acid phosphatase content in M cells compared to adjacent enterocytes, Anat. Rec. 216: 521–527.PubMedCrossRefGoogle Scholar
  96. Owen, R. L., Pierce, N. F., Apple, R. T., and Cray, W. C., Jr., 1986b, 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.PubMedCrossRefGoogle Scholar
  97. Pappo, J., and Owen, R. L., 1988, Absence of secretory component expression by epithelial cells overlying rabbit gut-associated lymphoid tissue, Gastroenterology 95:1173–1177.PubMedGoogle Scholar
  98. Parton, R. G., Prydz, K., Bomsel, M., Simons, K., and Griffiths, G., 1989, Meeting of the apical and basolateral endocytic pathways of the Madin-Darby canine kidney cell in late endosomes, J. Cell Biol. 109:3259–3272.PubMedCrossRefGoogle Scholar
  99. Paul, R. W., Choi, A. H., and Lee, P. W., 1989, The alpha-anomeric form of sialic acid is the minimal receptor determinant recognized by reovirus, Virology 172:382–385.PubMedCrossRefGoogle Scholar
  100. Phillips, T. E., Phillips, T. H., and Neutra, M. R., 1987, Macromolecules can pass through occluding junctions of rat ileal epithelium during cholinergic stimulation, Cell Tissue Res. 247:547–554.PubMedCrossRefGoogle Scholar
  101. Prydz, K., Brandli, A. W., Bomsel, M., and Simons, K., 1990, Surface distribution of the mannose 6-phosphate receptors in epithelial Madin-Darby canine kidney cells, J. Biol. Chem. 265:12629–12635.PubMedGoogle Scholar
  102. Pusztai, A., 1989, Transport of proteins through the membranes of the adult gastrointestinal tract—A potential for drug delivery? Adv. Drug Deliv. Rev. 3:215–228.CrossRefGoogle Scholar
  103. Rabinowitz, S., Horstmann, H., Gordon, S., and Griffiths, G., 1992, Immunocytochemical characterization of the endocytic and phagolysosomal compartments in peritoneal macro-phages, J. Cell Biol. 116:95–112.PubMedCrossRefGoogle Scholar
  104. Rodewald, R., 1980, Distribution of immunoglobulin G receptors in the small intestine of the young rat, J. Cell Biol. 85:18–32.PubMedCrossRefGoogle Scholar
  105. Rodriguez-Boulan, E., and Nelson, W. J., 1989, Morphogenesis of the polarized epithelial cell phenotype, Science 245:718–725.PubMedCrossRefGoogle Scholar
  106. Roy, M. J., and Varvayanis, M., 1987, Development of dome epithelium in gut-associated lymphoid tissues: Association of IgA with M cells, Cell Tissue Res. 248:645–651.PubMedCrossRefGoogle Scholar
  107. Schaerer, E., Neutra, M. R., and Kraehenbuhl, J. P., 1991, Molecular and cellular mechanisms involved in transepithelial transport, J. Membr. Biol. 123:93–103.PubMedCrossRefGoogle Scholar
  108. Schmidt, G. H., Wilkinson, M. M., and Ponder, B. A. J., 1985, Cell migration pathway in the intestinal epithelium: An in situ marker system using mouse aggregation chimeras, Cell 40:425–429.PubMedCrossRefGoogle Scholar
  109. Schroer, T. A., and Sheetz, M. P., 1989, Role of kinesin and kinesin-associated proteins in organelle transport, in: Cell Movement (J. R. McIntosh and F. D. Warner, eds.), Liss, New York, pp. 295–306.Google Scholar
  110. Semenza, G., 1986, Anchoring and biosynthesis of stalked brush border membrane glycoproteins, Annu. Rev. Cell Biol. 2:255–314.PubMedCrossRefGoogle Scholar
  111. Sicinski, P., Rowinski, J., Warchol, J. B., Jarzcabek, Z., Gut, W., Szczygiel, B., Bielecki, K., and Koch, G., 1990, Poliovirus type 1 enters the human host through intestinal M cells, Gastroenterology 98:56–58.PubMedGoogle Scholar
  112. Siminoski, K., Gonnella, P., Bernanke, J., Owen, L., Neutra, M., and Murphy, R. A., 1986, Uptake and transepithelial transport of nerve growth factor in suckling rat ileum, J. Cell Biol. 103:1979–1990.PubMedCrossRefGoogle Scholar
  113. Simister, N. E., and Mostov, K. E., 1989, An Fc receptor structurally related to MHC class I antigens, Nature 337:184–187.PubMedCrossRefGoogle Scholar
  114. Slot, J. W., and Geuze, H. J., 1984, Transcytosis of IgA in duodenal epithelial cells observed by immunocytochemistry, J. Cell Biol. 99:7a.Google Scholar
  115. Smith, M. W., James, P. S., and Tivey, D. R., 1987, M cell numbers increase after transfer of SPF mice to a normal animal house environment, Am. J. Pathol. 128:385.PubMedGoogle Scholar
  116. Smith, P. L., Wall, D. A., Gochoco, C. H., and Wilson, G., 1992, Oral delivery of peptides and proteins, Adv. Drug Deliv. Rev. 8:253–290.CrossRefGoogle Scholar
  117. Specian, R. D., and Neutra, M. R., 1984, The cytoskeleton of intestinal goblet cells, Gastroenterology 87:1313–1325.PubMedGoogle Scholar
  118. Sztul, E., Kaplin, A., Saucan, L., and Palade, G., 1991, Protein traffic between distinct plasma membrane domains: Isolation and characterization of vesicular carriers involved in transcytosis, Cell 64:81–89.PubMedCrossRefGoogle Scholar
  119. Trahair, J. F., and Robinson, P. M., 1986, The development of the ovine small intestine, Anat. Rec. 214:294–303.PubMedCrossRefGoogle Scholar
  120. Trahair, J. F., and Robinson, P. M., 1989, Enterocyte ultrastructure and uptake of immunoglobulins in the small intestine of the neonatal lamb, J. Anat. 166:103–111.PubMedGoogle Scholar
  121. van der Sluijs, P., Bennett, M. K., Antony, C., Simons, K., and Kreis, T. E., 1990, Binding of exocytic vesicles from MDCK cells to microtubules in vitro, J. Cell Sci. 95:545–553.PubMedGoogle Scholar
  122. Wassef, J. S., Keren, D. F., and Mailloux, J. L., 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.PubMedGoogle Scholar
  123. Weinman, M. D., Allan, C. H., Trier, J. S., and Hagen, S. J., 1989, Repair of microvilli in the rat small intestine after damage with lectins contained in the red kidney bean, Gastroenterology 97:1193–1204.PubMedGoogle Scholar
  124. Weltzin, R. A., Lucia-Jandris, P., Michetti, P., Fields, B. N., and Kraehenbuhl, J. P., 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.PubMedCrossRefGoogle Scholar
  125. Wilson, J. M., Whitney, J. A., and Neutra, M. R., 1987, Identification of an endosomal antigen specific to absorptive cells of suckling rat ileum, J. Cell Biol. 105:691–703.PubMedCrossRefGoogle Scholar
  126. Winner, L. S., III, Mack, J., Weltzin, R. A., Mekalanos, J. J., Kraehenbuhl, J. P., and Neutra, M. R., 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.PubMedGoogle Scholar
  127. Wolf, J. L., Rubin, D. H., Finberg, R., Kauffman, R. S., Sharpe, A. H., Trier, J. S., and Fields, B. N., 1981, Intestinal M cells: A pathway for entry of reovirus into the host, Science 211: 471–472.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Marian R. Neutra
    • 1
  • Jean-Pierre Kraehenbuhl
    • 2
  1. 1.Gastrointestinal Cell Biology Laboratory, Children’s Hospital and Department of PediatricsHarvard Medical SchoolBostonUSA
  2. 2.Swiss Institute for Cancer Research and Institute of BiochemistryUniversity of LausanneEpalingesSwitzerland

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