Bacterial Characteristics and Follicle Surface Structure: Their Roles in Peyer’s Patch Uptake and Transport of Vibrio cholerae

  • Robert L. Owen
  • William C. CrayJr.
  • Thomas H. Ermak
  • Nathaniel F. Pierce
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 237)


Structural and functional specializations in the intestinal mucosal barrier over Peyer’s patches facilitate contact with and uptake of adherent luminal particles and soluble molecules. These specializations include local reduction in mucus-secreting goblet cells, interruption of the muscularis mucosae by lymphoid follicles(which may alter mucosal motility), and the presence of M cells. M cells are epithelial cells with irregular, widely spaced microvilli, reduced or absent lysosomes, an active transcellular transport system, and a pliable basolateral surface usually invaginated by lymphoid cells. At their luminal surfaces M cells form coated and uncoated vesicles, which are transported to intercellular spaces in the follicle epithelium where initial contact of intestinal antigen and lymphoid cells occurs. The mucus blanket which lies across the microvilli of enterocytes (intestinal absorptive cells) is broken over M cells, allowing microorganisms and particles to approach M cell luminal membranes. Studies with labeled lectins have demonstrated a thin but detectable glycocalyx coat on M cell membranes. Sugars detected by these lectins include beta-D-galactose (Ricinus communis agglutinin), sialic acid and N-acetyl-D-glucosamine (wheat germ agglutinin), but not alpha-D-mannose or alpha-D-glucose (Con A binds only sparsely). Cationized ferritin distributes evenly on M cell luminal membranes indicating that anionic sites are present.


Lymphoid Follicle Secretory Component Intestinal Mucosal Barrier Ricinus Communis Agglutinin Cell Microvillus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    R. L. Owen. 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 (1977).PubMedGoogle Scholar
  2. 2.
    R. L. Owen, N. F. Pierce, R. T. Apple, and W. C. Cray Jr., 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 (1986).PubMedCrossRefGoogle Scholar
  3. 3.
    R. L. Owen and D. K. Bhalla, Cytochemical analysis of alkaline phosphatase and esterase activities and of lectin-binding and anionic sites in rat and mouse Peyer’s patch M cells, Amer J Anat 168: 199 (1983).PubMedCrossRefGoogle Scholar
  4. 4.
    W. A. Bye, C. H. Allan, and J. S. Trier, Structure, distribution, and origin of M cells in Peyer’s patches of mouse ileum, Gastroenterology 86: 789 (1984).PubMedGoogle Scholar
  5. 5.
    M. R. Neutra, T. L. Phillips, E. L. Mayer, and D. J. Fishkind, Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer’s patch, Cell Tissue Res 247: 537 (1987).PubMedCrossRefGoogle Scholar
  6. 6.
    J. L. Wolf, R. S. Kauffman, R. Finberg, R. Dambrauskas, B. K. Fields, and J. S. Trier, Determinants of reovirus interaction with the intestinal M cells and absorptive cells of murine intestine, Gastroenterology 85: 291 (1983).PubMedGoogle Scholar
  7. 7.
    L. R. Inman and J. R. Cantey, Specific adherence of Escherichia lcoli (strain RDEC-1) to membranous (M) cells of the Peyer’s patch in Escherichia coli diarrhea in the rabbit, J Clin Invest 71: 1 (1983).PubMedCrossRefGoogle Scholar
  8. 8.
    Y. Fujimura, Functional morphology of microfold cells (M cells) in Peyer’s patches — phagocytosis and transport of BCG by M cells into rabbit Peyer’s patches, Gastroenterologie Japonica 21: 325 (1986).Google Scholar
  9. 9.
    M. A. Marcial and J. L. Madara, Cryptosporid ium: cellular localization, structural analysis of absorptive cell-parasite membrane-membrane interactions in guinea pigs, and suggestion of protozoan transport by M cells, Gastroenterology 90: 583 (1986).PubMedGoogle Scholar
  10. 10.
    R. L. Owen, R. T. Apple, and D. K. Bhalla, 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 (1986).PubMedCrossRefGoogle Scholar
  11. 11.
    R. L. Owen, N. F. Pierce, and W. C. Cray Jr., Effects of bacterial inactivation methods, toxin production and oral immunization on uptake of Vibrio cholerae by Peyer’s patch lymphoid follicles, in: “Advances in Research on Cholera and Related Diarrheas,” Vol. 4, S. Kuwahara and N. F. Pierce, eds., KTK Scientific. Publishers, Tokyo (1987).Google Scholar
  12. 12.
    S. Kohbata, H. Yokoyama, and E. Yabuuchi, 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 (1986).PubMedGoogle Scholar
  13. 13.
    N. F. Pierce, J. B. Kaper, J. J. Mekalanos, W. C. Cray Jr., and K. Richardson, Determinants of the immunogenieity of live virulent and mutant Vibrio cholerae 01 in rabbit intestine, Infect Immun 55: 477 (1987).PubMedGoogle Scholar
  14. 14.
    H. J. A. Egberts, J. F. J. G. Koninkx, J. F. van Dijk, and J. M. V. M. Mouwen, Biological and pathobiological aspects of the glycocalyx of the small intestinal epithelium, a review, Veterinary Quarterly 6: 186 (1984).CrossRefGoogle Scholar
  15. 15.
    J. Pappq, J. P. Kraehenbuhl, and R. L. Owen, Absence of expression of secretory component by epithelial cells overlying gut-associated lymphoid tissue, Clin Res 35: 190A (1987).Google Scholar
  16. 16.
    P. S. Carman and R. C. Povey, Pathogenesis of canine parvovirus-2 in dogs: histopathology and antigen identification in tissues, Res Vet Sci 38: 141 (1985).PubMedGoogle Scholar
  17. 17.
    G. N. Woode, J. F. Pohlenz, N. E. Kelso Gourley, and J. A. Fagerland, Astrovirus and Breda virus infections of dome cell epithelium of bovine ileum, J Clin Micro 19: 623 (1984).Google Scholar
  18. 18.
    T. H. Ermak and R. L. Owen, Differential distribution of lymphocytes and accessory cells in mouse Peyer’s patches, Anat Rec 215: 144 (1986).PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • Robert L. Owen
    • 1
  • William C. CrayJr.
    • 2
  • Thomas H. Ermak
    • 1
  • Nathaniel F. Pierce
    • 2
  1. 1.Intestinal Immunology Research CenterUniversity of California, San Francisco and Cell Biology and Aging Section (151E), Veterans Administration Medical CenterSan FranciscoUSA
  2. 2.Department of MedicineJohns Hopkins University School of Medicine and Francis Scott Key Medical CenterBaltimoreUSA

Personalised recommendations