Skip to main content
SpringerLink
Log in

Structural specializations for antigen uptake and processing in the digestive tract

  • Published:
Springer Seminars in Immunopathology Aims and scope Submit manuscript

Conclusions

Epithelial adaptations for antigen uptake and lymphoid organ cytoarchitecture differ according to the characteristics of specific sites throughout the mucosa but all facilitate antigen uptake. Whether surrounding mucosa is stratified squamous epithelium as in the oropharynx or columnar epithelium as in the intestine, organized lymphoid tissue in each area displays surface specializations which reduce local barriers and facilitate the approach and uptake of microorganisms, particles and macromolecules. In lymphoid tissue in each of these sites cellular defense mechanisms are arrayed for local containment, antigen processing and initiation of immune responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Abe K, Ito T (1977) A qualitative and quantitative morphologic study of Peyer's patches of the mouse. Arch Histol Jpn 40: 407

    Google Scholar 

  2. Anderson JC (1974) The response of the tonsil and associated lymph nodes of gnotobiotic piglets to the presence of bacterial antigen in the oral cavity. J Anat 117: 191

    Google Scholar 

  3. Bhalla DK, Owen RL (1982) Cell renewal and migration in lymphoid follicles of Peyer's patches and cecum — An autoradiographic study in mice. Gastroenterology 82: 232

    Google Scholar 

  4. Bhalla DK, Murakami T, Owen RL (1981) Microcirculation of intestinal lymphoid follicles in rat Peyer's patches. Gastroenterology 81: 481

    Google Scholar 

  5. Bland PW, Britton DC (1984) Morphological study of antigen-sampling structures in the rat large intestine. Infect Immun 43: 693

    Google Scholar 

  6. Bland PW, Warren LG (1986) Antigen presentation by epithelial cells of the rat small intestine. I. Kinetics, antigen specificity and blocking by anti-Ia antisera. Immunology 58: 1

    Google Scholar 

  7. Bland PW, Warren LG (1986) Antigen presentation by epithelial cells of the rat small intestine. II. Selective induction of suppressor T cells. Immunology 58: 9

    Google Scholar 

  8. 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

    Google Scholar 

  9. Bockman DE, Cooper MD (1975) Early lymphoepithelial relationships in human appendix: a combined light and electron microscopic study. Gastroenterology 68: 1160

    Google Scholar 

  10. Bockman DE (1983) Functional histology of appendix. Arch Histol Jpn 46: 271

    Google Scholar 

  11. Bye WA, Allan CH, Trier JS (1984) Structure, distribution and origin of M cells in Peyer's patches of mouse ileum. Gastroenterology 86: 789

    Google Scholar 

  12. Carlson JR, Owen RL (1987) Structure and functional role of Peyer's patches. In: MN Marsh (ed) Immunopathology of the small intestine. Wiley, Chichester, pp 21–40

    Google Scholar 

  13. Cornes JS (1965) Number, size and distribution of Peyer's patches in the human small intestine. I. The development of Peyer's patches. Gut 6: 225

    Google Scholar 

  14. Crouse DA, Perry GA, Murphy BO, Sharp JG (1989) Charcteristics of submucosal lymphoid tissue located in the proximal colon of the rat. J Anat 162: 53

    Google Scholar 

  15. Egberts HJA, Brinkhoff MGM, Mouwen JMVM (1985) Biology and pathology of the intestinal M-cell. A review. Vet Q 7: 333

    Google Scholar 

  16. Ermak TH, Owen RL (1986) Differential distribution of lymphocytes and accessory cells in mouse Peyer's patches. Anat Rec 215: 144

    Google Scholar 

  17. Ermak TH, Owen RL (1987) Phenotype and distribution of T cells in Peyer's patches of athymic mice. Histochemistry 87: 321

    Google Scholar 

  18. Ermak TH, Steger HJ, Owen RL, Heyworth MF (1988) Modulation of lymphocytes subsets in Peyer's patches of mice treated with monoclonal antibody against helper T cells. J Histochem Cytochem 36: 417

    Google Scholar 

  19. Ermak TH, Steger HJ, Owen RL, Strober S (1988) Depletion and repopulation of Peyer's patches from mice after total lymphoid irradiation. Lab Invest 59: 591

    Google Scholar 

  20. Ermak TH, Steger HJ, Strober S, Owen RL (1989) M cells and granular mononuclear cells in Peyer's patch domes of mice depleted of their lymphocytes by total lymphoid irradiation. Am J Pathol 134: 529

    Google Scholar 

  21. Fujikura S (1985) A study of Peyer's patch of the terminal ileum. Part 2: A clinico-statistical study. Gastroenterol Endosc Jpn 27: 326

    Google Scholar 

  22. Fujimura Y (1986) Functional morphology of microfold cells (M cells) in Peyer's patches — Phagocytosis and transport of BCG by M cells into rabbit Peyer's patches. Gastroenterol Jpn 21: 325

    Google Scholar 

  23. Geboes K, De Woolf-Peeters C, Rutgeerts P, Janssens J, Vantrappen G, Desmet V (1983) Lymphocytes and Langerhans cells in the human oesophageal epithelium. Virchows Arch [A] 401: 45

    Google Scholar 

  24. Ginsberg CH (1987) The independent function of the gastrointestinal immune system. Clin Aspects Autoimmun 2: 8

    Google Scholar 

  25. Gorgollón P (1978) The normal human appendix: a light and electron microscopic study. J Anat 126: 87

    Google Scholar 

  26. Howie AJ (1980) Scanning and transmission electron microscopy on the epithelium of human palatine tonsils. J Pathol 130: 91

    Google Scholar 

  27. Jacob E, Baker SJ, Swaminathan SP (1987) ‘M’ cells in the follicle-associated epithelium of the human colon. Histopathology 11: 941

    Google Scholar 

  28. Jalkanen S, Reichert RA, Gallatin WM, Bargatze RF, Weissman IL, Butcher EC (1986) Homing receptors and the control of lymphocyte migration. Immunol Rev 91: 39

    Google Scholar 

  29. Joel DD, Laissue JA, LeFevre ME (1978) Distribution and fate of ingested carbon particles in mice. J Reticuloendothel Soc 24: 477

    Google Scholar 

  30. Karchev T, Kabakchiev P (1982) Electron-microscope observations on the tonsillar epithelium in children with recurrent tonsilitis. Int J Pediatr Otorhinolaryngol 4: 149

    Google Scholar 

  31. Karchev T, Kabakchiev P (1984) M-cells in the epithelium of the nasopharyngeal tonsil. Rhinology 22: 201

    Google Scholar 

  32. Keljo DJ, Hamilton JR (1983) Quantitative determination of macromolecular transport rate across intestinal Peyer's patches. Am J Physiol 244: 637

    Google Scholar 

  33. Landsverk T (1981) The epithelium covering Peyer's patches in young milk-fed calves. An ultrastructural and enzyme histochemical investigation. Acta Vet Scand 22: 198

    Google Scholar 

  34. Landsverk T (1981) Peyer's patches and the follicle-associated epithelium in diarrheic calves. Pathomorphology, morphometry and acid phosphatase histochemistry. Acta Vet Scand 22: 459

    Google Scholar 

  35. LeFevre ME, Warren JB, Joel DD (1985) Particles and macrophages in murine Peyer's patches. Exp Cell Biology 53: 121

    Google Scholar 

  36. Madara JL, Bye WA, Trier JS (1984) Structural features of and cholesterol distribution in M-cell membranes in guinea pig, rat, and mouse Peyer's patches. Gastroenterology 87: 1091

    Google Scholar 

  37. Marcial MA, Madara JL (1986) Cryptosporidium: 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

    Google Scholar 

  38. McClugage SG, Low FN, Zimny ML (1986) Porosity of the basement membrane overlying Peyer's patches in rats and monkeys. Gastroenterology 91: 1128

    Google Scholar 

  39. Neutra MR, Hall 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

    Google Scholar 

  40. Ogawa K, Miyoshi M (1985) Intercellular spaces in the lymph nodule associated epithelium of the rabbit Peyer's patch and appendix. Arch Histol Jpn 48: 53

    Google Scholar 

  41. Ohtani O, Ohtsuka A, Owen RL (1986) Three-dimensional organization of the lymphatics in the rabbit appendix. A scanning electron and light microscopic study. Gastroenterology 91: 947

    Google Scholar 

  42. Ohtsuka A, Piazza AJ, Ermak TH, Owen RL (1989) Correlation of extracellular matrix components with cytoarchitecture of mouse Peyer's patches. Clin Res 37: 417A

  43. O'Leary AD, Sweeney EC (1986) Lymphoglandular complexes of the colon: structure and distribution. Histopathol 10: 267

    Google Scholar 

  44. 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

    Google Scholar 

  45. Owen RL, Bhalla DK (1983) Lympho-epithelial organs and lymph nodes. In: Hodges GM, Carr KE (eds) Biomedical research applications of scanning electron microscopy vol 3. Academic Press, London, pp 79–169

    Google Scholar 

  46. 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

    Google Scholar 

  47. Owen RL, Jones AL (1974) Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66: 189

    Google Scholar 

  48. Owen RL, Nemanic P (1978) Antigen processing structures of the mammalian intestinal tract: an SEM study of lymphoepithelial organs. Scanning Electron Microsc 2: 367

    Google Scholar 

  49. Owen RL, Allen CL, Stevens DP (1981) Phagocytosis of Giardia muris by macrophages in Peyer's patch epithelium in mice. Infect Immun 33: 591

    Google Scholar 

  50. Owen RL, Apple RT, Bhalla DK (1986) 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

    Google Scholar 

  51. Owen RL, Pierce NF, Apple RT, Cray WC (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

    Google Scholar 

  52. Owen RL, Pierce NF, Cray WC Jr (1988) Effects of bacterial inactivation methods, toxin production, and oral immunization on uptake of Vibrio cholerae by Peyer's patch lymphoid follicles. In: Kuwahara S, Pierce NF (eds) Advances in research on cholera and related diseases. KTK Scientific Publishers, Tokyo, pp 189–197

    Google Scholar 

  53. Pabst R (1987) The anatomical basis for the immune function of the gut. Anat Embryol (Berl) 176: 135

    Google Scholar 

  54. Pappo J (1989) Generation and characterization of monoclonal antibodies recognizing follicle epithelial M cells in rabbit gut-associated lymphoid tissue. Cell Immunol 120: 31

    Google Scholar 

  55. 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

    Google Scholar 

  56. Pappo J, Owen RL (1988) Absence of secretory component expression by epithelial cells overlying rabbit gut-associated lymphoid tissue. Gastroenterology 95: 1173

    Google Scholar 

  57. Pappo J, Owen RL (1988) The lymphoid system and immunologic defense of the digestive tract. In: Motto PM, Fujita H (eds) Ultrastructure of the digestive tract. Martinus Nijhoff, Boston, pp 181–199

    Google Scholar 

  58. Pappo J, Steger HJ, Owen RL (1988) Differential adherence of epithelium overlying gutassociated lymphoid tissue: an ultrastructural study. Lab Invest 58: 692

    Google Scholar 

  59. von Rosen L, Podjaski B, Bettman I, Otto HF (1981) Observations on the ultrastructure and function of the so-called “microfold” or “membraneous” cells (M cells) by means of peroxidase as a tracer. An experimental study with special attention to the physiological parameters of resorption. Virchows Arch [A] 390: 289

    Google Scholar 

  60. Rosner AJ, Keren DF (1984) Demonstration of M cells in the specialized follicle-associated epithelium overlying isolated lymphoid follicles in the gut. J Leukocyte Biol 35: 397

    Google Scholar 

  61. Roy M, Ruiz A, Varvayanis M (1987) A novel antigen is common to the dome epithelium of gut- and bronchus-associated lymphoid tissues. Cell Tissue Res 248: 635

    Google Scholar 

  62. 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

    Google Scholar 

  63. Smith MW, Peacock MA (1980) M cell distribution in follicle-associated epithelium of mouse Peyer's patches. Am J Anat 519: 167

    Google Scholar 

  64. 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

    Google Scholar 

  65. Sobhon P (1971) The light and electron microscopic studies of Peyer's patches in non germ-free adult mice. J Morphol 135: 457

    Google Scholar 

  66. Spalding DM, Koopman WJ, Eldridge JH, McGhee JR, Steinman RM (1983) Accessory cells in murine Peyer's patches. I. Identification and enrichment of a functional dendritic cell. J Exp Med 157: 1646

    Google Scholar 

  67. Spencer J, Finn T, Isaacson PG (1986) Human Peyer's patches: an immunohistochemical study. Gut 27: 405

    Google Scholar 

  68. Spencer J, MacDonald TT, Finn T, Isaacson PG (1986) The development of gut-associated lymphoid tissue in the terminal ileum of fetal human intestine. Clin Exp Immunol 64: 536

    Google Scholar 

  69. Tabata K, Ohtsuki H, Okabe S (1984) Role of lymphoid nodules in pathogenesis of indomethacin-induced gastric lesions in dogs. Digest Dis Sci 29: 346

    Google Scholar 

  70. Torres-Medina A (1981) Morphological characteristics of the epithelial surface of aggregated lymphoid follicles (Peyer's patches) in the small intestine of newborn gnotobiotic calves and pigs. Am J Vet Res 42: 232

    Google Scholar 

  71. Witmer MD, Steinman RM (1984) The anatomy of peripheral lymphoid organs with emphasis on accessory cells: light-microscopic immunocytochemical studies of mouse spleen, lymph node, and Peyer's patch. Am J Anat 170: 465

    Google Scholar 

  72. Wolf JL, Bye WA (1984) The membranous epithelial (M) cell and the mucosal immune system. Annu Rev Med 35: 95

    Google Scholar 

  73. 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

    Google Scholar 

  74. 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

    Google Scholar 

  75. Woode GN, Pohlenz JF, Kelso Gourley NE, Fagerland JA (1984) Astrovirus and Breda virus infections of dome cell epithelium of bovine ileum. J Clin Microsc 19: 623

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Medicine, University of California, San Francisco, USA

    Robert L. Owen & Thomas H. Ermak

  2. Cell Biology and Aging Section (151E), V. A. Medical Center, 94121, San Francisco, CA, USA

    Robert L. Owen & Thomas H. Ermak

Authors
  1. Robert L. Owen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas H. Ermak
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Owen, R.L., Ermak, T.H. Structural specializations for antigen uptake and processing in the digestive tract. Springer Semin Immunopathol 12, 139–152 (1990). https://doi.org/10.1007/BF00197502

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00197502

Keywords

Search

Navigation