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Cell and Tissue Research

, Volume 319, Issue 3, pp 395–404 | Cite as

Differentiation of the follicle-associated epithelium in ileal Peyer’s patch and production of 50-nm particles are maintained in B-cell-depleted fetal sheep

  • K.-I. LieEmail author
  • C. M. Press
  • P. McCullagh
  • S. J. McClure
  • T. Landsverk
Regular Article

Abstract

To evaluate the dependence of the differentiation of the follicle-associated epithelium (FAE) on the presence of follicular B-cells, the FAE of ileal Peyer’s patch follicles was examined in B-cell-depleted fetal lambs. The FAE of these rudimentary follicles, which are devoid of lymphocytes, showed normal differentiation, including carbonic anhydrase reactivity and ultrastructural characteristics of transcytosis, extensive interdigitation of the lateral plasma membrane and the shedding of membrane-bounded particles, approximately 50 nm in size, resembling exosomes. These 50-nm membrane-bounded particles were abundant in the extracellular space of the epithelium and the dome but no particles were found in the rudimentary follicles. This study confirms that the rudimentary follicles consist of clusters of follicular dendritic cells. Our findings suggest that the differentiation of FAE of ileal Peyer’s patch and the production of the 50-nm particles constitute features that appear to be independent of B-cells.

Keywords

Follicle-associated epithelium Anti-IgM Ileal Peyer’s patch Sheep (Merino and Norwegian Dala) 

Notes

Acknowledgements

The authors thank Ingjerd Andersen and Else Engeland for their skilful technical assistance.

References

  1. Aleksandersen M, Lie K-I, Gjerde B, Landsverk T (2002) Lymphocyte depletion in ileal Peyer’s patch follicles in lambs infected with Eimeria ovinoidalis. Clin Diagn Lab Immunol 9:83–91CrossRefPubMedGoogle Scholar
  2. Alitheen N, McClure S, McCullagh P (2001) Segregation of B lymphocytes into stationary apoptotic and migratory proliferating subpopulations in agglomerate cultures with ileal epithelium. Eur J Immunol 31:2558–2565Google Scholar
  3. Beh KJ (1988) Monoclonal antibodies against sheep immunoglobulin light chain, IgM and IgA. Vet Immunol Immunopathol 18:19–27CrossRefPubMedGoogle Scholar
  4. Charlton KA, Moyle S, Porter AJ, Harris WJ (2000) Analysis of the diversity of a sheep antibody repertoire as revealed from a bacteriophage display library. J Immunol 164:6221–6229Google Scholar
  5. Collas P, Cline R, Landsverk HB, Hein WR, Goldsby RA, Osborne BA, Landsverk T (2002) DNA-containing extracellular 50-nm particles in the ileal Peyer’s patch of sheep. Eur J Cell Biol 81:69–76PubMedGoogle Scholar
  6. Debard N, Sierro F, Kraehenbuhl JP (1999) Development of Peyer’s patches, follicle-associated epithelium and M cell: lessons from immunodeficient and knockout mice. Semin Immunol 11:183–191Google Scholar
  7. Debard N, Sierro F, Browning J, Kraehenbuhl JP (2001) Effect of mature lymphocytes and lymphotoxin on the development of the follicle-associated epithelium and M cells in mouse Peyer’s patches. Gastroenterology 120:1173–1182PubMedGoogle Scholar
  8. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 273:20121–20127Google Scholar
  9. Golovkina TV, Shlomchik M, Hannum L, Chervonsky A (1999) Organogenic role of B lymphocytes in mucosal immunity. Science 286:1965–1968CrossRefPubMedGoogle Scholar
  10. Griebel PJ, Hein WR (1996) Expanding the role of Peyer’s patches in B-cell ontogeny. Immunol Today 17:30–39Google Scholar
  11. Hein WR, Dudler L (1999) Diversification of sheep immunoglobulins. Vet Immunol Immunopathol 72:17–20Google Scholar
  12. Karlsson M, Lundin S, Dahlgren U, Kahu H, Pettersson I, Telemo E (2001) “Tolerosomes” are produced by intestinal epithelial cells. Eur J Immunol 31:2892–2900Google Scholar
  13. Kazimierczak J, Sommer EW, Philippe E, Droz B (1986) Carbonic anhydrase activity in primary sensory neurons. I. Requirements for the cytochemical localization in the dorsal root ganglion of chicken and mouse by light and electron microscopy. Cell Tissue Res 245:487–495PubMedGoogle Scholar
  14. 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 277:949–952CrossRefPubMedGoogle Scholar
  15. Landsverk T (1981) The epithelium covering Peyer’s patches in young milk-fed calves. An ultrastructural and enzyme histochemical investigation. Acta Vet Scand 22:198–210PubMedGoogle Scholar
  16. Landsverk T (1987) The follicle-associated epithelium of the ileal Peyer’s patch in ruminants is distinguished by its shedding of 50 nm particles. Immunol Cell Biol 65:251–261PubMedGoogle Scholar
  17. Landsverk T, Jansson A, Nicander L, Ploen L (1987) Carbonic anhydrase—a marker for particles shed from the epithelium to the lymphoid follicles of the ileal Peyer’s patch in goat kids and lambs. Immunol Cell Biol 65:425–429Google Scholar
  18. Landsverk T, Trevella W, Nicander L (1990a) Transfer of carbonic anhydrase-positive particles from the follicle-associated epithelium to lymphocytes of Peyer’s patches in foetal sheep and lambs. Cell Tissue Res 261:239–247PubMedGoogle Scholar
  19. Landsverk T, Lium B, Matovelo JA, Liven E, Nordstoga K (1990b) Peyer’s patches in experimental Salmonella dublin infection in calves. Microvascular and epithelial changes contributing to atrophy of lymphoid follicles. Acta Pathol Microbiol Immunol Scand 98:255–268Google Scholar
  20. McCullagh P, Press CM, McClure SJ, Larsen HJ, Landsverk T (2003) The effect of dosage, gestational age and splenectomy on anti-IgM interception of prenatal B-cell development in sheep. Clin Dev Immunol 10:19–26CrossRefPubMedGoogle Scholar
  21. Murk J-L, Stoorvogel W, Kleijmeer MJ, Geuze HJ (2002) The plasticity of multivesicular bodies and the regulation of antigen presentation. Semin Cell Dev Biol 13:303–311CrossRefPubMedGoogle Scholar
  22. Nicander L, Halleraker M, Landsverk T (1991) Ontogeny of reticular cells in the ileal Peyer’s patch of sheep and goats. Am J Anat 191:237–249PubMedGoogle Scholar
  23. van Niel G, Raposo G, Candalh C, Boussac M, Hershberg R, Cerf-Bensussan N, Heyman M (2001) Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 121:337–349PubMedGoogle Scholar
  24. 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 72:440–451PubMedGoogle Scholar
  25. Owen RL, Jones AL (1974) Epithelial cell specialization within human Peyer’s patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66:189–203PubMedGoogle Scholar
  26. Press CM, McClure SJ, Landsverk T (1991) Computer-assisted morphometric analysis of absorptive and follicle-associated epithelia of Peyer’s patches in sheep foetuses and lambs indicates the presence of distinct T- and B-cell components. Immunology 72:386–392PubMedGoogle Scholar
  27. Press CM, Halleraker M, Landsverk T (1992) Ontogeny of leukocyte populations in the ileal Peyer’s patch of sheep. Dev Comp Immunol 16:229–241CrossRefPubMedGoogle Scholar
  28. Press CM, Reynolds JD, McClure SJ, Simpson-Morgan MW, Landsverk T (1996) Fetal lambs are depleted of IgM+ cells following a single injection of an anti-IgM antibody early in gestation. Immunology 88:28–34CrossRefPubMedGoogle Scholar
  29. Press CM, Reynolds JD, McClure SJ, Landsverk T (1998) Development of accessory cells in B-cell compartments is retarded in B-cell-depleted fetal sheep. Dev Immunol 6:223–231PubMedGoogle Scholar
  30. Prinz M, Huber G, Macpherson AJ, Heppner FL, Glatzel M, Eugster HP, Wagner N, Aguzzi A (2003) Oral prion infection requires normal numbers of Peyer’s patches but not of enteric lymphocytes. Am J Pathol 162:1103–1111PubMedGoogle Scholar
  31. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183:1161–1172CrossRefPubMedGoogle Scholar
  32. Reynaud C-A, Mackay CR, Muller RG, Weill J-C (1991) Somatic generation of diversity in a mammalian primary lymphoid organ: the sheep ileal Peyer’s patches. Cell 64:995–1005CrossRefPubMedGoogle Scholar
  33. Reynolds JD (1987) Peyer’s patches and the early development of B lymphocytes. Curr Top Microbiol Immunol 135:43–56PubMedGoogle Scholar
  34. Reynolds JD (1997) The genesis, tutelage and exodus of B cells in the ileal Peyer’s patch of sheep. Int Rev Immunol 15:265–299PubMedGoogle Scholar
  35. Reynolds JD, Morris B (1983) The evolution and involution of Peyer’s patches in fetal and postnatal sheep. Eur J Immunol 13:627–635PubMedGoogle Scholar
  36. Ridderstråle Y (1976) Intracellular localization of carbonic anhydrase in the frog nephron. Acta Physiol Scand 98:465–469PubMedGoogle Scholar
  37. Sierro F, Pringault E, Assman PS, Kraehenbuhl JP, Debard N (2000) Transient expression of M-cell phenotype by enterocyte-like cells of the follicle-associated epithelium of mouse Peyer’s patches. Gastroenterology 119:734–743PubMedGoogle Scholar
  38. Simon-Assmann P, Kedinger M (1993) Heterotypic cellular cooperation in gut morphogenesis and differentiation. Semin Cell Biol 4:221–230CrossRefPubMedGoogle Scholar
  39. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G (2002) The biogenesis and functions of exosomes. Traffic 3:321–330CrossRefPubMedGoogle Scholar
  40. Tew JG, Wu J, Fakher M, Szakal AK, Qin D (2001) Follicular dendritic cells: beyond the necessity of T-cell help. Trends Immunol 22:361–367CrossRefPubMedGoogle Scholar
  41. Yancopoulos GD, Oltz EM, Rathbun G, Berman JE, Smith RK, Lansford RD, Rothman P, Okada A, Lee G, Morrow M, Kaplan K, Prockop S, Alt FW (1990) Isolation of coordinately regulated genes that are expressed in discrete stages of B-cell development. Proc Natl Acad Sci USA 87:5759–5763Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • K.-I. Lie
    • 1
    Email author
  • C. M. Press
    • 1
  • P. McCullagh
    • 2
  • S. J. McClure
    • 3
  • T. Landsverk
    • 1
  1. 1.Department of Basic Sciences and Aquatic MedicineNorwegian School of Veterinary ScienceOsloNorway
  2. 2.John Curtin School of Medical ResearchAustralian National UniversityCanberraAustralia
  3. 3.F.D. McMaster LaboratoryCSIRO Livestock IndustriesArmidaleAustralia

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