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. 2000 Apr;196(Pt 3):443–451. doi: 10.1046/j.1469-7580.2000.19630443.x

Ultrastructural study on the follicle-associated epithelium of nasal-associated lymphoid tissue in specific pathogen-free (SPF) and conventional environment-adapted (SPF-CV) rats

KWANG IL JEONG 1,✉, HODAKA SUZUKI 1, HIROYUKI NAKAYAMA 1, KUNIO DOI 1
PMCID: PMC1468080  PMID: 10853966

Abstract

Membranous (M) cells in follicle-associated epithelium (FAE) play an important role in the mucosal immunity through transport of a variety of foreign antigens to the underlying mucosa-associated lymphoid tissue (MALT). We aimed to investigate the ultrastructure of M cells in the FAE covering nasal-associated lymphoid tissue (NALT) both in specific pathogen-free (SPF) rats and in conventional environment-adapted (SPF-CV) rats aged 8–38 wk. In NALT of both SPF and SPF-CV rats, FAE included the nonciliated microvillous cell, which appears to be an analogue of M cell previously described in other MALT. In SPF rats, M cells increased in number only slightly with age, and they maintained morphological uniformity irrespective of age. In SPF-CV rats, M cells selectively increased in number resulting in prominent expansion of FAE surface area in parallel with the duration of maintenance in a conventional environment. In addition, M cells in SPF-CV rats showed heterogeneity in their surface morphology such as the length and number of microvilli and cell surface area and outline. In addition, the FAE was stratified by various subtypes of M cells, which were characterised by several subcellular alterations including the presence of many keratin filaments, homogeneous dark bodies and extensive cytoplasmic interfoliation with wide intercellular spaces filled with amorphous proteinaceous material. These characteristics of M cells in SPF-CV rat were intimately related with a preferential influx of immunocompetent cells into the FAE, which was not seen or was very rare in SPF rats irrespective of age. The results suggest the possibility that NALT may effectively carry out the mucosal immune response against antigenic stimuli of different magnitude through the unique dynamics of M cells which seem to be influenced by the infiltration of immunocompetent cells.

Keywords: NALT, M cells, structural heterogeneity, immune surveillance

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Selected References

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  1. Amerongen H. M., Weltzin R., Farnet C. M., Michetti P., Haseltine W. A., Neutra M. R. Transepithelial transport of HIV-1 by intestinal M cells: a mechanism for transmission of AIDS. J Acquir Immune Defic Syndr. 1991;4(8):760–765. [PubMed] [Google Scholar]
  2. Asanuma H., Thompson A. H., Iwasaki T., Sato Y., Inaba Y., Aizawa C., Kurata T., Tamura S. Isolation and characterization of mouse nasal-associated lymphoid tissue. J Immunol Methods. 1997 Mar 28;202(2):123–131. doi: 10.1016/s0022-1759(96)00243-8. [DOI] [PubMed] [Google Scholar]
  3. Bienenstock J., Johnston N., Perey D. Y. Bronchial lymphoid tissue. I. Morphologic characteristics. Lab Invest. 1973 Jun;28(6):686–692. [PubMed] [Google Scholar]
  4. Bockman D. E., Cooper M. D. Pinocytosis by epithelium associated with lymphoid follicles in the bursa of Fabricius, appendix, and Peyer's patches. An electron microscopic study. Am J Anat. 1973 Apr;136(4):455–477. doi: 10.1002/aja.1001360406. [DOI] [PubMed] [Google Scholar]
  5. Borghesi C., Regoli M., Bertelli E., Nicoletti C. Modifications of the follicle-associated epithelium by short-term exposure to a non-intestinal bacterium. J Pathol. 1996 Nov;180(3):326–332. doi: 10.1002/(SICI)1096-9896(199611)180:3<326::AID-PATH656>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
  6. Boysen M. The surface structure of the human nasal mucosa. I. Ciliated and metaplastic epithelium in normal individuals. A correlated study by scanning/transmission electron and light microscopy. Virchows Arch B Cell Pathol Incl Mol Pathol. 1982;40(3):279–294. [PubMed] [Google Scholar]
  7. Bye W. A., Allan C. H., Trier J. S. Structure, distribution, and origin of M cells in Peyer's patches of mouse ileum. Gastroenterology. 1984 May;86(5 Pt 1):789–801. [PubMed] [Google Scholar]
  8. Förster R., Mattis A. E., Kremmer E., Wolf E., Brem G., Lipp M. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell. 1996 Dec 13;87(6):1037–1047. doi: 10.1016/s0092-8674(00)81798-5. [DOI] [PubMed] [Google Scholar]
  9. Ichimiya I., Kawauchi H., Fujiyoshi T., Tanaka T., Mogi G. Distribution of immunocompetent cells in normal nasal mucosa: comparisons among germ-free, specific pathogen-free, and conventional mice. Ann Otol Rhinol Laryngol. 1991 Aug;100(8):638–642. doi: 10.1177/000348949110000807. [DOI] [PubMed] [Google Scholar]
  10. Jeong K. I., Uetsuka K., Nakayama H., Doi K. Glycoconjugate expression in follicle-associated epithelium (FAE) covering the nasal-associated lymphoid tissue (NALT) in specific pathogen-free and conventional rats. Exp Anim. 1999 Jan;48(1):23–29. doi: 10.1538/expanim.48.23. [DOI] [PubMed] [Google Scholar]
  11. Kernéis S., Bogdanova A., Kraehenbuhl J. P., Pringault E. Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria. Science. 1997 Aug 15;277(5328):949–952. doi: 10.1126/science.277.5328.949. [DOI] [PubMed] [Google Scholar]
  12. Mair T. S., Batten E. H., Stokes C. R., Bourne F. J. The histological features of the immune system of the equine respiratory tract. J Comp Pathol. 1987 Sep;97(5):575–586. doi: 10.1016/0021-9975(87)90008-9. [DOI] [PubMed] [Google Scholar]
  13. Morin M. J., Warner A., Fields B. N. A pathway for entry of reoviruses into the host through M cells of the respiratory tract. J Exp Med. 1994 Oct 1;180(4):1523–1527. doi: 10.1084/jem.180.4.1523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Owen R. L., Jones A. L. Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology. 1974 Feb;66(2):189–203. [PubMed] [Google Scholar]
  15. Owen R. L. Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology. 1977 Mar;72(3):440–451. [PubMed] [Google Scholar]
  16. Regoli M., Bertelli E., Borghesi C., Nicoletti C. Three-dimensional (3D-) reconstruction of M cells in rabbit Peyer's patches: definition of the intraepithelial compartment of the follicle-associated epithelium. Anat Rec. 1995 Sep;243(1):19–26. doi: 10.1002/ar.1092430104. [DOI] [PubMed] [Google Scholar]
  17. Regoli M., Borghesi C., Bertelli E., Nicoletti C. A morphological study of the lymphocyte traffic in Peyer's patches after an in vivo antigenic stimulation. Anat Rec. 1994 May;239(1):47–54. doi: 10.1002/ar.1092390106. [DOI] [PubMed] [Google Scholar]
  18. Savidge T. C., Smith M. W., James P. S., Aldred P. Salmonella-induced M-cell formation in germ-free mouse Peyer's patch tissue. Am J Pathol. 1991 Jul;139(1):177–184. [PMC free article] [PubMed] [Google Scholar]
  19. Siciński P., Rowiński J., Warchoł J. B., Jarzabek Z., Gut W., Szczygieł B., Bielecki K., Koch G. Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology. 1990 Jan;98(1):56–58. doi: 10.1016/0016-5085(90)91290-m. [DOI] [PubMed] [Google Scholar]
  20. Smith M. W., James P. S., Tivey D. R. M cell numbers increase after transfer of SPF mice to a normal animal house environment. Am J Pathol. 1987 Sep;128(3):385–389. [PMC free article] [PubMed] [Google Scholar]
  21. Smith M. W., Peacock M. A. "M" cell distribution in follicle-associated epithelium of mouse Peyer's patch. Am J Anat. 1980 Oct;159(2):167–175. doi: 10.1002/aja.1001590205. [DOI] [PubMed] [Google Scholar]
  22. Spit B. J., Hendriksen E. G., Bruijntjes J. P., Kuper C. F. Nasal lymphoid tissue in the rat. Cell Tissue Res. 1989 Jan;255(1):193–198. doi: 10.1007/BF00229081. [DOI] [PubMed] [Google Scholar]
  23. Wolf J. L., Kauffman R. S., Finberg R., Dambrauskas R., Fields B. N., Trier J. S. Determinants of reovirus interaction with the intestinal M cells and absorptive cells of murine intestine. Gastroenterology. 1983 Aug;85(2):291–300. [PubMed] [Google Scholar]

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