Skip to main content
SpringerLink
Log in

Ultrastructural study of M cells from colonic lymphoid nodules obtained by colonoscopic biopsy

  • Original Articles
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

The present study was undertaken to investigate ultrastructurally the epithelium covering lymphoid nodules obtained from colonoscopic biopsies of the human colon and rectum. Colonoscopy using the dye spraying contrast, method was performed in nine patients who showed x-ray evidence of lymphonodular hyperplasia. Fifty-two colonoscopical biopsy specimens, of lymphoid nodules were obtained from the ascending, transverse, and descending colon and rectosigmoid region. All specimens were observed by light and electron microscopy. Light microscopy disclosed large lymphoid follicles protruding into the lumen with a “dome-type” configuration. These extended to the lamina propria of the mucosa and were associated with a massive lymphoid aggregation extending as far as the muscularis mucosa from the submucosa. The epithelium covering these nodules contained a few goblet cells and many lymphocytes. Observation of the elevated surface at the apex by scanning electron microscopy revealed M cells with sparse microvilli in the dome epithelium surrounded by crypts. Transmission electron microscopy disclosed M cells enfolding many immature or mature lymphocytes and plasmocytes. The M cells had cytoplasmic microvilli (so-called “microfolds”) on their surfaces, well-developed tubulovesicular systems, and vacuoles in the cytoplasm. The basic structure of the M cells as observed by scanning and transmission electron microscopy was the same as that of M cells in the Peyer's patches of humans and mice. The apical surface of the colonic lymphoid follicles in Crohn's disease patients was associated with erosions observed by scanning electron microscopy. The erosions proved to be the naked surface of the dome after removal of the epithelium and many holes from 2.0 to 6.0 μm in diameter were observed on the naked surface. At high magnification, lymphocytes were seen projecting from holes (18%) on the naked surface of the dome. These ultrastructural findings indicate that human colonic lymphoid follicles are very similar to those seen in other species.

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. Owen RL, Jones AL: Epithelial cell specialization within human Peyer's patches: An ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66:189–203, 1974

    Google Scholar 

  2. Owen RL: Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in neonatal unobstructed mouse intestine. Gastroenterology 72:440–451, 1977

    Google Scholar 

  3. Wolf JL, Rubin DH, Finberg R, Kauffman RS, Sharpe AH, Trier JS, Fields BN: Intestinal M cells: A pathway for entry of reovirus into the host. Science 212:471–472, 1981

    Google Scholar 

  4. Siciński P, Rowiński J, Warchol JB, Jarzabek S Gut W, Szczygie B, Bielecki, Koch G. Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology 98:56–58, 1990

    Google Scholar 

  5. Inman LR, Cantey JR: Specific adherence ofEscherichia coli (strain RDEC-1) to membranous (M) cells of the Peyer's patch inEscherichia coli diarrhea in the rabbit. J Clin Invest 71:1–8, 1983

    Google Scholar 

  6. Fujimura Y: 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 21:325–335, 1986

    Google Scholar 

  7. Kohbata S, Yokoyama H, Yabuuchi E: Cytopathogenic effect ofSalmonella typhi GIFU 10007 on M cells of murine ileal Peyer's patches in ligated ileal loop: An ultrastructural study. Microbiol Immunol 30:1225–1237, 1986

    Google Scholar 

  8. Owen RL, Pierce NF, Apple RT Cray WC Jr: M cell transport ofVibrio 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, 1986

    Google Scholar 

  9. Fujimura Y, Ohtani K, Kamoi R, Kato T, Kozuka K, Miyashima N, Uchida J, Kihara T, Mine H: An ultrastructural study of ileal invasion process ofYersinia, pseudotuberculosis in rabbits. J Clin Electron Microsc 22:712–713, 1989

    Google Scholar 

  10. Walker RI, Schmauder-Chock, Paker JL: Selective association and transport ofCampylobacter jejuni through M cells of rabbit Peyer's patches. Can J Microbiol 34:1142–1147, 1988

    Google Scholar 

  11. Wassef JS, Keren DF, Mailloux JL: Role of M cells in intestinal antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun 57:858–863, 1989

    Google Scholar 

  12. Grutzkau A, Hanski C, Hahn H, Riecken EO: Involvement of M cells in the bacterial invasion of Peyer's patches: A common mechanism shared byYersinia enterocolitica and other enteroinvasive bacteria Gut 31:1011–1015, 1990

    Google Scholar 

  13. Fujimura Y, Arita S, Kihara T: Uptake of BCG into immunized and nonimmunized rabbit Peyer's patches-morphology and quantitative analysis. Kawasaki Med J 16:181–190, 1990

    Google Scholar 

  14. O'Leary AD, Sweeney EC: Lymphoglandular complexes of the colon: Structure and distribution. Histopathology 10: 267–283, 1986

    Google Scholar 

  15. Jacob E, Backer SJ, Swaminathan SP: “M” cells in the follicle-associated epithelium of the human colon. Histopathology 11:941–952, 1987

    Google Scholar 

  16. Owen RL, Nemanic P: Antigen processing structures of the mammalian intestinal tract: An SEM study of lymphoepithelial organs. Scanning Electron Microsc Part II:367–378, 1978

    Google Scholar 

  17. Uchida J: Electron microscopic study of microfold cells (M cells) in normal and inflamed human appendix. Gastroenterol Jpn 23:251–262, 1988

    Google Scholar 

  18. Hoshi H, Mori T: Identification of the bursa-dependent and thymus-dependent areas in tonsilla caecalis of chickens. Tohoku J Exp Med 111:309–322, 1973

    Google Scholar 

  19. Atkins AM, Schofield GC: Lymphoglandular complexes in the large intestine of the dog. J Anat 113:169–178, 1972

    Google Scholar 

  20. Bland PW, Britton D: Morphological study of antigensampling structures in the rat large intestine. Infect Immun 43:693–699, 1984

    Google Scholar 

  21. Owen RL, Bass DM, Piazza AJ: Colonic lymphoid patches: A portal of entry in mice for type 1 reovirus administered anally. Gastroenterology 89:A468, 1990 (abstract)

    Google Scholar 

  22. Kealy WF: Colonic lymphoid-glandular complex (microbursa): Nature and morphology. J Clin Pathol 29:241–244, 1976

    Google Scholar 

  23. Tada M, Katoh S, Kohli Y, Kawai K: On the dye spraying method in colonofiberscopy. Endoscopy 8:70–74, 1976

    Google Scholar 

  24. Kelvin FM, Oddson TA, Rice RP, Garbutt JT, Bradenham BP: Double contrast barium enema in Crohn's disease and ulcerative colitis. Am J Roentgenol 131:207–213, 1978

    Google Scholar 

  25. Ell SR, Frank PH: Spectrum of lymphoid hyperplasia: Colonic manifestations sarcoidosis, infectious mononucleosis and Crohn's disease. Gastrointest Radiol 6:329–332, 1981

    Google Scholar 

  26. Kaplan B, Benson J, Rothstein F, Dahms B, Halpin T: Lymphonodular hyperplasia of the colon as a pathologic finding in children with lower gastrointestinal bleeding. J Pediatr Gastroenterol Nutr 3:704–708, 1984

    Google Scholar 

  27. Venkitachalam PS, Hirsch E, Elguezabal A, Littman L: Multiple lymphoid polyposis and familial polyposis of the colon: A genetic relationship. Dis Colon Rectum 21:336–341, 1978

    Google Scholar 

  28. De smet AA, Turbergen DG, Martel W: Nodular lymphoid hyperplasia of the colon associated with dysgammaglobulinemia. Am J Roentgenol 127:515–517, 1976

    Google Scholar 

  29. Crooks DJM, Brown WR: The distribution of intestinal nodular lymphoid hyperplasia in immunoglobulin deficiency. Clin Radiol 31:701–706, 1980

    Google Scholar 

  30. Brown RA, Glick SN, Teplick SK: Diffuse lymphoid follicles of the colon associated with colonic carcinoma. Am J Roentgenol 142:105–109, 1983

    Google Scholar 

  31. Burbige EJ, Sobky Reda ZF: Endoscopic appearance of colonic lymphoid nodules: A normal variant. Gastroenterology 72:524–526, 1977

    Google Scholar 

  32. Riddlesberger MM, Leventhal E: Nodular colonic mucosa of childhood: Normal or pathologic? Gastroenterology 79:265–270, 1980

    Google Scholar 

  33. Kenney PJ, Koehler RE, Shackelford GD: The clinical significance of large lymphoid follicles of the colon. Radiology 142:41–46, 1982

    Google Scholar 

  34. Laufer I, deSa D: Lymphoid follicular pattern: A normal feature of the pediatric colon.. Am J Roentgenol 130:51–55, 1978

    Google Scholar 

  35. Cornes JS: Number, size, and distribution of Peyer's patches in the human small intestine. Gut 6:225–233, 1965

    Google Scholar 

  36. Dukes C, Bussey HJR: The number of lymphoid follicles of the human large intestine. J Pathol Bacteriol 29:111–116 1926

    Google Scholar 

  37. Kelvin FM, Max RJ, Norton GA, Oddson TA, Rice RP, Thompson WM, Garbutt JT: Lymphoid follicular pattern of the colon in adults. Am J Roentgenol 133:821–825, 1979

    Google Scholar 

  38. Langman JM, Rowland R: The number and distribution of lymphoid follicles in the human large intestine. J Anat 194:189–194, 1986

    Google Scholar 

  39. Ahronheim GA: The transmission of AIDS. Nature 313:534, 1985

    Google Scholar 

  40. Evans BA, Dawson SG, Mclean KA, Teece SA, Key PR, Bond RA, Macrae KD, Jesson WJ, Mortimer PP: Sexual lifestyle and clinical findings related to HTLV-III/LAV status in homosexual men. Genitourin Med 62:384–389, 1986

    Google Scholar 

  41. Smith MW, Peacock MA: “M” cell distribution in follicleassociated epithelium of mouse Peyer's patch. Am J Anat 159:167–175, 1980

    Google Scholar 

  42. Smith MW, Peacock MA: Lymphocyte induced formation of antigen transporting “M” cells from fully differentiated mouse enterocytes.In Mechanisms of Intestinal Adaptation. JWL Robinson, RH Dowling, EO Riecken (eds). Lancaster, MTP Press, 1982, pp 573–583

    Google Scholar 

  43. Bhalla DK, Owen RL: Cell renewal and migration in lymphoid follicles of Peyer's patches, and cecum—an autoradiographic study in mice. Gastroenterology 82:232–242, 1982

    Google Scholar 

  44. Bye WA, Allan CH, Trier JS: Structure, distribution, and origin of M cells in Peyer's patches of mouse ileum. Gastroenterology 86:789–801, 1984

    Google Scholar 

  45. Fujimura Y, Kihara T, Ohtani K, Kamoi R, Kato T, Kozuka K, Miyashima N, Uchida J: Distribution of microfold cells (M cells) in human follicle-associated epithelium. Gastroenterol Jpn 25:130, 1990

    Google Scholar 

  46. Rickert RR, Carter HW: The “early” ulcerative lesion of Crohn's disease: Correlative light- and scanning electronmicroscopic studies. J Clin Gastroenterol 2:11–19, 1980

    Google Scholar 

  47. Crouse DA, Perry GA, Murphy BO, Sharp JG: Characteristics of submucosal lymphoid tissue located in the proximal colon of the rat. J Anat 162:53–65, 1989

    Google Scholar 

  48. Owen RL, Piazza AJ, Ermak TH: Ultrastructural and cytoarchitectural features of lymphoreticular organs in the colon and rectum of adult BALB/c mice. Am J Anat 190:10–18, 1991

    Google Scholar 

  49. Shimazui T: An ultrastructural study of the pathway and the location of migrating lymphocytes through the intestinal microfold cells (M cells). J Clin Electron Microsc 18:127–140, 1985

    Google Scholar 

  50. McClugage SG, Low FN, Zimny ML: Porsity, of the basement membrane overlying Peyer's patches in rats and monkeys. Gastroenterology 91:1128–1133, 1986

    Google Scholar 

  51. Cerf-Bensussan N, Quaroni A, Kurnick JT, Bhan AK: Intraepithelial lymphocytes modulate Ia expression by intestinal epithelial cells. J Immunol 132:2244–2251, 1984

    Google Scholar 

  52. Scott H, Solheim BG, Brandtzaeg P, Thorsby E: HLA-DR antigens in the epithelium of the human small intestine. Scand J Immunol 12:77–82, 1980

    Google Scholar 

  53. Natali PG, De Martino G, Quaranta V, Nicotra RM, Frezza F, Pellegrino MA, Ferrone S: Expression of Ia-like antigens in normal human nonlymphoid tissue. Transplantation 31:75–78, 1981

    Google Scholar 

  54. Hirata I, Austin LL, Blackwell WH, Weber JR, Dobbins WO III: Immunoelectron microscopic localization of HLA-DR antigen in control small intestine and colon and in inflammatory, bowel disease. Dig Dis Sci 31:1317–1330, 1986

    Google Scholar 

  55. Lynch HT, Frozen P, Schuelke GS: Hereditary colon cancer; polyposis and nonpolyposis variants. CA 35:95–114, 1985

    Google Scholar 

  56. Bland PW, Britton DC: Colonic lymphoid tissue and its influence on tumor induction in dimethylhydrazine-treated rats. Br J Cancer 4:275, 1981

    Google Scholar 

  57. Nauss KM, Locniskar M, Pavlina T, Newberne PM: Morphology and distribution of 1,2-dimethylhydrazine dihydrochloride-induced colon tumors and their relationship to gut-associated lymphoid tissue in the rat. J Natl Cancer Inst 73:915–924, 1984

    Google Scholar 

  58. Oohara T, Ogino A, Tohma H: Microscopic adenomas in non-polyposis coli: Incidence and relation to basal cells and lymphoid follicles. Dis Colon Rectum 24:120–126, 1981

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Gastroenterology, Department of Medicine, Kawasaki Medical School, 677 Matsushima, 701-01, Kurashiki, Okayama, Japan

    Yoshinori Fujimura MD, Masayo Hosobe MD & Tsuyoshi Kihara MD

Authors
  1. Yoshinori Fujimura MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masayo Hosobe MD
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tsuyoshi Kihara MD
    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

Fujimura, Y., Hosobe, M. & Kihara, T. Ultrastructural study of M cells from colonic lymphoid nodules obtained by colonoscopic biopsy. Digest Dis Sci 37, 1089–1098 (1992). https://doi.org/10.1007/BF01300292

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01300292

Key Words

Search

Navigation