M cells as portals of infection: Clinical and pathophysiological aspects

Infectious Agents and Disease

Volumn 5, Issue 3, 1996, Pages 144-156

  Fujimura, Yoshinori ^a,b   Owen, Robert L ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KAWASAKI MEDICAL SCHOOL   (Japan)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN; IMMUNOCOMPETENT CELL; INFECTION; LYMPH FOLLICLE; PATHOGENESIS; PATHOPHYSIOLOGY; PEYER PATCH; PRIORITY JOURNAL; REVIEW;

ANIMALS; ANTIGENS; APPENDIX; BRONCHI; COLON; CROHN DISEASE; EPITHELIUM; HIV INFECTIONS; HUMANS; INFECTION; INTESTINAL MUCOSA; LYMPHOID TISSUE; MUCOUS MEMBRANE; PEYER'S PATCHES; SALMONELLA INFECTIONS; TONSIL;

EID: 0029884377     PISSN: 10562044     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (108)

1. Kumagai K. Über den resorptions Vergang der corpuscularen Bestanteile im Darm. Kekkaku 1922;4:429-31.
2. Oka H. Pathoanatomy and clinical study of intestinal tuberculosis (In Japanese). Jpn J Gastroenterol 1937;36:551-78.
3. Schmedtje JF. Some histochemical characteristics of lymphoepithelial cells of the rabbit appendix epithelium. Anat Rec 1965;151:412-3.
4. Bockman DE, Cooper MD. 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;136:455-77.
5. Owen RL, Jones AL. Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology 1974;66:189-203.
6. Owen RL. Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peter's patches in normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology 1977;d72:440-51.
7. Cornes JS. Number, size, and distribution of Peyer's patches in the human small intestine. Gut 1965;6:225-33.
8. Dukes C, Bussey HJR. The number of lymphoid follicles of the human large intestine. J Pathol Bacteriol 1926;29: 111-6.
9. Langman JM, Rowland R. The number and distribution of lymphoid follicles in the human large intestine. J Anat 1986; 194:189-94.
10. O'Leary AD, Sweeney EC. Lymphoglandular complex of the colon: structure and distribution. Histopathology 1986; 10:269-83.
11. Fujiyoshi T, Watanabe T, Ichimiya I, Mogi G. Functional architecture of the nasopharyngeal tonsil. Am J Otolarngol 1989;10:124-31.
12. Bienenstock J, Johnston N, Perey DYE. Bronchial lymphoid tissue. I. Morphological characteristics. Lab Invest 1973;28:686-92.
13. Kihara T, Fujimura Y, Uchida J, Miyashima N, Nagasaki S: Structure and origin of microfold cells in solitary lymphoid follicle of human larynx. J Clin Electron Microsc 1986;19:5-6.
14. Latkovic S. Ultrastructure of M cells in the conjunctival epithelium of the guinea pig. Curr Eye Res 1989;8:751-5.
15. Uchida J. Electron microscopic study of microfold cells (M cells) in normal and inflamed human appendix. Gastroenterol Jpn 1988;23:251-62.
16. Jacob E, Backer SJ, Swaminathan SP. "M" cells in the follicle-associated epithelium of the human colon. Histopathology 1987;11:941-52.
17. Fujimura Y, Hosobe M, Kihara T. Ultrastructural study of M cells from colonic lymphoid nodules obtained by colonoscopic biopsy. Dig Dis Sci 1992;37:1089-98.
18. Hosobe M. Distribution of "dome" type lymphoid follicles and morphology of microfold cells (M cells) in the human Bauhin's valve, cecum and proximal ascending colon. Med Electron Microsc 1993;26:139-49.
19. Fujimura Y, Kihara T, Hosobe M, et al. Measurement of microvilli of microfold cells (M-cells) and absorptive cells in follicle-associated epithelium of mouse Peyer's patches. Gastroenterol Jpn 1990;25:508.
20. 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 1985;18: 127-40.
21. McClugage SG, Low FN, Zimny ML. Porosity of the basement membrane overlying Peyer's patches in rats and monkeys. Gastroenterology 1986;91:1128-233.
22. Owen RL, Apple RT, Bhalla DK. 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 1986;216:521-7.
23. Bye WA, Allan CH, Trier JS. Structure, distribution, and origin of M cells in Peyer's patches of mouse ileum. Gastroenterology 1984;86:789-801.
24. Kanou T. Morphological study of microfold cells of intestinal lymphoid follicles in Peyer's patches. Kawasaki Med J 1984;10:181-9.
25. 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 1991; 190:10-8.
26. Owen RL, Bhalla DK. 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 Anal 1983;168:199-212.
27. Pappo J, Owen RL. Absence of secretory component expression by epithelial cells overlying rabbit gut-associated lymphoid tissue. Gastroenterology 1988;76:1173-7.
28. Bjerke K, Brandtzaeg P. Lack of relation between expression of HLA-DR and secretory component (SC) in follicle-associated epithelium of human Peyer's patches. Clin Exp Immunol 1988;71:502-7.
29. Jarry A, Robaszkiewicz M, Brousse N, Potet F. Immune cells associated with M cells in the follicle-associated epithelium of Peyer's patches in the rat. Cell Tissue Res 1989; 255:293-8.
30. Kato T. A study of secretory immunoglobulin A on membranous epithelial cells (M cells) and adjacent absorptive cells of rabbit Peyer's patches. Gastroenterol Jpn 1990;25: 15-23.
31. Weltzin R, Lucia-Jandris P, Michetti P, Fields BN, Kraehenbuhl JP, Neutra MR. Binding and transepithelial transport of immunoglobulins by intestinal M cells: demonstration using monoclonal IgA antibodies against enteric viral protein. J Cell Biol 1989;108:1673-85.
32. Moxey PC, Trier JS. Specialized cell types in the human fetal small intestine. Anal Rec 1978;191:269-86.
33. Wolf JL, Dambrauskas R, Sharpe AH, Trier JS. Adherence to and penetration of intestinal epithelium by reovirus type 1 in neonatal mice. Gastroenterology 1987;92:82-91.
34. Asari M, Kano Y, Wakuri S, Nishita T, Matsushita H, Oshige H. The ultrastructure of bovine ileal follicle-associated epithelial (FAE) cells during the perinatal period. J Anal 1989;163:7-16.
35. Smith MW, Peacock MA. "M" cell distribution in follicle-associated epithelium of mouse Peyer's patch. Am J Anal 1980;159:167-75.
36. Bhalla DK, Owen RL. Cell renewal and migration in lymphoid follicles of Peyer's patches and cecum: an autoradiographic study in mice. Gastroenterology 1982;82:232-42.
37. Savidge TC, Smith MW, James PW, Aldred P. Salmonella induced M cell formation in germ-free mouse Peyer's patch tissue. Am J Pathol 1991;139:177-84.
38. Fujimura Y, Kihara T, Ohtani K, et al. Distribution of microfold cells (M cells) in human follicle-associated epithelium. Gastroenterol Jpn 1990;25:130.
39. Jepson MA, Simmon NL, Hirst GL, Hirst BH. Identification of M cells and their distribution in rabbit intestinal Peyer's patches and appendix. Cell Tissue Res 1993;273: 127-36.
40. Smith MW, James PS, Tivey DR. M cell numbers increase after transfer of SPF mice to a normal animal house environment. Am J Pathol 1987;128:385-9.
41. Siciński P, Rowiński J, Warchoł JB, Bern W. Morphometric evidence against lymphocyte-induced differentiation of M cells from absorptive cells in mouse Peyer's patches. Gastroenterology 1986;90:609-16.
42. Kernéis S, Bogdanova A, Kraehenbuhl JP, Pringault E. Experimental models for the induction of M cells from intestinal cells. Clin Immunol Immunopathol 1995;76:89.
43. +-ATPase expression in the epithelia of rabbit gut-associated lymphoid tissues. Pfluger's Arch 1994;427:343-7.
44. Savidge TC, Smith MW, Mayel-Afshar S, Collins AJ, Freeman TC. Selective regulation of epithelial gene expression in rabbit Payer's patch tissue. Pflüger's Arch 1994;428: 391-9.
45. Giannasca PJ, Giannasca KT, Falk P, Gordon JI, Neutra MR. Regional differences in glycoconjugates of intestinal M cells in mice: potential targets for mucosal vaccines. Am J Physiol 1994;267:G1108-21.
46. Gebert A, Hach G. Differential binding of lectins to M cells and enterocytes in the rabbit cecum. Gastroenterology 1993;105:1350-61.
47. Jepson MA, Mason CM, Simmons NL, Hirst BH. Enterocytes in the follicle-associated epithelia of rabbit small intestine display distinctive lectin-binding properties. Histochem Cell Biol 1995;103:131-4.
48. Gaidar YA. Vimentin-positive epithelial cells in the cupolas of the aggregated lymphoid noduli (Peyer's patches) of the rabbit. Arkh Anat Gistol Embriol 1989;97:84-8.
49. Gebert A, Hach G, Bartels H. Co-localization of vimentin and cytokeratins in M-cells of rabbit gut-associated lymphoid tissue (GALT). Cell Tissue Res 1992;269:331-40.
50. Jepson MA, Mason CM, Bennett MK, Simmons NL, Hirst BH. Coexpression of vimentin and cytokeratins in M cells of rabbit intestinal lymphoid follicle-associated epithelium. Histochem J 1992;24:33-9.
51. Mayrhofer G, Pugh CW, Barclay AN. The distribution, ontogeny and origin in the rat of Ia-positive cells with dendritic morphology and of Ia antigen in epithelia, with special reference to the intestine. Eur J Immunol 1983;13:112-22.
52. Brandtzaeg P, Bjerke K. Human Peyer's patches: lymphoepithelial relationship and characteristics of immunoglobulin producing cells. Immunol Invest 1989;18:29-45.
53. Allan CH, Mendrick DL, Trier JS. Rat intestinal M cells contain acidic endosomal-lysosomal compartments and express class II major histocompatibility complex determinants. Gastroenterology 1993;104:698-708.
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 1986;31:1317-30.
55. Nagura H, Ohtani H, Masada T, Kimura M, Nakamura S, HLA-DR expression on M cells overlying Peyer's patches is a common feature of human small intestine. Acta Pathol Jpn 1991;41:818-23.
56. Finzi G, Gornaggia M, Capella C, et al. Cathepsin E in follicle associated epithelium of intestine and tonsils: localization to M cells and possible role in antigen processing. Histochemistry 1993;99:201-11.
57. Ermak TH, Owen RL. Differential distribution of lymphocytes and accessory cells in mouse Peyer's patches. Anat Rec 1986;215:144-52.
58. Ermak TH, Steger HJ, Pappo J. Phenotypically distinct subpopulations of T cells in domes and M cell pockets of rabbit gut-associated lymphoid tissues. Immunology 1990; 71:530-7.
59. Farstad IN, Halstensen TS, Fausa O, Brandtzaeg P. Heterogeneity of M cell associated B and T cells in human Peyer's patches. Immunology 1994;83:457-64.
60. Owen RL. Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer' patches in the normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology 1977;72:440-51.
61. von Rosen L, Podjaski B, Bettman I, Otto HF. Observations on the untrastructure and function of the so-called "microfold" or "membranous" cells (M cells) by means of peroxidase as a tracer. Virchow Arch Pathol Anal 1981; 390:289-312.
62. Neutra MR, Phillips TL, Mayer EL, Fishkind DJ. Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer's patches. Cell Tissue Res 1987;247:537-46.
63. Shakhlamov VA, Gaidar YA, Baranov VN. Electron cytochemical investigation of cholera toxin absorption by epithelium of Peyer's patches in guinea pigs. Bull Exp Biol Med 1981;90:1159-61.
64. Pappo J, Ermak TH. Uptake and translocation of fluorescent latex particles by rabbit Peyer's patch follicle epithelium: a quantitative model for M cell uptake. Clin Exp Immunol 1989;76:144-8.
65. Amerongen HM, Michetti P, Weltzin R, Lee TH, Kraehenbuhl JP, Neutra MR. Transepithelial delivery of a recombinant HIV-1 protein on hydroxyapatite for production and monoclonal anti-gp 120 IgA antibodies [Abstract]. J Cell Biol 1991;115:237a.
66. Ermak TH, Dougherty EP, Bhagat HR, Kabok Z, Pappo J. Uptake and transport of copolymer biodegradable microspheres by rabbit Peyer's patch M cells. Cell Tissue Res 1995;279:433-6.
67. Wolf JL, Kauffman RS, Finberg R, Dambrauskas R, Fields BN, Trier JS. Determinants of reovirus interaction with the intestinal M cells and absorptive cells of murine intestine. Gastroenterology 1983;85:291-300.
68. Siciński P, Rowiński J, Warchoł JB, et al. Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology 1990;98:56-8.
69. Amerongen HM, Weltzin R, Farnet CM, Michetti P, Haseltine WA, Neutra MR. Transepithelial transport of HIV-1 by intestinal M cells: a mechanisms for transmission of AIDS. J Acquir Immune Defic Syndr 1991;4:760-5.
70. Neutra MR, Kraehenbuhl JP. Transepithelial transport and mucosal defence. I. The role of M cells. Trends Cell Biol 1992;2:134-8.
71. Owen RL, Pierce NF, Apple RT, Cray WC 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 1986;153: 1108-118.
72. Kohbata S, Yokoyama H, Yabuuchi E. 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 1986;30:1225-37.
73. 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 1986;21:325-35.
74. Momotani E, Whipple DL, Thiermann AB, Cheville NF. Role of M cells and macrophages in the entrance of Mycobacterium paratuberculosis into domes of ileal Peyer's patches in calves. Vet Pathol 1988;25:131-7.
75. Ackermann MR, Cheville NF, Deyoe BL. Bovine ileal dome lymphoepithelial cells: endocytosis and transport of Brucella abortus strain 19. Vet Pathol 1988;25:28-35.
76. Nagasaki S, Kamoi R, Kato T, et al. M cell transport of Streptococcus pyogenes, Su strain, ATCC 2106 and OK-432 from the intestinal lumen into rabbit Peyer's patches. J Clin Electron Microsc 1988;21:588-9.
77. Walker RI, Schmauder-Chock EA, Parker JL, Burr D. Selective association and transport of Campylobacter jejuni through M cells of rabbit Peyer's patches. Can J Microbiol 1988;34:1142-7.
78. Grützkau A, Hanski C, Hahn H, Riecken EO. Involvement of M cells in the bacterial invasion of Peyer's patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut 1990;31:1011-5.
79. Fujimura Y, Kihara T, Mine H. Membranous cells as a portal of Yersinia pseudotuberculosis entry into rabbit ileum. J Clin Electron Microsc 1992;25:35-45.
80. Wassef JS, Keren DF, Mailloux JL. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun 1989;57: 858-63.
81. Kamoi R. Morphological studies of Salmonella enteritidis uptake by microfold cells (M cells) of the Peyer' patch (In Japanese). Kawasaki Igakkaishi 1991;17:225-35.
82. Inman LR, Cantey JR. Peyer's patch lymphoid follicle epithelial adherence of a rabbit enteropathologic Escherichia coli strain RDEC-1: role of plasmid mediated pili in initial adherence. J Clin Invest 1984;74:90-5.
83. Uchida J. An ultrastructural study on active uptake and transport of bacteria by microfold cells (M cells) to the lymphoid follicles in the rabbit appendix. J Clin Electron Microsc 1987;20:379-94.
84. Marcial MA, Madara JL. Cryptosporidium: cellular localization, structural analysis of absorptive cell-parasite membrane-membrane interactions in guinea pigs, and suggestion of protozoan transport by M cells. Gastroenterology 1986;90:583-94.
85. Yamamoto T, Fujita K, Yokota T. Adherence characteristics to human small intestinal mucosa of Escherichia coli isolated from patients with diarrhea or urinary tract infections. J Infect Dis 1990;162:896-908.
86. Sass W, Dreyer HP, Seifert J. Rapid insorption of small particles in the gut. Am J Gastroenterol 1990;85:255-60.
87. Owen RL, Allen CL, Stevens DP. Phagocytosis of Giardia muris by macrophages in Peyer's patch epithelium in mice. Infect Immun 1981;33:591-601.
88. Bockman DE, Stevens W. Gut-associated lymphoepithelial tissue: bidirectional transport of tracer by specialized epithelial cells associated with lymphoid follicles. J Reticuloendothel Soc 1977;21:245-52.
89. Brown W, Smith P, Le M, Huffer W, Boedeker E. Histomorphometric estimation of the uptake of polystyrene particles by intestinal lymphoid tissues [Abstract]. Gastroenterology 1994;106:A656.
90. Weltzin R, Lucia-Jandris P, Michetti P, Fields BN, Kraehenbuhl JP, Neutra MR. Binding and transepithelial transport of immunoglobulins by intestinal M cells: demonstration using monoclonal IgA antibodies against enteric viral proteins. J Cell Biol 1989;108:1673-85.
91. Owen RL, Pierce NF, Cray WC Jr. Effects of bacterial infection 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 diarrheas. Tokyo: KTK Scientific Publishers. 1988:189-97.
92. Fujimura Y, Arita S, Kihara T. Uptake of BCG into immunized and nonimmunized rabbit Peyer's patches: morphology and quantitative analysis. Kawasaki Med J 1990;16: 181-90.
93. Ermak TH, Steger HJ, Strober S, Owen RL. M cells and granular mononuclear cells in Peyer's patch domes of mice depleted of their lymphocytes by total lymphoid irradiation. Am J Pathol 1989;134:529-37.
94. Owen RL, Lüthen RE, Piazza AJ. Effects of irradiation on Peyer's patch follicle structure and particle transport [Abstract]. Gastroenterology 1993;104:A759.
95. Bienenstock J, McDermott M, Befus D, O'Neill M. A common mucosal immunologic system involving the bronchus, breast, and bowel. Adv Exp Med Biol 1978;107:53-9.
96. Fujimura Y, Kihara T. Immunohistochemical localization of intercellular adhesion molecule-1 in follicle associated epithelium of Peyer's patches. Gut 1994;35:46-50.
97. Kleinman RE, Walker WA. The enteromammary immune system: an important new concept in breast milk host defence. Dig Dis Sci 1979;24:876-82.
98. Hizawa K, Iida M, Kohrogi N, et al. Crohn's disease: early recognition and progress of aphthous lesions. Radiology 1994;190:451-4.
99. Fujimura Y, Iida M. Role of FAE in colonic lymphoid nodules in the formation of early lesions of Crohn's disease [Abstract]. Clin Immunol Immunopathol 1995;76:89.
100. Vantrappen G, Ponette A, Geboes K, Bertrand P. Yersinia enteritis and enterocolitis. Gastroenterology 1977;72:220-7.
101. Carr-Locke DL, Finlay DBL. Radiological demonstration of colonic aphthoid ulcers in a patient with intestinal tuberculosis. Gut 1982;24:453-5.
102. Matsui T, Iida M, Tada S, et al. The value of double contrast barium enema in amebic colitis. Gastroentest Radiol 1989;14:73-8.
103. Nakamura S, Iida M, Tominaga M, Yao T, Hirata N, Fujishima M. Salmonella colitis: assessment with double con-trast barium enema. Examination in seven patients. Radiology 1992;184:537-40.
104. Tielbeek AV, Rosenbusch G, Muytjens HL, Yap SH, Strijk SP, Boetes C. Roentgenologic changes of the colon in Campylobacter infection. Gastrointest Radiol 1985;10:358-61.
105. Wakefield AJ, Pittilo RM, Sim R, et al. Evidence of persistent measels virus infection in Crohn's disease. J Med Virol 1993;39:345-53.
106. Jones BD, Ghori N, Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 1994;180:15-23.
107. Evans BA, Dawson SG, McLean KA, et al. Sexual lifestyle and clinical findings related to HTLV-III/LAV status in homosexual man. Genitourin Med 1986;62:384-9.
108. Owen RL, Bass DM, Piazza AJ. Colonic lymphoid patches: a portal of entry in mice for type 1 reovirus administered anally [Abstract]. Gastroenterology 1990;98:A468.