Role of Intestinal M Cells in Microbial Pathogenesis

Marian R. Neutra; Philippe Sansonetti; Jean-Pierre Kraehenbuhl

doi:10.1128/9781555817848.ch2

Chapter 2 : Role of Intestinal M Cells in Microbial Pathogenesis

Authors: Marian R. Neutra¹, Philippe Sansonetti², Jean-Pierre Kraehenbuhl³

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Affiliations: 1: Department of Pediatrics, Harvard Medical School, GI Cell Biology Laboratory, Children's Hospital, Boston, MA 02115; 2: Unité de Pathogenie Microbienne Moleculaire, Institut Pasteur, 75724 Paris Cedex 15, France; 3: Swiss Institute for Experimental Cancer Research, Institute of Biochemistry, University of Lausanne, CH–1066 Epalinges, Switzerland

Content Type: Monograph

Publication Year: 2003

Category: Clinical Microbiology

Book DOI: 10.1128/9781555817848

Chapter DOI: 10.1128/9781555817848.ch2

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Abstract:

The intestinal epithelium is remarkable in its ability to serve multiple functions simultaneously. Mucosal lymphoid follicles with associated follicle-associated epithelium (FAE) are widely distributed in the digestive tract. The Peyer's patches have been most extensively studied because they consist of large aggregates of follicles visible on the antimesenteric surface of the intestine. The ability of pathogens to exploit the M-cell transport pathway is indeed impressive when one considers the rarity of these cells in the epithelium. M cells can engulf noninvasive microorganisms including Vibrio cholerae by actin-dependent phagocytosis, while certain pathogens such as Salmonella spp. disrupt the M-cell apical cytoskeletal organization and induce macropinocytosis. Information about the events immediately following M-cell transport is scarce. Although pathogens can exploit subepithelial antigen-presenting cells and use the migration of these cells to reach local and distant targets, in most cases M-cell-mediated uptake of microorganisms probably results in immune responses that are beneficial to the host. The ability of poliovirus to use the M-cell pathway for penetration of the epithelial barrier is now being exploited as an oral vaccine strategy. A clearer understanding of adherence mechanisms will facilitate the design of mucosal vaccines that are targeted to organized mucosal lymphoid tissues for efficient induction of protective immune responses.

Citation: Neutra M, Sansonetti P, Kraehenbuhl J. 2003. Role of Intestinal M Cells in Microbial Pathogenesis, p 23-42. In Hecht G (ed), Microbial Pathogenesis and the Intestinal Epithelial Cell. ASM Press, Washington, DC. doi: 10.1128/9781555817848.ch2

Key Concept Ranking

Peyer's Patches: 0.6327414
Human immunodeficiency virus 1: 0.46888897
Type III Secretion System: 0.45449147
Immune Systems: 0.44951954

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Role of Intestinal M Cells in Microbial Pathogenesis

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FIGURE 1

Interactions of bacteria and viruses with M cells. The schematic drawings in panels A, B, and D depict the apical pole of an M cell and the brush borders of adjacent enterocytes in the FAE. A portion of the M-cell intraepithelial pocket with lymphocytes and part of a phagocytic cell (Φ) are shown. (C) An entire M cell along with associated cells within the pocket and under the epithelium. (A) V. cholerae and enteropathogenic E. coli (EPEC) are noninvasive pathogens that colonize enterocyte surfaces but also adhere to M cells. V. cholerae is endocytosed and transported to the pocket, but EPEC induces formation of attaching and effacing lesions on the M-cell surface. (B) S. enterica serovars Typhi and Typhimurium adhere preferentially (but not exclusively) to M cells. They invade the Peyer's patch by inducing ruffling of the M-cell apical surface and macropinocytosis. (C) Shigella flexneri is efficiently transported by M cells. Once on the basolateral side of the epithelium, S. flexneri invades both epithelial and subepithelial cells, which in turn release cytokines and chemokines that recruit polymorphonuclear leukocytes (PMNs). (D) Reovirus adheres selectively to M cells in mice. HIV can adhere to the surface of the FAE in experimental animals. M-cell adherence results in transcytosis of virus into the M-cell pocket. (Reproduced with permission from reference 114 .)

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FIGURE 1

References

/content/book/10.1128/9781555817848.chap2

1. Allan, C. H.,, D. L. Mendrick,, and J. S. Trier. 1993. Rat intestinal epithelial M cells contain acidic endosomal lysosomal compartments and express class II major histocompatibility complex determinants. Gastroenterology 104:698–708.

2. Amerongen, H. M.,, G. A. R. Wilson,, B. N. Fields,, and M. R. Neutra. 1994. Proteolytic processing of reovirus is required for adherence to intestinal M cells. J. Virol. 68:8428–8432.

3. Amerongen, H. M.,, R. A. Weltzin,, C. M. Farnet,, P. Michetti,, W. A. Haseltine,, and M. R. Neutra. 1991. Transepithelial transport of HIV-1 by intestinal M cells: a mechanism for transmission of AIDS. J. Acquir. Immune Defic. Syndr. 4:760–765.

4. Apter, F. M.,, P. Michetti, , L. S. Winner III,, J. A. Mack,, J. J. Mekalanos,, and M. R. Neutra. 1993. Analysis of the roles of antilipopolysaccharide and anti-cholera toxin IgA antibodies in protection against Vibrio cholerae and cholera toxin using monoclonal IgA antibodies in vivo. Infect. Immun. 61:5279–5285.

5. Baggiolini, M. 1998. Chemokines and leukocyte traffic. Nature 392:565–568.

6. Banchereau, J.,, and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392:245–252.

7. Bass, D. M.,, D. Bodkin,, R. Dambrauskas,, J. S. Trier,, B. N. Fields,, and J. L. Wolf. 1990. Intraluminal proteolytic activation plays an important role in replication of type 1 reovirus in the intestines of neonatal mice. J. Virol. 64:1830–1833.

8. Bass, D. M.,, J. S. Trier,, R. Dambrauskas,, and J. L. Wolf. 1988. Reovirus type 1 infection of small intestinal epithelium in suckling mice and its effect on M cells. Lab. Invest. 55:226–235.

9. Baumler, A. J.,, R. M. Tsolis,, and F. Heffron. 1996. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer’s patch. Proc. Natl. Acad. Sci. USA 93:279–283.

10. Bisaillon, M.,, L. Bernier,, S. Sénéchal,, and G. Lemay. 1999. A glycosyl hydrolase activity of mammalian reovirus sigma1 protein can contribute to viral infection through a mucus layer. J. Mol. Biol. 286:759–773.

11. Bockman, D. E.,, and M. D. Cooper. 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. 136:455–478.

12. Bodkin, D. K.,, M. L. Nibert,, and B. N. Fields. 1989. Proteolytic digestion of reovirus in the intestinal lumen of neonatal mice. J. Virol. 63:4676–4681.

13. Bomsel, M. 1997. Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nature Med. 3:42–47.

14. Borghesi, C.,, M. J. Taussig,, and C. Nicoletti. 1999. Rapid appearance of M cells after microbial challenge is restricted at the periphery of the follicle-associated epithelium of Peyer’s patch. Lab. Invest. 79:1393–1401.

15. Bourdet-Sicard, R.,, C. Egile,, P. J. Sansonetti,, and G. TranVanNhieu. 2000. Diversion of cytoskeletal processes by Shigella during invasion of epithelial cells. Microbes Infect. 2:813–819.

16. Brandtzaeg, P.,, and I. N. Farstad,. 1999. The human mucosal B cell system, p. 439–468. In R. Ogra, , J. Mestecky, , J. McGhee, , J. Bienenstock, , M. Lamm, , and W. Strober (ed.), Mucosal Immunology. Academic Press, Inc., New York, N.Y.

17. Brandtzaeg, P.,, E. S. Baekkevold,, I. N. Farstad,, F. L. Jahnsen,, F. E. Johansen,, E. M. Nilsen,, and T. Yamanaka. 1999. Regional specialization in the mucosal immune system: what happens in the microcompartments? Immunol. Today 20:141–151.

18. Brandtzaeg, P.,, I. N. Farstad,, and G. Haraldsen. 1999. Regional specialization in the mucosal immune system: primed cells do not always home along the same track. Immunol. Today 20: 267–277.

19. Butor, C.,, A. Couedel-Courteille,, J. G. Guilet,, and A. Venet. 1996. Differential distribution of galactosylceramide, H antigen, and carcinoembryonic antigen in rhesus macaque digestive mucosa. J. Histochem. Cytochem. 44:1021–1031.

20. Bye, W. A.,, C. H. Allan,, and J. S. Trier. 1984. Structure, distribution and origin of M cells in Peyer’s patches of mouse ileum. Gastroenterology 86:789–801.

21. Carter, P. B.,, and F. M. Collins. 1974. The route of enteric infection in normal mice. J. Exp. Med. 139:1189–1203.

22. Chappell, J. D.,, J. L. Duong,, B. A. Wright,, and T. S. Dermody. 2000. Identification of carbohydrate-binding domains in the attachment proteins of type 1 and type 3 reoviruses. J. Virol. 74:8472–8479.

23. Chen, H.,, V. Torchilin,, and R. Langer. 1996. Lectin-bearing polymerized liposomes as potential oral vaccine carriers. Pharm. Res. 13: 1378–1383.

24. Clark, M. A.,, B. H. Hirst,, and M. A. Jepson. 1998. M-cell surface β1 integrin expression and invasin-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer’s patch M cells. Infect. Immun. 66:1237–1244.

25. Clark, M. A.,, M. A. Jepson,, N. L. Simmons,, T. A. Booth,, and B. H. Hirst. 1993. Differential expression of lectin-binding sites defines mouse intestinal M-cells. J. Histochem. Cytochem. 41:1679–1687.

26. Clark, M. A.,, M. A. Jepson,, N. L. Simmons,, and B. H. Hirst. 1994. Preferential interaction of Salmonella typhimurium with mouse Peyer’s patch M cells. Res. Microbiol. 145:543–552.

27. Clerici, M.,, E. A. Clark,, P. Polacino,, I. Axberg,, L. Kuller,, N. I. Casey,, W. R. Morton,, G. M. Shearer,, and R. E. Benveniste. 1994. T-cell proliferation to subinfectious SIV correlates with lack of infection after challenge of macaques. AIDS 8:1391–1395.

28. Colman, P. M.,, J. N. Varghese,, and W. G. Laver. 1983. Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature (London) 303:41–47.

29. Cook, D. N.,, D. M. Prosser,, R. Forster,, J. Zhang,, N. A. Kuklin,, S. J. Abbondanzo,, X. D. Niu,, S. C. Chen,, D. J. Manfra,, M. T. Wiekowski,, L. M. Sullivan,, S. R. Smith,, H. B. Greenberg,, S. K. Narula,, M. Lipp,, and S. A. Lira. 2000. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 12:495–503.

30. Corthésy, B.,, M. Kaufmann,, A. Phalipon,, M. C. Peitsch,, M. R. Neutra,, and J.-P. Kraehenbuhl. 1996. A pathogen-specific epitope inserted into recombinant secretory immunoglobulin A is immunogenic by the oral route. J. Biol. Chem. 271:33670–33677.

31. Crotty, S.,, C. J. Miller,, B. L. Lohman,, M. R. Neagu,, L. Compton,, D. Lu,, F. X. Lu,, L. Fritts,, J. D. Lifson,, and R. Andino. 2001. Protection against simian immunodeficiency virus vaginal challenge by using Sabin poliovirus vectors. J. Virol. 75:7435–7452.

32. Debard, N.,, F. Sierro,, J. Browning,, and J.-P. Kraehenbuhl. 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: 1173–1182.

33. DeVinney, R.,, D. G. Knoechel,, and B. B. Finlay. 1999. Enteropathogenic Escherichia coli: cellular harrassment. Curr. Opin. Microbiol. 2:83–88.

34. Donnenberg, M. S.,, J. B. Kaper,, and B. B. Finlay. 1997. Interactions between enteropathogenic Escherichia coli and host epithelial cells. Trends Microbiol. 5:109–114.

35. Dupont, H. L.,, M. M. Levine,, R. B. Hornick,, and S. B. Formal. 1989. Inoculum size in shigellosis and implications for expected mode of transmission. J. Infect. Dis. 159:1126–1128.

36. Fagarasan, S.,, K. Kinoshita,, M. Muramatsu,, K. Ikuta,, and T. Honjo. 2001. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 413:639–643.

37. Fällmann, M.,, C. Persson,, and H. Wolf-Watz. 1997. Yersinia proteins that target host-cell signaling pathways. J. Clin. Invest. 99:1153–1157.

38. Fantini, J.,, D. G. Cook,, N. Nathanson,, S. L. Spitalnik,, and F. Gonzalez-Scarano. 1993. Infection of colonic epithelial cell lines by type 1 human immunodeficiency virus (HIV-1) is associated with cell surface expression of galactosyl ceramide, a potential alternative gp120 receptor. Proc. Natl. Acad. Sci. USA 90:2700–2704.

39. Finke, D.,, and J.-P. Kraehenbuhl. 2001. Formation of Peyer’s patches. Curr. Opin. Gen. Dev. 11:562–569.

40. Finlay, B. B.,, and S. Falkow. 1990. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J. Infect. Dis. 162:1096–1106.

41. Finzi, G.,, M. Cornaggia,, C. Capella,, R. Fiocca,, F. Bosi,, E. Solcia,, and I. M. Samloff. 1993. Cathepsin E in follicle associated epithelium of intestine and tonsils: localization to M cells and possible role in antigen processing. Histochemistry 99:201–211.

42. Fox, C. H.,, D. Kotler,, A. Tierney,, C. S. Wilson,, and A. S. Fauci. 1989. Detection of HIV-1 RNA in the lamina propria of patients with AIDS and gastrointestinal disease. J. Infect. Dis. 159:467–471.

43. Frey, A.,, K. T. Giannasca,, R. Weltzin,, P. J. Giannasca,, H. Reggio,, W. I. Lencer,, and M. R. Neutra. 1996. Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells— implications for microbial attachment and oral vaccine targeting. J. Exp. Med. 184:1045–1059.

44. 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. 21:325–335.

45. Fujimura, Y.,, M. Hosobe,, and T. Kihara. 1992. Ultrastructural study of M cells from colonic lymphoid nodules obtained by colonoscopic biopsy. Digest. Dis. Sci. 37:1089–1098.

46. Fujimura, Y.,, T. Kihara,, and H. Mine. 1992. Membranous cells as a portal of Yersinia pseudotuberculosis entry into rabbit ileum. J. Clin. Electron Microsc. 25:35–45.

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

48. Furuta, Y.,, K. Erikkson,, B. Svennerholm,, P. Fredman,, P. Horal,, S. Jeansson,, A. Vahlne,, J. Holmgren,, and C. Czerkinsky. 1994. Infection of vaginal and colonic epithelial cells by the human immunodeficiency virus type 1 is neutralized by antibodies raised against conserved epitopes in the envelope glycoprotein gp120. Proc. Natl. Acad. Sci. USA 91:12559–12563.

49. Gebert, A.,, and G. Hach. 1993. Differential binding of lectins to M cells and enterocytes in the rabbit cecum. Gastroenterology 105:1350–1361.

50. Gebert, A.,, S. Fassbender,, K. Werner,, and A. Weissferdt. 1999. The development of M cells in Peyer’s patches is restricted to specialized dome-associated crypts. Am. J. Pathol. 154:1573–1582.

51. Giannasca, K. T.,, P. J. Giannasca,, and M. R. Neutra. 1996. Adherence of Salmonella typhimurium to Caco-2 cells: identification of a glycoconjugate receptor. Infect. Immun. 64:135–145.

52. Giannasca, P. J.,, J. A. Boden,, and T. P. Monath. 1997. Targeted delivery of antigen to hamster nasal lymphoid tissue with M-celldirected lectins. Infect. Immun. 65:4288–4298.

53. Giannasca, P. J.,, K. T. Giannasca,, A. M. Leichtner,, and M. R. Neutra. 1999. Human intestinal M cells display the sialyl Lewis A antigen. Infect. Immun. 67:946–953.

54. Giannasca, P. J.,, K. T. Giannasca,, P. Falk,, J. I. Gordon,, and M. R. Neutra. 1994. Regional differences in glycoconjugates of intestinal M cells in mice: potential targets for mucosal vaccines. Am. J. Physiol. 267:G1108–G1121.

55. Grutzkau, A.,, C. Hanski,, H. Hahn,, and E. O. Riecken. 1990. Involvement of M cells in the bacterial invasion of Peyer’s patches: a common mechanism shared by Yersinia enterocolitica and other enteroinvasive bacteria. Gut 31: 1011–1015.

56. Hale, T. L., 1998. Bacillary dysentery. In W. J. Hausler, and M. Sussman (ed.) , Topley and Wilson’s Microbiology and Microbial Infections. Bacterial Infections , vol. 3. Arnold, London, United Kingdom.

57. Hein, W. R. 1999. Organization of mucosal lymphoid tissue. Curr. Top. Microbiol. Immunol. 236:1–15.

58. Heppner, F. L.,, A. D. Christ,, M. A. Klein,, M. Prinz,, M. Fried,, J.-P. Kraehenbuhl,, and A. Aguzzi. 2001. Transepithelial prion transport by M cells. Nature Med. 7:1–2.

59. Hersh, D.,, D. M. Monack,, M. R. Smith,, N. Ghori,, S. Falkow,, and A. Zychlinsky. 1999. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc. Natl. Acad. Sci. USA 96:2396–2401.

60. Hilbi, H.,, J. E. Moss,, D. Hersh,, Y. Chen,, J. Arondel,, S. Banerjee,, P. J. Sansonetti,, and A. Zychlinsky. 1998. Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J. Biol. Chem. 273:32895–32900.

61. Hohmann, A. W.,, G. Schmidt,, and D. Rowley. 1978. Intestinal colonization and virulence of Salmonella in mice. Infect. Immun. 22: 763–770.

62. Holgersson, J.,, N. Stromberg,, and M. E. Breimer. 1988. Glycolipids of human large intestine: differences in glycolipid expression related to anatomical localization, epithelial/nonepithelial tissue and the ABO, Le and Se phenotypes of the donors. Biochemie 70:1565–1574.

63. Hopkins, S.,, F. Niedergang,, I. E. Corthésy-Theulaz,, and J.-P. Kraehenbuhl. 2000. A recombinant Salmonella typhimurium vaccine strain is taken up and survives within murine Peyer’s patch dendritic cells. Cell. Microbiol. 2:56–68.

64. Huang, F. P.,, N. Platt,, M. Wykes,, J. R. Major,, T. J. Powell,, C. D. Jenkins,, and G. G. MacPherson. 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 191:435–443.

65. Huang, G. T. J.,, L. Eckmann,, T. C. Savidge,, and M. F. Kagnoff. 1996. Infection of human intestinal epithelial cells with invasive bacteria upregulates apical intercellular adhesion molecule-1 (ICAM-1) expression and neutrophil adhesion. J. Clin. Invest. 98:572–583.

66. Hynes, R. O. 1992. Integrins: versatility, modulation and signalling in cell adhesion. Cell 69: 11–25.

67. Inman, L. R.,, and J. R. Cantey. 1984. Peyer’s patch lymphoid follicle epithelial adherence of a rabbit enteropathogenic Escherichia coli (strain RDEC-1). Role of plasmid-mediated pili in initial adherence. J. Clin. Invest. 74:90–95.

68. Inman, L. R.,, and J. R. Cantey. 1983. Specific adherence of Escherichia coli (strain RDEC-1) to membranous (M) cells of the Peyer’s patch in Escherichia coli diarrhea in the rabbit. J. Clin. Invest. 71:1–8.

69. Isberg, R. R.,, and D. L. Voorhis. 1987. Identification of invasin, a protein that allows enteric bacteria to penetrate mammalian cells. Cell 50: 769–778.

70. Isberg, R. R.,, and J. M. Leong. 1990. Multiple β1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60:861–871.

71. Iwasaki, A.,, and B. L. Kelsall. 2000. Localization of distinct Peyer’s patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3α, MIP-3β, and secondary lymphoid organ chemokine. J. Exp. Med. 191:1381–1393.

72. Izadpanah, A.,, M. B. Dwinell,, L. Eckmann,, N. M. Varki,, and M. F. Kagnoff. 2001. Regulated MIP-3alpha/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am. J. Physiol. 280:G710–G719.

73. Jepson, M. A.,, M. A. Clark,, N. Foster,, C. M. Mason,, M. K. Bennett,, N. L. Simmons,, and B. H. Hirst. 1996. Targeting to intestinal M cells. J. Anat. 189:507–516.

74. Jepson, M. A.,, M. A. Clark,, N. L. Simmons,, and B. H. Hirst. 1993. Epithelial M cells in the rabbit caecal lymphoid patch display distinctive surface characteristics. Histochemistry 100:441–447.

75. Jertborn, M.,, A.-M. Svennerholm,, and J. Holmgren. 1986. Saliva, breast milk, and serum antibody responses as indirect measures of intestinal immunity after oral cholera vaccination. J. Clin. Microbiol. 24:203–209.

76. Jones, B. D.,, N. Ghori,, and S. Falkow. 1994. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer’s patches. J. Exp. Med. 180:15–23.

77. Jung, H. C.,, L. Eckmann,, S. K. Yang,, A. Panja,, J. Fierer,, E. Morzycka-Wroblewska,, and M. F. Kagnoff. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Invest. 95:55–65.

78. Kagnoff, M. F.,, and L. Eckmann. 1997. Epithelial cells as sensors for microbial infection. J. Clin. Invest. 100:S51–S55.

79. Karch, H.,, J. Heesemann,, R. Laufs,, H. P. Kroll,, J. B. Kaper,, and M. M. Levine. 1987. Serological response to type 1-like somatic fimbriae in diarrheal infection due to classical enteropathogenic Escherichia coli. Microb. Pathogen 2: 425–434.

80. Kealy, W. F. 1976. Colonic lymphoid-glandular complex (microbursa): nature and morphology. J. Clin. Pathol. 29:241–244.

81. Kelsall, B. L.,, and W. Strober. 1996. Distinct populations of dendritic cells are present in the subepithelial dome and T cell regions of murine Peyer’s patches. J. Exp. Med. 183:237–247.

82. Kelsall, B.,, and W. Strober,. 1999. Gutassociated lymphoid tissue: antigen handling and T cell responses , p. 293–318. In R. Ogra, , J. Mestecky, , J. McGhee, , J. Bienenstock, , M. Lamm, , and W. Strober (ed.), Mucosal Immunology. Academic Press Inc., New York, N.Y.

83. Kernéis, S.,, A. Bogdanova,, J.-P. Kraehenbuhl,, and E. Pringault. 1997. Conversion by Peyer’s patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277: 948–952.

84. Khatri, I. A.,, C. Ho,, R. D. Specian,, and J. F. Forstner. 2001. Characteristics of rodent intestinal mucin Muc3 and alterations in a mouse model of human cystic fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G1321–1330.

85. Knutton, S.,, D. R. Lloyd,, and A. S. Mc-Neish. 1987. Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect. Immun. 55:69–77.

86. Kohbata, S.,, H. Yokobata,, and E. Yabuuchi. 1986. 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. 30:1225–1237.

87. Kraehenbuhl, J.-P.,, and M. R. Neutra. 2000. Epithelial M cells: differentiation and function. Annu. Rev. Cell Dev. Biol. 16:301–332.

88. Lee, P. W. K.,, and R. Gilmore,. 1998. Reovirus cell attachment protein s1: structurefunction relationships and biogenesis, p. 137–153. In K. L. Tyler, and M. B. A. Oldstone (ed.), Reoviruses. I: Structure, Proteins, and Genetics. Springer-Verlag, Berlin, Germany.

89. Lee, S. H.,, D. L. Hava,, M. K. Waldor,, and A. Camilli. 1999. Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99:625–634.

90. Lelouard, H.,, H. Reggio,, P. Mangeat,, M. R. Neutra,, and P. Montcourrier. 1999. Mucin related epitopes distinguish M cells and enterocytes in rabbit appendix and Peyer’s patches. Infect. Immun. 67:357–367.

91. Lencer, W. I.,, T. R. Hirst,, and R. K. Holmes. 1999. Membrane traffic and the cellular uptake of cholera toxin. Biochim. Biophys. Acta 1450:177–190.

92. MacPherson, A. J.,, D. Gatto,, E. Sainsbury,, G. R. Harriman,, H. Hengartner,, and R. M. Zinkernagel. 2000. A primitive T cellindependent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288: 2222–2226.

93. MacPherson, G. G.,, and L. M. Liu. 1999. Dendritic cells and Langerhans cells in the uptake of mucosal antigens. Curr. Top. Microbiol. Immunol. 256:33–54.

94. Madara, J. L.,, S. Nash,, R. Moore,, and K. Atisook. 1990. Structure and function of the intestinal epithelial barrier in health and disease. Monogr. Pathol. 306–324.

95. Maldonado-Lopez, R.,, T. De Smedt,, P. Michel,, J. Godfroid,, B. Pajak,, C. Hierman,, K. Thielemans,, O. Leo,, J. Urbain,, and M. Moser. 1999. CD8 alpha+ and CD8 alphasubclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189:587–592.

96. Mantis, N. J.,, A. Frey,, and M. R. Neutra. 2000. Accessibility of glycolipid and oligosaccharide epitopes on apical surfaces of rabbit villus and follicle-associated epithelium. Am. J. Physiol. Gastrointest. Liver Physiol. 278:G915–G929.

97. Mantis, N. J.,, M. C. Cheung,, K. R. Chintalacharuvu,, J. Rey,, B. Corthesy,, and M. R. Neutra. 2002. Selective adherence of IgA to murine Peyer’s patch M cells: evidence for a novel IgA receptor. J. Immunol. 169:1844–1851.

98. Marra, A.,, and R. R. Isberg. 1997. Invasindependent and invasin-independent pathways for translocation of Yersinia pseudotuberculosis across the Peyer’s patch intestinal epithelium. Infect. Immun. 65:3412–3421.

99. Masurier, C.,, B. Salomon,, N. Guettari,, N. Pioche,, F. Lachapelle,, M. Guigon,, and D. Klatzmann. 1998. Dendritic cells route human immunodeficiency virus to lymph nodes after vaginal or intravenous administration to mice. J. Virol. 72:7822–7829.

100. Mathan, M. M.,, and V. I. Mathan. 1991. Morphology of rectal mucosa of patients with shigellosis. Rev. Infect. Dis. 13(Suppl. 4):S314–S318.

101. Maury, J.,, C. Nicoletti,, L. Guzzo-Chambraud,, and S. Maroux. 1995. The filamentous brush border glycocalyx, a mucin-like marker of enterocyte hyper-polarization. Eur. J. Biochem. 228:323–331.

102. McClugage, S. G.,, F. N. Low,, and M. L. Zimmy. 1986. Porosity of the basement membrane overlying Peyer’s patches in rats and monkeys. Gastroenterology 91:1128–1133.

103. McGhee, J. R.,, M. E. Lamm,, and W. Strober,. 1999. Mucosal immune responses, p. 485–506. In R. Ogra, , J. Mestecky, , J. McGhee, , J. Bienenstock, , M. Lamm, , and W. Strober (ed.), Mucosal Immunology, 2nd ed. Academic Press Inc., New York, N.Y.

104. Mendelsohn, C. L.,, E. Wimmer,, and V. R. Racaniello. 1989. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 56:855–865.

105. Miller, J. F.,, J. J. Mekalanos,, and S. Falkow. 1989. Coordinate regulation and sensory transduction in the control of bacterial virulence. Science 243:916–921.

106. Miller, S. I. 1991. PhoP/PhoQ: macrophagespecific modulator of Salmonella virulence? Molec. Microbiol. 5:2073-2078.

107. Mills, S., , A. Boland, , M. P. Sory, , P. Van der Smissen, , C. Kerbourch, , B. B. Finlay, , and G. Cornelis. 1997. Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanism and involving YopP presumably acting as an effector protein. Proc. Natl. Acad. Sci. USA 94:12638–12643.

108. Milman, G.,, and O. Sharma. 1994. Mechanisms of HIV/SIV mucosal transmission. AIDS Res. Human Retrovir. 10:1305–1312.

109. Momotani, E.,, D. L. Whipple,, A. B. Thiermann,, and N. F. Cheville. 1988. Role of M cells and macrophages in the entrance of Mycobacterium paratuberculosis into domes of ileal Peyer’s patches in calves. Vet. Pathol. 25:131–137.

110. Monack, D. M.,, J. Mecsas,, N. Ghori,, and S. Falkow. 1997. Yersinia signals macrophages to undergo apoptosis and Yop J is necessary for the cell death. Proc. Natl. Acad. Sci. USA 94: 10385–10390.

111. Morin, M. J.,, A. Warner,, and B. N. Fields. 1994. A pathway for entry of reoviruses into the host through M cells of the respiratory tract. J. Exp. Med. 180:1523–1527.

112. Morrow, C. D.,, M. J. Novak,, D. C. Ansardi,, D. C. Porter,, and Z. Moldoveanu. 1998. Recombinant viruses as vectors for mucosal immunity. Curr. Top. Microbiol. Immunol. 236:255–274.

113. Mounier, J.,, T. Vasselon,, R. Hellio,, M. Lesourd,, and P. J. Sansonetti. 1992. Shigella flexneri enters human colonic Caco-2 cells through the basolateral pole. Infect. Immun. 60: 237–248.

114. Neutra, M. R.,, A. Frey,, and J.-P. Kraehenbuhl. 1996. Epithelial M cells: gateways for mucosal infection and immunization. Cell 86: 345–348.

115. Neutra, M. R.,, P. J. Giannasca,, K. T. Giannasca,, and J.-P. Kraehenbuhl,. 1995. M cells and microbial pathogens, p. 163–178. In M. Blaser, , P. D. Smith, , J. I. Ravdin, , H. B. Greenberg, , and R. L. Guerrant (ed.), Infections of the Gastrointestinal Tract. Raven Press, New York, N.Y.

116. Neutra, M. R.,, T. L. Phillips,, E. L. Mayer,, and D. J. Fishkind. 1987. Transport of membrane-bound macromolecules by M cells in follicle-associated epithelium of rabbit Peyer’s patch. Cell Tiss. Res. 247:537–546.

117. Neutra, M. R.,, E. Pringault,, and J. P. Kraehenbuhl. 1996. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu. Rev. Immunol. 14:275–300.

118. Neutra, M. R.,, N. J. Mantis,, A. Frey,, and P. J. Giannasca. 1999. The composition and function of M cell apical membranes: implications for microbial pathogenesis. Sem. Immunol. 11:171–181.

119. Neutra, M. R.,, P. Sansonetti,, and J. P. Kraehenbuhl,. 2002. M cells and microbial pathogens, p. 141–156. In M. J. Blaser, , P. D. Smith, , J. I. Ravdin, , H. B. Greenberg, , and L. Guerrant (ed.), Infections of the Gastrointestinal Tract. Raven Press, New York, N.Y.

120. Nibert, M. L., 1998. Structure of mammalian orthoreovirus particles, p. 1–30. In K. L. Tyler, and M. B. A. Oldstone (ed.), Reoviruses I: Structure, Proteins, and Genetics. Springer-Verlag, Berlin, Germany.

121. Nibert, M. L.,, D. B. Furlong,, and B. N. Fields. 1991. Mechanisms of viral pathogenesis. Distinct forms of reoviruses and their roles during replication in cells and host. J. Clin. Invest. 88:727–734.

122. Ogra, P. L.,, and D. T. Karzon. 1969. Distribution of poliovirus antibody in serum, nasopharynx and alimentary tract following segmental immunization of lower alimentary tract with polio-vaccine. J. Immunol. 102:1423–1430.

123. O’Leary, A. D.,, and E. C. Sweeney. 1986. Lymphoglandular complexes of the colon: structure and distribution. Histopathology 10: 267–283.

124. Owen, R. 1999. Uptake and transport of intestinal macromolecules and microorganisms by M cells in Peyer’s patches—a personal and historic perspective. Semin. Immunol. 11:1–7.

125. Owen, R. L.,, D. M. Bass,, and A. J. Piazza. 1990. Colonic lymphoid patches. A portal of entry in mice for type I reovirus administered anally. Gastroenterology 98:A468.

126. Owen, R. L.,, and D. K. Bhalla. 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. 168:199–212.

127. Owen, R. L.,, A. J. Piazza,, and T. H. Ermak. 1991. Ultrastructural and cytoarchitectural features of lymphoreticular organs in the colon and rectum of adult BALB/c mice. Am. J. Anat. 190:10–18.

128. Owen, R. L.,, N. F. Pierce,, R. T. Apple,, and W. C. J. Cray. 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. 153:1108–1118.

129. Pappo, J.,, and T. H. Ermak. 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. 76:144–148.

130. Pappo, J.,, and R. L. Owen. 1988. Absence of secretory component expression by epithelial cells overlying rabbit gut-associated lymphoid tissue. Gastroenterology 95:1173–1177.

131. Pauza, C. D.,, P. Emau,, M. S. Salvato,, P. Trivedi,, D. MacKensie,, M. Malkovsky,, H. Uno,, and K. T. Schultz. 1993. Pathogenesis of SIV mac51 after atraumatic inoculation of the rectal mucosa in rhesus monkeys. J. Med. Primatol. 22:154–161.

132. Penheiter, K. L.,, N. Mathur,, D. Giles,, T. Fahlen,, and B. D. Jones. 1997. Non-invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroy M cells of ileal Peyer’s patches. Mol. Microbiol. 24:697–709.

133. Pepe, J. C.,, and V. L. Miller. 1993. Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc. Natl. Acad. Sci. USA 90: 6473–6477.

134. Pron, B.,, C. Boumalia,, F. Jaubert,, P. Berche,, G. Milon,, F. Geissman,, and J. L. Gaillard. 2001. Dendritic cells are early cellular targets of Listeria monocytogenes after intestinal delivery and are involved in bacterial spread in the host. Cell. Microbiol. 3:331–340.

135. Racaniello, V. R.,, and R. Ren. 1996. Poliovirus biology and pathogenesis. Curr. Top. Microbiol. Immunol. 206:305–325.

136. Rafiee, P.,, H. Leffler,, J. C. Byrd,, F. J. Cassels,, E. C. Boedeker,, and Y. S. Kim. 1991. A sialoglycoprotein complex linked to the microvillus cytoskeleton acts as a receptor for pilus (AF/R1) mediated adhesion of enteropathogenic Escherichia coli (RDEC-1) in rabbit small intestine. J. Cell Biol. 115:1021–1029.

137. Rescigno, M.,, M. Urbano,, B. Valzasina,, M. Francolini,, G. Rotta,, R. Bonasio,, F. Granucci,, J.-P. Kraehenbuhl,, and P. Ricciardi-Castagnoli. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nature Immunol. 2:361–367.

138. Rissoan, M. C.,, V. Soumelis,, N. Kadowaki,, G. Grouard,, F. Briere,, R. W. Malefyt,, and Y. J. Liu. 1999. Reciprocal control of T helper cell and dendritic cell differentiation. Science 283:1183–1186.

139. Roy, M. J.,, and M. Varvayanis. 1987. Development of dome epithelium in gut-associated lymphoid tissues: association of IgA with M cells. Cell Tissue Res. 248:645–651.

140. Ruckdeschel, K.,, A. Roggenkamp,, V. Lafont,, P. Mangeat,, J. Heesemann,, and B. Rouot. 1997. Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis. Infect. Immun. 65: 4813–4821.

141. Sansonetti, P. J. 1991. Genetic and molecular basis of epithelial cell invasion by Shigella species. Rev. Infect. Dis. 13:S285–S292.

142. Sansonetti, P. J.,, J. Arondel,, J. R. Cantey,, M. C. Prevost,, and M. Huerre. 1996. Infection of rabbit Peyer’s patches by Shigella flexneri: effect of adhesive or invasive bacterial phenotypes on follicle-associated epithelium. Infect. Immun. 64:2752–2764.

143. Sansonetti, P. J.,, J. Mounier,, M. C. Prevost,, and R. M. Mege. 1994. Cadherin expression is required for the spread of Shigella flexneri between epithelial cells. Cell 76:829–839.

144. Sansonetti, P. J.,, A. Phalipon,, J. Arondel,, K. Thirumalai,, S. Banerjee,, S. Akira,, K. Takeda,, and A. Zychlinsky. 2000. Caspase-1 activation of IL-1b and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12:581–590.

145. Sansonetti, P. J.,, and A. Phalipon. 1999. M cells as ports of entry for enteroinvasive pathogens: mechanisms of interaction, consequences for the disease process. Semin. Immunol. 11:193–203.

146. Savidge, T. C.,, and M. W. Smith. 1995. Evidence that membranous (M) cell genesis is immunoregulated. Adv. Exp. Med. Biol. 371:239–241.

147. Savidge, T. C.,, M. W. Smith,, P. S. James,, and P. Aldred. 1991. Salmonella-induced M-cell formation in germ-free mouse Peyer’s patch tissue. Am. J. Pathol. 139:177–184.

148. Schulte, R.,, S. Kernéis,, S. Klinke,, H. Bartels,, S. Preger,, J.-P. Kraehenbuhl,, E. Pringault,, and I. B. Autenrieth. 2000. Translocation of Yersinia enterocolitica across reconstituted intestinal epithelial monolayers is triggered by Yersinia invasin binding to beta 1 integrins apically expressed on M-like cells. Cell Microbiol. 2:173–185.

149. Sharma, R.,, E. J. M. Van Damme,, W. J. Peumans,, P. Sarsfield,, and U. Schumacher. 1996. Lectin binding reveals divergent carbohydrate expression in human and mouse Peyer’s patches. Histochem. Cell Biol. 105:459–465.

150. Shea, J.,, M. Hensel,, C. Gleeson,, and D. Holden. 1996. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 93:2593–2597.

151. Shibuya, A.,, N. Sakamoto,, Y. Shimizu,, K. Shibuya,, M. Osawa,, T. Hiroyama,, H. J. Eyre,, G. R. Sutherland,, Y. Endo,, T. Fujita,, T. Miyabayashi,, S. Sakano,, T. Tsuji,, E. Nakayama,, J. H. Phillips,, L. L. Lanier,, and H. Nakauchi. 2000. Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat. Immunol. 1:441–446.

152. Shreedhar, V. K.,, B. L. Kelsall,, and M. R. Neutra. 2003. Cholera toxin induces migration of dendritic cells from the subepithelial dome region to T-and B-cell areas of Peyer’s patches. Infect. Immun. 71:504–509.

153. Sicinski, P.,, J. Rowinski,, J. B. Warchol,, Z. Jarzcabek,, W. Gut,, B. Szczygiel,, K. Bielecki,, and G. Koch. 1990. Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology 98:56–58.

154. Sierro, F.,, B. Dubois,, A. Coste,, D. Kaiserlian,, J.-P. Kraehenbuhl,, and J. C. Sirard. 2001. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc. Natl. Acad. Sci. USA 98: 13722–13727.

155. Sierro, F.,, E. Pringault,, P. Simon Assman,, J.-P. Kraehenbuhl,, and N. Debard. 2000. Transient expression of M cell phenotype by enterocyte-like cells of the follicle-associated epithelium of mouse Peyer’s patches. Gastroenterology 119:734–743.

156. Silvey, K. J.,, A. B. Hutchings,, M. Vajdy,, M. M. Petzke,, and M. R. Neutra. 2001. Role of IgA in protection against reovirus entry into murine Peyer’s patches. J. Virol. 75:10870–10879.

157. Silvey, K. J.,, M. Vajdy,, N. J. Mantis,, and M. R. Neutra. 1999. Reovirus: a model to study M cell specific interactions and secretory antibody function in the intestine. Immunol. Lett. 69:65.

158. Sirard, J. C.,, F. Niedergang,, and J.-P. Kraehenbuhl. 1999. Live attenuated Salmonella: a paradigm of mucosal vaccines. Immunol. Rev. 171:5–26.

159. Smith, M. W.,, P. S. James,, and D. R. Tivey. 1987. M cell numbers increase after transfer of SPF mice to a normal animal house environment. Am. J. Pathol. 128:385–389.

160. Takeuchi, A. 1967 . Electron microscope studies of experimental Salmonella infection. I. Pen etration into the intestinal epithelium by Salmonella typhimurium. Am. J. Pathol. 50:109–136.

161. Tanaka, Y.,, T. Imai,, M. Baba,, I. Ishikawa,, M. Uehira,, H. Nomiyama,, and O. Yoshie. 1999. Selective expression of liver and activation-regulated chemokine (LARC) in intestinal epithelium in mice and humans. Eur. J. Immunol. 29:633–642.

162. Uchida, J. 1987. 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. 20: 379–394.

163. Ueki, T.,, M. Mizuno,, T. Ueso,, T. Kiso,, and T. Tsuji. 1995. Expression of ICAM-1 on M cells covering isolated lymphoid follicles of the human colon. Acta Med. Okayama(3) 49: 145–151.

164. Vasquez-Torres, A.,, J. Jones-Carson,, A. J. Baumler,, S. Falkow,, R. Valdivia,, W. Brown,, M. Le,, R. Berggren,, W. T. Parks,, and F. Fang. 1999. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401:804–808.

165. Walker, R. I.,, E. A. Schauder-Chock,, and J. L. Parker. 1988. Selective association and transport of Campylobacter jejuni through M cells of rabbit Peyer’s patches. Can. J. Microbiol. 34: 1142–1147.

166. Wassef, J. S.,, D. F. Keren,, and J. L Mailloux. 1989. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect. Immun. 57:858–863.

167. Weltzin, R. A.,, P. Lucia,, P. Jandris,, P. Michetti,, B. N. Fields,, J.-P. Kraehenbuhl,, and M. R. Neutra. 1989. Binding and transepithelial transport of immunoglobulins by intestinal M cells: demonstration using monoclonal IgA antibodies against enteric viral proteins. J. Cell Biol. 108:1673–1685.

168. Winner, L. S. III, , J. Mack, , R. A. Weltzin, , J. J. Mekalanos, , J.-P. Kraehenbuhl, , and M. R. Neutra. 1991. New model for analysis of mucosal immunity: intestinal secretion of specific monoclonal immunoglobulin A from hybridoma tumors protects against Vibrio cholerae infection. Infect. Immun. 59:977–982.

169. Wold, A. E.,, J. Mestecky,, M. Tomana,, A. Kobata,, H. Ohbayashi,, T. Endo,, and C. Svanborg-Eden. 1990. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin. Infect. Immun. 58:3073–3077.

170. Wolf, J. L.,, D. H. Rubin,, R. Finberg,, R. S. Kauffman,, A. H. Sharpe,, J. S. Trier,, and B. N. Fields. 1981. Intestinal M cells: a pathway for entry of reovirus into the host. Science 212:471–472.

171. Yamamoto, T.,, and T. Yokota. 1989. Adherence targets of Vibrio parahaemolyticus in human small intestines. Infect. Immun. 57:2410–2419.

172. Yamamoto, T.,, and T. Yokota. 1989. Vibrio cholerae O1 adherence to human small intestinal M cells in vitro. J. Infect. Dis. 160:168–169.

173. Zhou, F.,, J.-P. Kraehenbuhl,, and M. R. Neutra. 1995. Mucosal IgA response to rectally administered antigen formulated in IgA-coated liposomes. Vaccine 13:637–644.

174. Zychlinsky, A.,, M. C. Prévost,, and P. J. Sansonetti. 1992. Shigella flexneri induces apoptosis in infected macrophages. Nature 358:167–169.