Improving M cell mediated transport across mucosal barriers: Do certain bacteria hold the keys?

Immunology

Volumn 113, Issue 1, 2004, Pages 15-22

  Man, Angela L ^a   Prieto Garcia, Maria Elena ^a   Nicoletti, Claudio ^a  

^a INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

Antigen delivery; M cells; Mucosal immunity; Mucosal associated lymphoid tissue (MALT)

Indexed keywords

GREEN FLUORESCENT PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN;

ACTIN FILAMENT; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; CELL INTERACTION; CELL ISOLATION; CELL MEMBRANE TRANSPORT; CELL STRAIN CACO 2; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; DENDRITIC CELL; HUMAN; INTESTINE LYMPHATIC TISSUE; MAJOR HISTOCOMPATIBILITY COMPLEX; MUCOSAL IMMUNITY; PEYER PATCH; PRIORITY JOURNAL; REVIEW; STREPTOCOCCUS PNEUMONIAE; TIGHT JUNCTION; UPREGULATION;

ANIMALS; BACTERIA; BIOLOGICAL TRANSPORT, ACTIVE; EPITHELIAL CELLS; HUMANS; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; MICE; PEYER'S PATCHES;

EID: 4444318921     PISSN: 00192805     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2004.01964.x     Document Type: Review

References (85)

1. Madara JL, Nash S, Moore R, Atisook K. Structure and function of the intestinal epithelial barrier in health and disease. Monogr Pathol 1990; 31:306-24.
2. Bjarnason I, MacPherson Hollander D. Intestinal permeability. Gastroenterology 1995; 108:1566-81.
3. McGhee JR, Kiyono H. New perspective in vaccine development: mucosal immunity to infections. Infect Agents Dis 1993; 2:55-73.
4. Frey A, Giannasca KT, Weltzin R et al. Role of glycocalix in regulating access to plasma membranes of intestinal epithelial cell: implications for microbial attachment and oral vaccine targeting. J Exp Med 1996; 1996:1045-59.
5. Kett K, Baklien K, Bakken A, Kral JG, Fausa O, Brandtzaeg P. Intestinal B cell isotype response in relation to local bacteria load: evidence for IgA subclass adaptation. Gastroenterology 1995; 109:819-25.
6. Maury J, Nicoletti C, Guzzo-Chambraud F, Maroux S. The filamentous brush border glycocalix, a mucine-like marker of enterocytes hyper polarization. Eur J Biochem 1995; 228:323-31.
7. Semenza G. Anchoring and biosynthesis of stalked brush border membrane proteins: glycosidases and peptidases of enterocytes and renal tubuli. Annu Rev Cell Biol 1990; 2:255-313.
8. Neutra MR, Frey A, Kraehenbuhl JP, Epithelial M cells. Gateways for mucosal infection and immunization. Cell 1996; 86:345-8.
9. Neutra MR, Pringault E, Kraehenbuhl JP. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol 1996; 14:275-300.
10. Holmgren J, Czerkinsky C, Eriksson K, Mharandi A. Mucosal immunization and adjuvants: a brief overview of recent advances and challenges. Vaccine 2003; 21 (Suppl. 2):89-95.
11. Brandtzaeg P, Baekkevold ES, Farstad IN et al. Regional specialization in the mucosal immune system: what happens in the microcompartments? Immunol Today 1999; 20:141-51.
12. Jang MH, Kweon MN, Iwatani K et al. Intestinal villous M cells: an antigen entry site in the mucosal epithelium. Proc Nat Acad Sci USA 2004; 101:6110-5.
13. Neutra MR, Mantis NJ, Kraehenbuhl JP. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nature Immunol 2001; 2:1004-9.
14. Allan CH, Trier JS. Structure and permeability differ in subepithelial villus and Peyer's patches follicles capillaries. Gastroenterology 1991; 100:1172-9.
15. Hein WR. Organization of mucosal lymphoid tissue. Curr Top Microbiol Immunol 1999; 236:1-15.
16. Pappo J, Owen RL. Absence of secretory component expression by epithelial cells overlying rabbit gut-associated lymphoid tissue. Gastroenterology 1988; 95:1173-7.
17. Gehrke I, Pabst R. The epithelium overlying rabbit bronchus-associated lymphoid tissue does not express the secretory component of immunoglobulin. Cell Tissue Res 1990; 259:397-9.
18. Giannnasca 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; 227:1108-21.
19. 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.
20. Owen RL, Jones AL. Epithelial cell specialization within human Peyer's patch: an ultrastructural study of intestinal lymphoid follicle. Gastroenterology 1974; 66:189-203.
21. Fujimura Y. Evidence of M cells as portals of entry for antigens in the nasopharyngeal lymphoid tissue of humans. Virchows Arch 2000; 436:560-6.
22. Zuercher AW, Coffin SE, Thurnheer MC, Fundova P, Cebra JJ. Nasal-associated lymphoid tissue is a mucosal inductive site for virus-specific humoral and cellular immune responses. J Immunol 2002; 168:1796-803.
23. Hou Y, Hu WG, Hirano T, Gu XX. A new intra-NALT route elicits mucosal and systemic immunity against Moraxella catarrhalis in a mouse challenge model. Vaccine 2002; 20:2375-81.
24. Huang FP, Platt N, Wykes M et al. A discrete subpopulation of dentritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J Exp Med 2000; 191:435-43.
25. Rescigno M, Urbano M, Valzasina B et al. Dentritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001; 2:361-8.
26. Ruedl C, Hubele S. Maturation of Peyer's patches dentritic cells in vitro upon stimulation via cytokines or CD40 triggering. Eur J Immunol 1997; 27:1325-30.
27. Kelsall BL, Strober W. Distinct populations of dentritic cells are present in subepithelial dome and T cell regions of the murine Peyer's patch. J Exp Med 1996; 183:237-47.
28. Iwasaki A, Kelsall BL. Localization of distinct Peyer's patch dentritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3α, MIP-3β, and secondary lymphoid organ chemokine. J Exp Med 2000; 191:1381-94.
29. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dentritic cells carrying commensal bacteria. Science 2004; 303:1662-5.
30. Wang X, Hone DM, Haddad A, Shata MT, Pascual DW. M cell DNA vaccination for CTL immunity to HIV. J Immunol 2003; 171:4717-25.
31. Clark MA, Jepson MA, Hirst BH. Exploiting M cells for drug and vaccine delivery. Adv Drug Del Rev 2001; 50:81-106.
32. Bockman DE. Functional histology of appendix. Arch Histol Cytol 1983; 46:271-92.
33. Bye WA, Allan CH, Trier JS. Structure, organization and distribution of M cells in Peyer's patches. Gastroenterology 1984; 86:789-801.
34. Fujimura Y. Functional morphology of microfold cells (M) in Peyer's patches. Phagocytosis and transport of BCG by M cells into rabbit Peyer's patches. Gastroenterol Jpn 1986; 21:325-30.
35. Borghesi C, Bertelli E, Regoli M, Nicoletti C. Modifications of the FAE by short term exposure to a non-intestinal bacterium. J Pathol 1996; 180:326-32.
36. Neutra MR, Phillips TL, Mayer EL, Fishkind DJ. Transport of membrane-bound macromolecules by M cells in the FAE of rabbit Peyer's patches. Cell Tissue Res 1987; 247:536-46.
37. Owen RL. Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in normal unobstructed mouse intestine: an ultrastructural study. Gastroenterology 1977; 72:440-51.
38. Gebert A. The role of M cells in the protection of mucosal membrane. Histochem Cell Biol 1997; 108:455-70.
39. Druben DG, Nelson WJ. Origin of cells polarity. Cell 1996; 84:335-44.
40. Wolf JL, Bye WA. The membranous (M) epithelial cells and the mucosal immune system. Annu Rev Med 1984; 35:95-112.
41. Regoli M, Bertelli E, Borghesi C, Nicoleti C. Three (3D)-reconstruction of M cells in rabbit Peyer's patches: definition of intraepithelial compartment of the follicle-associated epithelium. Anat Rec 1995; 243:19-26.
42. Neutra MR. Current concepts in mucosal immunity. V. Role of M cells in transepithelial transport of antigens and pathogens to the intestinal immune system. Am J Physiol 1998; 274:G785-91.
43. Clark MA, Jepson MA, Simmons NL, Booth TA, Hirst BH. Differential expression of lectin binding sites defines mouse intestinal M cells. J Histochem Cytochem 1993; 41:1679-87.
44. Falk P, Roth KA, Gordon JI. Lecins are sensitive tools for defining the differentiation programs of epithelial cell lineages in the developing and adult mouse gastrointestinal tract. Am J Physiol 1994; 266:G987-G1003.
45. Gebert A, Hach G. Differential binding of lectins to M cells and enterocytes in the rabbit caecum. Gastroenterology 1993; 105:1350-61.
46. Clark MA, Jepson MA, Simmons NL, Hirst BH. Differential surface characteristics of M cells from mouse intestinal Peyer's patch and caecal patches. Histochem J 1994; 26:271-80.
47. Giannasca PJ, Giannasca KT, Leichtner AM, Neutra MR. Human intestinal M cells display the sialyl Lewis A antigen. Infect Immun 1999; 67:946-53.
48. Neutra MR, Giannasca PJ, Giannasca KT. M cells and microbial pathogens. In: Blaser M, Smith PD, Ravodin JI, eds. Infections of the GI Tract. New York: Raven Press, 1995:163-78.
49. Clark MA, Blair H, Liang L, Brey RN, Brayden D, Hirst BH. Targeting polymerised liposomoe vaccine carriers to intestinal M cells. Vaccine 2002; 20:208-17.
50. Jepson MA, Clark MA, Hirst BH. M cell targeting by lectins: a strategy from mucosal vaccination and drug delivery. Adv Drug Del Rev 2004; 56:511-25.
51. Finzi G, Cornaggia 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.
52. 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; 104:698-08.
53. Pappo J, Mahlman RT. Follicle epithelial M cells are a source of IL-1 in Peyer's patches. Immunology 1993; 78:505-7.
54. Granucci F, Ricciardi-Castagnoli P. Interactions of bacterial pathogens with dentritic cells during invasion of mucosal surfaces. Curr Options Microbiol 2003; 6:72-6.
55. Kohobata S, Yokobata H, Yabuuchi E. Cytopathogenic effect of Salmonella typhi GIFU 10 007 on cells of murine ileal Peyer's patches in ligated ileal loops: an ultrastructural study. Microbiol Immunol 1986; 30:1225-37.
56. 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.
57. Perdomo JL, Cavaillon JM, Huerre M, Ohayon H, Gounon P, Sansonetti PJ. Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J Exp Med 1994; 180:1307-19.
58. Grutzkau A, Hanski C, Hahn H, Riecken EO. Involvement of M cells in the bacterial invation of Peyer's patch: a common mechanism shared by Yersinia enterocolitica and other entero-invasive bacteria. Gut 1990; 3:1011-5.
59. Meynell HM, Thomas NW, James PS, Holland J, Taussig MJ, Nicoletti C. Up-regulation of microsphere transport across the follicle-associated epithelium of Peyer's patch by exposure to S. pneumoniae R36a. FASEB J 1999; 13:611-9.
60. Borghesi C, Taussig MJ, Nicoletti C. Rapid appearance of M cells after microbial challenge is restricted at the periphery of the follicle-associated epithelium of Peyer's patch. Lab Invest 1999; 79:1391-01.
61. Gebert A, Steinmetz I, Fassbender S, Wendlandt KH. Antigen transport in Peyer's patches: increased uptake by constant numbers of M cells. Am J Pathol 2004; 64:65-72.
62. Hermiston M, Green RP, Gordon JI. Chimeric-transgenic mice represent a powerful tool for studying how the proliferation and differentiation programs of intestinal epithelial cells lineages are regulated. Proc Natl Acad Sci USA 1993; 90:8866-70.
63. Heath JP. Epithelial cell migration in the intestine. Cell Biol Int 1996; 20:139-40.
64. Louvard D, Kedinger M, Hauri HP. The differentiating intestinal epithelial cells: establishment and maintenance of functions thought interactions between cellular structures. Annu Rev Cell Biol 1992; 8:157-95.
65. Ponder BA, Schmidt GH, Wilkinson MM, Wood MJ, Monk M, Reid A. Derivation of mouse intestinal crypts from single progenitor cells. Nature 1985; 313:689-91.
66. Rubin DC, Ong D, Gordon JI. Cellular differentiation in the emerging fetal rat small intestinal epithelium: mosaic pattern of gene expression. Proc Natl Acad Sci USA 1989; 86:1278-82.
67. Giannasca PJ, Giannasca KT, Falk P, Gordon JI, Neutra MR. Regional differences in glycoconjugates of intestinal M cells in mice: potential targets for mucosal vaccine. Am J Physiol 1994; 267:G1108-21.
68. Gebert A, Posselt W. Glyconjugate expression defines the origin and differentiation pathway of intestinal M cells. J Histochem Cytochem 1997; 45:1341-50.
69. Lelouard H, Sahuquet A, Reggio H, Montcourrier P. Rabbit M cells and dome enterocytes are distinct cell lineages. J Cell Sci 2001; 114:2077-83.
70. Gebert A, Fassbender S, Werner K, Weissferdt A. The development of M cells in Peyer's patches is restricted to specialized dome-associated crypts. Am J Pathol 1999; 154:1573-82.
71. Smith MW, Peacock MA. Lymphocyte induced formation of antigen transporting M cells from fully differentiated mouse enterocytes. In: Robinson JWL, ed. Mechanisms of Intestinal Adaptation: Lancaster: MTP, 1982:573-83.
72. Kerneis S, Bogdanova A, Kraehenbulh JP, Pringault E. Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 1997; 277:949-52.
73. Delie F, Rubas W. A human colonic cell line sharing similarities with enterocytes as a model to examine oral absorption: advantages and limitations of the caco-2 model. Crit Rev Ther Drug Carrier Syst 1997; 14:221-86.
74. Owen RL. Mid-life crisis for M cells. Gut 1998; 42:11-2.
75. Golovkina TV, Shlomchik M, Hannum L, Chervonsky A. Organogenic role of B lymphocytes in mucosal immunity. Science 1999; 286:1965-8.
76. Debard N, Sierro F, Browning J, Kraehenbuhl JP. Effect of mature lymphocytes and lymphotoxin on the development of the follicle-associated epithelium and M cells in the Peyer's patches. Gastroenterology 2001; 120:1173-82.
77. El Bahi S, Caliot E, Bens M et al. Lymphoepithelial interations trigger specific regulation of gene expression in the M cell-containing follicle-associated epithelium of Peyer's patches. J Immunol 2002; 168:3713-20.
78. Lo D, Tynan W, Dickerson J et al. Cell culture modeling of specialized tissue: identification of genes expressed specifically by follicle-associated epithelium of Peyer's patch by expression profiling of Caco-2/Raji co-cultures. Int Immunol 2004; 16:91-9.
79. Sharma R, Schumacher U, Adam E. Lectin histochemistry revealed the appearance of M cell in Peyer's patches of SCID mice after syngeneic normal bone marrow transplantation. J Histochem Cytochem 1998; 46:143-8.
80. Savidge TC, Smith MW, James PS, Aldred P. Salmonella-induced M-cell formation in germ-free mouse peyer's patch tissue. Am J Pathol 1991; 139:177-84.
81. Gullberg E, Leonard M, Karlsson J et al. Expression of specific markers and particle transport in a new human intestinal M-cell model. Biochem Biophys Res Commun 2000; 279:808-13.
82. Robinson K, Chamberlain LM, Lopez MC et al. Mucosal and cellular immune responses elicited by recombinant Lactococcus lactis strains expressing tetanus tocxin fragment C. Infect Immun 2004; 72:2753-61.
83. Bowe F, Pickard DJ, Anderson RJ, Londono-Arcila P, Dougan G. Development of attenuated Salmonella starins that express heterologous antigens. Meth Mol Med 2003; 87:83-100.
84. Mathiowitz E, Jacob JS, Jong YS et al. Biologically erodable microspheres as potential oral drug delivery systems. Nature 1997; 386:410-4.
85. Brayden DJ. Oral vaccination in man using antigens in particles: current status. Eur J Pharm Sci 2001; 14:183-9.