M cell specific markers in man and domestic animals: Valuable tools in vaccine development

Comparative Immunology, Microbiology and Infectious Diseases

Volumn 36, Issue 4, 2013, Pages 353-364

  Casteleyn, Christophe ^a   Van den Broeck, Wim ^b   Gebert, Andreas ^c   Tambuyzer, Bart R ^a   Van Cruchten, Steven ^a   Van Ginneken, Chris ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Cell marker; Domestic animals; Follicle associated epithelium; Immunohistochemistry; Lectins; Lymphoid tissue; M cells; MALT; Man; Mucosal vaccine

Indexed keywords

CELL MARKER; MUCOSAL VACCINE; UNCLASSIFIED DRUG; VACCINE;

CATTLE; CHICKEN; DOMESTIC ANIMAL; EXPERIMENTAL ANIMAL; HORSE; HUMAN; IMMUNE RESPONSE; LYMPHOID TISSUE; M CELL; MOUSE; MUCOSA ASSOCIATED LYMPHOID TISSUE; MUCOSA CELL; NONHUMAN; PEYER PATCH; RABBIT; RAT; REVIEW; SPECIES DIFFERENCE; SWINE;

ANIMALS; BIOLOGICAL MARKERS; HUMANS; IMMUNITY, MUCOSAL; LYMPHOID TISSUE; MUCOUS MEMBRANE; VACCINES;

ANIMALIA;

EID: 84879000393     PISSN: 01479571     EISSN: 18781667     Source Type: Journal    
DOI: 10.1016/j.cimid.2013.03.002     Document Type: Review

References (133)

1. Gebert A., Pabst R. M cells at locations outside the gut. Seminars in Immunology 1999, 11:165-170.
2. Liebler-Tenorio E., Pabst R. MALT structure and function in farm animals. Veterinary Research 2006, 37:257-280.
3. Debard N., Sierro F., Kraehenbuhl J.-P. Development of Peyer's patches, follicle-associated epithelium and M cell: lessons from immunodeficient and knockout mice. Seminars in Immunology 1999, 11:183-191.
4. Kraehenbuhl J.-P., Neutra M.R. Epithelial M cells: differentiation and function. Annual Review of Cell and Developmental Biology 2000, 16:301-332.
5. Claeys S., De Belder T. The role of mucosal epithelium in antigen presentation. International Journal of Pediatric Otorhinolaryngology 2003, 67S1:S77-S79.
6. Gebert A. The role of M cells in the protection of mucosal membranes. Histochemistry and Cell Biology 1997, 108:455-470.
7. Yamanaka T., Straumfors A., Morton H.C., Fausa O., Brandtzaeg P., Farstad I.N. M cell pockets of human Peyer's patches are specialized extensions of germinal centers. European Journal of Immunology 2001, 31:107-117.
8. Jepson M.A., Clark M.A. Studying M cells and their role in infection. Trends in Microbiology 1998, 6:359-365.
9. Hathaway L.J., Kraehenbuhl J.-P. The role of M cells in mucosal immunity. Cellular and Molecular Life Sciences 2000, 57:323-332.
10. Gebert A., Rothkötter H.J., Pabst R. M cells in Peyer's patches of the intestine. International Review of Cytology 1996, 167:91-159.
11. Neutra M.R., Mantis N.J., Frey A., Giannasca P.J. The composition and function of M cell apical membranes: implications for microbial pathogenesis. Seminars in Immunology 1999, 11:171-181.
12. Clark M.A., Jepson M.A., Hirst B.H. Exploiting M cells for drug and vaccine delivery. Advanced Drug Delivery Reviews 2001, 50:81-106.
13. Clark M.A., Jepson M.A., Simmons N.L., Hirst B.H. Differential surface characteristics of M cells from mouse intestinal Peyer's and cecal patches. Histochemical Journal 1994, 26:271-280.
14. Kitagawa H., Shiraishi S., Imagawa T., Uehara M. Ultrastructural characteristics and lectin-binding properties of M cells in the follicle-associated epithelium of chicken caecal tonsils. Journal of Anatomy 2000, 197:607-616.
15. Miller H., Zhang J., KuoLee R., Patel G.B., Chen W. Intestinal M cells: the fallible sentinels?. World Journal of Gastroenterology 2007, 13:1477-1486.
16. Savidge T.C. The life and times of an intestinal M cell. Trends in Microbiology 1996, 4:301-306.
17. Verbrugghe P., Kujala P., Waelput W., Peters P.J., Cuvelier C.A. Clusterin in human gut-associated lymphoid tissue, tonsils, and adenoids: localization to M cells and follicular dendritic cells. Histochemistry and Cell Biology 2008, 129:311-320.
18. Owen R.L., Jones A.L. Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles. Gastroenterology 1974, 66:189-203.
19. Finzi G., Cornaggia M., Capella C., Fiocca R., Bosi F., Solcia E., Samloff I.M. Cathepsin E in follicle associated epithelium of intestine and tonsils: localization to M cells and possible role in antigen processing. Histochemistry 1993, 99:201-211.
20. Pappo J., Mahlman R.T. Follicle epithelial M cells are a source of interleukin-1 in Peyer's patches. Immunology 1993, 78:505-507.
21. Lee J.-H., Kong S.-K., Wu Z.-S., Wu Q., Choe J., Cho H.Y., Ha S.Y., Kee S.H., Kim Y.-S. Class II β-tubulin is a novel marker for human tonsillar M cells and follicular dendritic cells. Journal of Oral Pathology and Medicine 2010, 39:533-539.
22. Koshi R., Mustafa Y., Perry M.E. Vimentin, cytokeratin 8 and cytokeratin 18 are not specific markers for M-cells in the human palatine tonsils. Journal of Anatomy 2001, 199:663-674.
23. Wong N.A.C.S., Herriot M., Rae F. An immunohistochemical study and review of potential markers of human intestinal M cells. European Journal of Histochemistry 2003, 47:143-150.
24. Giannasca P.J., Giannasca K.T., Leichtner A.M., Neutra M.R. Human intestinal M cells display the sialyl Lewis A antigen. Infection and Immunity 1999, 67:946-953.
25. Pielage J.F., Cichon C., Greune L., Hirashima M., Kucharzik T., Schmidt M.A. Reversible differentiation of Caco-2 cells reveals galectin-9 as a surface marker molecule for human follicle-associated epithelia and M cell-like cells. International Journal of Biochemistry and Cell Biology 2007, 39:1886-1901.
26. Nagura H., Ohtani H., Masuda T., Kimura M., Nakamra S. HLA-DR expression on M cells overlying Peyer's patches is a common feature of human small intestine. Acta Pathologica Japonica 1991, 41:818-823.
27. Kucharzik T., Lügering N., Schmid K.W., Schmidt M.A., Domschke W. Human intestinal M cells exhibit enterocyte-like intermediate filaments. Gut 1998, 42:54-62.
28. Clark M.A., Jepson M.A., Simmons N.L., Booth T.A., Hirst B.H. Differential expression of lectin-binding sites defines mouse intestinal M-cells. Journal of Histochemistry and Cytochemistry 1993, 41:1679-1687.
29. Smith M.W., Peacock M.A. M cell distribution in follicle-associated epithelium of mouse Peyer's patch. American Journal of Anatomy 1980, 159:167-175.
30. 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, 86:789-801.
31. Mach J., Hshieh T., Hsieh D., Grubbs N., Chervonsky A. Development of intestinal M cells. Immunological Reviews 2005, 206:177-189.
32. Owen R.L., Pierce N.F., Apple R.T., Cray W.C. M cell transport of Vibrio cholerae from the intestinal lumen into Peyer's patches: a mechanism for antigen sampling and for microbial transepithelial migration. Journal of Infectious Diseases 1986, 153:1108-1118.
33. Inman L.R., Cantey J.R. Specific adherence of Escherichia coli (Strain RDEC-1) to membranous (M) cells of the Peyer's patch in Escherichia coli diarrhea in the rabbit. Journal of Clinical Investigation 1983, 71:1-8.
34. Owen R.L., Bhalla D.K. Cytochemical analysis of alkaline phosphatase and esterase activities and of lectin-binding and anionic sites in rat and mouse Peyer's patch M cells. American Journal of Anatomy 1983, 168:199-212.
35. Smith M.W., James P.S., Tivey D.R. M cell numbers increase after transfer of SPF mice to a normal animal house environment. American Journal of Pathology 1987, 128:385-389.
36. Clark M.A., Jepson M.A., Hirst B.H. Lectin binding defines and differentiates M-cells in mouse small intestine and caecum. Histochemistry and Cell Biology 1995, 104:161-168.
37. D'Souza B., Bhowmik T., Shashidharamurthy R., Oettinger C., Selvaraj P., D'Souza M. Oral microparticle vaccine for melanoma using M-cell targeting. Journal of Drug Targeting 2012, 20:166-173.
38. Giannasca P.J., Giannasca K.T., Falk P., Gordon J.I., Neutra M.R. Regional differences in glycoconjugates of intestinal M cells in mice: potential targets for mucosal vaccines. American Journal of Physiology 1994, 267:G1108-G1121.
39. Clark M.A., Jepson M.A., Simmons N.L., Hirst B.H. Selective binding and transcytosis of Ulex europaeus 1 lectin by mouse Peyer's patch M-cells in vivo. Cell and Tissue Research 1995, 282:455-461.
40. Jepson M.A., Mason C.M., Clark M.A., Simmons N.L., Hirst B.H. Variations in lectin binding properties of intestinal M cells. Journal of Drug Targeting 1995, 3:75-77.
41. Sharma R., Van Damme E.J., Peumans W.J., Sarsfield P., Schumacher U. Lectin binding reveals divergent carbohydrate expression in human and mouse Peyer's patches. Histochemistry and Cell Biology 1996, 106:459-465.
42. Foster N., Clark M.A., Jepson M.A., Hirst B.H. Ulex europaeus 1 lectin targets microspheres to mouse Peyer's patch M-cells in vivo. Vaccine 1998, 16:536-541.
43. Terahara K., Nochi T., Yoshida M., Takahashi Y., Goto Y., Hatai H., Kurokawa S., Jang M.H., Kweon M.-N., Domino S.E., Hiroi T., Yuki Y., Tsunetsugu-Yokota Y., Kobayashi K., Kiyono H. Distinct fucosylation of M cells and epithelial cells by Fut1 and Fut2, respectively, in response to intestinal environmental stress. Biochemical and Biophysical Research Communications 2011, 404:822-828.
44. Drickamer K. Making a fitting choice: common aspects of sugar-binding sites in plant and animal lectins. Structure 1997, 5:465-468.
45. Woodley J.F. Lectins for gastrointestinal targeting - 15 years on. Journal of Drug Targeting 2000, 7:325-333.
46. Sharon N., Lis H. History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 2004, 14:53R-62R.
47. Naeem A., Saleemuddin M., Khan R.H. Glycoprotein targeting and other applications of lectins in biotechnology. Current Protein and Peptide Science 2007, 8:261-271.
48. Sharon N. Lectins: past, present and future. Biochemical Society Transactions 2008, 36:1457-1460.
49. Kernéis S., Bogdanova A., Colucci-Guyon E., Kraehenbuhl J.-P., Pringault E. Cytosolic distribution of villin in M cells from mouse Peyer's patches correlates with the absence of a brush border. Gastroenterology 1996, 110:515-521.
50. Clark M.A., Hirst B.H., Jepson M.A. M-cell surface β1 integrin expression and invasion-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer's patch M cells. Infection and Immunity 1998, 66:1237-1243.
51. Verbrugghe P., Waelput W., Dieriks B., Waeytens A., Vandesompele J., Cuvelier C.A. Murine M cells express annexin V specifically. Journal of Pathology 2006, 209:240-249.
52. Clark M.A., Hirst B.H. Expression of junction-associated proteins differentiates mouse intestinal M cells from enterocytes. Histochemistry and Cell Biology 2002, 118:137-147.
53. Terahara K., Yoshida M., Igarashi O., Nochi T., Soares Pontes G., Hase K., Ohno H., Kurokawa S., Mejima M., Takayama N., Yuki Y., Lowe A.W., Kiyono H. Comprehensive gene expression profiling of Peyer's patch M cells, villous M-like cells, and intestinal epithelial cells. Journal of Immunology 2008, 180:7840-7846.
54. Hase K., Kawano K., Nochi T., Soares Pontes G., Fukuda S., Ebisawa M., Kadokura K., Tobe T., Fujimura Y., Kawano S., Yabashi A., Waguri S., Nakato G., Kimura S., Murakami T., Iimura M., Hamura K., Fukuoka S., Lowe A.W., Itoh K., Kiyono H., Ohno H. Uptake through glycoprotein 2 of FimH(+) bacteria by M cells initiates mucosal immune response. Nature 2009, 462:226-230.
55. Kawano K., Ebisawa M., Hase K., Fukuda S., Hijikata A., Kawano S., Date Y., Tsuneda S., Itoh K., Ohno H. Psg18 is specifically expressed in follicle-associated epithelium. Cell Structure and Function 2007, 32:115-126.
56. Takata S., Ohtani O., Watanabe Y. Lectin binding patterns in rat nasal-associated lymphoid tissue (NALT) and the influence of various types of lectin on particle uptake in NALT. Archives of Histology and Cytology 2000, 63:305-312.
57. Rautenberg K., Cichon C., Heyer G., Demel M., Schmidt M.A. Immunocytochemical characterization of the follicle-associated epithelium of Peyer's patches: anti-cytokeratin 8 antibody (clone 4.1.18) as a molecular marker for rat M cells. European Journal of Cell Biology 1996, 71:363-370.
58. Rautenberg K., Cichon C., Schmidt M.A. Towards targeting strategies for oral immunization-identification of marker antigens in rat M cells. Behring Institute Mitteilungen 1997, 98:361-375.
59. Flint N., Pemberton P.W., Lobley R.W., Evans G.S. Cytokeratin expression in epithelial cells isolated from the crypt and villus regions of the rodent small intestine. Epithelial Cell Biology 1994, 3:16-23.
60. Perry M.E. The specialized structure of crypt epithelium in the human palatine tonsil and its functional significance. Journal of Anatomy 1994, 185:111-127.
61. Casteleyn C., Breugelmans S., Simoens P., Van den Broeck W. The tonsils revisited: review of the anatomical localization and histological characteristics of the tonsils of domestic and laboratory animals. Clinical and Developmental Immunology 2011, (open access journal; doi: 10.1155/2011/472460).
62. Mage R.G., Lanning D., Knight K.L. B cell and antibody repertoire development in rabbits: the requirement of gut-associated lymphoid tissues. Developmental and Comparative Immunology 2006, 30:137-153.
63. Casteleyn C., Broos A.M.C., Simoens P., Van den Broeck W. Nasal cavity-associated lymphoid tissue (NALT) in the rabbit. Veterinary Immunology and Immunopathology 2010, 133:212-218.
64. Gebert A. M-cells in the rabbit tonsil exhibit distinctive glycoconjugates in their apical membranes. Journal of Histochemistry and Cytochemistry 1996, 44:1033-1042.
65. Gebert A. M cells in the rabbit palatine tonsil: the distribution, spatial arrangement and membrane subdomains as defined by confocal lectin histochemistry. Anatomy and Embryology 1997, 195:353-358.
66. Gebert A. Identification of M-cells in the rabbit tonsil by vimentin immunohistochemistry and in vivo protein transport. Histochemistry and Cell Biology 1995, 104:211-220.
67. Carapelli A., Regoli M., Nicoletti C., Ermini L., Fonzi L., Bertelli E. Rabbit tonsil-associated M-cells express cytokeratin 20 and take up particulate antigen. Journal of Histochemistry and Cytochemistry 2004, 52:1323-1331.
68. Jepson M.A., Mason C.M., Bennett M.K., Simmons N.L., Hirst B.H. Co-expression of vimentin and cytokeratins in M cells of rabbit intestinal lymphoid follicle-associated epithelium. Histochemical Journal 1992, 24:33-39.
69. Fonzi L., Masucci A., Gasparoni A., Bertelli E. Cytokeratin 20-expressing M cells in tonsils take up particulate antigen. A site for the delivery of vaccines against oral pathogens?. Bulletin du Groupement International Pour la Recherche Scientifique En Stomatologie et Odontologie 2004, 46:72-77.
70. Gebert A., Hach G., Bartels H. Co-localization of vimentin and cytokeratins in M cells of rabbit gut-associated lymphoid tissue (GALT). Cell and Tissue Research 1992, 269:331-340.
71. Jepson M.A., Simmons N.L., Hirst G.L., Hirst B.H. Identification of M cells and their distribution in rabbit intestinal Peyer's patches and appendix. Cell and Tissue Research 1993, 273:127-136.
72. Lelouard H., Reggio H., Mangeat P., Neutra M., Montcourrier P. Mucin-related epitopes distinguish M cells and enterocytes in rabbit appendix and Peyer's patches. Infection and Immunity 1999, 67:357-367.
73. Gaǐdar IuA. Vimentin-positive epithelial cells in aggregated lymphoid nodules (Peyer's patches) in rabbits. Arkhiv Anatomii, Gistologii i Embryologii 1989, 97:84-88.
74. Gebert A., Hach G. Differential binding of lectins to M cells and enterocytes in the rabbit cecum. Gastroenterology 1993, 105:1350-1361.
75. Pappo J. Generation and characterization of monoclonal antibodies recognizing follicle epithelial M cells in the rabbit gut-associated lymphoid tissues. Cellular Immunology 1989, 120:31-41.
76. Ermak T.H., Steger H.J., Pappo J. Phenotypically distinct subpopulations of T cells in domes and M cells pockets of the rabbit gut-associated lymphoid tissue. Immunology 1990, 71:530-537.
77. Pappo J., Ermak T.H., Steger H.J. Monoclonal antibody-directed targeting of fluorescent polystyrene microspheres to Peyer's patch M cells. Immunology 1991, 73:277-280.
78. Lelouard H., Sahuquet A., Reggio H., Montcourrier P. Rabbit M cells and dome enterocytes are distinct cell lineages. Journal of Cell Science 2001, 114:2077-2083.
79. Lelouard H., Reggio H., Roy C., Sahuquet A., Mangeat P., Montcourrier P. Glycocalix on rabbit intestinal M cells displays carbohydrate epitopes from Muc2. Infection and Immunity 2001, 69:1061-1071.
80. Roy M.J. Precocious development of lectin (Ulex europaeus agglutinin I) receptors in dome epithelium of gut-associated lymphoid tissues. Cell and Tissue Research 1987, 248:483-489.
81. Gebert A., Rothkötter H.J., Pabst R. Cytokeratin 18 is an M-cell marker in porcine Peyer's patches. Cell and Tissue Research 1994, 276:213-221.
82. Torres-Medina A. Morphological characteristics of the intestinal surface of aggregated lymphoid follicles (Peyer's patches) in the small intestine of newborn gnotobiotic calves and pigs. American Journal of Veterinary Research 1981, 42:232-236.
83. Jeong K.-I., Sohn Y.-S., Ahn K., Choi C., Han D.U., Chae C. Lectin Histochemistry of Peyer's patches in the porcine ileum. Journal of Veterinary Medical Science 2002, 64:535-538.
84. Hondo T., Kanaya T., Takakura I., Watanabe H., Takahashi Y., Nagasawa Y., Terada S., Ohwada S., Watanabe K., Kitazawa H., Rose M.T., Yamaguchi T., Aso H. Cytokeratin 18 is a specific marker of bovine intestinal M cell. American Journal of Physiology-Gastrointestinal and Liver Physiology 2011, 300:G442-G453.
85. Kumar P., Timoney J.F., Sheoran A.S. M cells and associated lymphoid tissue of the equine nasopharyngeal tonsil. Equine Veterinary Journal 2001, 33:224-230.
86. Kumar P., Timoney J.F. Light and electron microscope studies on the nasopharynx and nasopharyngeal tonsil of the horse. Anatomia, Histologia, Embryologia 2001, 30:77-84.
87. Kumar P., Timoney J.F. Histology and ultrastructure of the equine lingual tonsil, I. Crypt epithelium and associated structures. Anatomia, Histologia, Embryologia 2005, 34:27-33.
88. Kumar P., Timoney J.F. Histology and ultrastructure of the equine lingual tonsil, II. Lymphoid tissue and associated high endothelial venules. Anatomia, Histologia, Embryologia 2005, 34:98-104.
89. Kumar P., Timoney J.F. Histology, immunohistochemistry and ultrastructure of the equine tubal tonsil. Anatomia, Histologia, Embryologia 2005, 34:141-148.
90. Kumar P., Timoney J.F. Histology, immunohistochemistry and ultrastructure of the equine palatine tonsil. Anatomia, Histologia, Embryologia 2005, 34:192-198.
91. Kumar P., Timoney J.F. Histology, immunohistochemistry and ultrastructure of the tonsil of soft palate of the horse. Anatomia, Histologia, Embryologia 2006, 35:1-6.
92. Casteleyn C., Doom M., Lambrechts E., Van den Broeck W., Simoens P., Cornillie P. Locations of gut-associated lymphoid tissue in the 3-month-old chicken: a review. Avian Pathology 2010, 39:143-150.
93. Nagy N., Oláh I. Pyloric tonsil as a novel gut-associated lymphoepithelial organ of the chicken. Journal of Anatomy 2007, 211:407-411.
94. Jeurissen S.H., Wagenaar F., Janse E.M. Further characterization of M cells in gut-associated lymphoid tissues of the chicken. Poultry Science 1999, 78:965-972.
95. Befus A.D., Johnston N., Leslie G.A., Bienenstock J. Gut-associated lymphoid tissue in the chicken, I. Morphology, ontogeny, and some functional characteristics of Peyer's patches. Journal of Immunology 1980, 125:2626-2632.
96. Burns R.B. Histology and immunology of Peyer's patches in the domestic fowl (Gallus domesticus). Research in Veterinary Science 1982, 32:359-367.
97. Burns R.B., Maxwell M.H. Ultrastructure of Peyer's patches in the domestic fowl and turkey. Journal of Anatomy 1986, 147:235-243.
98. Kato A., Hashimoto Y., Kon Y., Sugimura M. Are there M cells on the cecal tonsil of chickens?. Journal of Veterinary Medical Science 1992, 54:999-1006.
99. Kitagawa H., Hiratsuka Y., Imagawa T., Uehara M. Distribution of lymphoid tissue in the caecal mucosa of chickens. Journal of Anatomy 1998, 192:293-298.
100. Kitagawa H., Imagawa T., Uehara M. The apical caecal diverticulum of the chicken identified as a lymphoid organ. Journal of Anatomy 1996, 189:667-672.
101. 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. American Journal of Anatomy 1973, 136:455-477.
102. Sayegh C.E., Ratcliffe M.J.H. Perinatal deletion of B cells expressing surface Ig molecules that lack V(D)J-encoded determinants in the bursa of Fabricius is not due to intrafollicular competition. Journal of Immunology 2000, 164:5041-5048.
103. Jörns J., Mangold U., Neumann U., Van Damme E.J.M., Peumans W.J., Pfüller U., Schumacher U. Lectin histochemistry of the lymphoid organs of the chicken. Anatomy and Embryology 2003, 207:85-94.
104. Pohlmeyer I., Jörns J., Schumacher U., Van Damme E.J.M., Peumans W.J., Pfüller U., Neumann U. Lectin histochemical investigations of the distal gut of chicks with special emphasis on the follicle-associated epithelium. Journal of Veterinary Medicine Series A 2005, 52:138-146.
105. Brayden D.J., Jepson M.A., Baird A.W. Intestinal Peyer's patch M cells and oral vaccine targeting. Drug Discovery Today 2005, 10:1145-1157.
106. Brayden D.J., Baird A.W. Apical membrane receptors on intestinal M cells: potential targets for vaccine delivery. Advanced Drug Delivery Reviews 2004, 56:721-726.
107. Misumi S., Masuyama M., Takamune N., Nakayama D., Mitsumata R., Matsumoto H., Urata N., Takahashi Y., Muneoka A., Sukamoto H., Fukuzaki K., Shoji S. Targeted delivery of immunogen to primate M cells with tetragalloyl lysine dendrimer. Journal of Immunology 2009, 182:6061-6070.
108. Jepson M.A., Clark M.A., Hirst B.H. M cell targeting by lectins: a strategy for mucosal vaccination and drug delivery. Advanced Drug Delivery Reviews 2004, 56:511-525.
109. Vyas S.P., Gupta P.N. Implication of nanoparticles/microparticles in mucosal vaccine delivery. Expert Review of Vaccines 2007, 6:401-418.
110. Azizi A., Kumar A., Diaz-Mitoma F., Mestecky J. Enhancing oral vaccine potency by targeting intestinal M cells. PLOS Pathogens 2010, 6:e1001147.
111. Kim S.-H., Lee K.-Y., Jang Y.-S. Mucosal immune system and M cell-targeting strategies for oral mucosal vaccination. Immune Network 2012, 12:165-175.
112. Lai Y.H., D'Souza M.J. Microparticle transport in the human intestinal M cell model. Journal of Drug Targeting 2008, 16:36-42.
113. Chionh Y.-T., Wee J.L.K., Every A.L., Ng G.Z., Sutton P. M-cell targeting of whole killed bacteria induces protective immunity against gastrointestinal pathogens. Infection and Immunity 2009, 77:2962-2970.
114. Foxwell A.R., Cripps A.W., Kyd J.M. Optimization of oral immunization through receptor-mediated targeting of M cells. Human vaccine 2007, 3:220-223.
115. Devriendt B., De Geest B.G., Goddeeris B.M., Cox E. Crossing the barrier: Targeting epithelial receptors for enhanced oral vaccine delivery. Journal of Controlled Release 2012, 160:431-439.
116. Murphy K., Travers P., Walport M. Janeway's immunobiology 2008, Garland Science, London. 7th ed.
117. Roth-Walter F., Bohle B., Schöll I., Untersmayr E., Scheiner O., Boltz-Nitulescu G., Gabor F., Brayden D.J., Jensen-Jarolim E. Targeting antigens to murine and human M cells with Aleuria aurantia lectin-functionalized microparticles. Immunology Letters 2005, 100:182-188.
118. Wilkhu J., McNeil S.E., Kirby D.J., Perrie Y. Formulation design considerations for oral vaccines. Therapeutic Delivery 2011, 2:1141-1164.
119. Garinot M., Fiévez V., Pourcelle V., Stoffelbach F., des Rieux A., Plapied L., Theate I., Freichels H., JérÔme C., Marchand-Brynaert J., Schneider Y.-J., Préat V. PEGylated PLGA-based nanoparticles targeting M cells for oral vaccination. Journal of Controlled Release 2007, 120:195-204.
120. Clark M.A., Blair H., Liang L., Brey R.N., Brayden D., Hirst B. Targeting polymerized liposome vaccine carriers to intestinal M cells. Vaccine 2002, 20:208-217.
121. Azizi A., Ghunaim H., Diaz-Mitoma F., Mestecky J. Mucosal HIV vaccines: a holy grail or a dud?. Vaccine 2010, 28:4015-4026.
122. Carr K.E., Smyth S.H., McCullough M.T., Morris J.F., Moyes S.M. Morphological aspects of interactions between microparticles and mammalan cells: intestinal uptake and onward movement. Progress in Histochemistry and Cytochemistry 2012, 46:185-252.
123. Tyrer P., Foxwell A.R., Kyd J., Harvey M., Sizer P., Cripps A. Validation and quantification of an in vitro M-cell model. Biochemical and Biophysical Research Communications 2002, 299:377-383.
124. Gullberg E., Leonard M., Karlsson J., Hopkins A.M., Brayden D., Baird A.W., Artursson P. Expression of specific markers and particle transport in a new human intestinal M-cell model. Biochemical and Biophysical Research Communications 2000, 279:808-813.
125. van der Lubben I.M., van Opdorp F.A., Hengeveld M.R., Onderwater J.J., Koerten H.K., Verhoef J.C., Borchard G., Junginger H.E. Transport of chitosan microparticles for mucosal vaccine delivery in a human intestinal M-cell model. Journal of Drug Targeting 2002, 10:449-456.
126. Li H.F., Bai R.Y., Xing Y.M., Nie J.M., Diao Y. M cell in vitro model and its application in oral delivery of macromolecular drugs. Yao Xue Xue Bao 2011, 46:1429-1435.
127. Kernéis S., Bogdanova A., Colucci-Guyon E., Kraehenbuhl J.-P., Pringault E. Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport. Science 1997, 277:949-952.
128. Kadiyala I., Loo Y., Roy K., Rice J., Leong K.W. Transport of Chitosan-DNA nanoparticles in human intestinal M-cell model versus normal intestinal enterocytes. European Journal of Pharmaceutical Sciences 2010, 39:103-109.
129. Miyazawa K., Kanaya T., Takakura I., Tanaka S., Hondo T., Watanabe H., Rose M.T., Kitazawa H., Yamaguchi T., Katamine S., Nishida N., Aso H. Transcytosis of murine adapted bovine spongiform encephalopathy agents in an in vitro bovine M cell model. Journal of Virology 2010, 84:12285-12291.
130. Blanco L.P., DiRita V.J. Bacterial-associated cholera toxin and GM1 binding are required for transcytosis of classical biotype Vibrio cholerae through an in vitro M cell model system. Cellular Microbiology 2006, 8:982-998.
131. Martinez-Argudo I., Sands C., Jepson M.A. Translocation of enteropathogenic Escherichia coli across an in vitro M cell model is regulated by its type III secretion system. Cellular Microbiology 2007, 9:1538-1546.
132. Martinez-Argudo I., Jepson M.A. Salmonella translocates across an in vitro M cell model independently of SP-1 and SP-2. Microbiology 2008, 154:3887-3894.
133. Lim J.S., Na H.S., Lee H.C., Choy H.E., Park S.C., Han J.M., Cho K.A. Caveolae-mediated entry of Salmonella typhimurium in a human M-cell model. Biochemical and Biophysical Research Communications 2009, 390:1322-1327.