The role of M cells in mucosal immunity
Open accessAbstract
Mucosa-associated lymphoid tissue in the respiratory and digestive tracts are covered by a specialized epithelium, the follicle-associated epithelium, which includes M cells, which are specialized for the uptake and transcytosis of macromolecules and microorganisms. Following transcytosis, antigens are released to cells of the immune system in lymphoid aggregates beneath the epithelium where antigen processing and presentation and stimulation of specific B and T lymphocytes are achieved. Circulation of the lymphoid cells enables their homing to their original, and other, mucosal sites where they exert the effector function. Such a response may be dominated by secretory immunoglobulin A release and may include cytotoxic T lymphocyte action. Binding of particles to the apical M cell membrane may be nonspecific or due to specific interaction between molecules such as integrins and lectins. Exploiting the specific binding to M cells is an aim for mucosal vaccination, for example to increase the efficiency of uptake of an oral vaccine by its conjugation to an M-cell-specific molecule. Alternatively, an M-cell-specific live vector, such as attenuated Salmonella bacteria, may be used to deliver epitopes of other organisms. Mucosal vaccination efficiency may also be enhanced by a temporary increase in the number of M cells. Therefore, investigation of the properties and ontogeny of M cells must be pursued to allow the development of better mucosal vaccines for the future.
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Lectins selectively bind to carbohydrate residues of epithelial cell glycocalyx and can be used on particle surfaces to target M cells.
“Lectins are proteins that selectively bind to carbohydrate residues of epithelial cells’ glycocalyx and may serve as molecules on particle surface for specifically targeting M cells [103,104].”
From Use of lectin-functionalized particles for oral immunotherapy (2012) · cites this paper as [104]
Lectins binding to the M-cell glycocalyx may serve as specific targeters on carrier systems for antigen or drug delivery to the immune system.
“lectins binding to the M-cell glycocalyx may serve as specific targeters on carrier systems for antigen or drug delivery to the immune system [9,13–15].”
From Characterization of Vibrio cholerae neuraminidase as an immunomodulator for novel formulation of oral allergy immunotherapy (2018) · cites this paper as [9]
M-cells in the follicle-associated epithelium are responsible for uptake and transport of intact particulate structures to mucosa-associated lymphatic tissue.
“M-cells located within the follicle associated epithelium are responsible for uptake and transport of intact particulate structures to the mucosa-associated lymphatic tissue [8,9].”
From Characterization of Vibrio cholerae neuraminidase as an immunomodulator for novel formulation of oral allergy immunotherapy (2018) · cites this paper as [9]
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Jung, H. C., Eckmann, L., Yang, S. K., Panja, A. B., Fierer, J., Morzycka-Wroblewska, E., & Kagnoff, M. F. (1995) · Journal of Clinical Investigation · doi:10.1172/jci117676 · Cited by 1,197 · see citing works
Mestecky, J. F., & McGhee, J. R. (1987) · Advances in immunology · doi:10.1016/s0065-2776(08)60240-0 · Cited by 947 · see citing works
Owen, R. L., & Jones, A. L. (1974) · Gastroenterology · doi:10.1016/s0016-5085(74)80102-2 · Cited by 765 · see citing works
Conversion by Peyer's Patch Lymphocytes of Human Enterocytes into M Cells that Transport Bacteria
Kernéis, S. M., Bogdanova, A. A., Kraehenbühl, J.-P., & Pringault, E. (1997) · Science · doi:10.1126/science.277.5328.949 · Cited by 630 · see citing works
Epithelial M Cells: Gateways for Mucosal Infection and Immunization
Neutra, M. R., Frey, A., & Kraehenbühl, J.-P. (1996) · Cell · doi:10.1016/s0092-8674(00)80106-3 · Cited by 549 · see citing works
Rasmussen, S. J., Eckmann, L., Quayle, A. J., Shen, L., Zhang, Y., Anderson, D. J., Fierer, J., Stephens, R. S., & Kagnoff, M. F. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119136 · Cited by 514 · see citing works
Intestinal M Cells: A Pathway for Entry of Reovirus into the Host
Wolf, J. L., Rubin, D. H., Finberg, R. W., Kauffman, R. S., Sharpe, A. H., Trier, J. S., & Fields, B. N. (1981) · Science · doi:10.1126/science.6259737 · Cited by 483 · see citing works
Intracellular neutralization of virus by immunoglobulin A antibodies.
Mazanec, M. B., Kaetzel, C. S., Lamm, M. E., Fletcher, D., & Nedrud, J. G. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.15.6901 · Cited by 441 · see citing works
Frey, A., Giannasca, K. T., Weltzin, R., Giannasca, P. J., Reggio, H., Lencer, W. I., & Neutra, M. R. (1996) · The Journal of experimental medicine · doi:10.1084/jem.184.3.1045 · Cited by 401 · see citing works
Intravascular and Mucosal Immunoglobulin A: Two Separate but Related Systems of Immune Defense?
Conley, M. E., & DELACROIX, D. L. (1987) · Annals of Internal Medicine · doi:10.7326/0003-4819-106-6-892 · Cited by 377 · see citing works
Clark, M. A., Hirst, B. H., & Jepson, M. A. (1998) · Infection and Immunity · doi:10.1128/iai.66.3.1237-1243.1998 · Cited by 363 · see citing works
Owen, R. L., Pierce, N. F., Apple, R. T., & Cray, W. C. (1986) · The Journal of Infectious Diseases · doi:10.1093/infdis/153.6.1108 · Cited by 350 · see citing works
Brandtzaeg, P., Farstad, I. N., & Haraldsen, G. (1999) · Immunology Today · doi:10.1016/s0167-5699(99)01468-1 · Cited by 278 · see citing works
Structure, Distribution, and Origin of M Cells in Peyer’s Patches of Mouse Ileum
Bye, W. A., Allan, C. H., & Trier, J. S. (1984) · Gastroenterology · doi:10.1016/s0016-5085(24)05125-4 · Cited by 277 · see citing works
Neutra, M., Phillips, T., Mayer, E., & Fishkind, D. (1987) · Cell and Tissue Research · doi:10.1007/bf00215747 · Cited by 253 · see citing works
Preferential interaction of Salmonella typhimurium with mouse Peyer's patch M cells
Clark, M. A., Jepson, M. A., Simmons, N. L., & Hirst, B. H. (1994) · Research in Microbiology · doi:10.1016/0923-2508(94)90031-0 · Cited by 235 · see citing works
Weltzin, R., Lucia-Jandris, P., Michetti, P., Fields, B. N., Kraehenbuhl, J. P., & Neutra, M. R. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.5.1673 · Cited by 230 · see citing works
Self-citationKohbata, S., Yokoyama, H., & Yabuuchi, E. (1986) · Microbiology and Immunology · doi:10.1111/j.1348-0421.1986.tb03055.x · Cited by 218 · see citing works
Pappo, J., & Ermak, T. H. (1989) · PubMed Central · Cited by 216 · see citing works
Transepithelial transport of HIV-1 by intestinal M cells: a mechanism for transmission of AIDS.
Amerongen, H. M., Weltzin, R., Farnet, C. M., Michetti, P., Haseltine, W. A., & Neutra, M. R. (1991) · PubMed · Cited by 208 · see citing works
Inman, L. R., & Cantey, J. R. (1983) · Journal of Clinical Investigation · doi:10.1172/jci110737 · Cited by 205 · see citing works
Autenrieth, I. B., & Firsching, R. (1996) · Journal of Medical Microbiology · doi:10.1099/00222615-44-4-285 · Cited by 197 · see citing works
Owen, R. L., & Bhalla, D. K. (1983) · American Journal of Anatomy · doi:10.1002/aja.1001680207 · Cited by 176 · see citing works
Nasal lymphoid tissue in the rat
Spit, B. J., Hendriksen, E. G. J., Bruijntjes, J. P., & Kuper, C. F. (1989) · Cell and Tissue Research · doi:10.1007/bf00229081 · Cited by 157 · see citing works
Human Intestinal M Cells Display the Sialyl Lewis A Antigen
Giannasca, P. J., Giannasca, K. T., Leichtner, A. M., & Neutra, M. R. (1999) · Infection and Immunity · doi:10.1128/iai.67.2.946-953.1999 · Cited by 155 · see citing works
Laurent, F., Eckmann, L., Savidge, T., Morgan, G., Theodos, C. M., Naciri, M., & Kagnoff, M. F. (1997) · Infection and Immunity · doi:10.1128/iai.65.12.5067-5073.1997 · Cited by 153 · see citing works
Salmonella-induced M-cell formation in germ-free mouse Peyer's patch tissue.
Savidge, T., Mw, S., James, P. S., & Aldred, P. (1991) · PubMed Central · Cited by 151 · see citing works
Ulex europaeus 1 lectin targets microspheres to mouse Peyer's patch M-cells in vivo
Foster, N. M. (1998) · Vaccine · doi:10.1016/s0264-410x(97)00222-3 · Cited by 145 · see citing works
Comparison of Murine Nasal-associated Lymphoid Tissue and Peyer's Patches
Heritage, P., Underdown, B. J., Arsenault, A. L., Snider, D. P., & McDermott, M. R. (1997) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.156.4.97-03017 · Cited by 132 · see citing works
Shyjan, A. M., Bertagnolli, M. M., Kenney, C. J., & Briskin, M. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.8.2851 · Cited by 130 · see citing works
London, S., Rubin, D. H., & Cebra, J. J. (1987) · The Journal of Experimental Medicine · doi:10.1084/jem.165.3.830 · Cited by 118 · see citing works
Allan, C. H., Mendrick, D. L., & Trier, J. S. (1993) · Gastroenterology · doi:10.1016/0016-5085(93)91004-2 · Cited by 113 · see citing works
Finzi, G., Cornaggia, M., Capella, C., Fiocca, R., Bosi, F., Solcia, E., & Samloff, I. M. (1993) · Histochemistry · doi:10.1007/bf00269138 · Cited by 108 · see citing works
Pappo, J., Ermak, T. H., & Steger, H. J. (1991) · PubMed Central · Cited by 101 · see citing works
Cytokeratin 18 is an M-cell marker in porcine Peyer's patches
Gebert, A., Rothk�tter, H.-J., & Pabst, R. (1994) · Cell and Tissue Research · doi:10.1007/bf00306106 · Cited by 97 · see citing works
Klavinskis, L. S., Bergmeier, L. A., Gao, L., Mitchell, E. A., Ward, R. G., Layton, G. T., Brookes, R. H., Meyers, N., & Lehner, T. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.157.6.2521 · Cited by 93 · see citing works
The Development of M Cells in Peyer's Patches Is Restricted to Specialized Dome-Associated Crypts
Gebert, A., Fassbender, S., Werner, K., & Weissferdt, A. (1999) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65410-7 · Cited by 92 · see citing works
Mucosal IgA response to rectally administered antigen formulated in IgA-coated liposomes
Zhou, F. (1995) · Vaccine · doi:10.1016/0264-410x(94)00029-m · Cited by 89 · see citing works
Selective binding and transcytosis of Ulex europaeus 1 lectin by mouse Peyer's patch M-cells in vivo
Clark, M. A., Jepson, M. A., Simmons, N. L., & Hirst, B. H. (1995) · Cell and Tissue Research · doi:10.1007/bf00318877 · Cited by 88 · see citing works
Lectin binding reveals divergent carbohydrate expression in human and mouse Peyer's patches
Sharma, R. P., Damme, E. J. M. V., Peumans, W. J., Sarsfield, P., & Schumacher, U. (1996) · Histochemistry and Cell Biology · doi:10.1007/bf01457659 · Cited by 84 · see citing works
Differential binding of lectins to M cells and enterocytes in the rabbit cecum
Gebert, A., & Hach, G. (1993) · Gastroenterology · doi:10.1016/0016-5085(93)90139-4 · Cited by 77 · see citing works
Differential surface characteristics of M cells from mouse intestinal Peyer's and caecal patches
Clark, M. A., Jepson, M. A., Simmons, N. L., & Hirst, B. H. (1994) · The Histochemical Journal · doi:10.1007/bf00166108 · Cited by 76 · see citing works
Meynell, H. M., Thomas, N. W., James, P. S., Holland, J., Taussig, M., & Nicoletti, C. (1999) · The FASEB Journal · doi:10.1096/fasebj.13.6.611 · Cited by 76 · see citing works
Cellular and molecular partners involved in gut morphogenesis and differentiation
Kédinger, M., Lefèbvre, O., Duluc, I., Freund, J., & Simon-Assmann, P. M. (1998) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1998.0249 · Cited by 75 · see citing works
Safety and immunogenicity of Salmonella typhi Ty21a vaccine in young Thai children
Cryz, S. J., Vanprapar, N., Thisyakorn, U., Olanratmanee, T., Losonsky, G. A., Levine, M. M., & Chearskul, S. (1993) · Infection and Immunity · doi:10.1128/iai.61.3.1149-1151.1993 · Cited by 71 · see citing works
M‐cells are damaged and increased in number in inflamed human ileal mucosa
Cuvelier, C. A., Quatacker, J. R., Mielants, H., Vos, M. D., Veys, E. M., & Roels, H. (1994) · Histopathology · doi:10.1111/j.1365-2559.1994.tb00550.x · Cited by 71 · see citing works
Expression and immunogenicity of a streptococcal M protein epitope inserted in Salmonella flagellin
Newton, S. M. C., Kotb, M., Poirier, T. P., Stocker, B. A. D., & Beachey, E. H. (1991) · Infection and Immunity · doi:10.1128/iai.59.6.2158-2165.1991 · Cited by 63 · see citing works
Immunomorphological Characteristics of Human Peyer’s Patches
Brandtzæg, P., & Bjerke, K. (2009) · Digestion · doi:10.1159/000200396 · Cited by 62 · see citing works
Kaetzel, C. S., Robinson, J., & Lamm, M. E. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.152.1.72 · Cited by 61 · see citing works
Kerneis, S., Bogdanova, A., Colucci-Guyon, E., Kraehenbuhl, J., & Pringault, E. (1996) · Gastroenterology · doi:10.1053/gast.1996.v110.pm8566599 · Cited by 59 · see citing works
Bjerke, K., Brandtzaeg, P., & FAUSA, O. (1988) · PubMed · Cited by 59 · see citing works
Breel, M., van der Ende, M. B., Sminia, T., & Kraal, G. (1988) · PubMed Central · Cited by 58 · see citing works
Debard, N., Sierro, F., & Kraehenbühl, J.-P. (1999) · Seminars in Immunology · doi:10.1006/smim.1999.0174 · Cited by 56 · see citing works
Differential surface characteristics of M cells from mouse intestinal Peyer's and caecal patches
Clark, M. A., Jepson, M. A., Simmons, N. L., et al. (1994) · The Histochemical Journal · doi:10.1007/bf02388442 · Cited by 56 · see citing works
Corthésy, B., Kaufmann, M., Phalipon, A., Peitsch, M. C., Neutra, M. R., & Kraehenbühl, J.-P. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.52.33670 · Cited by 52 · see citing works
Sabin, A. B. (1984) · Clinical Infectious Diseases · doi:10.1093/clinids/6.supplement_2.s391 · Cited by 48 · see citing works
Oral delivery of micro-encapsulated DNA vaccines.
Jones, D. H., Clegg, J. C. S., & Farrar, G. H. (1998) · PubMed · Cited by 46 · see citing works
Kernéis, S. M., & Pringault, E. (1999) · Seminars in Immunology · doi:10.1006/smim.1999.0176 · Cited by 44 · see citing works
M-cells in the rabbit tonsil exhibit distinctive glycoconjugates in their apical membranes.
Gebert, A. (1996) · Journal of Histochemistry & Cytochemistry · doi:10.1177/44.9.8773569 · Cited by 34 · see citing works
Follicle epithelial M cells are a source of interleukin-1 in Peyer's patches.
Pappo, J., & Mahlman, R. T. (1993) · PubMed · Cited by 33 · see citing works
Gebert, A., & Hach, G. (1992) · Histochemistry and Cell Biology · doi:10.1007/bf00271042 · Cited by 31 · see citing works
Conjugation of cholera toxin or its B subunit to liposomes for targeted delivery of antigens
Harokopakis, E., Childers, N. K., Michalek, S. M., Zhang, S. S., & Tomasi, M. (1995) · Journal of Immunological Methods · doi:10.1016/0022-1759(95)00102-g · Cited by 31 · see citing works
Expression of ICAM-I on M cells covering isolated lymphoid follicles of the human colon.
Ueki, T., Mizuno, M., Uesu, T., Kiso, T., & Tsuji, T. (1995) · PubMed · doi:10.18926/amo/30412 · Cited by 27 · see citing works
Kato, T. (1990) · Gastroenterologia Japonica · doi:10.1007/bf02785325 · Cited by 25 · see citing works
The Rabbit M-Cell Marker Vimentin is Present in Epithelial Cells of the Tonsil Crypt
Gebert, A., Willführ, B., & Pabst, R. (1995) · Acta Oto-Laryngologica · doi:10.3109/00016489509139389 · Cited by 24 · see citing works
Application of Basic Principles of Mucosal Immunity to Vaccine Development
Staats, H. F., & McGhee, J. R. (1996) · Elsevier eBooks · doi:10.1016/b978-012410580-5/50003-0 · Cited by 24 · see citing works
Apoptosis of Villous Epithelial Cells and Follicle-Associated Epithelial Cells in Chicken Cecum.
Takeuchi, T., Kitagawa, H., Imagawa, T., & Uehara, M. (1999) · Journal of Veterinary Medical Science · doi:10.1292/jvms.61.149 · Cited by 22 · see citing works
Gebert, A. (1997) · Anatomy and Embryology · doi:10.1007/s004290050055 · Cited by 21 · see citing works
Expression of ICAM-1 on M cells covering isolated lymphoid follicles of the human colon
亨, 植. (1995) · Institutional Repositories DataBase (IRDB) · doi:10.11501/3104897 · Cited by 11 · see citing works
Oral Tolerance and Anti-Pathological Vaccines
Czerkinsky, C. C., Sun, J., & Holmgren, J. R. (1999) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-59951-4_5 · Cited by 8 · see citing works
Sensitized Liposomes as an Antigen Delivery System for the Stimulation of Mucosal Immunity
Velez, C. N., Tonkonogy, S. L., Lichtman, S. N., & Cho, M. J. (1997) · Journal of drug targeting · doi:10.3109/10611869708995854 · Cited by 8 · see citing works
Chloride conductance and intracellular chloride accumulation in mouse Peyer's patch enterocytes.
Cremaschi, D., James, P. S., Rossetti, C., & Mw, S. (1990) · The Journal of Physiology · doi:10.1113/jphysiol.1990.sp018161 · Cited by 6 · see citing works
Selective binding and transcytosis of Ulex europaeus 1 lectin by mouse Peyer?s patch M-cells in vivo
Clark, M. A., Jepson, M. A., Simmons, N. L., et al. (1995) · Cell and Tissue Research · doi:10.1007/s004410050496 · Cited by 4 · see citing works
Cytokeratin 18 is an M-cell marker in porcine Peyer's patches
Gebert, A., Rothk�tter, H.-J., & Pabst, R. (1994) · Cell and Tissue Research · doi:10.1007/s004410050083 · Cited by 3 · see citing works
Bronchial epithelium associated to lymphoid tissue does not selectively express vimentin.
Alonso, L. M., Cortés, A., Barrutia, M. G., Romo, T., Varas, A., & Zapata, A. G. (1997) · PubMed · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Chylomicrons promote intestinal absorption of lipopolysaccharides
Ghoshal, S., Witta, J., Zhong, J., de Villiers, W., & Eckhardt, E. (2009) · Journal of Lipid Research · doi:10.1194/jlr.m800156-jlr200 · Cited by 662 · see citing works
Intestinal barrier dysfunction in inflammatory bowel diseases
McGuckin, M. A., Eri, R., Simms, L. A., Florin, T. H. J., & Radford-Smith, G. (2009) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20539 · Cited by 627 · see citing works
Chitosan-based delivery systems for protein therapeutics and antigens
Amidi, M., Mastrobattista, E., Jiskoot, W., & Hennink, W. E. (2009) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2009.11.009 · Cited by 622 · see citing works
Manco, M., Putignani, L., & Bottazzo, G. F. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0030 · Cited by 479 · see citing works
The Role of Gut Microbiota on Insulin Resistance
Caricilli, A. M., & Saad, M. A. (2013) · Nutrients · doi:10.3390/nu5030829 · Cited by 273 · see citing works
Exploiting M cells for drug and vaccine delivery
Clark, M. A. (2001) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(01)00149-1 · Cited by 247 · see citing works
Metabolic endotoxemia: a molecular link between obesity and cardiovascular risk
Neves, A. L., Coelho, J., Couto, L., Leite-Moreira, A., & Roncon-Albuquerque, R. (2013) · Journal of Molecular Endocrinology · doi:10.1530/jme-13-0079 · Cited by 211 · see citing works
Influence of the gastrointestinal microbiota on development of the immune system in young animals.
Bauer, E., Williams, B. A., Smidt, H., Verstegen, M. W. A., & Mosenthin, R. (2006) · PubMed · Cited by 210 · see citing works
Current Understanding of Gastrointestinal Immunoregulation and Its Relation to Food Allergy
Brandtzæg, P. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04131.x · Cited by 208 · see citing works
Plant-produced vaccines: promise and reality
Rybicki, E. P. (2008) · Drug Discovery Today · doi:10.1016/j.drudis.2008.10.002 · Cited by 203 · see citing works
Mechanistic study of the adjuvant effect of biodegradable nanoparticles in mucosal vaccination
Slütter, B., Plapied, L., Fievez, V., Alonso, M. J., Rieux, A. D., Schneider, Y., van Riet, E., Jiskoot, W., & Véronique Préat, A. (2009) · Journal of Controlled Release · doi:10.1016/j.jconrel.2009.05.011 · Cited by 192 · see citing works
Enhancing Oral Vaccine Potency by Targeting Intestinal M Cells
Azizi, A., Kumar, A., Diaz-Mitoma, F., & Mestecky, J. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001147 · Cited by 180 · see citing works
Weissmann, C., Enari, M., Klöhn, P., Rossi, D., & Flechsig, E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.172403799 · Cited by 161 · see citing works
Targeting polymerised liposome vaccine carriers to intestinal M cells
Clark, M. A., Blair, H. J., Liang, L., Brey, R. N., Brayden, D. J., & Hirst, B. H. (2001) · Vaccine · doi:10.1016/s0264-410x(01)00258-4 · Cited by 130 · see citing works
Endotoxemia, nutrition, and cardiometabolic disorders
Kallio, K. A. E., Hätönen, K. A., Lehto, M., Salomaa, V., Männistö, S., & Pussinen, P. J. (2015) · Acta Diabetologica · doi:10.1007/s00592-014-0662-3 · Cited by 125 · see citing works
Intranasal vaccine: Factors to consider in research and development
Xu, H., Cai, L., Hufnagel, S., & Cui, Z. (2021) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2021.121180 · Cited by 103 · see citing works
Mucosal Vaccination via the Respiratory Tract
Hellfritzsch, M., & Scherließ, R. (2019) · Pharmaceutics · doi:10.3390/pharmaceutics11080375 · Cited by 99 · see citing works
Intranasal vaccination against plague, tetanus and diphtheria
Alpar, H. O., Eyles, J. E., Williamson, E. D., & Somavarapu, S. (2001) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(01)00166-1 · Cited by 91 · see citing works
Espinosa, J. C., Morales, M., Castilla, J., Rogers, M. S., & Torres, J. M. (2007) · Journal of General Virology · doi:10.1099/vir.0.82647-0 · Cited by 86 · see citing works
Drainage of Tears: Impact on the Ocular Surface and Lacrimal System
Paulsen, F. P., Schaudig, U. H., & Thale, A. B. (2003) · The Ocular Surface · doi:10.1016/s1542-0124(12)70013-7 · Cited by 78 · see citing works
Physiopathology of intestinal barrier and the role of zonulin
Caviglia, G. P., Rosso, C., Ribaldone, D. G., Dughera, F., Fagoonee, S., Astegiano, M., & Pellicano, R. (2019) · Minerva Biotecnologica · doi:10.23736/s1120-4826.19.02554-0 · Cited by 76 · see citing works
Weissmann, C., Enari, M., Klöhn, P., Rossi, D., & Flechsig, E. (2002) · The Journal of Infectious Diseases · doi:10.1086/344575 · Cited by 75 · see citing works
Antigen Delivery to Mucosa-Associated Lymphoid Tissues Using Liposomes as a Carrier
Zhou, F., & Neutra, M. R. (2002) · Bioscience Reports · doi:10.1023/a:1020103109483 · Cited by 73 · see citing works
das Neves, J., Arzi, R. S., & Sosnik, A. (2020) · Chemical Society Reviews · doi:10.1039/c8cs00948a · Cited by 72 · see citing works
In Vitro Adhesion Specificity of Indigenous Lactobacilli within the Avian Intestinal Tract
Edelman, S., Westerlund‐Wikström, B., Leskelä, S., Kettunen, H., Rautonen, N., Apajalahti, J., & Korhonen, T. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.10.5155-5159.2002 · Cited by 69 · see citing works
Wang, Y., Ghoshal, S., Ward, M. R., de Villiers, W. J. S., Woodward, J. G., & Eckhardt, E. R. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008442 · Cited by 68 · see citing works
Al-Mariri, A., Tibor, A., Lestrate, P., Mertens, P., Bolle, X. D., & Letesson, J. (2002) · Infection and Immunity · doi:10.1128/iai.70.4.1915-1923.2002 · Cited by 67 · see citing works
Kunisawa, J., Nakagawa, S., & Mayumi, T. (2001) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(01)00214-9 · Cited by 63 · see citing works
Targeting mucosal dendritic cells with microbial antigens from probiotic lactic acid bacteria
Mohamadzadeh, M., Duong, T., Hoover, T. A., & Klaenhammer, T. R. (2008) · Expert Review of Vaccines · doi:10.1586/14760584.7.2.163 · Cited by 60 · see citing works
Kunisawa, J., Nakanishi, T., Takahashi, I., Okudaira, A., Tsutsumi, Y. M., Katayama, K., Nakagawa, S., Kiyono, H., & Mayumi, T. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.3.1406 · Cited by 59 · see citing works
Establishment of Mycobacterium avium subsp. paratuberculosis infection in the intestine of ruminants
Sigurðardóttir, O. (2004) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2003.10.032 · Cited by 58 · see citing works
Prions and the lymphoreticular system
Weissmann, C., Raeber, A. J., Montrasio, F., Hegyi, I., Frigg, R., Klein, M. A., & Aguzzi, A. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2000.0763 · Cited by 57 · see citing works
Recent Advances in Cell‐Based In Vitro Models to Recreate Human Intestinal Inflammation
Macedo, M. H., Neto, M. D., Pastrana, L. M., Gonçalves, C., & Xavier, M. (2023) · Advanced Science · doi:10.1002/advs.202301391 · Cited by 56 · see citing works
M cell-targeted delivery of vaccines and therapeutics
KuoLee, R., & Chen, W. (2008) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.5.6.693 · Cited by 54 · see citing works
Wang, Y., Ghoshal, S., Ward, M. R., de Villiers, W. J. S., Woodward, J. G., & Eckhardt, E. R. M. (2010) · PLoS ONE · doi:10.1371/annotation/bc95caf3-62cf-4ecd-8a79-9116e62f4a50 · Cited by 54 · see citing works
M cell-derived vesicles suggest a unique pathway for trans-epithelial antigen delivery
Sakhon, O. S., Ross, B. N., Gusti, V., Pham, A. J., Vu, K., & Lo, D. D. (2015) · Tissue Barriers · doi:10.1080/21688370.2015.1004975 · Cited by 53 · see citing works
Cell-based in vitro models for intestinal permeability studies
Pereira, C., Costa, J. R., Sarmento, B. F. C. C., & Araújo, F. (2015) · Elsevier eBooks · doi:10.1016/b978-0-08-100094-6.00005-5 · Cited by 53 · see citing works
Bioadhesive nanoparticles of fungal chitosan for oral DNA delivery
Plapied, L., Vandermeulen, G., Vroman, B., Véronique Préat, A., & Rieux, A. D. (2010) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2010.07.041 · Cited by 51 · see citing works
Corr, S. C., Hill, C., & Gahan, C. G. M. (2006) · Microbial Pathogenesis · doi:10.1016/j.micpath.2006.08.003 · Cited by 50 · see citing works
Immunological Foundations to the Quest for New Vaccine Adjuvants
Burdin, N., Guy, B., & Moingeon, P. E. (2004) · BioDrugs · doi:10.2165/00063030-200418020-00002 · Cited by 49 · see citing works
Functional Anatomy and Immunological Interactions of Ocular Surface and Adnexa
Paulsen, F. P. (2008) · KARGER eBooks · doi:10.1159/000131068 · Cited by 47 · see citing works
Ryz, N. R., Lochner, A., Bhullar, K., Ma, C., Huang, T., Bhinder, G., Bosman, E. S., Wu, X., Innis, S. M., Jacobson, K., et al. (2015) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00006.2015 · Cited by 46 · see citing works
Weissmann, C., Enari, M., Klöhn, P., Rossi, D., & Flechsig, E. (2002) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2002-1434 · Cited by 43 · see citing works
Conjunctiva-associated lymphoid tissue in avian mucosal immunity
van Ginkel, F. W., Gulley, S. L., Lammers, A., Hoerr, F. J., Gurjar, R. S., & Toro, H. (2011) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2011.04.012 · Cited by 41 · see citing works
Invited Review: Ruminal microbes, microbial products, and systemic inflammation
Garcia, M., Bradford, B. J., & Nagaraja, T. G. (2017) · The Professional Animal Scientist · doi:10.15232/pas.2017-01663 · Cited by 41 · see citing works
Use of lectin-functionalized particles for oral immunotherapy
Diesner, S. C., Wang, X.-Y., Jensen-Jarolim, E., Untersmayr, E., & Gabor, F. (2012) · Therapeutic Delivery · doi:10.4155/tde.11.146 · Cited by 40 · see citing works
Gene transfer approaches for the treatment of inflammatory bowel disease
Wirtz, S. J., & Neurath, M. F. (2003) · Gene Therapy · doi:10.1038/sj.gt.3302013 · Cited by 39 · see citing works
Rey, C., Chang, Y., Latour‐Lambert, P., Varet, H., Proux, C., Legendre, R., Coppée, J., & Enninga, J. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008446 · Cited by 37 · see citing works
Regulation of oral antigen delivery early in life: Implications for oral tolerance and food allergy
Yokanovich, L. T., Newberry, R. D., & Knoop, K. A. (2021) · Clinical & Experimental Allergy · doi:10.1111/cea.13823 · Cited by 36 · see citing works
Stanley, A. C., Huntley, J. F., Jeffrey, M., & Buxton, D. (2001) · Journal of Comparative Pathology · doi:10.1053/jcpa.2001.0506 · Cited by 35 · see citing works
Mucosal immunity and viral infections
Freiborst, J., & Ogra, P. L. O. (2001) · Annals of Medicine · doi:10.3109/07853890109002074 · Cited by 35 · see citing works
In vitro M‐like cells genesis through a tissue‐engineered triple‐culture intestinal model
Araújo, F., Pereira, C., Costa, J. R., Barrias, C. C., Granja, P. L., & Sarmento, B. F. C. C. (2015) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.33508 · Cited by 34 · see citing works
Expression and Manufacture of Pharmaceutical Proteins in Genetically Engineered Horticultural Plants
Chen, Q. (2011) · Taylor & Francis eBooks · doi:10.1201/b10952-5 · Cited by 34 · see citing works
Formulation Design Considerations for Oral Vaccines
Wilkhu, J. S., McNeil, S. E., Kirby, D. J., & Perrie, Y. (2011) · Therapeutic Delivery · doi:10.4155/tde.11.82 · Cited by 33 · see citing works
Biomimetic design in microparticulate vaccines
Keegan, M. E., Whittum‐Hudson, J. A., & Saltzman, W. M. (2003) · Biomaterials · doi:10.1016/s0142-9612(03)00351-x · Cited by 32 · see citing works
Ellis, J. A., Krakowka, G. S., Dayton, A. D., & Konoby, C. (2002) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.2002.220.43 · Cited by 29 · see citing works
Lessons Learned from Protective Immune Responses to Optimize Vaccines against Cryptosporidiosis
Lemieux, M., Sonzogni-Desautels, K., & Ndao, M. (2017) · Pathogens · doi:10.3390/pathogens7010002 · Cited by 28 · see citing works
Ultramicroscopic Examination of the Ovine Tonsillar Epithelia
Casteleyn, C. R., Cornelissen, M., Simoens, P., & Broeck, W. V. D. (2010) · The Anatomical Record · doi:10.1002/ar.21098 · Cited by 26 · see citing works
Apoptotic process of porcine intestinal M cells
Miyazawa, K., Aso, H., Kanaya, T., Kido, T., Minashima, T., Watanabe, K., Ohwada, S., Kitazawa, H., Rose, M. T., Tahara, K., et al. (2005) · Cell and Tissue Research · doi:10.1007/s00441-005-0086-z · Cited by 25 · see citing works
Jobe, M., Agbla, S. C., Todorčević, M., Darboe, B., Danso, E., de Barros, J.-P. P., Lagrost, L., Karpe, F., & Prentice, A. M. (2022) · International Journal of Obesity · doi:10.1038/s41366-022-01193-1 · Cited by 23 · see citing works
Pohlmeyer, I., Jörns, J., Schumacher, U., Van Damme, E. J. M., Peumans, W. J., Pfüller, U., & Neumann, U. (2005) · Journal of Veterinary Medicine Series A · doi:10.1111/j.1439-0442.2005.00696.x · Cited by 20 · see citing works
M cell specific markers in man and domestic animals: Valuable tools in vaccine development
Casteleyn, C. R., Broeck, W. V. D., Gebert, A., Tambuyzer, B. R., Cruchten, S. J. M. V., & Ginneken, C. J. V. (2013) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2013.03.002 · Cited by 20 · see citing works
Advances in Oral Vaccine Delivery Options
Webster, D. E., Gahan, M. E., Strugnell, R. A., & Wesselingh, S. L. (2003) · American Journal of Drug Delivery · doi:10.2165/00137696-200301040-00002 · Cited by 19 · see citing works
Staining patterns for actin and villin distinguish M cells in bovine follicle-associated epithelium
Kanaya, T., Aso, H., Miyazawa, K., Kido, T., Minashima, T., Watanabe, K., Ohwada, S., Kitazawa, H., Rose, M. T., & Yamaguchi, T. (2006) · Research in Veterinary Science · doi:10.1016/j.rvsc.2006.05.009 · Cited by 19 · see citing works
O’Brien, L., Fitzpatrick, E., Baird, A. W., & Campion, D. P. (2008) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2008.04.002 · Cited by 18 · see citing works
The identification of intestinal M cells in the sacculus rotundus and appendix of the Angora rabbit
Beyaz, F., Ergün, E., BAYRAKTAROĞLU, A. G., & Ergün, L. (2010) · Veterinary Research Communications · doi:10.1007/s11259-010-9349-6 · Cited by 16 · see citing works
Particulate transepithelial drug carriers: barriers and functional polymers
Babiuch, K., Gottschaldt, M., Werz, O., & Schubert, U. S. (2012) · RSC Advances · doi:10.1039/c2ra20726e · Cited by 16 · see citing works
Mucosal Immunity - Mucosal Tolerance
Wiedermann, U. (2003) · KARGER eBooks · doi:10.1159/000071551 · Cited by 14 · see citing works
Prakash, S. (2008) · Biologics · doi:10.2147/btt.s2372 · Cited by 12 · see citing works
Prims, S., Pintens, N., Vergauwen, H., Cruchten, S. J. M. V., Ginneken, C. J. V., & Casteleyn, C. R. (2016) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2016.12.009 · Cited by 11 · see citing works
Delivery of Antigens Used for Vaccination: Recent Advances and Challenges
Scherließ, R. (2011) · Therapeutic Delivery · doi:10.4155/tde.11.80 · Cited by 11 · see citing works
Beyaz, F., Ergün, E., BAYRAKTAROĞLU, A. G., & Ergün, L. (2010) · Cell and Tissue Research · doi:10.1007/s00441-010-1005-5 · Cited by 11 · see citing works
Harada, T., Ogawa, Y., Eguchi, M., Fang, S., Sato, M., Uchida, K., Nakayama, H., & Shimoji, Y. (2013) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2013.03.013 · Cited by 11 · see citing works
Modulation of oral vaccine efficacy by the gut microbiota
Hou, Y., Li, J., & Wu, Y. (2025) · npj Vaccines · doi:10.1038/s41541-025-01240-8 · Cited by 10 · see citing works
Recombinant Salmonella Bacteria Vectoring HIV/AIDS Vaccines
Chin’ombe, N. (2013) · The Open Virology Journal · doi:10.2174/1874357901307010121 · Cited by 10 · see citing works
Breugelmans, S., Spiegelaere, W. D., Casteleyn, C. R., Simoens, P., & Broeck, W. V. D. (2010) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2010.11.005 · Cited by 10 · see citing works
Diesner, S. C., Bergmayr, C., Wang, X.-Y., Heiden, D., Exenberger, S., Roth-Walter, F., Starkl, P., Ret, D., Pali-Schöll, I., Gabor, F., et al. (2018) · Clinical Immunology · doi:10.1016/j.clim.2018.03.017 · Cited by 9 · see citing works
Proteases in intestinal health and disease
Deraison, C., & Vergnolle, N. (2025) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-025-01129-w · Cited by 9 · see citing works
Slavov, E., Georgiev, I. P., Dzhelebov, P., Kanelov, I., Andonova, M., Georgieva, T. M., & Dimitrova, S. (2010) · Veterinary Research Communications · doi:10.1007/s11259-010-9345-x · Cited by 9 · see citing works
Host immune response to Cryptosporidium spp.: Insights and perspectives for vaccine development
Ali, M., Xu, C., Ji, Y., & Li, K. (2025) · Animals and zoonoses. · doi:10.1016/j.azn.2025.01.005 · Cited by 8 · see citing works
Epidemiology of Poultry Salmonellosis: A Review
Akpabio, U. (2015) · Journal of Veterinary Advances · doi:10.5455/jva.20150507071046 · Cited by 8 · see citing works
Ozbilgin, M. K., Polat, S., Mete, U. O., Tap, Ö., & Kaya, M. (2004) · PubMed · Cited by 8 · see citing works
Gut Microbiota and Health: Understanding the Role of Diet
Alasmar, R. M., Kavitha, V., Shanmugakonar, M., & Al‐Naemi, H. A. (2019) · Food and Nutrition Sciences · doi:10.4236/fns.2019.1011097 · Cited by 7 · see citing works
Devekuşunda (Struthio camelus) Konjunktiva İlişkili Lenfoid Doku
BAYRAKTAROĞLU, A. G., Korkmaz, D., Aşti, R. N., Kurtdede, N., & Altunay, H. (2009) · Kafkas Universitesi Veteriner Fakultesi Dergisi · doi:10.9775/kvfd.2010.2455 · Cited by 7 · see citing works
Lactic Acid Bacteria as Mucosal Delivery Vehicles
Wells, J. M., & Mercenier, A. (2003) · Springer eBooks · doi:10.1007/978-1-4615-0191-6_9 · Cited by 7 · see citing works
Novel antigen delivery technologies: a review
Jain, D. K., Jain, V. K., & Singh, R. (2011) · Drug Delivery and Translational Research · doi:10.1007/s13346-011-0014-6 · Cited by 6 · see citing works
Peyer’s Patch: Targeted Drug Delivery for Therapeutics Benefits
Patel, R. P., Shah, P., Barve, K. H., Patel, N. A., & Gandhi, J. (2019) · Springer eBooks · doi:10.1007/978-981-13-3642-3_5 · Cited by 6 · see citing works
Bacterial Interactions with Mucosal Epithelial Cells
Hurwitz, J. L., Orihuela, C. J., DiRita, V. J., & TUOMANEN, E. I. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-415847-4.00049-5 · Cited by 6 · see citing works
Juan Dionisio, C., Alberto Manchego, S., Kim Lam Chiok, C., Nieves Sandoval, C., Juan More, B., Danilo Pezo, C., & Hermelinda Rivera, G. (2014) · Revista de Investigaciones Veterinarias del Perú · doi:10.15381/rivep.v25i2.8486 · Cited by 5 · see citing works
Orally delivered malaria vaccines: not too hard to swallow
Wang, L., Webster, D. E., Wesselingh, S. L., & Coppel, R. L. (2004) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.4.10.1585 · Cited by 5 · see citing works
Immunity in the Gut: Mechanisms and Functions
Brandtzaeg, P. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802241-2.00002-x · Cited by 5 · see citing works
Relatinship Between Insulin Resistance, Diabetes Mellitus and Obesity of Gut Microbiata
Yetkin, İ., Satış, H., & Satış, N. K. (2018) · Turkish Journal of Diabetes and Obesity · doi:10.25048/tjdo.2018.22 · Cited by 5 · see citing works
Role of Chemokine Ligand CCL20 and its Receptor CCR6 in lntestinal Inflammation
Basheer, W., Kunde, D., & Eri, R. D. (2013) · Immunology and Infectious Diseases · doi:10.13189/iid.2013.010203 · Cited by 4 · see citing works
Trivedi, S., & Ranasinghe, C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126487 · Cited by 4 · see citing works
Light and Electron-Microscopic Studies on the Tubal Tonsil of the Buffalo (Bubalus bubalis)
Girgiri, I. A., & Kumar, P. (2020) · Journal of Buffalo Science · doi:10.6000/1927-520x.2019.08.03.08 · Cited by 4 · see citing works
Loss of Sialic Acid Binding Domain Redirects Protein σ1 to Enhance M Cell-Directed Vaccination
Złotkowska, D., Maddaloni, M., Riccardi, C., Walters, N., Holderness, K., Callis, G. M., Rynda‐Apple, A., & Pascual, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036182 · Cited by 4 · see citing works
Innate and Mucosal Immunity in the Developing Gastrointestinal Tract
Martin, C. R., & Walker, W. A. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4377-0134-0.10070-8 · Cited by 4 · see citing works
Roles of zinc in the gut-liver axis
Grüngreiff, K., Reinhold, D., & Maret, W. (2026) · Annals of Hepatology · doi:10.1016/j.aohep.2026.102188 · Cited by 3 · see citing works
Transmission of Bovine Spongiform Encephalopathy
Espinosa, J. C., Morales, M., Herva, M. E., & Torres, J. M. (2006) · Future Virology · doi:10.2217/17460794.1.3.393 · Cited by 3 · see citing works
Bacterial Interactions with Mucosal Epithelial Cells
Orihuela, C. J., Fogg, G. C., DiRita, V. J., & TUOMANEN, E. I. (2005) · Elsevier eBooks · doi:10.1016/b978-012491543-5/50044-9 · Cited by 3 · see citing works
- Authors
- Hathaway, L. J., & Kraehenbuhl*, J.-P.
- Affiliations
- University of Lausanne (CH)
- ORCID
- Hathaway, L. J.
- Venue
- Cellular and Molecular Life Sciences CMLS
- Published
- 2000-02
- Volume
- 57
- Issue
- 2
- Pages
- 323-332
- ISSN
- 1420-682X (ISSN-L)
- 1420-9071
- PMC
- PMC11146756
- OpenAlex
- W2023538174
- Cited by
- 131
- References
- 72
- Citations by year
- 2026: 1 · 2025: 5 · 2023: 2 · 2022: 1 · 2021: 2 · 2020: 4 · 2019: 5 · 2018: 5 · 2017: 3 · 2016: 3 · 2015: 10 · 2014: 4 · 2013: 9 · 2012: 4
- FWCI
- 0.78
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cellular and Molecular Life Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmaceutical Science › Advanced Drug Delivery Systems
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- M cells, mucosal immunity, follicle-associated epithelium, mucosa-associated lymphoid tissue, transcytosis, antigen uptake, antigen presentation, B cells, T cells, secretory IgA, cytotoxic T lymphocytes, integrins, lectins, mucosal immunization, oral vaccine delivery
- MeSH terms
- Animals, Cell Differentiation, Humans, Mucous Membrane, Stem Cells, Vaccines, Antigen Presentation, Immunity, Mucosal
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