Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium
Open accessAbstract
The transcytosis of antigens across the gut epithelium by microfold cells (M cells) is important for the induction of efficient immune responses to some mucosal antigens in Peyer's patches. Recently, substantial progress has been made in our understanding of the factors that influence the development and function of M cells. This review highlights these important advances, with particular emphasis on: the host genes which control the functional maturation of M cells; how this knowledge has led to the rapid advance in our understanding of M-cell biology in the steady state and during aging; molecules expressed on M cells which appear to be used as "immunosurveillance" receptors to sample pathogenic microorganisms in the gut; how certain pathogens appear to exploit M cells to infect the host; and finally how this knowledge has been used to specifically target antigens to M cells to attempt to improve the efficacy of mucosal vaccines.
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M-cells have a plasma membrane rich in specific carbohydrate residues such as α-L fucose and monoganglioside (GM1).
“Since they have a plasma membrane rich in specific carbohydrate residues, such as α-L fucose and monoganglioside (GM1) [10–12]”
From Characterization of Vibrio cholerae neuraminidase as an immunomodulator for novel formulation of oral allergy immunotherapy (2018) · cites this paper as [12]
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“Although the expression of the mature GP2þ M cells was completely absent in the FAE of Spi-B / mice, a small number of mAb NKM 16-2-4þ M cells were evident (B10mAb NKM 16-2-4þ M cells/FAE).(22) One interpretation of these apparently contradictory data is that a small population of M cells in the FAE may mature indepen…”
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The functional maturation of M cells is dramatically reduced in the Peyer's patches of aged mice
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“This specialized microenvironment beneath the M-cell enables the efficient transfer of lumenal antigens to MNP.7,8 Studies show that in the absence of M cells, or antigen sampling by M cells, antigen-specific T-cell responses in the Peyer’s patches of mice orally infected with Salmonella Typhimurium are reduced.2,9 Th…”
BackgroundInfluentialLo, D. D. (2003) · International Immunology · doi:10.1093/intimm/dxh011 · Cited by 83 · see citing works
M cells expressing the complement C5a receptor are efficient targets for mucosal vaccine delivery
Kim, S., Jung, D., Yang, I., Kim, J., Lee, K., Nochi, T., Kiyono, H., & Jang, Y. (2011) · European Journal of Immunology · doi:10.1002/eji.201141592 · Cited by 80 · cited 3× · see citing works
“The conjugation of antigens to either Co1 or OmpH could mediate their delivery to M cells in the Peyer’s patches and induce enhanced mucosal immune responses after oral administration.(53,54)”
BackgroundInvestigation of lectinized liposomes as M-cell targeted carrier-adjuvant for mucosal immunization
Gupta, P. N., & Vyas, S. P. (2010) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2010.08.027 · Cited by 78 · cited 1× · see citing works
“antigen-encapsulated liposomes coupled to UEA-1 (termed lectinized liposomes) also led to increased uptake by Peyer’s patch M cells and the induction of higher antigen-specific secretory IgA responses.(97) Alternative approaches to target antigens to the a(1,2)fucose-containing carbohydrate moiety on M cells have also…”
BackgroundRole of Immunoglobulin A in Protection against Reovirus Entry into Murine Peyer's Patches
Silvey, K. J., Hutchings, A. B., Vajdy, M., Petzke, M. M., & Neutra, M. R. (2001) · Journal of Virology · doi:10.1128/jvi.75.22.10870-10879.2001 · Cited by 78 · cited 1× · see citing works
“Secretory IgA can block lumenal pathogens from binding to gut epithelial cells and in doing so can provide protection against intestinal reovirus infection.(57) Similarly, secretory IgAmay also mediate the lumenal trapping of certain bacteria such as Shigella flexneri retaining them within the mucus layer overlying th…”
BackgroundMeynell, 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 · cited 2× · see citing works
“For example, apparent increases in M-cell-density or antigen transcytosis in the FAE have been described following exposure to S. Typhimurium81 and Streptococcus pneumoniae R36a.82,83 The RANKL- and Spi-B-dependent differentiation ofM cells from immature precursors in the crypts typically takes approximately 4 days,2,…”
BackgroundKotarsky, K., Sitnik, K., Stenstad, H., Kotarsky, H., Schmidtchen, A., Koslowski, M. J., Wehkamp, J., & Agace, W. W. (2009) · Mucosal Immunology · doi:10.1038/mi.2009.115 · Cited by 75 · see citing works
Mucosal immunity and tolerance in the elderly
Fujihashi, K., & McGhee, J. R. (2004) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2004.05.009 · Cited by 74 · see citing works
Borghesi, C., Taussig, M. J., & Nicoletti, C. (1999) · PubMed · Cited by 71 · see citing works
Bermudez, L. E., Petrofsky, M., Sommer, S., & Barletta, R. G. (2010) · Infection and Immunity · doi:10.1128/iai.01411-09 · Cited by 70 · see citing works
Tumanov, A. V., Kuprash, D. V., Mach, J. A., Nedospasov, S. A., & Chervonsky, A. V. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.1.86 · Cited by 69 · cited 1× · see citing works
“However, hematopoietic cell populations within the Peyer’s patches, including theCD11cþ B cells, do not express RANKL,(37) and B-cell-derived TNF and lymphotoxin are each dispensable for the development of FAE andM cells.(45) Although the above studies together provide a plausible model by which lympho-epithelial inte…”
BackgroundCan DCs be distinguished from macrophages by molecular signatures?
Hume, D. A., Mabbott, N., Raza, S., & Freeman, T. C. (2013) · Nature Immunology · doi:10.1038/ni.2516 · Cited by 69 · see citing works
Self-citationBasis for the Age‐related Decline in Intestinal Mucosal Immunity
Schmucker, D. L., Owen, R. L., Outenreath, R. L., & Thoreux, K. (2003) · Journal of Immunology Research · doi:10.1080/10446670310001642168 · Cited by 69 · see citing works
Lack of oral tolerance in aging is due to sequential loss of Peyer's patch cell interactions
Kato, H. (2003) · International Immunology · doi:10.1093/intimm/dxg011 · Cited by 69 · cited 1× · see citing works
“This age-related decline in immune competence is associated with diminished antigenspecific IgA antibody titers in the intestinal lumen(86,89) and a decreased ability to generate tolerance to harmless antigens.(87) Despite the important role of M cells in mucosal immunity in the Peyer’s patches, nothing was known abou…”
BackgroundTaylor, R. T., Patel, S. R., Lin, E. E., Butler, B. R., Lake, J. G., Newberry, R. D., & Williams, I. R. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.9.5659 · Cited by 68 · cited 7× · see citing works
“Consistent with this role, Notch and the ligand Jagged1 also appear to influence the patterning ofM cells across 668 VOLUME 6 NUMBER 4 | JULY 2013 |www.nature.com/mi the FAE.30 The optimal distribution of M cells across the FAE may be important to ensure efficient immune surveillance, while at the same time maintainin…”
BackgroundInfluentialSelf-citationListerial invasion protein internalin B promotes entry into ileal Peyer's patches in vivo
Chiba, S., Nagai, T., Hayashi, T., Baba, Y., Nagai, S., & Koyasu, S. (2010) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2010.00292.x · Cited by 66 · see citing works
New Approach for M-Cell-Specific Molecules Screening by Comprehensive Transcriptome Analysis
Nakato, G., Fukuda, S., Hase, K., Goitsuka, R., Cooper, M. D., & Ohno, H. (2009) · DNA Research · doi:10.1093/dnares/dsp013 · Cited by 65 · see citing works
Self-citationSuzuki, H., Sekine, S., Kataoka, K., Pascual, D. W., Maddaloni, M., Kobayashi, R., Fujihashi, K., Kozono, H., McGhee, J. R., & Fujihashi, K. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.05.037 · Cited by 63 · cited 1× · see citing works
“Under these conditions, the mice were shown to be tolerogenic to ovalbumin and were resistant to peripheral challenge due to the generation of antigen-specific regulatory T cells.(102,103)”
BackgroundThe role of M cells of human nasopharyngeal lymphoid tissue in influenza virus sampling
Fujimura, Y., Takeda, M., 伊海, 英., Haruma, K., Akisada, T., Harada, T., Sakai, T., & Ohuchi, M. (2004) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-003-0898-8 · Cited by 63 · see citing works
M cell targeting by a Claudin 4 targeting peptide can enhance mucosal IgA responses
Lo, D. D., Ling, J., & Eckelhoefer, A. H. (2012) · BMC Biotechnology · doi:10.1186/1472-6750-12-7 · Cited by 62 · see citing works
Verbrugghe, P., Kujala, P., Waelput, W., Peters, P. J., & Cuvelier, C. A. (2007) · Histochemistry and Cell Biology · doi:10.1007/s00418-007-0369-4 · Cited by 61 · see citing works
Effects of age on antibody affinity maturation
Dunn‐Walters, D. K., Banerjee, M., & Mehr, R. (2003) · Biochemical Society Transactions · doi:10.1042/bst0310447 · Cited by 60 · see citing works
Aging impacts isolated lymphoid follicle development and function
McDonald, K. G., Leach, M. R., Huang, C. C., Wang, C., & Newberry, R. D. (2011) · Immunity & Ageing · doi:10.1186/1742-4933-8-1 · Cited by 60 · cited 1× · see citing works
“Expression of the chemokine CCL20 was also reduced in the FAE of aged Peyer’s patches, consistentwith data from an independent study of the effects of aging on isolated lymphoid follicles.(90) As a consequence of the impaired CCL20 expression, the attraction cells (including the ‘‘M-cell-inducing’’ CD11cþ B cells(37))…”
BackgroundBrown, K., Wathne, G. J., Sales, J., Bruce, M. E., & Mabbott, N. A. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802695 · Cited by 57 · see citing works
Self-citationCCR6hiCD11cint B cells promote M-cell differentiation in Peyer's patch
Ebisawa, M., Hase, K., Takahashi, D., Kitamura, H., Knoop, K. A., Williams, I. R., & Ohno, H. (2011) · International Immunology · doi:10.1093/intimm/dxq478 · Cited by 57 · see citing works
Self-citationMurine M cells express annexin V specifically
Verbrugghe, P., Waelput, W., Dieriks, B. V., Waeytens, A., Vandesompele, J., & Cuvelier, C. (2006) · The Journal of Pathology · doi:10.1002/path.1970 · Cited by 55 · see citing works
Annexin A5 Binds to Lipopolysaccharide and Reduces Its Endotoxin Activity
Rand, J. H., Wu, X.-X., Lin, E. Y., Griffel, A., Gialanella, P., & McKitrick, J. C. (2012) · mBio · doi:10.1128/mbio.00292-11 · Cited by 55 · cited 1× · see citing works
“ANXA5 is expressed by immature andmatureMcells(48) and can bind toGram-negative bacteria with high affinity via the lipid A domain of lipopolysaccharide (LPS).(49) The endotoxin activity of LPS is blocked when bound to ANXA5, implying an important anti-inflammatory role to protect the host against LPS-mediated endotox…”
BackgroundTargeted Delivery of Immunogen to Primate M Cells with Tetragalloyl Lysine Dendrimer
Misumi, S., Masuyama, M., Takamune, N., Nakayama, D., Mitsumata, R., Matsumoto, H., Urata, N., Takahashi, Y., Muneoka, A., Sukamoto, T., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802928 · Cited by 53 · cited 1× · see citing works
“Alternative approaches to target antigens to the a(1,2)fucose-containing carbohydrate moiety on M cells have also been explored, for example, by using the non-toxic, smallmolecular UEA-1 mimetic, tetragalloyl-D-lysine dendrimer.(98) The mAb NKM 16-2-4 specifically recognizes the a(1,2)fucose-containing carbohydrate mo…”
MethodEffect of age on susceptibility to Salmonella Typhimurium infection in C57BL/6 mice
Ren, Z., Gay, R., Thomas, A., Pae, M., Wu, D., Logsdon, L. K., Mecsas, J. C., & Meydani, S. N. (2009) · Journal of Medical Microbiology · doi:10.1099/jmm.0.013250-0 · Cited by 51 · cited 1× · see citing works
“For example, the effects of aging on M-cell status may impede the early M-cell-dependent uptake of these pathogens into the Peyer’s patches and in doing so significantly reduce disease susceptibility.(91,92)”
BackgroundResistance of Chemokine Receptor 6-Deficient Mice to Yersinia Enterocolitica Infection
Westphal, S., Lügering, A., Wedel, J., von Eiff, C., Maaser, C., Spahn, T. W., Heusipp, G., Schmidt, M. A., Herbst, H., Williams, I. R., et al. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.070393 · Cited by 50 · see citing works
Self-citationBradford, B. M., Sester, D. P., Hume, D. A., & Mabbott, N. A. (2011) · Immunobiology · doi:10.1016/j.imbio.2011.08.006 · Cited by 47 · see citing works
Self-citationKnoop, K. A., Butler, B. R., Kumar, N., Newberry, R. D., & Williams, I. R. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.06.004 · Cited by 46 · see citing works
Self-citationChionh, Y. T., Wee, J. L. K., Every, A. L., Ng, G. Z., & SUTTON, P. R. N. (2009) · Infection and Immunity · doi:10.1128/iai.01522-08 · Cited by 46 · see citing works
Low-Dose Tolerance Is Mediated by the Microfold Cell Ligand, Reovirus Protein σ1
Rynda, A., Maddaloni, M., Złotkowska, D., Ochoa‐Repáraz, J., Maślanka, T., Crist, K., Riccardi, C., Barszczewska, B., Fujihashi, K., McGhee, J. R., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.8.5187 · Cited by 44 · see citing works
Ponnusamy, D., Periasamy, S., Tripathi, B. N., & Pal, A. (2012) · Research in Veterinary Science · doi:10.1016/j.rvsc.2012.09.023 · Cited by 44 · see citing works
Osanai, A., Sashinami, H., Asano, K., Li, S., Hu, D., & Nakane, A. (2010) · Infection and Immunity · doi:10.1128/iai.00466-10 · Cited by 40 · see citing works
Man, A., Lodi, F., Bertelli, E., Regoli, M., Pin, C., Mulholland, F., Satoskar, A. R., Taussig, M., & Nicoletti, C. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.8.5673 · Cited by 37 · see citing works
CD137 Is Required for M Cell Functional Maturation but Not Lineage Commitment
Hsieh, E.-H., Fernandez, X., Wang, J., Hamer, M., Calvillo, S., Croft, M., Kwon, B. S., & Lo, D. D. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090811 · Cited by 35 · see citing works
Wang, X., Kochetkova, I., Haddad, A., Hoyt, T., Hone, D. M., & Pascual, D. W. (2005) · Vaccine · doi:10.1016/j.vaccine.2005.02.023 · Cited by 35 · see citing works
Wang, J., López‐Fraga, M., Rynko, A. E., & Lo, D. D. (2009) · Cytokine · doi:10.1016/j.cyto.2009.05.001 · Cited by 34 · see citing works
Differential intestinal M‐cell gene expression response to gut commensals
Lapthorne, S., MacSharry, J. A., Scully, P., Nally, K., & Shanahan, F. (2012) · Immunology · doi:10.1111/j.1365-2567.2012.03581.x · Cited by 29 · cited 1× · see citing works
“Fold change in gene expression by M-cell-like differentiated Caco-2 cells when compared with undifferentiated controls (GSE25330, GSE7745).(115)”
BackgroundKobayashi, A., Donaldson, D. S., Kanaya, T., Fukuda, S., Baillie, J. K., Freeman, T. C., Ohno, H., Williams, I. R., & Mabbott, N. A. (2012) · DNA Research · doi:10.1093/dnares/dss022 · Cited by 24 · cited 1× · see citing works
“In the intestine, M cells have also been described within the villous epithelium,(8,11,12) but whether these cells are functionally equivalent to those within the FAE overlying the organized lymphoid follicles remains to be determined.(13)”
BackgroundSelf-citationSirard, J., Didierlaurent, A. M., Cayet, D., Sierro, F., & Rumbo, M. (2009) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2009.03.001 · Cited by 21 · see citing works
Jagged1 and Notch1 help edit M cell patterning in Peyer’s patch follicle epithelium
Hsieh, E.-H., & Lo, D. D. (2012) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2012.04.003 · Cited by 21 · cited 8× · see citing works
“Consistent with this role, Notch and the ligand Jagged1 also appear to influence the patterning ofM cells across 668 VOLUME 6 NUMBER 4 | JULY 2013 |www.nature.com/mi the FAE.30 The optimal distribution of M cells across the FAE may be important to ensure efficient immune surveillance, while at the same time maintainin…”
BackgroundInfluentialNonhuman primate intestinal villous M-like cells: An effective poliovirus entry site
Takahashi, Y., Misumi, S., Muneoka, A., Masuyama, M., Tokado, H., Fukuzaki, K., Takamune, N., & Shoji, S. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.01.120 · Cited by 19 · see citing works
ONISHI, S., MIYATA, H., Inamoto, T., Qi, W.-M., Yamamoto, K., YOKOYAMA, T., Warita, K., Hoshi, N., & KITAGAW, H. (2007) · Journal of Veterinary Medical Science · doi:10.1292/jvms.69.1123 · Cited by 15 · see citing works
Selective transport of staphylococcal enterotoxin A through in vitro generated human M cells
Maresca, M., Dumay, E. M., Fantini, J., & Caporiccio, B. (2007) · Microbes and Infection · doi:10.1016/j.micinf.2007.07.006 · Cited by 15 · cited 1× · see citing works
“Data from in vitro studies imply that M cells may also aid the passage of staphylococcal enterotoxin A across the gut epithelium.(80) Together, these examples show that whereas the sampling of intestinal bacteria by M cells may be important for the induction of specific immunity in the Peyer’s patches, this function h…”
ResultSuzuki, R., Nourani, M. R., Saino‐Saito, S., Abe, H., Nochi, T., Kiyono, H., Spener, F., Kondo, H., & Owada, Y. (2009) · Histochemistry and Cell Biology · doi:10.1007/s00418-009-0638-5 · Cited by 5 · see citing works
Chionh, Y. T., & SUTTON, P. R. N. (2010) · Gut Microbes · doi:10.4161/gmic.1.1.10096 · Cited by 4 · see citing works
Bradford, B. M., Hume, D., & Mabbott, N. A. (2011) · Cited by 3 · see citing works
Self-citationSasaki, I., Hoshino, K., Sugiyama, T., Yamazaki, C., Yano, T., Iizuka, A., Hemmi, H., Tanaka, T., Saito, M., Sugiyama, M., et al. (2012) · Cited by 1 · see citing works
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Intestinal epithelial cells: regulators of barrier function and immune homeostasis
Peterson, L. W., & Artis, D. (2014) · Nature reviews. Immunology · doi:10.1038/nri3608 · Cited by 3,191 · see citing works
A single-cell survey of the small intestinal epithelium
Haber, A. L., Biton, M., Rogel, N., Herbst, R. H., Shekhar, K., Smillie, C., Burgin, G., Delorey, T. M., Howitt, M. R., Katz, Y., et al. (2017) · Nature · doi:10.1038/nature24489 · Cited by 1,750 · see citing works
Regional specialization within the intestinal immune system
Mowat, A. M., & Agace, W. W. (2014) · Nature reviews. Immunology · doi:10.1038/nri3738 · Cited by 1,769 · see citing works
Intra- and Inter-cellular Rewiring of the Human Colon during Ulcerative Colitis
Smillie, C. S., Biton, M., Ordovás-Montañés, J., Sullivan, K. M., Burgin, G., Graham, D. B., Herbst, R. H., Rogel, N., Slyper, M., Waldman, J., et al. (2019) · Cell · doi:10.1016/j.cell.2019.06.029 · Cited by 1,386 · see citing works
“Microfold (M) cells are typically associated with lymphoid tissue in the human small intestine, where they are important for recognition of the gut microbiota (Mabbott et al., 2013).”
BackgroundTales from the crypt: new insights into intestinal stem cells
Gehart, H., & Clevers, H. C. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-018-0081-y · Cited by 984 · see citing works
Intestinal barrier and gut microbiota: Shaping our immune responses throughout life
Takiishi, T., Fenero, C. I. M., & Câmara, N. O. S. (2017) · Tissue Barriers · doi:10.1080/21688370.2017.1373208 · Cited by 1,009 · see citing works
“They also have a specialized follicle epithelium of microfold (M) cells, capable of sampling and transporting antigens from lumen to the underlying immune machinery.(10) M cells can be considered double-edged swords because they mediate the passage of the antigens to the mucosal lymphoid tissue for initiation of immun…”
BackgroundSynthetic Nanoparticles for Vaccines and Immunotherapy
Irvine, D. J., Hanson, M. C., Rakhra, K., & Tokatlian, T. (2015) · Chemical Reviews · doi:10.1021/acs.chemrev.5b00109 · Cited by 770 · see citing works
Homeostatic mini-intestines through scaffold-guided organoid morphogenesis
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Roles of intestinal epithelial cells in the maintenance of gut homeostasis
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Safety Assessment of Graphene-Based Materials: Focus on Human Health and the Environment
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Food allergy: immune mechanisms, diagnosis and immunotherapy
Yu, W., Hussey, D. M., & Nadeau, K. C. (2016) · Nature reviews. Immunology · doi:10.1038/nri.2016.111 · Cited by 676 · see citing works
Xu, M., Qi, Y., Liu, G. H., Song, Y., Jiang, X., & Du, B. (2023) · ACS Nano · doi:10.1021/acsnano.3c05853 · Cited by 647 · see citing works
Leaky Gut As a Danger Signal for Autoimmune Diseases
Mu, Q., Kirby, J. L., Reilly, C. M., & Luo, X. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00598 · Cited by 618 · see citing works
Biology of the RANKL–RANK–OPG System in Immunity, Bone, and Beyond
Walsh, M. C., & Choi, Y. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00511 · Cited by 599 · see citing works
T Helper Cell Cytokines Modulate Intestinal Stem Cell Renewal and Differentiation
Biton, M., Haber, A. L., Rogel, N., Burgin, G., Beyaz, S., Schnell, A., Ashenberg, O., Su, C., Smillie, C. S., Shekhar, K., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.008 · Cited by 580 · see citing works
“Microfold (M) cells are the key sentinels of antigen sampling in the small intestine (Mabbott et al., 2013), but are rare and localized to Peyer's patches.”
Gut Bacteria and Neurotransmitters
Dicks, L. M. T. (2022) · Microorganisms · doi:10.3390/microorganisms10091838 · Cited by 482 · see citing works
“Mucins also regulate the adhesion of microbial cells to the gut wall [79].”
BackgroundMahmud, M. R., Akter, S., Tamanna, S. K., Mazumder, L., Esti, I. Z., Banerjee, S., Akter, S., Hasan, M. R., Acharjee, M., Hossain, M. S., et al. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2096995 · Cited by 498 · see citing works
Oral delivery of therapeutic peptides and proteins: Technology landscape of lipid-based nanocarriers
Haddadzadegan, S., Dorkoosh, F. A., & Bernkop‐Schnürch, A. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.114097 · Cited by 434 · see citing works
Gänger, S., & Schindowski, K. (2018) · Pharmaceutics · doi:10.3390/pharmaceutics10030116 · Cited by 447 · see citing works
“They are also able to transport whole virus, bacteria or even parasites across the epithelium [60,62,64,65], but M cells themselves do not present exogenous antigens [63].”
BackgroundInfluentialHuman gut-associated lymphoid tissues (GALT); diversity, structure, and function
Mörbe, U., Jørgensen, P. L., Fenton, T. M., von Burg, N., Riis, L. B., Spencer, J., & Agace, W. W. (2021) · Mucosal Immunology · doi:10.1038/s41385-021-00389-4 · Cited by 430 · see citing works
Current state and challenges in developing oral vaccines
Ramirez, J. E. V., Sharpe, L. A., & Peppas, N. A. (2017) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2017.04.008 · Cited by 410 · see citing works
“M cells - <1% of total cells in the intestinal lumen -Cover lymphatic bodies, including lymphoid follicles and Peyer’s patches -Short microvilli and thin mucus layer -Heavily invaginated -Have a protruding glycocalyx -Efficient transcytosis activity -Antigen sampling -Active transportation of pathogens -Receptor-media…”
BackgroundEpithelial Toll-like receptors and their role in gut homeostasis and disease
Burgueño, J. F., & Abreu, M. T. (2020) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0261-4 · Cited by 404 · see citing works
The role of microbial amyloid in neurodegeneration
Friedland, R. P., & Chapman, M. R. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006654 · Cited by 389 · see citing works
Recent advances of PLGA micro/nanoparticles for the delivery of biomacromolecular therapeutics
Ding, D., & Zhu, Q. (2018) · Materials Science and Engineering C · doi:10.1016/j.msec.2017.12.036 · Cited by 384 · see citing works
Lai, N. Y., Musser, M. A., Pinho-Ribeiro, F. A., Baral, P., Jacobson, A. R., Ma, P., Potts, D. E., Chen, Z., Paik, D., Soualhi, S., et al. (2019) · Cell · doi:10.1016/j.cell.2019.11.014 · Cited by 349 · see citing works
“M cells are specialized antigen-sampling cells in PP follicle-associated epithelia (FAE) that transcytose luminal antigens to underlying phagocytes to initiate mucosal immunity (Mabbott et al., 2013; Williams and Owen, 2015).”
BackgroundThe Effects of Secretory IgA in the Mucosal Immune System
Li, Y., Jin, L., & Chen, T. (2020) · BioMed Research International · doi:10.1155/2020/2032057 · Cited by 345 · see citing works
“Mucosal antigens were captured by the underlying DCs by extending their dendrites [24] or through the transcytosis of M cells [25].”
BackgroundMechanisms of Molecular Mimicry Involving the Microbiota in Neurodegeneration
Friedland, R. P. (2015) · Journal of Alzheimer's Disease · doi:10.3233/jad-142841 · Cited by 338 · see citing works
“Proteins from gut bacteria may gain access to neurons in the myenteric plexus because of the sampling of gut contents by epithelial microfold (M) cells as well as dendritic cells which deliver antigens to immune cells in Peyer's patches [58] [59].”
BackgroundMucosal Ecological Network of Epithelium and Immune Cells for Gut Homeostasis and Tissue Healing
Kurashima, Y., & Kiyono, H. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-051116-052424 · Cited by 331 · see citing works
Gieryńska, M., Szulc‐Dąbrowska, L., Struzik, J., Mielcarska, M. B., & Gregorczyk-Zboroch, K. P. (2022) · Animals · doi:10.3390/ani12020145 · Cited by 326 · see citing works
Molecular and cellular mechanisms of food allergy and food tolerance
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- Authors
- Mabbott, N. A., Donaldson, D. S., Ohno, H., Williams, I. R., & Mahajan, A.
- Affiliations
- Roslin Institute (GB)
- RIKEN Center for Integrative Medical Sciences (JP)
- Emory University (US)
- Corresponding author
- Mabbott, N A
- Venue
- Mucosal Immunology
- Publisher
- Elsevier BV
- Published
- 2013-07
- Volume
- 6
- Issue
- 4
- Pages
- 666-677
- ISSN
- 1933-0219 (ISSN-L)
- PMC
- PMC3686595
- OpenAlex
- W2085355903
- Cited by
- 721
- References
- 118
- Citations by year
- 2026: 52 · 2025: 48 · 2024: 61 · 2023: 66 · 2022: 50 · 2021: 68 · 2020: 71 · 2019: 54 · 2018: 78 · 2017: 56 · 2016: 43 · 2015: 46 · 2014: 22 · 2013: 5
- FWCI
- 3.37
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Mucosal Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- National Institutes of Health
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council (BB/G003947/1, BB/F019726/1, BB/J014672/1, BBS/E/D/20231759, BB/J0004332/1, BB/K021257/1, BBS/E/D/20251968, BBS/E/D/20251967, JPA1797)
- Japan Society for the Promotion of Science (24249029)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK064730, DK-064730)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- M cells, Peyer's patches, intestinal epithelium, mucosal immunity, immune surveillance, host genes, aging, mucosal vaccines, antigen targeting
- MeSH terms
- Age Factors, Animals, Antigens, Antigens, Surface, Cell Communication, Cell Differentiation, Humans, Intestinal Mucosa, Peyer's Patches, Stem Cells, Transcription Factors, Monitoring, Immunologic, Receptors, G-Protein-Coupled, RANK Ligand, Host-Pathogen Interactions
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