The DOI matches its Crossref record; 117 of the 118 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche
Sato, T., Vries, R. G., Snippert, H. J., van de Wetering, M., Barker, N., Stange, D. E., van Es, J. H., Abo, A., Kujala, P., Peters, P. J., et al. (2009) · Nature · doi:10.1038/nature07935 · Cited by 7,204
Rescigno, M., Urbano, M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., Granucci, F., Kraehenbuhl, J.-P., & Ricciardi‐Castagnoli, P. (2001) · Nature Immunology · doi:10.1038/86373 · Cited by 2,554 · cited 2×
“Although the incidence is rare in the steady state, certain inflammatory stimuli appear to recruit MNP from the lamina propria to the gut epithelium where they insert their dendrites through the tight junctions between enterocytes to directly sample the luminal contents.(108,109) In addition to this ‘‘periscoping’’ ac…”
BackgroundSnippert, H. J., van der Flier, L. G., Sato, T., van Es, J. H., van den Born, M., Kroon-Veenboer, C., Barker, N., Klein, A. M., van Rheenen, J., Simons, B. D., et al. (2010) · Cell · doi:10.1016/j.cell.2010.09.016 · Cited by 1,951
Induction of Protective IgA by Intestinal Dendritic Cells Carrying Commensal Bacteria
Macpherson, A. J., & Uhr, T. (2004) · Science · doi:10.1126/science.1091334 · Cited by 1,584 · cited 1×
“Viable commensal bacteria and unprocessed antigen can also be recovered from classical DCmigrating within afferent mesenteric lymph.(113,114) These contrasting characteristics raise the question of whether the cells throughwhich antigens are initially sampled across the intestinal epithelium (M cells, enterocytes, gob…”
BackgroundSecretory IgA's complex roles in immunity and mucosal homeostasis in the gut
Mantis, N. J., Rol, N., & Corthésy, B. (2011) · Mucosal Immunology · doi:10.1038/mi.2011.41 · Cited by 1,283
Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine
Mcdole, J. R., Wheeler, L. W., McDonald, K. G., Wang, B., Konjufca, V. H., Knoop, K. A., Newberry, R. D., & Miller, M. J. (2012) · Nature · doi:10.1038/nature10863 · Cited by 976
Huang, F., Platt, N., Wykes, M., Major, J. R., Powell, T. J., Jenkins, C. D., & MacPherson, G. G. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.191.3.435 · Cited by 902
Jones, B. D., Ghori, N., & Falkow, S. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.180.1.15 · Cited by 883
Differential Lysosomal Proteolysis in Antigen-Presenting Cells Determines Antigen Fate
Delamarre, L., Pack, M., Chang, H. C., Mellman, I., & Trombetta, E. S. (2005) · Science · doi:10.1126/science.1108003 · Cited by 776
Uptake through glycoprotein 2 of FimH+ bacteria by M cells initiates mucosal immune response
Hase, K., Kawano, K., Nochi, T., Pontes, G. S., Fukuda, S., Ebisawa, M., Kadokura, K., Tobe, T., Fujimura, Y., Kawano, S., et al. (2009) · Nature · doi:10.1038/nature08529 · Cited by 663 · cited 4×
“In the absence of GP2 expression by M cells, the transcytosis of type-I-piliated bacteria was impeded.(9) Furthermore, GP2-dependent bacterial transcytosis by M cells was shown to be important for the immunosurveillance of FimHþ bacteria in the gut lumen.”
BackgroundInfluentialSelf-citation
Flagged first, then by citations
1 of the 118 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
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 3,367
Regional specialization within the intestinal immune system
Mowat, A. M., & Agace, W. W. (2014) · Nature reviews. Immunology · doi:10.1038/nri3738 · Cited by 1,882
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
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 1,417
“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 1,046
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
“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 779
Homeostatic mini-intestines through scaffold-guided organoid morphogenesis
Nikolaev, M., Mitrofanova, O., Broguiere, N., Geraldo, S., Dutta, D., Tabata, Y., Elci, B., Brandenberg, N., Kolotuev, I., Gjorevski, N., et al. (2020) · Nature · doi:10.1038/s41586-020-2724-8 · Cited by 755
Roles of intestinal epithelial cells in the maintenance of gut homeostasis
Okumura, R., & Takeda, K. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.20 · Cited by 732
Safety Assessment of Graphene-Based Materials: Focus on Human Health and the Environment
Fadeel, B., Bussy, C., Merino, S., Vázquez, E., Emmanuel Flahaut, B., Mouchet, F., Evariste, L., Gauthier, L., Koivisto, A. J., Vogel, U. B., et al. (2018) · ACS Nano · doi:10.1021/acsnano.8b04758 · Cited by 693
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
Xu, M., Qi, Y., Liu, G. H., Song, Y., Jiang, X., & Du, B. (2023) · ACS Nano · doi:10.1021/acsnano.3c05853 · Cited by 654
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 634
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
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 597
“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
“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 513
Gänger, S., & Schindowski, K. (2018) · Pharmaceutics · doi:10.3390/pharmaceutics10030116 · Cited by 447
“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].”
BackgroundInfluentialOral 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
Human 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
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 425
“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 422
The role of microbial amyloid in neurodegeneration
Friedland, R. P., & Chapman, M. R. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006654 · Cited by 398
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 394
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 357
“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
“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
“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 336
Gieryńska, M., Szulc‐Dąbrowska, L., Struzik, J., Mielcarska, M. B., & Gregorczyk-Zboroch, K. P. (2022) · Animals · doi:10.3390/ani12020145 · Cited by 346
Molecular and cellular mechanisms of food allergy and food tolerance
Chinthrajah, R. S., Hernandez, J. D., Boyd, S. D., Galli, S. J., & Nadeau, K. C. (2016) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2016.02.004 · Cited by 321
Ulcerative colitis: Recent advances in the understanding of disease pathogenesis
Porter, R. J., Kalla, R., & Ho, G. (2020) · F1000Research · doi:10.12688/f1000research.20805.1 · Cited by 308
Crosstalk Between Gut Microbiota and Innate Immunity and Its Implication in Autoimmune Diseases
Jiao, Y., Wu, L., Huntington, N. D., & Zhang, X. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00282 · Cited by 321
The gut microbiome and hypertension
O’Donnell, J. A., Zheng, T., Méric, G., & Marques, F. Z. (2023) · Nature Reviews Nephrology · doi:10.1038/s41581-022-00654-0 · Cited by 302
Functional interactions between innate lymphoid cells and adaptive immunity
Sonnenberg, G. F., & Hepworth, M. R. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0194-8 · Cited by 277
Ríos, D., Wood, M. B., Li, J., Chassaing, B., Gewirtz, A. T., & Williams, I. R. (2015) · Mucosal Immunology · doi:10.1038/mi.2015.121 · Cited by 266
Self-citationNguyen, T., Duong, V., & Maeng, H. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13071103 · Cited by 272
“After the selective endocytosis of antigens, M cells transport them to intraepithelial macrophages and lymphocytes prior to their migration to lymph nodes [147].”
BackgroundZhang, S., Langer, R., & Traverso, G. (2017) · Nano Today · doi:10.1016/j.nantod.2017.08.006 · Cited by 258
Critical Review on Zeolite Clinoptilolite Safety and Medical Applications in vivo
Kraljević Pavelić, S., Simović Medica, J., Gumbarević, D., Filošević, A., Pržulj, N., & Pavelić, K. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01350 · Cited by 247
The challenges of oral drug delivery via nanocarriers
Reinholz, J., Landfester, K., & Mailänder, V. (2018) · Drug Delivery · doi:10.1080/10717544.2018.1501119 · Cited by 237
“Their natural function is the transcytosis of antigens across the gut epithelium (Mabbott et al., 2013).”
BackgroundAn update on oral drug delivery via intestinal lymphatic transport
Zhang, Z., Lü, Y., Qi, J., & Wu, W. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2020.12.022 · Cited by 250
New insights into intestinal phages
Sausset, R., Petit, M., Gaboriau‐Routhiau, V., & Paepe, M. D. (2020) · Mucosal Immunology · doi:10.1038/s41385-019-0250-5 · Cited by 238
Ahluwalia, B., Magnusson, M. K., & Öhman, L. (2017) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365521.2017.1349173 · Cited by 242
“(a) Antigens can enter through the microfold (M) cells in the follicle associated epithelium (FAE) and be passed on to the dendritic cells (DCs) underlying in the subepithelial dome (SED), and the DCs then present the antigen directly to T-cells in the Peyer’s patches.”
BackgroundInfluentialKobayashi, N., Takahashi, D., Takano, S., Kimura, S., & Hase, K. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02345 · Cited by 244
The role of CSF1R-dependent macrophages in control of the intestinal stem-cell niche
Sehgal, A., Donaldson, D. S., Pridans, C., Sauter, K. A. D., Hume, D. A., & Mabbott, N. A. (2018) · Nature Communications · doi:10.1038/s41467-018-03638-6 · Cited by 208
Self-citationFunctional circuits and signal processing in the enteric nervous system
Fung, C., & Berghe, P. V. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03543-6 · Cited by 220
“Although M cells constitute a first line of defense, they can also be exploited by pathogens as a route of invasion [179].”
BackgroundThe regulation of gut mucosal IgA B-cell responses: recent developments
Lycke, N. Y., & Bemark, M. (2017) · Mucosal Immunology · doi:10.1038/mi.2017.62 · Cited by 210
The influence of commensal bacteria on infection with enteric viruses
Karst, S. M. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2015.25 · Cited by 198
Mucosal immune response in biology, disease prevention and treatment
Zhou, X., Wu, Y., Zhu, Z., Lu, C., Zhang, C., Zeng, L., Xie, F., Zhang, L., & Zhou, F. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-02043-4 · Cited by 230
Probiotic Modulation of Innate Cell Pathogen Sensing and Signaling Events
Llewellyn, A., & Foey, A. (2017) · Nutrients · doi:10.3390/nu9101156 · Cited by 171
“DCs are present in the Peyer’s patches and recgonise antigens present in the lumen, which have been transported to the Peyer’s patch via specialised IECs called microfold- or M cells [51].”
Mucosal vaccines: Strategies and challenges
Li, M., Wang, Y., Sun, Y., Cui, H., Zhu, S., & Qiu, H. (2019) · Immunology Letters · doi:10.1016/j.imlet.2019.10.013 · Cited by 186
de Kivit, S., Tobin, M. C., Forsyth, C. B., Keshavarzian, A., & LANDAY, A. L. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00060 · Cited by 185
Cabinian, A., Sinsimer, D., Tang, M., Zumba, O., Mehta, H., Toma, A., Sant’Angelo, D. B., Laouar, Y., & Laouar, A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0156762 · Cited by 171
Salmonella Virulence and Immune Escape
Wang, M., Qazi, I. H., Wang, L., Zhou, G., & Han, H. (2020) · Microorganisms · doi:10.3390/microorganisms8030407 · Cited by 184
Intestinal Health of Pigs Upon Weaning: Challenges and Nutritional Intervention
Zheng, L., Duarte, M. E., Loftus, A. S., & Kim, S. W. (2021) · Frontiers in Veterinary Science · doi:10.3389/fvets.2021.628258 · Cited by 168
Niche signals and transcription factors involved in tissue-resident macrophage development
T’Jonck, W., Guilliams, M., & Bonnardel, J. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.02.005 · Cited by 173
The Microbiome and Food Allergy
Iweala, O. I., & Nagler‐Anderson, C. (2019) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042718-041621 · Cited by 171
Human Gut-Associated Natural Killer Cells in Health and Disease
Poggi, A. D., Benelli, R., Venè, R., Costa, D., Ferrari, N., Tosetti, F., & Zocchi, M. R. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00961 · Cited by 161
“M cells take up different molecules from the gut lumen that, through transcytosis, come in contact with the underlying lymphoid cells (55).”
BackgroundYang, Z., DeLoid, G. M., Zarbl, H., Baw, J., & Demokritou, P. (2023) · NanoImpact · doi:10.1016/j.impact.2023.100481 · Cited by 174
Identification of subepithelial mesenchymal cells that induce IgA and diversify gut microbiota
Nagashima, K., Sawa, S., Nitta, T., Tsutsumi, M., Okamura, T., Penninger, J. M., Nakashima, T., & Takayanagi, H. (2017) · Nature Immunology · doi:10.1038/ni.3732 · Cited by 154
Oral delivery of nanoparticle-based vaccines
Marasini, N., Skwarczyński, M., & Tóth, I. (2014) · Expert Review of Vaccines · doi:10.1586/14760584.2014.936852 · Cited by 157
“Microfold-cells (M-cells) express a wide range of M-cell-specific receptors on their apical surface in the luminal region, which are involved in phagocytosis of the antigens or pathogens (FIGURE 2A) [12].”
BackgroundDelivery strategies to enhance oral vaccination against enteric infections
Davitt, C. J. H., & Lavelle, E. C. (2015) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.03.007 · Cited by 160
Dissecting the Heterogeneity in T-Cell Mediated Inflammation in IBD
Tindemans, I., Joosse, M. E., & Samsom, J. N. (2020) · Cells · doi:10.3390/cells9010110 · Cited by 152
“There are at least three mechanisms that contribute to antigen uptake in the intestine; (i) the follicle-associated epithelium of the Peyer′s patches contains specialized microfold cells (M-cells) that can transport microbial antigens across the mucosal epithelium from the lumen to the subepithelial dome in the Peyer′…”
BackgroundThe microbiome–systemic diseases connection
van der Meulen, T. A., Harmsen, H., Bootsma, H., Spijkervet, F., Kroese, F., & Vissink, A. (2016) · Oral Diseases · doi:10.1111/odi.12472 · Cited by 144
“Therefore, M cells fulfil an important immunosurveillance post in the intestinal epithelium (Mabbott et al, 2013).”
BackgroundAging of the mammalian gastrointestinal tract: a complex organ system
Saffrey, M. J. (2013) · AGE · doi:10.1007/s11357-013-9603-2 · Cited by 141
“It has been suggested that neuronal defences against ROS-induced damage may break down during aging and disruption to neurotrophic factor support has been proposed as a mechanism contributing to neuronal aging in the gut (e.g. see Camilleri et al. 2008).”
BackgroundRegulation of the Intestinal Barrier Function by Host Defense Peptides
Robinson, K., Deng, Z., Hou, Y., & Zhang, G. (2015) · Frontiers in Veterinary Science · doi:10.3389/fvets.2015.00057 · Cited by 145
Wang, D., Jiang, Q., Dong, Z., Meng, T., Hu, F., Wang, J., & Yuan, H. (2023) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2023.115130 · Cited by 144
Sucrosomial® Iron: A New Generation Iron for Improving Oral Supplementation
Gómez-Ramírez, S., Brilli, E., Tarantino, G., & Muñoz, M. (2018) · Pharmaceuticals · doi:10.3390/ph11040097 · Cited by 132
“M cells have been shown to provide a pathway for delivering orally administered vesicle-like particles to the lymphatic system [43,44].”
BackgroundKim, S., & Jang, Y. (2017) · Clinical and Experimental Vaccine Research · doi:10.7774/cevr.2017.6.1.15 · Cited by 134
“Although antigen uptake by M cells was previously thought to be non-specific, many recent studies have shown that a specific antigen delivery mechanism is involved [19].”
Primary Cell-Derived Intestinal Models: Recapitulating Physiology
Dutton, J. S., Hinman, S. S., Kim, R., Wang, Y., & Allbritton, N. L. (2018) · Trends in biotechnology · doi:10.1016/j.tibtech.2018.12.001 · Cited by 141
Edible Vaccines: Promises and Challenges
Kurup, V. M., & Thomas, J. (2019) · Molecular Biotechnology · doi:10.1007/s12033-019-00222-1 · Cited by 134
The development and function of mucosal lymphoid tissues: a balancing act with micro-organisms
Randall, T. D., & Mebius, R. E. (2014) · Mucosal Immunology · doi:10.1038/mi.2014.11 · Cited by 132
“This epithelial layer contains specialized epithelial cells termed M cells for the distinct microfold ridges on their apical surface.(15) A distinct layer of DCs is found immediately below the dome epithelium(16) and Figure 1 Different types of lymphoid organs are present at mucosal sites.”
BackgroundBellmann, S., Carlander, D., Fasano, A., Momcilovic, D., Scimeca, J. A., Waldman, W. J., Gombau, L., Tsytsikova, L., Canady, R., Pereira, D. I. A., et al. (2015) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1333 · Cited by 137
Day, C. J., Tran, E. N. H., Semchenko, E. A., Tram, G., Hartley‐Tassell, L. E., Ng, P. S. K., King, R. M., Ulanovsky, R., McAtamney, S., Apicella, M. A., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421082112 · Cited by 127
“GP2 is a heavily glycosylated protein that is an established marker for M cells (47).”
BackgroundTakegahara, N., Kim, H., & Choi, Y. (2022) · Bone · doi:10.1016/j.bone.2022.116353 · Cited by 136
Age-related changes in intestinal immunity and the microbiome
Walrath, T., Dyamenahalli, K. U., Hulsebus, H. J., McCullough, R. L., Idrovo, J., Boe, D. M., McMahan, R. H., & Kovacs, E. J. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.3ri0620-405rr · Cited by 129
Role of the Intestinal Epithelium and Its Interaction With the Microbiota in Food Allergy
Ali, A., HuiYing, T., & Kaiko, G. E. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.604054 · Cited by 131
A novel 3D intestine barrier model to study the immune response upon exposure to microplastics
Lehner, R., Wohlleben, W., Septiadi, D., Landsiedel, R., Petri-Fink, A., & Rothen-Rutishauser, B. (2020) · Archives of Toxicology · doi:10.1007/s00204-020-02750-1 · Cited by 123
Human Microbiome and its Association With Health and Diseases
Thani, A. A. A., Marei, H. E. S., Hamdi, W. S., Nasrallah, G. K., Zowalaty, M. E. E., Khodor, S. A., Al‐Asmakh, M., Aziz, H. A., & Cenciarelli, C. (2015) · Journal of Cellular Physiology · doi:10.1002/jcp.25284 · Cited by 130
“Dysbiosis of the gut microbiota is thought to play a crucial role in the development of mucosal lesions (Manichanh et al., 2012) and intestinal inflammation is generally believed to be associated with a specific reduction in the Bacteroidetes and Firmicutes phyla specially reductions in the…”
BackgroundHost‐microbe interaction in the gastrointestinal tract
Parker, A., Lawson, M. A., Vaux, L., & Pin, C. (2017) · Environmental Microbiology · doi:10.1111/1462-2920.13926 · Cited by 127
“…epithelium overlying Peyer’s patches and isolated lymphoid follicles, have shortened microvilli and altered extracellular matrix, allowing uptake and shuttling of antigens to innate and adaptive immune cells of the lamina propria and gut-associated lymphoid tissues (Mabbott et al., 2013) (Fig.”
BackgroundIn vivo development of immune tissue in human intestinal organoids transplanted into humanized mice
Bouffi, C., Wikenheiser‐Brokamp, K. A., Chaturvedi, P., Sundaram, N., Goddard, G. R., Wunderlich, M., Brown, N. E., Staab, J. F., Latanich, R., Zachos, N. C., et al. (2023) · Nature Biotechnology · doi:10.1038/s41587-022-01558-x · Cited by 121
The impact of ageing on the intestinal epithelial barrier and immune system
Man, A., Gicheva, N., & Nicoletti, C. (2014) · Cellular Immunology · doi:10.1016/j.cellimm.2014.04.001 · Cited by 118
Bioengineered human colon organoids with in vivo-like cellular complexity and function
Mitrofanova, O., Nikolaev, M., Xu, Q., Broguière, N., Cubela, I., Camp, J. G., Bscheider, M., & Lütolf, M. P. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.05.007 · Cited by 119
Impact of TGEV infection on the pig small intestine
Xia, L., Yang, Y., Wang, J., Jing, Y., & Yang, Q. (2018) · Virology Journal · doi:10.1186/s12985-018-1012-9 · Cited by 111
Candida albicans infection and intestinal immunity
Tong, Y., & Tang, J. (2017) · Microbiological Research · doi:10.1016/j.micres.2017.02.002 · Cited by 109
The Peyer’s Patch Mononuclear Phagocyte System at Steady State and during Infection
Silva, C. D., Wagner, C., Bonnardel, J., Gorvel, J., & Lelouard, H. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01254 · Cited by 112
Interactions between Intestinal Microflora/Probiotics and the Immune System
Zhang, C., Wang, H., & Chen, T. (2019) · BioMed Research International · doi:10.1155/2019/6764919 · Cited by 110
STAT3-Activating Cytokines: A Therapeutic Opportunity for Inflammatory Bowel Disease?
Nguyen, P. M., Putoczki, T. L., & Ernst, M. (2015) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2014.0225 · Cited by 100
Alkie, T. N., Yitbarek, A., Hodgins, D. C., Kulkarni, R. R., Taha-Abdelaziz, K., & Sharif, S. (2019) · Avian Pathology · doi:10.1080/03079457.2019.1607966 · Cited by 107
“The study also suggests the presence of microfold-cells (M-cells) in the follicle associated epithelium overlaying the BALT, that may be involved in antigen sampling comparable to M-cells residing in Peyer’s patches of mice (Mabbott et al., 2013).”
BackgroundResultImmunological Outcomes of Allergen-Specific Immunotherapy in Food Allergy
Schoos, A. M., Bullens, D. M. A., Chawes, B., Costa, J. S., Vlieger, L. D., DunnGalvin, A., Epstein, M. M., Garssen, J., Hilger, C., Knipping, K., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.568598 · Cited by 99
“Food proteins can pass the intestinal epithelial barrier through transcytosis, paracellular diffusion or endocytosis by microfold (M)-cells (16, 17).”
BackgroundThe role of gastrointestinal permeability in food allergy
Samadi, N., Klems, M., & Untersmayr, E. (2018) · Annals of Allergy Asthma & Immunology · doi:10.1016/j.anai.2018.05.010 · Cited by 101
Development of in vitro enteroids derived from bovine small intestinal crypts
Hamilton, C. A., Young, R. A., Jayaraman, S., Sehgal, A., Paxton, E. A., Thomson, S., Katzer, F., Hope, J. C., Innes, E. A., Morrison, L. J., et al. (2018) · Veterinary Research · doi:10.1186/s13567-018-0547-5 · Cited by 101
Self-citationAntigen targeting to M cells for enhancing the efficacy of mucosal vaccines
Kim, S., & Jang, Y. (2014) · Experimental & Molecular Medicine · doi:10.1038/emm.2013.165 · Cited by 102
Compartmentalizing intestinal epithelial cell toll-like receptors for immune surveillance
Yu, S., & Gao, N. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1931-1 · Cited by 98
“In addition, microfold cells with high phagocytotic and transcytotic activities account for 10 % of follicle-associated epithelia that overlie gut-associated lymphoid tissues [13].”
Activated Peyer′s patch B cells sample antigen directly from M cells in the subepithelial dome
Komban, R. J., Strömberg, A., Biram, A., Cervin, J., Lebrero‐Fernández, C., Mabbott, N. A., Yrlid, U., Shulman, Z., Bemark, M., & Lycke, N. Y. (2019) · Nature Communications · doi:10.1038/s41467-019-10144-w · Cited by 102
Self-citationLoktionov, A. S. (2019) · World Journal of Gastroenterology · doi:10.3748/wjg.v25.i27.3503 · Cited by 102
Thymic mimetic cells function beyond self-tolerance
Givony, T., Leshkowitz, D., Castillo, D. D., Nevo, S., Kadouri, N., Dassa, B., Gruper, Y., Khalaila, R., Ben‐Nun, O., Gome, T., et al. (2023) · Nature · doi:10.1038/s41586-023-06512-8 · Cited by 96
“Similarly, the microfoldTEC subset shared a transcriptional signature with mucosal M-cells, including genes linked to endocytosis and transcytosis (for example, Anxa5 and Marcksl1 ) and genes involved in the formation of tunnelling nanotubes (for example, Tnfaip2 ) 18 .”
BackgroundAn Insight Into the Intestinal Web of Mucosal Immunity, Microbiota, and Diet in Inflammation
Yap, Y. A., & Mariño, E. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02617 · Cited by 100
“These microfold cells or M cells facilitate the sampling of luminal antigens and intact microorganisms for presentation to the intestinal immune system (53, 54).”
BackgroundM cell-dependent antigen uptake on follicle-associated epithelium for mucosal immune surveillance
Nakamura, Y., Kimura, S., & Hase, K. (2018) · Inflammation and Regeneration · doi:10.1186/s41232-018-0072-y · Cited by 97
Diet-induced gut dysbiosis and inflammation: Key drivers of obesity-driven NASH
Kang, G. G., Trevaskis, N. L., Murphy, A. J., & Febbraio, M. A. (2023) · iScience · doi:10.1016/j.isci.2022.105905 · Cited by 94
Chitosan-based particulate systems for the delivery of mucosal vaccines against infectious diseases
Singh, B., Maharjan, S., Cho, K., Cui, L., Park, I., Choi, Y., & Cho, C. (2017) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2017.10.101 · Cited by 92
Metadata
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
