Cited by 721Immunotherapy and Immune ResponsesImmune Response and InflammationT-cell and B-cell Immunology

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Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium

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Mabbott, N A, Donaldson, D S, Ohno, H, Williams, I R, Mahajan, A·2013·Mucosal Immunology

DOI 10.1038/mi.2013.30PMC PMC3686595

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Abstract

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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c-Jun N-Terminal Kinase Phosphorylation of MARCKSL1 Determines Actin Stability and Migration in Neurons and in Cancer Cells
Björkblom, B., Padzik, A., Mohammad, H., Westerlund, N., Komulainen, E., Hollós, P., Parviainen, L., Papageorgiou, A. C., Iljin, K., Kallioniemi, O., et al. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.00713-12 · Cited by 105 · cited 1×
“Although their precise roles are uncertain, the immature M-cell markers such as ANXA5 and MARCKS-like protein 1 may be involved in cytoskeletal regulation to help adapt the differentiating epithelial cell towards one specialized for transcytosis.(27,28) An independent study has also investigated the requirement for Sp…”
Background
Enhanced mucosal and systemic immune response with intranasal immunization of mice with HIV peptides entrapped in PLG microparticles in combination with Ulex Europaeus-I lectin as M cell target
Manocha, M., Pal, P. C., Chitralekha, K. T., Thomas, B. E., Tripathi, V., Gupta, S. D., Paranjape, R., Kulkarni, S., & Rao, D. N. (2005) · Vaccine · doi:10.1016/j.vaccine.2005.06.031 · Cited by 103
The functional maturation of M cells is dramatically reduced in the Peyer's patches of aged mice
Kobayashi, A., Donaldson, D. S., Erridge, C., Kanaya, T., Williams, I. R., Ohno, H., Mahajan, A., & Mabbott, N. A. (2013) · Mucosal Immunology · doi:10.1038/mi.2012.141 · Cited by 101
Self-citation
Lymphotoxin β receptor signaling induces the chemokine CCL20 in intestinal epithelium
Rumbo, M., Sierro, F., Debard, N., Kraehenbühl, J.-P., & Finke, D. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.04.018 · Cited by 93
Cutting Edge: Brucella abortus Exploits a Cellular Prion Protein on Intestinal M Cells as an Invasive Receptor
Nakato, G., Hase, K., Suzuki, M., Kimura, M., Ato, M., Hanazato, M., Tobiume, M., Horiuchi, M., Atarashi, R., Nishida, N., et al. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1103332 · Cited by 87 · cited 2×
“Cellular prion protein Continuing with the immunosurveillance theme, the cellular prion protein (PrP) is also expressed highly on the apical membrane ofM cells(26) and has been implicated in the sampling of microorganisms from the gut lumen.(47) The GPI-anchored PrP protein is expressed highly by many cell populations…”
BackgroundSelf-citation
Meta-analysis of lineage-specific gene expression signatures in mouse leukocyte populations
Mabbott, N. A., Baillie, J. K., Hume, D. A., & Freeman, T. C. (2010) · Immunobiology · doi:10.1016/j.imbio.2010.05.012 · Cited by 86
Self-citation
Distinct Gene Expression Profiles Characterize Cellular Phenotypes of Follicle-Associated Epithelium and M Cells
Hase, K. (2005) · DNA Research · doi:10.1093/dnares/12.2.127 · Cited by 86
Convergent and Divergent Development among M Cell Lineages in Mouse Mucosal Epithelium
Wang, J., Gusti, V., Saraswati, A., & Lo, D. D. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1102077 · Cited by 83 · cited 5×
“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…”
BackgroundInfluential
Cell culture modeling of specialized tissue: identification of genes expressed specifically by follicle-associated epithelium of Peyer's patch by expression profiling of Caco-2/Raji co-cultures
Lo, D. D. (2003) · International Immunology · doi:10.1093/intimm/dxh011 · Cited by 83
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×
“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)”
Background
Investigation 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×
“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…”
Background
Role 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×
“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…”
Background
Up‐regulation of microsphere transport across the follicle‐associated epithelium of Peyer's patch by exposure to Streptococcus pneumoniae R36a
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 · cited 2×
“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,…”
Background
A novel role for constitutively expressed epithelial-derived chemokines as antibacterial peptides in the intestinal mucosa
Kotarsky, 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
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
Rapid appearance of M cells after microbial challenge is restricted at the periphery of the follicle-associated epithelium of Peyer's patch.
Borghesi, C., Taussig, M. J., & Nicoletti, C. (1999) · PubMed · Cited by 71
Peyer's Patch-Deficient Mice Demonstrate That Mycobacterium avium subsp. paratuberculosis Translocates across the Mucosal Barrier via both M Cells and Enterocytes but Has Inefficient Dissemination
Bermudez, L. E., Petrofsky, M., Sommer, S., & Barletta, R. G. (2010) · Infection and Immunity · doi:10.1128/iai.01411-09 · Cited by 70
Lymphotoxin and TNF Produced by B Cells Are Dispensable for Maintenance of the Follicle-Associated Epithelium but Are Required for Development of Lymphoid Follicles in the Peyer’s Patches
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×
“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…”
Background
Can 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
Self-citation
Basis 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
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×
“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…”
Background
Lymphotoxin-Independent Expression of TNF-Related Activation-Induced Cytokine by Stromal Cells in Cryptopatches, Isolated Lymphoid Follicles, and Peyer’s Patches
Taylor, 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×
“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-citation
Listerial 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
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
Self-citation
Ovalbumin-Protein σ1 M-Cell Targeting Facilitates Oral Tolerance With Reduction of Antigen-Specific CD4+ T Cells
Suzuki, 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×
“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)”
Background
The 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
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
Clusterin in human gut-associated lymphoid tissue, tonsils, and adenoids: localization to M cells and follicular dendritic cells
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
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
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×
“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))…”
Background
The Effects of Host Age on Follicular Dendritic Cell Status Dramatically Impair Scrapie Agent Neuroinvasion in Aged Mice
Brown, 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
Self-citation
CCR6hiCD11cint 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
Self-citation
Murine 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
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×
“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…”
Background
Targeted 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×
“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…”
Method
Effect 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×
“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)”
Background
Resistance 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
Self-citation
Defining the anatomical localisation of subsets of the murine mononuclear phagocyte system using integrin alpha X (Itgax, CD11c) and colony stimulating factor 1 receptor (Csf1r, CD115) expression fails to discriminate dendritic cells from macrophages
Bradford, B. M., Sester, D. P., Hume, D. A., & Mabbott, N. A. (2011) · Immunobiology · doi:10.1016/j.imbio.2011.08.006 · Cited by 47
Self-citation
Distinct Developmental Requirements for Isolated Lymphoid Follicle Formation in the Small and Large Intestine
Knoop, 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
Self-citation
M-Cell Targeting of Whole Killed Bacteria Induces Protective Immunity against Gastrointestinal Pathogens
Chionh, 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
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
Mycobacterium avium subsp. paratuberculosis invades through M cells and enterocytes across ileal and jejunal mucosa of lambs
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
Mouse Peptidoglycan Recognition Protein PGLYRP-1 Plays a Role in the Host Innate Immune Response against Listeria monocytogenes Infection
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
Macrophage Migration Inhibitory Factor Plays a Role in the Regulation of Microfold (M) Cell-Mediated Transport in the Gut
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
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
Transgene vaccination using Ulex europaeus agglutinin I (UEA-1) for targeted mucosal immunization against HIV-1 envelope
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
TNFR and LTβR agonists induce follicle-associated epithelium and M cell specific genes in rat and human intestinal epithelial cells
Wang, J., López‐Fraga, M., Rynko, A. E., & Lo, D. D. (2009) · Cytokine · doi:10.1016/j.cyto.2009.05.001 · Cited by 34
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×
“Fold change in gene expression by M-cell-like differentiated Caco-2 cells when compared with undifferentiated controls (GSE25330, GSE7745).(115)”
Background
Identification of Novel Genes Selectively Expressed in the Follicle-Associated Epithelium from the Meta-Analysis of Transcriptomics Data from Multiple Mouse Cell and Tissue Populations
Kobayashi, 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×
“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-citation
Toll-like receptor 5- and lymphotoxin β receptor-dependent epithelial Ccl20 expression involves the same NF-κB binding site but distinct NF-κB pathways and dynamics
Sirard, 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
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×
“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…”
BackgroundInfluential
Nonhuman 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
Immunohistochemical Study on the Delayed Progression of Epithelial Apoptosis in Follicle-Associated Epithelium of Rat Peyer's Patch
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
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×
“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…”
Result
Localization of fatty acid binding protein of epidermal type common to dendritic cells and presumptive macrophages in Peyer’s patches and epithelial M cells of mouse intestine
Suzuki, 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
Targeting of whole killed bacteria to gastrointestinal M-cells induces humoral immunity in the female reproductive tract
Chionh, Y. T., & SUTTON, P. R. N. (2010) · Gut Microbes · doi:10.4161/gmic.1.1.10096 · Cited by 4
Defining anatomical localisation and subsets of the murine mononuclear phagocyte system using integrin alpha X (ITGAX/CD11c) and colony stimulating factor 1 receptor (CSF1-R/CD115) expression fails to discriminate macrophages from dendritic cells
Bradford, B. M., Hume, D., & Mabbott, N. A. (2011) · Cited by 3
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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 3,367
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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
ORCID: Mabbott, N A
Donaldson, D S
Ohno, H
Williams, I R
Mahajan, A
Venue: Mucosal Immunology
Publisher: Elsevier BV
Published: 2013-07
Volume: 6
Issue: 4
Pages: 666-677
ISSN: 1933-0219 (ISSN-L)
DOI: 10.1038/mi.2013.30
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 3132 d)
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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Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium

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