The DOI matches its Crossref record.
Cytosolic distribution of villin in M cells from mouse Peyer's patches correlates with the absence of a brush border
Open accessAbstract
Background & aims The follicle-associated epithelium (FAE) of Peyer's patches mainly consists of two cell types: absorptive enterocytes with a brush border and M cells without this apical specialization. To study the controversial ontogeny of M cells (mesenchymal vs. epithelial origin), the expression pattern of tissue-specific cytoskeletal proteins, markers of cell origin that play a crucial role in the specific shape of epithelial cells and brush border assembly, was investigated.Methods The localization of cytokeratins, vimentin, and villin was determined on mouse FAE using immunocytochemistry and electron microscopy.Results Epithelial-specific cytokeratins were expressed in both absorptive enterocytes and M cells, whereas vimentin was not detected in mouse FAE. Villin, a tissue-specific, actin-binding protein of the brush border, was expressed in the two cell types. This protein had an unusual cytoplasmic distribution in FAE cells lacking a brush border and in cells having an intraepithelial pocket filled with lymphocytes.Conclusions The presence of villin and the absence of vimentin in M cells support the intestinal origin of M cells. The cytoplasmic distribution of villin provides a new identification criteria for M cells and reflects the reorganization of the F-actin network, which correlates with the inability of M cells to assemble a brush border.
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?
M cells have reduced digestive function because they lack brush-border enzymes such as alkaline phosphatase, which makes them interesting for drug targeting.
“With the loss of brush-border enzymes, such as alkaline phosphatase, M cells show a reduced digestive function, which makes them even more interesting for drug targeting [26,27].”
From Use of lectin-functionalized particles for oral immunotherapy (2012) · cites this paper as [26]
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
Still being checked.
Research works printed but not linked: 11
- Coluccio LM, Bretscher A. Reassociation of microvilli core pro- epithelial cell lineages of mouse digestive and urogenital tracts. Development 1992;115:717-728.
- JA, Louvard D. Villin expression in the visceral endoderm and 20. Shibayama T, Carboni JM, Mooseker MS. Assembly of the intesti- in the gut anlage during early mouse embryogenesis. EMBO J nal brush border: appearance and distribution of microvillar core 1988;7:3321-3329. proteins in developing chick enterocytes. J Cell Biol 1987;105:
- J, Busslinger M, Beug H. Activation of an inducible c-fosER fusion 21. Matsudaira PT, Burgess DR. Identification and organization of protein causes loss of epithelial polarity and trigger epithelial- the components in the isolated microvillus cytoskeleton. J Cell fibroblastoid conversion. Cell 1992;71:1103-1116. Biol 1979;83:667-673.
- Colucci-Guyon E, Portier MM, Dunia I, Paulin D, Pournin S, Babi- 22. Bretscher A, Weber K. Villin is a major protein of the microvillus net C. Mice lacking vimentin develop and reproduce without an cytoskeleton which binds both G and F-actin in a calcium-depen- obvious phenotype. Cell 1994;79:678-694. dent manner. Cell 1980;20:839-847.
- Boller K, Arpin M, Pringault E, Mangeat P, Reggio H. Differential 23. Pringault E, Robine S, Louvard D. Structure of the human villin distribution of villin and villin mRNA in mouse intestinal epithelial gene. Proc Natl Acad Sci USA 1991;88:10811-10815. cells. Differentiation 1985;39:51-57.
- Friederich E, Huet C, Arpin M, Louvard D. Villin induces microvilli 34. Glenney JJR, Geisler N, Kaulfus P, Weber K. Demonstration of at growth and actin redistribution in transfected fibroblasts. Cell least two different actin binding sites in villin, a calcium-regulated 1989;59:461-475.
- modulator of F-actin organization. J Biol Chem 1981;256:8156- 8161.
- Friederich E, Pringault E, Arpin M, Louvard D. From the structure 35. Owen RL, Bhalla DK. Cytochemical analysis of alkaline phospha- to the function of villin, an actin-binding protein of the brush tase and esterase activities and of lectin-binding and anionic border. Bioessays 1990;12:403-408. sites in rat and mouse Peyer's patch M cells. Am J Anat 26. Costa de Beauregard MA, Pringault E, Robine S, Louvard D. Sup- 1983;168:199-212.
- pression of villin expression by antisense RNA impairs brush border assembly in polarized epithelial intestinal cells. EMBO J Received July 24, 1995. Accepted October 23, 1995. 1995;14:409-421. Address requests for reprints to: Eric Pringault, Ph.D., Swiss Insti- 27.
- Robine S, Huet C, Moll R, Sahuquillo-Merino C, Coudrier E, Zwei- tute for Experimental Cancer Research, CH-1066 Epalinges-Lau- baum A, Louvard D. Can villin be used to identify malignant and sanne, Switzerland. Fax: (41) 21-652-6933. undifferentiated normal digestive epithelial cells? Proc Natl Acad Supported by grants from the Fonds National de la Recherche Sci USA 1985;82:8488-8492. Scientifique Suisse (FNRS, grant 31-37612-93), the Sandoz Founda- 28.
- Pringault E, Arpin M, Garcia A, Findori J, Louvard D. A human tion (Basel, Switzerland), and the Ipsen Foundation (Paris, France). cDNA villin clone to investigate the differentiation of intestinal S. Kerneis was the recipient of a fellowship from the Institut National and kidney cells in vivo and in culture. EMBO J 1986;5:3119- de la Sante ´et de la Recherche Medicale (INSERM, France) and from 3124. the Muschamp Foundation, Switzerland.
Cited by
Sorted by citations
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
Self-citationEpithelial M Cells: Differentiation and Function
Kraehenbühl, J.-P., & Neutra, M. R. (2000) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.16.1.301 · Cited by 475
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
Role of M Cells in Intestinal Barrier Function
Kucharzik, T. F., Lügering, N., Rautenberg, K., Lügering, A., Schmidt, M. A., Stoll, R., & Domschke, W. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb05240.x · Cited by 141
Neutra, M. R. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.274.5.g785 · Cited by 133
The role of M cells in mucosal immunity
Hathaway, L. J., & Kraehenbuhl*, J.-P. (2000) · Cellular and Molecular Life Sciences CMLS · doi:10.1007/pl00000693 · Cited by 131
The composition and function of M cell apical membranes: Implications for microbial pathogenesis
Neutra, M. R., Mantis, N. J., Frey, A., & Giannasca, P. J. (1999) · Seminars in Immunology · doi:10.1006/smim.1999.0173 · Cited by 116
Unsolved mysteries of intestinal M cells
Nicoletti, C. (2000) · Gut · doi:10.1136/gut.47.5.735 · Cited by 102
The role of M cells in the protection of mucosal membranes
Gebert, A. (1997) · Histochemistry and Cell Biology · doi:10.1007/s004180050186 · Cited by 90
M Cells in Antigen Sampling in Mucosal Tissues
Neutra, M. R. (1999) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-59951-4_2 · Cited by 89
Salas, P. J. I., Rodríguez‐Puebla, M. L., Viciana, A. L., Vega-Salas, D. E., & Hauri, H.-P. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.137.2.359 · Cited by 86
Lo, D. D. (2003) · International Immunology · doi:10.1093/intimm/dxh011 · Cited by 83
Kernéis, S., Caliot, E., Stubbe, H., Bogdanova, A., Kraehenbuhl, J.-P., & Pringault, E. (2000) · Microbes and Infection · doi:10.1016/s1286-4579(00)01266-1 · Cited by 79
Self-citationMicroparticle targeting to M cells
Ermak, T. (1998) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(98)00043-x · Cited by 75
Intestinal M cells and their role in bacterial infection
Clark, M. A., & Jepson, M. A. (2003) · International Journal of Medical Microbiology · doi:10.1078/1438-4221-00242 · Cited by 65
Kurashima, Y., Kigoshi, T., Murasaki, S., Arai, F., Shimada, K., Seki, N., Kim, Y.-G., Hase, K., Ohno, H., Kawano, K., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21277-2 · Cited by 64
Debard, N., Sierro, F., & Kraehenbühl, J.-P. (1999) · Seminars in Immunology · doi:10.1006/smim.1999.0174 · Cited by 56
Mucin-Related Epitopes Distinguish M Cells and Enterocytes in Rabbit Appendix and Peyer’s Patches
Lelouard, H., Reggio, H., Mangeat, P. H., Neutra, M. R., & Montcourrier, P. (1999) · Infection and Immunity · doi:10.1128/iai.67.1.357-367.1999 · Cited by 55
Validation and quantitation of an in vitro M-cell model
Tyrer, P., Ruth Foxwell, A., Kyd, J., Harvey, M., Sizer, P., & Cripps, A. (2002) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02631-1 · Cited by 51
Baranov, V. I., & Hammarstr�m, S. (2004) · Histochemistry and Cell Biology · doi:10.1007/s00418-003-0613-5 · Cited by 48
The life and times of an intestinal M cell
Savidge, T. (1996) · Trends in Microbiology · doi:10.1016/0966-842x(96)10052-4 · Cited by 48
Kersting, S., Bruewer, M., Schuermann, G., Klotz, A., Utech, M., Hansmerten, M., Krieglstein, C. F., Senninger, N. J., Schulzke, J.-D., Naim, H. Y., et al. (2004) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63308-1 · Cited by 47
Receptor mediated targeting of M-cells
Tyrer, P. C., Foxwell, A. R., Kyd, J. M., Otczyk, D. C., & Cripps, A. W. (2007) · Vaccine · doi:10.1016/j.vaccine.2007.01.028 · Cited by 44
Kernéis, S. M., & Pringault, E. (1999) · Seminars in Immunology · doi:10.1006/smim.1999.0176 · Cited by 44
Self-citationIdentification of cytokeratins as accessory mediators of Salmonella entry into eukaryotic cells☆
Carlson, S. A., Omary, M. B., & Jones, B. D. (2002) · Life Sciences · doi:10.1016/s0024-3205(01)01512-0 · Cited by 43
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
The Mechanisms of M-cell Differentiation
Kanaya, T., & Ohno, H. (2014) · Bioscience of Microbiota Food and Health · doi:10.12938/bmfh.33.91 · Cited by 38
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
Bahi, S. E., Caliot, É., Bens, M., Bogdanova, A. A., Kernéis, S. M., Kahn, A., Vandewalle, A., & Pringault, E. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.8.3713 · Cited by 33
Self-citationExpression of junction-associated proteins differentiates mouse intestinal M cells from enterocytes
Clark, A. M., & Hirst, B. H. (2002) · Histochemistry and Cell Biology · doi:10.1007/s00418-002-0433-z · Cited by 32
Establishment and Evaluation of an in vitro M Cell Model using C2BBe1 Cells and Raji Cells
Masuda, K., Kajikawa, A., & Igimi, S. (2011) · Bioscience and Microflora · doi:10.12938/bifidus.30.37 · Cited by 27
An immunohistochemical study and review of potential markers of human intestinal M cells
Wong, N., Herriot, M. M., & Rae, F. (2009) · European Journal of Histochemistry · doi:10.4081/820 · Cited by 24
Human intestinal M cells exhibit enterocyte-like intermediate filaments
Kucharzik, T. F., Lügering, N., Schmid, K. W., Schmidt, M. A., Stoll, R., & Domschke, W. (1998) · Gut · doi:10.1136/gut.42.1.54 · Cited by 23
Hamzaoui, N., & Pringault, E. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb11111.x · Cited by 23
Self-citationThe immunopathology of M cells
Davis, I. C., & Owen, R. L. (1997) · Springer Seminars in Immunopathology · doi:10.1007/bf00824051 · Cited by 21
Cellular and Molecular Basis for Antigen Transport Across Epithelial Barriers
Neutra, M. R., & Kraehenbühl, J.-P. (2005) · Elsevier eBooks · doi:10.1016/b978-012491543-5/50011-5 · Cited by 21
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
Schimpel, C., Werzer, O., Fröhlich, E., Leitinger, G., Absenger‐Novak, M., Teubl, B. J., Zimmer, A., & Roblegg, E. (2015) · Beilstein Journal of Nanotechnology · doi:10.3762/bjnano.6.151 · Cited by 20
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
Structure and Function of Villin
Khurana, S. (2006) · Advances in molecular and cell biology · doi:10.1016/s1569-2558(06)37005-1 · Cited by 18
Peyer's Patches Epithelium in the Rat
Onori, P., Franchitto, A., Sferra, R., Vetuschi, A., & Gaudio, E. (2001) · Digestive Diseases and Sciences · doi:10.1023/a:1010778532240 · Cited by 18
Differentiation of a murine intestinal epithelial cell line (MIE) toward the M cell lineage
Kanaya, T., Miyazawa, K., Takakura, I., Itani, W., Watanabe, K., Ohwada, S., Kitazawa, H., Rose, M. T., McConochie, H. R., Okano, H., et al. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00378.2007 · Cited by 18
Caliot, É., Libon, C., Kernéis, S. M., & Pringault, E. (2000) · Scandinavian Journal of Immunology · doi:10.1046/j.1365-3083.2000.00819.x · Cited by 15
Self-citationC. A. Rubio, J. S. (1999) · Scandinavian Journal of Gastroenterology · doi:10.1080/003655299750026245 · Cited by 12
The neonatal Fc receptor is not required for mucosal infection by mouse mammary tumor virus
Velin, D., Acha‐Orbea, H., & Kraehenbühl, J. P. (1996) · Journal of Virology · doi:10.1128/jvi.70.10.7250-7254.1996 · Cited by 11
Keigi, C. H. I. N., ONISHI, S., Yuji, M., Inamoto, T., Qi, W.-M., Yamamoto, K., Warita, K., YOKOYAMA, T., Hoshi, N., & Kitagawa, H. (2007) · Journal of Veterinary Medical Science · doi:10.1292/jvms.69.193 · Cited by 11
Satake, N., Ishida, Y., Otoh, Y., Hinohara, S., Kobayashi, H., Sakashita, A., Maseki, N., & Kaneko, Y. (1997) · Genes Chromosomes and Cancer · doi:10.1002/(sici)1098-2264(199709)20:1 · Cited by 91
Mucosal Vaccine Delivery and M Cell Targeting
Gupta, P. N. (2014) · Advances in delivery science and technology · doi:10.1007/978-3-319-11355-5_9 · Cited by 6
Fischer, T., Klinger, A., von Smolinski, D., Orzekowsky-Schroeder, R., Nitzsche, F., Bölke, T., Vogel, A., Hüttmann, G., & Gebert, A. (2020) · Cell and Tissue Research · doi:10.1007/s00441-020-03167-z · Cited by 2
Immunocomposition of Gastrointestinal Tract of Gut
Madakka, M., Rajesh, N., & Jinka, R. (2020) · Diagnostics and therapeutic advances in GI malignancies · doi:10.1007/978-981-15-6487-1_2 · Cited by 2
El-Bassouny, D. R., & Essa, T. M. (2013) · The Egyptian Journal of Histology · doi:10.1097/01.ehx.0000437938.07612.a2 · Cited by 1
Immunologie des Intestinaltrakts
Stallmach, A., & Zeitz, M. (1999) · Springer eBooks · doi:10.1007/978-3-642-59960-6_5 · Cited by 1
The Expression of Cytokeratins in Bovine Intestinal Microfold (M) Cells
Kanaya, T., Hondo, T., Miyazawa, K., Michael, T., & Aso, H. (2012) · InTech eBooks · doi:10.5772/35084
Pringault, E. (1996) · Elsevier eBooks · doi:10.1016/b978-012394330-9/50005-3
Self-citationDas Immunsystem im Gastrointestinaltrakt — Mechanismen der Entzündung
Stallmach, A., & Zeitz, M. (2000) · Springer eBooks · doi:10.1007/978-3-642-57194-7_23
Mucosal Immunology of the Small Bowel
Gassel, A. M., & Greiner, A. (1998) · Springer eBooks · doi:10.1007/978-3-642-72140-3_42
Caliot, É., Libon, C., Kernéis, S. M., & Pringault, E. (2000) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.2000.00819.x
Self-citationPublisher, B. S. P. B. S. (2014) · Current Topics in Medicinal Chemistry · doi:10.2174/156802661409140429144414
Rôle de la GTPase atypique RhoU dans l'homéostasie intestinale
Slaymi, C. (2014) · theses.fr (ABES) · doi:10.70675/6fbf53aez89c0z4815zbd1fz4a003ca52cad
Metadata
- Authors
- Kerneis, S., Bogdanova, A., Colucci-Guyon, E., Kraehenbuhl, J., & Pringault, E.
- Affiliations
- University of Lausanne (CH)
- ORCID
- Bogdanova, A
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 1996-02
- Volume
- 110
- Issue
- 2
- Pages
- 515-521
- ISSN
- 0016-5085 (ISSN-L)
- OpenAlex
- W1980143291
- Cited by
- 59
- References
- 0
- Citations by year
- 2021: 1 · 2020: 2 · 2015: 1 · 2014: 4 · 2013: 2 · 2012: 2
- FWCI
- 4.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Gastroenterology (publishedVersion)
- PubMed (publishedVersion)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Topics
- Health Sciences › Medicine › Gastroenterology › Digestive system and related health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Skin and Cellular Biology Research
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- villin, M cells, Peyer's patches, follicle-associated epithelium, brush border, vimentin, cytokeratin, enterocyte differentiation, crypt epithelium, actin-binding proteins, mouse intestine, cell migration and differentiation, immunocytochemistry, electron microscopy
- MeSH terms
- Animals, Carrier Proteins, Cytosol, Epithelial Cells, Epithelium, Immunohistochemistry, Keratins, Mice, Inbred BALB C, Microfilament Proteins, Microscopy, Electron, Microscopy, Fluorescence, Microvilli, Peyer's Patches, Vimentin, Mice
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
