{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,10]],"date-time":"2026-10-10T07:09:01Z","timestamp":1791616141711,"version":"4.3.4"},"reference-count":104,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2023,1,10]],"date-time":"2023-01-10T00:00:00Z","timestamp":1673308800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"ERC","doi-asserted-by":"publisher","award":["771059"],"award-info":[{"award-number":["771059"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004622","name":"Dutch Cancer Society","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100004622","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000054","name":"NCI","doi-asserted-by":"publisher","award":["1R01CA220327"],"award-info":[{"award-number":["1R01CA220327"]}],"id":[{"id":"10.13039\/100000054","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000005","name":"US Department of Defense","doi-asserted-by":"publisher","award":["PC180541"],"award-info":[{"award-number":["PC180541"]}],"id":[{"id":"10.13039\/100000005","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,2,22]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Microfold (M) cells reside in the intestinal epithelium of Peyer's patches (PP). Their unique ability to take up and transport antigens from the intestinal lumen to the underlying lymphoid tissue is key in the regulation of the gut-associated immune response. Here, we applied a multi-omics approach to investigate the molecular mechanisms that drive M cell differentiation in mouse small intestinal organoids. We generated a comprehensive profile of chromatin accessibility changes and transcription factor dynamics during in vitro M cell differentiation, allowing us to uncover numerous cell type-specific regulatory elements and associated transcription factors. By using single-cell RNA sequencing, we identified an enterocyte and M cell precursor population. We used our newly developed computational tool SCEPIA to link precursor cell-specific gene expression to transcription factor motif activity in cis-regulatory elements, uncovering high expression of and motif activity for the transcription factor ONECUT2. Subsequent in vitro and in vivo perturbation experiments revealed that ONECUT2 acts downstream of the RANK\/RANKL signalling axis to support enterocyte differentiation, thereby restricting M cell lineage specification. This study sheds new light on the mechanism regulating cell fate balance in the PP, and it provides a powerful blueprint for investigation of cell fate switches in the intestinal epithelium.<\/jats:p>","DOI":"10.1093\/nar\/gkac1236","type":"journal-article","created":{"date-parts":[[2022,12,14]],"date-time":"2022-12-14T09:58:46Z","timestamp":1671011926000},"page":"1277-1296","source":"Crossref","is-referenced-by-count":19,"title":["ONECUT2 regulates RANKL-dependent enterocyte and microfold cell differentiation in the small intestine; a multi-omics study"],"prefix":"10.1093","volume":"51","author":[{"given":"Maria\u00a0V","family":"Luna\u00a0Velez","sequence":"first","affiliation":[{"name":"Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute , Nijmegen \u00a0 6525 \u00a0AJ, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hannah K","family":"Neikes","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute , Nijmegen \u00a0 6525 \u00a0AJ, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rebecca R","family":"Snabel","sequence":"additional","affiliation":[{"name":"Department of Molecular Developmental Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences , Nijmegen \u00a0 6525 \u00a0AJ, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yarah","family":"Quint","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute , Nijmegen \u00a0 6525 \u00a0AJ, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chen","family":"Qian","sequence":"additional","affiliation":[{"name":"Department of Surgery, Division of Cancer Biology , Cedars-Sinai Medical Center, Los Angeles , CA \u00a090048, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aniek","family":"Martens","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute , Nijmegen \u00a0 6525 \u00a0AJ, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gert\u00a0Jan\u00a0C","family":"Veenstra","sequence":"additional","affiliation":[{"name":"Department of Molecular Developmental Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences , Nijmegen \u00a0 6525 \u00a0AJ, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael R","family":"Freeman","sequence":"additional","affiliation":[{"name":"Department of Surgery, Division of Cancer Biology , Cedars-Sinai Medical Center, Los Angeles , CA \u00a090048, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0411-3219","authenticated-orcid":false,"given":"Simon\u00a0J","family":"van\u00a0Heeringen","sequence":"additional","affiliation":[{"name":"Department of Molecular Developmental Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences , Nijmegen \u00a0 6525 \u00a0AJ, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0836-6894","authenticated-orcid":false,"given":"Michiel","family":"Vermeulen","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute , Nijmegen \u00a0 6525 \u00a0AJ, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,1,10]]},"reference":[{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1146\/annurev.cellbio.16.1.301","article-title":"Epithelial M cells: differentiation and function","volume":"16","author":"Kraehenbuhl","year":"2000","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1111\/j.1574-695X.2007.00359.x","article-title":"M-cells: origin, morphology and role in mucosal immunity and microbial pathogenesis","volume":"52","author":"Corr","year":"2008","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"2023022200015081400_","first-page":"760","article-title":"Transepithelial transport of HIV-1 by intestinal M cells: a mechanism for transmission of AIDS","volume":"4","author":"Amerongen","year":"1991","journal-title":"J. Acquir. Immune Defic. Syndr."},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1111\/j.1749-6632.1992.tb39745.x","article-title":"M cell-mediated antigen transport and monoclonal IgA antibodies for mucosal immune protection","volume":"664","author":"Amerongen","year":"1992","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/S0092-8674(00)80106-3","article-title":"Epithelial M cells: gateways for mucosal infection and immunization","volume":"86","author":"Neutra","year":"1996","journal-title":"Cell"},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"6934","DOI":"10.1128\/JVI.00204-14","article-title":"Efficient norovirus and reovirus replication in the mouse intestine requires microfold (M) cells","volume":"88","author":"Gonzalez-Hernandez","year":"2014","journal-title":"J. Virol."},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.coi.2004.03.005","article-title":"Regulation of IgA synthesis at mucosal surfaces","volume":"16","author":"Fagarasan","year":"2004","journal-title":"Curr. Opin. Immunol."},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"3639","DOI":"10.1128\/MCB.00434-12","article-title":"Peyer's patch M cells derived from Lgr5(+) stem cells require SpiB and are induced by RankL in cultured \u2018miniguts","volume":"32","author":"de\u00a0Lau","year":"2012","journal-title":"Mol. Cell. Biol."},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1038\/nature24489","article-title":"A single-cell survey of the small intestinal epithelium","volume":"551","author":"Haber","year":"2017","journal-title":"Nature"},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1093\/dnares\/12.2.127","article-title":"Distinct gene expression profiles characterize cellular phenotypes of follicle-associated epithelium and M cells","volume":"12","author":"Hase","year":"2005","journal-title":"DNA Res."},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1038\/nature07935","article-title":"Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche","volume":"459","author":"Sato","year":"2009","journal-title":"Nature"},{"key":"2023022200015081400_","doi-asserted-by":"crossref","first-page":"e8227","DOI":"10.15252\/msb.20188227","article-title":"Integrative multi-omics analysis of intestinal organoid differentiation","volume":"14","author":"Lindeboom","year":"2018","journal-title":"Mol. 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