ONECUT2 regulates RANKL-dependent enterocyte and microfold cell differentiation in the small intestine; a multi-omics study
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 appr...
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| Published in: | Nucleic acids research Vol. 51; no. 3; pp. 1277 - 1296 |
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| Main Authors: | , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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Oxford University Press
22-02-2023
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| Abstract | 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. |
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| AbstractList | Abstract 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. 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. 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. Graphical Abstract Upon RANKL stimulation enterocytes and microfold cells originate from a common progenitor cell population. Transcription factors SPIB and SOX drive microfold cell differentiation while ONECUT2 promotes enterocyte cell differentiation by inducing transcriptional activation of Hnf4g . |
| Author | Qian, Chen Freeman, Michael R Neikes, Hannah K Quint, Yarah Veenstra, Gert Jan C van Heeringen, Simon J Luna Velez, Maria V Snabel, Rebecca R Vermeulen, Michiel Martens, Aniek |
| Author_xml | – sequence: 1 givenname: Maria V surname: Luna Velez fullname: Luna Velez, Maria V organization: Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute, Nijmegen 6525 AJ, The Netherlands – sequence: 2 givenname: Hannah K surname: Neikes fullname: Neikes, Hannah K organization: Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute, Nijmegen 6525 AJ, The Netherlands – sequence: 3 givenname: Rebecca R surname: Snabel fullname: Snabel, Rebecca R organization: Department of Molecular Developmental Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Nijmegen 6525 AJ, The Netherlands – sequence: 4 givenname: Yarah surname: Quint fullname: Quint, Yarah organization: Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute, Nijmegen 6525 AJ, The Netherlands – sequence: 5 givenname: Chen surname: Qian fullname: Qian, Chen organization: Department of Surgery, Division of Cancer Biology, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA – sequence: 6 givenname: Aniek surname: Martens fullname: Martens, Aniek organization: Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute, Nijmegen 6525 AJ, The Netherlands – sequence: 7 givenname: Gert Jan C surname: Veenstra fullname: Veenstra, Gert Jan C organization: Department of Molecular Developmental Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Nijmegen 6525 AJ, The Netherlands – sequence: 8 givenname: Michael R surname: Freeman fullname: Freeman, Michael R organization: Department of Surgery, Division of Cancer Biology, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA – sequence: 9 givenname: Simon J orcidid: 0000-0002-0411-3219 surname: van Heeringen fullname: van Heeringen, Simon J organization: Department of Molecular Developmental Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Nijmegen 6525 AJ, The Netherlands – sequence: 10 givenname: Michiel orcidid: 0000-0003-0836-6894 surname: Vermeulen fullname: Vermeulen, Michiel organization: Department of Molecular Biology, Radboud University Nijmegen, Faculty of Science, Radboud Institute for Molecular Life Sciences, Oncode Institute, Nijmegen 6525 AJ, The Netherlands |
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| Cites_doi | 10.1038/nmeth.2089 10.1093/biomet/37.1-2.17 10.1038/nbt.1630 10.1016/j.stem.2020.03.002 10.1016/j.gastro.2005.06.007 10.1152/physrev.00058.2009 10.1242/dev.179432 10.4049/jimmunol.178.9.5659 10.1016/j.immuni.2007.10.011 10.1016/j.coi.2004.03.005 10.1038/s41588-019-0384-0 10.3389/fimmu.2013.00185 10.15252/embj.2020105770 10.1038/ni.3732 10.1093/bioinformatics/btw313 10.1093/jmcb/mjaa034 10.1038/nature06196 10.1038/nature24489 10.1038/nmeth.3542 10.1093/nar/gkw257 10.1098/rstb.1998.0246 10.1101/gr.201574.115 10.1038/mi.2012.141 10.1038/mi.2015.121 10.1038/nbt.3519 10.1053/j.gastro.2017.03.035 10.1093/dnares/dss022 10.1016/j.isci.2021.103444 10.1128/JVI.00204-14 10.1093/bioinformatics/bty560 10.1126/science.277.5328.949 10.1111/j.1574-695X.2007.00359.x 10.1196/annals.1309.005 10.1016/S0092-8674(00)80106-3 10.1038/s41598-019-45839-z 10.1038/ncb3210 10.4049/jimmunol.0901563 10.1186/gb-2008-9-9-r137 10.1093/nar/gkz273 10.12688/f1000research.7563.1 10.1016/j.bbrc.2017.09.004 10.1038/s41586-019-0969-x 10.1186/s13059-016-0938-8 10.1128/IAI.01145-07 10.15252/embj.201694959 10.1101/474403 10.1038/mi.2014.99 10.1093/nar/29.9.e45 10.1016/j.chom.2012.10.009 10.1038/nmeth.4463 10.1093/nar/gkab598 10.1038/s41596-020-0336-2 10.1016/S0016-5085(74)80102-2 10.1093/bioinformatics/bty916 10.1084/jem.20181604 10.3389/fimmu.2019.02345 10.1038/nature07935 10.1038/ni.2352 10.1016/S0008-8749(03)00155-2 10.1126/science.286.5446.1965 10.1038/s41591-018-0241-1 10.15252/msb.20188227 10.32614/CRAN.package.gplots 10.1111/j.1749-6632.1992.tb39745.x 10.1038/s41586-018-0414-6 10.1186/s41232-018-0072-y 10.1137/1.9781611974010.89 10.1038/s41587-021-00870-2 10.1128/MCB.00434-12 10.1038/nmeth.2688 10.1038/nature10730 10.1073/pnas.93.18.9460 10.1038/s41598-018-37977-7 10.1152/physiolgenomics.00017.2010 10.1093/bioinformatics/btw777 10.1146/annurev.cellbio.16.1.301 10.1109/TPAMI.2016.2635657 10.21105/joss.00320 10.1038/nmeth.4396 10.1016/j.cell.2019.05.031 10.1093/nar/gkx1081 10.1093/bioinformatics/bts635 10.1038/1270 10.1006/bbrc.2002.6760 10.1186/s13059-014-0550-8 10.1111/j.1749-6632.2000.tb05240.x 10.3389/fimmu.2021.791095 10.1111/tra.12707 10.1093/dnares/12.2.127 10.1016/j.scr.2014.10.008 10.1073/pnas.1016071107 10.1258/002367781780958577 10.1038/nature10408 10.1038/nature11247 10.1093/bioinformatics/btu638 10.1371/journal.pone.0038338 |
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| References | Kimura (2023022200015081400_) 2019; 216 La Manno (2023022200015081400_) 2018; 560 Boonekamp (2023022200015081400_) 2020; 12 Chen (2023022200015081400_) 2018; 34 Hashizume (2023022200015081400_) 2008; 76 Melsted (2023022200015081400_) 2021; 39 Taylor (2023022200015081400_) 2007; 178 van Heeringen (2023022200015081400_) 2017 Martinoli (2023022200015081400_) 2007; 27 Mao (2023022200015081400_) 2017; 39 Wang (2023022200015081400_) 2016; 26 Li (2023022200015081400_) 2013 Bray (2023022200015081400_) 2016; 34 Golovkina (2023022200015081400_) 1999; 286 Fagarasan (2023022200015081400_) 2004; 16 Guillermin (2023022200015081400_) 2021; 40 Li (2023022200015081400_) 2020; 26 Davis (2023022200015081400_) 2018; 46 Moolenbeek (2023022200015081400_) 1981; 15 van Heeringen (2023022200015081400_) 2021 Dusing (2023022200015081400_) 2010; 42 Amerongen (2023022200015081400_) 1991; 4 Kobayashi (2023022200015081400_) 2012; 19 McCarthy (2023022200015081400_) 2017; 33 Haber (2023022200015081400_) 2017; 551 Kraehenbuhl (2023022200015081400_) 2000; 16 Kim (2023022200015081400_) 2017; 152 Nagashima (2023022200015081400_) 2017; 493 Macpherson (2023022200015081400_) 2004; 1029 Kimura (2023022200015081400_) 2015; 8 Soneson (2023022200015081400_) 2015; 4 Corr (2023022200015081400_) 2008; 52 Kobayashi (2023022200015081400_) 2013; 6 McLean (2023022200015081400_) 2010; 28 Moran (2023022200015081400_) 1950; 37 Bruse (2023022200015081400_) 2018 Ross-Innes (2023022200015081400_) 2012; 481 Kobayashi (2023022200015081400_) 2019; 10 Rios (2023022200015081400_) 2016; 9 Potten (2023022200015081400_) 1998; 353 Amerongen (2023022200015081400_) 1992; 664 Nigmatullina (2023022200015081400_) 2017; 36 Cai (2023022200015081400_) 2019 de Lau (2023022200015081400_) 2012; 32 Schneider (2023022200015081400_) 2012; 9 Liu (2023022200015081400_) 2015; 17 McConnell (2023022200015081400_) 2010; 90 Knoop (2023022200015081400_) 2009; 183 Lo (2023022200015081400_) 2003; 224 Neutra (2023022200015081400_) 1996; 86 Lemaigre (2023022200015081400_) 1996; 93 Wester (2023022200015081400_) 2021; 24 Tetreault (2023022200015081400_) 2012; 7 Chen (2023022200015081400_) 2019; 51 Aibar (2023022200015081400_) 2017; 14 Sato (2023022200015081400_) 2009; 459 Love (2023022200015081400_) 2014; 15 Corthésy (2023022200015081400_) 2013; 4 Korinek (2023022200015081400_) 1998; 19 Stuart (2023022200015081400_) 2019; 177 Buenrostro (2023022200015081400_) 2013; 10 ENCODE Project Consortium (2023022200015081400_) 2012; 489 van der Raadt (2023022200015081400_) 2019; 47 Kucharzik (2023022200015081400_) 2000; 915 Xu (2023022200015081400_) 2021; 49 Kanaya (2023022200015081400_) 2012; 13 Anders (2023022200015081400_) 2015; 31 Zhang (2023022200015081400_) 2008; 9 Dobin (2023022200015081400_) 2013; 29 Amemiya (2023022200015081400_) 2019; 9 Nagashima (2023022200015081400_) 2017; 18 Creyghton (2023022200015081400_) 2010; 107 Wilmore (2023022200015081400_) 2021; 12 Owen (2023022200015081400_) 1974; 66 Cao (2023022200015081400_) 2019; 566 Tahoun (2023022200015081400_) 2012; 12 Chen (2023022200015081400_) 2019; 146 Tian (2023022200015081400_) 2011; 478 Vanhorenbeeck (2023022200015081400_) 2002; 292 Gu (2023022200015081400_) 2016; 32 Kropp (2023022200015081400_) 2016; 9 Schmidl (2023022200015081400_) 2015; 12 Nandan (2023022200015081400_) 2015; 14 Kanaya (2023022200015081400_) 2020; 21 Lindeboom (2023022200015081400_) 2018; 14 Nandan (2023022200015081400_) 2009; 24 van der Sande (2023022200015081400_) 2020 Nakamura (2023022200015081400_) 2018; 38 Barker (2023022200015081400_) 2007; 449 van de Sande (2023022200015081400_) 2020; 15 Kernéis (2023022200015081400_) 1997; 277 Hase (2023022200015081400_) 2005; 12 Hashimshony (2023022200015081400_) 2016; 17 Korotkevich (2023022200015081400_) 2021 Rotinen (2023022200015081400_) 2018; 24 Gerlach (2023022200015081400_) 2019; 9 Corces (2023022200015081400_) 2017; 14 Gonzalez-Hernandez (2023022200015081400_) 2014; 88 Warnes (2023022200015081400_) 2005 Moerman (2023022200015081400_) 2019; 35 Mao (2023022200015081400_) 2015 Ramírez (2023022200015081400_) 2016; 44 Gregorieff (2023022200015081400_) 2005; 129 Pfaffl (2023022200015081400_) 2001; 29 |
| References_xml | – volume: 9 start-page: 671 year: 2012 ident: 2023022200015081400_ article-title: NIH Image to ImageJ: 25 years of image analysis publication-title: Nat. Methods doi: 10.1038/nmeth.2089 contributor: fullname: Schneider – volume: 37 start-page: 17 year: 1950 ident: 2023022200015081400_ article-title: Notes on continuous stochastic phenomena publication-title: Biometrika doi: 10.1093/biomet/37.1-2.17 contributor: fullname: Moran – year: 2019 ident: 2023022200015081400_ article-title: OrgM: a Fiji macro for automated measurement of object area, diameter and roundness from bright field images contributor: fullname: Cai – volume: 28 start-page: 495 year: 2010 ident: 2023022200015081400_ article-title: GREAT improves functional interpretation of cis-regulatory regions publication-title: Nat. Biotechnol. doi: 10.1038/nbt.1630 contributor: fullname: McLean – volume: 26 start-page: 675 year: 2020 ident: 2023022200015081400_ article-title: Lats1/2 Sustain Intestinal Stem Cells and Wnt Activation through TEAD-Dependent and Independent Transcription publication-title: Cell Stem Cell doi: 10.1016/j.stem.2020.03.002 contributor: fullname: Li – volume: 129 start-page: 626 year: 2005 ident: 2023022200015081400_ article-title: Expression pattern of Wnt signaling components in the adult intestine publication-title: Gastroenterology doi: 10.1016/j.gastro.2005.06.007 contributor: fullname: Gregorieff – volume: 90 start-page: 1337 year: 2010 ident: 2023022200015081400_ article-title: Mammalian Krüppel-like factors in health and diseases publication-title: Physiol. Rev. doi: 10.1152/physrev.00058.2009 contributor: fullname: McConnell – volume: 146 start-page: dev179432 year: 2019 ident: 2023022200015081400_ article-title: HNF4 factors control chromatin accessibility and are redundantly required for maturation of the fetal intestine publication-title: Development doi: 10.1242/dev.179432 contributor: fullname: Chen – volume: 178 start-page: 5659 year: 2007 ident: 2023022200015081400_ article-title: Lymphotoxin-independent expression of TNF-related activation-induced cytokine by stromal cells in cryptopatches, isolated lymphoid follicles, and Peyer's patches publication-title: J. Immunol. doi: 10.4049/jimmunol.178.9.5659 contributor: fullname: Taylor – volume: 27 start-page: 975 year: 2007 ident: 2023022200015081400_ article-title: Entry route of Salmonella typhimurium directs the type of induced immune response publication-title: Immunity doi: 10.1016/j.immuni.2007.10.011 contributor: fullname: Martinoli – volume: 16 start-page: 277 year: 2004 ident: 2023022200015081400_ article-title: Regulation of IgA synthesis at mucosal surfaces publication-title: Curr. Opin. Immunol. doi: 10.1016/j.coi.2004.03.005 contributor: fullname: Fagarasan – volume: 51 start-page: 777 year: 2019 ident: 2023022200015081400_ article-title: A reinforcing HNF4-SMAD4 feed-forward module stabilizes enterocyte identity publication-title: Nat. Genet. doi: 10.1038/s41588-019-0384-0 contributor: fullname: Chen – volume: 9 start-page: 43 year: 2016 ident: 2023022200015081400_ article-title: Onecut transcription factors in development and disease publication-title: Trends Dev. Biol. contributor: fullname: Kropp – volume: 4 start-page: 185 year: 2013 ident: 2023022200015081400_ article-title: Multi-faceted functions of secretory IgA at mucosal surfaces publication-title: Front. Immunol. doi: 10.3389/fimmu.2013.00185 contributor: fullname: Corthésy – volume: 40 start-page: e105770 year: 2021 ident: 2023022200015081400_ article-title: Wnt and Src signals converge on YAP-TEAD to drive intestinal regeneration publication-title: EMBO J. doi: 10.15252/embj.2020105770 contributor: fullname: Guillermin – year: 2021 ident: 2023022200015081400_ article-title: vanheeringen-lab/scepia: version 0.5.1 (0.5.1) contributor: fullname: van Heeringen – volume: 18 start-page: 675 year: 2017 ident: 2023022200015081400_ article-title: Identification of subepithelial mesenchymal cells that induce IgA and diversify gut microbiota publication-title: Nat. Immunol. doi: 10.1038/ni.3732 contributor: fullname: Nagashima – volume: 32 start-page: 2847 year: 2016 ident: 2023022200015081400_ article-title: Complex heatmaps reveal patterns and correlations in multidimensional genomic data publication-title: Bioinformatics doi: 10.1093/bioinformatics/btw313 contributor: fullname: Gu – volume: 12 start-page: 562 year: 2020 ident: 2023022200015081400_ article-title: Intestinal organoids as tools for enriching and studying specific and rare cell types: advances and future directions publication-title: J. Mol. Cell Biol. doi: 10.1093/jmcb/mjaa034 contributor: fullname: Boonekamp – volume: 449 start-page: 1003 year: 2007 ident: 2023022200015081400_ article-title: Identification of stem cells in small intestine and colon by marker gene Lgr5 publication-title: Nature doi: 10.1038/nature06196 contributor: fullname: Barker – volume: 551 start-page: 333 year: 2017 ident: 2023022200015081400_ article-title: A single-cell survey of the small intestinal epithelium publication-title: Nature doi: 10.1038/nature24489 contributor: fullname: Haber – volume: 12 start-page: 963 year: 2015 ident: 2023022200015081400_ article-title: ChIPmentation: fast, robust, low-input ChIP-seq for histones and transcription factors publication-title: Nat. Methods doi: 10.1038/nmeth.3542 contributor: fullname: Schmidl – volume: 44 start-page: W160 year: 2016 ident: 2023022200015081400_ article-title: deepTools2: a next generation web server for deep-sequencing data analysis publication-title: Nucleic Acids Res. doi: 10.1093/nar/gkw257 contributor: fullname: Ramírez – volume: 353 start-page: 821 year: 1998 ident: 2023022200015081400_ article-title: Stem cells in gastrointestinal epithelium: numbers, characteristics and death publication-title: Philos. Trans. R. Soc. Lond. Ser. B, Biol. Sci. doi: 10.1098/rstb.1998.0246 contributor: fullname: Potten – volume: 26 start-page: 1417 year: 2016 ident: 2023022200015081400_ article-title: Modeling cis-regulation with a compendium of genome-wide histone H3K27ac profiles publication-title: Genome Res. doi: 10.1101/gr.201574.115 contributor: fullname: Wang – volume: 6 start-page: 1027 year: 2013 ident: 2023022200015081400_ article-title: The functional maturation of M cells is dramatically reduced in the Peyer's patches of aged mice publication-title: Mucosal Immunol doi: 10.1038/mi.2012.141 contributor: fullname: Kobayashi – volume: 9 start-page: 907 year: 2016 ident: 2023022200015081400_ article-title: Antigen sampling by intestinal M cells is the principal pathway initiating mucosal IgA production to commensal enteric bacteria publication-title: Mucosal Immunol doi: 10.1038/mi.2015.121 contributor: fullname: Rios – volume: 34 start-page: 525 year: 2016 ident: 2023022200015081400_ article-title: Near-optimal probabilistic RNA-seq quantification publication-title: Nat. Biotechnol. doi: 10.1038/nbt.3519 contributor: fullname: Bray – volume: 152 start-page: 1845 year: 2017 ident: 2023022200015081400_ article-title: SP and KLF transcription factors in digestive physiology and diseases publication-title: Gastroenterology doi: 10.1053/j.gastro.2017.03.035 contributor: fullname: Kim – volume: 19 start-page: 407 year: 2012 ident: 2023022200015081400_ article-title: 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 publication-title: DNA Res. doi: 10.1093/dnares/dss022 contributor: fullname: Kobayashi – volume: 24 start-page: 103444 year: 2021 ident: 2023022200015081400_ article-title: Retinoic acid signaling drives differentiation toward the absorptive lineage in colorectal cancer publication-title: Iscience doi: 10.1016/j.isci.2021.103444 contributor: fullname: Wester – volume: 88 start-page: 6934 year: 2014 ident: 2023022200015081400_ article-title: Efficient norovirus and reovirus replication in the mouse intestine requires microfold (M) cells publication-title: J. Virol. doi: 10.1128/JVI.00204-14 contributor: fullname: Gonzalez-Hernandez – volume: 34 start-page: i884 year: 2018 ident: 2023022200015081400_ article-title: fastp: an ultra-fast all-in-one FASTQ preprocessor publication-title: Bioinformatics doi: 10.1093/bioinformatics/bty560 contributor: fullname: Chen – volume: 277 start-page: 949 year: 1997 ident: 2023022200015081400_ article-title: Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria publication-title: Science doi: 10.1126/science.277.5328.949 contributor: fullname: Kernéis – volume: 52 start-page: 2 year: 2008 ident: 2023022200015081400_ article-title: M-cells: origin, morphology and role in mucosal immunity and microbial pathogenesis publication-title: FEMS Immunol. Med. Microbiol. doi: 10.1111/j.1574-695X.2007.00359.x contributor: fullname: Corr – volume: 4 start-page: 760 year: 1991 ident: 2023022200015081400_ article-title: Transepithelial transport of HIV-1 by intestinal M cells: a mechanism for transmission of AIDS publication-title: J. Acquir. Immune Defic. Syndr. contributor: fullname: Amerongen – volume: 1029 start-page: 36 year: 2004 ident: 2023022200015081400_ article-title: Compartmentalization of the mucosal immune responses to commensal intestinal bacteria publication-title: Ann. N. Y. Acad. Sci. doi: 10.1196/annals.1309.005 contributor: fullname: Macpherson – volume: 86 start-page: 345 year: 1996 ident: 2023022200015081400_ article-title: Epithelial M cells: gateways for mucosal infection and immunization publication-title: Cell doi: 10.1016/S0092-8674(00)80106-3 contributor: fullname: Neutra – volume: 9 start-page: 9354 year: 2019 ident: 2023022200015081400_ article-title: The ENCODE blacklist: identification of problematic regions of the genome publication-title: Sci. Rep. doi: 10.1038/s41598-019-45839-z contributor: fullname: Amemiya – year: 2013 ident: 2023022200015081400_ article-title: Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM contributor: fullname: Li – volume: 17 start-page: 1036 year: 2015 ident: 2023022200015081400_ article-title: Redeployment of Myc and E2f1-3 drives Rb-deficient cell cycles publication-title: Nat. Cell Biol. doi: 10.1038/ncb3210 contributor: fullname: Liu – volume: 183 start-page: 5738 year: 2009 ident: 2023022200015081400_ article-title: RANKL is necessary and sufficient to initiate development of antigen-sampling M cells in the intestinal epithelium publication-title: J. Immunol. doi: 10.4049/jimmunol.0901563 contributor: fullname: Knoop – volume: 9 start-page: R137 year: 2008 ident: 2023022200015081400_ article-title: Model-based analysis of ChIP-Seq (MACS) publication-title: Genome Biol. doi: 10.1186/gb-2008-9-9-r137 contributor: fullname: Zhang – volume: 47 start-page: 5587 year: 2019 ident: 2023022200015081400_ article-title: ONECUT transcription factors induce neuronal characteristics and remodel chromatin accessibility publication-title: Nucleic Acids Res. doi: 10.1093/nar/gkz273 contributor: fullname: van der Raadt – volume: 4 start-page: 1521 year: 2015 ident: 2023022200015081400_ article-title: Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences publication-title: F1000Research doi: 10.12688/f1000research.7563.1 contributor: fullname: Soneson – volume: 493 start-page: 437 year: 2017 ident: 2023022200015081400_ article-title: Targeted deletion of RANKL in M cell inducer cells by the Col6a1-Cre driver publication-title: Biochem. Biophys. Res. Commun. doi: 10.1016/j.bbrc.2017.09.004 contributor: fullname: Nagashima – volume: 566 start-page: 496 year: 2019 ident: 2023022200015081400_ article-title: The single-cell transcriptional landscape of mammalian organogenesis publication-title: Nature doi: 10.1038/s41586-019-0969-x contributor: fullname: Cao – volume: 17 start-page: 77 year: 2016 ident: 2023022200015081400_ article-title: CEL-Seq2: sensitive highly-multiplexed single-cell RNA-Seq publication-title: Genome Biol. doi: 10.1186/s13059-016-0938-8 contributor: fullname: Hashimshony – volume: 76 start-page: 927 year: 2008 ident: 2023022200015081400_ article-title: Peyer's patches are required for intestinal immunoglobulin A responses to Salmonella spp publication-title: Infect. Immun. doi: 10.1128/IAI.01145-07 contributor: fullname: Hashizume – volume: 36 start-page: 869 year: 2017 ident: 2023022200015081400_ article-title: Id2 controls specification of Lgr5(+) intestinal stem cell progenitors during gut development publication-title: EMBO J. doi: 10.15252/embj.201694959 contributor: fullname: Nigmatullina – year: 2018 ident: 2023022200015081400_ article-title: GimmeMotifs: an analysis framework for transcription factor motif analysis doi: 10.1101/474403 contributor: fullname: Bruse – volume: 8 start-page: 650 year: 2015 ident: 2023022200015081400_ article-title: Visualization of the entire differentiation process of murine M cells: suppression of their maturation in cecal patches publication-title: Mucosal Immunol doi: 10.1038/mi.2014.99 contributor: fullname: Kimura – volume: 29 start-page: e45 year: 2001 ident: 2023022200015081400_ article-title: A new mathematical model for relative quantification in real-time RT-PCR publication-title: Nucleic Acids Res. doi: 10.1093/nar/29.9.e45 contributor: fullname: Pfaffl – volume: 24 start-page: 1343 year: 2009 ident: 2023022200015081400_ article-title: The role of Krüppel-like factors in the reprogramming of somatic cells to induced pluripotent stem cells publication-title: Histol. Histopathol. contributor: fullname: Nandan – volume: 12 start-page: 645 year: 2012 ident: 2023022200015081400_ article-title: Salmonella transforms follicle-associated epithelial cells into M cells to promote intestinal invasion publication-title: Cell Host Microbe doi: 10.1016/j.chom.2012.10.009 contributor: fullname: Tahoun – volume: 14 start-page: 1083 year: 2017 ident: 2023022200015081400_ article-title: SCENIC: single-cell regulatory network inference and clustering publication-title: Nat. Methods doi: 10.1038/nmeth.4463 contributor: fullname: Aibar – volume: 49 start-page: 7966 year: 2021 ident: 2023022200015081400_ article-title: ANANSE: an enhancer network-based computational approach for predicting key transcription factors in cell fate determination publication-title: Nucleic Acids Res. doi: 10.1093/nar/gkab598 contributor: fullname: Xu – volume: 15 start-page: 2247 year: 2020 ident: 2023022200015081400_ article-title: A scalable SCENIC workflow for single-cell gene regulatory network analysis publication-title: Nat. Protoc. doi: 10.1038/s41596-020-0336-2 contributor: fullname: van de Sande – volume: 66 start-page: 189 year: 1974 ident: 2023022200015081400_ article-title: Epithelial cell specialization within human Peyer's patches: an ultrastructural study of intestinal lymphoid follicles publication-title: Gastroenterology doi: 10.1016/S0016-5085(74)80102-2 contributor: fullname: Owen – volume: 35 start-page: 2159 year: 2019 ident: 2023022200015081400_ article-title: GRNBoost2 and Arboreto: efficient and scalable inference of gene regulatory networks publication-title: Bioinformatics doi: 10.1093/bioinformatics/bty916 contributor: fullname: Moerman – volume: 216 start-page: 831 year: 2019 ident: 2023022200015081400_ article-title: Sox8 is essential for M cell maturation to accelerate IgA response at the early stage after weaning in mice publication-title: J. Exp. Med. doi: 10.1084/jem.20181604 contributor: fullname: Kimura – volume: 10 start-page: 2345 year: 2019 ident: 2023022200015081400_ article-title: The Roles of Peyer's Patches and Microfold Cells in the Gut Immune System: relevance to Autoimmune Diseases publication-title: Front. Immunol. doi: 10.3389/fimmu.2019.02345 contributor: fullname: Kobayashi – volume: 459 start-page: 262 year: 2009 ident: 2023022200015081400_ article-title: Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche publication-title: Nature doi: 10.1038/nature07935 contributor: fullname: Sato – volume: 13 start-page: 729 year: 2012 ident: 2023022200015081400_ article-title: The Ets transcription factor Spi-B is essential for the differentiation of intestinal microfold cells publication-title: Nat. Immunol. doi: 10.1038/ni.2352 contributor: fullname: Kanaya – volume: 224 start-page: 8 year: 2003 ident: 2023022200015081400_ article-title: Peptidoglycan recognition protein expression in mouse Peyer's Patch follicle associated epithelium suggests functional specialization publication-title: Cell. Immunol. doi: 10.1016/S0008-8749(03)00155-2 contributor: fullname: Lo – volume: 286 start-page: 1965 year: 1999 ident: 2023022200015081400_ article-title: Organogenic role of B lymphocytes in mucosal immunity publication-title: Science doi: 10.1126/science.286.5446.1965 contributor: fullname: Golovkina – volume: 24 start-page: 1887 year: 2018 ident: 2023022200015081400_ article-title: ONECUT2 is a targetable master regulator of lethal prostate cancer that suppresses the androgen axis publication-title: Nat. Med. doi: 10.1038/s41591-018-0241-1 contributor: fullname: Rotinen – volume: 14 start-page: e8227 year: 2018 ident: 2023022200015081400_ article-title: Integrative multi-omics analysis of intestinal organoid differentiation publication-title: Mol. Syst. Biol. doi: 10.15252/msb.20188227 contributor: fullname: Lindeboom – year: 2005 ident: 2023022200015081400_ article-title: gplots: various R programming tools for plotting data doi: 10.32614/CRAN.package.gplots contributor: fullname: Warnes – volume: 664 start-page: 18 year: 1992 ident: 2023022200015081400_ article-title: M cell-mediated antigen transport and monoclonal IgA antibodies for mucosal immune protection publication-title: Ann. N. Y. Acad. Sci. doi: 10.1111/j.1749-6632.1992.tb39745.x contributor: fullname: Amerongen – year: 2021 ident: 2023022200015081400_ article-title: Fast gene set enrichment analysis contributor: fullname: Korotkevich – volume: 560 start-page: 494 year: 2018 ident: 2023022200015081400_ article-title: RNA velocity of single cells publication-title: Nature doi: 10.1038/s41586-018-0414-6 contributor: fullname: La Manno – volume: 38 start-page: 15 year: 2018 ident: 2023022200015081400_ article-title: M cell-dependent antigen uptake on follicle-associated epithelium for mucosal immune surveillance publication-title: Inflamm. Regen. doi: 10.1186/s41232-018-0072-y contributor: fullname: Nakamura – start-page: 792 volume-title: Proceedings of the 2015 SIAM International Conference on Data Mining (SDM) year: 2015 ident: 2023022200015081400_ article-title: SimplePPT: a Simple Principal Tree Algorithm doi: 10.1137/1.9781611974010.89 contributor: fullname: Mao – year: 2020 ident: 2023022200015081400_ article-title: seq2science (v0.3.1) contributor: fullname: van der Sande – volume: 39 start-page: 813 year: 2021 ident: 2023022200015081400_ article-title: Modular, efficient and constant-memory single-cell RNA-seq preprocessing publication-title: Nat. Biotechnol. doi: 10.1038/s41587-021-00870-2 contributor: fullname: Melsted – volume: 32 start-page: 3639 year: 2012 ident: 2023022200015081400_ article-title: Peyer's patch M cells derived from Lgr5(+) stem cells require SpiB and are induced by RankL in cultured ‘miniguts publication-title: Mol. Cell. Biol. doi: 10.1128/MCB.00434-12 contributor: fullname: de Lau – volume: 10 start-page: 1213 year: 2013 ident: 2023022200015081400_ article-title: Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position publication-title: Nat. Methods doi: 10.1038/nmeth.2688 contributor: fullname: Buenrostro – volume: 481 start-page: 389 year: 2012 ident: 2023022200015081400_ article-title: Differential oestrogen receptor binding is associated with clinical outcome in breast cancer publication-title: Nature doi: 10.1038/nature10730 contributor: fullname: Ross-Innes – volume: 93 start-page: 9460 year: 1996 ident: 2023022200015081400_ article-title: Hepatocyte nuclear factor 6, a transcription factor that contains a novel type of homeodomain and a single cut domain publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.93.18.9460 contributor: fullname: Lemaigre – volume: 9 start-page: 1469 year: 2019 ident: 2023022200015081400_ article-title: Combined quantification of intracellular (phospho-)proteins and transcriptomics from fixed single cells publication-title: Sci. Rep. doi: 10.1038/s41598-018-37977-7 contributor: fullname: Gerlach – volume: 42 start-page: 115 year: 2010 ident: 2023022200015081400_ article-title: Onecut-2 knockout mice fail to thrive during early postnatal period and have altered patterns of gene expression in small intestine publication-title: Physiol. Genomics doi: 10.1152/physiolgenomics.00017.2010 contributor: fullname: Dusing – volume: 33 start-page: 1179 year: 2017 ident: 2023022200015081400_ article-title: Scater: pre-processing, quality control, normalization and visualization of single-cell RNA-seq data in R publication-title: Bioinformatics doi: 10.1093/bioinformatics/btw777 contributor: fullname: McCarthy – volume: 16 start-page: 301 year: 2000 ident: 2023022200015081400_ article-title: Epithelial M cells: differentiation and function publication-title: Annu. Rev. Cell Dev. Biol. doi: 10.1146/annurev.cellbio.16.1.301 contributor: fullname: Kraehenbuhl – volume: 39 start-page: 2227 year: 2017 ident: 2023022200015081400_ article-title: Principal graph and structure learning based on reversed graph embedding publication-title: IEEE Trans. Pattern Anal. Mach. Intell. doi: 10.1109/TPAMI.2016.2635657 contributor: fullname: Mao – year: 2017 ident: 2023022200015081400_ article-title: genomepy: download genomes the easy way doi: 10.21105/joss.00320 contributor: fullname: van Heeringen – volume: 14 start-page: 959 year: 2017 ident: 2023022200015081400_ article-title: An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues publication-title: Nat. Methods doi: 10.1038/nmeth.4396 contributor: fullname: Corces – volume: 177 start-page: 1888 year: 2019 ident: 2023022200015081400_ article-title: Comprehensive Integration of Single-Cell Data publication-title: Cell doi: 10.1016/j.cell.2019.05.031 contributor: fullname: Stuart – volume: 46 start-page: D794 year: 2018 ident: 2023022200015081400_ article-title: The Encyclopedia of DNA elements (ENCODE): data portal update publication-title: Nucleic Acids Res. doi: 10.1093/nar/gkx1081 contributor: fullname: Davis – volume: 29 start-page: 15 year: 2013 ident: 2023022200015081400_ article-title: STAR: ultrafast universal RNA-seq aligner publication-title: Bioinformatics doi: 10.1093/bioinformatics/bts635 contributor: fullname: Dobin – volume: 19 start-page: 379 year: 1998 ident: 2023022200015081400_ article-title: Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4 publication-title: Nat. Genet. doi: 10.1038/1270 contributor: fullname: Korinek – volume: 292 start-page: 848 year: 2002 ident: 2023022200015081400_ article-title: OC-3, a novel mammalian member of the ONECUT class of transcription factors publication-title: Biochem. Biophys. Res. Commun. doi: 10.1006/bbrc.2002.6760 contributor: fullname: Vanhorenbeeck – volume: 15 start-page: 550 year: 2014 ident: 2023022200015081400_ article-title: Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 publication-title: Genome Biol. doi: 10.1186/s13059-014-0550-8 contributor: fullname: Love – volume: 915 start-page: 171 year: 2000 ident: 2023022200015081400_ article-title: Role of M cells in intestinal barrier function publication-title: Ann. N. Y. Acad. Sci. doi: 10.1111/j.1749-6632.2000.tb05240.x contributor: fullname: Kucharzik – volume: 12 start-page: 791095 year: 2021 ident: 2023022200015081400_ article-title: IgA plasma cells are long-lived residents of gut and bone marrow that express isotype- and tissue-specific gene expression patterns publication-title: Front. Immunol. doi: 10.3389/fimmu.2021.791095 contributor: fullname: Wilmore – volume: 21 start-page: 34 year: 2020 ident: 2023022200015081400_ article-title: Intestinal M cells: tireless samplers of enteric microbiota publication-title: Traffic doi: 10.1111/tra.12707 contributor: fullname: Kanaya – volume: 12 start-page: 127 year: 2005 ident: 2023022200015081400_ article-title: Distinct gene expression profiles characterize cellular phenotypes of follicle-associated epithelium and M cells publication-title: DNA Res. doi: 10.1093/dnares/12.2.127 contributor: fullname: Hase – volume: 14 start-page: 10 year: 2015 ident: 2023022200015081400_ article-title: Krüppel-like factor 5 is essential for proliferation and survival of mouse intestinal epithelial stem cells publication-title: Stem Cell Res doi: 10.1016/j.scr.2014.10.008 contributor: fullname: Nandan – volume: 107 start-page: 21931 year: 2010 ident: 2023022200015081400_ article-title: Histone H3K27ac separates active from poised enhancers and predicts developmental state publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1016071107 contributor: fullname: Creyghton – volume: 15 start-page: 57 year: 1981 ident: 2023022200015081400_ article-title: The ‘Swiss roll’: a simple technique for histological studies of the rodent intestine publication-title: Lab. Anim. doi: 10.1258/002367781780958577 contributor: fullname: Moolenbeek – volume: 478 start-page: 255 year: 2011 ident: 2023022200015081400_ article-title: A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable publication-title: Nature doi: 10.1038/nature10408 contributor: fullname: Tian – volume: 489 start-page: 57 year: 2012 ident: 2023022200015081400_ article-title: An integrated encyclopedia of DNA elements in the human genome publication-title: Nature doi: 10.1038/nature11247 contributor: fullname: ENCODE Project Consortium – volume: 31 start-page: 166 year: 2015 ident: 2023022200015081400_ article-title: HTSeq–a Python framework to work with high-throughput sequencing data publication-title: Bioinformatics doi: 10.1093/bioinformatics/btu638 contributor: fullname: Anders – volume: 7 start-page: e38338 year: 2012 ident: 2023022200015081400_ article-title: Krüppel-like factor 5 protects against murine colitis and activates JAK-STAT signaling in vivo publication-title: PLoS One doi: 10.1371/journal.pone.0038338 contributor: fullname: Tetreault |
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| Snippet | 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... Abstract Microfold (M) cells reside in the intestinal epithelium of Peyer's patches (PP). Their unique ability to take up and transport antigens from the... |
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| SubjectTerms | Animals Cell Differentiation Enterocytes Intestinal Mucosa Intestine, Small M Cells Mice Molecular Biology Multiomics Transcription Factors - metabolism |
| Title | ONECUT2 regulates RANKL-dependent enterocyte and microfold cell differentiation in the small intestine; a multi-omics study |
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