{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T07:09:39Z","timestamp":1790838579946,"version":"4.1.0"},"reference-count":59,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2021,8,17]],"date-time":"2021-08-17T00:00:00Z","timestamp":1629158400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006447","name":"Universit\u00e4t Z\u00fcrich","doi-asserted-by":"publisher","award":["Walter and Gertrud Siegenthaler Fellowship"],"award-info":[{"award-number":["Walter and Gertrud Siegenthaler Fellowship"]}],"id":[{"id":"10.13039\/501100006447","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006447","name":"Universit\u00e4t Z\u00fcrich","doi-asserted-by":"publisher","award":["Hartmann Mueller Foundation"],"award-info":[{"award-number":["Hartmann Mueller Foundation"]}],"id":[{"id":"10.13039\/501100006447","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006447","name":"Universit\u00e4t Z\u00fcrich","doi-asserted-by":"publisher","award":["Fonds zur Foerderung des Akademischen Nachwuchses"],"award-info":[{"award-number":["Fonds zur Foerderung des Akademischen Nachwuchses"]}],"id":[{"id":"10.13039\/501100006447","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Swiss National Science Foundation","award":["PZ00P3_185880"],"award-info":[{"award-number":["PZ00P3_185880"]}]},{"name":"Swiss National Science Foundation","award":["320030E_190969"],"award-info":[{"award-number":["320030E_190969"]}]},{"name":"Swiss National Science Foundation","award":["320030_184753"],"award-info":[{"award-number":["320030_184753"]}]},{"name":"Swiss National Science Foundation","award":["314730_166381"],"award-info":[{"award-number":["314730_166381"]}]},{"name":"Swiss National Science Foundation","award":["33CS30-148422"],"award-info":[{"award-number":["33CS30-148422"]}]},{"name":"Novartis Foundation for Medical-Biological Research","award":["#19A013"],"award-info":[{"award-number":["#19A013"]}]},{"name":"Stiftung Experimentelle Biomedizin","award":["Stiftung Experimentelle Biomedizin"],"award-info":[{"award-number":["Stiftung Experimentelle Biomedizin"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Gut microbiota appears to be involved in the pathogenesis of primary sclerosing cholangitis (PSC). The protein tyrosine phosphatase nonreceptor 2 (PTPN2) gene risk variant rs1893217 is associated with gut dysbiosis in inflammatory bowel disease (IBD), and PTPN2 was mentioned as a possible risk gene for PSC. This study assessed the microbial profile of ulcerative colitis (UC) patients with PSC and without PSC (non-PSC). Additionally, effects of the PTPN2 risk variant were assessed. In total, 216 mucosal samples from ileum, colon, and rectum were collected from 7 PSC and 42 non-PSC patients, as well as 28 control subjects (non-IBD). The microbial composition was derived from 16S rRNA sequencing data. Overall, bacterial richness was highest in PSC patients, who also had a higher relative abundance of the genus Roseburia compared to non-PSC, as well as Haemophilus, Fusobacterium, Bifidobacterium, and Actinobacillus compared to non-IBD, as well as a lower relative abundance of Bacteroides compared to non-PSC and non-IBD, respectively. After exclusion of patients with the PTPN2 risk variant, Brachyspira was higher in PSC compared to non-PSC, while, solely in colon samples, Eubacterium and Tepidimonas were higher in PSC vs. non-IBD. In conclusion, this study underlines the presence of gut mucosa-associated microbiome changes in PSC patients and rather weakens the role of PTPN2 as a PSC risk gene.<\/jats:p>","DOI":"10.3390\/microorganisms9081752","type":"journal-article","created":{"date-parts":[[2021,8,17]],"date-time":"2021-08-17T03:43:04Z","timestamp":1629171784000},"page":"1752","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Modulation of the Mucosa-Associated Microbiome Linked to the PTPN2 Risk Gene in Patients with Primary Sclerosing Cholangitis and Ulcerative Colitis"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8739-5919","authenticated-orcid":false,"given":"Luisa","family":"Denoth","sequence":"first","affiliation":[{"name":"Department of Gastroenterology and Hepatology, University Hospital Zurich, R\u00e4mistrasse 100, 8091 Z\u00fcrich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0947-5235","authenticated-orcid":false,"given":"Pascal","family":"Juillerat","sequence":"additional","affiliation":[{"name":"Maurice M\u00fcller Laboratories, Department for Biomedical Research, University of Bern, 3012 Bern, Switzerland"},{"name":"Department of Visceral Surgery and Medicine, Bern University Hospital, University of Bern, 3012 Bern, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9263-948X","authenticated-orcid":false,"given":"Andreas E.","family":"Kremer","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Hepatology, University Hospital Zurich, R\u00e4mistrasse 100, 8091 Z\u00fcrich, Switzerland"},{"name":"Department of Medicine 1, Friedrich-Alexander-University Erlangen-N\u00fcrnberg and University Hospital Erlangen, 91054 Erlangen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1733-9188","authenticated-orcid":false,"given":"Gerhard","family":"Rogler","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Hepatology, University Hospital Zurich, R\u00e4mistrasse 100, 8091 Z\u00fcrich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Scharl","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Hepatology, University Hospital Zurich, R\u00e4mistrasse 100, 8091 Z\u00fcrich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1888-9226","authenticated-orcid":false,"given":"Bahtiyar","family":"Yilmaz","sequence":"additional","affiliation":[{"name":"Maurice M\u00fcller Laboratories, Department for Biomedical Research, University of Bern, 3012 Bern, Switzerland"},{"name":"Department of Visceral Surgery and Medicine, Bern University Hospital, University of Bern, 3012 Bern, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0518-5505","authenticated-orcid":false,"given":"Sena","family":"Bluemel","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Hepatology, University Hospital Zurich, R\u00e4mistrasse 100, 8091 Z\u00fcrich, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"name":"on behalf of the Swiss IBD Cohort Study","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,8,17]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1136\/gut.21.10.870","article-title":"Primary sclerosing cholangitis: A review of its clinical features, cholangiography, and hepatic histology","volume":"21","author":"Chapman","year":"1980","journal-title":"Gut"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.1053\/j.gastro.2009.11.046","article-title":"Genome-wide association analysis in primary sclerosing cholangitis","volume":"138","author":"Karlsen","year":"2010","journal-title":"Gastroenterology"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1016\/j.autrev.2014.01.028","article-title":"Diagnosis and classification of ulcerative colitis","volume":"13","author":"Conrad","year":"2014","journal-title":"Autoimmun. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1016\/0016-5085(91)70019-T","article-title":"Prevalence of primary sclerosing cholangitis in patients with ulcerative colitis","volume":"100 Pt 1","author":"Olsson","year":"1991","journal-title":"Gastroenterology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1136\/gut.2004.046615","article-title":"PSC-IBD: A unique form of inflammatory bowel disease associated with primary sclerosing cholangitis","volume":"54","author":"Loftus","year":"2005","journal-title":"Gut"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1053\/j.gastro.2013.06.052","article-title":"Pathogenesis of primary sclerosing cholangitis and advances in diagnosis and management","volume":"145","author":"Eaton","year":"2013","journal-title":"Gastroenterology"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1002\/hep.23294","article-title":"Diagnosis and management of primary sclerosing cholangitis","volume":"51","author":"Chapman","year":"2010","journal-title":"Hepatology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.1016\/j.gastro.2003.07.011","article-title":"Incidence, clinical spectrum, and outcomes of primary sclerosing cholangitis in a United States community","volume":"125","author":"Bambha","year":"2003","journal-title":"Gastroenterology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2768","DOI":"10.3748\/wjg.v26.i21.2768","article-title":"Gut microbiome in primary sclerosing cholangitis: A review","volume":"26","author":"Little","year":"2020","journal-title":"World J. Gastroenterol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1002\/hep.1840130425","article-title":"Biliary tract disease in rats with experimental small bowel bacterial overgrowth","volume":"13","author":"Lichtman","year":"1991","journal-title":"Hepatology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1016\/0016-5085(90)90833-M","article-title":"Hepatic inflammation in rats with experimental small intestinal bacterial overgrowth","volume":"98","author":"Lichtman","year":"1990","journal-title":"Gastroenterology"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2178","DOI":"10.1053\/j.gastro.2018.02.019","article-title":"Alterations in Intestinal Microbiota Lead to Production of Interleukin 17 by Intrahepatic \u03b3\u03b4 T-Cell Receptor-Positive Cells and Pathogenesis of Cholestatic Liver Disease","volume":"154","author":"Tedesco","year":"2018","journal-title":"Gastroenterology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1038\/s41564-018-0333-1","article-title":"Gut pathobionts underlie intestinal barrier dysfunction and liver T helper 17 cell immune response in primary sclerosing cholangitis","volume":"4","author":"Nakamoto","year":"2019","journal-title":"Nat. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"580","DOI":"10.1111\/apt.15375","article-title":"Consistent alterations in faecal microbiomes of patients with primary sclerosing cholangitis independent of associated colitis","volume":"50","author":"Liwinski","year":"2019","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1136\/gutjnl-2015-310500","article-title":"The gut microbial profile in patients with primary sclerosing cholangitis is distinct from patients with ulcerative colitis without biliary disease and healthy controls","volume":"66","author":"Kummen","year":"2017","journal-title":"Gut"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1136\/gutjnl-2018-317791","article-title":"Fungi participate in the dysbiosis of gut microbiota in patients with primary sclerosing cholangitis","volume":"69","author":"Lemoinne","year":"2020","journal-title":"Gut"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1826","DOI":"10.1038\/s41564-019-0483-9","article-title":"Quantitative microbiome profiling disentangles inflammation- and bile duct obstruction-associated microbiota alterations across PSC\/IBD diagnoses","volume":"4","author":"Sabino","year":"2019","journal-title":"Nat. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1111\/apt.13552","article-title":"The features of mucosa-associated microbiota in primary sclerosing cholangitis","volume":"43","author":"Torres","year":"2016","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"814","DOI":"10.14309\/ajg.0000000000000604","article-title":"Targeting the Gut Microbiome as a Treatment for Primary Sclerosing Cholangitis: A Conceptional Framework","volume":"115","author":"Shah","year":"2020","journal-title":"Am. J. Gastroenterol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1093\/ecco-jcc\/jjaa021","article-title":"A Pilot Integrative Analysis of Colonic Gene Expression, Gut Microbiota, and Immune Infiltration in Primary Sclerosing Cholangitis-Inflammatory Bowel Disease: Association of Disease with Bile Acid Pathways","volume":"14","author":"Quraishi","year":"2020","journal-title":"J. Crohns Colitis"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Yilmaz, B., Spalinger, M.R., Biedermann, L., Franc, Y., Fournier, N., Rossel, J.B., Juillerat, P., Rogler, G., Macpherson, A.J., and Scharl, M. (2018). The presence of genetic risk variants within PTPN2 and PTPN22 is associated with intestinal microbiota alterations in Swiss IBD cohort patients. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0199664"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1007\/s00011-013-0673-5","article-title":"Associations between PTPN2 polymorphisms and susceptibility to ulcerative colitis and Crohn\u2019s disease: A meta-analysis","volume":"63","author":"Zhang","year":"2014","journal-title":"Inflamm. Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1038\/ng2068","article-title":"Robust associations of four new chromosome regions from genome-wide analyses of type 1 diabetes","volume":"39","author":"Todd","year":"2007","journal-title":"Nat. Genet."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"900","DOI":"10.1002\/ibd.21913","article-title":"Crohn\u2019s disease-associated polymorphism within the PTPN2 gene affects muramyl-dipeptide-induced cytokine secretion and autophagy","volume":"18","author":"Scharl","year":"2012","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1038\/nrgastro.2016.154","article-title":"Genetics of primary sclerosing cholangitis and pathophysiological implications","volume":"14","author":"Jiang","year":"2017","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1038\/s41591-018-0308-z","article-title":"Microbial network disturbances in relapsing refractory Crohn\u2019s disease","volume":"25","author":"Yilmaz","year":"2019","journal-title":"Nat. Med."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Sundquist, A., Bigdeli, S., Jalili, R., Druzin, M.L., Waller, S., Pullen, K.M., El-Sayed, Y.Y., Taslimi, M.M., Batzoglou, S., and Ronaghi, M. (2007). Bacterial flora-typing with targeted, chip-based Pyrosequencing. BMC Microbiol., 7.","DOI":"10.1186\/1471-2180-7-108"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.mimet.2012.07.008","article-title":"Microbial 16S rRNA Ion Tag and community metagenome sequencing using the Ion Torrent (PGM) Platform","volume":"91","author":"Whiteley","year":"2012","journal-title":"J. Microbiol. Methods"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/nmeth.f.303","article-title":"QIIME allows analysis of high-throughput community sequencing data","volume":"7","author":"Caporaso","year":"2010","journal-title":"Nat. Methods"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"McMurdie, P.J., and Holmes, S. (2013). phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0061217"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1492","DOI":"10.12688\/f1000research.8986.1","article-title":"Bioconductor Workflow for Microbiome Data Analysis: From raw reads to community analyses","volume":"5","author":"Callahan","year":"2016","journal-title":"F1000Research"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"R79","DOI":"10.1186\/gb-2012-13-9-r79","article-title":"Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment","volume":"13","author":"Morgan","year":"2012","journal-title":"Genome Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1055\/s-0037-1608801","article-title":"The Microbiome in Primary Sclerosing Cholangitis: Current Evidence and Potential Concepts","volume":"37","author":"Hov","year":"2017","journal-title":"Semin Liver Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1159\/000444479","article-title":"The Clinical Relevance of the IBD-Associated Variation within the Risk Gene Locus Encoding Protein Tyrosine Phosphatase Non-Receptor Type 2 in Patients of the Swiss IBD Cohort","volume":"93","author":"Spalinger","year":"2016","journal-title":"Digestion"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Rinninella, E., Raoul, P., Cintoni, M., Franceschi, F., Miggiano, G.A.D., Gasbarrini, A., and Mele, M.C. (2019). What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms, 7.","DOI":"10.3390\/microorganisms7010014"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Stojanov, S., Berlec, A., and \u0160trukelj, B. (2020). The Influence of Probiotics on the Firmicutes\/Bacteroidetes Ratio in the Treatment of Obesity and Inflammatory Bowel disease. Microorganisms, 8.","DOI":"10.3390\/microorganisms8111715"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Abenavoli, L., Scarpellini, E., Colica, C., Boccuto, L., Salehi, B., Sharifi-Rad, J., Aiello, V., Romano, B., De Lorenzo, A., and Izzo, A.A. (2019). Gut Microbiota and Obesity: A Role for Probiotics. Nutrients, 11.","DOI":"10.3390\/nu11112690"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5","DOI":"10.3748\/wjg.v24.i1.5","article-title":"Relationship between intestinal microbiota and ulcerative colitis: Mechanisms and clinical application of probiotics and fecal microbiota transplantation","volume":"24","author":"Shen","year":"2018","journal-title":"World J. Gastroenterol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"598152","DOI":"10.3389\/fimmu.2020.598152","article-title":"Gut Microbiome of Children and Adolescents with Primary Sclerosing Cholangitis in Association with Ulcerative Colitis","volume":"11","author":"Cortez","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1136\/gutjnl-2016-311915","article-title":"The gut-adherent microbiota of PSC-IBD is distinct to that of IBD","volume":"66","author":"Quraishi","year":"2017","journal-title":"Gut"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1016\/j.chom.2019.04.002","article-title":"Bacteroides-Derived Sphingolipids Are Critical for Maintaining Intestinal Homeostasis and Symbiosis","volume":"25","author":"Brown","year":"2019","journal-title":"Cell Host Microbe"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1136\/gutjnl-2015-311004","article-title":"Primary sclerosing cholangitis is characterised by intestinal dysbiosis independent from IBD","volume":"65","author":"Sabino","year":"2016","journal-title":"Gut"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.chom.2013.07.007","article-title":"Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment","volume":"14","author":"Kostic","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"8783","DOI":"10.3748\/wjg.v20.i27.8783","article-title":"Primary sclerosing cholangitis as an independent risk factor for colorectal cancer in the context of inflammatory bowel disease: A review of the literature","volume":"20","author":"Wang","year":"2014","journal-title":"World J. Gastroenterol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.apsb.2015.01.006","article-title":"The human gut sterolbiome: Bile acid-microbiome endocrine aspects and therapeutics","volume":"5","author":"Ridlon","year":"2015","journal-title":"Acta Pharm. Sin. B"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1016\/j.femsre.2004.09.003","article-title":"The interaction between bacteria and bile","volume":"29","author":"Begley","year":"2005","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"14","DOI":"10.3390\/pathogens3010014","article-title":"Metabolism of cholesterol and bile acids by the gut microbiota","volume":"3","year":"2013","journal-title":"Pathogens"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"13580","DOI":"10.1073\/pnas.0804437105","article-title":"Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome","volume":"105","author":"Jones","year":"2008","journal-title":"Proc. Nat. Acad. Sci. USA"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/s40168-019-0628-3","article-title":"Taxonomic profiling and populational patterns of bacterial bile salt hydrolase (BSH) genes based on worldwide human gut microbiome","volume":"7","author":"Song","year":"2019","journal-title":"Microbiome"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1287","DOI":"10.1002\/ibd.21891","article-title":"Protein tyrosine phosphatase nonreceptor type 2 regulates autophagosome formation in human intestinal cells","volume":"18","author":"Scharl","year":"2012","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"918","DOI":"10.1038\/mi.2014.122","article-title":"PTPN2 controls differentiation of CD4\u207a T cells and limits intestinal inflammation and intestinal dysbiosis","volume":"8","author":"Spalinger","year":"2015","journal-title":"Mucosal Immunol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1117","DOI":"10.1136\/gutjnl-2020-321466","article-title":"Association between Brachyspira and irritable bowel syndrome with diarrhoea","volume":"70","author":"Jabbar","year":"2020","journal-title":"Gut"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1038\/nrm2026","article-title":"The ARP2\/3 complex: An actin nucleator comes of age","volume":"7","author":"Goley","year":"2006","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1114","DOI":"10.1016\/j.bbapap.2017.06.005","article-title":"Deciphering the protein-protein interaction network regulating hepatocellular carcinoma metastasis","volume":"1865","author":"Qin","year":"2017","journal-title":"Biochim. Biophys. Acta Proteins Proteom."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1356","DOI":"10.1016\/j.prp.2018.05.028","article-title":"ARP3 promotes tumor metastasis and predicts a poor prognosis in hepatocellular carcinoma","volume":"214","author":"Lv","year":"2018","journal-title":"Pathol. Res. Pract."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.prp.2018.10.011","article-title":"Actin related protein 3 (ARP3) promotes apoptosis of intestinal epithelial cells in ulcerative colitis","volume":"215","author":"Zhang","year":"2019","journal-title":"Pathol. Res. Pract."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1083\/jcb.201306032","article-title":"Loss of Arp2\/3 induces an NF-\u03baB-dependent, nonautonomous effect on chemotactic signaling","volume":"203","author":"Wu","year":"2013","journal-title":"J. Cell Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1802866","DOI":"10.1080\/19490976.2020.1802866","article-title":"Gut microbes from the phylogenetically diverse genus","volume":"12","author":"Mukherjee","year":"2020","journal-title":"Gut Microbes"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Jeong, J.Y., Kim, T.B., Kim, J., Choi, H.W., Kim, E.J., Yoo, H.J., Lee, S., Jun, H.R., Yoo, W., and Kim, S. (2020). Diversity in the Extracellular Vesicle-Derived Microbiome of Tissues According to Tumor Progression in Pancreatic Cancer. Cancers, 12.","DOI":"10.3390\/cancers12092346"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/8\/1752\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:45:17Z","timestamp":1760165117000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/8\/1752"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,8,17]]},"references-count":59,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2021,8]]}},"alternative-id":["microorganisms9081752"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9081752","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,8,17]]}}}