{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,15]],"date-time":"2026-05-15T05:19:53Z","timestamp":1778822393253,"version":"3.51.4"},"reference-count":45,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2020,7,11]],"date-time":"2020-07-11T00:00:00Z","timestamp":1594425600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","award":["IP7\/ 01KI1725D, PAC-Campylobacter, Research Network Zoonotic Infectious Diseases"],"award-info":[{"award-number":["IP7\/ 01KI1725D, PAC-Campylobacter, Research Network Zoonotic Infectious Diseases"]}],"id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006360","name":"Bundesministerium f\u00fcr Wirtschaft und Energie","doi-asserted-by":"publisher","award":["ZIM; ZF4117904 AJ8"],"award-info":[{"award-number":["ZIM; ZF4117904 AJ8"]}],"id":[{"id":"10.13039\/501100006360","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Human infections with the food-borne enteropathogens Campylobacter are progressively rising. Recent evidence revealed that pre-existing intestinal inflammation facilitates enteropathogenic infection subsequently exacerbating the underlying disease. Given that only little is known about C. coli\u2013host interactions and particularly during intestinal inflammation, the aim of the present study was to survey gastrointestinal colonization properties, gut microbiota changes and pro-inflammatory sequelae upon peroral C. coli-infection of IL-10-\/- mice with chronic colitis. C. coli colonized the gastrointestinal tract of mice with varying efficiencies until day 28 post-infection and induced macroscopic and microscopic inflammatory changes as indicated by shorter colonic lengths, more distinct histopathological changes in the colonic mucosa and higher numbers of apoptotic colonic epithelial cells when compared to mock-infected controls. Furthermore, not only colonic innate and adaptive immune cell responses, but also enhanced systemic TNF-\u03b1 secretion could be observed following C. coli as opposed to mock challenge. Notably, C. coli induced intestinal inflammatory sequelae were accompanied with gut microbiota shifts towards higher commensal enterobacterial loads in the infected gut lumen. Moreover, the pathogen translocated from the intestinal tract to extra-intestinal tissue sites in some cases, but never to systemic compartments. Hence, C. coli accelerates inflammatory immune responses in IL-10-\/- mice with chronic colitis.<\/jats:p>","DOI":"10.3390\/pathogens9070560","type":"journal-article","created":{"date-parts":[[2020,7,14]],"date-time":"2020-07-14T04:46:01Z","timestamp":1594701961000},"page":"560","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Inflammatory Immune Responses and Gut Microbiota Changes Following Campylobacter coli Infection of IL-10-\/- Mice with Chronic Colitis"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6399-651X","authenticated-orcid":false,"given":"Markus M.","family":"Heimesaat","sequence":"first","affiliation":[{"name":"Institute of Microbiology, Infectious Diseases and Immunology, Charit\u00e9\u2014University Medicine Berlin, Corporate Member of Freie Universit\u00e4t Berlin, Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health, 12203 Berlin, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Claudia","family":"Genger","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, Infectious Diseases and Immunology, Charit\u00e9\u2014University Medicine Berlin, Corporate Member of Freie Universit\u00e4t Berlin, Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health, 12203 Berlin, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nina","family":"Biesemeier","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, Infectious Diseases and Immunology, Charit\u00e9\u2014University Medicine Berlin, Corporate Member of Freie Universit\u00e4t Berlin, Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health, 12203 Berlin, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sigri","family":"Klove","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, Infectious Diseases and Immunology, Charit\u00e9\u2014University Medicine Berlin, Corporate Member of Freie Universit\u00e4t Berlin, Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health, 12203 Berlin, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dennis","family":"Weschka","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, Infectious Diseases and Immunology, Charit\u00e9\u2014University Medicine Berlin, Corporate Member of Freie Universit\u00e4t Berlin, Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health, 12203 Berlin, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Soraya","family":"Mousavi","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, Infectious Diseases and Immunology, Charit\u00e9\u2014University Medicine Berlin, Corporate Member of Freie Universit\u00e4t Berlin, Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health, 12203 Berlin, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Stefan","family":"Bereswill","sequence":"additional","affiliation":[{"name":"Institute of Microbiology, Infectious Diseases and Immunology, Charit\u00e9\u2014University Medicine Berlin, Corporate Member of Freie Universit\u00e4t Berlin, Humboldt-Universit\u00e4t zu Berlin, and Berlin Institute of Health, 12203 Berlin, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,7,11]]},"reference":[{"key":"ref_1","unstructured":"World Health Organization (WHO) (2020, April 06). Campylobacter. Available online: https:\/\/www.who.int\/news-room\/fact-sheets\/detail\/campylobacter."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1007\/s00103-011-1289-y","article-title":"Die Campylobacteriose des Menschen","volume":"54","author":"Alter","year":"2011","journal-title":"Bundesgesundheitsblatt\u2014Gesundheitsforschung\u2014Gesundheitsschutz"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1556\/EuJMI.2.2012.1.9","article-title":"Colonization properties of Campylobacter jejuni in chickens","volume":"2","author":"Pielsticker","year":"2012","journal-title":"Eur. J. Microbiol. Immunol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1128\/mr.50.1.81-94.1986","article-title":"Pathophysiology of Campylobacter enteritis","volume":"50","author":"Walker","year":"1986","journal-title":"Microbiol. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1159\/000060405","article-title":"Campylobacter jejuni","volume":"8","author":"Kist","year":"2001","journal-title":"Contrib. Microbiol."},{"key":"ref_6","unstructured":"(2017). Human campylobacteriosis. Campylobacter, Academic Press. Chapter 1."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"945","DOI":"10.1136\/gut.26.9.945","article-title":"Campylobacter colitis: Histological immunohistochemical and ultrastructural findings","volume":"26","author":"Duursma","year":"1985","journal-title":"Gut"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1128\/CMR.00055-07","article-title":"Host-Pathogen Interactions in Campylobacter Infections: The Host Perspective","volume":"21","author":"Janssen","year":"2008","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"a018119","DOI":"10.1101\/cshperspect.a018119","article-title":"The Evolution of Campylobacter jejuni and Campylobacter coli","volume":"7","author":"Sheppard","year":"2015","journal-title":"Cold Spring Harb. Perspect. Boil."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"S125","DOI":"10.1086\/513783","article-title":"Association between Campylobacter infection and Guillain-Barr\u00e9 syndrome","volume":"176","author":"Allos","year":"1997","journal-title":"J. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1097\/00054725-200205000-00009","article-title":"Role of Infections in the Manifestation or Reactivation of Inflammatory Bowel Diseases","volume":"8","author":"Stallmach","year":"2002","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1588","DOI":"10.1053\/j.gastro.2006.02.004","article-title":"Acute Gastroenteritis Is Followed by an Increased Risk of Inflammatory Bowel Disease","volume":"130","year":"2006","journal-title":"Gastroenterology"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1053\/j.gastro.2009.04.001","article-title":"Increased Short- and Long-Term Risk of Inflammatory Bowel Disease after Salmonella or Campylobacter Gastroenteritis","volume":"137","author":"Gradel","year":"2009","journal-title":"Gastroenterology"},{"key":"ref_14","first-page":"G1","article-title":"A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease?","volume":"298","author":"Kalischuk","year":"2010","journal-title":"Am. J. Physiol. Liver Physiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1097\/MOG.0b013e32834c453e","article-title":"Gastrointestinal infection as a trigger for inflammatory bowel disease","volume":"28","author":"Mann","year":"2012","journal-title":"Curr. Opin. Gastroenterol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1016\/S0140-6736(80)92078-4","article-title":"Campylobacter Jejuni Causing Flare-up in Inflammatory Bowel Disease","volume":"316","author":"Newman","year":"1980","journal-title":"Lancet"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.diagmicrobio.2003.12.004","article-title":"Campylobacter infection in 682 bulgarian patients with acute enterocolitis, inflammatory bowel disease, and other chronic intestinal diseases","volume":"49","author":"Boyanova","year":"2004","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1159\/000212076","article-title":"Prospective, Observational, Cross-Sectional Study of Intestinal Infections among Acutely Active Inflammatory Bowel Disease Patients","volume":"80","author":"Bernal","year":"2009","journal-title":"Digestion"},{"key":"ref_19","first-page":"287","article-title":"Risk factors and clinical implication of superimposed Campylobacter jejuni infection in patients with underlying ulcerative colitis","volume":"4","author":"Arora","year":"2015","journal-title":"Gastroenterol. Rep."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"159","DOI":"10.4161\/gmic.2.3.16104","article-title":"Intestinal steroid profiles and microbiota composition in colitic mice","volume":"2","author":"Wohlgemuth","year":"2011","journal-title":"Gut Microbes"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Heimesaat, M.M., Alutis, M., Grundmann, U., Fischer, A., Tegtmeyer, N., B\u00f6hm, M., K\u00fchl, A.A., G\u00f6bel, U.B., Backert, S., and Bereswill, S. (2014). The role of serine protease HtrA in acute ulcerative enterocolitis and extra-intestinal immune responses during Campylobacter jejuni infection of gnotobiotic IL-10 deficient mice. Front. Microbiol., 4.","DOI":"10.3389\/fcimb.2014.00077"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"8785","DOI":"10.4049\/jimmunol.177.12.8785","article-title":"Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii","volume":"177","author":"Heimesaat","year":"2006","journal-title":"J. Immunol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Bereswill, S., Fischer, A., Plickert, R., Haag, L.-M., Otto, B., K\u00fchl, A.A., Dashti, J.I., Zautner, A.E., Mu\u00f1oz, M., and Loddenkemper, C. (2011). Novel Murine Infection Models Provide Deep Insights into the \u201cM\u00e9nage \u00e0 Trois\u201d of Campylobacter jejuni, Microbiota and Host Innate Immunity. PLoS ONE, 6.","DOI":"10.1371\/annotation\/5247af81-4595-44b7-9c3f-2e45ad85abfa"},{"key":"ref_24","first-page":"4557","article-title":"A guide to histomorphological evaluation of intestinal inflammation in mouse models","volume":"7","author":"Erben","year":"2014","journal-title":"Int. J. Clin. Exp. Pathol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1097\/00004836-199206000-00008","article-title":"Microbic Superinfection in Relapse of Inflammatory Bowel Disease","volume":"14","author":"Weber","year":"1992","journal-title":"J. Clin. Gastroenterol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1097\/01.meg.0000131040.38607.09","article-title":"Enteric infection in relapse of inflammatory bowel disease","volume":"16","author":"Mylonaki","year":"2004","journal-title":"Eur. J. Gastroenterol. Hepatol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.crohns.2011.07.012","article-title":"Intestinal superinfections in patients with inflammatory bowel diseases","volume":"6","author":"Antonelli","year":"2012","journal-title":"J. Crohns. Coliti."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Genger, C., Kl\u00f8ve, S., Mousavi, S., Bereswill, S., and Heimesaat, M.M. (2020). The conundrum of colonization resistance against Campylobacter reloaded: The gut microbota composition in conventional mice does not prevent from Campylobacter coli infection. Eur. J. Microbiol. Immunol.","DOI":"10.1556\/1886.2020.00004"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.mimet.2013.06.031","article-title":"Molecular methods to investigate adhesion, transmigration, invasion and intracellular survival of the foodborne pathogen Campylobacter jejuni","volume":"95","author":"Backert","year":"2013","journal-title":"J. Microbiol. Methods"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1038\/s41579-018-0037-9","article-title":"Campylobacter jejuni: Collective components promoting a successful enteric lifestyle","volume":"16","author":"Burnham","year":"2018","journal-title":"Nat. Rev. Genet."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Kl\u00f8ve, S., Genger, C., Mousavi, S., Weschka, D., Bereswill, S., and Heimesaat, M.M. (2020). Toll-Like Receptor-4 Dependent Intestinal and Systemic Sequelae Following Peroral Campylobacter coli Infection of IL10 Deficient Mice Harboring a Human Gut Microbiota. Pathog., 9.","DOI":"10.3390\/pathogens9050386"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1038\/nrgastro.2017.88","article-title":"Gut microbiota and IBD: Causation or correlation?","volume":"14","author":"Ni","year":"2017","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1136\/gut.2006.104497","article-title":"Exacerbation of murine ileitis by Toll-like receptor 4 mediated sensing of lipopolysaccharide from commensal Escherichia coli","volume":"56","author":"Heimesaat","year":"2007","journal-title":"Gut"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Heimesaat, M.M., Fischer, A., Siegmund, B., Kupz, A., Niebergall, J., Fuchs, D., Jahn, H.-K., Freudenberg, M., Loddenkemper, C., and Batra, A. (2007). Shift Towards Pro-inflammatory Intestinal Bacteria Aggravates Acute Murine Colitis via Toll-like Receptors 2 and 4. PLoS ONE, 2.","DOI":"10.1371\/journal.pone.0000662"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Erridge, C., Duncan, S.H., Bereswill, S., and Heimesaat, M.M. (2010). The Induction of Colitis and Ileitis in Mice Is Associated with Marked Increases in Intestinal Concentrations of Stimulants of TLRs 2, 4, and 5. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009125"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1136\/gut.2009.197434","article-title":"MyD88\/TLR9 mediated immunopathology and gut microbiota dynamics in a novel murine model of intestinal graft-versus-host disease","volume":"59","author":"Heimesaat","year":"2010","journal-title":"Gut"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1556\/1886.2016.00036","article-title":"Dissecting the interplay between intestinal microbiota and host immunity in health and disease: Lessons learned from germfree and gnotobiotic animal models","volume":"6","author":"Fiebiger","year":"2016","journal-title":"Eur. J. Microbiol. Immunol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1053\/gast.2002.30294","article-title":"Mucosal flora in inflammatory bowel disease","volume":"122","author":"Swidsinski","year":"2002","journal-title":"Gastroenterology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3380","DOI":"10.1128\/JCM.43.7.3380-3389.2005","article-title":"Spatial Organization and Composition of the Mucosal Flora in Patients with Inflammatory Bowel Disease","volume":"43","author":"Swidsinski","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Rausch, S., Held, J., Fischer, A., Heimesaat, M.M., K\u00fchl, A.A., Bereswill, S., and Hartmann, S. (2013). Small Intestinal Nematode Infection of Mice Is Associated with Increased Enterobacterial Loads alongside the Intestinal Tract. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0074026"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"372","DOI":"10.3389\/fimmu.2017.00397","article-title":"Immune Responses to Broad-Spectrum Antibiotic Treatment and Fecal Microbiota Transplantation in Mice","volume":"8","author":"Ekmekciu","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1556\/1886.2015.00033","article-title":"The role of gelatinases inCampylobacter jejuniinfection of gnotobiotic mice","volume":"5","author":"Alutis","year":"2015","journal-title":"Eur. J. Microbiol. Immunol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1556\/1886.2015.00020","article-title":"Matrix Metalloproteinase-2 Mediates Intestinal Immunopathogenesis inCampylobacter jejuni-infected infant mice","volume":"5","author":"Alutis","year":"2015","journal-title":"Eur. J. Microbiol. Immunol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Heimesaat, M.M., Lugert, R., Fischer, A., Alutis, M., K\u00fchl, A.A., Zautner, A.E., Tareen, A.M., G\u00f6bel, U.B., and Bereswill, S. (2014). Impact of Campylobacter jejuni cj0268c Knockout Mutation on Intestinal Colonization, Translocation, and Induction of Immunopathology in Gnotobiotic IL-10 Deficient Mice. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0090148"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Vamanu, E., and Gatea, F. (2020). Correlations between Microbiota Bioactivity and Bioavailability of Functional Compounds: A Mini-Review. Biomedicines, 8.","DOI":"10.3390\/biomedicines8020039"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/7\/560\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:50:19Z","timestamp":1760176219000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/7\/560"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,11]]},"references-count":45,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2020,7]]}},"alternative-id":["pathogens9070560"],"URL":"https:\/\/doi.org\/10.3390\/pathogens9070560","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,7,11]]}}}