Human colon mucosal biofilms from healthy or colon cancer hosts are carcinogenic
Mucus-invasive bacterial biofilms are identified on the colon mucosa of approximately 50% of colorectal cancer (CRC) patients and approximately 13% of healthy subjects. Here, we test the hypothesis that human colon biofilms comprise microbial communities that are carcinogenic in CRC mouse models. Ho...
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| Vydáno v: | The Journal of clinical investigation Ročník 129; číslo 4; s. 1699 - 1712 |
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| Hlavní autoři: | , , , , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
United States
American Society for Clinical Investigation
01.04.2019
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| Témata: | |
| ISSN: | 0021-9738, 1558-8238, 1558-8238 |
| On-line přístup: | Získat plný text |
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| Abstract | Mucus-invasive bacterial biofilms are identified on the colon mucosa of approximately 50% of colorectal cancer (CRC) patients and approximately 13% of healthy subjects. Here, we test the hypothesis that human colon biofilms comprise microbial communities that are carcinogenic in CRC mouse models. Homogenates of human biofilm-positive colon mucosa were prepared from tumor patients (tumor and paired normal tissues from surgical resections) or biofilm-positive biopsies from healthy individuals undergoing screening colonoscopy; homogenates of biofilm-negative colon biopsies from healthy individuals undergoing screening colonoscopy served as controls. After 12 weeks, biofilm-positive, but not biofilm-negative, human colon mucosal homogenates induced colon tumor formation in 3 mouse colon tumor models (germ-free ApcMinΔ850/+;Il10-/- or ApcMinΔ850/+ and specific pathogen-free ApcMinΔ716/+ mice). Remarkably, biofilm-positive communities from healthy colonoscopy biopsies induced colon inflammation and tumors similarly to biofilm-positive tumor tissues. By 1 week, biofilm-positive human tumor homogenates, but not healthy biopsies, displayed consistent bacterial mucus invasion and biofilm formation in mouse colons. 16S rRNA gene sequencing and RNA-Seq analyses identified compositional and functional microbiota differences between mice colonized with biofilm-positive and biofilm-negative communities. These results suggest human colon mucosal biofilms, whether from tumor hosts or healthy individuals undergoing screening colonoscopy, are carcinogenic in murine models of CRC. |
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| AbstractList | Mucus-invasive bacterial biofilms are identified on the colon mucosa of approximately 50% of colorectal cancer (CRC) patients and approximately 13% of healthy subjects. Here, we test the hypothesis that human colon biofilms comprise microbial communities that are carcinogenic in CRC mouse models. Homogenates of human biofilm-positive colon mucosa were prepared from tumor patients (tumor and paired normal tissues from surgical resections) or biofilm-positive biopsies from healthy individuals undergoing screening colonoscopy; homogenates of biofilm-negative colon biopsies from healthy individuals undergoing screening colonoscopy served as controls. After 12 weeks, biofilm-positive, but not biofilm-negative, human colon mucosal homogenates induced colon tumor formation in 3 mouse colon tumor models (germ-free ApcMinΔ850/+;Il10–/– or ApcMinΔ850/+ and specific pathogen–free ApcMinΔ716/+ mice). Remarkably, biofilm-positive communities from healthy colonoscopy biopsies induced colon inflammation and tumors similarly to biofilm-positive tumor tissues. By 1 week, biofilm-positive human tumor homogenates, but not healthy biopsies, displayed consistent bacterial mucus invasion and biofilm formation in mouse colons. 16S rRNA gene sequencing and RNA-Seq analyses identified compositional and functional microbiota differences between mice colonized with biofilm-positive and biofilm-negative communities. These results suggest human colon mucosal biofilms, whether from tumor hosts or healthy individuals undergoing screening colonoscopy, are carcinogenic in murine models of CRC. Mucus-invasive bacterial biofilms are identified on the colon mucosa of approximately 50% of colorectal cancer (CRC) patients and approximately 13% of healthy subjects. Here, we test the hypothesis that human colon biofilms comprise microbial communities that are carcinogenic in CRC mouse models. Homogenates of human biofilm-positive colon mucosa were prepared from tumor patients (tumor and paired normal tissues from surgical resections) or biofilm-positive biopsies from healthy individuals undergoing screening colonoscopy; homogenates of biofilm-negative colon biopsies from healthy individuals undergoing screening colonoscopy served as controls. After 12 weeks, biofilm-positive, but not biofilm-negative, human colon mucosal homogenates induced colon tumor formation in 3 mouse colon tumor models (germ-free ApcMinΔ850/+;Il10-/- or ApcMinΔ850/+ and specific pathogen-free ApcMinΔ716/+ mice). Remarkably, biofilm-positive communities from healthy colonoscopy biopsies induced colon inflammation and tumors similarly to biofilm-positive tumor tissues. By 1 week, biofilm-positive human tumor homogenates, but not healthy biopsies, displayed consistent bacterial mucus invasion and biofilm formation in mouse colons. 16S rRNA gene sequencing and RNA-Seq analyses identified compositional and functional microbiota differences between mice colonized with biofilm-positive and biofilm-negative communities. These results suggest human colon mucosal biofilms, whether from tumor hosts or healthy individuals undergoing screening colonoscopy, are carcinogenic in murine models of CRC.Mucus-invasive bacterial biofilms are identified on the colon mucosa of approximately 50% of colorectal cancer (CRC) patients and approximately 13% of healthy subjects. Here, we test the hypothesis that human colon biofilms comprise microbial communities that are carcinogenic in CRC mouse models. Homogenates of human biofilm-positive colon mucosa were prepared from tumor patients (tumor and paired normal tissues from surgical resections) or biofilm-positive biopsies from healthy individuals undergoing screening colonoscopy; homogenates of biofilm-negative colon biopsies from healthy individuals undergoing screening colonoscopy served as controls. After 12 weeks, biofilm-positive, but not biofilm-negative, human colon mucosal homogenates induced colon tumor formation in 3 mouse colon tumor models (germ-free ApcMinΔ850/+;Il10-/- or ApcMinΔ850/+ and specific pathogen-free ApcMinΔ716/+ mice). Remarkably, biofilm-positive communities from healthy colonoscopy biopsies induced colon inflammation and tumors similarly to biofilm-positive tumor tissues. By 1 week, biofilm-positive human tumor homogenates, but not healthy biopsies, displayed consistent bacterial mucus invasion and biofilm formation in mouse colons. 16S rRNA gene sequencing and RNA-Seq analyses identified compositional and functional microbiota differences between mice colonized with biofilm-positive and biofilm-negative communities. These results suggest human colon mucosal biofilms, whether from tumor hosts or healthy individuals undergoing screening colonoscopy, are carcinogenic in murine models of CRC. Mucus-invasive bacterial biofilms are identified on the colon mucosa of approximately 50% of colorectal cancer (CRC) patients and approximately 13% of healthy subjects. Here, we test the hypothesis that human colon biofilms comprise microbial communities that are carcinogenic in CRC mouse models. Homogenates of human biofilm-positive colon mucosa were prepared from tumor patients (tumor and paired normal tissues from surgical resections) or biofilm-positive biopsies from healthy individuals undergoing screening colonoscopy; homogenates of biofilm-negative colon biopsies from healthy individuals undergoing screening colonoscopy served as controls. After 12 weeks, biofilm-positive, but not biofilm-negative, human colon mucosal homogenates induced colon tumor formation in 3 mouse colon tumor models (germ-free [Apc.sup.Min[DELTA]850/+]; [Il10.sup.-/-] or [Apc.sup.Min[DELTA]850/+] and specific pathogen-free [Apc.sup.Min[DELTA]716/+] mice). Remarkably, biofilm-positive communities from healthy colonoscopy biopsies induced colon inflammation and tumors similarly to biofilm-positive tumor tissues. By 1 week, biofilm-positive human tumor homogenates, but not healthy biopsies, displayed consistent bacterial mucus invasion and biofilm formation in mouse colons. 16S rRNA gene sequencing and RNA-Seq analyses identified compositional and functional microbiota differences between mice colonized with biofilm-positive and biofilm-negative communities. These results suggest human colon mucosal biofilms, whether from tumor hosts or healthy individuals undergoing screening colonoscopy, are carcinogenic in murine models of CRC. |
| Audience | Academic |
| Author | Wu, Xinqun Anders, Robert A. Pardoll, Drew M. Jobin, Christian Drewes, Julia L. Chung, Liam Perez-Chanona, Ernesto Wu, Shaoguang Sears, Cynthia L. Pope, Jillian L. Besharati, Sepideh Housseau, Franck Tomkovich, Sarah Liu, Xiuli Fathi, Payam Fodor, Anthony A. Dejea, Christine M. White, James R. Gauthier, Josee Sun, Xiaolun Ding, Hua Winglee, Kathryn Mühlbauer, Marcus Yang, Ye Gharaibeh, Raad Z. Wang, Hao |
| AuthorAffiliation | 7 Department of Infectious Diseases and Immunology, University of Florida, Gainesville, Florida, USA 2 Bloomberg-Kimmel Institute for Immunotherapy, Departments of Oncology and Medicine and the Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins School of Medicine, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA 4 Department of Pathology, Immunology and Laboratory Medicine, University of Florida, Gainesville, Florida, USA 5 Department of Pathology, Johns Hopkins University, Baltimore, Maryland, USA 3 Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, North Carolina, USA 1 Department of Medicine, University of Florida, Gainesville, Florida, USA 6 Resphera Biosciences, Baltimore, Maryland, USA |
| AuthorAffiliation_xml | – name: 6 Resphera Biosciences, Baltimore, Maryland, USA – name: 2 Bloomberg-Kimmel Institute for Immunotherapy, Departments of Oncology and Medicine and the Sidney Kimmel Comprehensive Cancer Center, Johns Hopkins School of Medicine, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA – name: 7 Department of Infectious Diseases and Immunology, University of Florida, Gainesville, Florida, USA – name: 5 Department of Pathology, Johns Hopkins University, Baltimore, Maryland, USA – name: 1 Department of Medicine, University of Florida, Gainesville, Florida, USA – name: 4 Department of Pathology, Immunology and Laboratory Medicine, University of Florida, Gainesville, Florida, USA – name: 3 Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, North Carolina, USA |
| Author_xml | – sequence: 1 givenname: Sarah orcidid: 0000-0003-1638-5307 surname: Tomkovich fullname: Tomkovich, Sarah – sequence: 2 givenname: Christine M. surname: Dejea fullname: Dejea, Christine M. – sequence: 3 givenname: Kathryn orcidid: 0000-0002-3623-0700 surname: Winglee fullname: Winglee, Kathryn – sequence: 4 givenname: Julia L. orcidid: 0000-0002-5060-0624 surname: Drewes fullname: Drewes, Julia L. – sequence: 5 givenname: Liam surname: Chung fullname: Chung, Liam – sequence: 6 givenname: Franck surname: Housseau fullname: Housseau, Franck – sequence: 7 givenname: Jillian L. surname: Pope fullname: Pope, Jillian L. – sequence: 8 givenname: Josee surname: Gauthier fullname: Gauthier, Josee – sequence: 9 givenname: Xiaolun orcidid: 0000-0001-5601-0812 surname: Sun fullname: Sun, Xiaolun – sequence: 10 givenname: Marcus surname: Mühlbauer fullname: Mühlbauer, Marcus – sequence: 11 givenname: Xiuli surname: Liu fullname: Liu, Xiuli – sequence: 12 givenname: Payam surname: Fathi fullname: Fathi, Payam – sequence: 13 givenname: Robert A. surname: Anders fullname: Anders, Robert A. – sequence: 14 givenname: Sepideh orcidid: 0000-0003-3200-1895 surname: Besharati fullname: Besharati, Sepideh – sequence: 15 givenname: Ernesto surname: Perez-Chanona fullname: Perez-Chanona, Ernesto – sequence: 16 givenname: Ye orcidid: 0000-0002-7576-3067 surname: Yang fullname: Yang, Ye – sequence: 17 givenname: Hua surname: Ding fullname: Ding, Hua – sequence: 18 givenname: Xinqun orcidid: 0000-0003-4661-799X surname: Wu fullname: Wu, Xinqun – sequence: 19 givenname: Shaoguang surname: Wu fullname: Wu, Shaoguang – sequence: 20 givenname: James R. surname: White fullname: White, James R. – sequence: 21 givenname: Raad Z. surname: Gharaibeh fullname: Gharaibeh, Raad Z. – sequence: 22 givenname: Anthony A. surname: Fodor fullname: Fodor, Anthony A. – sequence: 23 givenname: Hao surname: Wang fullname: Wang, Hao – sequence: 24 givenname: Drew M. surname: Pardoll fullname: Pardoll, Drew M. – sequence: 25 givenname: Christian surname: Jobin fullname: Jobin, Christian – sequence: 26 givenname: Cynthia L. orcidid: 0000-0003-4059-1661 surname: Sears fullname: Sears, Cynthia L. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30855275$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2019 American Society for Clinical Investigation Copyright American Society for Clinical Investigation Apr 2019 2019 American Society for Clinical Investigation 2019 American Society for Clinical Investigation |
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| SubjectTerms | Animal models Animals Biofilms Biomedical research Biopsy Cancer patients Carcinogenesis Carcinogens Colon - metabolism Colon - microbiology Colon cancer Colonic Neoplasms - genetics Colonic Neoplasms - metabolism Colonic Neoplasms - microbiology Colonic Neoplasms - pathology Colonoscopy Colorectal cancer Colorectal carcinoma Diagnosis Gastrointestinal diseases Gastrointestinal Microbiome Genes Genetic aspects Genetic research Genomes Germfree Humans Hypotheses Inflammation Inflammatory bowel disease Interleukin 1 Interleukin 10 Invasiveness Laboratory rats Mice Mice, Knockout Microbial mats Microbiota Microbiota (Symbiotic organisms) Mucosa Mucus Neoplasms, Experimental - genetics Neoplasms, Experimental - metabolism Neoplasms, Experimental - microbiology Neoplasms, Experimental - pathology RNA RNA sequencing rRNA 16S Tumorigenesis Tumors |
| Title | Human colon mucosal biofilms from healthy or colon cancer hosts are carcinogenic |
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