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
Hlavní autoři: Tomkovich, Sarah, Dejea, Christine M., Winglee, Kathryn, Drewes, Julia L., Chung, Liam, Housseau, Franck, Pope, Jillian L., Gauthier, Josee, Sun, Xiaolun, Mühlbauer, Marcus, Liu, Xiuli, Fathi, Payam, Anders, Robert A., Besharati, Sepideh, Perez-Chanona, Ernesto, Yang, Ye, Ding, Hua, Wu, Xinqun, Wu, Shaoguang, White, James R., Gharaibeh, Raad Z., Fodor, Anthony A., Wang, Hao, Pardoll, Drew M., Jobin, Christian, Sears, Cynthia L.
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States American Society for Clinical Investigation 01.04.2019
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ISSN:0021-9738, 1558-8238, 1558-8238
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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.
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
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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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Snippet Mucus-invasive bacterial biofilms are identified on the colon mucosa of approximately 50% of colorectal cancer (CRC) patients and approximately 13% of healthy...
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StartPage 1699
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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