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Human colon mucosal biofilms from healthy or colon cancer hosts are carcinogenic
Open accessAbstract
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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“The enrichment of bacterial species from the oral cavity is characteristic of the CRC GOMS50,76–79, along with an enrichment in invasive polymicrobial bacterial biofilms in patients with right-sided tumours76,80,81.”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [80]
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“It is now well appreciated that gut microbiota affect anticancer immunity, controlling spontaneous tumor growth (Arthur et al., 2012; Dejea et al., 2018; Tomkovich et al., 2019) as well as response to chemo- and immunotherapy (Iida et al., 2013; Mager et al., 2020; Paulos et al., 2007; Sivan et al., 2015; Tanoue et al., 2019; Vetizou et al., 2015; Viaud et al., 2013).”
From Microbiota triggers STING-type I IFN-dependent monocyte reprogramming of the tumor microenvironment (2021) · cites this paper as Tomkovich et al., 2019
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БІОПЛІВКИ ЯК ФОРМА ІСНУВАННЯ МІКРООРГАНІЗМІВ В ОРГАНІЗМІ ЛЮДИНИ
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Metadata
- Authors
- Tomkovich, S., Dejea, C. M., Winglee, K., Drewes, J. L., Chung, L., Housseau, F., Pope, J. L., Gauthier, J., Sun, X., Mühlbauer, M., Liu, X., Fathi, P., Anders, R. A., Besharati, S., Perez-Chanona, E., Yang, Y., Ding, H., Wu, X., Wu, S., White, J. R., Gharaibeh, R. Z., Fodor, A. A., Wang, H., Pardoll, D. M., Jobin, C., & Sears, C. L.
- Affiliations
- University of Florida (US)
- Johns Hopkins University (US)
- University of North Carolina at Charlotte (US)
- Resphera Biosciences (US)
- Corresponding author
- Jobin, Christian
- Sears, Cynthia L.
- ORCID
- Tomkovich, Sarah
- Dejea, Christine M.
- Winglee, Kathryn
- Drewes, Julia L.
- Chung, Liam
- Housseau, Franck
- Sun, Xiaolun
- Mühlbauer, Marcus
- Liu, Xiuli
- Anders, Robert A.
- Besharati, Sepideh
- 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.
- Venue
- Journal of Clinical Investigation
- Published
- 2019-03-11
- Volume
- 129
- Issue
- 4
- Pages
- 1699-1712
- ISSN
- 0021-9738 (ISSN-L)
- 1558-8238
- PMC
- PMC6436866
- OpenAlex
- W2921953499
- Cited by
- 209
- References
- 49
- Citations by year
- 2026: 15 · 2025: 20 · 2024: 29 · 2023: 33 · 2022: 24 · 2021: 45 · 2020: 31 · 2019: 11
- FWCI
- 9.18
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NIH (R01DK073338, R01DK47700, R01 CA151393, R01CA196845, P50 CA62924, P30 CA006973, P30 DK089502, K99 CA230192, S10OD016374)
- Bloomberg Philanthropies (Microbiome Project)
- Johns Hopkins Discovery Award (Internal award)
- Commonwealth Foundation (Johns Hopkins)
- Cancer Research Institute/Fight Colorectal Cancer coalition (CRC discovery award)
- University of Florida Health Cancer Center Funds (internal award)
- University of Florida Department of Medicine Gatorade Fund (internal award)
- Crohn’s and Colitis Foundation (CCFA Ref. #409472)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
- Keywords
- colorectal cancer, carcinogenesis, gut microbiota, ApcMin/+ mice, germ-free mice, colonic inflammation, tumor formation, microbial communities, 16S rRNA gene sequencing, RNA-seq
- MeSH terms
- Gastrointestinal Microbiome, Animals, Colon, Colonic Neoplasms, Humans, Neoplasms, Experimental, Mice, Knockout, Biofilms, Mice, Carcinogenesis
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