The DOI matches its Crossref record; 49 of the 49 references it cites were found in a registry or an index.
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]
Experimental — accuracy not yet measuredIn the citing paper
“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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Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482
QIIME allows analysis of high-throughput community sequencing data
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., et al. (2010) · Nature Methods · doi:10.1038/nmeth.f.303 · Cited by 34,887
vegan: Community Ecology Package
Oksanen, J., Simpson, G. L., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., Sólymos, P., Stevens, M. H. H., Szöcs, E., et al. (2001) · doi:10.32614/cran.package.vegan · Cited by 27,099
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00062-07 · Cited by 20,145
A genetic model for colorectal tumorigenesis
Fearon, E. R., & Vogelstein, B. (1990) · Cell · doi:10.1016/0092-8674(90)90186-i · Cited by 12,132
A human gut microbial gene catalogue established by metagenomic sequencing
MetaHIT Consortium, Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., et al. (2010) · Nature · doi:10.1038/nature08821 · Cited by 11,624
nlme : Linear and nonlinear mixed effects models
DebRoy, S. (2006) · Medical Entomology and Zoology · Cited by 10,009
Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
Langille, M. G. I., Zaneveld, J., Caporaso, J. G., McDonald, D., Knights, D., Reyes, J. A., Clemente, J. C., Burkepile, D. E., Vega Thurber, R. L., Knight, R., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2676 · Cited by 9,116
Global patterns and trends in colorectal cancer incidence and mortality
Arnold, M., Sierra, M. S., Laversanne, M., Soerjomataram, I., Jemal, A., & Bray, F. (2016) · Gut · doi:10.1136/gutjnl-2015-310912 · Cited by 5,392
Intestinal inflammation targets cancer-inducing activity of the microbiota
Arthur, J. C., Perez-Chanona, E., Mühlbauer, M., Tomkovich, S., Uronis, J. M., Fan, T.-J., Campbell, B. J., Abujamel, T., Dogan, B., Rogers, A. B., et al. (2012) · Science · doi:10.1126/science.1224820 · Cited by 2,263
Cited by
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Inflammation and cancer: triggers, mechanisms, and consequences
Greten, F. R., & Grivennikov, S. I. (2019) · Immunity · doi:10.1016/j.immuni.2019.06.025 · Cited by 3,806
“, 2017), ability to form biofilms and initiate the outgrowth of the consortia of invasive bacteria (Dejea et al., 2018; Tomkovich et al., 2019) or ability to induce low grade inflammation disrupting the barrier (Wu et al.”
BackgroundBacterial Biofilm and its Role in the Pathogenesis of Disease
Vestby, L. K., Grønseth, T., Simm, R., & Nesse, L. L. (2020) · Antibiotics · doi:10.3390/antibiotics9020059 · Cited by 1,196
“recently reported that human colon mucosal biofilms were carcinogenic in murine CRC-models, whether the biofilm associated microbiota were from CRC-patients or healthy individuals [104] .”
BackgroundGut Microbiome: Profound Implications for Diet and Disease
Hills, R. D., Pontefract, B., Mishcon, H. R., Black, C. A., Sutton, S. C., & Theberge, C. R. (2019) · Nutrients · doi:10.3390/nu11071613 · Cited by 1,143
Colorectal Cancer in Inflammatory Bowel Disease: Mechanisms and Management
Shah, S. C., & Itzkowitz, S. H. (2021) · Gastroenterology · doi:10.1053/j.gastro.2021.10.035 · Cited by 904
Microbiota triggers STING-type I IFN-dependent monocyte reprogramming of the tumor microenvironment
Lam, K. C., Araya, R. E., Huang, A., Chen, Q., Di Modica, M., Rodrigues, R. R., Lopès, A., Johnson, S. B., Schwarz, B., Bohrnsen, E., et al. (2021) · Cell · doi:10.1016/j.cell.2021.09.019 · Cited by 604
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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