Thursday, November 7, 2024
No menu items!
HomeNatureColibactin-driven colon cancer requires adhesin-mediated epithelial binding

Colibactin-driven colon cancer requires adhesin-mediated epithelial binding

  • Brennan, C. A. & Garrett, W. S. Fusobacterium nucleatum—symbiont, opportunist and oncobacterium. Nat. Rev. Microbiol. 17, 156–166 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Janney, A., Powrie, F. & Mann, E. H. Host-microbiota maladaptation in colorectal cancer. Nature 585, 509–517 (2020).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • O’Keefe, S. J. Diet, microorganisms and their metabolites, and colon cancer. Nat. Rev. Gastroenterol. Hepatol. 13, 691–706 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tilg, H., Adolph, T. E., Gerner, R. R. & Moschen, A. R. The intestinal microbiota in colorectal cancer. Cancer Cell 33, 954–964 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wong, S. H. & Yu, J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications. Nat. Rev. Gastroenterol. Hepatol. 16, 690–704 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pleguezuelos-Manzano, C. et al. Mutational signature in colorectal cancer caused by genotoxic pks+ E. coli. Nature 580, 269–273 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Slowicka, K. et al. Zeb2 drives invasive and microbiota-dependent colon carcinoma. Nat. Cancer 1, 620–634 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Morgan, E. et al. Global burden of colorectal cancer in 2020 and 2040: incidence and mortality estimates from GLOBOCAN. Gut 72, 338–344 (2023).

    Article 
    PubMed 

    Google Scholar
     

  • Keum, N. & Giovannucci, E. Global burden of colorectal cancer: emerging trends, risk factors and prevention strategies. Nat. Rev. Gastroenterol. Hepatol. 16, 713–732 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • GBD 2019 Colorectal Cancer Collaborators. The global, regional, and national burden of colorectal cancer and its attributable risk factors in 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol. Hepatol. 4, 913–933 (2019).

    Article 

    Google Scholar
     

  • Zepeda-Rivera, M. et al. A distinct Fusobacterium nucleatum clade dominates the colorectal cancer niche. Nature https://doi.org/10.1038/s41586-024-07182-w (2024).

  • Buc, E. et al. High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS ONE 8, e56964 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arthur, J. C. et al. Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat. Commun. 5, 4724 (2014).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Dejea, C. M. et al. Patients with familial adenomatous polyposis harbor colonic biofilms containing tumorigenic bacteria. Science 359, 592–597 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nougayrede, J. P. et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 313, 848–851 (2006).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Cuevas-Ramos, G. et al. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc. Natl Acad. Sci. USA 107, 11537–11542 (2010).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rosendahl Huber, A. et al. Improved detection of colibactin-induced mutations by genotoxic E. coli in organoids and colorectal cancer. Cancer Cell 42, 487–496 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cougnoux, A. et al. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut 63, 1932–1942 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Brugiroux, S. et al. Genome-guided design of a defined mouse microbiota that confers colonization resistance against Salmonella enterica serovar Typhimurium. Nat. Microbiol. 2, 16215 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bonnet, M. et al. Colonization of the human gut by E. coli and colorectal cancer risk. Clin. Cancer Res. 20, 859–867 (2014).

    Article 
    PubMed 

    Google Scholar
     

  • Arthur, J. C. et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338, 120–123 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tomkovich, S. et al. Locoregional effects of microbiota in a preclinical model of colon carcinogenesis. Cancer Res. 77, 2620–2632 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Salesse, L. et al. Colibactin-producing Escherichia coli induce the formation of invasive carcinomas in a chronic inflammation-associated mouse model. Cancers 13, 2060 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lucas, C. et al. Autophagy of intestinal epithelial cells inhibits colorectal carcinogenesis induced by colibactin-producing Escherichia coli in ApcMin/+ mice. Gastroenterology 158, 1373–1388 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, Z. R. et al. Divergent biosynthesis yields a cytotoxic aminomalonate-containing precolibactin. Nat. Chem. Biol. 12, 773–775 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wernke, K. M. et al. Structure and bioactivity of colibactin. Bioorg. Med. Chem. Lett. 30, 127280 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Conover, M. S. et al. Inflammation-induced adhesin-receptor interaction provides a fitness advantage to uropathogenic E. coli during chronic infection. Cell Host Microbe 20, 482–492 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jones, C. H. et al. FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc. Natl Acad. Sci. USA 92, 2081–2085 (1995).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kalas, V. et al. Structure-based discovery of glycomimetic FmlH ligands as inhibitors of bacterial adhesion during urinary tract infection. Proc. Natl Acad. Sci. USA 115, E2819–E2828 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Maddirala, A. R. et al. Biphenyl Gal and GalNAc FmlH lectin antagonists of uropathogenic E. coli (UPEC): optimization through iterative rational drug design. J. Med. Chem. 62, 467–479 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stentebjerg-Olesen, B., Chakraborty, T. & Klemm, P. Type 1 fimbriation and phase switching in a natural Escherichia coli fimB null strain, Nissle 1917. J. Bacteriol. 181, 7470–7478 (1999).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dreux, N. et al. Point mutations in FimH adhesin of Crohn’s disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response. PLoS Pathog. 9, e1003141 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Iebba, V. et al. Microevolution in fimH gene of mucosa-associated Escherichia coli strains isolated from pediatric patients with inflammatory bowel disease. Infect. Immun. 80, 1408–1417 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schwartz, D. J. et al. Positively selected FimH residues enhance virulence during urinary tract infection by altering FimH conformation. Proc. Natl Acad. Sci. USA 110, 15530–15537 (2013).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reinisch, W. et al. Safety, pharmacokinetic, and pharmacodynamic study of sibofimloc, a novel FimH blocker in patients with active Crohn’s disease. J. Gastroenterol. Hepatol. 37, 832–840 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chevalier, G. et al. Blockage of bacterial FimH prevents mucosal inflammation associated with Crohn’s disease. Microbiome 9, 176 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reuter, C., Alzheimer, M., Walles, H. & Oelschlaeger, T. A. An adherent mucus layer attenuates the genotoxic effect of colibactin. Cell Microbiol. https://doi.org/10.1111/cmi.12812 (2018).

  • Zhao, Z., Xu, S., Zhang, W., Wu, D. & Yang, G. Probiotic Escherichia coli NISSLE 1917 for inflammatory bowel disease applications. Food Funct. 13, 5914–5924 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Olier, M. et al. Genotoxicity of Escherichia coli Nissle 1917 strain cannot be dissociated from its probiotic activity. Gut Microbes 3, 501–509 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Giaffer, M. H., Holdsworth, C. D. & Duerden, B. I. Virulence properties of Escherichia coli strains isolated from patients with inflammatory bowel disease. Gut 33, 646–650 (1992).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Darfeuille-Michaud, A. et al. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn’s disease. Gastroenterology 115, 1405–1413 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Harnack, C. et al. Short-term mucosal disruption enables colibactin-producing E. coli to cause long-term perturbation of colonic homeostasis. Gut Microbes 15, 2233689 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • van der Post, S. et al. Structural weakening of the colonic mucus barrier is an early event in ulcerative colitis pathogenesis. Gut 68, 2142–2151 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Desai, M. S. et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167, 1339–1353 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dalmasso, G. et al. Colibactin-producing Escherichia coli enhance resistance to chemotherapeutic drugs by promoting epithelial to mesenchymal transition and cancer stem cell emergence. Gut Microbes 16, 2310215 (2024).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • de Oliveira Alves, N. et al. The colibactin-producing Escherichia coli alters the tumor microenvironment to immunosuppressive lipid overload facilitating colorectal cancer progression and chemoresistance. Gut Microbes 16, 2320291 (2024).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Volpe, M. R. et al. A small molecule inhibitor prevents gut bacterial genotoxin production. Nat. Chem. Biol. 19, 159–167 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Blanco-Miguez, A. et al. Targeted depletion of pks+ bacteria from a fecal microbiota using specific antibodies. mSystems 8, e0007923 (2023).

    Article 
    PubMed 

    Google Scholar
     

  • Gencay, Y. E. et al. Engineered phage with antibacterial CRISPR-Cas selectively reduce E. coli burden in mice. Nat. Biotechnol. https://doi.org/10.1038/s41587-023-01759-y (2023).

  • Spaulding, C. N. et al. Selective depletion of uropathogenic E. coli from the gut by a FimH antagonist. Nature 546, 528–532 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Greene, S. E., Hibbing, M. E., Janetka, J., Chen, S. L. & Hultgren, S. J. Human urine decreases function and expression of type 1 pili in uropathogenic Escherichia coli. mBio 6, e00820 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640–6645 (2000).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ramesh, P., Kirov, A. B., Huels, D. J. & Medema, J. P. Isolation, propagation, and clonogenicity of intestinal stem cells. Methods Mol. Biol. 2002, 61–73 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ewels, P., Magnusson, M., Lundin, S. & Kaller, M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047–3048 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Andrews, S. FastQC: a quality control tool for high throughput sequence data (2010).

  • Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Danecek, P. et al. Twelve years of SAMtools and BCFtools. Gigascience 10, giab008 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liao, Y., Smyth, G. K. & Shi, W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 41, e108 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Love MI, A. S., Kim, V. & Huber, W. RNA-seq workflow: gene-level exploratory analysis and differential expression. F1000Research 4, 1070 (2016).

    Article 

    Google Scholar
     

  • Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Korotkevich, G. et al. Fast gene set enrichment analysis. Preprint at bioRxiv https://doi.org/10.1101/060012 (2019).

  • Stephens, M. False discovery rates: a new deal. Biostatistics 18, 275–294 (2017).

    MathSciNet 
    PubMed 

    Google Scholar
     

  • Hanzelmann, S., Castelo, R. & Guinney, J. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinform. 14, 7 (2013).

    Article 

    Google Scholar
     

  • Kolde, R. Pheatmap: pretty heatmaps (2012).

  • Thakur, S. D., Obradovic, M., Dillon, J. R., Ng, S. H. & Wilson, H. L. Development of flow cytometry based adherence assay for Neisseria gonorrhoeae using 5′-carboxyfluorosceinsuccidyl ester. BMC Microbiol. 19, 67 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Martin, H. M. et al. Enhanced Escherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterology 127, 80–93 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wirth, T. et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60, 1136–1151 (2006).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Vizcaino, M. I., Engel, P., Trautman, E. & Crawford, J. M. Comparative metabolomics and structural characterizations illuminate colibactin pathway-dependent small molecules. J. Am. Chem. Soc. 136, 9244–9247 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • RELATED ARTICLES

    Most Popular

    Recent Comments