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Objective  The opportunistic pathogen  Streptococcus gallolyticus  is one of the few intestinal bacteria that has been consistently linked to colorectal cancer (CRC). This study aimed to identify novel  S. gallolyticus -induced pathways in colon epithelial cells that could further explain how  S. gallolyticus  contributes to CRC development.    Design and Results  Transcription profiling of  in vitro  cultured CRC cells that were exposed to  S. gallolyticus  revealed the specific induction of oxidoreductase pathways. Most prominently,  CYP1A  and  ALDH1  genes that encode phase I biotransformation enzymes were responsible for the detoxification or bio-activation of toxic compounds. A common feature is that these enzymes are induced through the Aryl hydrocarbon receptor (AhR). Using the specific inhibitor CH223191, we showed that the induction of  CYP1A  was dependent on the AhR both  in vitro  using multiple CRC cell lines as  in vivo  using wild-type C57bl6 mice colonized with  S. gallolyticus . Furthermore, we showed that CYP1 could also be induced by other intestinal bacteria and that a yet unidentified diffusible factor from the  S. galloltyicus  secretome (SGS) induces CYP1A enzyme activity in an AhR-dependent manner. Importantly, priming CRC cells with SGS increased the DNA damaging effect of the polycyclic aromatic hydrocarbon 3-methylcholanthrene.    Conclusion  This study shows that gut bacteria have the potential to modulate the expression of biotransformation pathways in colonic epithelial cells in an AhR-dependent manner. This offers a novel theory on the contribution of intestinal bacteria to the etiology of CRC by modifying the capacity of intestinal epithelial or (pre-)cancerous cells to (de)toxify dietary components, which could alter intestinal susceptibility to DNA damaging events.

frontiers in cellular and infection microbiology

Streptococcus gallolyticus Increases Expression and Activity of Aryl Hydrocarbon Receptor-Dependent CYP1 Biotransformation Capacity in Colorectal Epithelial Cells