Preclinical and clinical evidence of the association of colibactin-producing Escherichia coli with anxiety and depression in colon cancer
2024
Rondepierre, Fabien | Meynier, Maëva | Gagniere, Johan | Deneuvy, Vincent | Deneuvy, Anissa | Roche, Gwenaelle | Baudu, Elodie | Pereira, Bruno | Bonnet, Richard | Barnich, Nicolas | Carvalho, Frédéric Antonio | Pezet, Denis | Bonnet, Mathilde | Jalenques, Isabelle | Service Psychiatrie Adulte [CHU Clermont-Ferrand] ; CHU Gabriel Montpied [Clermont-Ferrand] ; CHU Clermont-Ferrand-CHU Clermont-Ferrand-Pôle Psychiatrie Enfant-Adulte [CHU Clermont-Ferrand] ; CHU Clermont-Ferrand-CHU Gabriel Montpied [Clermont-Ferrand] ; CHU Clermont-Ferrand | Microbes, Intestin, Inflammation et Susceptibilité de l'Hôte (M2iSH) ; Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre de Recherche en Nutrition Humaine d'Auvergne (CRNH d'Auvergne)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Clermont Auvergne (UCA) | Neuro-Dol (Neuro-Dol) ; Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Clermont Auvergne (UCA) | Service Chirurgie Digestive et Hépatobiliaire [CHU Clermont-Ferrand] ; CHU Estaing [Clermont-Ferrand] ; CHU Clermont-Ferrand-CHU Clermont-Ferrand-Pôle Spécialités médicales et chirurgicales [CHU Clermont-Ferrand] ; CHU Clermont-Ferrand | Service Biostatistiques, Télématiques, Traitement de l’image [CHU Clermont-Ferrand] ; CHU Gabriel Montpied [Clermont-Ferrand] ; CHU Clermont-Ferrand-CHU Clermont-Ferrand-Pôle Santé Publique [CHU Clermont-Ferrand] ; CHU Gabriel Montpied [Clermont-Ferrand] ; CHU Clermont-Ferrand-CHU Clermont-Ferrand | Service Bactériologie [CHU Clermont-Ferrand] ; CHU Gabriel Montpied [Clermont-Ferrand] ; CHU Clermont-Ferrand-CHU Clermont-Ferrand-Pôle Biologie médicale et Anatomie pathologique [CHU Clermont-Ferrand] ; CHU Gabriel Montpied [Clermont-Ferrand] ; CHU Clermont-Ferrand-CHU Clermont-Ferrand | Institut Pascal (IP) ; Centre National de la Recherche Scientifique (CNRS)-Université Clermont Auvergne (UCA)-Institut national polytechnique Clermont Auvergne (INP Clermont Auvergne) ; Université Clermont Auvergne (UCA)-Université Clermont Auvergne (UCA)
International audience
Afficher plus [+] Moins [-]anglais. BACKGROUND The association between the intestinal microbiota and psychiatric disorders is becoming increasingly apparent. The gut microbiota contributes to colorectal carcinogenesis (CRC), as demonstrated with colibactin-producing Escherichia coli (CoPEC). AIM To evaluate the association between CoPEC prevalence and anxiety- and depressive-like behaviors with both preclinical and clinical approaches. METHODS Patients followed after a CRC surgery and for whom the prevalence of CoPEC has been investigated underwent a psychiatric interview. Results were compared according to the CoPEC colonization. In parallel C57BL6/J wild type mice and mice with a CRC susceptibility were chronically infected with a CoPEC strain. Their behavior was assessed using the Elevated Plus Maze test, the Forced Swimming Test and the Behavior recognition system PhenoTyper®. RESULTS In a limited cohort, all patients with CoPEC colonization presented with psychiatric disorders several years before cancer diagnosis, whereas only one patient (17%) without CoPEC did. This result was confirmed in C57BL6/J wild-type mice and in a CRC susceptibility mouse model (adenomatous polyposis colimultiple intestinal neoplasia/+). Mice exhibited a significant increase in anxiety- and depressive-like behaviors after chronic infection with a CoPEC strain. CONCLUSION This finding provides the first evidence that CoPEC infection can induce microbiota-gut-brain axis disturbances in addition to its procarcinogenic properties.
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