Active thrombin produced by the intestinal epithelium controls mucosal biofilms

Jean-Paul Motta, Alexandre Denadai-Souza, David Sagnat, Laura Guiraud, Anissa Edir, Chrystelle Bonnart, Mireille Sebbag, Perrine Rousset, Ariane Lapeyre, Carine Seguy, Noa Mathurine-Thomas, Heather J. Galipeau, Delphine Bonnet, Laurent Alric, Andre G. Buret, John L. Wallace, Antoine Dufour, Elena F. Verdu, Morley D. Hollenberg, Eric Oswald, Matteo Serino, Celine Deraison and Nathalie Vergnolle ()
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Jean-Paul Motta: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Alexandre Denadai-Souza: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
David Sagnat: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Laura Guiraud: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Anissa Edir: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Chrystelle Bonnart: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Mireille Sebbag: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Perrine Rousset: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Ariane Lapeyre: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Carine Seguy: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Noa Mathurine-Thomas: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Heather J. Galipeau: McMaster University
Delphine Bonnet: Department of Internal Medicine and Digestive Diseases
Laurent Alric: Department of Internal Medicine and Digestive Diseases
Andre G. Buret: University of Calgary
John L. Wallace: University of Calgary Cumming School of Medicine
Antoine Dufour: University of Calgary Cumming School of Medicine
Elena F. Verdu: McMaster University
Morley D. Hollenberg: University of Calgary Cumming School of Medicine
Eric Oswald: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Matteo Serino: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Celine Deraison: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039
Nathalie Vergnolle: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, U1220, CHU Purpan, CS60039

Nature Communications, 2019, vol. 10, issue 1, 1-12

Abstract: Abstract Proteolytic homeostasis is important at mucosal surfaces, but its actors and their precise role in physiology are poorly understood. Here we report that healthy human and mouse colon epithelia are a major source of active thrombin. We show that mucosal thrombin is directly regulated by the presence of commensal microbiota. Specific inhibition of luminal thrombin activity causes macroscopic and microscopic damage as well as transcriptomic alterations of genes involved in host-microbiota interactions. Further, luminal thrombin inhibition impairs the spatial segregation of microbiota biofilms, allowing bacteria to invade the mucus layer and to translocate across the epithelium. Thrombin cleaves the biofilm matrix of reconstituted mucosa-associated human microbiota. Our results indicate that thrombin constrains biofilms at the intestinal mucosa. Further work is needed to test whether thrombin plays similar roles in other mucosal surfaces, given that lung, bladder and skin epithelia also express thrombin.

Date: 2019
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DOI: 10.1038/s41467-019-11140-w

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