Gut microbial β-glucuronidases regulate host luminal proteases and are depleted in irritable bowel syndrome View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2022-04-28

AUTHORS

Adam L. Edwinson, Lu Yang, Stephanie Peters, Nikita Hanning, Patricio Jeraldo, Pratik Jagtap, Joshua B. Simpson, Tzu-Yi Yang, Praveen Kumar, Subina Mehta, Asha Nair, Margaret Breen-Lyles, Lakshmikanth Chikkamenahalli, Rondell P. Graham, Benedicte De Winter, Robin Patel, Surendra Dasari, Purna Kashyap, Timothy Griffin, Jun Chen, Gianrico Farrugia, Matthew R. Redinbo, Madhusudan Grover

ABSTRACT

Intestinal proteases mediate digestion and immune signalling, while increased gut proteolytic activity disrupts the intestinal barrier and generates visceral hypersensitivity, which is common in irritable bowel syndrome (IBS). However, the mechanisms controlling protease function are unclear. Here we show that members of the gut microbiota suppress intestinal proteolytic activity through production of unconjugated bilirubin. This occurs via microbial β-glucuronidase-mediated conversion of bilirubin conjugates. Metagenomic analysis of faecal samples from patients with post-infection IBS (n = 52) revealed an altered gut microbiota composition, in particular a reduction in Alistipes taxa, and high gut proteolytic activity driven by specific host serine proteases compared with controls. Germ-free mice showed 10-fold higher proteolytic activity compared with conventional mice. Colonization with microbiota samples from high proteolytic activity IBS patients failed to suppress proteolytic activity in germ-free mice, but suppression of proteolytic activity was achieved with colonization using microbiota from healthy donors. High proteolytic activity mice had higher intestinal permeability, a higher relative abundance of Bacteroides and a reduction in Alistipes taxa compared with low proteolytic activity mice. High proteolytic activity IBS patients had lower fecal β-glucuronidase activity and end-products of bilirubin deconjugation. Mice treated with unconjugated bilirubin and β-glucuronidase-overexpressing E. coli significantly reduced proteolytic activity, while inhibitors of microbial β-glucuronidases increased proteolytic activity. Together, these data define a disease-relevant mechanism of host–microbial interaction that maintains protease homoeostasis in the gut. More... »

PAGES

680-694

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  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1038/s41564-022-01103-1

    DOI

    http://dx.doi.org/10.1038/s41564-022-01103-1

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1147404773

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/35484230


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