Local immune response to food antigens drives meal-induced abdominal pain

Javier Aguilera-Lizarraga, Morgane V. Florens, Maria Francesca Viola, Piyush Jain, Lisse Decraecker, Iris Appeltans, Maria Cuende-Estevez, Naomi Fabre, Kim Van Beek, Eluisa Perna, Dafne Balemans, Nathalie Stakenborg, Stavroula Theofanous, Goele Bosmans, Stéphanie U. Mondelaers, Gianluca Matteoli, Sales Ibiza Martínez, Cintya Lopez-Lopez, Josue Jaramillo-Polanco, Karel Talavera, Yeranddy A. Alpizar, Thorsten B. Feyerabend, Hans-Reimer Rodewald, Ricard Farre, Frank A. Redegeld, Jiyeon Si, Jeroen Raes, Christine Breynaert, Rik Schrijvers, Cédric Bosteels, Bart N. Lambrecht, Scott D. Boyd, Ramona A. Hoh, Deirdre Cabooter, Maxim Nelis, Patrick Augustijns, Sven Hendrix, Jessica Strid, Raf Bisschops, David E. Reed, Stephen J. Vanner, Alexandre Denadai-Souza, Mira M. Wouters and Guy E. Boeckxstaens ()
Additional contact information
Javier Aguilera-Lizarraga: Metabolism and Ageing
Morgane V. Florens: Metabolism and Ageing
Maria Francesca Viola: Metabolism and Ageing
Piyush Jain: Metabolism and Ageing
Lisse Decraecker: Metabolism and Ageing
Iris Appeltans: Metabolism and Ageing
Maria Cuende-Estevez: Metabolism and Ageing
Naomi Fabre: Metabolism and Ageing
Kim Van Beek: Metabolism and Ageing
Eluisa Perna: Metabolism and Ageing
Dafne Balemans: Metabolism and Ageing
Nathalie Stakenborg: Metabolism and Ageing
Stavroula Theofanous: Metabolism and Ageing
Goele Bosmans: Metabolism and Ageing
Stéphanie U. Mondelaers: Metabolism and Ageing
Gianluca Matteoli: Metabolism and Ageing
Sales Ibiza Martínez: Metabolism and Ageing
Cintya Lopez-Lopez: Gastrointestinal Diseases Research Unit, Queen’s University
Josue Jaramillo-Polanco: Gastrointestinal Diseases Research Unit, Queen’s University
Karel Talavera: Laboratory for Ion Channel Research, VIB Center for Brain and Disease Research, KU Leuven Department of Cellular and Molecular Medicine
Yeranddy A. Alpizar: Hasselt University
Thorsten B. Feyerabend: German Cancer Research Center
Hans-Reimer Rodewald: German Cancer Research Center
Ricard Farre: Metabolism and Ageing
Frank A. Redegeld: Utrecht University
Jiyeon Si: Rega Institute
Jeroen Raes: Rega Institute
Christine Breynaert: Immunology and Transplantation
Rik Schrijvers: Immunology and Transplantation
Cédric Bosteels: Laboratory of Immunoregulation, VIB Center for Inflammation Research
Bart N. Lambrecht: Laboratory of Immunoregulation, VIB Center for Inflammation Research
Scott D. Boyd: Stanford University School of Medicine
Ramona A. Hoh: Stanford University School of Medicine
Deirdre Cabooter: KU Leuven Department of Pharmaceutical and Pharmacological Sciences
Maxim Nelis: KU Leuven Department of Pharmaceutical and Pharmacological Sciences
Patrick Augustijns: KU Leuven Department of Pharmaceutical and Pharmacological Sciences
Sven Hendrix: Hasselt University
Jessica Strid: Imperial College London
Raf Bisschops: Metabolism and Ageing
David E. Reed: Gastrointestinal Diseases Research Unit, Queen’s University
Stephen J. Vanner: Gastrointestinal Diseases Research Unit, Queen’s University
Alexandre Denadai-Souza: Metabolism and Ageing
Mira M. Wouters: Metabolism and Ageing
Guy E. Boeckxstaens: Metabolism and Ageing

Nature, 2021, vol. 590, issue 7844, 151-156

Abstract: Abstract Up to 20% of people worldwide develop gastrointestinal symptoms following a meal1, leading to decreased quality of life, substantial morbidity and high medical costs. Although the interest of both the scientific and lay communities in this issue has increased markedly in recent years, with the worldwide introduction of gluten-free and other diets, the underlying mechanisms of food-induced abdominal complaints remain largely unknown. Here we show that a bacterial infection and bacterial toxins can trigger an immune response that leads to the production of dietary-antigen-specific IgE antibodies in mice, which are limited to the intestine. Following subsequent oral ingestion of the respective dietary antigen, an IgE- and mast-cell-dependent mechanism induced increased visceral pain. This aberrant pain signalling resulted from histamine receptor H1-mediated sensitization of visceral afferents. Moreover, injection of food antigens (gluten, wheat, soy and milk) into the rectosigmoid mucosa of patients with irritable bowel syndrome induced local oedema and mast cell activation. Our results identify and characterize a peripheral mechanism that underlies food-induced abdominal pain, thereby creating new possibilities for the treatment of irritable bowel syndrome and related abdominal pain disorders.

Date: 2021
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DOI: 10.1038/s41586-020-03118-2

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