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Intestinal development and homeostasis require activation and apoptosis of diet-reactive T cells

Journal article
Authors A. Visekruna
S. Hartmann
Y. R. Sillke
R. Glauben
F. Fischer
H. Raifer
H. Mollenkopf
W. Bertrams
B. Schmeck
M. Klein
A. Pagenstecher
M. Lohoff
R. Jacob
O. Pabst
Paul William Bland
M. Luu
R. Romero
B. Siegmund
K. Rajalingam
U. Steinhoff
Published in The Journal of clinical investigation
Volume 129
Issue 5
Pages 1972–1983
ISSN 1558-8238
Publication year 2019
Published at Institute of Biomedicine, Department of Microbiology and Immunology
Pages 1972–1983
Language en
Links dx.doi.org/10.1172/JCI98929
Keywords Gastroenterology, Homeostasis, Immunology, Inflammatory bowel disease, T cells
Subject categories Immunology in the medical area, Gastroenterology and Hepatology

Abstract

The impact of food antigens on intestinal homeostasis and immune function is poorly understood. Here, we explored the impact of dietary antigens on the phenotype and fate of intestinal T cells. Physiological uptake of dietary proteins generated a highly activated CD44+Helios+CD4+ T cell population predominantly in Peyer patches. These cells are distinct from regulatory T cells and develop independently of the microbiota. Alimentation with a protein-free, elemental diet led to an atrophic small intestine with low numbers of activated T cells, including Tfh cells and decreased amounts of intestinal IgA and IL-10. Food-activated CD44+Helios+CD4+ T cells in the Peyer patches are controlled by the immune checkpoint molecule PD-1. Blocking the PD-1 pathway rescued these T cells from apoptosis and triggered proinflammatory cytokine production, which in IL-10-deficient mice was associated with intestinal inflammation. In support of these findings, our study of patients with Crohn's disease revealed significantly reduced frequencies of apoptotic CD4+ T cells in Peyer patches as compared with healthy controls. These results suggest that apoptosis of diet-activated T cells is a hallmark of the healthy intestine.

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