IL-22BP Modulates Injury in Acute Pancreatitis but Delays Tissue Recovery in Chronic PancreatitisSummary

Background & Aims: In acute pancreatitis, interleukin (IL)-22 signaling is increased, whereas overall expression of the cytokine paradoxically drops, suggesting an additional level of control. Here, we investigate the regulation of IL-22 signaling by its soluble neutralizing receptor interle...

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Bibliographic Details
Main Authors: Lei Sun, Andrew G. Spiteri, Brian D. Griffith, Yaqing Zhang, Marina Pasca Di Magliano, Alberto C. Olivei, Jake J. McGue, Jacob Edwards, Timothy L. Frankel
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Cellular and Molecular Gastroenterology and Hepatology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352345X2500061X
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Summary:Background & Aims: In acute pancreatitis, interleukin (IL)-22 signaling is increased, whereas overall expression of the cytokine paradoxically drops, suggesting an additional level of control. Here, we investigate the regulation of IL-22 signaling by its soluble neutralizing receptor interleukin-22 binding protein (IL-22BP) in the context of both acute and chronic pancreatitis. Methods: Cerulein was used to induce acute and chronic pancreatitis in both wild-type mice and IL-22BP knockout mice. Histology, multiplex immunofluorescence and flow cytometry were performed to compare differences in tissue injury, recovery, fibrosis, and inflammation at various times of recovery. Results: Loss of IL-22BP resulted in increased canonical IL-22 signaling and the expression of the anti-autophagy protein Bcl-XL. This was associated with decreased severity of acute pancreatitis, as evidenced by lower serum amylase and tissue injury. In chronic pancreatitis, IL-22BP expression was induced in the inflammatory and recovery phases and genetic deletion resulted in unchecked IL-22 signaling, as demonstrated by persistent p-Stat3 signaling and proliferation of both epithelial cells and fibroblasts. Loss of IL-22BP increased myeloid cell infiltration, which persisted throughout recovery. Mechanistically, IL-22 activity forced persistent acinar to ductal metaplasia and delayed tissue recovery. Conclusions: IL-22BP plays an important role in modulating IL-22 activity during tissue injury and recovery after pancreatitis. Loss of IL-22BP attenuated acute pancreatitis but promoted chronic fibrosis and inflammation through uncontrolled IL-22 signaling and subsequent deleterious effects on epithelial cells, fibroblasts, and immune infiltration.
ISSN:2352-345X