Article

GPR84 signaling promotes intestinal mucosal inflammation via enhancing NLRP3 inflammasome activation in macrophages

Qing Zhang1,2, Lin-hai Chen1, Hui Yang1, You-chen Fang1, Si-wei Wang1,3, Min Wang1, Qian-ting Yuan1, Wei Wu4, Yang-ming Zhang5, Zhan-ju Liu4, Fa-jun Nan1,2,6, Xin Xie1,2,3
1 State Key Laboratory of Drug Research, The National Center for Drug Screening, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China
2 School of Pharmaceutical Science and Technology, Hangzhou Institute for Advanced Study, University of Chinese Academy of Sciences, Hangzhou 310024, China
3 University of Chinese Academy of Sciences, Beijing 100049, China
4 Department of Gastroenterology, The Shanghai Tenth People’s Hospital, Tongji University, Shanghai 200072, China
5 Burgeon Therapeutics Co., Ltd, Shanghai 201203, China
6 Yantai Key Laboratory of Nanomedicine and Advanced Preparations, Yantai Institute of Materia Medica, Yantai 264000, China
Correspondence to: Zhan-ju Liu: liuzhanju88@126.com, Fa-jun Nan: fjnan@simm.ac.cn, Xin Xie: xxie@simm.ac.cn,
DOI: 10.1038/s41401-021-00825-y
Received: 13 July 2021
Accepted: 16 November 2021
Advance online: 15 December 2021

Abstract

The putative medium-chain free fatty acid receptor GPR84 is a G protein-coupled receptor primarily expressed in myeloid cells that constitute the innate immune system, including neutrophils, monocytes, and macrophages in the periphery and microglia in the brain. The fact that GPR84 expression in leukocytes is remarkably increased under acute inflammatory stimuli such as lipopolysaccharide (LPS) and TNFα suggests that it may play a role in the development of inflammatory and fibrotic diseases. Here we demonstrate that GPR84 is highly upregulated in inflamed colon tissues of active ulcerative colitis (UC) patients and dextran sulfate sodium (DSS)-induced colitis mice. Infiltrating GPR84+ macrophages are significantly increased in the colonic mucosa of both the UC patients and the mice with colitis. Consistently, GPR84−/− mice are resistant to the development of colitis induced by DSS. GPR84 activation imposes pro-inflammatory properties in colonic macrophages through enhancing NLRP3 inflammasome activation, while the loss of GPR84 prevents the M1 polarization and properties of proinflammatory macrophages. CLH536, a novel GPR84 antagonist discovered by us, suppresses colitis by reducing the polarization and function of pro-inflammatory macrophages. These results define a unique role of GPR84 in innate immune cells and intestinal inflammation, and suggest that GPR84 may serve as a potential drug target for the treatment of UC.
Keywords: GPR84; medium chain fatty acid receptor; GPCR; inflammatory bowel diseases; ulcerative colitis; NLRP3 inflammasome; macrophages

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