Enteric glial cells favor accumulation of anti-inflammatory macrophages during the resolution of muscularis inflammation

Michelle Stakenborg, Saeed Abdurahiman, Veronica De Simone, Gera Goverse, Nathalie Stakenborg, Lies van Baarle, Qin Wu, Dimitri Pirottin, Jung-Seok Kim, Louise Chappell-Maor, Isabel Pintelon, Sofie Thys, Emilie Pollenus, Louis Boon, Philippe Van den Steen, Marlene Hao, Jo A Van Ginderachter, Guy E Boeckxstaens, Jean-Pierre Timmermans, Steffen JungThomas Marichal, Sales Ibiza*, Gianluca Matteoli*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

20 Citations (Scopus)

Abstract

Monocyte-derived macrophages (Mφs) are crucial regulators during muscularis inflammation. However, it is unclear which micro-environmental factors are responsible for monocyte recruitment and anti-inflammatory Mφ differentiation in this paradigm. Here, we investigate Mφ heterogeneity at different stages of muscularis inflammation and determine how environmental cues can attract and activate tissue-protective Mφs. Results showed that muscularis inflammation induced marked alterations in mononuclear phagocyte populations associated with a rapid infiltration of Ly6c+ monocytes that locally acquired unique transcriptional states. Trajectory inference analysis revealed two main pro-resolving Mφ subpopulations during the resolution of muscularis inflammation, i.e. Cd206+ MhcIIhi and Timp2+ MhcIIlo Mφs. Interestingly, we found that damage to the micro-environment upon muscularis inflammation resulted in EGC activation, which in turn stimulated monocyte infiltration and the consequent differentiation in anti-inflammatory CD206+ Mφs via CCL2 and CSF1, respectively. In addition, CSF1-CSF1R signaling was shown to be essential for the differentiation of monocytes into CD206+ Mφs and EGC proliferation during muscularis inflammation. Our study provides a comprehensive insight into pro-resolving Mφ differentiation and their regulators during muscularis inflammation. We deepened our understanding in the interaction between EGCs and Mφs, thereby highlighting pro-resolving Mφ differentiation as a potential novel therapeutic strategy for the treatment of intestinal inflammation.
Original languageEnglish
Number of pages13
JournalMucosal Immunology
DOIs
Publication statusPublished - 7 Sept 2022

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