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ZEB1 promotes pathogenic Th1 and Th17 cell differentiation in multiple sclerosis

Published:24 August 2021 DOI: 10.1016/j.celrep.2021.109602 PMID: 34433042
Yuan Qian,?Gabriel Arellano,?Igal Ifergan,?Jean Lin,?Caroline Snowden,?Taehyeung Kim,?Jane Joy Thomas,?Calvin Law,?Tianxia Guan,?Roumen D Balabanov,?Susan M Kaech,?Stephen D Miller,?Jaehyuk Choi

Abstract

Inappropriate CD4+ T helper (Th) differentiation can compromise host immunity or promote autoimmune disease. To identify disease-relevant regulators of T?cell fate, we examined mutations that modify risk for multiple sclerosis (MS), a canonical organ-specific autoimmune disease. This analysis identified a role for Zinc finger E-box-binding homeobox (ZEB1). Deletion of ZEB1 protects against experimental autoimmune encephalitis (EAE), a mouse model of multiple sclerosis (MS). Mechanistically, ZEB1 in CD4+ T?cells is required for pathogenic Th1 and Th17 differentiation. Genomic analyses of paired human and mouse expression data elucidated an unexpected role for ZEB1 in JAK-STAT signaling. ZEB1 inhibits miR-101-3p that represses JAK2 expression, STAT3/STAT4 phosphorylation, and subsequent expression of interleukin-17 (IL-17) and interferon gamma (IFN-γ). Underscoring its clinical relevance, ZEB1 and JAK2 downregulation decreases pathogenic cytokines expression in T?cells from MS patients. Moreover, a Food and Drug Administration (FDA)-approved JAK2 inhibitor is effective in EAE. Collectively, these findings identify a conserved, potentially targetable mechanism regulating disease-relevant inflammation.

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