Progesterone attenuates Th17-cell pathogenicity in autoimmune uveitis via Id2/Pim1 axis

J Neuroinflammation. 2023 Jun 21;20(1):144. doi: 10.1186/s12974-023-02829-3.

Abstract

Background: Autoimmune uveitis (AU) is the most common ophthalmic autoimmune disease (AD) and is characterized by a complex etiology, high morbidity, and high rate of blindness. AU remission has been observed in pregnant female patients. However, the effects of progesterone (PRG), a critical hormone for reproduction, on the treatment of AU and the regulatory mechanisms remain unclear.

Methods: To this end, we established experimental autoimmune uveitis (EAU) animal models and constructed a high-dimensional immune atlas of EAU-model mice undergoing PRG treatment to explore the underlying therapeutic mechanisms of PRG using single-cell RNA sequencing.

Results: We found that PRG ameliorated retinal lesions and inflammatory infiltration in EAU-model mice. Further single-cell analysis indicated that PRG reversed the EAU-induced expression of inflammatory genes (AP-1 family, S100a family, and Cxcr4) and pathological processes related to inflammatory cell migration, activation, and differentiation. Notably, PRG was found to regulate the Th17/Treg imbalance by increasing the reduced regulatory functional mediators of Tregs and diminishing the overactivation of pathological Th17 cells. Moreover, the Id2/Pim1 axis, IL-23/Th17/GM-CSF signaling, and enhanced Th17 pathogenicity during EAU were reversed by PRG treatment, resulting in the alleviation of EAU inflammation and treatment of AD.

Conclusions: Our study provides a comprehensive single-cell map of the immunomodulatory effects of PRG therapy on EAU and elaborates on the possible therapeutic mechanisms, providing novel insights into its application for treating autoimmune diseases.

Keywords: Autoimmune uveitis; Id2; Progesterone; Single-cell RNA sequencing; Th17 cells; Treg.

MeSH terms

  • Animals
  • Autoimmune Diseases*
  • Disease Models, Animal
  • Female
  • Inflammation
  • Mice
  • Mice, Inbred C57BL
  • Progesterone / pharmacology
  • Progesterone / therapeutic use
  • Th17 Cells
  • Uveitis*
  • Virulence

Substances

  • Progesterone