Role of Glutaminase 2 in Promoting CD4+ T Cell Production of Interleukin‐2 by Supporting Antioxidant Defense in Systemic Lupus Erythematosus

OBJECTIVE Glutaminase (GLS) isoenzymes GLS1 and GLS2 catalyze the first step of glutaminolysis. GLS1 is requisite for Th17 differentiation and its inhibition suppresses autoimmune disease in animals but the function of GLS2 is not known. The aim of this study was to investigate the role of GLS2 in CD4+ T cell function and systemic lupus erythematosus (SLE) pathogenesis. METHODS We measured reactive oxygen species (ROS) levels, lipid peroxidation, and mitochondrial mass/polarization by flow cytometry, IL-2 production by dual luciferase assay, and CpG-DNA methylation of the Il-2 gene by real-time PCR. The impact of the overexpression of wild type GLS1 and GLS2, or mutated GLS2 at the PDZ domain-binding motif in CD4+ T cells was examined. Furthermore, GLS2 expression in CD4+ T cells from lupus-prone mice and patients with SLE was analyzed by Western blotting. RESULTS GLS2, but not GLS1, reduced ROS levels, lipid peroxidation and restored mitochondrial function in T cells. GLS2 promoted IL-2 production through the demethylation of the Il-2 promoter. Mutation of the PDZ domain-binding motif abated the ability of GLS2 to regulate IL-2 and ROS levels. In lupus-prone mice and patients with SLE, the expression of GLS2 was decreased in CD4+ T cells. Finally, GLS2 overexpression corrected ROS levels and restored IL-2 production by lupus CD4+ cells. CONCLUSION Our findings suggest that GLS2 has a crucial role in IL-2 production by CD4+ T cells by supporting the antioxidant defense and offer a new approach to correct IL-2 production by T cell in SLE.