Introduction: Granuloma formation is a central feature of sarcoidosis, marked by the organized accumulation and transformation of activated macrophages and T cells sustained by a proinflammatory cytokine milieu. Increasing evidence points to a multifactorial etiology involving genetic susceptibility, microbial agents, and environmental triggers. Indoleamine 2,3-dioxygenase 1 (IDO1) is an immunoregulatory enzyme predominantly expressed in antigen-presenting cells, that catalyzes the rate-limiting step of tryptophan catabolism along the kynurenine pathway, thereby modulating immune responses through metabolic control. By promoting local tryptophan depletion and accumulation of immunosuppressive metabolites, IDO1 contributes to the regulation of T cell proliferation, differentiation, and tolerance.
Objectives: This study aimed to determine whether IDO1 acts as an immunometabolic checkpoint, playing a role in the pathological mechanisms underlying granuloma formation in sarcoidosis.
Materials and Methods: To achieve this, we applied different experimental in vitro and in vivo models of granuloma formation using peripheral blood mononuclear cells (PBMCs) from sarcoidosis patients harboring loss-of-function genetic variants and gene-deleted mice in IDO1, respectively.
Results: Using a large genomics dataset, we revealed a correlation between the rs7820268 variant in IDO1 and the risk of sarcoidosis. This variant was correlated with distinct immunological profiles, influencing immune cell composition in baseline bronchoalveolar lavage samples, lung functional capacity, and ultimately, disease phenotype. PBMCs from risk genotype carriers exhibited an impaired response to IFN-γ stimulation characterized by reduced IDO1 transcript and protein expression, suggesting impaired IDO1-mediated immunoregulation. As a proxy for clinical observations, an in vitro model of granuloma formation demonstrated that risk carriers exhibit reduced hIDO1 expression accompanied by larger granuloma-like structures. Consistently, IDO1-deficient mice exhibited enhanced leukocyte recruitment and inflammation. Current work aims to define how IDO1 interacts with known molecular hallmarks of granulomatous inflammation.
Conclusions: Consistent findings across patient samples and cellular and in vivo models support a critical role for IDO1 in modulating granulomatous inflammation and disease progression in sarcoidosis.