Interleukin-6 is critical in the development of pulmonary vascular disease in <i>Gcn2-</i>deficient mice.

Schwiening, Max; Gao, Qingyue; Southwood, Mark; Crosby, Alexi; Moore, Stephen; Valer, Jose A; Veale, Niki; Dunmore, Benjamin J et al. · Proc Natl Acad Sci U S A · 2026

basic_science · Level V

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Abstract

Biallelic mutations in EIF2AK4, encoding Eukaryotic Translation Initiation Factor 2α kinase 4 or General Control Nonderepressible 2 (GCN2), cause pulmonary veno-occlusive disease (PVOD), a fatal form of pulmonary hypertension. The mechanisms linking GCN2 deficiency with pulmonary vascular pathology are poorly understood. To investigate this, we developed two mouse models: genetic ablation of <i>Gcn2</i>, to mirror <i>GCN2</i>-mutation positive PVOD, and a pharmacological model using mitomycin C, a drug which can cause PVOD as an idiosyncratic drug reaction. Both models were phenotyped, and lungs from wild-type and <i>Gcn2</i>-deficient mice were analyzed using single-cell RNA sequencing. We show that homozygous loss of <i>Gcn2</i> is sufficient to induce mild pulmonary hypertension in mice. Single-cell transcriptomic profiling identified adventitial fibroblasts as the cell population exhibiting the most <i>Gcn2</i>-dependent transcriptional changes. Pathway analysis revealed upregulation of inflammatory signaling in <i>Gcn2<sup>-/-</sup></i> adventitial fibroblasts. Consistent with this, we demonstrate a proinflammatory phenotype in <i>Gcn2<sup>-/-</sup></i> mouse fibroblasts and in <i>Gcn2<sup>-/-</sup></i> mice. Using a mitomycin C-induced murine model, genetic deletion of interleukin-6 (<i>Il6</i>) rescued the pulmonary vascular phenotype. Furthermore, chronic lipopolysaccharide exposure exaggerated pulmonary hypertension in <i>Gcn2<sup>-/-</sup></i> mice, and <i>Il6</i> ablation rescued both baseline and lipopolysaccharide-exacerbated disease. Pharmacological inhibition or genetic ablation of the Integrated Stress Response, which can be driven by GCN2-activation, phenocopies <i>Gcn2</i> deficiency. Therefore, we establish a regulatory effect of an intact GCN2-Integrated Stress Response on IL-6 signaling. Together, we show that interleukin-6 is a critical mediator of both <i>Gcn2</i> deficiency-associated and mitomycin C-triggered pulmonary vascular disease in mice and highlight IL-6-dependent pathways as potential therapeutic targets.