Eden G TenBarge, Ashley D Wise, Morgan L Hetzel, Helene A Hoover, Helia Esfandiari, Bailey E Holder, Eva Belevska, Ellie C Mennen, Sarah R McDaniel, Nicole M Vaccaro, Courtney C Lucca, Jonathan M Williams, Jennifer Ferris, Timothy E Sparer, Leslie J Crofford, Jeffry D Bieber, Andrew J Monteith
Patients with systemic lupus erythematosus (SLE) are susceptible to bacterial infections, but the mechanisms remain unclear. We found that Staphylococcus aureus triggers mitochondria-dependent suicidal neutrophil extracellular trap (NET)osis through lactate sensing in healthy neutrophils, whereas this response is defective in SLE. Sustained Toll-like receptor (TLR) 7/9 signaling reduced mitochondrial lactate dehydrogenase B (LDHB), thereby impairing lactate sensing and suicidal NETosis. Instead, SLE neutrophils were biased toward vital NET release, a less bactericidal, type I interferon (IFN)-driven process initiated by staphylococcal pore-forming toxins and amplified by elevated systemic IFNα. In lupus-prone mice, combined hydroxychloroquine (HCQ) and interferon-alpha/beta receptor (IFNAR) blockade restored LDHB expression, rebalanced suicidal and vital NET responses, and improved bacterial clearance. Neutrophils from SLE patients showed similar defects that were reversed by HCQ and the IFNAR-blocking antibody anifrolumab. These findings define an immunometabolic checkpoint linking chronic autoimmune signaling to defective antibacterial defense in SLE and identify therapeutic routes to restore innate immunity.