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SIGNR1 promotes immune dysfunction in systemic candidiasis by modulating neutrophil lifespan via T cell-derived histones and G-CSF

Ioannou, M.; Hoving, D.; Aramburu, I. V.; De Vasconcelos, N. M.; Temkin, M. I.; Wang, Q.; Vernardis, S.; Demichev, V.; Tsourouktsoglou, T.-D.; Boeing, S.; Goldstone, R.; David, S.; Klaus Stahl, K.; Bode, C.; Ralser, M.; Papagiannopoulos, V.

2021-08-09 immunology
10.1101/2021.08.09.455510 bioRxiv
Show abstract

The mechanisms regulating immune dysfunction during sepsis are poorly understood. Here, we show that neutrophil-derived myeloperoxidase delays the onset of immune dysfunction during systemic candidiasis by controlling microbes captured by splenic marginal zone (MZ) macrophages. In contrast, SIGNR1-mediated microbe capture accelerates MZ colonization and immune dysfunction by triggering T cell death, T cell-dependent chromatin release and the synergistic induction of G-CSF by histones and fungi. Histones and G-CSF promote the prevalence of immature Ly6Glow neutrophils with defective oxidative burst, by selectively shortening the lifespan of mature Ly6Ghigh neutrophils. Consistently, T cell deficiency, or blocking SIGNR1, G-CSF or histones delayed neutrophil dysfunction. Furthermore, histones and G-CSF in the plasma of sepsis patients, shortened neutrophil lifespan and correlated with neutrophil mortality markers associated with a poor prognosis. Hence, the compromise of internal antimicrobial barrier sites drives neutrophil dysfunction by selectively modulating neutrophil lifespan via pathogenic T cell death, extracellular histones, and G-CSF.

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