Department of Biochemistry and Molecular Biology, Virginia Commonwealth University School of Medicine, Richmond, Virginia, USA.
Department of Microbiology and Immunology, Virginia Commonwealth University School of Medicine, Richmond, Virginia, USA.
FASEB J. 2023 Mar;37(3):e22799. doi: 10.1096/fj.202201821R.
Genome-wide association studies have linked the ORM (yeast)-like protein isoform 3 (ORMDL3) to asthma severity. Although ORMDL3 is a member of a family that negatively regulates serine palmitoyltransferase (SPT) and thus biosynthesis of sphingolipids, it is still unclear whether ORMDL3 and altered sphingolipid synthesis are causally related to non-Th2 severe asthma associated with a predominant neutrophil inflammation and high interleukin-17 (IL-17) levels. Here, we examined the effects of ORMDL3 overexpression in a preclinical mouse model of allergic lung inflammation that is predominantly neutrophilic and recapitulates many of the clinical features of severe human asthma. ORMDL3 overexpression reduced lung and circulating levels of dihydrosphingosine, the product of SPT. However, the most prominent effect on sphingolipid levels was reduction of circulating S1P. The LPS/OVA challenge increased markers of Th17 inflammation with a predominant infiltration of neutrophils into the lung. A significant decrease of neutrophil infiltration was observed in the Ormdl3 transgenic mice challenged with LPS/OVA compared to the wild type and concomitant decrease in IL-17, that plays a key role in the pathogenesis of neutrophilic asthma. LPS decreased survival of murine neutrophils, which was prevented by co-treatment with S1P. Moreover, S1P potentiated LPS-induced chemotaxis of neutrophil, suggesting that S1P can regulate neutrophil survival and recruitment following LPS airway inflammation. Our findings reveal a novel connection between ORMDL3 overexpression, circulating levels of S1P, IL-17 and neutrophil recruitment into the lung, and questions the potential involvement of ORMDL3 in the pathology, leading to development of severe neutrophilic asthma.
全基因组关联研究将酵母样蛋白同型 3(ORMDL3)与哮喘严重程度联系起来。尽管 ORMDL3 是负调控丝氨酸棕榈酰转移酶(SPT)从而影响鞘脂生物合成的家族成员,但 ORMDL3 和改变的鞘脂合成是否与非 Th2 严重哮喘相关的因果关系,其特征为中性粒细胞炎症和高水平白细胞介素-17(IL-17)仍不清楚。在这里,我们研究了 ORMDL3 过表达在以中性粒细胞为主的变应性肺炎症的临床前小鼠模型中的作用,该模型重现了许多严重人类哮喘的临床特征。ORMDL3 过表达降低了肺部和循环中二氢鞘氨醇的水平,这是 SPT 的产物。然而,对鞘脂水平最显著的影响是循环 S1P 的减少。LPS/OVA 挑战增加了 Th17 炎症的标志物,以中性粒细胞为主的浸润到肺部。与野生型相比,在 LPS/OVA 挑战的 Ormdl3 转基因小鼠中观察到中性粒细胞浸润的显著减少,同时 IL-17 减少,IL-17 在中性粒细胞性哮喘的发病机制中起关键作用。LPS 降低了小鼠中性粒细胞的存活率,而 S1P 共处理可预防这种降低。此外,S1P 增强了 LPS 诱导的中性粒细胞趋化作用,这表明 S1P 可以调节 LPS 气道炎症后的中性粒细胞存活和募集。我们的发现揭示了 ORMDL3 过表达、循环 S1P 水平、IL-17 和中性粒细胞募集到肺部之间的新联系,并质疑 ORMDL3 在导致严重中性粒细胞性哮喘的发病机制中的潜在作用。