Aging and Critical Care Research Laboratory, University of Kentucky, Lexington, Kentucky, USA.
Department of Surgery, University of Kentucky, Lexington, Kentucky, USA.
J Cell Physiol. 2022 Jan;237(1):706-719. doi: 10.1002/jcp.30551. Epub 2021 Aug 9.
Elevated plasma levels of plasminogen activator inhibitor-1 (PAI-1) are documented in patients with sepsis and levels positively correlate with disease severity and mortality. Our previous work demonstrated that visceral adipose tissues (VAT) are a major source of PAI-1, especially in the aged (murine endotoxemia), that circulating PAI-1 protein levels match the trajectory of PAI-1 transcript levels in VAT (clinical sepsis), and that PAI-1 in both VAT and plasma are positively associated with acute kidney injury (AKI) in septic patients. In the current study utilizing preclinical sepsis models, PAI-1 tissue distribution was examined and cellular sources, as well as mechanisms mediating PAI-1 induction in VAT, were identified. In aged mice with sepsis, PAI-1 gene expression was significantly higher in VAT than in other major organs. VAT PAI-1 gene expression correlated with PAI-1 protein levels in both VAT and plasma. Moreover, VAT and plasma levels of PAI-1 were positively associated with AKI markers, modeling our previous clinical data. Using explant cultures of VAT, we determined that PAI-1 is secreted robustly in response to recombinant transforming growth factor β (TGFβ) and tumor necrosis factor α (TNFα) treatment; however, neutralization was effective only for TNFα indicating that TGFβ is not an endogenous modulator of PAI-1. Within VAT, TNFα was localized to neutrophils and macrophages. PAI-1 protein levels were fourfold higher in stromal vascular fraction (SVF) cells compared with mature adipocytes, and among SVF cells, both immune and nonimmune compartments expressed PAI-1 in a similar fashion. PAI-1 was localized predominantly to macrophages within the immune compartment and preadipocytes and endothelial cells within the nonimmune compartment. Collectively, these results indicate that induction and secretion of PAI-1 from VAT is facilitated by a complex interaction among immune and nonimmune cells. As circulating PAI-1 contributes to AKI in sepsis, understanding PAI-1 regulation in VAT could yield novel strategies for reducing systemic consequences of PAI-1 overproduction.
血浆纤溶酶原激活物抑制剂-1(PAI-1)水平升高已在脓毒症患者中得到证实,且其水平与疾病严重程度和死亡率呈正相关。我们之前的工作表明,内脏脂肪组织(VAT)是 PAI-1 的主要来源,尤其是在老年(小鼠内毒素血症)中,循环 PAI-1 蛋白水平与 VAT 中 PAI-1 转录水平的轨迹相匹配(临床脓毒症),并且 VAT 和血浆中的 PAI-1 与脓毒症患者的急性肾损伤(AKI)呈正相关。在本研究中,我们利用临床前脓毒症模型,检查了 PAI-1 的组织分布,并确定了其细胞来源以及介导 VAT 中 PAI-1 诱导的机制。在脓毒症老年小鼠中,VAT 中的 PAI-1 基因表达显著高于其他主要器官。VAT 的 PAI-1 基因表达与 VAT 和血浆中的 PAI-1 蛋白水平相关。此外,VAT 和血浆中的 PAI-1 水平与 AKI 标志物呈正相关,这与我们之前的临床数据模型一致。使用 VAT 的离体培养物,我们确定 PAI-1 可强烈响应重组转化生长因子 β(TGFβ)和肿瘤坏死因子 α(TNFα)的治疗而分泌;然而,中和仅对 TNFα 有效,表明 TGFβ 不是 PAI-1 的内源性调节剂。在 VAT 内,TNFα 定位于中性粒细胞和巨噬细胞。与成熟脂肪细胞相比,基质血管部分(SVF)细胞中的 PAI-1 蛋白水平高 4 倍,在 SVF 细胞中,免疫和非免疫细胞均以相似的方式表达 PAI-1。PAI-1 主要定位于免疫细胞中的巨噬细胞以及非免疫细胞中的前脂肪细胞和内皮细胞。总之,这些结果表明,VAT 中 PAI-1 的诱导和分泌是由免疫和非免疫细胞之间的复杂相互作用促进的。由于循环 PAI-1 导致脓毒症中的 AKI,因此了解 VAT 中 PAI-1 的调节可能会产生减少 PAI-1 过度产生对全身影响的新策略。