Laboratory for Fetal and Regenerative Biology, Department of Surgery, University of Colorado Denver-Anschutz Medical Campus and Children's Hospital Colorado, Aurora, CO 80045, USA.
Int J Mol Sci. 2020 May 8;21(9):3328. doi: 10.3390/ijms21093328.
A central feature of diabetic wounds is the persistence of chronic inflammation, which is partly due to the prolonged presence of pro-inflammatory (M1) macrophages in diabetic wounds. Persistence of the M1 macrophage phenotype and failure to transition to the regenerative or pro-remodeling (M2) macrophage phenotype plays an indispensable role in diabetic wound impairment; however, the mechanism underlying this relationship remains unclear. Recently, microRNAs have been shown to provide an additional layer of regulation of gene expression. In particular, microRNA-21 (miR-21) is essential for an inflammatory immune response. We hypothesize that miR-21 plays a role in regulating inflammation by promoting M1 macrophage polarization and the production of reactive oxygen species (ROS). To test our hypothesis, we employed an in vivo mouse skin wound model in conjunction with an in vitro mouse model to assess miR-21 expression and macrophage polarization. First, we found that miR-21 exhibits a distinct expression pattern in each phase of healing in diabetic wounds. MiR-21 abundance was higher during early and late phases of wound repair in diabetic wounds, while it was significantly lower in the middle phase of wounding (at days 3 and 7 following wounding). In macrophage cells, M1 polarized macrophages exhibited an upregulation of miR-21, as well as the M1 and pro-inflammatory markers IL-1b, TNFa, iNos, IL-6, and IL-8. Overexpression of miR-21 in macrophage cells resulted in an upregulation of miR-21 and also increased expression of the M1 markers IL-1b, TNFa, iNos, and IL-6. Furthermore, hyperglycemia induced NOX2 expression and ROS production through the HG/miR-21/PI3K/NOX2/ROS signaling cascade. These findings provide evidence that miR-21 is involved in the regulation of inflammation. Dysregulation of miR-21 may explain the abnormal inflammation and persistent M1 macrophage polarization seen in diabetic wounds.
糖尿病伤口的一个主要特征是慢性炎症的持续存在,这在一定程度上是由于促炎(M1)巨噬细胞在糖尿病伤口中的长期存在。M1 巨噬细胞表型的持续存在和向再生或促重塑(M2)巨噬细胞表型的转变失败在糖尿病伤口损伤中起着不可或缺的作用;然而,这种关系的机制尚不清楚。最近,microRNAs 被证明提供了基因表达的额外调节层。特别是,microRNA-21 (miR-21) 对炎症免疫反应至关重要。我们假设 miR-21 通过促进 M1 巨噬细胞极化和活性氧物质 (ROS) 的产生来在调节炎症中发挥作用。为了验证我们的假设,我们采用了体内小鼠皮肤伤口模型结合体外小鼠模型来评估 miR-21 表达和巨噬细胞极化。首先,我们发现 miR-21 在糖尿病伤口愈合的每个阶段都表现出明显的表达模式。miR-21 在糖尿病伤口修复的早期和晚期阶段丰度较高,而在创伤的中间阶段(创伤后第 3 天和第 7 天)则显著降低。在巨噬细胞中,M1 极化的巨噬细胞上调了 miR-21 以及 M1 和促炎标志物 IL-1b、TNFa、iNos、IL-6 和 IL-8。在巨噬细胞中过表达 miR-21 导致 miR-21 上调,并增加了 M1 标志物 IL-1b、TNFa、iNos 和 IL-6 的表达。此外,高血糖通过 HG/miR-21/PI3K/NOX2/ROS 信号级联诱导 NOX2 表达和 ROS 产生。这些发现提供了证据表明 miR-21 参与了炎症的调节。miR-21 的失调可能解释了糖尿病伤口中异常炎症和持续的 M1 巨噬细胞极化。