Tsilingiris Dimitrios, Natsi Anastasia-Maria, Gavriilidis Efstratios, Antoniadou Christina, Eleftheriadou Ioanna, Anastasiou Ioanna A, Tentolouris Anastasios, Papadimitriou Evangelos, Eftalitsidis Evgenios, Kolovos Panagiotis, Tsironidou Victoria, Giatromanolaki Alexandra, Koffa Maria, Tentolouris Nikolaos, Skendros Panagiotis, Ritis Konstantinos
First Department of Internal Medicine, University Hospital of Alexandroupolis, Democritus University of Thrace, Alexandroupolis, Greece.
Laboratory of Molecular Hematology, Department of Medicine, Democritus University of Thrace, Alexandroupolis, Greece.
Eur J Immunol. 2025 Apr;55(4):e202451664. doi: 10.1002/eji.202451664.
Neutrophils interact with and activate fibroblasts through the release of neutrophil extracellular traps (NETs). We investigated the role of NETs-fibroblast crosstalk in the cutaneous wound healing of type 2 diabetes (T2D). Neutrophils/NETs, serum, and primary human skin fibroblasts (HSFs) were obtained from individuals with T2D and age/sex-matched controls. NET-stimulation studies were performed on neutrophils/HSFs, with and without specific inhibitors, while HSF healing capacity was assessed using a scratch wound healing assay. T2D HSFs display a profibrotic phenotype, showing increased CCN2/CTGF, α-smooth muscle actin, and collagen release, albeit with impaired healing capacity, elevated type I collagen C-terminal telopeptide, and collagen degradation associated with increased (∼3.5-fold) matrix metalloproteinase-9 (MMP-9) in T2D neutrophils/NETs. IL-8 induced the expression of MMP-9 in neutrophils/NETs. Moreover, T2D neutrophils/NETs exhibited increased IL-8 content, which acted in an autocrine/paracrine fashion to further augment its production by neutrophils/HSFs. The findings were validated in normoglycemic individuals during a hyperglycemic clamp with concomitant lipid infusion and further corroborated immunohistochemically in diabetic plantar ulcer biopsies. This novel, vicious circle of NETs/interleukin-8/MMP-9/HSFs was hindered by IL-8 or MMP-9 blockade via specific inhibitors or by dismantling the NET-scaffold with DNase I, suggesting candidate therapeutic targets in wound healing impairment of T2D.
中性粒细胞通过释放中性粒细胞胞外陷阱(NETs)与成纤维细胞相互作用并激活成纤维细胞。我们研究了NETs与成纤维细胞的相互作用在2型糖尿病(T2D)皮肤伤口愈合中的作用。从T2D患者以及年龄和性别匹配的对照个体中获取中性粒细胞/NETs、血清和原代人皮肤成纤维细胞(HSFs)。在有或没有特异性抑制剂的情况下,对中性粒细胞/HSFs进行NET刺激研究,同时使用划痕伤口愈合试验评估HSF的愈合能力。T2D HSFs表现出促纤维化表型,显示CCN2/结缔组织生长因子(CTGF)、α平滑肌肌动蛋白和胶原蛋白释放增加,尽管其愈合能力受损,I型胶原蛋白C末端肽升高,且T2D中性粒细胞/NETs中与基质金属蛋白酶-9(MMP-9)增加(约3.5倍)相关的胶原蛋白降解增加。白细胞介素-8(IL-8)诱导中性粒细胞/NETs中MMP-9的表达。此外,T2D中性粒细胞/NETs的IL-8含量增加,其以自分泌/旁分泌方式作用,进一步增强中性粒细胞/HSFs对其的产生。在正常血糖个体进行高血糖钳夹并同时输注脂质期间,这些发现得到了验证,并在糖尿病足底溃疡活检中通过免疫组织化学进一步得到证实。通过特异性抑制剂阻断IL-8或MMP-9,或用脱氧核糖核酸酶I破坏NET支架,可阻碍NETs/白细胞介素-8/MMP-9/HSFs这一新型恶性循环,提示这可能是T2D伤口愈合受损的候选治疗靶点。