Yujra Veronica Quispe, Silveira Ericka Janine Dantas da, Ribeiro Daniel Araki, Castilho Rogerio Moraes, Squarize Cristiane Helena
Laboratory of Epithelial Biology, Department of Periodontics and Oral Medicine, School of Dentistry, University of Michigan (UM), Ann Arbor, Michigan, USA.
Department of Biosciences, Federal University of São Paulo (UNIFESP), São Paulo, Brazil.
J Cell Biochem. 2024 Feb;125(2):e30513. doi: 10.1002/jcb.30513. Epub 2024 Jan 16.
Wound healing can be influenced by genes that control the circadian cycle, including Per2 and BMAL1, which coordinate the functions of several organs, including the skin. The aim of the study was to evaluate the role of PER2 during experimental skin wound healing. Two groups (control and Per2-KO), consisting of 14 male mice each, were anesthetized by inhalation, and two 6 mm wounds were created on their dorsal skin using a punch biopsy. A silicone ring was sutured around the wound perimeter to restrict contraction. The wound healing process was clinically measured daily (closure index) until complete wound repair. On Day 6, histomorphometric analysis was performed using the length and thickness of the epithelial migration tongue, in addition to counting vessels underlying the lesion by immunofluorescence assay and maturation of collagen fibers through picrosirius staining. Bromodeoxyuridine (BrdU) incorporation and quantification were performed using the subcutaneous injection technique 2 h before euthanasia and through immunohistochemical analysis of the proliferative index. In addition, the qualitative analysis of myofibroblasts and periostin distribution in connective tissue was performed by immunofluorescence. Statistically significant differences were observed in the healing time between the experimental groups (means: 15.5 days for control mice and 13.5 days for Per2-KO; p = 0.001). The accelerated healing observed in the Per2-KO group (p < 0.05) was accompanied by statistical differences in wound diameter and length of the migrating epithelial tongue (p = 0.01) compared to the control group. Regarding BrdU immunoreactivity, higher expression was observed in the intact epithelium of Per2-KO animals (p = 0.01), and this difference compared to control was also present, to a lesser extent, at the wound site (p = 0.03). Immunofluorescence in the connective tissue underlying the wound showed a higher angiogenic potential in the Per2-KO group in the intact tissue area and the wound region (p < 0.01), where increased expression of myofibroblasts was also observed. Qualitative analysis revealed the distribution of periostin protein and collagen fibers in the connective tissue underlying the wound, with greater organization and maturation during the analyzed period. Our research showed that the absence of the Per2 gene positively impacts the healing time of the skin in vivo. This acceleration depends on the increase of epithelial proliferative and angiogenic capacity of cells carrying the Per2 deletion.
伤口愈合会受到控制昼夜节律周期的基因影响,包括Per2和BMAL1,它们协调包括皮肤在内的多个器官的功能。本研究的目的是评估PER2在实验性皮肤伤口愈合过程中的作用。将两组(对照组和Per2基因敲除组),每组14只雄性小鼠,通过吸入进行麻醉,然后使用打孔活检在其背部皮肤上制造两个6毫米的伤口。在伤口周边缝合一个硅胶环以限制收缩。每天对伤口愈合过程进行临床测量(闭合指数),直至伤口完全修复。在第6天,除了通过免疫荧光测定法对病变下方的血管进行计数以及通过天狼星红染色对胶原纤维的成熟情况进行分析外,还利用上皮迁移舌的长度和厚度进行组织形态计量学分析。在安乐死2小时前,采用皮下注射技术并通过免疫组化分析增殖指数来进行溴脱氧尿苷(BrdU)掺入和定量分析。此外,通过免疫荧光对结缔组织中的肌成纤维细胞和骨膜素分布进行定性分析。实验组之间在愈合时间上观察到统计学上的显著差异(平均值:对照组小鼠为15.5天,Per2基因敲除组为13.5天;p = 0.001)。与对照组相比,Per2基因敲除组观察到的愈合加速(p < 0.05)伴随着伤口直径和迁移上皮舌长度的统计学差异(p = 0.01)。关于BrdU免疫反应性,在Per2基因敲除动物的完整上皮中观察到更高的表达(p = 0.01),并且与对照组相比,在伤口部位也存在较小程度的这种差异(p = 0.03)。伤口下方结缔组织的免疫荧光显示,在完整组织区域和伤口区域,Per2基因敲除组具有更高的血管生成潜力(p < 0.01),在该区域还观察到肌成纤维细胞表达增加。定性分析揭示了伤口下方结缔组织中骨膜素蛋白和胶原纤维的分布,在分析期间组织化和成熟程度更高。我们的研究表明,Per2基因缺失对体内皮肤的愈合时间有积极影响。这种加速取决于携带Per2缺失的细胞上皮增殖和血管生成能力增强。