Kong Lingfan, Wei Lingyun, Wang Lin, Geng Mengyu, Wang Wenzhen, Liu Xiaochun
Third Hospital of Shanxi Medical University, Shanxi Bethune Hospital, Shanxi Academy of Medical Sciences, Tongji Shanxi Hospital, Taiyuan, 030032, China.
Sci Rep. 2025 Jul 1;15(1):21977. doi: 10.1038/s41598-025-08509-x.
Pelvic organ prolapse (POP) and its subtypes are serious concerns affecting a woman's quality of life and pose a challenge for her social reintegration. Prolonged labor leading to trauma of the pelvic floor muscles during delivery, surgical or other trauma, aging and menopause, lifestyle changes, and genetic factors may contribute to the tissue degeneration and prolapse of pelvic organs. The purpose of this research was to evaluate the potential contributions of IGF-1 and LARP6 to the pathophysiology of poliomyelitis- dysplastic scoliosis and help in devising preventive and therapeutic measures. This study included a population of 15 women suffering from POP as a case group and a control group of 15 women who underwent total hysterectomy for benign gynecological diseases. Their vaginal wall tissue samples were obtained, and differences in expression of IGF-1, LARP6, Collagen I/III and MMP2 were analyzed using Western blot (WB), immunohistochemistry (IHC), and multiplex immunofluorescence (mIHC) techniques. Collagen deposition and other histopathological changes were examined by HE staining and Masson staining. Patients' with POP's vaginal wall tissues were used for isolating and culturing primary fibroblasts, which were then subjected to varying concentrations and time durations of IGF-1 treatment to optimize the culture conditions, measuring Collagen I and III expression levels as indicators. Changes in the expression levels of LARP6, collagen metabolism related proteins, and PI3K/AKT signaling pathway were investigated using WB and RT-qPCR, further analysis was done by applying PI3K/AKT signaling pathway inhibitors; CCK-8 and Tunnel histomorphology analysis were used to evaluate cell proliferation and apoptosis, respectively. Moreover, a LARP6 knockdown model was created whereby siRNAs specifically targeting the LARP6 transcript were transfected into cells, and subsequently, the protein and mRNA levels of collagen I, III, MMP2, and TIMP1 were analyzed by WB and RT-qPCR. LARP6 and IGF-1 expression was found to be significantly lower in the vaginal wall tissues of POP patients compared with controls. Histological staining revealed that collagen fiber structures in the POP group were loose, disorganized, and discontinuous. In primary fibroblasts, IGF-1 was able to up-regulate LARP6 and collagen expression in a dose- and time-dependent manner and favorable to the secretion of LARP6 and collagen through PI3K/Akt signaling pathway. The knockdown of LARP6 by siRNA technology demonstrated significant reduction of collagen secretion expression suggesting interferences of LARP6 inhibits collagen synthesis in fibroblasts. IGF-1 has a strong correlation with LARP6 in relation to the development of POP. The reduction in fibroblasts in the subepithelial layer of the vaginal wall is probably associated with POP, while depletion of collagen synthesis and escalation of collagen breakdown may serve as the pathophysiologic foundation for POP. In patients suffering from POP, IGF-1 has the capability to enhance the expression of LARP6 and collagen in their fibroblasts, which highly depends on the activity of the PI3K/AKT signaling pathway. This study unveils new insights and possible molecular approaches to the pathophysiology of POP.
盆腔器官脱垂(POP)及其亚型是影响女性生活质量的严重问题,对其重新融入社会构成挑战。分娩时产程延长导致盆底肌肉创伤、手术或其他创伤、衰老和绝经、生活方式改变以及遗传因素等,都可能导致盆腔器官组织退化和脱垂。本研究的目的是评估胰岛素样生长因子-1(IGF-1)和富含亮氨酸重复序列6(LARP6)对脊髓灰质炎-发育异常性脊柱侧凸病理生理学的潜在影响,并有助于制定预防和治疗措施。本研究纳入了15名患有盆腔器官脱垂的女性作为病例组,以及15名因良性妇科疾病接受全子宫切除术的女性作为对照组。获取她们的阴道壁组织样本,采用蛋白质免疫印迹法(WB)、免疫组织化学法(IHC)和多重免疫荧光法(mIHC)分析IGF-1、LARP6、Ⅰ/Ⅲ型胶原蛋白和基质金属蛋白酶2(MMP2)表达的差异。通过苏木精-伊红染色(HE染色)和马松染色检查胶原蛋白沉积及其他组织病理学变化。取盆腔器官脱垂患者的阴道壁组织分离培养原代成纤维细胞,然后用不同浓度和时间的IGF-1处理以优化培养条件,以Ⅰ型和Ⅲ型胶原蛋白表达水平作为指标进行检测。采用WB和逆转录-定量聚合酶链反应(RT-qPCR)研究LARP6、胶原蛋白代谢相关蛋白及磷脂酰肌醇-3激酶/蛋白激酶B(PI3K/AKT)信号通路表达水平的变化,应用PI3K/AKT信号通路抑制剂进行进一步分析;分别采用细胞计数试剂盒-8(CCK-8)法和TUNEL组织形态学分析评估细胞增殖和凋亡。此外,构建LARP6基因敲低模型,将特异性靶向LARP6转录本的小干扰RNA(siRNA)转染到细胞中,随后通过WB和RT-qPCR分析Ⅰ型、Ⅲ型胶原蛋白、MMP2和基质金属蛋白酶组织抑制因子1(TIMP1)的蛋白质和mRNA水平。结果发现,与对照组相比,盆腔器官脱垂患者阴道壁组织中IGF-1和LARP6表达明显降低。组织学染色显示,盆腔器官脱垂组的胶原纤维结构松散、紊乱且不连续。在原代成纤维细胞中,IGF-1能够以剂量和时间依赖性方式上调LARP6和胶原蛋白的表达,并通过PI3K/Akt信号通路促进LARP6和胶原蛋白的分泌。采用siRNA技术敲低LARP6后,胶原蛋白分泌表达显著降低,提示干扰LARP6可抑制成纤维细胞中的胶原蛋白合成。在盆腔器官脱垂的发生发展过程中,IGF-1与LARP6密切相关。阴道壁上皮下层成纤维细胞减少可能与盆腔器官脱垂有关,而胶原蛋白合成减少和分解增加可能是盆腔器官脱垂的病理生理基础。在盆腔器官脱垂患者中,IGF-1能够增强其成纤维细胞中LARP6和胶原蛋白的表达,这高度依赖于PI3K/AKT信号通路的活性。本研究揭示了盆腔器官脱垂病理生理学的新见解和可能的分子机制。