Zhu Chunling, Liao Chengshui, Bai Yilin, Yang Rui, Zhang Boyang, Zhao Xueqin, Zhang Wei, Xia Xiaojing, Zhang Huihui, Sun Huarun, Luo Weiyu, Hu Jianhe, Wen Yuliang, Bai Yueyu, Wang Lei, Ding Ke, Zhang Xueming
College of Animal Science and Veterinary Medicine, Henan Institute of Science and Technology, Xinxiang, 453003, Henan, China.
College of Veterinary Medicine, Jilin University, Changchun, 130000, Jilin, China.
Sci Rep. 2025 Mar 19;15(1):9422. doi: 10.1038/s41598-025-93507-2.
Oxidative stress and disruption of blood‒testis barrier permeability are considered key factors in the pathogenesis of testicular inflammation, degeneration, and functional impairment, which play crucial roles in male infertility. Antimicrobial peptides (AMPs) are internationally recognized as some of the most promising alternatives to antibiotics. However, the molecular mechanisms by which AMPs regulate oxidative stress and the blood‒testis barrier in the testis are still poorly understood. In this study, we orally administered 0.5 mg/kg antimicrobial peptide MPX (MPX) to mice for 20 and 40 days and evaluated its effects on Lipopolysaccharide LPS-induced testicular oxidative stress and blood‒testis barrier repair, and elucidateed the pharmacokinetics of MPX in mice. The experiment was divided into six groups, control, LPS, MPX, MPX + LPS, Polymyxin and Polymyxin + LPS, respectively. The results showed that oral administration of MPX effectively increased testicular Glutathione (GSH), Total superoxide dismutase (T-SOD), and Catalase (CAT) levels and reduced Nitric oxide (NO) and Malondialdehyde (MDA) levels in the testes and Lactate dehydrogenase (LDH) levels in serum; these findings were consistent with the oxidative stress parameters in the liver. MPX significantly upregulated the expression of Kelch-like ECH-associated protein 1 (Keap1), Nuclear factor erythroid 2-related factor 2 (Nrf2), and Glutamate cysteine ligase, modifier (GLCM) in the testes while downregulating the expression of Glutamate cysteine ligase, catalytic (GCLC) and Inducible nitric oxide synthase (iNOS), thus exerting a regulatory effect on oxidative stress. MPX also effectively increased sperm count and motility and counteracted the LPS-induced blood‒testis barrier damage, and its molecular mechanism involved upregulating the expression of Slug, which subsequently promoted high expression of Claudin, Occludin, Zonula occludens-1 (ZO-1), N-cadherin, and E-cadherin in the testes. After intragastric administration of FITC-MPX for 30 min, FITC-MPX was mainly distributed in the stomach and thoracic cavity, then showed multi-tissue distribution after 30 min. The fluorescence signal could be detected in the testis 1 h later, which confirmed that MPX had testicular targeting. Moreover, both intraperitoneal and intravenous injection of FITC-MPX also confirmed its testicular targeting ability. In conclusion, this study systematically evaluated the long-term effects of the orally administered antimicrobial peptide MPX on oxidative stress and the blood‒testis barrier in the male reproductive system. This study laid the foundation for the antimicrobial peptide MPX to be used in the treatment of male testicular inflammatory diseases.
氧化应激和血睾屏障通透性破坏被认为是睾丸炎症、退化和功能损害发病机制中的关键因素,这些因素在男性不育中起着至关重要的作用。抗菌肽(AMPs)在国际上被公认为是抗生素最有前景的替代品之一。然而,AMPs调节睾丸氧化应激和血睾屏障的分子机制仍知之甚少。在本研究中,我们给小鼠口服0.5mg/kg抗菌肽MPX(MPX),持续20天和40天,评估其对脂多糖(LPS)诱导的睾丸氧化应激和血睾屏障修复的影响,并阐明MPX在小鼠体内的药代动力学。实验分为六组,分别为对照组、LPS组、MPX组、MPX+LPS组、多粘菌素组和多粘菌素+LPS组。结果表明,口服MPX可有效提高睾丸中谷胱甘肽(GSH)、总超氧化物歧化酶(T-SOD)和过氧化氢酶(CAT)水平,降低睾丸中一氧化氮(NO)和丙二醛(MDA)水平以及血清中乳酸脱氢酶(LDH)水平;这些结果与肝脏中的氧化应激参数一致。MPX显著上调睾丸中类Kelch样ECH相关蛋白1(Keap1)、核因子红细胞2相关因子2(Nrf2)和谷氨酸半胱氨酸连接酶修饰亚基(GLCM)的表达,同时下调谷氨酸半胱氨酸连接酶催化亚基(GCLC)和诱导型一氧化氮合酶(iNOS)的表达,从而对氧化应激发挥调节作用。MPX还能有效增加精子数量和活力,并抵消LPS诱导的血睾屏障损伤,其分子机制涉及上调Slug的表达,随后促进睾丸中紧密连接蛋白(Claudin)、闭合蛋白(Occludin)、紧密连接蛋白1(ZO-1)、N-钙黏蛋白和E-钙黏蛋白的高表达。胃内给予FITC-MPX 30分钟后,FITC-MPX主要分布在胃和胸腔,30分钟后呈现多组织分布。1小时后可在睾丸中检测到荧光信号,这证实了MPX具有睾丸靶向性。此外,腹腔注射和静脉注射FITC-MPX也证实了其睾丸靶向能力。总之,本研究系统评估了口服抗菌肽MPX对男性生殖系统氧化应激和血睾屏障的长期影响。本研究为抗菌肽MPX用于治疗男性睾丸炎症性疾病奠定了基础。