DNA damage-inducible transcript 3-mediated endoplasmic reticulum stress drives manganese-induced apoptosis in bovine testicular Leydig cells

DNA损伤诱导转录物3介导的内质网应激驱动锰诱导的牛睾丸间质细胞凋亡

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Abstract

Manganese (Mn) is an essential trace element, but it is also an environmental pollutant. Excessive Mn accumulation in animals induces toxic effects, particularly reproductive damage. The mechanism of Mn toxicity in ruminants is unclear. This study investigated the mechanism of Mn toxicity on bovine Leydig cells. Bovine Leydig cells were treated with Mn at a semi-inhibitory concentration of 70 μM for 24 h, and this concentration was subsequently set as the Mn-treated experimental group. Multiple analytical approaches were employed, including the examination of cellular ultrastructure, measurement of oxidative stress indicators, analysis of apoptosis-related genes, and RNA-Seq sequencing for the screening of differentially expressed genes. The results showed that Mn treatment led to abnormal damage to the ultrastructure of mitochondria and endoplasmic reticulum. An increase in reactive oxygen species (ROS) and malondialdehyde (MDA) levels, along with a decrease in glutathione peroxidase (GSH-Px) activity, provided evidence of oxidative stress induction. Additionally, Mn exposure upregulated the expression of apoptosis-related genes Caspase-3 and BAX, while downregulating the expression of BCL-2, indicating the initiation of apoptosis. RNA-Seq analysis revealed that the DDIT3 gene, associated with endoplasmic reticulum stress, exhibited highly significant differential expression. Further experiments showed that knockdown of the DDIT3 gene effectively alleviated Mn-induced apoptosis in bovine Leydig cells. In conclusion, Mn exposure promotes apoptosis in bovine Leydig cells, and interference with DDIT3 can mitigate this apoptotic process, which provides valuable references for the prevention and control of Mn pollution in animal husbandry and the management of the reproductive health of breeding bulls.

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