Zheng Cuimiao, Tan Hao, Niu Gang, Huang Xi, Lu Jingyi, Chen Siqi, Li Haoyuan, Zhu Jiayu, Zhou Zhou, Xu Manman, Pan Chaoyun, Liu Junxiu, Li Jie
Department of Obstetrics and Gynecology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, 510080, China.
Department of Biochemistry and Molecular Biology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, 510080, China.
Adv Sci (Weinh). 2025 Apr;12(14):e2416467. doi: 10.1002/advs.202416467. Epub 2025 Feb 14.
Lactate derived from aerobic glycolysis is crucial for DNA damage repair and chemoresistance. Nevertheless, it is frequently noted that cancer cells depend on glutaminolysis to replenish essential metabolites. Whether and how glutaminolysis might enhance lactate production and facilitate DNA repair in cancer cells remains unknown. Here, it is shown that malate enzyme 2 (ME2), which metabolizes glutamine-derived malate to pyruvate, contributes to lactate production and chemotherapy resistance in ovarian cancer. Mechanistically, chemotherapy reduces the expression of glucose transporters and impairs glucose uptake in cancer cells. The resultant decrease in intracellular glucose levels triggers the acetylation of ME2 at lysine 156 by ACAT1, which in turn potentiates ME2 enzyme activity and facilitates lactate production from glutamine. ME2-derived lactate contributes to the development of acquired chemoresistance in cancer cells subjected to prolonged chemotherapy, primarily by facilitating the lactylation of proteins involved in homologous recombination repair. Targeting ACAT1 to inhibit ME2 acetylation effectively reduced chemoresistance in both in vitro and in vivo models. These findings underscore the significance of acetylated ME2-mediated lactate production from glutamine in chemoresistance, particularly under conditions of reduced intracellular glucose within cancer cell, thereby complementing the Warburg effect and offering new perspectives on the metabolic links to chemotherapy resistance.
有氧糖酵解产生的乳酸对DNA损伤修复和化疗耐药性至关重要。然而,人们经常注意到癌细胞依赖谷氨酰胺分解来补充必需代谢物。谷氨酰胺分解是否以及如何增强癌细胞中的乳酸产生并促进DNA修复仍不清楚。在此,研究表明苹果酸酶2(ME2)将谷氨酰胺衍生的苹果酸代谢为丙酮酸,有助于卵巢癌中的乳酸产生和化疗耐药性。从机制上讲,化疗会降低葡萄糖转运蛋白的表达并损害癌细胞对葡萄糖的摄取。细胞内葡萄糖水平的降低会触发ACAT1对ME2赖氨酸156位点的乙酰化,这反过来又增强了ME2的酶活性并促进了谷氨酰胺产生乳酸。ME2衍生的乳酸主要通过促进参与同源重组修复的蛋白质的乳酰化,促进了长期接受化疗的癌细胞获得性化疗耐药性的发展。靶向ACAT1以抑制ME2乙酰化在体外和体内模型中均有效降低了化疗耐药性。这些发现强调了乙酰化ME2介导的谷氨酰胺产生乳酸在化疗耐药性中的重要性,特别是在癌细胞内葡萄糖减少的情况下,从而补充了瓦伯格效应,并为化疗耐药性的代谢联系提供了新的视角。