Puente-Cobacho Beatriz, Esteo Cintia, Altea-Manzano Patricia, Garcia-Perez Jose Luis, Quiles José L, Sanchez-Rovira Pedro, Martín-Salvago María D, Molina-Jiménez Lucía, Luque Rafael J, Fendt Sarah-Maria, Vera-Ramirez Laura
Department of Genomic Medicine, GENYO, Centre for Genomics and Oncology, Pfizer-University of Granada and Andalusian Regional Government, PTS, Granada, Spain; Department of Physiology, Institute of Nutrition and Food Technology "José Mataix Verdú", Biomedical Research Center, University of Granada, Granada, Spain.
Laboratory of Cellular Metabolism and Metabolic Regulation, VIB-KU Leuven Center for Cancer Biology, Leuven, Belgium; Laboratory of Cellular Metabolism and Metabolic Regulation, Department of Oncology, KU Leuven and Leuven Cancer Institute (LKI), Leuven, Belgium.
Redox Biol. 2025 Mar;80:103480. doi: 10.1016/j.redox.2024.103480. Epub 2024 Dec 31.
Dormant disseminated tumor cells (DTCs) remain viable for years to decades before establishing a clinically overt metastatic lesion. DTCs are known to be highly resilient and able to overcome the multiple biological hurdles imposed along the metastatic cascade. However, the specific metabolic adaptations of dormant DTCs remain to be elucidated. Here, we reveal that dormant DTCs upregulate de novo lipogenesis and favor the activation and incorporation of monounsaturated fatty acids (MUFAs) to their cellular membranes through the activation of acyl-coenzyme A synthetase long-chain family member 3 (ACSL3). Pharmacologic inhibition of de novo lipogenesis or genetic knockdown of ACSL3 results in lipid peroxidation and non-apoptotic cell death through ferroptosis. Clinically, ACSL3 was found to be overexpressed in quiescent DTCs in the lymph nodes of breast cancer patients and to significantly correlate with shorter disease-free and overall survival. Our work provides new insights into the molecular mechanisms enabling the survival of dormant DTCs and supports the use of de novo lipogenesis inhibitors to prevent breast cancer metastasis.
休眠的播散肿瘤细胞(DTCs)在形成临床明显的转移病灶之前可存活数年至数十年。已知DTCs具有高度的抗逆性,能够克服转移级联过程中遇到的多种生物学障碍。然而,休眠DTCs的具体代谢适应性仍有待阐明。在此,我们发现休眠DTCs上调从头脂肪生成,并通过激活酰基辅酶A合成酶长链家族成员3(ACSL3),促进单不饱和脂肪酸(MUFAs)激活并掺入其细胞膜。从头脂肪生成的药理学抑制或ACSL3的基因敲低会导致脂质过氧化和通过铁死亡引起的非凋亡性细胞死亡。在临床上,发现ACSL3在乳腺癌患者淋巴结中的静止DTCs中过表达,并且与较短的无病生存期和总生存期显著相关。我们的工作为使休眠DTCs存活的分子机制提供了新的见解,并支持使用从头脂肪生成抑制剂来预防乳腺癌转移。