Laboratory of Molecular Pathology, Department of Health Sciences, Università del Piemonte Orientale, Via Solaroli 17, 28100 Novara, Italy.
Stephenson Cancer Center, The University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA.
Int J Mol Sci. 2024 May 23;25(11):5691. doi: 10.3390/ijms25115691.
One aspect of ovarian tumorigenesis which is still poorly understood is the tumor-stroma interaction, which plays a major role in chemoresistance and tumor progression. Cancer-associated fibroblasts (CAFs), the most abundant stromal cell type in the tumor microenvironment, influence tumor growth, metabolism, metastasis, and response to therapy, making them attractive targets for anti-cancer treatment. Unraveling the mechanisms involved in CAFs activation and maintenance is therefore crucial for the improvement of therapy efficacy. Here, we report that CAFs phenoconversion relies on the glucose-dependent inhibition of autophagy. We show that ovarian cancer cell-conditioning medium induces a metabolic reprogramming towards the CAF-phenotype that requires the autophagy-dependent glycolytic shift. In fact, 2-deoxy-D-glucose (2DG) strongly hampers such phenoconversion and, most importantly, induces the phenoreversion of CAFs into quiescent fibroblasts. Moreover, pharmacological inhibition (by proline) or autophagy gene knockdown (by siBECN1 or siATG7) promotes, while autophagy induction (by either 2DG or rapamycin) counteracts, the metabolic rewiring induced by the ovarian cancer cell secretome. Notably, the nutraceutical resveratrol (RV), known to inhibit glucose metabolism and to induce autophagy, promotes the phenoreversion of CAFs into normal fibroblasts even in the presence of ovarian cancer cell-conditioning medium. Overall, our data support the view of testing autophagy inducers for targeting the tumor-promoting stroma as an adjuvant strategy to improve therapy success rates, especially for tumors with a highly desmoplastic stroma, like ovarian cancer.
卵巢肿瘤发生的一个方面仍然理解得很差,那就是肿瘤-基质相互作用,它在化疗耐药性和肿瘤进展中起着重要作用。癌症相关成纤维细胞(CAFs)是肿瘤微环境中最丰富的基质细胞类型,影响肿瘤生长、代谢、转移和对治疗的反应,使其成为抗癌治疗的有吸引力的靶点。因此,揭示 CAFs 激活和维持的机制对于提高治疗效果至关重要。在这里,我们报告 CAFs 表型转化依赖于葡萄糖依赖性自噬抑制。我们表明,卵巢癌细胞条件培养基诱导代谢重编程为 CAF 表型,这需要自噬依赖性糖酵解转移。事实上,2-脱氧-D-葡萄糖(2DG)强烈阻碍了这种表型转化,最重要的是,诱导 CAFs 向静止成纤维细胞的表型逆转。此外,药理学抑制(通过脯氨酸)或自噬基因敲低(通过 siBECN1 或 siATG7)促进,而自噬诱导(通过 2DG 或 rapamycin)则抑制卵巢癌细胞分泌组诱导的代谢重排。值得注意的是,营养保健品白藜芦醇(RV)已知能抑制葡萄糖代谢并诱导自噬,即使在卵巢癌细胞条件培养基存在的情况下,它也能促进 CAFs 向正常成纤维细胞的表型逆转。总的来说,我们的数据支持了测试自噬诱导剂作为一种辅助策略来提高治疗成功率的观点,特别是对于具有高度促结缔组织增生性基质的肿瘤,如卵巢癌。