Qi Chunhui, Cao Bin, Gong Zhiwen, Zhang Weiyu, Yang Pengfei, Qin Haorui, Zhao Yan, Chen Yingchun
Guangdong Provincial Engineering Research Center of Molecular Imaging, The Fifth Affiliated Hospital, Sun Yat-sen University, Zhuhai 519000, China; Department of Infectious Diseases, The Fifth Affiliated Hospital, Sun Yat-sen University, Zhuhai 519000, Guangdong Province, China; Guangdong-Hong Kong-Macao University Joint Laboratory of Interventional Medicine, The Fifth Affiliated Hospital, Sun Yat-sen University, Zhuhai 519000, China.
Department of Cardiology, The 7th People's Hospital of Zhengzhou, Zhengzhou, Henan Province 450016, China.
Cell Signal. 2025 Mar;127:111589. doi: 10.1016/j.cellsig.2025.111589. Epub 2025 Jan 5.
Metabolic reprogramming plays a critical role in tumorigenesis and progression, including hepatocellular carcinoma (HCC). The Solute Carriers (SLCs) family is responsible for the transport of a range of nutrients and has been linked to various cancers. Cancer stem cells (CSC) are a contributing factor to the recurrence and metastasis of HCC. However, the regulatory genes that govern this process remain unclear. The present study identified SLC35C2 as a crucial factor in maintaining the stem-cell characteristics of HCC cells through CRISPR-dCas9 screening. Further investigation demonstrated that SLC35C2 was significantly elevated in HCC tissues and correlated with a poor prognosis in HCC patients. It is an independent prognostic factor for HCC patients. The knockdown and overexpression of SLC35C2 inhibited or promoted stemness in HCC cell. Both in vitro and in vivo studies demonstrated that SLC35C2 promoted the proliferation, migration, invasion and metastasis in HCC cells. Through RNA-seq and lipidomics analysis, it was found that SLC35C2 regulated lipid reprogramming, particularly triglyceride synthesis. Mechanistically, SLC35C2 stimulated lipogenesis through the up-regulation of SREBP1, ACC, FAS, and SCD-1, thereby increasing lipid accumulation in HCC cells. SLC35C2 interacted with ACSL4, which plays a critical role in lipogenesis, and to protect it from degradation. Inhibition of ACSL4 with PRGL493 can reverse the lipogenesis, stemness and proliferation induced by SLC35C2 overexpression. In conclusion, our study demonstrates the pivotal role of SLC35C2 in stemness and malignant progression in HCC by promoting lipogenesis. These findings suggest that SLC35C2 is a prognostic marker and promising therapeutic target for HCC treatment.
代谢重编程在肿瘤发生和进展中起着关键作用,包括肝细胞癌(HCC)。溶质载体(SLC)家族负责多种营养物质的运输,并与多种癌症有关。癌症干细胞(CSC)是HCC复发和转移的一个促成因素。然而,控制这一过程的调控基因仍不清楚。本研究通过CRISPR-dCas9筛选确定SLC35C2是维持HCC细胞干细胞特性的关键因素。进一步研究表明,SLC35C2在HCC组织中显著升高,且与HCC患者的不良预后相关。它是HCC患者的一个独立预后因素。SLC35C2的敲低和过表达分别抑制或促进HCC细胞的干性。体外和体内研究均表明,SLC35C2促进HCC细胞的增殖、迁移、侵袭和转移。通过RNA测序和脂质组学分析发现,SLC35C2调节脂质重编程,特别是甘油三酯的合成。机制上,SLC35C2通过上调SREBP1、ACC、FAS和SCD-1刺激脂肪生成,从而增加HCC细胞中的脂质积累。SLC35C2与在脂肪生成中起关键作用的ACSL4相互作用,并保护其不被降解。用PRGL493抑制ACSL4可逆转SLC35C2过表达诱导的脂肪生成、干性和增殖。总之,我们的研究证明了SLC35C2通过促进脂肪生成在HCC的干性和恶性进展中起关键作用。这些发现表明,SLC35C2是HCC治疗的一个预后标志物和有前景的治疗靶点。