Li Shaojun, Shen Wanbo, Yu Tingdong, Ran Fengming, Song Zhengrui, Yao Qian, Zha Yong
Hepatobiliary Pancreatic Surgery, Yunnan Cancer Hospital, The Third Affiliated Hospital of Kunming Medical University, Peking University Cancer Hospital Yunnan, Kunming, PR China; Hospital of Honghe State Affiliated to Kunming Medical University, Honghe, Yunnan, PR China.
Hepatobiliary Pancreatic Surgery, Yunnan Cancer Hospital, The Third Affiliated Hospital of Kunming Medical University, Peking University Cancer Hospital Yunnan, Kunming, PR China.
Transl Oncol. 2025 Aug;58:102429. doi: 10.1016/j.tranon.2025.102429. Epub 2025 Jun 6.
The most common subtype of primary liver cancer is hepatocellular carcinoma (HCC), which accounts for about 90 % of primary liver cancers. Tumor microenvironment (TME) plays important roles in HCC development. TME coexists and interacts with various immune cells. Macrophages are the main components of immune cells in TME. However, the specific mechanism of macrophages in HCC development is not fully understood. We conducted a preliminary study on the gene expression differences between HCC macrophages and paracancer macrophages by single-cell sequencing. Results demonstrated that FCGR2A was highly expressed in liver cancer tissues, and FCGR2A was mainly expressed in M2 macrophages in cancer tissues. The expression level of FCGR2A was correlated with extrahepatic metastasis, maximum tumor diameter, CNLC stage, satellite nodule, and differentiation degree. High FCGR2A expression predicts worse overall survival (OS) and progression-free survival (PFS) in HCC patients. In vivo experiments have verified that both FCGR2A mRNA and protein levels are markedly upregulated in M2 macrophages. Transfection of FCGR2A has been demonstrated to drive the polarization of M2 macrophages through augmenting IL-4 secretion. Further experiments showed that FCGR2A regulated and activated the IL-4/JAK/STAT6 pathway. Inhibition of JAK/STAT6 signaling pathway is capable of counteracting the promoting influence of FCGR2A-induced M2 macrophages on HCC cell proliferation. What's more,macrophages with high FCGR2A expression showed immunosuppressive influence on NK and T cells viabilities and killing activities on HCC tumor cells. Our findings reveal a crucial FCGR2A /IL-4/JAK/STAT6 axis for M2 polarization and provide a rationale for therapeutics of macrophages targeting HCC.
原发性肝癌最常见的亚型是肝细胞癌(HCC),约占原发性肝癌的90%。肿瘤微环境(TME)在HCC发展中起重要作用。TME与各种免疫细胞共存并相互作用。巨噬细胞是TME中免疫细胞的主要成分。然而,巨噬细胞在HCC发展中的具体机制尚未完全明确。我们通过单细胞测序对HCC巨噬细胞和癌旁巨噬细胞之间的基因表达差异进行了初步研究。结果表明,FCGR2A在肝癌组织中高表达,且FCGR2A主要在癌组织中的M2巨噬细胞中表达。FCGR2A的表达水平与肝外转移、最大肿瘤直径、CNLC分期、卫星结节及分化程度相关。FCGR2A高表达预示着HCC患者的总生存期(OS)和无进展生存期(PFS)较差。体内实验证实,M2巨噬细胞中FCGR2A的mRNA和蛋白水平均明显上调。已证实转染FCGR2A可通过增加IL-4分泌来驱动M2巨噬细胞极化。进一步实验表明,FCGR2A调节并激活IL-4/JAK/STAT6通路。抑制JAK/STAT6信号通路能够抵消FCGR2A诱导的M2巨噬细胞对HCC细胞增殖的促进作用。此外,FCGR2A高表达的巨噬细胞对NK细胞和T细胞的活力以及对HCC肿瘤细胞的杀伤活性具有免疫抑制作用。我们的研究结果揭示了一条关键的FCGR2A /IL-4/JAK/STAT6轴在M2极化中的作用,并为靶向HCC的巨噬细胞治疗提供了理论依据。