Curriculum in Genetics and Molecular Biology, and.
UNC Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
JCI Insight. 2024 Nov 22;9(22):e175098. doi: 10.1172/jci.insight.175098.
Immune evasion by tumors is promoted by low T cell infiltration, ineffective T cell activity directed against the tumor, and reduced tumor antigen presentation. The TET2 DNA dioxygenase gene is frequently mutated in hematopoietic malignancies and loss of TET enzymatic activity is found in a variety of solid tumors. We showed previously that vitamin C (VC), a cofactor of TET2, enhances tumor-associated T cell recruitment and checkpoint inhibitor therapy responses in a TET2-dependent manner. Using single-cell RNA sequencing (scRNA-seq) analysis performed on B16-OVA melanoma tumors, we have shown here that an additional function for TET2 in tumors is to promote expression of certain antigen presentation machinery genes, which is potently enhanced by VC. Consistently, VC promoted antigen presentation in cell-based and tumor assays in a TET2-dependent manner. Quantifying intercellular signaling from the scRNA-seq dataset showed that T cell-derived IFN-γ-induced signaling within the tumor and tumor microenvironment requires tumor-associated TET2 expression, which is enhanced by VC treatment. Analysis of patient tumor samples indicated that TET activity directly correlates with antigen presentation gene expression and with patient outcomes. Our results demonstrate the importance of tumor-associated TET2 activity as a critical mediator of tumor immunity, which is augmented by high-dose VC therapy.
肿瘤的免疫逃逸是由低 T 细胞浸润、针对肿瘤的无效 T 细胞活性和减少的肿瘤抗原呈递所促进的。TET2 DNA 双加氧酶基因在造血恶性肿瘤中经常发生突变,并且在各种实体肿瘤中发现 TET 酶活性丧失。我们之前表明,维生素 C(VC)是 TET2 的辅助因子,以 TET2 依赖的方式增强与肿瘤相关的 T 细胞募集和检查点抑制剂治疗反应。通过对 B16-OVA 黑色素瘤肿瘤进行单细胞 RNA 测序(scRNA-seq)分析,我们在这里表明,TET2 在肿瘤中的另一个功能是促进某些抗原呈递机制基因的表达,而 VC 则能显著增强这一功能。一致地,VC 以 TET2 依赖的方式在基于细胞和肿瘤的测定中促进抗原呈递。从 scRNA-seq 数据集定量细胞间信号表明,T 细胞衍生的 IFN-γ诱导的肿瘤内和肿瘤微环境中的信号需要肿瘤相关的 TET2 表达,而 VC 处理可增强这种表达。对患者肿瘤样本的分析表明,TET 活性与抗原呈递基因表达以及患者的预后直接相关。我们的结果表明,肿瘤相关的 TET2 活性作为肿瘤免疫的关键介质的重要性,而高剂量 VC 治疗可增强这种活性。