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Sun, Yunfan; Wu, Liang; Zhong, Yu; Zhou, Kaiqian; Hou, Yong; Wang, Zifei; Zhang, Zefan; Xie, Jiarui; Wang, Chunqing; Chen, Dandan; Huang, Yaling; Wei, Xiaochan; Shi, Yinghong; Zhao, Zhikun; Li, Yuehua; Guo, Ziwei; Yu, Qichao; Xu, Liqin; Volpe, Giacomo; Qiu, Shuangjian; Zhou, Jian; Ward, Carl; Sun, Huichuan; Yin, Ye; Xu, Xun; Wang, Xiangdong; Esteban, Miguel A.; Yang, Huanming; Wang, Jian; Dean, Michael; Zhang, Yaguang; Liu, Shiping; Yang, Xinrong; Fan, Jia
Cell, 01/2021, Volume: 184, Issue: 2Journal Article
Hepatocellular carcinoma (HCC) has high relapse and low 5-year survival rates. Single-cell profiling in relapsed HCC may aid in the design of effective anticancer therapies, including immunotherapies. We profiled the transcriptomes of ∼17,000 cells from 18 primary or early-relapse HCC cases. Early-relapse tumors have reduced levels of regulatory T cells, increased dendritic cells (DCs), and increased infiltrated CD8+ T cells, compared with primary tumors, in two independent cohorts. Remarkably, CD8+ T cells in recurrent tumors overexpressed KLRB1 (CD161) and displayed an innate-like low cytotoxic state, with low clonal expansion, unlike the classical exhausted state observed in primary HCC. The enrichment of these cells was associated with a worse prognosis. Differential gene expression and interaction analyses revealed potential immune evasion mechanisms in recurrent tumor cells that dampen DC antigen presentation and recruit innate-like CD8+ T cells. Our comprehensive picture of the HCC ecosystem provides deeper insights into immune evasion mechanisms associated with tumor relapse. Display omitted •ScRNA-seq reveals a distinct immune ecosystem in early-relapse HCC•Decreased Tregs, increased DCs, and CD8+ T cells were observed in early-relapse HCC•CD8+ T cells have an innate-like, low cytotoxic, and low clonal expansion phenotype•Recurrent malignant cells mediate the compromised antitumor immune response Single-cell analysis of primary and relapsed hepatocellular carcinoma tumors from patients reveal innate-like CD8+ T cells with low cytotoxicity and clonal expansion in the latter that may explain the compromised antitumor immunity and poor prognosis associated with liver cancer.
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