Translational Cancer Genomics, Wellcome Sanger Institute, Hinxton, UK; Open Targets, Cambridge, UK.
Gene Editing and Cellular Research and Development, Wellcome Sanger Institute, Hinxton, UK; Open Targets, Cambridge, UK.
Cancer Cell. 2023 Feb 13;41(2):288-303.e6. doi: 10.1016/j.ccell.2022.12.009. Epub 2023 Jan 19.
Interferon-γ (IFN-γ) signaling mediates host responses to infection, inflammation and anti-tumor immunity. Mutations in the IFN-γ signaling pathway cause immunological disorders, hematological malignancies, and resistance to immune checkpoint blockade (ICB) in cancer; however, the function of most clinically observed variants remains unknown. Here, we systematically investigate the genetic determinants of IFN-γ response in colorectal cancer cells using CRISPR-Cas9 screens and base editing mutagenesis. Deep mutagenesis of JAK1 with cytidine and adenine base editors, combined with pathway-wide screens, reveal loss-of-function and gain-of-function mutations, including causal variants in hematological malignancies and mutations detected in patients refractory to ICB. We functionally validate variants of uncertain significance in primary tumor organoids, where engineering missense mutations in JAK1 enhanced or reduced sensitivity to autologous tumor-reactive T cells. We identify more than 300 predicted missense mutations altering IFN-γ pathway activity, generating a valuable resource for interpreting gene variant function.
干扰素-γ (IFN-γ) 信号转导介导宿主对感染、炎症和抗肿瘤免疫的反应。IFN-γ 信号通路中的突变会导致免疫失调、血液系统恶性肿瘤以及癌症中免疫检查点阻断 (ICB) 的耐药性;然而,大多数临床观察到的变异体的功能仍然未知。在这里,我们使用 CRISPR-Cas9 筛选和碱基编辑诱变,系统地研究了结直肠癌细胞中 IFN-γ 反应的遗传决定因素。使用胞嘧啶和腺嘌呤碱基编辑器对 JAK1 进行深度诱变,结合通路范围的筛选,揭示了失活和激活功能的突变,包括血液系统恶性肿瘤中的因果变异和在对 ICB 耐药的患者中检测到的突变。我们在原代肿瘤类器官中对意义不明的变异进行了功能验证,其中 JAK1 的错义突变工程增强或降低了对自体肿瘤反应性 T 细胞的敏感性。我们鉴定了 300 多个预测的改变 IFN-γ 通路活性的错义突变,为解释基因变异功能提供了有价值的资源。