Yuki Tachida, Kannan V Manian, Rossano Butcher, Jonathan M Levy, Nachiket Pendse, Erin Hennessey, David R Liu, Eric A Pierce, Qin Liu, Jason Comander
{"title":"个体碱基编辑靶点的系统经验评价:验证USH2A治疗靶点及方法比较。","authors":"Yuki Tachida, Kannan V Manian, Rossano Butcher, Jonathan M Levy, Nachiket Pendse, Erin Hennessey, David R Liu, Eric A Pierce, Qin Liu, Jason Comander","doi":"10.1016/j.ymthe.2025.01.042","DOIUrl":null,"url":null,"abstract":"<p><p>Base editing shows promise for the correction of human mutations at a higher efficiency than other repair methods and is especially attractive for mutations in large genes that are not amenable to gene augmentation therapy. Here, we demonstrate a comprehensive workflow for in vitro screening of potential therapeutic base editing targets for the USH2A gene and empirically validate the efficiency of adenine and cytosine base editor/guide combinations for correcting 35 USH2A mutations. Editing efficiency and bystander edits are compared between different target templates (plasmids vs. transgenes) and assays (next-generation sequencing vs. Sanger), as well as comparisons between unbiased empirical results and computational predictions. Based on these observations, practical assay recommendations are discussed. Finally, a humanized knockin mouse model was created with the best-performing target, the nonsense mutation c.11864G>A p.(Trp3955∗). Split-intein AAV9 delivery of editing reagents resulted in the restoration of USH2A protein and a correction rate of 65% ± 3% at the mutant base pair and of 52% ± 3% excluding bystander amino acid changes. This efficiency is higher than that seen in a retinal gene editing program testing in a clinical trial. These results demonstrate the effectiveness of this overall strategy to identify and test base editing reagents with the potential for human therapeutic applications.</p>","PeriodicalId":19020,"journal":{"name":"Molecular Therapy","volume":" ","pages":"1466-1484"},"PeriodicalIF":12.1000,"publicationDate":"2025-04-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Systematic empirical evaluation of individual base editing targets: Validating therapeutic targets in USH2A and comparison of methods.\",\"authors\":\"Yuki Tachida, Kannan V Manian, Rossano Butcher, Jonathan M Levy, Nachiket Pendse, Erin Hennessey, David R Liu, Eric A Pierce, Qin Liu, Jason Comander\",\"doi\":\"10.1016/j.ymthe.2025.01.042\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Base editing shows promise for the correction of human mutations at a higher efficiency than other repair methods and is especially attractive for mutations in large genes that are not amenable to gene augmentation therapy. Here, we demonstrate a comprehensive workflow for in vitro screening of potential therapeutic base editing targets for the USH2A gene and empirically validate the efficiency of adenine and cytosine base editor/guide combinations for correcting 35 USH2A mutations. Editing efficiency and bystander edits are compared between different target templates (plasmids vs. transgenes) and assays (next-generation sequencing vs. Sanger), as well as comparisons between unbiased empirical results and computational predictions. Based on these observations, practical assay recommendations are discussed. Finally, a humanized knockin mouse model was created with the best-performing target, the nonsense mutation c.11864G>A p.(Trp3955∗). Split-intein AAV9 delivery of editing reagents resulted in the restoration of USH2A protein and a correction rate of 65% ± 3% at the mutant base pair and of 52% ± 3% excluding bystander amino acid changes. This efficiency is higher than that seen in a retinal gene editing program testing in a clinical trial. These results demonstrate the effectiveness of this overall strategy to identify and test base editing reagents with the potential for human therapeutic applications.</p>\",\"PeriodicalId\":19020,\"journal\":{\"name\":\"Molecular Therapy\",\"volume\":\" \",\"pages\":\"1466-1484\"},\"PeriodicalIF\":12.1000,\"publicationDate\":\"2025-04-02\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Molecular Therapy\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1016/j.ymthe.2025.01.042\",\"RegionNum\":1,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2025/1/28 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q1\",\"JCRName\":\"BIOTECHNOLOGY & APPLIED MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular Therapy","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1016/j.ymthe.2025.01.042","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/28 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
摘要
与其他修复方法相比,碱基编辑有望以更高的效率纠正人类突变,尤其对无法接受基因增强治疗的大基因突变具有吸引力。在这里,我们展示了一个全面的工作流程,用于体外筛选USH2A基因潜在的治疗性碱基编辑靶点,并经验验证了腺嘌呤和胞嘧啶碱基编辑/指南组合纠正35个USH2A突变的效率。比较了不同目标模板(质粒与转基因)和检测(下一代测序与桑格测序)之间的编辑效率和旁观者编辑,以及无偏经验结果和计算预测之间的比较。基于这些观察,讨论了实际的测定建议。最后,以无意义突变c.11864G> a p.(Trp3955*)为靶点,建立了人源敲入小鼠模型。分裂插入的AAV9传递编辑试剂导致USH2A蛋白的恢复,突变碱基对的校正率为65±3%,排除旁观者氨基酸变化的校正率为52±3%。这种效率高于临床试验中视网膜基因编辑程序测试的效率。这些结果证明了这种识别和测试具有人类治疗应用潜力的碱基编辑试剂的总体策略的有效性。
Systematic empirical evaluation of individual base editing targets: Validating therapeutic targets in USH2A and comparison of methods.
Base editing shows promise for the correction of human mutations at a higher efficiency than other repair methods and is especially attractive for mutations in large genes that are not amenable to gene augmentation therapy. Here, we demonstrate a comprehensive workflow for in vitro screening of potential therapeutic base editing targets for the USH2A gene and empirically validate the efficiency of adenine and cytosine base editor/guide combinations for correcting 35 USH2A mutations. Editing efficiency and bystander edits are compared between different target templates (plasmids vs. transgenes) and assays (next-generation sequencing vs. Sanger), as well as comparisons between unbiased empirical results and computational predictions. Based on these observations, practical assay recommendations are discussed. Finally, a humanized knockin mouse model was created with the best-performing target, the nonsense mutation c.11864G>A p.(Trp3955∗). Split-intein AAV9 delivery of editing reagents resulted in the restoration of USH2A protein and a correction rate of 65% ± 3% at the mutant base pair and of 52% ± 3% excluding bystander amino acid changes. This efficiency is higher than that seen in a retinal gene editing program testing in a clinical trial. These results demonstrate the effectiveness of this overall strategy to identify and test base editing reagents with the potential for human therapeutic applications.
期刊介绍:
Molecular Therapy is the leading journal for research in gene transfer, vector development, stem cell manipulation, and therapeutic interventions. It covers a broad spectrum of topics including genetic and acquired disease correction, vaccine development, pre-clinical validation, safety/efficacy studies, and clinical trials. With a focus on advancing genetics, medicine, and biotechnology, Molecular Therapy publishes peer-reviewed research, reviews, and commentaries to showcase the latest advancements in the field. With an impressive impact factor of 12.4 in 2022, it continues to attract top-tier contributions.