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11 reviewsg 1,9, He Tian1,2,9, Xiaowei Chen 1,9, Bozhao Li3,9, Guangyu Bai1,1234567890():,;1234567890():,;Accepted: 25 September 2024Qingyuan Cai4, Jiachen Xu5,6,Wei Guo 1, ShuaiboWang1, Yue Peng7, Qing Liang1,Liyan Xue 8 & Shugeng Gao 1Check for updatesNeoadjuvant immunochemotherapy (nICT) has dramatically changed thetreatment landscape of operable esophageal squamous cell carcinoma (ESCC),but factors influencing tumor response to nICT are not well understood. Here,using single-cell RNA sequencing paired with T cell receptor sequencing, weprofile tissues from ESCC patients accepting nICT treatment and characterizethe tumor microenvironment context. CXCL13+CD8+ Tex cells, a subset ofexhausted CD8+ T cells, are revealed to highly infiltrate in pre-treatmenttumors and show prominent progenitor exhaustion phenotype in posttreatment samples from responders. We validate CXCL13+CD8+ Tex cells as apredictor of improved response to nICT and reveal CXCL13 to potentiate antiPD-1 efficacy in vivo. Post-treatment tumors from non-responders are enrichedfor CXCL13+CD8+ Tex cells with notably remarkable exhaustion phenotype andTNFRSF4+CD4+ Tregs with activated immunosuppressive function and a significant clone expansion. Several critical markers for therapeutic resistance arealso identified, including LRRC15+ fibroblasts and SPP1+ macrophages, whichmay recruit Tregs to form an immunosuppressive landscape. Overall, ourfindings unravel immune features of distinct therapeutic response to nICTtreatment, providing a rationale for optimizing individualized neoadjuvantstrategy in ESCC.