Role of T cell exhaustion and tissue-resident memory T cells in the expression and prognosis of colorectal cancer

Abstract The tumour microenvironment (TME) is complex and dynamic, and changes significantly with tumour progression. Studying the evolving state of T cells, especially tumour-specific subsets, has become feasible. However, the roles of exhausted T cells (Tex) and pre-exhausted tissue-resident memor...

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Main Authors: Han Wu, Pei-Wen Fan, Ya-Ning Feng, Cheng Chang, Ting Gui, Jia-bei Meng, Ruo-Zheng Wang
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-14409-x
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author Han Wu
Pei-Wen Fan
Ya-Ning Feng
Cheng Chang
Ting Gui
Jia-bei Meng
Ruo-Zheng Wang
author_facet Han Wu
Pei-Wen Fan
Ya-Ning Feng
Cheng Chang
Ting Gui
Jia-bei Meng
Ruo-Zheng Wang
author_sort Han Wu
collection DOAJ
description Abstract The tumour microenvironment (TME) is complex and dynamic, and changes significantly with tumour progression. Studying the evolving state of T cells, especially tumour-specific subsets, has become feasible. However, the roles of exhausted T cells (Tex) and pre-exhausted tissue-resident memory T cells (pf-Trm), which emerge after prolonged antigen stimulation, remain unclear. Using single-cell sequencing data, we analyzed the immune landscape of patients with colorectal cancer (CRC) across clinical stages to quantify the abundance of T cell subtypes. Functional enrichment analysis revealed that early stage Tex cells retained some functionality, whereas advanced stage Tex cells showed a significant functional loss. Early stage pf-Trm cells actively participate in immune surveillance and antigen presentation, whereas advanced stage pf-Trm cells exhibit reduced functions. Flow cytometry analysis of clinical cohorts was used to measure the proportions of Tex and pf-Trm. Elevated levels of PD-1 and Tim-3 have been detected in TILs from CRC patients. Data from The Cancer Genome Atlas (TCGA) linked high Tex levels to poor prognosis in CRC, while pf-Trm correlated with better outcomes in early CRC but worse outcomes in advanced CRC due to functional exhaustion. Thus, Tex and pf-Trm cells may serve as prognostic biomarkers, and Tim-3 and CD103 may be promising targets for immune checkpoint inhibitors.
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spelling doaj-art-7baef1aca6644abd8d4815e0fa2f586c2025-08-20T04:01:51ZengNature PortfolioScientific Reports2045-23222025-08-0115111610.1038/s41598-025-14409-xRole of T cell exhaustion and tissue-resident memory T cells in the expression and prognosis of colorectal cancerHan Wu0Pei-Wen Fan1Ya-Ning Feng2Cheng Chang3Ting Gui4Jia-bei Meng5Ruo-Zheng Wang6Xinjiang Key Laboratory of Oncology, The Third Affiliated Teaching Hospital (Affiliated Cancer Hospital) of Xinjiang Medical UniversityXinjiang Key Laboratory of Oncology, The Third Affiliated Teaching Hospital (Affiliated Cancer Hospital) of Xinjiang Medical UniversityXinjiang Key Laboratory of Oncology, The Third Affiliated Teaching Hospital (Affiliated Cancer Hospital) of Xinjiang Medical UniversityClinical Key Specialty of Radiotherapy, Health and Welfare CommissionXinjiang Key Laboratory of Oncology, The Third Affiliated Teaching Hospital (Affiliated Cancer Hospital) of Xinjiang Medical UniversityXinjiang Key Laboratory of Oncology, The Third Affiliated Teaching Hospital (Affiliated Cancer Hospital) of Xinjiang Medical UniversityXinjiang Key Laboratory of Oncology, The Third Affiliated Teaching Hospital (Affiliated Cancer Hospital) of Xinjiang Medical UniversityAbstract The tumour microenvironment (TME) is complex and dynamic, and changes significantly with tumour progression. Studying the evolving state of T cells, especially tumour-specific subsets, has become feasible. However, the roles of exhausted T cells (Tex) and pre-exhausted tissue-resident memory T cells (pf-Trm), which emerge after prolonged antigen stimulation, remain unclear. Using single-cell sequencing data, we analyzed the immune landscape of patients with colorectal cancer (CRC) across clinical stages to quantify the abundance of T cell subtypes. Functional enrichment analysis revealed that early stage Tex cells retained some functionality, whereas advanced stage Tex cells showed a significant functional loss. Early stage pf-Trm cells actively participate in immune surveillance and antigen presentation, whereas advanced stage pf-Trm cells exhibit reduced functions. Flow cytometry analysis of clinical cohorts was used to measure the proportions of Tex and pf-Trm. Elevated levels of PD-1 and Tim-3 have been detected in TILs from CRC patients. Data from The Cancer Genome Atlas (TCGA) linked high Tex levels to poor prognosis in CRC, while pf-Trm correlated with better outcomes in early CRC but worse outcomes in advanced CRC due to functional exhaustion. Thus, Tex and pf-Trm cells may serve as prognostic biomarkers, and Tim-3 and CD103 may be promising targets for immune checkpoint inhibitors.https://doi.org/10.1038/s41598-025-14409-xColorectal cancerTumour microenvironmentT-cell exhaustionPre-failure tissue-resident memory T cellsClinical prognosis
spellingShingle Han Wu
Pei-Wen Fan
Ya-Ning Feng
Cheng Chang
Ting Gui
Jia-bei Meng
Ruo-Zheng Wang
Role of T cell exhaustion and tissue-resident memory T cells in the expression and prognosis of colorectal cancer
Scientific Reports
Colorectal cancer
Tumour microenvironment
T-cell exhaustion
Pre-failure tissue-resident memory T cells
Clinical prognosis
title Role of T cell exhaustion and tissue-resident memory T cells in the expression and prognosis of colorectal cancer
title_full Role of T cell exhaustion and tissue-resident memory T cells in the expression and prognosis of colorectal cancer
title_fullStr Role of T cell exhaustion and tissue-resident memory T cells in the expression and prognosis of colorectal cancer
title_full_unstemmed Role of T cell exhaustion and tissue-resident memory T cells in the expression and prognosis of colorectal cancer
title_short Role of T cell exhaustion and tissue-resident memory T cells in the expression and prognosis of colorectal cancer
title_sort role of t cell exhaustion and tissue resident memory t cells in the expression and prognosis of colorectal cancer
topic Colorectal cancer
Tumour microenvironment
T-cell exhaustion
Pre-failure tissue-resident memory T cells
Clinical prognosis
url https://doi.org/10.1038/s41598-025-14409-x
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