Single-cell and spatial transcriptome analyses reveal tertiary lymphoid structures linked to tumour progression and immunotherapy response in nasopharyngeal carcinoma

Yang Liu, Shuang-Yan Ye, Shuai He, Dong-Mei Chi, Xiu-Zhi Wang, Yue-Feng Wen, Dong Ma, Run-Cong Nie, Pu Xiang, You Zhou, Zhao-Hui Ruan, Rou-Jun Peng, Chun-Ling Luo, Pan-Pan Wei, Guo-Wang Lin, Jian Zheng, Qian Cui, Mu-Yan Cai, Jing-Ping Yun, Junchao Dong, Hai-Qiang Mai, Xiaojun Xia and Jin-Xin Bei ()
Additional contact information
Yang Liu: Sun Yat-sen University Cancer Center
Shuang-Yan Ye: Sun Yat-sen University
Shuai He: Sun Yat-sen University Cancer Center
Dong-Mei Chi: Sun Yat-sen University Cancer Center
Xiu-Zhi Wang: Sun Yat-sen University Cancer Center
Yue-Feng Wen: Affiliated Cancer Hospital & Institute of Guangzhou Medical University
Dong Ma: Sun Yat-sen University Cancer Center
Run-Cong Nie: Sun Yat-sen University Cancer Center
Pu Xiang: Sun Yat-sen University Cancer Center
You Zhou: Sun Yat-sen University Cancer Center
Zhao-Hui Ruan: Sun Yat-sen University Cancer Center
Rou-Jun Peng: Sun Yat-sen University Cancer Center
Chun-Ling Luo: Sun Yat-sen University Cancer Center
Pan-Pan Wei: Sun Yat-sen University Cancer Center
Guo-Wang Lin: Southern Medical University
Jian Zheng: Sun Yat-sen University Cancer Center
Qian Cui: Southern Medical University
Mu-Yan Cai: Sun Yat-sen University Cancer Center
Jing-Ping Yun: Sun Yat-sen University Cancer Center
Junchao Dong: Sun Yat-sen University
Hai-Qiang Mai: Sun Yat-sen University Cancer Center
Xiaojun Xia: Sun Yat-sen University Cancer Center
Jin-Xin Bei: Sun Yat-sen University Cancer Center

Nature Communications, 2024, vol. 15, issue 1, 1-22

Abstract: Abstract Tertiary lymphoid structures are immune cell aggregates linked with cancer outcomes, but their interactions with tumour cell aggregates are unclear. Using nasopharyngeal carcinoma as a model, here we analyse single-cell transcriptomes of 343,829 cells from 77 biopsy and blood samples and spatially-resolved transcriptomes of 31,316 spots from 15 tumours to decipher their components and interactions with tumour cell aggregates. We identify essential cell populations in tertiary lymphoid structure, including CXCL13+ cancer-associated fibroblasts, stem-like CXCL13+CD8+ T cells, and B and T follicular helper cells. Our study shows that germinal centre reaction matures plasma cells. These plasma cells intersperse with tumour cell aggregates, promoting apoptosis of EBV-related malignant cells and enhancing immunotherapy response. CXCL13+ cancer-associated fibroblasts promote B cell adhesion and antibody production, activating CXCL13+CD8+ T cells that become exhausted in tumour cell aggregates. Tertiary lymphoid structure-related cell signatures correlate with prognosis and PD-1 blockade response, offering insights for therapeutic strategies in cancers.

Date: 2024
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DOI: 10.1038/s41467-024-52153-4

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