The tumor immune microenvironment of nasopharyngeal carcinoma after gemcitabine plus cisplatin treatment

Gemcitabine plus cisplatin (GP) chemotherapy is the standard of care for nasopharyngeal carcinoma (NPC). However, the mechanisms underpinning its clinical activity are unclear. Here, using single-cell RNA sequencing and T cell and B cell receptor sequencing of matched, treatment-naive and post-GP ch...

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Published inNature medicine Vol. 29; no. 6; pp. 1424 - 1436
Main Authors Lv, Jiawei, Wei, Yuan, Yin, Jian-Hua, Chen, Yu-Pei, Zhou, Guan-Qun, Wei, Chen, Liang, Xiao-Yu, Zhang, Yuan, Zhang, Cui-Juan, He, Shi-Wei, He, Qing-Mei, Huang, Zhuo-Li, Guan, Jia-Li, Shen, Jia-Yi, Li, Xiao-Min, Li, Jun-Yan, Li, Wen-Fei, Tang, Ling-Long, Mao, Yan-Ping, Guo, Rui, Sun, Rui, Zheng, Yu-Hui, Zhou, Wen-Wen, Xiong, Ke-Xu, Wang, Si-Qi, Jin, Xin, Liu, Na, Li, Gui-Bo, Kuang, Dong-Ming, Sun, Ying, Ma, Jun
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.06.2023
Nature Publishing Group
Subjects
631/250
631/67
Antitumor activity
Biomarkers
Biomedical and Life Sciences
Biomedicine
Cancer
Cancer Research
CD8 antigen
Chemotherapy
Cisplatin
Combined treatment
Cytotoxicity
Gemcitabine
Gene sequencing
Germinal centers
Health services
Immune response
Immune system
Immunotherapy
Infectious Diseases
Lymphocytes
Lymphocytes B
Lymphocytes T
Major histocompatibility complex
Metabolic Diseases
Microenvironments
Molecular Medicine
Nasopharyngeal carcinoma
Neurosciences
Patients
Throat cancer
Toll-like receptors
Tumors
Online AccessGet full text

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Abstract Gemcitabine plus cisplatin (GP) chemotherapy is the standard of care for nasopharyngeal carcinoma (NPC). However, the mechanisms underpinning its clinical activity are unclear. Here, using single-cell RNA sequencing and T cell and B cell receptor sequencing of matched, treatment-naive and post-GP chemotherapy NPC samples ( n  = 15 pairs), we show that GP chemotherapy activated an innate-like B cell (ILB)-dominant antitumor immune response. DNA fragments induced by chemotherapy activated the STING type-I-interferon-dependent pathway to increase major histocompatibility complex class I expression in cancer cells, and simultaneously induced ILB via Toll-like receptor 9 signaling. ILB further expanded follicular helper and helper type 1 T cells via the ICOSL–ICOS axis and subsequently enhanced cytotoxic T cells in tertiary lymphoid organ-like structures after chemotherapy that were deficient for germinal centers. ILB frequency was positively associated with overall and disease-free survival in a phase 3 trial of patients with NPC receiving GP chemotherapy ( NCT01872962 , n  = 139). It also served as a predictor for favorable outcomes in patients with NPC treated with GP and immunotherapy combined treatment ( n  = 380). Collectively, our study provides a high-resolution map of the tumor immune microenvironment after GP chemotherapy and uncovers a role for B cell-centered antitumor immunity. We also identify and validate ILB as a potential biomarker for GP-based treatment in NPC, which could improve patient management. Analysis of tumor samples from patients with nasopharyngeal carcinoma shows that gemcitabine plus cisplatin chemotherapy activates a unique population of innate-like B cells, which enhance the cytotoxic CD8 + T cell response and are associated with better clinical outcomes.
AbstractList Gemcitabine plus cisplatin (GP) chemotherapy is the standard of care for nasopharyngeal carcinoma (NPC). However, the mechanisms underpinning its clinical activity are unclear. Here, using single-cell RNA sequencing and T cell and B cell receptor sequencing of matched, treatment-naive and post-GP chemotherapy NPC samples (n = 15 pairs), we show that GP chemotherapy activated an innate-like B cell (ILB)-dominant antitumor immune response. DNA fragments induced by chemotherapy activated the STING type-I-interferon-dependent pathway to increase major histocompatibility complex class I expression in cancer cells, and simultaneously induced ILB via Toll-like receptor 9 signaling. ILB further expanded follicular helper and helper type 1 T cells via the ICOSL–ICOS axis and subsequently enhanced cytotoxic T cells in tertiary lymphoid organ-like structures after chemotherapy that were deficient for germinal centers. ILB frequency was positively associated with overall and disease-free survival in a phase 3 trial of patients with NPC receiving GP chemotherapy (NCT01872962, n = 139). It also served as a predictor for favorable outcomes in patients with NPC treated with GP and immunotherapy combined treatment (n = 380). Collectively, our study provides a high-resolution map of the tumor immune microenvironment after GP chemotherapy and uncovers a role for B cell-centered antitumor immunity. We also identify and validate ILB as a potential biomarker for GP-based treatment in NPC, which could improve patient management.Analysis of tumor samples from patients with nasopharyngeal carcinoma shows that gemcitabine plus cisplatin chemotherapy activates a unique population of innate-like B cells, which enhance the cytotoxic CD8+ T cell response and are associated with better clinical outcomes.
Gemcitabine plus cisplatin (GP) chemotherapy is the standard of care for nasopharyngeal carcinoma (NPC). However, the mechanisms underpinning its clinical activity are unclear. Here, using single-cell RNA sequencing and T cell and B cell receptor sequencing of matched, treatment-naive and post-GP chemotherapy NPC samples (n = 15 pairs), we show that GP chemotherapy activated an innate-like B cell (ILB)-dominant antitumor immune response. DNA fragments induced by chemotherapy activated the STING type-I-interferon-dependent pathway to increase major histocompatibility complex class I expression in cancer cells, and simultaneously induced ILB via Toll-like receptor 9 signaling. ILB further expanded follicular helper and helper type 1 T cells via the ICOSL-ICOS axis and subsequently enhanced cytotoxic T cells in tertiary lymphoid organ-like structures after chemotherapy that were deficient for germinal centers. ILB frequency was positively associated with overall and disease-free survival in a phase 3 trial of patients with NPC receiving GP chemotherapy ( NCT01872962 , n = 139). It also served as a predictor for favorable outcomes in patients with NPC treated with GP and immunotherapy combined treatment (n = 380). Collectively, our study provides a high-resolution map of the tumor immune microenvironment after GP chemotherapy and uncovers a role for B cell-centered antitumor immunity. We also identify and validate ILB as a potential biomarker for GP-based treatment in NPC, which could improve patient management.Gemcitabine plus cisplatin (GP) chemotherapy is the standard of care for nasopharyngeal carcinoma (NPC). However, the mechanisms underpinning its clinical activity are unclear. Here, using single-cell RNA sequencing and T cell and B cell receptor sequencing of matched, treatment-naive and post-GP chemotherapy NPC samples (n = 15 pairs), we show that GP chemotherapy activated an innate-like B cell (ILB)-dominant antitumor immune response. DNA fragments induced by chemotherapy activated the STING type-I-interferon-dependent pathway to increase major histocompatibility complex class I expression in cancer cells, and simultaneously induced ILB via Toll-like receptor 9 signaling. ILB further expanded follicular helper and helper type 1 T cells via the ICOSL-ICOS axis and subsequently enhanced cytotoxic T cells in tertiary lymphoid organ-like structures after chemotherapy that were deficient for germinal centers. ILB frequency was positively associated with overall and disease-free survival in a phase 3 trial of patients with NPC receiving GP chemotherapy ( NCT01872962 , n = 139). It also served as a predictor for favorable outcomes in patients with NPC treated with GP and immunotherapy combined treatment (n = 380). Collectively, our study provides a high-resolution map of the tumor immune microenvironment after GP chemotherapy and uncovers a role for B cell-centered antitumor immunity. We also identify and validate ILB as a potential biomarker for GP-based treatment in NPC, which could improve patient management.
Gemcitabine plus cisplatin (GP) chemotherapy is the standard of care for nasopharyngeal carcinoma (NPC). However, the mechanisms underpinning its clinical activity are unclear. Here, using single-cell RNA sequencing and T cell and B cell receptor sequencing of matched, treatment-naive and post-GP chemotherapy NPC samples ( n  = 15 pairs), we show that GP chemotherapy activated an innate-like B cell (ILB)-dominant antitumor immune response. DNA fragments induced by chemotherapy activated the STING type-I-interferon-dependent pathway to increase major histocompatibility complex class I expression in cancer cells, and simultaneously induced ILB via Toll-like receptor 9 signaling. ILB further expanded follicular helper and helper type 1 T cells via the ICOSL–ICOS axis and subsequently enhanced cytotoxic T cells in tertiary lymphoid organ-like structures after chemotherapy that were deficient for germinal centers. ILB frequency was positively associated with overall and disease-free survival in a phase 3 trial of patients with NPC receiving GP chemotherapy ( NCT01872962 , n  = 139). It also served as a predictor for favorable outcomes in patients with NPC treated with GP and immunotherapy combined treatment ( n  = 380). Collectively, our study provides a high-resolution map of the tumor immune microenvironment after GP chemotherapy and uncovers a role for B cell-centered antitumor immunity. We also identify and validate ILB as a potential biomarker for GP-based treatment in NPC, which could improve patient management. Analysis of tumor samples from patients with nasopharyngeal carcinoma shows that gemcitabine plus cisplatin chemotherapy activates a unique population of innate-like B cells, which enhance the cytotoxic CD8 + T cell response and are associated with better clinical outcomes.
Gemcitabine plus cisplatin (GP) chemotherapy is the standard of care for nasopharyngeal carcinoma (NPC). However, the mechanisms underpinning its clinical activity are unclear. Here, using single-cell RNA sequencing and T cell and B cell receptor sequencing of matched, treatment-naive and post-GP chemotherapy NPC samples (n = 15 pairs), we show that GP chemotherapy activated an innate-like B cell (ILB)-dominant antitumor immune response. DNA fragments induced by chemotherapy activated the STING type-I-interferon-dependent pathway to increase major histocompatibility complex class I expression in cancer cells, and simultaneously induced ILB via Toll-like receptor 9 signaling. ILB further expanded follicular helper and helper type 1 T cells via the ICOSL-ICOS axis and subsequently enhanced cytotoxic T cells in tertiary lymphoid organ-like structures after chemotherapy that were deficient for germinal centers. ILB frequency was positively associated with overall and disease-free survival in a phase 3 trial of patients with NPC receiving GP chemotherapy ( NCT01872962 , n = 139). It also served as a predictor for favorable outcomes in patients with NPC treated with GP and immunotherapy combined treatment (n = 380). Collectively, our study provides a high-resolution map of the tumor immune microenvironment after GP chemotherapy and uncovers a role for B cell-centered antitumor immunity. We also identify and validate ILB as a potential biomarker for GP-based treatment in NPC, which could improve patient management.
Author Sun, Ying
Mao, Yan-Ping
Zhou, Guan-Qun
Li, Wen-Fei
Wang, Si-Qi
Lv, Jiawei
Jin, Xin
Yin, Jian-Hua
Wei, Yuan
Zhou, Wen-Wen
Li, Gui-Bo
Zhang, Cui-Juan
Shen, Jia-Yi
Kuang, Dong-Ming
Huang, Zhuo-Li
Zheng, Yu-Hui
Wei, Chen
Liang, Xiao-Yu
Guo, Rui
He, Qing-Mei
Guan, Jia-Li
Chen, Yu-Pei
Sun, Rui
Li, Jun-Yan
Li, Xiao-Min
Liu, Na
Xiong, Ke-Xu
Zhang, Yuan
Ma, Jun
He, Shi-Wei
Tang, Ling-Long
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37280275$$D View this record in MEDLINE/PubMed
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2023. The Author(s), under exclusive licence to Springer Nature America, Inc.
Copyright_xml – notice: The Author(s), under exclusive licence to Springer Nature America, Inc. 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
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Snippet Gemcitabine plus cisplatin (GP) chemotherapy is the standard of care for nasopharyngeal carcinoma (NPC). However, the mechanisms underpinning its clinical...
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pubmed
crossref
springer
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Index Database
Enrichment Source
Publisher
StartPage 1424
SubjectTerms 631/250
631/67
Antitumor activity
Biomarkers
Biomedical and Life Sciences
Biomedicine
Cancer
Cancer Research
CD8 antigen
Chemotherapy
Cisplatin
Combined treatment
Cytotoxicity
Gemcitabine
Gene sequencing
Germinal centers
Health services
Immune response
Immune system
Immunotherapy
Infectious Diseases
Lymphocytes
Lymphocytes B
Lymphocytes T
Major histocompatibility complex
Metabolic Diseases
Microenvironments
Molecular Medicine
Nasopharyngeal carcinoma
Neurosciences
Patients
Throat cancer
Toll-like receptors
Tumors
Title The tumor immune microenvironment of nasopharyngeal carcinoma after gemcitabine plus cisplatin treatment
URI https://link.springer.com/article/10.1038/s41591-023-02369-6
https://www.ncbi.nlm.nih.gov/pubmed/37280275
https://www.proquest.com/docview/2828554297
https://www.proquest.com/docview/2823497398
Volume 29
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