Global characterization of T cells in non-small-cell lung cancer by single-cell sequencing

Xinyi Guo ¹, Yuanyuan Zhang ¹, Liangtao Zheng ², Chunhong Zheng ¹, Jintao Song ³, Qiming Zhang ¹, Boxi Kang ¹, Zhouzerui Liu ¹, Liang Jin ³, Rui Xing ⁴, Ranran Gao ¹, Lei Zhang ², Minghui Dong ¹, Xueda Hu ¹, Xianwen Ren ¹, Dennis Kirchhoff ⁵, Helge Gottfried Roider ⁵, Tiansheng Yan ⁶, Zemin Zhang ⁷

Affiliations

¹ BIOPIC, Beijing Advanced Innovation Centre for Genomics, and School of Life Sciences, Peking University, Beijing, China.
² Peking-Tsinghua Centre for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing, China.
³ Department of Thoracic Surgery, Peking University Third Hospital, Beijing, China.
⁴ Peking University Cancer Hospital & Institute, Beijing, China.
⁵ Bayer AG, Berlin, Germany.
⁶ Department of Thoracic Surgery, Peking University Third Hospital, Beijing, China. yts8966@163.com.
⁷ BIOPIC, Beijing Advanced Innovation Centre for Genomics, and School of Life Sciences, Peking University, Beijing, China. zemin@pku.edu.cn.

PMID: 29942094
361 citations

Abstract

Cancer immunotherapies have shown sustained clinical responses in treating non-small-cell lung cancer1-3, but efficacy varies and depends in part on the amount and properties of tumor infiltrating lymphocytes4-6. To depict the baseline landscape of the composition, lineage and functional states of tumor infiltrating lymphocytes, here we performed deep single-cell RNA sequencing for 12,346 T cells from 14 treatment-naïve non-small-cell lung cancer patients. Combined expression and T cell antigen receptor based lineage tracking revealed a significant proportion of inter-tissue effector T cells with a highly migratory nature. As well as tumor-infiltrating CD8+ T cells undergoing exhaustion, we observed two clusters of cells exhibiting states preceding exhaustion, and a high ratio of "pre-exhausted" to exhausted T cells was associated with better prognosis of lung adenocarcinoma. Additionally, we observed further heterogeneity within the tumor regulatory T cells (Tregs), characterized by the bimodal distribution of TNFRSF9, an activation marker for antigen-specific Tregs. The gene signature of those activated tumor Tregs, which included IL1R2, correlated with poor prognosis in lung adenocarcinoma. Our study provides a new approach for patient stratification and will help further understand the functional states and dynamics of T cells in lung cancer.

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Mapping the immune environment in clear cell renal carcinoma by single-cell genomics. Nicholas Borcherding, Ajaykumar Vishwakarma, +7 authors, Weizhou Zhang. less Commun Biol, 2021 Jan 29; 4(1). PMID: 33504936 Free PMC article.
A novel CD4+ CTL subtype characterized by chemotaxis and inflammation is involved in the pathogenesis of Graves' orbitopathy. Yue Wang, Ziyi Chen, +8 authors, Bingyin Shi. less Cell Mol Immunol, 2021 Jan 31; 18(3). PMID: 33514849 Free PMC article.
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Tumour heterogeneity and intercellular networks of nasopharyngeal carcinoma at single cell resolution. Yang Liu, Shuai He, +18 authors, Jin-Xin Bei. less Nat Commun, 2021 Feb 04; 12(1). PMID: 33531485 Free PMC article.
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Regulatory T Cells Inhibit T Cell Activity by Downregulating CD137 Ligand via CD137 Trogocytosis. Khang Luu, Mugdha Vijay Patwardhan, +3 authors, Herbert Schwarz. less Cells, 2021 Feb 13; 10(2). PMID: 33572150 Free PMC article.
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A road map from single-cell transcriptome to patient classification for the immune response to trauma. Tianmeng Chen, Matthew J Delano, +13 authors, Timothy R Billiar. less JCI Insight, 2020 Dec 16; 6(2). PMID: 33320841 Free PMC article.
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Single-cell differential splicing analysis reveals high heterogeneity of liver tumor-infiltrating T cells. Shang Liu, Biaofeng Zhou, +3 authors, Liang Wu, Yan Sun, Jie Chen, Shiping Liu. less Sci Rep, 2021 Mar 07; 11(1). PMID: 33674641 Free PMC article.
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Circulating mucosal-associated invariant T cells identify patients responding to anti-PD-1 therapy. Sara De Biasi, Lara Gibellini, +16 authors, Andrea Cossarizza. less Nat Commun, 2021 Mar 17; 12(1). PMID: 33723257 Free PMC article.
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A Novel Immune-Related Prognostic Model for Response to Immunotherapy and Survival in Patients With Lung Adenocarcinoma. Yujia Zheng, He Tian, +11 authors, Jie He. less Front Cell Dev Biol, 2021 Apr 06; 9. PMID: 33816503 Free PMC article.
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Decoding Cancer Biology One Cell at a Time. L Nicolas Gonzalez Castro, Itay Tirosh, Mario L Suvà. Cancer Discov, 2021 Apr 04; 11(4). PMID: 33811126 Free PMC article. Review.
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Single-cell transcriptomics reveal the intratumoral landscape of infiltrated T-cell subpopulations in oral squamous cell carcinoma. Jingtao Chen, Jiefeng Yang, +7 authors, Ming Song. less Mol Oncol, 2021 Jan 30; 15(4). PMID: 33513276 Free PMC article.
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scSensitiveGeneDefine: sensitive gene detection in single-cell RNA sequencing data by Shannon entropy. Zechuan Chen, Zeruo Yang, +2 authors, Xiaojun Yuan, Xiaoming Zhang, Pei Hao. less BMC Bioinformatics, 2021 Apr 24; 22(1). PMID: 33888056 Free PMC article.
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Computational modeling of malignant ascites reveals CCL5-SDC4 interaction in the immune microenvironment of ovarian cancer. Soochi Kim, Youngjin Han, +8 authors, Yong Sang Song. less Mol Carcinog, 2021 Mar 16; 60(5). PMID: 33721368 Free PMC article.
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Immune Checkpoints in Pediatric Solid Tumors: Targetable Pathways for Advanced Therapeutic Purposes. Claudia Cocco, Fabio Morandi, Irma Airoldi. Cells, 2021 May 01; 10(4). PMID: 33920505 Free PMC article. Review.
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Single-Cell TCR and Transcriptome Analysis: An Indispensable Tool for Studying T-Cell Biology and Cancer Immunotherapy. Anna Pasetto, Yong-Chen Lu. Front Immunol, 2021 Jun 25; 12. PMID: 34163487 Free PMC article. Review.
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Single-cell analyses reveal suppressive tumor microenvironment of human colorectal cancer. Yan Mei, Weiwei Xiao, +15 authors, Guangshuai Jia. less Clin Transl Med, 2021 Jun 30; 11(6). PMID: 34185431 Free PMC article.
Discovering Cellular Mitochondrial Heteroplasmy Heterogeneity with Single Cell RNA and ATAC Sequencing. Aidan S Marshall, Nick S Jones. Biology (Basel), 2021 Jul 03; 10(6). PMID: 34198745 Free PMC article. Review.
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HLA-DR cancer cells expression correlates with T cell infiltration and is enriched in lung adenocarcinoma with indolent behavior. Maria-Fernanda Senosain, Yong Zou, +11 authors, Pierre P Massion. less Sci Rep, 2021 Jul 15; 11(1). PMID: 34257356 Free PMC article.
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Bulk and single-cell transcriptome profiling reveal the metabolic heterogeneity in human breast cancers. Tian-Jian Yu, Ding Ma, +6 authors, Gen-Hong Di. less Mol Ther, 2021 Mar 08; 29(7). PMID: 33677091 Free PMC article.
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Characterizing the Metabolic and Immune Landscape of Non-small Cell Lung Cancer Reveals Prognostic Biomarkers Through Omics Data Integration. Fengjiao Wang, Yuanfu Zhang, +5 authors, Peng Wang. less Front Cell Dev Biol, 2021 Jul 24; 9. PMID: 34295900 Free PMC article.
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Targeting Neoepitopes to Treat Solid Malignancies: Immunosurgery. Eric de Sousa, Joana R Lérias, +11 authors, Markus Maeurer. less Front Immunol, 2021 Aug 03; 12. PMID: 34335558 Free PMC article. Review.
Sex-Based Dimorphism of Anticancer Immune Response and Molecular Mechanisms of Immune Evasion. Fabio Conforti, Laura Pala, +25 authors, Giuseppe Giaccone. less Clin Cancer Res, 2021 May 22; 27(15). PMID: 34016641 Free PMC article.
ERO1L Is a Novel and Potential Biomarker in Lung Adenocarcinoma and Shapes the Immune-Suppressive Tumor Microenvironment. Lihui Liu, Chao Wang, +6 authors, Jie Wang. less Front Immunol, 2021 Aug 07; 12. PMID: 34354701 Free PMC article.
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A single-cell atlas of liver metastases of colorectal cancer reveals reprogramming of the tumor microenvironment in response to preoperative chemotherapy. Li-Heng Che, Jing-Wen Liu, +14 authors, Jian-Ming Li. less Cell Discov, 2021 Sep 08; 7(1). PMID: 34489408 Free PMC article.
Dissecting esophageal squamous-cell carcinoma ecosystem by single-cell transcriptomic analysis. Xiannian Zhang, Linna Peng, +22 authors, Dongxin Lin. less Nat Commun, 2021 Sep 08; 12(1). PMID: 34489433 Free PMC article.
Peripheral blood transcriptome heterogeneity and prognostic potential in lung cancer revealed by RNA-Seq. Qi Zhang, Manchao Kuang, +5 authors, Shujun Cheng. less J Cell Mol Med, 2021 Jul 22; 25(17). PMID: 34288383 Free PMC article.
Active surveillance characterizes human intratumoral T cell exhaustion. Ran You, Jordan Artichoker, +5 authors, Matthew F Krummel. less J Clin Invest, 2021 Jul 23; 131(18). PMID: 34292884 Free PMC article.
Augmented Expansion of Treg Cells From Healthy and Autoimmune Subjects via Adult Progenitor Cell Co-Culture. James L Reading, Valerie D Roobrouck, +10 authors, Timothy Tree. less Front Immunol, 2021 Sep 21; 12. PMID: 34539651 Free PMC article.
Activin-A impedes the establishment of CD4+ T cell exhaustion and enhances anti-tumor immunity in the lung. Ioannis Morianos, Aikaterini Tsitsopoulou, +8 authors, Maria Semitekolou. less J Exp Clin Cancer Res, 2021 Sep 23; 40(1). PMID: 34548096 Free PMC article.
Mechanism of action of PD-1 receptor/ligand targeted cancer immunotherapy. Jannie Borst, Julia Busselaar, Douwe M T Bosma, Ferry Ossendorp. Eur J Immunol, 2021 Jun 10; 51(8). PMID: 34106465 Free PMC article. Review.
Multimodel preclinical platform predicts clinical response of melanoma to immunotherapy. Eva Pérez-Guijarro, Howard H Yang, +22 authors, Glenn Merlino. less Nat Med, 2020 Apr 15; 26(5). PMID: 32284588 Free PMC article.
IRIS-FGM: an integrative single-cell RNA-Seq interpretation system for functional gene module analysis. Yuzhou Chang, Carter Allen, +4 authors, Qin Ma. less Bioinformatics, 2021 Feb 18;. PMID: 33595622 Free PMC article.
Identifying Lung Cancer Cell Markers with Machine Learning Methods and Single-Cell RNA-Seq Data. Guo-Hua Huang, Yu-Hang Zhang, +3 authors, Lei Chen, You Li, Tao Huang, Yu-Dong Cai. less Life (Basel), 2021 Sep 29; 11(9). PMID: 34575089 Free PMC article.
Novel Immune Infiltrating Cell Signature Based on Cell Pair Algorithm Is a Prognostic Marker in Cancer. Hao Zhang, Zeyu Wang, +5 authors, Quan Cheng. less Front Immunol, 2021 Oct 02; 12. PMID: 34594324 Free PMC article.
CD177 modulates the function and homeostasis of tumor-infiltrating regulatory T cells. Myung-Chul Kim, Nicholas Borcherding, +32 authors, Weizhou Zhang. less Nat Commun, 2021 Oct 03; 12(1). PMID: 34599187 Free PMC article.
Resolving the Spatial and Cellular Architecture of Lung Adenocarcinoma by Multiregion Single-Cell Sequencing. Ansam Sinjab, Guangchun Han, +39 authors, Humam Kadara. less Cancer Discov, 2021 May 12; 11(10). PMID: 33972311 Free PMC article.
Layilin Anchors Regulatory T Cells in Skin. Pooja Mehta, Victoire Gouirand, +20 authors, Michael D Rosenblum. less J Immunol, 2021 Sep 03; 207(7). PMID: 34470859 Free PMC article.
Tumor-Infiltrating PD-1hiCD8+-T-Cell Signature as an Effective Biomarker for Immune Checkpoint Inhibitor Therapy Response Across Multiple Cancers. Zhenyu Yang, Yulan Deng, +3 authors, Jiahan Cheng, Shiyou Wei, Hao Luo, Lunxu Liu. less Front Oncol, 2021 Oct 05; 11. PMID: 34604032 Free PMC article.
Immunotherapeutic Potential of T Memory Stem Cells. Yujie Li, Dengqiang Wu, Xuejia Yang, Sufang Zhou. Front Oncol, 2021 Oct 05; 11. PMID: 34604060 Free PMC article. Review.
Single-cell data clustering based on sparse optimization and low-rank matrix factorization. Yinlei Hu, Bin Li, Falai Chen, Kun Qu. G3 (Bethesda), 2021 Apr 01;. PMID: 33787873 Free PMC article.
Inhibition of MAN2A1 Enhances the Immune Response to Anti-PD-L1 in Human Tumors. Sailing Shi, Shengqing Gu, +11 authors, X Shirley Liu. less Clin Cancer Res, 2020 Jul 30; 26(22). PMID: 32723834 Free PMC article.
Identification of tumor microenvironment-associated immunological genes as potent prognostic markers in the cancer genome analysis project HOPE. Ryota Kondou, Yasuto Akiyama, +31 authors, Ken Yamaguchi. less Mol Clin Oncol, 2021 Oct 12; 15(5). PMID: 34631056 Free PMC article.
Single-Cell RNA-Seq of T Cells in B-ALL Patients Reveals an Exhausted Subset with Remarkable Heterogeneity. Xiaofang Wang, Yanjuan Chen, +8 authors, Yangqiu Li. less Adv Sci (Weinh), 2021 Aug 09; 8(19). PMID: 34365737 Free PMC article.
Spatial deconvolution of HER2-positive breast cancer delineates tumor-associated cell type interactions. Alma Andersson, Ludvig Larsson, +10 authors, Joakim Lundeberg. less Nat Commun, 2021 Oct 16; 12(1). PMID: 34650042 Free PMC article.
Improving CAR T-Cell Persistence. Violena Pietrobon, Lauren Anne Todd, +3 authors, Francesco Marincola. less Int J Mol Sci, 2021 Oct 14; 22(19). PMID: 34639168 Free PMC article. Review.
Comprehensive Analysis of Clinical Significance, Immune Infiltration and Biological Role of m6A Regulators in Early-Stage Lung Adenocarcinoma. Bolun Zhou, Shugeng Gao. Front Immunol, 2021 Oct 16; 12. PMID: 34650549 Free PMC article.
Dysregulation of TFH-B-TRM lymphocyte cooperation is associated with unfavorable anti-PD-1 responses in EGFR-mutant lung cancer. Jae-Won Cho, Seyeon Park, +8 authors, Hye Ryun Kim. less Nat Commun, 2021 Oct 20; 12(1). PMID: 34663810 Free PMC article.
Single-cell transcriptomic analysis of the tumor ecosystems underlying initiation and progression of papillary thyroid carcinoma. Weilin Pu, Xiao Shi, +18 authors, Yu-Long Wang. less Nat Commun, 2021 Oct 20; 12(1). PMID: 34663816 Free PMC article.
Single-cell RNA sequencing reveals distinct tumor microenvironmental patterns in lung adenocarcinoma. Philip Bischoff, Alexandra Trinks, +17 authors, Frederick Klauschen. less Oncogene, 2021 Oct 20; 40(50). PMID: 34663877 Free PMC article.
Antigen dominance hierarchies shape TCF1+ progenitor CD8 T cell phenotypes in tumors. Megan L Burger, Amanda M Cruz, +22 authors, Tyler Jacks. less Cell, 2021 Sep 18; 184(19). PMID: 34534464 Free PMC article.
Atlas of clinically distinct cell states and ecosystems across human solid tumors. Bogdan A Luca, Chloé B Steen, +10 authors, Aaron M Newman. less Cell, 2021 Oct 02; 184(21). PMID: 34597583 Free PMC article.
CD161, a promising Immune Checkpoint, correlates with Patient Prognosis: A Pan-cancer Analysis. Wenrui Ye, Cong Luo, +2 authors, Chenglong Li, Zhixiong Liu, Fangkun Liu. less J Cancer, 2021 Oct 19; 12(21). PMID: 34659549 Free PMC article.
Characterizing Intercellular Communication of Pan-Cancer Reveals SPP1+ Tumor-Associated Macrophage Expanded in Hypoxia and Promoting Cancer Malignancy Through Single-Cell RNA-Seq Data. Jinfen Wei, Zixi Chen, +4 authors, Hongli Du. less Front Cell Dev Biol, 2021 Oct 23; 9. PMID: 34676217 Free PMC article.
High-Dimensional Single-Cell Transcriptomics in Melanoma and Cancer Immunotherapy. Camelia Quek, Xinyu Bai, +2 authors, Georgina V Long, Richard A Scolyer, James S Wilmott. less Genes (Basel), 2021 Oct 24; 12(10). PMID: 34681023 Free PMC article. Review.
Emerging concepts in PD-1 checkpoint biology. Kristen E Pauken, James A Torchia, +2 authors, Apoorvi Chaudhri, Arlene H Sharpe, Gordon J Freeman. less Semin Immunol, 2021 May 20; 52. PMID: 34006473 Free PMC article. Review.
Driver gene alterations profiling of Chinese non-small cell lung cancer and the effects of co-occurring alterations on immunotherapy. Shengjie Sun, Wenjuan Du, +5 authors, Zhiyong Wu. less Cancer Med, 2021 Oct 03; 10(20). PMID: 34599863 Free PMC article.
Single-cell sequencing reveals antitumor characteristics of intratumoral immune cells in old mice. Cangang Zhang, Lei Lei, +14 authors, Baojun Zhang. less J Immunother Cancer, 2021 Oct 14; 9(10). PMID: 34642245 Free PMC article.
Rapid Identification of the Tumor-Specific Reactive TIL Repertoire via Combined Detection of CD137, TNF, and IFNγ, Following Recognition of Autologous Tumor-Antigens. Arianna Draghi, Christopher Aled Chamberlain, +16 authors, Marco Donia. less Front Immunol, 2021 Oct 29; 12. PMID: 34707600 Free PMC article.
Integrating single cell sequencing with a spatial quantitative systems pharmacology model spQSP for personalized prediction of triple-negative breast cancer immunotherapy response. Shuming Zhang, Chang Gong, +5 authors, Elana J Fertig. less Immunoinformatics (Amst), 2021 Oct 29; 1-2. PMID: 34708216 Free PMC article.
Miscell: An efficient self-supervised learning approach for dissecting single-cell transcriptome. Hongru Shen, Yang Li, +13 authors, Xiangchun Li. less iScience, 2021 Oct 30; 24(11). PMID: 34712916 Free PMC article.
Correlation of MKI67 with prognosis, immune infiltration, and T cell exhaustion in hepatocellular carcinoma. Shi-Yi Wu, Pan Liao, +4 authors, Hong-Tao Sun. less BMC Gastroenterol, 2021 Nov 03; 21(1). PMID: 34724892 Free PMC article.
Elucidation of Tumor-Stromal Heterogeneity and the Ligand-Receptor Interactome by Single-Cell Transcriptomics in Real-world Pancreatic Cancer Biopsies. Jaewon J Lee, Vincent Bernard, +12 authors, Paola A Guerrero. less Clin Cancer Res, 2021 Aug 25; 27(21). PMID: 34426439 Free PMC article.
Cyclophosphamide enhances the antitumor potency of GITR engagement by increasing oligoclonal cytotoxic T cell fitness. Daniel Hirschhorn, Allison Betof Warner, +11 authors, Jedd D Wolchok. less JCI Insight, 2021 Oct 23; 6(20). PMID: 34676831 Free PMC article.
Deciphering cell lineage specification of human lung adenocarcinoma with single-cell RNA sequencing. Zhoufeng Wang, Zhe Li, +16 authors, Weimin Li. less Nat Commun, 2021 Nov 13; 12(1). PMID: 34764257 Free PMC article.
Identifying phenotype-associated subpopulations by integrating bulk and single-cell sequencing data. Duanchen Sun, Xiangnan Guan, +9 authors, Zheng Xia. less Nat Biotechnol, 2021 Nov 13; 40(4). PMID: 34764492 Free PMC article.
Peritumoral CD90+CD73+ cells possess immunosuppressive features in human non-small cell lung cancer. Limei Wang, Haitang Yang, +10 authors, Sean R R Hall. less EBioMedicine, 2021 Nov 06; 73. PMID: 34740105 Free PMC article.
Single cell T cell landscape and T cell receptor repertoire profiling of AML in context of PD-1 blockade therapy. Hussein A Abbas, Dapeng Hao, +31 authors, Andrew Futreal. less Nat Commun, 2021 Oct 20; 12(1). PMID: 34663807 Free PMC article.
T cell dysfunction in glioblastoma: a barrier and an opportunity for the development of successful immunotherapies. Josephina A Jansen, Antonio Omuro, Liliana E Lucca. Curr Opin Neurol, 2021 Sep 28; 34(6). PMID: 34569985 Free PMC article. Review.
Dynamic regulatory networks of T cell trajectory dissect transcriptional control of T cell state transition. Min Yan, Jing Hu, +9 authors, Xia Li. less Mol Ther Nucleic Acids, 2021 Nov 18; 26. PMID: 34786214 Free PMC article.
Single-cell analysis of diverse immune phenotypes in malignant pleural effusion. Zhong-Yin Huang, Ming-Ming Shao, +9 authors, Huan-Zhong Shi. less Nat Commun, 2021 Nov 20; 12(1). PMID: 34795282 Free PMC article.
mTOR-dependent translation drives tumor infiltrating CD8+ effector and CD4+ Treg cells expansion. Benedetta De Ponte Conti, Annarita Miluzio, +3 authors, Sara Ricciardi. less Elife, 2021 Nov 18; 10. PMID: 34787568 Free PMC article.
Single-cell atlas of tumor cell evolution in response to therapy in hepatocellular carcinoma and intrahepatic cholangiocarcinoma. Lichun Ma, Limin Wang, +15 authors, Xin Wei Wang. less J Hepatol, 2021 Jul 04; 75(6). PMID: 34216724 Free PMC article.
Determinants of anti-PD-1 response and resistance in clear cell renal cell carcinoma. Lewis Au, Emine Hatipoglu, +55 authors, TRACERx Renal Consortium. less Cancer Cell, 2021 Oct 30; 39(11). PMID: 34715028 Free PMC article.
Immune ageing at single-cell resolution. Denis A Mogilenko, Irina Shchukina, Maxim N Artyomov. Nat Rev Immunol, 2021 Nov 25;. PMID: 34815556 Free PMC article. Review.
Exposure to Tobacco Smoking Induces a subset of Activated Tumor-resident Tregs in Non-Small Cell Lung Cancer. Yudi Hu, Chaoqun Xu, +6 authors, Qiyuan Li. less Transl Oncol, 2021 Nov 13; 15(1). PMID: 34768099 Free PMC article.
RNA-Binding Protein Expression Alters Upon Differentiation of Human B Cells and T Cells. Nordin D Zandhuis, Benoit P Nicolet, Monika C Wolkers. Front Immunol, 2021 Dec 07; 12. PMID: 34867946 Free PMC article.
The Emerging Interplay Between Recirculating and Tissue-Resident Memory T Cells in Cancer Immunity: Lessons Learned From PD-1/PD-L1 Blockade Therapy and Remaining Gaps. Silvia Gitto, Ambra Natalini, Fabrizio Antonangeli, Francesca Di Rosa. Front Immunol, 2021 Dec 07; 12. PMID: 34867987 Free PMC article. Review.
Identification of Immune-Related Gene Signatures in Lung Adenocarcinoma and Lung Squamous Cell Carcinoma. Na Li, Jiahong Wang, Xianquan Zhan. Front Immunol, 2021 Dec 11; 12. PMID: 34887858 Free PMC article.
Application and prospects of single cell sequencing in tumors. Ruo Han Huang, Le Xin Wang, Jing He, Wen Gao. Biomark Res, 2021 Dec 14; 9(1). PMID: 34895349 Free PMC article. Review.
Single-Cell RNA Sequencing Reveals Multiple Pathways and the Tumor Microenvironment Could Lead to Chemotherapy Resistance in Cervical Cancer. Meijia Gu, Ti He, +3 authors, Yuncong Yuan, Suling Duan, Xin Li, Chao Shen. less Front Oncol, 2021 Dec 14; 11. PMID: 34900703 Free PMC article.
Neoantigen-driven B cell and CD4 T follicular helper cell collaboration promotes anti-tumor CD8 T cell responses. Can Cui, Jiawei Wang, +13 authors, Nikhil S Joshi. less Cell, 2021 Dec 02; 184(25). PMID: 34852236 Free PMC article.
Investigating immune and non-immune cell interactions in head and neck tumors by single-cell RNA sequencing. Cornelius H L Kürten, Aditi Kulkarni, +19 authors, Robert L Ferris. less Nat Commun, 2021 Dec 19; 12(1). PMID: 34921143 Free PMC article.
Alternative Splicing Events in Immune Infiltration of Lung Adenocarcinoma. Tianpeng Huang, Wei Ye, Xuejiao Lin. Med Sci Monit, 2021 Dec 06; 27. PMID: 34864813 Free PMC article.
CREM Is Correlated With Immune-Suppressive Microenvironment and Predicts Poor Prognosis in Gastric Adenocarcinoma. Kuai Yu, Linju Kuang, +6 authors, Aiping Le. less Front Cell Dev Biol, 2021 Dec 24; 9. PMID: 34938728 Free PMC article.
Single-Cell Transcriptome Analysis Reveals RGS1 as a New Marker and Promoting Factor for T-Cell Exhaustion in Multiple Cancers. Yunmeng Bai, Meiling Hu, +2 authors, Zixi Chen, Jinfen Wei, Hongli Du. less Front Immunol, 2021 Dec 28; 12. PMID: 34956194 Free PMC article.
Distinct exhaustion features of T lymphocytes shape the tumor-immune microenvironment with therapeutic implication in patients with non-small-cell lung cancer. Chang Gon Kim, Gamin Kim, +8 authors, Hye Ryun Kim. less J Immunother Cancer, 2021 Dec 16; 9(12). PMID: 34907028 Free PMC article.
Immunosuppression and outcomes in adult patients with de novo acute myeloid leukemia with normal karyotypes. Francesca Ferraro, Christopher A Miller, +24 authors, Timothy J Ley. less Proc Natl Acad Sci U S A, 2021 Dec 01; 118(49). PMID: 34845035 Free PMC article.
Single-cell RNA sequencing reveals a pro-invasive cancer-associated fibroblast subgroup associated with poor clinical outcomes in patients with gastric cancer. Xuechun Li, Zhao Sun, +12 authors, Xiaoyue Wang. less Theranostics, 2022 Jan 04; 12(2). PMID: 34976204 Free PMC article.
Overcoming microenvironmental resistance to PD-1 blockade in genetically engineered lung cancer models. Amaia Martinez-Usatorre, Ece Kadioglu, +10 authors, Michele De Palma. less Sci Transl Med, 2021 Aug 13; 13(606). PMID: 34380768 Free PMC article.
CancerSCEM: a database of single-cell expression map across various human cancers. Jingyao Zeng, Yadong Zhang, +9 authors, Jingfa Xiao. less Nucleic Acids Res, 2021 Oct 14; 50(D1). PMID: 34643725 Free PMC article.
Single-cell analysis of human non-small cell lung cancer lesions refines tumor classification and patient stratification. Andrew M Leader, John A Grout, +30 authors, Miriam Merad. less Cancer Cell, 2021 Nov 13; 39(12). PMID: 34767762 Free PMC article.
Tumor-Associated Regulatory T Cell Expression of LAIR2 Is Prognostic in Lung Adenocarcinoma. Dalam Ly, Quan Li, +6 authors, Li Zhang. less Cancers (Basel), 2022 Jan 12; 14(1). PMID: 35008369 Free PMC article.
Harnessing Antitumor CD4+ T Cells for Cancer Immunotherapy. Myriam Ben Khelil, Yann Godet, +3 authors, Romain Loyon. less Cancers (Basel), 2022 Jan 12; 14(1). PMID: 35008422 Free PMC article. Review.
Integrated single-cell RNA sequencing analysis reveals distinct cellular and transcriptional modules associated with survival in lung cancer. Li Zhang, Yiming Zhang, +22 authors, Weimin Li. less Signal Transduct Target Ther, 2022 Jan 15; 7(1). PMID: 35027529 Free PMC article.
Tumor-Infiltrating CD4+ Central Memory T Cells Correlated with Favorable Prognosis in Oral Squamous Cell Carcinoma. Jin Wu, Tianyi Zhang, +6 authors, Tong Su. less J Inflamm Res, 2022 Jan 18; 15. PMID: 35035226 Free PMC article.
Single-Cell RNA-Seq Technologies and Computational Analysis Tools: Application in Cancer Research. Qianqian Song, Liang Liu. Methods Mol Biol, 2022 Jan 20; 2413. PMID: 35044670 Review.
Deciphering the Immune-Tumor Interplay During Early-Stage Lung Cancer Development via Single-Cell Technology. Wei-Wei Chen, Wei Liu, +5 authors, Hanjie Li. less Front Oncol, 2022 Jan 21; 11. PMID: 35047383 Free PMC article. Review.
Resolving the difference between left-sided and right-sided colorectal cancer by single-cell sequencing. Wei Guo, Cuiyu Zhang, +3 authors, Xia Wang, Dandan Dou, Dawei Chen, Jingxin Li. less JCI Insight, 2021 Nov 19; 7(1). PMID: 34793335 Free PMC article.
Prognostic Landscape of Tumor-Infiltrating T and B Cells in Human Cancer. Ming Zheng, Yi-Ming Li, +7 authors, Zhi-Nan Chen. less Front Immunol, 2022 Jan 25; 12. PMID: 35069521 Free PMC article.
Dissecting Cellular Heterogeneity Based on Network Denoising of scRNA-seq Using Local Scaling Self-Diffusion. Xin Duan, Wei Wang, +2 authors, Minghui Tang, Feng Gao, Xudong Lin. less Front Genet, 2022 Jan 28; 12. PMID: 35082838 Free PMC article.
Dissecting the heterogeneity of the microenvironment in primary and recurrent nasopharyngeal carcinomas using single-cell RNA sequencing. Wen-Sa Peng, Xin Zhou, +9 authors, Chao-Su Hu. less Oncoimmunology, 2022 Feb 01; 11(1). PMID: 35096485 Free PMC article.
Cytotoxic CD4+ T cells in cancer: Expanding the immune effector toolbox. David Y Oh, Lawrence Fong. Immunity, 2021 Dec 16; 54(12). PMID: 34910940 Free PMC article. Review.
Single-cell immune profiling reveals functional diversity of T cells in tuberculous pleural effusion. Yi Cai, Yejun Wang, +13 authors, Xinchun Chen. less J Exp Med, 2022 Jan 22; 219(3). PMID: 35061012 Free PMC article.
A novel prognostic model based on single-cell RNA sequencing data for hepatocellular carcinoma. Juan Lu, Yanfei Chen, +3 authors, Xiaoqian Zhang, Jing Guo, Kaijin Xu, Lanjuan Li. less Cancer Cell Int, 2022 Jan 27; 22(1). PMID: 35078458 Free PMC article.
Systemic Immune Dysregulation Correlates With Clinical Features of Early Non-Small Cell Lung Cancer. Zhixing Hao, Mingjie Lin, +11 authors, Pin Wu. less Front Immunol, 2022 Feb 05; 12. PMID: 35116020 Free PMC article.
Temporal single-cell tracing reveals clonal revival and expansion of precursor exhausted T cells during anti-PD-1 therapy in lung cancer. Baolin Liu, Xueda Hu, +8 authors, Zemin Zhang. less Nat Cancer, 2022 Feb 06; 3(1). PMID: 35121991
Single-Cell RNA Sequencing in Lung Cancer: Revealing Phenotype Shaping of Stromal Cells in the Microenvironment. Jianhong Zhang, Chengyang Song, Ye Tian, Xueying Yang. Front Immunol, 2022 Feb 08; 12. PMID: 35126365 Free PMC article. Review.
Genetic Alteration, Prognostic and Immunological Role of Acyl-CoA Synthetase Long-Chain Family Member 4 in a Pan-Cancer Analysis. Yongsheng Yu, Xuepu Sun, Fei Chen, Miao Liu. Front Genet, 2022 Feb 08; 13. PMID: 35126480 Free PMC article.
Single-cell RNA sequencing identifies an Il1rn+/Trem1+ macrophage subpopulation as a cellular target for mitigating the progression of thoracic aortic aneurysm and dissection. Xuanyu Liu, Wen Chen, +5 authors, Zhou Zhou. less Cell Discov, 2022 Feb 09; 8(1). PMID: 35132073 Free PMC article.
CD161 expression and regulation defines rapidly responding effector CD4+ T cells associated with improved survival in HPV16-associated tumors. Chantal L Duurland, Saskia J Santegoets, +14 authors, Sjoerd H van der Burg. less J Immunother Cancer, 2022 Jan 19; 10(1). PMID: 35039463 Free PMC article.
An NK-like CAR T cell transition in CAR T cell dysfunction. Charly R Good, M Angela Aznar, +27 authors, Carl H June. less Cell, 2021 Dec 04; 184(25). PMID: 34861191 Free PMC article.
T cell-mediated elimination of cancer cells by blocking CEACAM6-CEACAM1 interaction. Jessica Pinkert, Hans-Henning Boehm, +28 authors, Joerg Willuda. less Oncoimmunology, 2022 Feb 11; 11(1). PMID: 35141051 Free PMC article.
PD-L1+CD8+ T cells enrichment in lung cancer exerted regulatory function and tumor-promoting tolerance. Yingxia Zheng, Li Han, +10 authors, Lisong Shen. less iScience, 2022 Feb 12; 25(2). PMID: 35146396 Free PMC article.
Signatures of GVHD and relapse after posttransplant cyclophosphamide revealed by immune profiling and machine learning. Shannon R McCurdy, Vedran Radojcic, +13 authors, Leo Luznik. less Blood, 2021 Oct 18; 139(4). PMID: 34657151 Free PMC article.
Functional and molecular characterization of PD1+ tumor-infiltrating lymphocytes from lung cancer patients. Jesse J Lipp, Limei Wang, +14 authors, Sean R R Hall. less Oncoimmunology, 2022 Feb 15; 11(1). PMID: 35154905 Free PMC article.
Revealing Clonal Responses of Tumor-Reactive T-Cells Through T Cell Receptor Repertoire Analysis. Hiroyasu Aoki, Shigeyuki Shichino, Kouji Matsushima, Satoshi Ueha. Front Immunol, 2022 Feb 15; 13. PMID: 35154125 Free PMC article. Review.
Myeloid antigen-presenting cell niches sustain antitumor T cells and license PD-1 blockade via CD28 costimulation. Jaikumar Duraiswamy, Riccardo Turrini, +33 authors, George Coukos. less Cancer Cell, 2021 Nov 06; 39(12). PMID: 34739845 Free PMC article.
Identification of Immune Subtypes of Lung Squamous Cell Carcinoma by Integrative Genome-Scale Analysis. Liyuan Yin, Wen Zhang, +7 authors, Qinghua Zhou. less Front Oncol, 2022 Feb 22; 11. PMID: 35186710 Free PMC article.
Efficient recovery of potent tumour-infiltrating lymphocytes through quantitative immunomagnetic cell sorting. Zongjie Wang, Sharif Ahmed, +7 authors, Shana O Kelley. less Nat Biomed Eng, 2022 Jan 29; 6(2). PMID: 35087171
Negative Regulation of the IL-1 System by IL-1R2 and IL-1R8: Relevance in Pathophysiology and Disease. Domenico Supino, Luna Minute, +3 authors, Cecilia Garlanda. less Front Immunol, 2022 Feb 26; 13. PMID: 35211118 Free PMC article. Review.
scDPN for High-throughput Single-cell CNV Detection to Uncover Clonal Evolution During HCC Recurrence. Liang Wu, Miaomiao Jiang, +9 authors, Shiping Liu. less Genomics Proteomics Bioinformatics, 2021 Jul 20; 19(3). PMID: 34280548 Free PMC article.
Single-cell Long Non-coding RNA Landscape of T Cells in Human Cancer Immunity. Haitao Luo, Dechao Bu, +9 authors, Furong Li. less Genomics Proteomics Bioinformatics, 2021 Jul 21; 19(3). PMID: 34284134 Free PMC article.
Analysis of the tumor immune environment identifies an immune gene set-based prognostic signature in non-small cell lung cancer. Guangran Guo, Longjun Yang, +7 authors, Lanjun Zhang. less Ann Transl Med, 2022 Mar 05; 10(1). PMID: 35242860 Free PMC article.
The interaction of CD4+ helper T cells with dendritic cells shapes the tumor microenvironment and immune checkpoint blockade response. Merav Cohen, Amir Giladi, +16 authors, Ido Amit. less Nat Cancer, 2022 Mar 05; 3(3). PMID: 35241835
Clinical Prognostic Value of the PLOD Gene Family in Lung Adenocarcinoma. Yiming Meng, Jing Sun, +2 authors, Guirong Zhang, Tao Yu, Haozhe Piao. less Front Mol Biosci, 2022 Mar 11; 8. PMID: 35265665 Free PMC article.
Improving Cancer Immunotherapy: Exploring and Targeting Metabolism in Hypoxia Microenvironment. Jinfen Wei, Meiling Hu, Hongli Du. Front Immunol, 2022 Mar 15; 13. PMID: 35281061 Free PMC article. Review.
Identification of the Crucial Role of CCL22 in F. nucleatum-Related Colorectal Tumorigenesis that Correlates With Tumor Microenvironment and Immune Checkpoint Therapy. Hufei Wang, Kangjia Luo, +12 authors, Rui Huang. less Front Genet, 2022 Mar 18; 13. PMID: 35295948 Free PMC article.
Landscape of Infiltrated Immune Cell Characterization in Uveal Melanoma to Improve Immune Checkpoint Blockade Therapy. Xiaohui Lv, Min Ding, Yan Liu. Front Immunol, 2022 Mar 22; 13. PMID: 35309331 Free PMC article.
NcRNA-Mediated High Expression of HMMR as a Prognostic Biomarker Correlated With Cell Proliferation and Cell Migration in Lung Adenocarcinoma. Xiulin Jiang, Lin Tang, +5 authors, Lincan Duan. less Front Oncol, 2022 Mar 22; 12. PMID: 35311097 Free PMC article.
AhR promotes phosphorylation of ARNT isoform 1 in human T cell malignancies as a switch for optimal AhR activity. Luke A Bourner, Israel Muro, +6 authors, Casey W Wright. less Proc Natl Acad Sci U S A, 2022 Mar 16; 119(12). PMID: 35290121 Free PMC article.
Ferroptosis-associated molecular classification characterized by distinct tumor microenvironment profiles in colorectal cancer. Wenqin Luo, Weixing Dai, +10 authors, Guoxiang Cai. less Int J Biol Sci, 2022 Mar 29; 18(5). PMID: 35342352 Free PMC article.
Revealing the transcriptional heterogeneity of organ-specific metastasis in human gastric cancer using single-cell RNA Sequencing. Haiping Jiang, Dingyi Yu, +6 authors, Xiaohui Fan. less Clin Transl Med, 2022 Feb 21; 12(2). PMID: 35184420 Free PMC article.
Reconstructing codependent cellular cross-talk in lung adenocarcinoma using REMI. Alice Yu, Yuanyuan Li, +7 authors, Sylvia K Plevritis. less Sci Adv, 2022 Mar 19; 8(11). PMID: 35302849 Free PMC article.
The impact of CCR8+ regulatory T cells on cytotoxic T cell function in human lung cancer. Miya Haruna, Azumi Ueyama, +13 authors, Hisashi Wada. less Sci Rep, 2022 Apr 01; 12(1). PMID: 35354899 Free PMC article.
Characteristics and Clinical Significance of T-Cell Receptor Repertoire in Hepatocellular Carcinoma. Zifei Wang, Yu Zhong, +10 authors, Yunfan Sun. less Front Immunol, 2022 Apr 05; 13. PMID: 35371059 Free PMC article.
Single-cell RNA sequencing technologies and applications: A brief overview. Dragomirka Jovic, Xue Liang, +3 authors, Hua Zeng, Lin Lin, Fengping Xu, Yonglun Luo. less Clin Transl Med, 2022 Mar 31; 12(3). PMID: 35352511 Free PMC article. Review.
IL-9/STAT3/fatty acid oxidation-mediated lipid peroxidation contributes to Tc9 cell longevity and enhanced antitumor activity. Liuling Xiao, Xingzhe Ma, +8 authors, Qing Yi. less J Clin Invest, 2022 Feb 23; 132(7). PMID: 35192544 Free PMC article.
Comprehensive Molecular Analyses of a TNF Family-Based Gene Signature as a Potentially Novel Prognostic Biomarker for Cervical Cancer. Yan Ma, Xiaoyan Zhang, +3 authors, Jiancheng Yang, Yanping Jin, Ying Xu, Jianping Qiu. less Front Oncol, 2022 Apr 09; 12. PMID: 35392242 Free PMC article.
Single-cell RNA sequencing coupled to TCR profiling of large granular lymphocyte leukemia T cells. Shouguo Gao, Zhijie Wu, +10 authors, Neal S Young. less Nat Commun, 2022 Apr 13; 13(1). PMID: 35411048 Free PMC article.
Immune checkpoint blockade sensitivity and progression-free survival associates with baseline CD8+ T cell clone size and cytotoxicity. Robert A Watson, Orion Tong, +8 authors, Benjamin P Fairfax. less Sci Immunol, 2021 Oct 02; 6(64). PMID: 34597125 Free PMC article.
Hepatocellular carcinoma-infiltrating γδ T cells are functionally defected and allogenic Vδ2+ γδ T cell can be a promising complement. Wenjing He, Yi Hu, +10 authors, Yangzhe Wu. less Clin Transl Med, 2022 Apr 08; 12(4). PMID: 35390227 Free PMC article.
Next-generation computational tools for interrogating cancer immunity. Francesca Finotello, Dietmar Rieder, Hubert Hackl, Zlatko Trajanoski. Nat Rev Genet, 2019 Sep 14; 20(12). PMID: 31515541 Review.
Gaussian graphical model-based heterogeneity analysis via penalized fusion. Mingyang Ren, Sanguo Zhang, Qingzhao Zhang, Shuangge Ma. Biometrics, 2021 Jan 28;. PMID: 33501648 Free PMC article.
Different subpopulations of regulatory T cells in human autoimmune disease, transplantation, and tumor immunity. Zhongyi Jiang, Haitao Zhu, +4 authors, Futian Du. less MedComm (2020), 2022 Apr 28; 3(2). PMID: 35474948 Free PMC article. Review.
AXL targeting restores PD-1 blockade sensitivity of STK11/LKB1 mutant NSCLC through expansion of TCF1+ CD8 T cells. Huiyu Li, Zhida Liu, +30 authors, Rolf A Brekken. less Cell Rep Med, 2022 May 03; 3(3). PMID: 35492873 Free PMC article.
High-throughput single-сell sequencing in cancer research. Qingzhu Jia, Han Chu, +2 authors, Zheng Jin, Haixia Long, Bo Zhu. less Signal Transduct Target Ther, 2022 May 04; 7(1). PMID: 35504878 Free PMC article. Review.
Landscape of helper and regulatory antitumour CD4+ T cells in melanoma. Giacomo Oliveira, Kari Stromhaug, +24 authors, Catherine J Wu. less Nature, 2022 May 05; 605(7910). PMID: 35508657
Decoding the pathogenesis of Diamond-Blackfan anemia using single-cell RNA-seq. Bingrui Wang, Chenchen Wang, +20 authors, Lihong Shi. less Cell Discov, 2022 May 10; 8(1). PMID: 35534476 Free PMC article.
Refining colorectal cancer classification and clinical stratification through a single-cell atlas. Ateeq M Khaliq, Cihat Erdogan, +28 authors, Ashiq Masood. less Genome Biol, 2022 May 11; 23(1). PMID: 35538548 Free PMC article.
Single-cell landscape of immunocytes in patients with extrahepatic cholangiocarcinoma. Lei Xu, Yun Lu, +5 authors, Jianming Wang. less J Transl Med, 2022 May 14; 20(1). PMID: 35562760 Free PMC article.
Single-Cell RNA Sequencing Analysis for Oncogenic Mechanisms Underlying Oral Squamous Cell Carcinoma Carcinogenesis with Candida albicans Infection. Yi-Ping Hsieh, Yu-Hsueh Wu, +10 authors, Tze-Ta Huang. less Int J Mol Sci, 2022 May 15; 23(9). PMID: 35563222 Free PMC article.
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The correlation of EZH2 expression with the progression and prognosis of hepatocellular carcinoma. Shi-Yi Wu, Zhao-Yu Xie, +5 authors, Hong-Tao Sun. less BMC Immunol, 2022 Jun 07; 23(1). PMID: 35659256

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