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A pan-cancer single-cell panorama of human natural killer cells
Open accessAbstract
dendritic cells, appear to mediate the regulation of NK cell anti-tumor immunity. Our study provides insights into NK-cell-based cancer immunity and highlights potential clinical utilities of NK cell subsets as therapeutic targets.
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“We then identified activated regulons for both tumor-infiltrating CD56brightCD16lo and CD56dim CD16hi NK cell subsets using SCENIC.49 Importantly, the tumor-enriched c6-DNAJB1 subset exhibitedmuch higher expression of transcription factors such as KLF6 and EGR3, which are associated with the inhibition of cytotoxicity…”
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“In particular, the CD56dim CD16hi subset c4-NFKBIA exhibited a relatively high inflammatory score among all NK cell subsets, predominantly expressing CCL3, CCL4, and CCL4L2, indicating their ability to recruit other immune cells such as T cells.36 Recent studies have associated the recruitment of type 1 conventional d…”
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BackgroundPan-cancer single-cell landscape of tumor-infiltrating T cells
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“of NK cells and utilized for NK cell infusion and in vitro propagation.(4,68) By contrast, TIGIT contributes to suppressing NK cellmediated immune responses as an inhibitory receptor.”
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“By contrast, TIGIT contributes to suppressing NK cellmediated immune responses as an inhibitory receptor.(28,69,70) Furthermore, in TCGA datasets, the abundance of LAMP3 DCs was correlated with CD56CD16 NK cells (Figures 6I, S6I, and S6J).”
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“Of particular note is the remarkable clinical success achieved by chimeric antigen receptor (CAR)NK cell therapies in lymphoma, myeloma, and leukemia.(5,6) However, NK-cell-based therapies are hindered in solid tumors partly due to the incomplete understanding of tumor-infiltrating NK cells, especially their infiltrat…”
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“Additionally, preferential expression of these markers in NK cell populations of particular tissues has been reported.(16) These motivated us to discover robust NK cell residency markers from the pan-cancer perspective in an unbiased manner.”
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“However, NK-cell-based therapies are hindered in solid tumors partly due to the incomplete understanding of tumor-infiltrating NK cells, especially their infiltration to tumor, phenotypic heterogeneities, and dysregulation within the TME.(7,8) In humans, NK cells can be subdivided into two major groups, CD56CD16 and C…”
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“of NK cells and utilized for NK cell infusion and in vitro propagation.(4,68) By contrast, TIGIT contributes to suppressing NK cellmediated immune responses as an inhibitory receptor.”
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Innate lymphoid cells and cancer
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Transcriptomic profiles of neoantigen-reactive T cells in human gastrointestinal cancers
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Minimal PD-1 expression in mouse and human NK cells under diverse conditions
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“In addition, although the inhibitory roles of TIGIT and TIM3 have been established in tumor-infiltrating NK cells,(27,28) it is still controversial whether other immune checkpoints, such as PD-1 and CTLA4, play the same role or are even expressed in those cells.(28,29) Furthermore, NK cells are sensitive to immunosupp…”
BackgroundNatural Killer Cells Suppress T Cell-Associated Tumor Immune Evasion
Freeman, A. J., Vervoort, S. J., Ramsbottom, K. M., Kelly, M. J., Michie, J., Pijpers, L., Johnstone, R. W., Kearney, C. J., & Oliaro, J. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.08.017 · Cited by 140
Discovery of specialized NK cell populations infiltrating human melanoma metastases.
de Andrade, L. D., Lu, Y.-H., Luoma, A. M., Ito, Y., Pan, D., Pyrdol, J. W., Yoon, C. H., Yuan, G.-C., & Wucherpfennig, K. (2019) · JCI Insight · doi:10.1172/jci.insight.133103 · Cited by 124 · cited 1×
“For example, we have identified a CD160HSPA1A liver-resident NK cell subset specifically enriched in hepatocellular carcinoma (HCC),(14) and others have reported specialized NK cell populations infiltrated in melanoma with regional variation.(15) In parallel, the distribution and function of human NK cell populations…”
Adaptive NK Cells Resist Regulatory T-cell Suppression Driven by IL37
Sarhan, D., Hippen, K. L., Lemire, A. M., Hying, S., Luo, X., Lenvik, T. R., Curtsinger, J., Davis, Z., Zhang, B., Cooley, S., et al. (2018) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-17-0498 · Cited by 120 · cited 1×
“External factors from other cell populations in the TME including myeloid-derived suppressor cells, Tregs, and tumor-associated macrophages can also suppress the anti-tumor function of NK cells.(4,77) Our analyses and experimental evidence support myeloid cells as core mediators of NK cells.”
BackgroundRhys, H. I., Dell’Accio, F., Pitzalis, C., Moore, A., Norling, L. V., & Perretti, M. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.02.003 · Cited by 115
Huang, D., Chen, X., Zeng, X., Lao, L., Li, J., Xing, Y., Lu, Y., Ouyang, Q., Chen, J., Yang, L., et al. (2021) · Nature Immunology · doi:10.1038/s41590-021-00939-9 · Cited by 114
Bade, B., Boettcher, H. E., Lohrmann, J., Hink-Schauer, C., Bratke, K., Jenne, D. E., Virchow, J. C., Jr., & Luttmann, W. (2005) · International Immunology · doi:10.1093/intimm/dxh320 · Cited by 91 · cited 1×
“CD56CD16 NK cells exhibited high expression of cytotoxic effector genes including perforin (PRF1) and most granzyme (GZMB, GZMA, and GZMH) except GZMK, which was instead exclusively expressed in CD56CD16 NK cells.(35) CD56CD16 NK cells expressed various cytokine genes such as IL18.”
BackgroundHuman AML activates the aryl hydrocarbon receptor pathway to impair NK cell development and function
Scoville, S. D., Nalin, A. P., Chen, L., Chen, L., Zhang, M. H., McConnell, K. K., Casas, S. B., Ernst, G., Traboulsi, A. A.-R., Hashi, N. J., et al. (2018) · Blood · doi:10.1182/blood-2018-03-838474 · Cited by 89 · cited 2×
“Such hypomaturation stage of NK cells has been associated with the reduction of overall survival and relapse-free survival of patients with AML.43,44 Compared with other NK cell populations, these CD56brightCD16hi cells exhibited distinctive phenotypic and functional shifts in terms of their extremely low activating a…”
ResultAlterations of NK Cell Phenotype in the Disease Course of Multiple Myeloma
Pazina, T., Macfarlane, A. W., Bernabei, L. L., Dulaimi, E., Kotcher, R. E., Yam, C., Bezman, N., Robbins, M. D. H., Ross, E. A., Campbell, K. S., et al. (2021) · Cancers · doi:10.3390/cancers13020226 · Cited by 73
Chrétien, A.-S., Fauriat, C., Orlanducci, F., Galseran, C., Rey, J., Bouvier, G., Gautherot, E., Granjeaud, S., Hamel‐Broza, J., Demerle, C., et al. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00573 · Cited by 69 · cited 2×
“Such hypomaturation stage of NK cells has been associated with the reduction of overall survival and relapse-free survival of patients with AML.43,44 Compared with other NK cell populations, these CD56brightCD16hi cells exhibited distinctive phenotypic and functional shifts in terms of their extremely low activating a…”
ResultCosta-García, M., Ataya, M., Moraru, M., Vilches, C., López‐Botet, M., & Muntasell, A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00687 · Cited by 64
T-Cell Ig and ITIM Domain Regulates Natural Killer Cell Activation in Murine Acute Viral Hepatitis
Bi, J., Zhang, Q., Liang, D., Xiong, L., Wei, H., Sun, R., & Tian, Z. (2013) · Hepatology · doi:10.1002/hep.26968 · Cited by 59 · cited 1×
“By contrast, TIGIT contributes to suppressing NK cellmediated immune responses as an inhibitory receptor.(28,69,70) Furthermore, in TCGA datasets, the abundance of LAMP3 DCs was correlated with CD56CD16 NK cells (Figures 6I, S6I, and S6J).”
BackgroundGuo, C., Wu, M., Huang, B., Zhao, R., Jin, L., Fu, B., Wang, P., Wang, D., Zheng, M., Fang, J., et al. (2022) · Genome Medicine · doi:10.1186/s13073-022-01049-3 · Cited by 55
Ziblat, A., Iraolagoitia, X. L. R., Núñez, S. Y., Torres, N. I., Secchiari, F., Sierra, J. M., Spallanzani, R. G., Rovegno, A. R., Secin, F. P., Fuertes, M. B., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.681615 · Cited by 33
Impaired intratumoral natural killer cell function in head and neck carcinoma
Mele, D., Pessino, G., Trisolini, G., Luchena, A., Benazzo, M., Morbini, P., Mantovani, S., Oliviero, B., Mondelli, M. U., & Varchetta, S. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.997806 · Cited by 24
Le, D. T., Huynh, T. R., Burt, B. M., Buren, G. V., Abeynaike, S. A., Zalfa, C., Nikzad, R., Kheradmand, F., Tyner, J. J., & Paust, S. (2021) · JCI Insight · doi:10.1172/jci.insight.140116 · Cited by 23
Wang, H., Zhang, X., Wald, D. N., Gong, S., Wang, W., & Wang, J. (2022) · Blood · doi:10.1182/blood-2022-168947 · Cited by 3
Cited by
Sorted by citations
Marín, D., Li, Y., Başar, R., Rafei, H., Daher, M., Dou, J., Mohanty, V., Dede, M., Nieto, Y. L., Uprety, N., et al. (2024) · Nature Medicine · doi:10.1038/s41591-023-02785-8 · Cited by 567
“This pattern mirrors the stress response observed in T cells in the context of immunotherapy resistance 34 and the poor cytotoxicity seen in tumor-associated NK cells in a recent pan-cancer single-cell atlas of human NK cells 28 .”
BackgroundMethodVivier, É., Rebuffet, L., Narni-Mancinelli, É., Cornen, S., Igarashi, R., & Fantin, V. R. (2024) · Nature · doi:10.1038/s41586-023-06945-1 · Cited by 496
“…cells characterized by reduced cytotoxicity and high expression of stress-associated proteins ( DNAJB1 and HSP gene family), inhibitory MHC-class-I-specific receptors (members of the KIR family) and several transcription factors that control the fitness of NK cells such as NR4A1, EGR3 and KLF6 29 .”
High-dimensional single-cell analysis of human natural killer cell heterogeneity
Rebuffet, L., Melsen, J. E., Escalière, B., Basurto-Lozada, D., Bhandoola, A., Björkström, N. K., Bryceson, Y. T., Castriconi, R., Cichocki, F. M., Colonna, M., et al. (2024) · Nature Immunology · doi:10.1038/s41590-024-01883-0 · Cited by 325
“We then confirmed the robustness of the classification of human blood NK cells into the NK1, NK2 and NK3 clusters by applying the derived transcriptional signatures to blood NK cells from other available datasets 11 (Extended Data Figs.”
Metabolic reprogramming and therapeutic resistance in primary and metastatic breast cancer
Liu, S., Zhang, X., Wang, W., Li, X., Sun, X., Zhao, Y., Wang, Q., Li, Y., Hu, F., & Ren, H. (2024) · Molecular Cancer · doi:10.1186/s12943-024-02165-x · Cited by 300
Pan-cancer single-cell dissection reveals phenotypically distinct B cell subtypes
Yu, Y., Chen, X., Pan, J., Ning, H., Zhang, Y., Bo, Y., Ren, X., Li, J., Qin, S., Wang, D., et al. (2024) · Cell · doi:10.1016/j.cell.2024.06.038 · Cited by 223
Metadata
- Authors
- Tang, F., Li, J., Qi, L., Liu, D., Bo, Y., Qin, S., Miao, Y., Yu, K., Hou, W., Li, J., Peng, J., Tian, Z., Zhu, L., Peng, H., Wang, D., & Zhang, Z.
- Affiliations
- Peking University (CN)
- Capital Medical University (CN)
- Shenzhen Bay Laboratory (CN)
- University of Science and Technology of China (CN)
- Corresponding author
- Zhu, Linnan
- Peng, Hui
- Wang, Dongfang
- Zhang, Zemin
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2023-09
- Volume
- 186
- Issue
- 19
- Pages
- 4235-4251.e20
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W4386034505
- Cited by
- 450
- References
- 91
- Citations by year
- 2026: 136 · 2025: 181 · 2024: 120 · 2023: 11
- FWCI
- 50.09
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Greater South Information System
- Funders
- National Natural Science Foundation of China (31991171, 592259205, 62203019, 81988101, 91959000, 92159305)
- Peking University
- Beijing Municipal Science and Technology Commission, Adminitrative Commission of Zhongguancun Science Park (Z221100007022002)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Keywords
- natural killer cells, pan-cancer, single-cell transcriptomics, NK cell subsets, cancer immunotherapy, dendritic cells, antitumor immunity
- MeSH terms
- Single-Cell Gene Expression Analysis, Dendritic Cells, Humans, Immunity, Innate, Immunotherapy, Killer Cells, Natural, Neoplasms, Myeloid Cells, Tumor Microenvironment
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