Precursors of human CD4 + cytotoxic T lymphocytes identified by single-cell transcriptome analysis

Patil, Veena S.; Madrigal, Ariel; Schmiedel, Benjamin J.; Clarke, James; O’Rourke, Patrick; de Silva, Aruna D.; Harris, Eva; Peters, Bjoern; Seumois, Gregory; Weiskopf, Daniela; Sette, Alessandro; Vijayanand, Pandurangan

doi:10.1126/sciimmunol.aan8664

Cited by 263T-cell and B-cell ImmunologyImmunotherapy and Immune ResponsesSingle-cell and spatial transcriptomics

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Precursors of human CD4 + cytotoxic T lymphocytes identified by single-cell transcriptome analysis

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Patil, Veena S., Madrigal, Ariel, Schmiedel, Benjamin J., Clarke, James, O’Rourke, Patrick, de Silva, Aruna D., Harris, Eva, Peters, Bjoern, Seumois, Gregory, Weiskopf, Daniela, Sette, Alessandro, Vijayanand, Pandurangan·2018·Science Immunology

DOI 10.1126/sciimmunol.aan8664PMC PMC5931334

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Abstract

Human CD4 + cytotoxic T lymphocytes that play a vital role in antiviral immunity are highly heterogeneous.

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The cytotoxic subset overexpressed Eomes, Gzmk, and Ctla2a, genes commonly associated with CD8 T cells and previously described in viral infection and cancer as CD4 cytotoxic T cells.
“cells overexpressing genes such as Eomes, Gzmk, and Ctla2a, which are commonly associated with CD8 T cells (denoted cytotoxic) and were previously described in the context of viral infection and cancer as CD4 cytotoxic T cells (32–34).”
From Aging promotes reorganization of the CD4 T cell landscape toward extreme regulatory and effector phenotypes (2019) · cites this paper as [32]

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Neoantigen vaccine generates intratumoral T cell responses in phase Ib glioblastoma trial
Keskin, D. B., Anandappa, A. J., Sun, J., Tirosh, I., Mathewson, N. D., Li, S., Oliveira, G., Giobbie-Hurder, A., Felt, K., Gjini, E., et al. (2019) · Nature · doi:10.1038/s41586-018-0792-9 · Cited by 1,432
Single-cell RNA-seq highlights intra-tumoral heterogeneity and malignant progression in pancreatic ductal adenocarcinoma
Peng, J., Sun, B.-F., Chen, C.-Y., Zhou, J.-Y., Chen, Y.-S., Chen, H., Liu, L., Huang, D., Jiang, J., Cui, G.-S., et al. (2019) · Cell Research · doi:10.1038/s41422-019-0195-y · Cited by 1,321
Transfer learning enables predictions in network biology
Theodoris, C. V., Xiao, L., Chopra, A., Chaffin, M. D., Al Sayed, Z. R., Hill, M. C., Mantineo, H., Brydon, E. M., Zeng, Z., Liu, X. S., et al. (2023) · Nature · doi:10.1038/s41586-023-06139-9 · Cited by 1,193
T cells in health and disease
Sun, L., Su, Y., Jiao, A., Wang, X., & Zhang, B. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01471-y · Cited by 1,119
A cell atlas of human thymic development defines T cell repertoire formation
Park, J.-E., Botting, R. A., Conde, C. D., Popescu, D.-M., Lavaert, M., Kunz, D. J., Goh, I., Stephenson, E., Ragazzini, R., Tuck, E. J., et al. (2020) · Science · doi:10.1126/science.aay3224 · Cited by 725
Intratumoral CD4+ T Cells Mediate Anti-tumor Cytotoxicity in Human Bladder Cancer
Oh, D. Y., Kwek, S. S., Raju, S. S., Li, T., McCarthy, E., Chow, E., Aran, D., Ilano, A., Pai, C.-C. S., Rancan, C., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.017 · Cited by 734
A genome-wide transcriptomic analysis of protein-coding genes in human blood cells
Uhlen, M., Karlsson, M. J., Zhong, W., Tebani, A., Pou, C., Mikes, J., Lakshmikanth, T., Forsström, B., Edfors, F., Odeberg, J., et al. (2019) · Science · doi:10.1126/science.aax9198 · Cited by 594
Imbalance of Regulatory and Cytotoxic SARS-CoV-2-Reactive CD4+ T Cells in COVID-19
Meckiff, B. J., Ramírez-Suástegui, C., Fajardo, V., Chee, S., Kusnadi, A., Simon, H. A., Eschweiler, S., Grifoni, A., Pelosi, E., Weiskopf, D., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.001 · Cited by 581
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Cytotoxic CD4+ T cells in cancer: Expanding the immune effector toolbox
Oh, D. Y., & Fong, L. (2021) · Immunity · doi:10.1016/j.immuni.2021.11.015 · Cited by 467
“While all populations expressed GZMA and other granule-associated proteins such as GNLY and NKG7, distinct states co-expressed either GZMB or GZMK, and PRF1 was more predominantly coexpressed with GZMB.”
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NOX4 inhibition potentiates immunotherapy by overcoming cancer-associated fibroblast-mediated CD8 T-cell exclusion from tumors
Ford, K., Hanley, C. J., Mellone, M., Szyndralewiez, C., Heitz, F., Wiesel, P., Wood, O., Machado, M., Lopez, M.-A., Ganesan, A.-P., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-3158 · Cited by 411
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Integrated single cell analysis of blood and cerebrospinal fluid leukocytes in multiple sclerosis
Schafflick, D., Xu, C. A., Hartlehnert, M., Cole, M. B., Schulte‐Mecklenbeck, A., Lautwein, T., Wolbert, J., Heming, M., Meuth, S. G., Kuhlmann, T., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-14118-w · Cited by 452
IgG4-related disease: an update on pathophysiology and implications for clinical care
Perugino, C. A., & Stone, J. H. (2020) · Nature Reviews Rheumatology · doi:10.1038/s41584-020-0500-7 · Cited by 435
Aging promotes reorganization of the CD4 T cell landscape toward extreme regulatory and effector phenotypes
Elyahu, Y., Hekselman, I., Eizenberg-Magar, I., Berner, O., Strominger, I., Schiller, M., Mittal, K., Nemirovsky, A., Eremenko, E., Vital, A., et al. (2019) · Science Advances · doi:10.1126/sciadv.aaw8330 · Cited by 324
Single-cell transcriptomics reveals expansion of cytotoxic CD4 T cells in supercentenarians
Hashimoto, K., Kouno, T., Ikawa, T., Hayatsu, N., Miyajima, Y., Yabukami, H., Terooatea, T., Sasaki, T., Suzuki, T., Valentine, M., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1907883116 · Cited by 343
NKG2A Blockade Potentiates CD8 T Cell Immunity Induced by Cancer Vaccines
van Montfoort, N., Borst, L., Korrer, M. J., Sluijter, M., Marijt, K. A., Santegoets, S. J. A. M., van Ham, V. J., Ehsan, I., Charoentong, P., André, P., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.028 · Cited by 334
Tumor-specific cytolytic CD4 T cells mediate immunity against human cancer
Cachot, A., Bilous, M., Liu, Y., Li, X., Saillard, M., Cenerenti, M., Rockinger, G. A., Wyss, T., Guillaume, P., Schmidt, J., et al. (2021) · Science Advances · doi:10.1126/sciadv.abe3348 · Cited by 340
Correlates of protection against SARS ‐ CoV ‐2 infection and COVID‐19 disease
Goldblatt, D., Alter, G., Crotty, S., & Plotkin, S. A. (2022) · Immunological Reviews · doi:10.1111/imr.13091 · Cited by 298
Long-term perturbation of the peripheral immune system months after SARS-CoV-2 infection
Ryan, F. J., Hope, C. M., Masavuli, M. G., Lynn, M. A., Mekonnen, Z. A., Yeow, A. E. L., García-Valtanen, P., Al-Delfi, Z., Gummow, J., Ferguson, C. C., et al. (2022) · BMC Medicine · doi:10.1186/s12916-021-02228-6 · Cited by 285
A CD4+ T cell population expanded in lupus blood provides B cell help through interleukin-10 and succinate
Caielli, S., Veiga, D. T., Balasubramanian, P., Athale, S., Domic, B., Murat, E., Banchereau, R., Xu, Z., Chandra, M., Chung, C.-H., et al. (2019) · Nature Medicine · doi:10.1038/s41591-018-0254-9 · Cited by 263
Single-cell transcriptomic analysis of tissue-resident memory T cells in human lung cancer
Clarke, J. D., Panwar, B., Madrigal, A., Singh, D. K., Gujar, R., Wood, O., Chee, S., Eschweiler, S., King, E. V., Awad, A. S., et al. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20190249 · Cited by 253
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Effector Functions of CD4+ T Cells at the Site of Local Autoimmune Inflammation—Lessons From Rheumatoid Arthritis
Chemin, K., Gerstner, C., & Malmström, V. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00353 · Cited by 243
Personalized neoantigen vaccine NEO-PV-01 with chemotherapy and anti-PD-1 as first-line treatment for non-squamous non-small cell lung cancer
Awad, M. M., Govindan, R., Balogh, K. N., Spigel, D. R., Garon, E. B., Bushway, M. E., Poran, A., Sheen, J. H., Kohler, V. L., Esaulova, E., et al. (2022) · Cancer Cell · doi:10.1016/j.ccell.2022.08.003 · Cited by 244
Single-cell transcriptomic analysis of allergen-specific T cells in allergy and asthma
Seumois, G., Ramírez-Suástegui, C., Schmiedel, B. J., Liang, S. Y., Peters, B., Sette, A., & Vijayanand, P. (2020) · Science Immunology · doi:10.1126/sciimmunol.aba6087 · Cited by 212
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M1 hot tumor-associated macrophages boost tissue-resident memory T cells infiltration and survival in human lung cancer
Garrido-Martin, E. M., Mellows, T., Clarke, J. D., Ganesan, A.-P., Wood, O., Cazaly, A. M., Seumois, G., Chee, S., Alzetani, A., King, E. V., et al. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-000778 · Cited by 202
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Cytotoxic CD4+ T lymphocytes may induce endothelial cell apoptosis in systemic sclerosis
Maehara, T., Kaneko, N., Perugino, C. A., Mattoo, H., Kers, J., Allard‐Chamard, H., Mahajan, V. S., Liu, H., Murphy, S. J. H., Ghebremichael, M. S., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci131700 · Cited by 202
Neurological Manifestations of COVID-19 Feature T Cell Exhaustion and Dedifferentiated Monocytes in Cerebrospinal Fluid
Heming, M., Li, X., Räuber, S. J., Mausberg, A. K., Börsch, A., Hartlehnert, M., Singhal, A., Lu, I., Fleischer, M., Szepanowski, F., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.12.011 · Cited by 180
Mixed-effects association of single cells identifies an expanded effector CD4 + T cell subset in rheumatoid arthritis
Fonseka, C. Y., Rao, D. A., Teslovich, N. C., Korsunsky, I., Hannes, S. K., Slowikowski, K., Gurish, M. F., Donlin, L. T., Lederer, J. A., Weinblatt, M. E., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aaq0305 · Cited by 172
The Era of Cytotoxic CD4 T Cells
Cenerenti, M., Saillard, M., Romero, P. J., & Jandus, C. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.867189 · Cited by 184
Human T Cell Response to Dengue Virus Infection
Tian, Y., Grifoni, A., Sette, A., & Weiskopf, D. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02125 · Cited by 160
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CD4+ T cells in antitumor immunity
Montauti, E. I., Oh, D. Y., & Fong, L. H. (2024) · Trends in cancer · doi:10.1016/j.trecan.2024.07.009 · Cited by 148
High Prevalence of MERS-CoV Infection in Camel Workers in Saudi Arabia
Alshukairi, A. N., Zheng, J. H., Zhao, J., Nehdi, A., Baharoon, S. A., Layqah, L. A., Bokhari, A. A., Johani, S. M. A., Samman, N., Boudjelal, M., et al. (2018) · mBio · doi:10.1128/mbio.01985-18 · Cited by 136
Single-Cell RNA Sequencing Reveals the Expansion of Cytotoxic CD4+ T Lymphocytes and a Landscape of Immune Cells in Primary Sjögren’s Syndrome
Hong, X., Meng, S., Tang, D., Wang, T., Ding, L., Yu, H., Li, H., Liu, D. J., Dai, Y., & Yang, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.594658 · Cited by 128
Colorectal Cancer Immune Infiltrates: Significance in Patient Prognosis and Immunotherapeutic Efficacy
Guo, L., Wang, C., Qiu, X., Pu, X., & Chang, P. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01052 · Cited by 122
Intratumoral follicular regulatory T cells curtail anti-PD-1 treatment efficacy
Eschweiler, S., Clarke, J. D., Ramírez-Suástegui, C., Panwar, B., Madrigal, A., Chee, S., Karydis, I., Woo, E. B. C., Alzetani, A., Elsheikh, S. E., et al. (2021) · Nature Immunology · doi:10.1038/s41590-021-00958-6 · Cited by 119
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Long-term skin-resident memory T cells proliferate in situ and are involved in human graft-versus-host disease
Strobl, J., Pandey, R. V., Krausgruber, T., Bayer, N., Kleißl, L., Reininger, B., Vieyra-Garcia, P. A., Wolf, P., Jentus, M. M., Mitterbauer, M., et al. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.abb7028 · Cited by 117
The Single-Cell Phenotypic Identity of Human CD8+ and CD4+ T Cells
Brummelman, J., Pilipow, K., & Lugli, E. (2018) · International review of cytology · doi:10.1016/bs.ircmb.2018.05.007 · Cited by 113
CTLs heterogeneity and plasticity: implications for cancer immunotherapy
Peng, S., Lin, A., Jiang, A., Zhang, C., Zhang, J., Cheng, Q., Luo, P., & Bai, Y. (2024) · Molecular Cancer · doi:10.1186/s12943-024-01972-6 · Cited by 114
An atlas of immune cell exhaustion in HIV-infected individuals revealed by single-cell transcriptomics
Wang, S., Zhang, Q., Hui, H., Agrawal, K., Karris, M., & Rana, T. M. (2020) · Emerging Microbes & Infections · doi:10.1080/22221751.2020.1826361 · Cited by 103
CD4+ and CD8+ cytotoxic T lymphocytes may induce mesenchymal cell apoptosis in IgG4-related disease
Perugino, C. A., Kaneko, N., Maehara, T., Mattoo, H., Kers, J., Allard‐Chamard, H., Mahajan, V. S., Liu, H., Della‐Torre, E., Murphy, S. J. H., et al. (2020) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2020.05.022 · Cited by 104
The Identity of Human Tissue-Emigrant CD8+ T Cells
Buggert, M., Vella, L. A., Nguyen, S., Wu, V. H., Chen, Z., Sekine, T., Perez‐Potti, A., Maldini, C. R., Manne, S., Darko, S. W., et al. (2020) · Cell · doi:10.1016/j.cell.2020.11.019 · Cited by 105
Integrated Multi-Omics Landscape of Liver Metastases
Yang, S., Qian, L., Li, Z., Li, Y., Bai, J., Zheng, B. J., Chen, K., Qiu, X., Cai, G., Wang, S., et al. (2022) · Gastroenterology · doi:10.1053/j.gastro.2022.11.029 · Cited by 102
Single-cell eQTL analysis of activated T cell subsets reveals activation and cell type–dependent effects of disease-risk variants
Schmiedel, B. J., González-Colín, C., Fajardo, V., Rocha, J., Madrigal, A., Ramírez-Suástegui, C., Bhattacharyya, S., Simon, H. A., Greenbaum, J., Peters, B., et al. (2022) · Science Immunology · doi:10.1126/sciimmunol.abm2508 · Cited by 98
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Intermittent PI3Kδ inhibition sustains anti-tumour immunity and curbs irAEs
Eschweiler, S., Ramírez-Suástegui, C., Li, Y., King, E. V., Chudley, L., Thomas, J., Wood, O., Witzleben, A. V., Jeffrey, D. L., McCann, K. J., et al. (2022) · Nature · doi:10.1038/s41586-022-04685-2 · Cited by 101
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Extremely Differentiated T Cell Subsets Contribute to Tissue Deterioration During Aging
Soto‐Heredero, G., Heras, M. M. G. D. L., Escrig-Larena, J. I., & Mittelbrunn, M. (2023) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101721-064501 · Cited by 96
The T cell differentiation landscape is shaped by tumour mutations in lung cancer
Ghorani, E., Reading, J. L., Henry, J. Y., de Massy, M. R., Rosenthal, R., Turati, V. A., Joshi, K., Furness, A. J. S., Aïssa, A. B., Saini, S. K., et al. (2020) · Nature Cancer · doi:10.1038/s43018-020-0066-y · Cited by 95
Human antimicrobial cytotoxic T lymphocytes, defined by NK receptors and antimicrobial proteins, kill intracellular bacteria
Balin, S. J., Pellegrini, M. A., Klechevsky, E., Won, S. T., Weiss, D. I., Choi, A. W., Hakimian, J. K., Lu, J. N., Ochoa, M. T., Bloom, B. R., et al. (2018) · Science Immunology · doi:10.1126/sciimmunol.aat7668 · Cited by 95
Clonally expanded CD8 T cells characterize amyotrophic lateral sclerosis-4
Campisi, L., Chizari, S., Ho, J., Gromova, A., Arnold, F. J., Mosca, L., Mei, X., Fstkchyan, Y. S., Torre, D., Beharry, C., et al. (2022) · Nature · doi:10.1038/s41586-022-04844-5 · Cited by 91
Thymus involution sets the clock of the aging T-cell landscape: Implications for declined immunity and tissue repair
Elyahu, Y., & Monsonego, A. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101231 · Cited by 92
TIM3+ TRBV11-2 T cells and IFNγ signature in patrolling monocytes and CD16+ NK cells delineate MIS-C
Hoste, L., Roels, L., Naesens, L., Bosteels, V., Vanhee, S., Dupont, S., Bosteels, C., Browaeys, R., Vandamme, N., Verstaen, K., et al. (2021) · The Journal of Experimental Medicine · doi:10.1084/jem.20211381 · Cited by 85
In vivo genome-wide CRISPR screens identify SOCS1 as intrinsic checkpoint of CD4 + T H 1 cell response
Galy, A. S. D., Menegatti, S., Fuentealba, J. R., Perrin, L., Lucibello, F., Helft, J., Darbois, A., Saitakis, M., Tosello, J., Rookhuizen, D. C., et al. (2021) · Science Immunology · doi:10.1126/sciimmunol.abe8219 · Cited by 79
Systems Immunology: Learning the Rules of the Immune System
Villani, A., Sarkizova, S., & Hacohen, N. (2018) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042617-053035 · Cited by 89
Single-cell transcriptome profiling and chromatin accessibility reveal an exhausted regulatory CD4+ T cell subset in systemic lupus erythematosus
Guo, C., Liu, Q., Zong, D., Zhang, W., Zuo, Z.-Q., Yu, Q., Sha, Q., Zhu, L., Gao, X., Fang, J., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111606 · Cited by 86
A novel CD4+ CTL subtype characterized by chemotaxis and inflammation is involved in the pathogenesis of Graves’ orbitopathy
Wang, Y., Chen, Z., Wang, T., Guo, H., Liu, Y., Dang, N., Hu, S., Wu, L., Zhang, C., Ye, K., et al. (2021) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-00615-2 · Cited by 82
Single-cell analysis pinpoints distinct populations of cytotoxic CD4 + T cells and an IL-10 + CD109 + T H 2 cell population in nasal polyps
Ma, J., Tibbitt, C. A., Georén, S. K., Christian, M., Murrell, B., Cardell, L., Bachert, C., & Coquet, J. M. (2021) · Science Immunology · doi:10.1126/sciimmunol.abg6356 · Cited by 80
Immunology in the Era of Single-Cell Technologies
Efremova, M., Vento‐Tormo, R., Park, J.-E., Teichmann, S. A., & James, K. R. (2020) · Annual Review of Immunology · doi:10.1146/annurev-immunol-090419-020340 · Cited by 80
Epitope prediction and identification- adaptive T cell responses in humans
Sidney, J., Peters, B., & Sette, A. (2020) · Seminars in Immunology · doi:10.1016/j.smim.2020.101418 · Cited by 83
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CD4+ Cytotoxic T cells – Phenotype, Function and Transcriptional Networks Controlling Their Differentiation Pathways
Preglej, T., & Ellmeier, W. (2022) · Immunology Letters · doi:10.1016/j.imlet.2022.05.001 · Cited by 85
Bifunctional cancer cell–based vaccine concomitantly drives direct tumor killing and antitumor immunity
Chen, K., Reinshagen, C., van Schaik, T., Rossignoli, F., Borges, P., Mendonca, N. C., Abdi, R., Simon, B. G., Reardon, D. A., Wakimoto, H., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.abo4778 · Cited by 81
Systems vaccinology and big data in the vaccine development chain
Raeven, R. H. M., van Riet, E., Meiring, H. D., Metz, B., & Kersten, G. F. A. (2018) · Immunology · doi:10.1111/imm.13012 · Cited by 79
Heterogeneity of T Cells in Atherosclerosis Defined by Single-Cell RNA-Sequencing and Cytometry by Time of Flight
Winkels, H., & Wolf, D. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.120.312137 · Cited by 70
Reinvestigation of Classic T Cell Subsets and Identification of Novel Cell Subpopulations by Single-Cell RNA Sequencing
Wang, X., Shen, X., Chen, S., Liu, H., Hong, N., Zhong, H., Chen, X. X., & Jin, W. (2021) · The Journal of Immunology · doi:10.4049/jimmunol.2100581 · Cited by 67
Primary and secondary anti-viral response captured by the dynamics and phenotype of individual T cell clones
Minervina, A. A., Pogorelyy, M. V., Komech, E. A., Карнаухов, В. К., Bächer, P., Rosati, E., Franke, A., Chudakov, D. M., Mamedov, I. Z., Lebedev, Y. B., et al. (2020) · eLife · doi:10.7554/elife.53704 · Cited by 68
Spectrum of mutational signatures in T-cell lymphoma reveals a key role for UV radiation in cutaneous T-cell lymphoma
Jones, C. L., Degasperi, A., Grandi, V., Amarante, T. D., Ambrose, J. C., Arumugam, P., Baple, E. L., Bleda, M., Boardman-Pretty, F., Boissiere, J. M., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-83352-4 · Cited by 65
CD4+ T Cells: Multitasking Cells in the Duty of Cancer Immunotherapy
Richardson, J. R., Schöllhorn, A., Gouttefangeas, C., & Schuhmacher, J. (2021) · Cancers · doi:10.3390/cancers13040596 · Cited by 66
Cross-Reactive T Cell Immunity to Dengue and Zika Viruses: New Insights Into Vaccine Development
Ngono, A. E., & Shresta, S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01316 · Cited by 63
Differential Pathogenic Th17 Profile in Mesenteric Lymph Nodes of Crohn's Disease and Ulcerative Colitis Patients
Bsat, M., Chapuy, L., Rubio, M., Wassef, R., Richard, C. S., Schwenter, F., Loungnarath, R., Soucy, G., Mehta, H., & Sarfati, M. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01177 · Cited by 60
Primary EBV Infection Induces an Acute Wave of Activated Antigen-Specific Cytotoxic CD4+ T Cells
Meckiff, B. J., Ladell, K., McLaren, J. E., Ryan, G. B., Leese, A. M., James, E. A., Price, D. A., & Long, H. M. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1900377 · Cited by 64
The outstanding antitumor capacity of CD4+ T helper lymphocytes
Li, T., Wu, B., Yang, T., Zhang, L., & Jin, K. (2020) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2020.188439 · Cited by 60
Protective heterologous T cell immunity in COVID-19 induced by the trivalent MMR and Tdap vaccine antigens
Mysore, V., Culleré, X., Settles, M. L., Ji, X., Kattan, M. W., Desjardins, M., Durbin-Johnson, B. P., Gilboa, T., Baden, L. R., Walt, D. R., et al. (2021) · Med · doi:10.1016/j.medj.2021.08.004 · Cited by 55
Extracellular traps released by antimicrobial TH17 cells contribute to host defense
Agak, G. W., Mouton, A., Teles, R. M. B., Weston, T. A., Morselli, M., Andrade, P. R., Pellegrini, M. A., & Modlin, R. L. (2020) · Journal of Clinical Investigation · doi:10.1172/jci141594 · Cited by 56
Modulating the quantity of HIV Env-specific CD4 T cell help promotes rare B cell responses in germinal centers
Lee, J. H., Hu, J. K., Georgeson, E., Nakao, C., Gröschel, B., Dileepan, T., Jenkins, M. K., Seumois, G., Vijayanand, P., Schief, W. R., et al. (2020) · The Journal of Experimental Medicine · doi:10.1084/jem.20201254 · Cited by 51
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EOMES and IL-10 regulate antitumor activity of T regulatory type 1 CD4+ T cells in chronic lymphocytic leukemia
Roessner, P. M., Cid, L. L., Lupar, E., Roider, T., Bordas, M., Schifflers, C., Arseni, L., Gaupel, A., Kilpert, F., Krötschel, M., et al. (2021) · Leukemia · doi:10.1038/s41375-021-01136-1 · Cited by 59
Aging weakens Th17 cell pathogenicity and ameliorates experimental autoimmune uveitis in mice
Li, H., Zhu, L., Wang, R., Xie, L., Ren, J., Ma, S., Zhang, W., Liu, X., Huang, Z., Chen, B., et al. (2021) · Protein & Cell · doi:10.1007/s13238-021-00882-3 · Cited by 53
Post-translational modifications such as citrullination are excellent targets for cancer therapy
Brentville, V. A., Vankemmelbeke, M., Metheringham, R. L., & Durrant, L. G. (2020) · Seminars in Immunology · doi:10.1016/j.smim.2020.101393 · Cited by 53
Dengue-specific CD8+ T cell subsets display specialized transcriptomic and TCR profiles
Tian, Y., Babor, M., Lane, J., Seumois, G., Liang, S. Y., Goonawardhana, N. D. S., Silva, A. D. D., Phillips, E. J., Mallal, S. A., Antunes, R. D. S., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci123726 · Cited by 53
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Transcriptional analysis of peripheral memory T cells reveals Parkinson’s disease-specific gene signatures
Dhanwani, R., Lima-Júnior, J. R., Sethi, A., Pham, J. W., Williams, G. P., Frazier, A., Xu, Y., Amara, A. W., Standaert, D. G., Goldman, J. G., et al. (2022) · npj Parkinson s Disease · doi:10.1038/s41531-022-00282-2 · Cited by 53
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An Efficient Method to Generate Monoclonal Antibodies from Human B Cells
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Dental niche cells directly contribute to tooth reconstitution and morphogenesis
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Authors: Patil, V. S., Madrigal, A., Schmiedel, B. J., Clarke, J., O’Rourke, P., de Silva, A. D., Harris, E., Peters, B., Seumois, G., Weiskopf, D., Sette, A., & Vijayanand, P.
Affiliations: La Jolla Institute for Immunology (US)
Division of Vaccine Discovery, La Jolla Institute for Allergy and Immunology, La Jolla, CA 92037, USA.
University of California, Berkeley (US)
Corresponding author: Vijayanand, Pandurangan
ORCID: Patil, Veena S.
Madrigal, Ariel
Schmiedel, Benjamin J.
Clarke, James
O’Rourke, Patrick
de Silva, Aruna D.
Harris, Eva
Peters, Bjoern
Seumois, Gregory
Weiskopf, Daniela
Sette, Alessandro
Vijayanand, Pandurangan
Venue: Science Immunology
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2018-01-26
Volume: 3
Issue: 19
ISSN: 2470-9468 (ISSN-L)
DOI: 10.1126/sciimmunol.aan8664
PMC: PMC5931334
OpenAlex: W2783929588
Cited by: 262
References: 74
Citations by year: 2026: 23 · 2025: 26 · 2024: 25 · 2023: 21 · 2022: 37 · 2021: 42 · 2020: 46 · 2019: 24 · 2018: 18
FWCI: 13.96
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Science Immunology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
ePrints Soton (University of Southampton) (acceptedVersion)
Funders: NIH Office of the Director (award317527, U19AI118626, award317529, U19AI118610, award360682, R01HL114093, award360683, R24AI108564)
William K. Bowes Jr Foundation (award317531)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
Keywords: cytotoxic CD4+ T cells, T cell differentiation, TCR clonotypes, CD127, single-cell transcriptomics, T cell subsets
MeSH terms: Humans, Immunologic Memory, Leukocytes, Mononuclear, Lymphocyte Activation, Receptors, Antigen, T-Cell, T-Lymphocytes, Cytotoxic, CD4-Positive T-Lymphocytes, Gene Expression Profiling, Single-Cell Analysis, Transcriptome

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Precursors of human CD4 + cytotoxic T lymphocytes identified by single-cell transcriptome analysis

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