Genome-wide analysis identifies NR4A1 as a key mediator of T cell dysfunction

Molecular and cellular insights into T cell exhaustion

Wherry, E. J., & Kurachi, M. (2015) · Nature Reviews Immunology · doi:10.1038/nri3862 · Cited by 4,652 · see citing works

Master Transcription Factors and Mediator Establish Super-Enhancers at Key Cell Identity Genes

Whyte, W. A., Orlando, D. A., Hnisz, D., Abraham, B. J., Lin, C. Y., Kagey, M. H., Rahl, P. B., Lee, T. I., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.03.035 · Cited by 4,143 · see citing works

Super-enhancers in the control of cell identity and disease

Hnisz, D., Abraham, B. J., Lee, T. I., Lau, A., Saint-André, V., Sigova, A. A., Hoke, H. A., & Young, R. A. (2013) · Cell · doi:10.1016/j.cell.2013.09.053 · Cited by 3,662 · see citing works

The B7 family revisited

Greenwald, R. J., Freeman, G. J., & Sharpe, A. H. (2005) · Annual Review of Immunology · doi:10.1146/annurev.immunol.23.021704.115611 · Cited by 2,318 · see citing works

Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation

Anderson, A. C., Joller, N., & Kuchroo, V. K. (2016) · Immunity · doi:10.1016/j.immuni.2016.05.001 · Cited by 2,096 · see citing works

Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade

Pauken, K. E., Sammons, M. A., Odorizzi, P. M., Manne, S., Godec, J., Khan, O., Drake, A. M., Chen, Z., Sen, D. R., Kurachi, M., et al. (2016) · Science · doi:10.1126/science.aaf2807 · Cited by 1,348 · see citing works

Global Mapping of H3K4me3 and H3K27me3 Reveals Specificity and Plasticity in Lineage Fate Determination of Differentiating CD4+ T Cells

Wei, G., Wei, L., Zhu, J., Zang, C., Hu-Li, J., Yao, Z., Cui, K., Kanno, Y., Roh, T.-Y., Watford, W. T., et al. (2009) · Immunity · doi:10.1016/j.immuni.2008.12.009 · Cited by 1,152 · see citing works

The epigenetic landscape of T cell exhaustion

Sen, D. R., Kaminski, J., Barnitz, R. A., Kurachi, M., Gerdemann, U., Yates, K. B., Tsao, H.-W., Godec, J., LaFleur, M. W., Brown, F. D., et al. (2016) · Science · doi:10.1126/science.aae0491 · Cited by 986 · see citing works

The Transcription Factor NFAT Promotes Exhaustion of Activated CD8 + T Cells

Martinez, G. J., Pereira, R. M., Äijö, T., Kim, E. Y., Marangoni, F., Pipkin, M. E., Togher, S., Heissmeyer, V., Zhang, Y. C., Crotty, S., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.01.006 · Cited by 857 · see citing works

Transcriptional Mechanisms Underlying Lymphocyte Tolerance

Macián, F., Garcia-Cozar, F. J., Im, S., Horton, H. F., Byrne, M. C., & Rao, A. (2002) · Cell · doi:10.1016/s0092-8674(02)00767-5 · Cited by 687 · see citing works

Tolerance and exhaustion: defining mechanisms of T cell dysfunction

Schietinger, A., & Greenberg, P. D. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.10.001 · Cited by 676 · see citing works

Molecular and Transcriptional Basis of CD4+ T Cell Dysfunction during Chronic Infection

Crawford, A., Angelosanto, J., Kao, C., Doering, T. A., Odorizzi, P. M., Barnett, B. E., & Wherry, E. J. (2014) · Immunity · doi:10.1016/j.immuni.2014.01.005 · Cited by 495 · see citing works

The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions

Chan, C. J., Martinet, L., Gilfillan, S., Souza-Fonseca-Guimarães, F., Chow, M. T., Town, L., Ritchie, D. S., Colonna, M., Andrews, D. M., & Smyth, M. J. (2014) · Nature Immunology · doi:10.1038/ni.2850 · Cited by 488 · see citing works

Egr-2 and Egr-3 are negative regulators of T cell activation

Safford, M., Collins, S. L., Lutz, M. A., Allen, A. N., Huang, C.-T., Kowalski, J., Blackford, A. L., Horton, M. R., Drake, C. G., Schwartz, R. H., et al. (2005) · Nature Immunology · doi:10.1038/ni1193 · Cited by 446 · see citing works

A Distinct Gene Module for Dysfunction Uncoupled from Activation in Tumor-Infiltrating T Cells

Singer, M., Wang, C., Cong, L., Marjanovic, N. D., Kowalczyk, M. S., Zhang, H., Nyman, J., Sakuishi, K., Kurtuluş, S., Gennert, D. G., et al. (2016) · Cell · doi:10.1016/j.cell.2016.08.052 · Cited by 414 · see citing works

Guidance of regulatory T cell development by Satb1-dependent super-enhancer establishment

Kitagawa, Y., Ohkura, N., Kidani, Y., Vandenbon, A., Hirota, K., Kawakami, R., Yasuda, K., Motooka, D., Nakamura, S., Kondo, M., et al. (2016) · Nature Immunology · doi:10.1038/ni.3646 · Cited by 372 · see citing works

Essential role of the E3 ubiquitin ligase Cbl-b in T cell anergy induction

Jeon, M.-S., Atfield, A., Venuprasad, K., Krawczyk, C., Sarao, R., Elly, C., Yang, C., Arya, S., Bachmaier, K., Su, L., et al. (2004) · Immunity · doi:10.1016/j.immuni.2004.07.013 · Cited by 348 · see citing works

BACH2 regulates CD8+ T cell differentiation by controlling access of AP-1 factors to enhancers

Roychoudhuri, R., Clever, D. C., Li, P., Wakabayashi, Y., Quinn, K. M., Klebanoff, C. A., Ji, Y., Sukumar, M., Eil, R. L., Yu, Z., et al. (2016) · Nature Immunology · doi:10.1038/ni.3441 · Cited by 317 · see citing works

Nr4a receptors are essential for thymic regulatory T cell development and immune homeostasis

Sekiya, T., Kashiwagi, I., Yoshida, R., Fukaya, T., Morita, R., Kimura, A., Ichinose, H., METZGER, D., Chambon, P., & Yoshimura, A. (2013) · Nature Immunology · doi:10.1038/ni.2520 · Cited by 314 · see citing works

Dynamic Changes in Chromatin Accessibility Occur in CD8 + T Cells Responding to Viral Infection

Scott-Browne, J. P., López-Moyado, I. F., Trifari, S., Wong, V., Chávez, L., Rao, A., & Pereira, R. M. (2016) · Immunity · doi:10.1016/j.immuni.2016.10.028 · Cited by 309 · see citing works

CD4+ T cell anergy prevents autoimmunity and generates regulatory T cell precursors

Kalekar, L. A., Schmiel, S. E., Nandiwada, S. L., Lam, W. Y., Barsness, L. O., Zhang, N., Stritesky, G. L., Malhotra, D., Pauken, K. E., Linehan, J. L., et al. (2016) · Nature Immunology · doi:10.1038/ni.3331 · Cited by 261 · see citing works

T‐cell tolerance or function is determined by combinatorial costimulatory signals

Nurieva, R., Thomas, S., Nguyen, T. D., Martín‐Orozco, N., Wang, Y., Murali‐Krishna, K., Yu, X., & Dong, C. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601146 · Cited by 245 · see citing works

Enhanced T cell responses due to diacylglycerol kinase ζ deficiency

Zhong, X., Hainey, E. A., Olenchock, B. A., Jordan, M. S., Maltzman, J. S., Nichols, K. E., Shen, H., & Koretzky, G. A. (2003) · Nature Immunology · doi:10.1038/ni958 · Cited by 221 · see citing works

Co-inhibitory Molecule B7 Superfamily Member 1 Expressed by Tumor-Infiltrating Myeloid Cells Induces Dysfunction of Anti-tumor CD8+ T Cells

Li, J., Lee, Y., Li, Y., Jiang, Y. Y., Lu, H., Zang, W., Zhao, X., Liu, L., Chen, Y., Tan, H., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.03.018 · Cited by 210 · see citing works

The E3 Ubiquitin Ligase GRAIL Regulates T Cell Tolerance and Regulatory T Cell Function by Mediating T Cell Receptor-CD3 Degradation

Nurieva, R., Zheng, S., Jin, W., Chung, Y., Zhang, Y., Martínez, G., Reynolds, J. M., Wang, S.-L., Lin, X., Sun, S., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.05.002 · Cited by 147 · see citing works

Early Growth Response Gene-2, a Zinc-Finger Transcription Factor, Is Required for Full Induction of Clonal Anergy in CD4+ T Cells

Harris, J. E., Bishop, K. D., Phillips, N. E., Mordes, J. P., Greiner, D. L., Rossini, A. A., & Czech, M. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.12.7331 · Cited by 137 · see citing works

Molecular regulation of T‐cell anergy

Zheng, Y., Zha, Y., & Gajewski, T. F. (2008) · EMBO Reports · doi:10.1038/sj.embor.7401138 · Cited by 117 · see citing works

Molecular mechanisms of T‐cell tolerance

Nurieva, R., Liu, X., & Dong, C. (2011) · Immunological Reviews · doi:10.1111/j.1600-065x.2011.01012.x · Cited by 88 · see citing works

Schnurri-3 (KRC) Interacts with c-Jun to Regulate the IL-2 Gene in T Cells

Oukka, M., Wein, M. N., & Glimcher, L. H. (2004) · The Journal of Experimental Medicine · doi:10.1084/jem.20030421 · Cited by 49 · see citing works

Cell cycle 'check points' T cell anergy

Rudd, C. E. (2006) · Nature Immunology · doi:10.1038/ni1106-1130 · Cited by 17 · see citing works

Defining ‘T cell exhaustion’

Blank, C. U., Haining, W. N., Held, W., Hogan, P. G., Kallies, A., Lugli, E., Lynn, R. C., Philip, M., Rao, A., Restifo, N. P., et al. (2019) · Nature Reviews Immunology · doi:10.1038/s41577-019-0221-9 · Cited by 1,603 · see citing works

CD8+ T cell differentiation and dysfunction in cancer

Philip, M., & Schietinger, A. (2022) · Nature Reviews Immunology · doi:10.1038/s41577-021-00574-3 · Cited by 1,052 · see citing works

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 1,060 · see citing works

Clinical implications of T cell exhaustion for cancer immunotherapy

Chow, A., Perica, K., Klebanoff, C. A., & Wolchok, J. D. (2022) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-022-00689-z · Cited by 1,044 · see citing works

c-Jun overexpression in CAR T cells induces exhaustion resistance

Lynn, R. C., Weber, E. W., Sotillo, E., Gennert, D., Xu, P., Good, Z., Anbunathan, H., Lattin, J., Jones, R., Tieu, V., et al. (2019) · Nature · doi:10.1038/s41586-019-1805-z · Cited by 891 · see citing works

TCF-1-centered transcriptional network drives an effector versus exhausted CD8 T cell-fate decision

Chen, Z., Ji, Z., Ngiow, S. F., Manne, S., Cai, Z., Huang, A. C., Johnson, J., Staupe, R. P., Bengsch, B., Xu, C., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.09.013 · Cited by 709 · see citing works

Proliferating Transitory T Cells with an Effector-like Transcriptional Signature Emerge from PD-1+ Stem-like CD8+ T Cells during Chronic Infection

Hudson, W. H., Gensheimer, J., Hashimoto, M., Wieland, A., Valanparambil, R. M., Li, P., Lin, J.-X., Konieczny, B. T., Im, S. J., Freeman, G. J., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.11.002 · Cited by 656 · see citing works

Cytokine Regulation and Function in T Cells

Dong, C. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-061020-053702 · Cited by 594 · see citing works

Metabolic and epigenetic regulation of T-cell exhaustion

Franco, F., Jaccard, A., Romero, P. J., Yu, Y.-R., & Ho, P. (2020) · Nature Metabolism · doi:10.1038/s42255-020-00280-9 · Cited by 457 · see citing works

LAG-3: from molecular functions to clinical applications

Maruhashi, T., Sugiura, D., Okazaki, I., & Okazaki, T. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-001014 · Cited by 462 · see citing works

A pan-cancer single-cell panorama of human natural killer cells

Tang, F., Li, J., Qi, L., Liu, D., Bo, Y., Qin, S., Miao, Y., Yu, K., Hou, W., Li, J., et al. (2023) · Cell · doi:10.1016/j.cell.2023.07.034 · Cited by 450 · see citing works

Single-cell sequencing links multiregional immune landscapes and tissue-resident T cells in ccRCC to tumor topology and therapy efficacy

Krishna, C., DiNatale, R. G., Kuo, F., Srivastava, R. M., Vuong, L. H., Chowell, D., Gupta, S., Vanderbilt, C., Purohit, T. A., Liu, M., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.03.007 · Cited by 427 · see citing works

T Cell Dysfunction and Exhaustion in Cancer

Zhang, Z., Liu, S., Zhang, B., Qiao, L., Zhang, Y., & Zhang, Y. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00017 · Cited by 385 · see citing works

Improving CAR-T immunotherapy: Overcoming the challenges of T cell exhaustion

Gumber, D., & Wang, L. D. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.103941 · Cited by 409 · see citing works

Tumor microenvironment remodeling after neoadjuvant immunotherapy in non-small cell lung cancer revealed by single-cell RNA sequencing

Hu, J., Zhang, L., Xia, H., Yan, Y., Zhu, X., Sun, F., Sun, L., Li, S., Li, D., Wang, J., et al. (2023) · Genome Medicine · doi:10.1186/s13073-023-01164-9 · Cited by 393 · see citing works

Transcriptional and epigenetic basis of Treg cell development and function: its genetic anomalies or variations in autoimmune diseases

Ohkura, N., & Sakaguchi, S. (2020) · Cell Research · doi:10.1038/s41422-020-0324-7 · Cited by 356 · see citing works

BATF and IRF4 cooperate to counter exhaustion in tumor-infiltrating CAR T cells

Seo, H., González‐Avalos, E., Zhang, W., Ramchandani, P., Yang, C., Lio, C. J., Rao, A., & Hogan, P. G. (2021) · Nature Immunology · doi:10.1038/s41590-021-00964-8 · Cited by 353 · see citing works

Exhausted CD8+T Cells in the Tumor Immune Microenvironment: New Pathways to Therapy

Jiang, W., He, Y., He, W., Wu, G. S., Zhou, X., Sheng, Q., Zhong, W., Lu, Y., Ding, Y., Qi, L., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.622509 · Cited by 339 · see citing works

cGAS-STING–mediated DNA sensing maintains CD8 ⁺ T cell stemness and promotes antitumor T cell therapy

Li, W., Lu, L., Lu, J., Wang, X., Yang, C., Jin, J., Wu, L., Hong, X., Li, F., Cao, D., et al. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.aay9013 · Cited by 305 · see citing works

VISTA is a checkpoint regulator for naïve T cell quiescence and peripheral tolerance

ElTanbouly, M. A., Zhao, Y., Nowak, E. C., Li, J., Schaafsma, E., Mercier, I. L., Ceeraz, S., Lines, J. L., Peng, C., Carrière, C., et al. (2020) · Science · doi:10.1126/science.aay0524 · Cited by 299 · see citing works

Second-Strand Synthesis-Based Massively Parallel scRNA-Seq Reveals Cellular States and Molecular Features of Human Inflammatory Skin Pathologies

Hughes, T. K., Wadsworth, M. H., Gierahn, T. M., Do, T. H., Weiss, D. I., Andrade, P. R., Ma, F., Silva, B. J. D. A., Shao, S., Tsoi, L. C., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.09.015 · Cited by 282 · see citing works

Rethinking peripheral T cell tolerance: checkpoints across a T cell’s journey

ElTanbouly, M. A., & Noelle, R. J. (2020) · Nature reviews. Immunology · doi:10.1038/s41577-020-00454-2 · Cited by 267 · see citing works

Androgen conspires with the CD8 + T cell exhaustion program and contributes to sex bias in cancer

Kwon, H., Schafer, J. M., Song, N., Kaneko, S., Li, A., Xiao, T., Ma, A., Allen, C., Das, K., Zhou, L., et al. (2022) · Science Immunology · doi:10.1126/sciimmunol.abq2630 · Cited by 243 · see citing works

Spatiotemporal single-cell roadmap of human skin wound healing

Liu, Z., Bian, X., Luo, L., Björklund, Å. K., Li, L., Zhang, L., Chen, Y., Guo, L. M., Gao, J., Cao, C., et al. (2024) · Cell stem cell · doi:10.1016/j.stem.2024.11.013 · Cited by 246 · see citing works

CD4 T-Cell Exhaustion: Does It Exist and What Are Its Roles in Cancer?

Hoyt-Miggelbrink, A. M., Jackson, J. D., Lorrey, S., Srinivasan, E. S., Polania, J. W., Wilkinson, D. S., & Fecci, P. E. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-21-0206 · Cited by 239 · see citing works

Low-dose decitabine priming endows CAR T cells with enhanced and persistent antitumour potential via epigenetic reprogramming

Wang, Y., Tong, C., Dai, H., Wu, Z., Han, X., Guo, Y., Chen, D., Wei, J., Ti, D., Liu, Z. Z., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20696-x · Cited by 237 · see citing works

Memory T cell, exhaustion, and tumor immunity

Ando, M., Ito, M., Srirat, T., Kondo, T., & Yoshimura, A. (2019) · Immunological Medicine · doi:10.1080/25785826.2019.1698261 · Cited by 226 · see citing works

The precursors of CD8+ tissue resident memory T cells: from lymphoid organs to infected tissues

Kok, L., Masopust, D., & Schumacher, T. N. (2022) · Nature Reviews Immunology · doi:10.1038/s41577-021-00590-3 · Cited by 230 · see citing works

TIGIT-CD226-PVR axis: advancing immune checkpoint blockade for cancer immunotherapy

Chiang, E. Y., & Mellman, I. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-004711 · Cited by 229 · see citing works

Divergent clonal differentiation trajectories of T cell exhaustion

Dániel, B., Yost, K. E., Hsiung, S., Sandor, K. D., Xia, Y., Qi, Y., Hiam-Galvez, K. J., Black, M., Raposo, C. J., Shi, Q., et al. (2022) · Nature Immunology · doi:10.1038/s41590-022-01337-5 · Cited by 226 · see citing works

Dynamics and genomic landscape of CD8+ T cells undergoing hepatic priming

Bénéchet, A. P., De Simone, G., Di Lucia, P., Cilenti, F., Barbiera, G., Le Bert, N., Fumagalli, V., Lusito, E., Moalli, F., Bianchessi, V., et al. (2019) · Nature · doi:10.1038/s41586-019-1620-6 · Cited by 222 · see citing works

Resolving the intertwining of inflammation and fibrosis in human heart failure at single-cell level

Rao, M., Wang, X., Guo, G., Wang, L., Chen, S., Yin, P., Chen, K., Chen, L., Zhang, Z., Chen, X., et al. (2021) · Basic Research in Cardiology · doi:10.1007/s00395-021-00897-1 · Cited by 214 · see citing works

BATF regulates progenitor to cytolytic effector CD8+ T cell transition during chronic viral infection

Chen, Y., Zander, R., Wu, X., Schauder, D., Kasmani, M. Y., Shen, J., Zheng, S., Burns, R., Taparowsky, E. J., & Cui, W. (2021) · Nature Immunology · doi:10.1038/s41590-021-00965-7 · Cited by 177 · see citing works

Single-cell CRISPR screens in vivo map T cell fate regulomes in cancer

Zhou, P., Shi, H., Huang, H., Sun, X., Yuan, S., Chapman, N. M., Connelly, J. P., Lim, S. A., Saravia, J., Anil, K. C., et al. (2023) · Nature · doi:10.1038/s41586-023-06733-x · Cited by 177 · see citing works

Lactic acid induces transcriptional repression of macrophage inflammatory response via histone acetylation

Shi, W., Cassmann, T. J., Bhagwate, A. V., Hitosugi, T., & Ip, W. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113746 · Cited by 181 · see citing works

Bile acid synthesis impedes tumor-specific T cell responses during liver cancer

Varanasi, S. K., Chen, D., Liu, Y., Johnson, M. A., Miller, C. M., Ganguly, S., Lande, K., LaPorta, M. A., Hoffmann, F. A., Mann, T. H., et al. (2025) · Science · doi:10.1126/science.adl4100 · Cited by 177 · see citing works

Depletion of BATF in CAR-T cells enhances antitumor activity by inducing resistance against exhaustion and formation of central memory cells

Zhang, X., Zhang, C., Qiao, M., Cheng, C., Tang, N., Lu, S., Sun, W. C., Xu, B., Cao, Y., Wei, X., et al. (2022) · Cancer Cell · doi:10.1016/j.ccell.2022.09.013 · Cited by 173 · see citing works

Counteracting CAR T cell dysfunction

Poorebrahim, M., Melief, J., de Coaña, Y. P., Wickström, S. L., Arregui, A. C., & Kiessling, R. W. (2020) · Oncogene · doi:10.1038/s41388-020-01501-x · Cited by 169 · see citing works

Single-cell transcriptome analysis reveals TOX as a promoting factor for T cell exhaustion and a predictor for anti-PD-1 responses in human cancer

Kim, K.-S., Park, S., Park, S. Y., Kim, G., Park, S. M., Cho, J.-W., Kim, D., Park, Y. M., Koh, Y. W., Kim, H. R., et al. (2020) · Genome Medicine · doi:10.1186/s13073-020-00722-9 · Cited by 158 · see citing works

Mechanisms of T-Cell Exhaustion in Pancreatic Cancer

Saka, D., Gökalp, M., Piyade, B., Çevik, N. C., Sever, E. A., Unutmaz, D., Ceyhan, G. O., Demir, İ. E., & Asimgil, H. (2020) · Cancers · doi:10.3390/cancers12082274 · Cited by 154 · see citing works

Neutralizing IL-8 potentiates immune checkpoint blockade efficacy for glioma

Liu, H., Zhao, Q., Tan, L., Wu, X., Huang, R., Zuo, Y., Chen, L., Yang, J.-G., Zhang, Z., Ruan, W., et al. (2023) · Cancer Cell · doi:10.1016/j.ccell.2023.03.004 · Cited by 148 · see citing works

Neuropilin-1: a checkpoint target with unique implications for cancer immunology and immunotherapy

Chuckran, C. A., Liu, C., Bruno, T. C., Workman, C. J., & Vignali, D. A. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-000967 · Cited by 147 · see citing works

Reinvigorating exhausted CD8 + cytotoxic T lymphocytes in the tumor microenvironment and current strategies in cancer immunotherapy

Hossain, M. A., Liu, G., Dai, B., Si, Y., Yang, Q., Wazir, J., Birnbaumer, L., & Yang, Y. (2020) · Medicinal Research Reviews · doi:10.1002/med.21727 · Cited by 136 · see citing works

The Next-Generation Immune Checkpoint LAG-3 and Its Therapeutic Potential in Oncology: Third Time’s a Charm

Lecocq, Q., Keyaerts, M., Devoogdt, N., & Breckpot, K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010075 · Cited by 133 · see citing works

Function of Nr4a Orphan Nuclear Receptors in Proliferation, Apoptosis and Fuel Utilization Across Tissues

Herring, J. A., Elison, W. S., & Tessem, J. S. (2019) · Cells · doi:10.3390/cells8111373 · Cited by 133 · see citing works

Distinct epigenetic features of tumor-reactive CD8+ T cells in colorectal cancer patients revealed by genome-wide DNA methylation analysis

Yang, R., Cheng, S., Luo, N., Gao, R., Yu, K., Kang, B., Wang, L., Zhang, Q., Fang, Q., Zhang, L., et al. (2019) · Genome biology · doi:10.1186/s13059-019-1921-y · Cited by 131 · see citing works

The Paradoxical Roles of Orphan Nuclear Receptor 4A (NR4A) in Cancer

Safe, S. H., & Karki, K. (2020) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-20-0707 · Cited by 130 · see citing works

Neuro-immune crosstalk in cancer: mechanisms and therapeutic implications

Pu, T., Sun, J., Ren, G., & Li, H. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02241-8 · Cited by 140 · see citing works

The Multifaceted Output of c-Jun Biological Activity: Focus at the Junction of CD8 T Cell Activation and Exhaustion

Papavassiliou, A. G., & Musti, A. M. (2020) · Cells · doi:10.3390/cells9112470 · Cited by 122 · see citing works

The phosphatase PAC1 acts as a T cell suppressor and attenuates host antitumor immunity

Lü, D., Liu, L., Sun, Y., Song, J., Yin, Q., Zhang, G., Fang, Q., Hu, Z., Yang, Z., Zhou, Z. C., et al. (2020) · Nature Immunology · doi:10.1038/s41590-019-0577-9 · Cited by 124 · see citing works

STAT3 regulates CD8+ T cell differentiation and functions in cancer and acute infection

Sun, Q., Zhao, X., Li, R., Liu, D., Pan, B., Xie, B., Chi, X., Cai, D., Wei, P., Xu, W., et al. (2023) · The Journal of Experimental Medicine · doi:10.1084/jem.20220686 · Cited by 124 · see citing works

Heterogeneity and fate choice: T cell exhaustion in cancer and chronic infections

Philip, M., & Schietinger, A. (2019) · Current Opinion in Immunology · doi:10.1016/j.coi.2019.04.014 · Cited by 121 · see citing works

Transcriptional regulatory network for the establishment of CD8+ T cell exhaustion

Seo, W., Jerin, C., & Nishikawa, H. (2021) · Experimental & Molecular Medicine · doi:10.1038/s12276-021-00568-0 · Cited by 118 · see citing works

Improving CAR T-Cell Persistence

Pietrobon, V., Todd, L. A., Goswami, A., Stefanson, O., Yang, Z., & Marincola, F. M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910828 · Cited by 118 · see citing works

Immune Regulatory Processes of the Tumor Microenvironment under Malignant Conditions

Pansy, K., Uhl, B., Krstić, J., Szmyra, M., Fechter, K., Santiso, A., Thüminger, L., Greinix, H., Kargl, J., Prochazka, K. T., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413311 · Cited by 110 · see citing works

Orphan Nuclear Receptor NR4A3 Promotes Vascular Calcification via Histone Lactylation

Ma, W., Jia, K., Cheng, H., Hong, X., Li, Z., Zhang, H., Xie, H., Sun, H., Yi, L., Chen, Z., et al. (2024) · Circulation Research · doi:10.1161/circresaha.123.323699 · Cited by 107 · see citing works

Role of the Orphan Nuclear Receptor NR4A Family in T-Cell Biology

Odagiu, L., May, J., Boulet, S., Baldwin, T. A., & Labrecque, N. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.624122 · Cited by 110 · see citing works

Single-cell profiling of human dura and meningioma reveals cellular meningeal landscape and insights into meningioma immune response

Wang, A. Z., Bowman-Kirigin, J. A., Desai, R. R., Kang, L., Patel, P. R., Patel, B., Khan, S. M., Bender, D. E., Marlin, M. C., Liu, J., et al. (2022) · Genome Medicine · doi:10.1186/s13073-022-01051-9 · Cited by 107 · see citing works

LSD1 inhibition sustains T cell invigoration with a durable response to PD-1 blockade

Liu, Y., Debo, B. M., Li, M., Shi, Z., Sheng, W., & Shi, Y. (2021) · Nature Communications · doi:10.1038/s41467-021-27179-7 · Cited by 103 · see citing works

The cancer-immune dialogue in the context of stress

Ma, Y., & Kroemer, G. (2023) · Nature reviews. Immunology · doi:10.1038/s41577-023-00949-8 · Cited by 110 · see citing works

Landscape of innate lymphoid cells in human head and neck cancer reveals divergent NK cell states in the tumor microenvironment

Moreno‐Nieves, U. Y., Tay, J. K., Saumyaa, S., Horowitz, N. B., Shin, J. H., Mohammad, I., Luca, B. A., Mundy, D. C., Gulati, G. S., Bedi, N., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2101169118 · Cited by 102 · see citing works

Rewiring mitochondrial metabolism to counteract exhaustion of CAR-T cells

Huang, Y., Si, X., Shao, M., Teng, X., Xiao, G., & Huang, H. (2022) · Journal of Hematology & Oncology · doi:10.1186/s13045-022-01255-x · Cited by 101 · see citing works

EpCAM-targeting CAR-T cell immunotherapy is safe and efficacious for epithelial tumors

Li, D., Guo, X., Yang, K., Yang, Y., Zhou, W., Huang, Y., Liang, X., Su, J., Jiang, L., Li, J., et al. (2023) · Science Advances · doi:10.1126/sciadv.adg9721 · Cited by 97 · see citing works

Single-Cell RNA-Seq Mapping of Human Thymopoiesis Reveals Lineage Specification Trajectories and a Commitment Spectrum in T Cell Development

Le, J., Park, J. E., Ha, V. L., Luong, A., Branciamore, S., Rodin, A. S., Gogoshin, G., Li, F., Loh, Y. E., Camacho, V., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.05.010 · Cited by 97 · see citing works

Nr4a1 and Nr4a3 reporter mice are differentially sensitive to T cell receptor signal strength and duration

Jennings, E., Elliot, T. A. E., Thawait, N., Kanabar, S., Yam-Puc, J. C., Ono, M., Toellner, K.-M., Wraith, D. C., Anderson, G., & Bending, D. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108328 · Cited by 94 · see citing works

Supervised discovery of interpretable gene programs from single-cell data

Kunes, R., Walle, T., Land, M., Nawy, T., & Pe’er, D. (2023) · Nature Biotechnology · doi:10.1038/s41587-023-01940-3 · Cited by 96 · see citing works

Nr4a1 suppresses cocaine-induced behavior via epigenetic regulation of homeostatic target genes

Carpenter, M. D., Hu, Q., Bond, A. M., Lombroso, S. I., Czarnecki, K. S., Lim, C. J., Song, H., Wimmer, M. E., Pierce, R. C., & Heller, E. A. (2020) · Nature Communications · doi:10.1038/s41467-020-14331-y · Cited by 92 · see citing works

Engineering better chimeric antigen receptor T cells

Zhang, H., Zhao, P., & Huang, H. (2020) · Experimental Hematology & Oncology · doi:10.1186/s40164-020-00190-2 · Cited by 93 · see citing works

BCL6 promotes a stem-like CD8 + T cell program in cancer via antagonizing BLIMP1

Sun, Q., Cai, D., Liu, D., Zhao, X., Li, R., Xu, W. M., Xie, B., Gou, M., Wei, K., Li, Y., et al. (2023) · Science Immunology · doi:10.1126/sciimmunol.adh1306 · Cited by 91 · see citing works

Reprogramming T cell differentiation and exhaustion in CAR-T cell therapy

Bulliard, Y., Andersson, B. S., Baysal, M. A., Damiano, J. S., & Tsimberidou, A. M. (2023) · Journal of Hematology & Oncology · doi:10.1186/s13045-023-01504-7 · Cited by 95 · see citing works

Decitabine priming increases anti–PD-1 antitumor efficacy by promoting CD8+ progenitor exhausted T cell expansion in tumor models

Li, X., Li, Y., Dong, L., Chang, Y., Zhang, X., Wang, C., Chen, M., Bo, X., Chen, H., Han, W., et al. (2023) · Journal of Clinical Investigation · doi:10.1172/jci165673 · Cited by 89 · see citing works

CAR density influences antitumoral efficacy of BCMA CAR T cells and correlates with clinical outcome

Rodriguez-Marquez, P., Calleja-Cervantes, M. E., Serrano, G., Oliver-Caldes, A., Palacios-Berraquero, M. L., Martin-Mallo, A., Calviño, C., Español-Rego, M., Ceballos, C., Lozano, T., et al. (2022) · Science Advances · doi:10.1126/sciadv.abo0514 · Cited by 109 · see citing works

NR4A nuclear receptors restrain B cell responses to antigen when second signals are absent or limiting

Tan, C., Hiwa, R., Mueller, J. L., Vykunta, V. S., Hibiya, K., Noviski, M., Huizar, J., Brooks, J. F., Garcia, J., Heyn, C., et al. (2020) · Nature Immunology · doi:10.1038/s41590-020-0765-7 · Cited by 87 · see citing works

Colorectal Cancer-Associated Immune Exhaustion Involves T and B Lymphocytes and Conventional NK Cells and Correlates With a Shorter Overall Survival

Sorrentino, C., D’Antonio, L., Fieni, C., Ciummo, S. L., & Carlo, E. D. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.778329 · Cited by 86 · see citing works

Clonal lineage tracing reveals mechanisms skewing CD8+ T cell fate decisions in chronic infection

Kasmani, M. Y., Zander, R., Chung, H. K., Chen, Y., Khatun, A., Damo, M., Topchyan, P., Johnson, K. E., Levashova, D., Burns, R., et al. (2023) · Journal of Experimental Medicine · doi:10.1084/jem.20220679 · Cited by 87 · see citing works

Regulators of CD8+ T cell exhaustion

Sun, Q., & Dong, C. (2025) · Nature reviews. Immunology · doi:10.1038/s41577-025-01221-x · Cited by 90 · see citing works

Regulatory Mechanisms of Inhibitory Immune Checkpoint Receptors Expression

Curdy, N., Lanvin, O., Laurent, C., Fournié, J., & Franchini, D. (2019) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.07.002 · Cited by 82 · see citing works

Fueling T-cell Antitumor Immunity: Amino Acid Metabolism Revisited

Han, C., Ge, M., Ho, P., & Zhang, L. (2021) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-21-0459 · Cited by 83 · see citing works

Cellular and molecular waypoints along the path of T cell exhaustion

Lan, X., Zebley, C. C., & Youngblood, B. (2023) · Science Immunology · doi:10.1126/sciimmunol.adg3868 · Cited by 84 · see citing works

Persistent STAT5 activation reprograms the epigenetic landscape in CD4 + T cells to drive polyfunctionality and antitumor immunity

Ding, Z., Shi, H., Aboelella, N. S., Fesenkova, K., Park, E.-J., Liu, Z., Pei, L., Li, J., McIndoe, R., Xu, H., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.aba5962 · Cited by 80 · see citing works

Nuclear receptors in health and disease: signaling pathways, biological functions and pharmaceutical interventions

Jin, P., Duan, X., Huang, Z., Dong, Y., Zhu, J., Guo, H., Tian, H., Zou, C., & Xie, K. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02270-3 · Cited by 86 · see citing works

Tonic-signaling chimeric antigen receptors drive human regulatory T cell exhaustion

Lamarche, C., Ward‐Hartstonge, K. A., Tian, M., Lin, D. T. S., Huang, Q. B., Brown, A., Edwards, K., Novakovsky, G., Qi, C. N., Kobor, M. S., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2219086120 · Cited by 86 · see citing works

CD8+ T cell exhaustion in the tumor microenvironment of breast cancer

Xie, H., Xi, X., Lei, T., Liu, H., & Xia, Z. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1507283 · Cited by 77 · see citing works

Integrative multi-omics approaches to explore immune cell functions: Challenges and opportunities

Wang, X., Dian, F., Yang, Y., Gimple, R. C., & Zhou, S. (2023) · iScience · doi:10.1016/j.isci.2023.106359 · Cited by 79 · see citing works

HBV-Specific CD8+ T-Cell Tolerance in the Liver

Baudi, I., Kawashima, K., & Isogawa, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.721975 · Cited by 76 · see citing works

NR4A1 regulates expression of immediate early genes, suppressing replication stress in cancer

Guo, H., Golczer, G., Wittner, B. S., Langenbucher, A., Zachariah, M. A., Dubash, T. D., Hong, X., Comaills, V., Burr, R., Ebright, R. Y., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.09.016 · Cited by 74 · see citing works

Tumor-specific cholinergic CD4+ T lymphocytes guide immunosurveillance of hepatocellular carcinoma

Zheng, C., Snow, B. E., Elia, A. J., Nechanitzky, R., Dominguez-Brauer, C., Liu, S., Tong, Y., Cox, M. A., Focaccia, E., Wakeham, A. C., et al. (2023) · Nature Cancer · doi:10.1038/s43018-023-00624-w · Cited by 75 · see citing works

Modular pooled discovery of synthetic knockin sequences to program durable cell therapies

Blaeschke, F., Chen, Y. Y., Apathy, R., Dániel, B., Chen, A. Y., Chen, P. A., Sándor, K., Zhang, W., Li, Z., Mowery, C. T., et al. (2023) · Cell · doi:10.1016/j.cell.2023.08.013 · Cited by 69 · see citing works

Developmental and cellular age direct conversion of CD4+ T cells into RORγ+ or Helios+ colon Treg cells

Pratama, A., Schnell, A., Mathis, D. J., & Benoist, C. O. (2019) · The Journal of Experimental Medicine · doi:10.1084/jem.20190428 · Cited by 70 · see citing works

Exhausted T cells and epigenetic status

Zeng, Z., Wei, F., & Ren, X. (2020) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2020.0338 · Cited by 69 · see citing works

PDL1‐positive exosomes suppress antitumor immunity by inducing tumor‐specific CD8+ T cell exhaustion during metastasis

Chen, J., Song, Y., Miao, F., Chen, G., Zhu, Y., Wu, N., Pang, L., Chen, Z., & Chen, X. (2021) · Cancer Science · doi:10.1111/cas.15033 · Cited by 69 · see citing works

Nuclear receptor Nur77: its role in chronic inflammatory diseases

Lith, S. C., & de Vries, C. J. M. (2021) · Essays in Biochemistry · doi:10.1042/ebc20210004 · Cited by 66 · see citing works

DCision-making in tumors governs T cell anti-tumor immunity

Alfei, F., Ho, P., & Lo, W. (2021) · Oncogene · doi:10.1038/s41388-021-01946-8 · Cited by 67 · see citing works

Cross-tissue multicellular coordination and its rewiring in cancer

Shi, Q., Chen, Y., Li, Y., Qin, S., Yang, Y., Gao, Y., Zhu, L., Wang, D., & Zhang, Z. (2025) · Nature · doi:10.1038/s41586-025-09053-4 · Cited by 72 · see citing works

Revitalizing T cells: breakthroughs and challenges in overcoming T cell exhaustion

Wu, Y., Wu, Y., Gao, Z., Yu, W., Zhang, L., & Zhou, F. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02327-3 · Cited by 69 · see citing works

Role of Epigenetic Regulation in Plasticity of Tumor Immune Microenvironment

Yang, Y., & Wang, Y. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.640369 · Cited by 62 · see citing works

Antigen-driven EGR2 expression is required for exhausted CD8+ T cell stability and maintenance

Wagle, M. V., Vervoort, S. J., Kelly, M. J., Byl, W. V. D., Peters, T. J., Martin, B. P., Martelotto, L. G., Nüssing, S., Ramsbottom, K. M., Torpy, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23044-9 · Cited by 59 · see citing works

T-cell exhaustion and stemness in antitumor immunity: Characteristics, mechanisms, and implications

Chi, X., Luo, S., Ye, P., Hwang, W., Cha, J., Yan, X., & Yang, W. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1104771 · Cited by 59 · see citing works

Regulation of cancer‐immunity cycle and tumor microenvironment by nanobiomaterials to enhance tumor immunotherapy

Yang, J., & Zhang, C. (2020) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1612 · Cited by 59 · see citing works

Inhibition of CD38 enzymatic activity enhances CAR-T cell immune-therapeutic efficacy by repressing glycolytic metabolism

Huang, Y., Shao, M., Teng, X., Si, X., Wu, L., Jiang, P., Liu, L., Cai, B., Wang, X., Han, Y., et al. (2024) · Cell Reports Medicine · doi:10.1016/j.xcrm.2024.101400 · Cited by 58 · see citing works

What’s driving T cell dysfunction?

Flemming, A. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0152-5 · Cited by 3 · see citing works

NR4A1 transcriptionally regulates the differentiation of stem-like CD8+ T cells in the tumor microenvironment

Hao, J., Li, R., Zhao, X., Liu, X., Chen, X., Xie, T., Li, X., Yao, C., Sun, Q., Wei, K., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114301 · Cited by 33 · see citing works

Distinct Roles of NR4A Family Members and TOX in CD8⁺ T Cell Exhaustion

Perez, K. C. (2026) · eScholarship (California Digital Library)

Reversible control of T cell exhaustion by NR4A transcription factors revealed through targeted protein degradationPreprint

Ehinger, E., Perez, K. C., Sanchez, E., Reveles, B. V., Dash, B., Arteaga-Vazquez, L. J., Johnson, E., Rao, A., & Hogan, P. G. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.02.701413 · Cited by 2 · see citing works

NR4A transcription factors limit CAR T cell function in solid tumours

Chen, J., López-Moyado, I. F., Seo, H., Lio, C.-W. J., Hempleman, L. J., Sekiya, T., Yoshimura, A., Scott-Browne, J. P., & Rao, A. (2019) · Nature · doi:10.1038/s41586-019-0985-x · Cited by 874 · see citing works