The DOI matches its Crossref record; 56 of the 56 references it cites were found in a registry or an index.
Molecular Signature of CD8+ T Cell Exhaustion during Chronic Viral Infection
Open accessAbstract
Chronic viral infections often result in T cell exhaustion. To determine the molecular signature of exhaustion, we compared the gene-expression profiles of dysfunctional lymphocytic choriomeningitis virus (LCMV)-specific CD8(+) T cells from chronic infection to functional LCMV-specific effector and memory CD8(+) T cells generated after acute infection. These data showed that exhausted CD8(+) T cells: (1) overexpressed several inhibitory receptors, including PD-1, (2) had major changes in T cell receptor and cytokine signaling pathways, (3) displayed altered expression of genes involved in chemotaxis, adhesion, and migration, (4) expressed a distinct set of transcription factors, and (5) had profound metabolic and bioenergetic deficiencies. T cell exhaustion was progressive, and gene-expression profiling indicated that T cell exhaustion and anergy were distinct processes. Thus, functional exhaustion is probably due to both active suppression and passive defects in signaling and metabolism. These results provide a framework for designing rational immunotherapies during chronic infections.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“T cells acquiring multiple inhibitory surface molecules in persistent disease settings such as chronic infection [37,38] and malignancies [30,**39,40], which effectively prevent T cell activation.”
From T cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment (2013) · cites this paper as [37]
In the citing paper
“Secretion of TNF-α in some populations of cells is reduced because of the contemporary arrest of p38-MAPK and PD-1 pathways.”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [194]
In the citing paper
“However, the telomerase activity in CD8+/CD45RA+ T cells is improved by blocking only the p38 pathway but not the PD-1 signaling, indicating that non-overlapping signaling pathways are involved (193, 194).”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [194]
In the citing paper
“In these cells that present characteristics of immune senescence (decreased proliferation, lower telomerase activity, and increased presence of DNA damage), the simultaneous blockade of both p38-MAPK and PD-1 signaling supports their proliferation, both in young and in older human beings.”
From Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention (2019) · cites this paper as [194]
Citations
Cites
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625
Restoring function in exhausted CD8 T cells during chronic viral infection
Barber, D. L., Wherry, E. J., Masopust, D., Zhu, B., Allison, J. P., Sharpe, A. H., Freeman, G. J., & Ahmed, R. (2005) · Nature · doi:10.1038/nature04444 · Cited by 4,057
Self-citationPD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression
Day, C. L., Kaufmann, D. E., Kiepiela, P., Brown, J. A., Moodley, E. S., Reddy, S., Mackey, E. W., Miller, J. D., Leslie, A. J., DePierres, C., et al. (2006) · Nature · doi:10.1038/nature05115 · Cited by 2,680
Self-citationGreenwald, 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
Viral Immune Evasion Due to Persistence of Activated T Cells Without Effector Function
Zajac, A. J., Blattman, J. N., Murali-Krishna, K., Sourdive, D. J. D., Suresh, M., Altman, J. D., & Ahmed, R. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.12.2205 · Cited by 1,978
Self-citationCTLA-4 and PD-1 Receptors Inhibit T-Cell Activation by Distinct Mechanisms
Parry, R. V., Chemnitz, J. M., Frauwirth, K. A., Lanfranco, A. R., Braunstein, I., Kobayashi, S. V., Linsley, P. S., Thompson, C. B., & Riley, J. L. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.21.9543-9553.2005 · Cited by 1,931
Joshi, N. S., Cui, W., Chandele, A., Lee, H. K., Urso, D. R., Hagman, J., Gapin, L., & Kaech, S. M. (2007) · Immunity · doi:10.1016/j.immuni.2007.07.010 · Cited by 1,861
Self-citationWherry, E. J., Blattman, J. N., Murali‐Krishna, K., der Most, R. G. V., & Ahmed, R. (2003) · Journal of Virology · doi:10.1128/jvi.77.8.4911-4927.2003 · Cited by 1,645
Self-citationLanier, L. L. (1998) · Annual Review of Immunology · doi:10.1146/annurev.immunol.16.1.359 · Cited by 1,641
Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction
Trautmann, L., Janbazian, L., Chomont, N., Said, E. A., Gimmig, S., Bessette, B., Boulassel, M.-R., Delwart, E., Sepulveda, H., Balderas, R. S., et al. (2006) · Nature Medicine · doi:10.1038/nm1482 · Cited by 1,565
Flagged first, then by citations
Cited by
Sorted by citations
Items 501–600 of 1,007
Zamora, A. E., Crawford, J. C., Allen, E. K., Guo, X.-Z. J., Bakke, J., Carter, R. A., Abdelsamed, H. A., Moustaki, A., Li, Y., Chang, T., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aat8549 · Cited by 93
Macrophage-Mediated Subversion of Anti-Tumour Immunity
Quaranta, V., & Schmid, M. C. (2019) · Cells · doi:10.3390/cells8070747 · Cited by 95
Dubrot, J., Lane-Reticker, S. K., Kessler, E., Ayer, A., Mishra, G., Wolfe, C. H., Zimmer, M. D., Du, P. P., Mahapatra, A., Ockerman, K. M., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.01.001 · Cited by 87
Self-citationXia, Y., Sándor, K., Pai, J. A., Dániel, B., Raju, S., Wu, R., Hsiung, S., Qi, Y., Tenzin, Y., Okamoto, M., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.05.003 · Cited by 91
Gu, X., Wei, H., Suo, C., Shen, S., Zhu, C., Chen, L., Yan, K., Li, Z., Bian, Z., Zhang, P., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-43988-4 · Cited by 95
Ha, S., West, E. E., Araki, K., Smith, K. A., & Ahmed, R. (2008) · Immunological Reviews · doi:10.1111/j.1600-065x.2008.00638.x · Cited by 90
Self-citationKim, K. H., Kim, H. K., Kim, H., Kim, C. G., Lee, H., Han, J. W., Choi, S. J., Jeong, S., Jeon, M., Kim, H., et al. (2020) · Cellular and Molecular Immunology · doi:10.1038/s41423-020-0427-6 · Cited by 90
FOXO1 constrains activation and regulates senescence in CD8 T cells
Delpoux, A., Marcel, N., Michelini, R. H., Katayama, C. D., Allison, K. A., Glass, C. K., Quiñones‐Parra, S. M., Murre, C., Loh, L., Kedzierska, K., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108674 · Cited by 92
Gulhati, P., Schalck, A. P., Jiang, S., Shang, X., Wu, C., Hou, P., Ruiz, S. H., Soto, L. M. S., Parra, E. R., Ying, H., et al. (2022) · Nature Cancer · doi:10.1038/s43018-022-00500-z · Cited by 89
Impairment of T Cell Function in Parasitic Infections
Rodrigues, V., Cordeiro‐da‐Silva, A., Laforge, M., Ouaissi, A., Akharid, K., Silvestre, R., & Estaquier, J. (2014) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0002567 · Cited by 90
Friedman, J., Moore, E. C., Zolkind, P., Robbins, Y., Clavijo, P. E., Sun, L., Greene, S., Morisada, M. V., Mydlarz, W. K., Schmitt, N., et al. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-2209 · Cited by 88
T cell exhaustion and immune-mediated disease — the potential for therapeutic exhaustion
McKinney, E. F., & Smith, K. G. C. (2016) · Current Opinion in Immunology · doi:10.1016/j.coi.2016.09.005 · Cited by 91
Prinz, P. U., Mendler, A. N., Masouris, I., Durner, L., Oberneder, R., & Noeßner, E. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1103028 · Cited by 89
Penaloza‐MacMaster, P., Provine, N. M., Ra, J., Borducchi, E. N., McNally, A. G., Simmons, N. L., Iampietro, M. J., & Barouch, D. H. (2012) · Journal of Virology · doi:10.1128/jvi.02058-12 · Cited by 83
Delpoux, A., Michelini, R. H., Verma, S., Lai, C.-Y., Omilusik, K. D., Utzschneider, D. T., Redwood, A., Goldrath, A. W., Benedict, C. A., & Hedrick, S. Μ. (2017) · The Journal of Experimental Medicine · doi:10.1084/jem.20170697 · Cited by 91
Johnnidis, J. B., Muroyama, Y., Ngiow, S. F., Chen, Z., Manne, S., Cai, Z., Song, S., Platt, J. M., Schenkel, J. M., Abdel-Hakeem, M. S., et al. (2021) · Science Immunology · doi:10.1126/sciimmunol.abe3702 · Cited by 91
Self-citationAlter, G., Kavanagh, D. G., Rihn, S. J., Luteijn, R. D., Brooks, D. G., Oldstone, M. B. A., van Lunzen, J., & Altfeld, M. A. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40913 · Cited by 90
Hongo, D., Tang, X., Dutt, S., Nádor, R. G., & Strober, S. (2011) · Blood · doi:10.1182/blood-2011-08-371948 · Cited by 88
Strong homeostatic TCR signals induce formation of self‐tolerant virtual memory CD8 T cells
Drobek, A., Moudrá, A., Mueller, D. L., Huranová, M., Horková, V., Přibíková, M., Ivánek, R., Oberle, S. G., Zehn, D., McCoy, K. D., et al. (2018) · The EMBO Journal · doi:10.15252/embj.201798518 · Cited by 88
Emerging role of metabolic reprogramming in tumor immune evasion and immunotherapy
Fan, C., Zhang, S., Gong, Z., Li, X., Xiang, B., Deng, H., Zhou, M., Li, Y., Li, Y., Xiong, W., et al. (2020) · Science China Life Sciences · doi:10.1007/s11427-019-1735-4 · Cited by 92
Mott, K. R., Bresee, C. J., Allen, S. J., BenMohamed, L., Wechsler, S. L., & Ghiasi, H. (2008) · Journal of Virology · doi:10.1128/jvi.02234-08 · Cited by 87
Ji, Y., Fioravanti, J., Zhu, W., Wang, H., Wu, T., Hu, J., Lacey, N. E., Gautam, S., Gall, J. B. L., Yang, X., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09882-8 · Cited by 88
KLF2 maintains lineage fidelity and suppresses CD8 T cell exhaustion during acute LCMV infection
Fagerberg, E., Attanasio, J., Dien, C., Singh, J., Kessler, E., Abdullah, L., Shen, J., Hunt, B. G., Connolly, K. A., Brouwer, E. D., et al. (2025) · Science · doi:10.1126/science.adn2337 · Cited by 90
Reuter, M. A., Pombo, C., & Betts, M. R. (2012) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2012.05.005 · Cited by 87
Diversity in CD8+ T cell differentiation
Parish, I. A., & Kaech, S. M. (2009) · Current Opinion in Immunology · doi:10.1016/j.coi.2009.05.008 · Cited by 91
Self-citationClonal 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
Self-citationLi, S., Li, K., Wang, K., Yu, H., Wang, X., Shi, M., Liang, Z., Zhou, Y., Hu, Y., Li, Y., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-43462-1 · Cited by 89
Frank, G. M., Lepisto, A. J., Freeman, M. L., Sheridan, B. S., Cherpes, T. L., & Hendricks, R. L. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0902373 · Cited by 85
HDAC6 selective inhibition of melanoma patient T-cells augments anti-tumor characteristics
Laino, A. S., Betts, B. C., Veerapathran, A., Dolgalev, I., Sarnaik, A. A., Quayle, S. N., Jones, S. S., Weber, J. S., & Woods, D. M. (2019) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-019-0517-0 · Cited by 85
Mechanisms of HBV immune evasion
Kuipery, A., Gehring, A. J., & Isogawa, M. (2020) · Antiviral Research · doi:10.1016/j.antiviral.2020.104816 · Cited by 87
Baxter, A. E., Huang, H., Giles, J. R., Chen, Z., Wu, J. E., Drury, S., Tuite-Dalton, K. A., Park, S. L., Torres, L., Simone, B. W., et al. (2023) · Immunity · doi:10.1016/j.immuni.2023.05.008 · Cited by 83
Self-citationRegulators of CD8+ T cell exhaustion
Sun, Q., & Dong, C. (2025) · Nature reviews. Immunology · doi:10.1038/s41577-025-01221-x · Cited by 91
CD8 T-Cell Memory Differentiation during Acute and Chronic Viral Infections
Kalia, V., Sarkar, S., & Ahmed, R. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6451-9_7 · Cited by 86
Self-citationPenna, A., Laccabue, D., Libri, I., Giuberti, T., Schivazappa, S., Alfieri, A., Mori, C., Canetti, D., Lampertico, P., Viganò, M., et al. (2012) · Journal of Hepatology · doi:10.1016/j.jhep.2011.12.032 · Cited by 84
Tumor-necrosis factor impairs CD4+ T cell–mediated immunological control in chronic viral infection
Beyer, M., Abdullah, Z., Chemnitz, J. M., Maisel, D., Sander, J., Lehmann, C., Thabet, Y., Shinde, P. V., Schmidleithner, L., Köhne, M., et al. (2016) · Nature Immunology · doi:10.1038/ni.3399 · Cited by 86
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 86
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 87
Schalck, A., Sakellariou-Thompson, D., Forget, M.-A., Sei, E., Hughes, T. G., Reuben, A., Bai, S., Hu, M., Kumar, T., Hurd, M. W., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-1248 · Cited by 85
Landscape of Exhausted Virus-Specific CD8 T Cells in Chronic LCMV Infection
Sandu, I., Cerletti, D., Oetiker, N., Borsa, M., Wagen, F., Spadafora, I., Welten, S. P. M., Stolz, U., Oxenius, A., & Claassen, M. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108078 · Cited by 78
Tumour immunotherapy: lessons from predator–prey theory
Hamilton, P. T., Anholt, B. R., & Nelson, B. H. (2022) · Nature reviews. Immunology · doi:10.1038/s41577-022-00719-y · Cited by 82
Chentoufi, A. A., Serafin, E. K., Tran, M. V., Dasgupta, G., Lim, C. H., Yu, D. C., Afifi, R. E., Jiang, X., Carpenter, D., Osorio, N., et al. (2011) · Journal of Virology · doi:10.1128/jvi.00587-11 · Cited by 84
Cancer vaccine formulation dictates synergy with CTLA-4 and PD-L1 checkpoint blockade therapy
Hailemichael, Y., Woods, A. N., Fu, T., He, Q., Nielsen, M. C., Hasan, F., Roszik, J., Xiao, Z., Vianden, C., Khong, H., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci93303 · Cited by 81
Cariani, E., & Missale, G. (2019) · Liver International · doi:10.1111/liv.14192 · Cited by 83
Hu, Y., Hudson, W. H., Kissick, H. T., Medina, C. B., Baptista, A. P., Ma, C., Liao, W., Germain, R. N., Turley, S. J., Zhang, N., et al. (2022) · The Journal of Experimental Medicine · doi:10.1084/jem.20211574 · Cited by 86
Self-citationWon, S., Lee, C., Bae, S., Lee, J., Choi, D., Kim, M., Song, S., Lee, J., Kim, E., Shin, H., et al. (2023) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12357 · Cited by 81
STAT1 Signaling in Astrocytes Is Essential for Control of Infection in the Central Nervous System
Hidano, S., Randall, L. M., Dawson, L. A., Dietrich, H. K., Konradt, C., Klover, P. J., John, B., Harris, T. H., Fang, Q., Turek, B. J., et al. (2016) · mBio · doi:10.1128/mbio.01881-16 · Cited by 81
Cutting Edge: Chromatin Accessibility Programs CD8 T Cell Memory
Scharer, C. D., Bally, A. P. R., Gandham, B., & Boss, J. M. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1602086 · Cited by 82
Linkage of CD8+ T cell exhaustion with high-fat diet-induced tumourigenesis
Kado, T., Nawaz, A., Takikawa, A., Usui, I., & Tobe, K. (2019) · Scientific Reports · doi:10.1038/s41598-019-48678-0 · Cited by 80
CTLA-4 (CD152): A versatile receptor for immune-based therapy
Lingel, H., & Brunner-Weinzierl, M. C. (2019) · Seminars in Immunology · doi:10.1016/j.smim.2019.101298 · Cited by 82
CD28 Costimulatory Domain–Targeted Mutations Enhance Chimeric Antigen Receptor T-cell Function
Boucher, J. C., Li, G., Kotani, H., Cabral, M. L., Morrissey, D., Lee, S. B., Spitler, K., Beatty, N. J., Cervantes, E. V., Shrestha, B., et al. (2020) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-20-0253 · Cited by 82
Birocchi, F., Cusimano, M., Rossari, F., Beretta, S., Rancoita, P. M. V., Ranghetti, A., Colombo, S., Costa, B., Angel, P. E., Sanvito, F., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abl4106 · Cited by 81
CAR affinity modulates the sensitivity of CAR-T cells to PD-1/PD-L1-mediated inhibition
Andreu-Saumell, I., Rodríguez-García, A., Mühlgrabner, V., Giménez-Alejandre, M., Marzal, B., Castellsagué, J., Brasó‐Maristany, F., Calderón, H., Angelats, L., Colell, S., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47799-z · Cited by 87
Zediak, V. P., Johnnidis, J. B., Wherry, E. J., & Berger, S. L. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003741 · Cited by 80
Self-citationCirculating and tumor-infiltrating Tim-3 in patients with colorectal cancer
Xu, B., Yuan, L., Gao, Q., Yuan, P., Zhao, P., Yuan, H., Fan, H., Li, T., Qin, P., Han, L., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.4112 · Cited by 80
Induction and function of virus-specific CD4+ T cell responses
Whitmire, J. K. (2011) · Virology · doi:10.1016/j.virol.2010.12.015 · Cited by 81
Snyder, C. M., Loewendorf, A. I., Bonnett, E. L., Croft, M., Benedict, C. A., & Hill, A. B. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900227 · Cited by 79
Zhao, M., Kiernan, C. H., Stairiker, C. J., Hope, J. L., León, L. G., van Meurs, M., Brouwers-Haspels, I., Boers, R., Boers, J., Gribnau, J. H., et al. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008555 · Cited by 81
The diversity of CD8+ T cell dysfunction in cancer and viral infection
Galluzzi, L., Smith, K. N., Liston, A., & Garg, A. D. (2025) · Nature reviews. Immunology · doi:10.1038/s41577-025-01161-6 · Cited by 94
Buchan, S. L., Manzo, T., Flutter, B. R., Rogel, A., Edwards, N., Zhang, L., Sivakumaran, S., Ghorashian, S., Carpenter, B., Bennett, C. L., et al. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1401644 · Cited by 79
Harker, J. A., Dolgoter, A., & Zúñiga, E. I. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.010 · Cited by 79
Taylor, J. J., Krawczyk, C. M., Mohrs, M., & Pearce, E. J. (2009) · Journal of Clinical Investigation · doi:10.1172/jci36534 · Cited by 79
IL-21 Restricts Virus-driven Treg Cell Expansion in Chronic LCMV Infection
Schmitz, I., Schneider, C., Fröhlich, A., Frebel, H., Christ, D., Leonard, W., Sparwasser, T., Oxenius, A., Freigang, S., & Kopf, M. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003362 · Cited by 88
Virus‐specific CD8 T cells: activation, differentiation and memory formation
Wiesel, M., Walton, S. M., Richter, K., & Oxenius, A. (2009) · Apmis · doi:10.1111/j.1600-0463.2009.02459.x · Cited by 80
Gaiha, G. D., McKim, K. J., Woods, M. W., Pertel, T., Rohrbach, J., Barteneva, N. S., Chin, C. R., Liu, D., Soghoian, D. Z., Cesa, K. T., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.12.011 · Cited by 76
Self-citationImmunotherapy for advanced thyroid cancers — rationale, current advances and future strategies
French, J. D. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-0398-9 · Cited by 80
Peng, L., Jin, X., Li, B.-Y., Zeng, X., Liao, B., Jin, T., Chen, J., Gao, X., Wang, W., He, Q., et al. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00962-8 · Cited by 77
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 79
Phares, T. W., Ramakrishna, C., Parra, G. I., Epstein, A. L., Chen, L., Atkinson, R., Stohlman, S. A., & Bergmann, C. C. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803557 · Cited by 81
Godefroy, E., Zhong, H., Pham, P., Friedman, D. F., & Yazdanbakhsh, K. (2015) · Haematologica · doi:10.3324/haematol.2015.132738 · Cited by 77
Tandon, R., Chew, G. M., Byron, M. M., Borrow, P., Niki, T., Hirashima, M., Barbour, J. D., Norris, P. J., Lanteri, M. C., Martin, J. N., et al. (2014) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2014.0004 · Cited by 77
Tse, S.-W., Cockburn, I. A., Zhang, H., Scott, A. L., & Zavala, F. P. (2013) · Genes and Immunity · doi:10.1038/gene.2013.20 · Cited by 81
Özkazanç, D., Yöyen-Ermiş, D., Tavukçuoğlu, E., Büyükaşık, Y., & Esendağlı, G. (2016) · Immunology · doi:10.1111/imm.12665 · Cited by 76
Regulation of T Cells in Cancer by Nitric Oxide
Navasardyan, I., & Bonavida, B. (2021) · Cells · doi:10.3390/cells10102655 · Cited by 80
Coinhibitory receptors and CD8 T cell exhaustion in chronic infections
Kuchroo, V. K., Anderson, A. C., & Petrovas, C. (2014) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0000000000000088 · Cited by 76
Böttcher, J. P., Schanz, O., Wohlleber, D., Abdullah, Z., Debey-Pascher, S., Staratschek-Jox, A., Höchst, B., Hegenbarth, S., Grell, J., Limmer, A., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.02.008 · Cited by 82
Innate Immune Sensing of HIV-1 by Dendritic Cells
Luban, J. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.10.002 · Cited by 79
T Cell Factor 1 Suppresses CD103+ Lung Tissue-Resident Memory T Cell Development
Wu, J., Madi, A., Mieg, A., Hotz‐Wagenblatt, A., Weisshaar, N., Ma, S., Möhr, K., Schlimbach, T., Hering, M., Borgers, H., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.03.048 · Cited by 76
Pillai, R., LeBoeuf, S. E., Hao, Y., New, C., Blum, J. L. E., Rashidfarrokhi, A., Huang, S. M., Bahamon, C., Wu, W., Karadal-Ferrena, B., et al. (2024) · Science Advances · doi:10.1126/sciadv.adm9859 · Cited by 81
An early precursor CD8+ T cell that adapts to acute or chronic viral infection
McManus, D. T., Valanparambil, R. M., Medina, C. B., Scharer, C. D., McGuire, D. J., Sobierajska, E., Hu, Y., Chang, D. Y., Wieland, A., Lee, J., et al. (2025) · Nature · doi:10.1038/s41586-024-08562-y · Cited by 76
Self-citationMechanisms of immunosenescence: lessons from models of accelerated immune aging
Saux, S. L., Weyand, C. M., & Goronzy, J. J. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06297.x · Cited by 76
Coinhibitory molecules in hematologic malignancies: targets for therapeutic intervention
Norde, W. J., Hobo, W. A., van der Voort, R., & Dolstra, H. (2012) · Blood · doi:10.1182/blood-2012-02-412510 · Cited by 76
Beckmann, N. D., Comella, P., Cheng, E., Lepow, L., Beckmann, A. G., Tyler, S. R., Mouskas, K., Simons, N. W., Hoffman, G. E., Francoeur, N. J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24981-1 · Cited by 71
Kang, H. J., Oh, J., Chun, S., Kim, D., Ryu, Y., Hwang, H. S., Kim, S., An, J., Cho, E. J., Lee, H., et al. (2019) · Journal of Hepatology · doi:10.1016/j.jhep.2019.03.018 · Cited by 73
CXCR5+CD8+ T cells are a distinct functional subset with an antitumor activity
Chu, F., Li, H. S., Liu, X., Cao, J., Ma, W., Ma, Y., Weng, J., Zhu, Z., Cheng, X., Wang, Z., et al. (2019) · Leukemia · doi:10.1038/s41375-019-0464-2 · Cited by 74
Galectin-9 and VISTA Expression Define Terminally Exhausted T Cells in HIV-1 Infection
Shahbaz, S., Dunsmore, G., Koleva, P. T., Xu, L., Houston, S. C., & Elahi, S. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1901481 · Cited by 73
Wei, Y., Davenport, T. C., Collora, J. A., Ma, H. K., Pinto-Santini, D., Lama, J. R., Alfaro, R., Duerr, A. C., & Ho, Y. (2023) · Immunity · doi:10.1016/j.immuni.2023.10.002 · Cited by 67
Beltra, J., Bourbonnais, S., Bédard, N., Charpentier, T., Boulangé, M., Michaud, E., Boufaied, I., Bruneau, J., Shoukry, N. H., Lamarre, A., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604256113 · Cited by 72
Hammer, Q., & Romagnani, C. (2016) · Advances in immunology · doi:10.1016/bs.ai.2016.10.001 · Cited by 72
Inhibitory Receptors and Immune Checkpoints Regulating Natural Killer Cell Responses to Cancer
Buckle, I., & Guillerey, C. (2021) · Cancers · doi:10.3390/cancers13174263 · Cited by 74
Metabolic regulation of the cancer-immunity cycle
Patterson, L. F. S., & Vardhana, S. A. (2021) · Trends in Immunology · doi:10.1016/j.it.2021.09.002 · Cited by 73
Single-cell RNA sequencing coupled to TCR profiling of large granular lymphocyte leukemia T cells
Gao, S., Wu, Z., Arnold, B., Diamond, C. E., Batchu, S., Giudice, V., Alemu, L., Raffo, D. Q., Feng, X., Kajigaya, S., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-29175-x · Cited by 70
Lin, Y., Song, Y., Zhang, Y., Li, X., Kan, L., & Han, S. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-06291-y · Cited by 76
Wang, C., McPherson, A. J., Jones, R. B., Kawamura, K. S., Lin, G. H. Y., Lang, P. A., Ambagala, T., Pellegrini, M., Calzascia, T., Aidarus, N., et al. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20110675 · Cited by 73
Cell-Intrinsic Barriers of T Cell-Based Immunotherapy
Ghoneim, H. E., Zamora, A. E., Thomas, P. G., & Youngblood, B. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2016.10.002 · Cited by 71
Cytokine-Mediated Regulation of CD8 T-Cell Responses During Acute and Chronic Viral InfectionPreprint
Hashimoto, M., Im, S. J., Araki, K., & Ahmed, R. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028464 · Cited by 78
Self-citationTherapeutic Depletion of Natural Killer Cells Controls Persistent Infection
Waggoner, S. N., Daniels, K. A., & Welsh, R. M. (2013) · Journal of Virology · doi:10.1128/jvi.03002-13 · Cited by 72
Platelet-derived growth factor beta is a potent inflammatory driver in paediatric high-grade glioma
Ross, J. L., Chen, Z., Herting, C. J., Grabovska, Y., Szulzewsky, F., Puigdelloses, M., Monterroza, L., Switchenko, J. M., Wadhwani, N. R., Cimino, P. J., et al. (2020) · Brain · doi:10.1093/brain/awaa382 · Cited by 70
Dynamic chromatin regulatory landscape of human CAR T cell exhaustion
Gennert, D. G., Lynn, R. C., Granja, J. M., Weber, E. W., Mumbach, M. R., Zhao, Y., Duren, Z., Sotillo, E., Greenleaf, W. J., Wong, W. H., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2104758118 · Cited by 70
Tillé, L., Cropp, D., Charmoy, M., Reichenbach, P., Andreatta, M., Wyss, T., Bodley, G., Crespo, I., Nassiri, S., Lourenço, J., et al. (2023) · Nature Immunology · doi:10.1038/s41590-023-01614-x · Cited by 74
Haining, W. N., Ebert, B. L., Subrmanian, A., Wherry, E. J., Eichbaum, Q. G., Evans, J., Mak, R. H., Rivoli, S., Pretz, J. L., Angelosanto, J., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.3.1859 · Cited by 69
Self-citation
Metadata
- Authors
- Wherry, E. J., Ha, S.-J., Kaech, S. M., Haining, W. N., Sarkar, S., Kalia, V., Subramaniam, S., Blattman, J. N., Barber, D. L., & Ahmed, R.
- Affiliations
- Emory University (US)
- Dana-Farber Cancer Institute (US)
- Corresponding author
- Wherry, E. John
- Ahmed, Rafi
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2007-10
- Volume
- 27
- Issue
- 4
- Pages
- 670-684
- ISSN
- 1074-7613 (ISSN-L)
- OpenAlex
- W2040353461
- Cited by
- 2,103
- References
- 56
- Citations by year
- 2026: 110 · 2025: 148 · 2024: 140 · 2023: 144 · 2022: 139 · 2021: 180 · 2020: 161 · 2019: 138 · 2018: 119 · 2017: 102 · 2016: 112 · 2015: 116 · 2014: 88 · 2013: 83 · 2012: 80
- FWCI
- 19.12
- Type
- journal article
- Language
- en
- Update notices
- erratum (2007-11-26)
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2116 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Allergy and Infectious Diseases (AI071309, AI 30048, R01AI071309)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
- Keywords
- CD8+ T cell exhaustion, chronic viral infection, lymphocytic choriomeningitis virus, PD-1, inhibitory receptors, T cell receptor signaling, cytokine signaling, T cell metabolism, bioenergetics, T cell migration, transcription factors, T cell anergy, gene expression profiling, immunotherapy
- MeSH terms
- Animals, Cell Differentiation, Chronic Disease, Female, Flow Cytometry, Immunologic Memory, Lymphocyte Activation, Lymphocytic choriomeningitis virus, Mice, Inbred C57BL, Molecular Sequence Data, Phenotype, Virus Diseases, Gene Expression, Clonal Anergy, CD8-Positive T-Lymphocytes, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review