Cited by 781Cancer Immunotherapy and BiomarkersT-cell and B-cell ImmunologyPhagocytosis and Immune Regulation

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PD-1 signaling in primary T cells

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Riley, James L.·2009·Immunological Reviews

DOI 10.1111/j.1600-065x.2009.00767.xPMC PMC3424066

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Abstract

Summary: Programmed death‐1 (PD‐1) is a cell surface molecule that regulates the adaptive immune response. Engagement of PD‐1 by its ligands PD‐L1 or PD‐L2 transduces a signal that inhibits T‐cell proliferation, cytokine production, and cytolytic function. While a great deal is known concerning the biologic roles PD‐1 plays in regulating the primary immune response and in T‐cell exhaustion, comparatively little is known regarding how PD‐1 ligation alters signaling pathways. PD‐1 ligation is known to inhibit membrane‐proximal T‐cell signaling events, while ligation of the related inhibitory molecule cytotoxic T‐lymphocyte antigen‐4 appears to target more downstream signaling pathways. A major obstacle to an in‐depth understanding of PD‐1 signaling is the lack of physiologic models in which to study signal transduction. This review focuses on: (i) signaling pathways altered by PD‐1 ligation, (ii) factors recruited upon PD‐1 phosphorylation, and (iii) exploring the hypothesis that PD‐1 ligation induces distinct signals during various stages of immune‐cell differentiation. Lastly, we describe models to dissect the function of the PD‐1 cytoplasmic tail using primary cells in the absence of agonist antibodies.

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Background
An Extended PD-L2 Cytoplasmic Domain Results From Alternative Splicing in NSCLC Cells
Dietz, L. L., Furman, N. T., Larsen, T. V., Daugaard, T. F., Thomsen, E. A., Lade‐Keller, J., Aagaard, L., Sørensen, B. S., & Nielsen, A. L. (2022) · Journal of Immunotherapy · doi:10.1097/cji.0000000000000439 · Cited by 7
cAMP responsive element modulator α promotes effector T cells in systemic autoimmune diseases
Carlsson, E., Cowell‐McGlory, T., & Hedrich, C. M. (2023) · Immunology · doi:10.1111/imm.13680 · Cited by 7
“PD-1 is expressed in activated T cells, as well as DN thymocytes [116 – 120], and plays a critical role in the limitation of inflammatory responses, including effector cytokine expression [121].”
Background
Clinical and Pharmacologic Features of Monoclonal Antibodies and Checkpoint Blockade Therapy in Multiple Myeloma
D’Agostino, M., Gazzera, G., Cetani, G., Bringhen, S., Boccadoro, M., & Gay, F. (2018) · Current Medicinal Chemistry · doi:10.2174/0929867325666180514114806 · Cited by 7
A novel humanized anti-PD-1 monoclonal antibody potentiates therapy in oral squamous cell carcinoma
Cai, Y., Wang, F., Liu, Q., Li, Z., Li, D., & Sun, Z. (2018) · Investigational New Drugs · doi:10.1007/s10637-018-0678-6 · Cited by 7
A Novel Renoprotective Strategy: Upregulation of PD-L1 Mitigates Cisplatin-Induced Acute Kidney Injury
Liu, J., Yang, D. C. H., Zhang, J., Hsu, S., Weiss, R. H., & Chen, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413304 · Cited by 7
“Previous studies have pointed to the vital role of the PD-1/PD-L1 axis in modulating the immunogenic activities of the T cells [26,27], as well as other immune cell types.”
Result
Recombinant Human Interleukin-15 and Anti-PD-L1 Combination Therapy Expands a CXCR3+PD1−/low CD8 T-Cell Subset in Simian Immunodeficiency Virus-Infected Rhesus Macaques
Chen, P., Chen, H., Moussa, M., Cheng, J., Li, T., Qin, J., Lifson, J. D., Sneller, M. C., Krymskaya, L., Godin, S., et al. (2019) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiz485 · Cited by 7
PD-L1 upregulation in activated fibroblasts promotes silica particle-induced pulmonary fibrosis
Zhao, Y., Qu, Y., Duan, M., Qi, Y., Xia, J., Hao, C., & Yao, W. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.139147 · Cited by 6
Prodrug-tethered lipid nanoparticles for synergistic messenger RNA cancer immunotherapy
Shi, Q., Gong, N., Wang, J., Palanki, R., Zheng, Q., Alameh, M., Dwivedi, G., Davis, B., Melamed, J. R., Luo, Z., et al. (2026) · Nature Nanotechnology · doi:10.1038/s41565-025-02102-z · Cited by 9
Proteomic Investigation of Immune Checkpoints and Some of Their Inhibitors
Agostini, M., Traldi, P., & Hamdan, M. H. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25179276 · Cited by 6
“PD-1 consists of an IgV-like domain, a transmembrane domain, a cytosolic domain, and a stalk region that separates the IgV domain from the plasma membrane [47,48].”
Background
Targeting PD-1 and CD85j can restore intratumoral CD4 + GzmB + T-cell functions to combat MHC-II-expressing tumors
Wang, B., Wang, X., Wang, T., Meng, K., Yu, T., Xi, Y., Hu, S., Xiong, H., Qu, R., Yuan, Z., et al. (2025) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2024-010890 · Cited by 7
“Thus, this study provides new insights into the molecular mechanisms underlying the differentiation of CD4 + GzmB + T cells and identifies the critical factors that drive CD4 + GzmB + T-cell transformation in the tumor microenvironment of MCH- II-expressing tumors.”
PD ‐1 Regulates the Glycolytic Pathway to Reverse Abnormal CD4 + T Cell Differentiation and Alleviate Hashimoto's Thyroiditis
Jiang, X., Luo, T., Zhao, X., Li, P., Gu, X., Wan, C., Xie, X., & Liu, H. (2025) · Immunology · doi:10.1111/imm.13953 · Cited by 6
“…have shown that, in patients with HT, the PD-1/PD-L1 pathway is expressed abnormally and that an enhanced PD-1/PD-L1 pathway may influence the onset and progression of HT. Programmed death receptor 1 (PD-1), also known as programmed cell death 1, is a monomeric glycoprotein of the CD28 family [12].”
Tethered Signaling in Inhibitory Immune Receptors
Pérez-Ferreros, P., Gaus, K., & Goyette, J. (2019) · Frontiers in Physics · doi:10.3389/fphy.2018.00158 · Cited by 6
Genome-wide characterization of copy number variations in diffuse large B-cell lymphoma with implications in targeted therapy
Dharanipragada, P., & Parekh, N. (2019) · Precision Clinical Medicine · doi:10.1093/pcmedi/pbz024 · Cited by 6
Exclusion of PD-1 from the immune synapse: A novel strategy to modulate T cell function
Hao, L. Y., Lerrer, S., Paiola, M., Moore, E. K., Gartshteyn, Y., Song, R., Goeckeritz, M., Black, M. J., Bukhari, S., Hu, X., et al. (2024) · Molecular Therapy Oncology · doi:10.1016/j.omton.2024.200839 · Cited by 6
“19 If PD-1 were re-localized away from the TCR, then the proximity of its cell-surface and intracellular binding partners and the TCR would also be disrupted.”
Cancer Immunotherapy: An Effective Tool in Cancer Control and Treatment
Kaur, K., & Khatik, G. L. (2019) · Current Cancer Therapy Reviews · doi:10.2174/1573394715666190913184853 · Cited by 12
Factor VIII Fc Fusion Protein but not FVIII Drives Human Monocyte‐Derived Dendritic Cell Activation via FcγRIIa
Kannicht, C., Danßmann, I., Weilandt, C., Derkow, K., Kohla, G., & Geyer, H. (2020) · HemaSphere · doi:10.1097/hs9.0000000000000330 · Cited by 6
“Engagement of CD274 with PD-1 on T cells can block T cell proliferation, cytokine production and inhibit T cell survival.(31) However, this inhibitory signal can be overturned by CD28 co-stimulation or IL-2.”
Background
Phase I study of the antiprogrammed cell death‐1 Ab spartalizumab (PDR001) in Japanese patients with advanced malignancies
Minami, H., Doi, T., Toyoda, M., Imamura, Y., Kiyota, N., Mitsuma, A., Shimokata, T., Naito, Y., Matsubara, N., Tajima, T., et al. (2020) · Cancer Science · doi:10.1111/cas.14678 · Cited by 6
“Disease control rate (CR + PR + SD), % (95% CI) 50 (12-88) 33 (4-78) 17 (0-64) 33 (13-59)”
Targeted Therapy and Immunotherapy in Nonmelanoma Skin Cancer
Aboul‐Fettouh, N., Kubicki, S. L., Chen, L. L., Silapunt, S., & Migden, M. R. (2022) · Dermatologic Clinics · doi:10.1016/j.det.2022.07.009 · Cited by 6
Expression of programmed death ligand 1 in drug-resistant osteosarcoma: An exploratory study
Skertich, N. J., Chu, F., Tarhoni, I., Szajek, S., Borgia, J. A., & Madonna, M. B. (2021) · Surgery Open Science · doi:10.1016/j.sopen.2021.07.001 · Cited by 6
Genetic editing of CISH enhances T cell effector programs independently of immune checkpoint cell surface ligand expressionPreprint
Arthofer, E., Chakraborty, K., Viney, L., Johnson, M. J., Webber, B. R., Moriarity, B. S., Lou, E., Choudhry, M. S., Klebanoff, C. A., & Henley, T. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.17.456714 · Cited by 6
Adoptive cell therapies in solid tumors: current clinical landscape, challenges, and future directions
Rizkallah, J., Wehbeh, B. E. D., Wassouf, W., Salameh, E., Joumaa, A., Haddad, F. J., Hamade, L., Charbel, N., Bakri, G. M., Awada, A., et al. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1800292 · Cited by 6
“For example, thymocyte selection – associated high mobility group box (TOX) becomes highly expressed following sustained TCR signaling (106), promoting upregulation of PD-1 and attenuating immune responses (107, 108).”
Immune Checkpoint Blockade and Adaptive Immune Resistance in Cancer
Wong, R. M. H., & Cameron, R. B. (2017) · InTech eBooks · doi:10.5772/66494 · Cited by 7
“Signaling through the PD-1 receptor on T cells results in downstream inhibition of PI3K/AKT activation [17].”
Background
Immune Checkpoint Inhibition—Does It Cause Rheumatic Diseases? Mechanisms of Cancer-Associated Loss of Tolerance and Pathogenesis of Autoimmunity
Thanarajasingam, U., & Abdel‐Wahab, N. (2020) · Rheumatic Disease Clinics of North America · doi:10.1016/j.rdc.2020.04.003 · Cited by 5
Alterations in the CD56− and CD56+ T Cell Subsets during COVID-19
Vavilova, J. D., Ustiuzhanina, M. O., Boyko, A. A., Streltsova, M. A., Kust, S. A., Kanevskiy, L. M., Iskhakov, R. N., Sapozhnikov, A. M., Gubernatorova, E. O., Drutskaya, M. S., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24109047 · Cited by 5
“The inhibitory PD-1 receptor demonstrates stable expression on the resting T cells and overexpression during activation [54,74].”
Background
Pembrolizumab-associated tumor development in a patient with Sézary syndrome
Malachowski, S. J., Hatch, L. A., Sokol, L., Messina, J. L., & Seminario‐Vidal, L. (2019) · JAAD Case Reports · doi:10.1016/j.jdcr.2019.11.005 · Cited by 5
“DISCUSSION Pembrolizumab is a monoclonal antibody that targets the PD-1 receptor on lymphocytes, crippling their ability to activate cytotoxic T cells via the PD-1 ligand.(4) Malignant cells may upregulate expression of PD-1 ligand to evade the host immune response; this phenomenon has been noted in circulating T cell…”
Background
An evaluation of pembrolizumab for classical Hodgkin lymphoma
Manji, F., Laister, R. C., & Kuruvilla, J. G. (2022) · Expert Review of Hematology · doi:10.1080/17474086.2022.2061947 · Cited by 5
“As the PI3K-AKT-mTOR pathway controls a multitude of phenomena including cell growth, survival and protein synthesis, many of these processes are aberrantly affected by PD-1 activation [11,12].”
Background
Present and future of immune checkpoint blockade: Monotherapy to adjuvant approaches
Patel, M. A. (2015) · World Journal of Immunology · doi:10.5411/wji.v5.i1.1 · Cited by 5
Optimisation of neoadjuvant pembrolizumab therapy for locally advanced MSI-H/dMMR colorectal cancer using data-driven delay integro-differential equations
Hawi, G., Kim, P., & Lee, P. P. (2025) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2025.112231 · Cited by 5
CgSHIP2 negatively regulates the mRNA expressions of CgIL-17s in response to Vibrio splendidus stimulation in Crassostrea gigas
Wang, M., Sun, J., Yan, X., Yang, W., Wang, W., Li, Y., Wang, L., & Song, L. (2024) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2024.109612 · Cited by 4
B Cell Subsets and Immune Checkpoint Expression in Patients with Chronic Lymphocytic Leukemia
Ntsethe, A., Mkhwanazi, Z. A., Dludla, P. V., & Nkambule, B. B. (2024) · Current Issues in Molecular Biology · doi:10.3390/cimb46030112 · Cited by 4
“However, the expression of these immune checkpoint molecules on B cell subsets did not correlate with B2M levels.”
Background
Expression of PD1 and BTLA on the CD8+ T Cell and γδT Cell Subsets in Peripheral Blood of Non-Small Cell Lung Cancer Patients
Bao, Y., Mo, J., Wu, J., & Chenxi, C. (2019) · Chinese Medical Sciences Journal · doi:10.24920/003498 · Cited by 3
Phosphorylation: A Fast Switch For Checkpoint Signaling
Wang, Y., Wang, P., & Xu, J. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-3266-5_15 · Cited by 4
Nanotechnology and Immunomodulators in Cancer
Volovat, C. D., Volovăț, S. R., & Agop, M. (2022) · Springer eBooks · doi:10.1007/978-981-16-6379-6_5 · Cited by 4
The landscape of TIGIT target and clinical application in diseases
Shu, R., Kong, X., Liu, J., Wang, L., Wang, X., Zou, X., Zheng, X., Ye, F., Xu, H., Li, Z., et al. (2022) · MedComm – Oncology · doi:10.1002/mog2.18 · Cited by 4
Immunotherapy and Targeted Therapy in the Management of Oral Cancers
Dutta, S., Singhal, S., Shah, R., & Haque, M. (2022) · Critical Reviews™ in Oncogenesis · doi:10.1615/critrevoncog.2022046361 · Cited by 4
Regulatory Rheumatoid Factor is Specific to PD-1 and Uses PD-1 Pathway to Control CD4 T Lymphocytes
Khramova, T., Beduleva, L., Sidorov, A., Terentiev, A., & Menshikov, I. (2023) · Immunological Investigations · doi:10.1080/08820139.2023.2250818 · Cited by 4
Exploring Costimulatory Blockade-Based Immunologic Strategies in Transplantation: Are They a Promising Immunomodulatory Approach for Organ and Vascularized Composite Allotransplantation?
Grosu-Bularda, A., Hodea, F.-V., Zamfirescu, D., Stoian, A., Teodoreanu, R. N., Lascăr, I., & Hariga, C.-S. (2024) · Journal of Personalized Medicine · doi:10.3390/jpm14030322 · Cited by 4
“Cell apoptosis has also been shown to be induced by PD-1 [86].”
Background
Chimeric tumor modeling reveals role of partial PDL1 expression in resistance to virally induced immunotherapy
Bartee, M. Y., Dryja, P., & Bartee, E. (2019) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-018-0496-6 · Cited by 4
Hypothetical Immunological and Immunogenetic Model of Heterogenous Effects of BCG Vaccination in SARS-CoV-2 Infections: BCG-induced Trained and Heterologous Immunity
Kovačić, D., Gajić, A. A., Latinović, D., & Softić, A. (2021) · Journal of Medical Science · doi:10.20883/medical.e551 · Cited by 4
Improving the role of immune checkpoint inhibitors in the management of advanced urothelial carcinoma, where do we stand?
Houssiau, H., & Seront, E. (2022) · Translational Oncology · doi:10.1016/j.tranon.2022.101387 · Cited by 4
“All these pathway enhance activation of inflamatory reaction through NF-kβ activation and Il-2 production [17,18].”
Background
Lack of Association Between PDCD-1 Polymorphisms and Colorectal Cancer Risk: A Case-Control Study
Lin, J., Chen, H., Huang, Y., Tang, W., Zhang, S., & Chen, Y. (2022) · Immunological Investigations · doi:10.1080/08820139.2022.2069504 · Cited by 4
Targeted Therapies in Melanoma
Fanale, D., Bronte, G., & Russo, A. D. (2015) · Current clinical pathology · doi:10.1007/978-1-4939-2047-1_16 · Cited by 4
Costimulation of Th17 cells: adding fuel or putting out the fire in the inflamed gut?
Zhang, Z., Rosenbaum, J. T., Zhong, W., Lim, C., & Hinrichs, D. J. (2010) · Seminars in Immunopathology · doi:10.1007/s00281-009-0190-3 · Cited by 4
“Phosphorylation of ITSM recruits protein tyrosine phosphatase SHP-2, which further modulates downstream signaling molecules such as phosphatidylinositol-3-kinase [111].”
Background
PD-L1 blockade improves immune dysfunction of spleen dendritic cells and T-cells in zymosan-induced multiple organs dysfunction syndromes.
Liu, Q., Lv, Y., Zhao, M., Jin, Y., & Lu, J.-Y. (2015) · Europe PMC (PubMed Central) · Cited by 4
Immune Cells Within the Tumor Microenvironment
Spano, D., & Zollo, M. (2013) · Springer eBooks · doi:10.1007/978-3-7091-1300-4_1 · Cited by 4
Immunotherapy as a targeted therapy in non-small cell lung cancer
Rocco, D., Gravara, L. D., Avellino, A., Montesarchio, V., & Battiloro, C. (2018) · Translational Cancer Research · doi:10.21037/tcr.2018.10.10 · Cited by 4
“The PD-1/PD-L1 axis is a keystone in the inhibition of T-cell activity and expansion, in particular the PD-L1PD-1 ligation causes the recruitment of Src-homology 2 domain-containing phosphatases 1 and 2 (SHP-1/SHP-2) that determines the de-phosphorylation of fundamental signaling kinases in the mechanisms of central a…”
Background
ADA1-Driven Metabolic Refueling Enhances CAR T Cell Therapy for Solid Tumors
Song, A. W., & Song, X. (2025) · Cancers · doi:10.3390/cancers18010034 · Cited by 4
“Naïve T cells rely on oxidative phosphorylation (OXPHOS) and fatty acid oxidation for homeostatic survival and are generally quiescent, making them less equipped to thrive in the inflammatory, nutrient-poor tumor bed [15,54].”

Authors: Riley, J. L.
Affiliations: University of Pennsylvania (US)
Corresponding author: Riley, James L.
ORCID: Riley, James L.
Venue: Immunological Reviews
Publisher: Wiley
Published: 2009-04-21
Volume: 229
Issue: 1
Pages: 114-125
ISSN: 0105-2896 (ISSN-L)
1600-065X
DOI: 10.1111/j.1600-065x.2009.00767.x
PMC: PMC3424066
OpenAlex: W2017712207
Cited by: 778
References: 95
Citations by year: 2026: 21 · 2025: 39 · 2024: 37 · 2023: 66 · 2022: 73 · 2021: 84 · 2020: 64 · 2019: 61 · 2018: 60 · 2017: 49 · 2016: 33 · 2015: 41 · 2014: 34 · 2013: 37 · 2012: 30
FWCI: 2.32
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Immunological Reviews (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (CA113783, R01CA113783)
National Institute of Allergy and Infectious Diseases (AI080192, P01AI080192, R01AI057838, AI057838, PD-1 PO1AI080192)
Topics: Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Keywords: PD-1 signaling, PDCD1, PD-L1, PD-L2, T cell exhaustion, T cell proliferation inhibition, cytotoxic T lymphocyte antigen 4, signal transduction, T cell differentiation, immune checkpoint, primary T cells
MeSH terms: Animals, Antigens, Surface, Humans, T-Lymphocytes, Signal Transduction, Antigens, CD, CD28 Antigens, Apoptosis Regulatory Proteins, Mice, Protein Tyrosine Phosphatase, Non-Receptor Type 6, Protein Tyrosine Phosphatase, Non-Receptor Type 11, CTLA-4 Antigen, Programmed Cell Death 1 Receptor

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PD-1 signaling in primary T cells

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