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
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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“In case of co-inhibitory genes, known to inhibit T-cell activation, cytolytic function and cytokine production (62), we observed that expression of PDCD1 (PD-1) was induced in all three CD8 T-cell subsets stimulated with PMA/ionomycin, whereas its ligand CD274 (PD-L1) was only expressed on Tinter.”
Background
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Background
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“in immune suppression by blocking CD3/CD28-induced activation of PI3K and other signalling pathways.(22,23) PD-1 Tfh cells in human blood were reported to be quiescent cells with a stable phenotype, consistent with their potential as memory cells.”
Background
Competition NMR for Detection of Hit/Lead Inhibitors of Protein–Protein Interactions
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Background
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Grzywnowicz, M., Karabon, L., Karczmarczyk, A., Zajac, M., Skórka, K., Zaleska, J., Własiuk, P., Chocholska, S., Tomczak, W., Bojarska-Junak, A. A., et al. (2015) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2015.1017820 · Cited by 26
The Effect of Adjuvanting Cancer Vaccines with Herpes Simplex Virus Glycoprotein D on Melanoma-Driven CD8+ T Cell Exhaustion
Zhang, Y., & Ertl, H. C. J. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302029 · Cited by 25
“protein kinase B pathway, albeit through distinct pathways (31, 32).”
Background
Challenges and future of biomarker tests in the era of precision oncology: Can we rely on immunohistochemistry (IHC) or fluorescencein situhybridization (FISH) to select the optimal patients for matched therapy?
Chae, Y. K., Arya, A., Chiec, L. S., Shah, H. A., Rosenberg, A. J., Patel, S. P., Raparia, K., Choi, J., Wainwright, D. A., Villaflor, V. M., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.19809 · Cited by 31
“The binding of PD-1 with corresponding ligands (PD-L1/PD-L2) induces inhibition of functioning and proliferation of T cells [199].”
Background
T‐cell cross‐reactivity may explain the large variation in how cancer patients respond to checkpoint inhibitors
Sioud, M. (2018) · Scandinavian Journal of Immunology · doi:10.1111/sji.12643 · Cited by 26
“Interactions between PD-1 and its ligands, PD-L1 and PDL2, expressed by DCs, tumour cells or other myeloid cells exert a critical function in the setting of persistent antigen expression, as in tumours and chronic viral infections.(33) Multiple studies showed that tumour-specific T cells display high levels of multipl…”
Background
Rewiring the T cell-suppressive cytokine landscape of the tumor microenvironment: a new frontier for precision anti-cancer therapy
Lopresti, L., Tatangelo, V., Baldari, C. T., & Patrussi, L. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1418527 · Cited by 27
Unravelling T cell exhaustion through co‐inhibitory receptors and its transformative role in cancer immunotherapy
Xiang, S., Li, S., & Xu, J. (2025) · Clinical and Translational Medicine · doi:10.1002/ctm2.70345 · Cited by 28
“28,29 They also modulate the PI3K/AKT/mTOR pathway 30,31 and the RAS signalling pathway, 32 relating to cell cycle regulation and metabolism.”
Avelumab in Gastric Cancer
Roviello, G., D’Angelo, A., Generali, D., Pittacolo, M., Ganzinelli, M., Iezzi, G., de Manzini, N., & Sobhani, N. (2019) · Immunotherapy · doi:10.2217/imt-2019-0011 · Cited by 27
SHP2 inhibitor PHPS1 ameliorates acute kidney injury by Erk1/2-STAT3 signaling in a combined murine hemorrhage followed by septic challenge model
Jiang, J., Hu, B., Chung, C., Chen, Y., Zhang, Y., Tindal, E. W., Li, J., & Ayala, A. (2020) · Molecular Medicine · doi:10.1186/s10020-020-00210-1 · Cited by 26
“…protein tyrosine phosphatase (PTP) family members, likely due to the fact that coinhibitory receptors from the Programmed Cell Death Receptor-1 (PD-1) family bear intracellular tyrosine inhibitory motifs (ITIM) and/or intracellular tyrosine switch motifs (ITSM) (Keir et al. 2008; Riley 2009).”
YB-1 promotes cell proliferation and metastasis by targeting cell-intrinsic PD-1/PD-L1 pathway in breast cancer
Wu, Q., Xu, Y., Li, X., Liu, H., You, T., Cai, T., & Yang, F. (2022) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2022.106314 · Cited by 25
Genomic alterations underlying immune privilege in malignant lymphomas
Mottok, A., & Steidl, C. (2015) · Current Opinion in Hematology · doi:10.1097/moh.0000000000000155 · Cited by 24
“PD-1 (encoded by PDCD1), a monomeric transmembrane receptor protein of the Ig superfamily [123], mediates cellintrinsic inhibition of T cell activation and proliferation through SHP-1/2 mediated suppression of phosphorylated proteins downstream of the TCR resulting in an anergic and exhausted T cell phenotype [124].”
Background
Mesenchymal stem cells ameliorate experimental autoimmune hepatitis by activation of the programmed death 1 pathway
Chen, Y., Chen, S., Liu, L.-Y., Zou, Z., Cai, Y., Wang, J.-G., Chen, B., Xu, L., Lin, Z., Wang, X.-D., et al. (2014) · Immunology Letters · doi:10.1016/j.imlet.2014.10.021 · Cited by 25
Activation of phagocytosis by immune checkpoint blockade
Li, C., Lai, Y., Hsu, J. L., & Hung, M. (2018) · Frontiers of Medicine · doi:10.1007/s11684-018-0657-5 · Cited by 27
MALDI Mass Spectrometry Imaging Linked with Top-Down Proteomics as a Tool to Study the Non-Small-Cell Lung Cancer Tumor Microenvironment
Berghmans, E., Raemdonck, G. V., Schildermans, K., Willems, H., Boonen, K., Maes, E., Mertens, I., Pauwels, P., & Baggerman, G. (2019) · Methods and Protocols · doi:10.3390/mps2020044 · Cited by 25
“Its interaction is an inhibitory signaling pathway that, in normal circumstances, downregulates immune T cells to maintain self-tolerance and end ineffective immune responses [5].”
Background
PD-L1 Expression Correlates With Young Age and CD8+ TIL Density in Poorly Differentiated Cervical Squamous Cell Carcinoma
Saglam, O., Zhou, J., Wang, X., & Conejo-Garcia, J. R. (2019) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0000000000000623 · Cited by 25
“duction and CD28-C80 costimulation (16).”
The Common Costimulatory and Coinhibitory Signaling Molecules in Head and Neck Squamous Cell Carcinoma
Liao, P., Wang, H., Tang, Y., Tang, Y.-J., & Liang, X. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02457 · Cited by 27
“Hence, T cell proliferation activity, cytokine secretion capacity and cytotoxic effects are weakened, and tumor cells finally get immune tolerance (67, 68).”
Background
Cellular Energy Metabolism in T-Lymphocytes
Gaber, T., Strehl, C., Sawitzki, B., Hoff, P., & Buttgereit, F. (2014) · International Reviews of Immunology · doi:10.3109/08830185.2014.956358 · Cited by 26
“This inhibits the metabolic switch to glucose metabolism, aerobic glycolysis, and glutaminolysis during T-cell activation, thereby reducing cellular ATP and metabolic growth substrates [78].”
Background
Abdominal immune-related adverse events: detection on ultrasonography, CT, MRI and 18F-Fluorodeoxyglucose positron emission tomography
Anderson, M., Kurra, V., Bradley, W. R., Kilcoyne, A., Mojtahed, A., & Lee, S. I. (2020) · British Journal of Radiology · doi:10.1259/bjr.20200663 · Cited by 24
Low-density neutrophils in chronic graft versus host disease (cGVHD) are primarily immature CD10– and enhance T cell activation
Matthews, N. C., Burton, C. S., & Alfred, A. (2021) · Clinical & Experimental Immunology · doi:10.1111/cei.13612 · Cited by 24
“This may be due to low expression of programmed cell death 1 (PD1) on patient T cells at the time of activation (50) or activation already occurring before PDL1induced immune synapse disruption (50) or inadequate expression of PDL1 because the dose of IFNγ was insufficient.”
Background
Clinical utility of nivolumab in the treatment of advanced melanoma
Carvajal, R. D., Asmar, R., & Yang, J. (2016) · Therapeutics and Clinical Risk Management · doi:10.2147/tcrm.s78039 · Cited by 26
“This results in downstream inhibition of the Ras and PI3K/Akt pathways, which in turn reduces T-cell proliferation and survival.(35,36) PD-1 signaling inhibits expression of the cell survival factor Bcl-xL and transcription factors associated with effector T-cell function.”
Background
PD-1-stimulated T cell subsets are transcriptionally and functionally distinct
Lerrer, S., Tocheva, A. S., Bukhari, S., Adam, K., & Mor, A. (2021) · iScience · doi:10.1016/j.isci.2021.103020 · Cited by 19
“Like CTLA-4, PD-1 can activate individual T cell functions, or even entire distinct T cell subsets (Shitara and Nishikawa, 2018; Tocheva et al., 2020; Riley, 2009; Hui et al., 2017; Patsoukis et al., 2020).”
Background
Nanobodies targeting the interaction interface of programmed death receptor 1 (PD-1)/PD-1 ligand 1 (PD-1/PD-L1)
Wen, B., Zhao, L., Wang, Y., Qiu, C., Xu, Z., Huang, K.-L., Zhu, H., Li, Z., & Li, H. (2019) · Preparative Biochemistry & Biotechnology · doi:10.1080/10826068.2019.1692217 · Cited by 23
SHP2 Targets ITK Downstream of PD-1 to Inhibit T Cell Function
Strazza, M., Adam, K. R., Lerrer, S., Straube, J., Sandigursky, S., Ueberheide, B. M., & Mor, A. (2021) · Inflammation · doi:10.1007/s10753-021-01437-8 · Cited by 23
“The phosphatase SHP2 is the major effector of PD-1 signaling and genetic studies have demonstrated limited T cell inhibition in this pathway in the absence of this enzyme [14].”
Background
Combination therapy with nivolumab (anti-PD-1 monoclonal antibody): A new era in tumor immunotherapy
Kiasari, B. A., Abbasi, A., Darestani, N. G., Adabi, N., Moradian, A., Yazdani, Y., Hosseini, G. S., Gholami, N., & Janati, S. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109365 · Cited by 26
Cancer immunotherapy and its facilitation by nanomedicine
Sui, C., Wu, H., Li, X., Wang, Y., Wei, J., Yu, J., & Wu, X. (2024) · Biomarker Research · doi:10.1186/s40364-024-00625-6 · Cited by 23
“(2) Similarly, targeting PD-1/PD-L1 can result in the overly activated immune T cells [128].”
Background
TLR 4‐induced B7‐H1 on keratinocytes negatively regulates CD 4+ T cells and CD 8+ T cells responses in oral lichen planus
Zhang, J., Tan, Y., Wei, M., Xiaojing, Y., Chen, G., Lü, R., Du, G., & Zhou, G. (2016) · Experimental Dermatology · doi:10.1111/exd.13244 · Cited by 23
The role and clinical significance of programmed cell death- ligand 1 expressed on CD19+B-cells and subsets in systemic lupus erythematosus
Jia, X., Zhu, Q., Wang, Y.-Y., Lu, Y. Z., Li, Z., Li, B., Tang, J., Wang, H.-T., Song, C., Xie, C., et al. (2018) · Clinical Immunology · doi:10.1016/j.clim.2018.11.015 · Cited by 23
T-Cell Compartmentalization and Functional Adaptation in Autoimmune Inflammation: Lessons From Pediatric Rheumatic Diseases
Mijnheer, G., & van Wijk, F. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00940 · Cited by 24
“The hyperphosphorylation of PKB/c-akt is interesting in the light of PD-1 signaling, since PD-1 is a strong negative regulator of PKB/c-akt (101).”
Background
Maternal soluble PD‐1 levels are significantly increased in women with preeclampsia
Gu, Y., Morgan, J. A., Lewis, D. F., Cooper, D. B., McCathran, C. E., & Wang, Y. (2019) · American Journal of Reproductive Immunology · doi:10.1111/aji.13193 · Cited by 23
Immune-Related Adverse Events: Pneumonitis
Jain, A., Shannon, V. R., & Sheshadri, A. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-02505-2_6 · Cited by 23
Co-inhibitory molecules: Controlling the effectors or controlling the controllers?
Thangavelu, G., Smolarchuk, C., & Anderson, C. C. (2010) · Self/Nonself · doi:10.4161/self.1.2.11548 · Cited by 22
Induction of T-Cell Infiltration and Programmed Death Ligand 2 Expression by Adeno-Associated Virus in Rhesus Macaque Skeletal Muscle and Modulation by Prednisone
Cramer, M. L., Shao, G., Rodino-Klapac, L. R., Chicoine, L. G., & Martin, P. T. (2017) · Human Gene Therapy · doi:10.1089/hum.2016.113 · Cited by 22
“Viruses often stimulate T-cell exhaustion by inducing expression of programmed cell death protein 1 (PD1) on the surface of T cells.(43) Lymphocytic choriomeningitis virus, hepatitis virus, and recombinant adeno-associated virus (rAAV) have all been shown to induce PD1 expression on CD8+ T cells after infection.”
BackgroundInfluential
ITGA5-expressing tumor cells interact with Schwann cells to drive nerve growth factor-mediated immunosuppression of NK cells
Liu, Y., Han, G., Feng, K., Lin, X., Zhong, W., Liu, Y., Wang, C., Zhang, C., & Liu, X. (2025) · Molecular Therapy · doi:10.1016/j.ymthe.2025.07.043 · Cited by 25
Checkpoint Inhibition: Will Combination with Radiotherapy and Nanoparticle-Mediated Delivery Improve Efficacy?
Lamichhane, P., Amin, N. P., Agarwal, M., & Lamichhane, N. (2018) · Medicines · doi:10.3390/medicines5040114 · Cited by 22
“This results in inhibition of proliferation, cytokine production, and cytotoxic activity of T cells, and promotes the apoptosis of T cells [5,6].”
Background
3D microenvironment attenuates simulated microgravity-mediated changes in T cell transcriptome
ElGindi, M., Sapudom, J., Laws, P., Garcia‐Sabaté, A., Daqaq, M. F., & Teo, J. C. M. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04531-8 · Cited by 20
Driver Mutations Dictate the Immunologic Landscape and Response to Checkpoint Immunotherapy of Glioblastoma
Yeo, A. T., Shah, R., Aliazis, K., Pal, R., Xu, T., Zhang, P., Rawal, S., Rose, C. M., Varn, F. S., Appleman, V. A., et al. (2023) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-22-0655 · Cited by 22
Navigating through the PD-1/PDL-1 Landscape: A Systematic Review and Meta-Analysis of Clinical Outcomes in Hepatocellular Carcinoma and Their Influence on Immunotherapy and Tumor Microenvironment
Ailia, M. J., Heo, J., & Yoo, S. Y. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076495 · Cited by 22
“Signals from the PD1 pathway help regulate T-cell activation, T-cell destiny and activities, T-cell tolerance, and the return to immunological homeostasis [12,13] (Figure 1).”
Background
Human Langerhans Cells Control Th Cells via Programmed Death-Ligand 1 in Response to Bacterial Stimuli and Nickel-Induced Contact Allergy
Hitzler, M., Majdic, O., Heine, G., Worm, M., Ebert, G., Luch, A., & Peiser, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046776 · Cited by 22
“There is strong evidence for further direct effects of PD signaling on T cell responses such as proliferation, cytolytic activity and exhaustion [19].”
A higher frequency of CD4 + CXCR5 + T follicular helper cells in patients with newly diagnosed Henoch–Schönlein purpura nephritis
Zhang, Z., Zhao, S., Zhang, L., Crew, R. M., Zhang, N., Sun, X., & Jiang, Y. (2016) · International Immunopharmacology · doi:10.1016/j.intimp.2015.12.037 · Cited by 22
Upregulation of inhibitory signaling receptor programmed death marker-1 (PD-1) in disease evolution from cutaneous lymphoid dyscrasias to mycosis fungoides and Sezary's syndrome
Nguyen, G. H., Olson, L. C., & MAGRO, C. M. J. (2017) · Annals of Diagnostic Pathology · doi:10.1016/j.anndiagpath.2017.02.003 · Cited by 22
Clinical evaluation of macrophages in cancer: role in treatment, modulation and challenges
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Immune Checkpoint Inhibition in Hodgkin Lymphoma
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“domain, and an intracellular domain bearing an immune receptor tyrosine-based inhibitory motif (ITIM).(6) PD-1 was established as a negative regulator of T cell responses through experiments”
Background
PD-1 endocytosis unleashes the cytolytic potential of checkpoint blockade in tumor immunity
Saad, E. B., Oroya, A., Anto, N. P., Bachais, M., & Rudd, C. E. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114907 · Cited by 20
Transmembrane adaptor protein PAG is a mediator of PD-1 inhibitory signaling in human T cells
Strazza, M., Azoulay‐Alfaguter, I., Peled, M., Adam, K. R., & Mor, A. (2021) · Communications Biology · doi:10.1038/s42003-021-02225-8 · Cited by 21
BRAF and MEK inhibitors differentially affect nivolumab-induced T cell activation by modulating the TCR and AKT signaling pathways
Yue, P., Harper, T. A., Bacot, S. M., Chowdhury, M., Lee, S., Akue, A. D., KuKuruga, M. A., Wang, T., & Feldman, G. M. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1512456 · Cited by 20
“PD-1 is mainly expressed on T cells, and its level of expression is increased upon cell activation.(22,23) PD-1 regulates the strength and quality of T cell responses, maintaining self-tolerance and limiting collateral tissue damage to the host in response to infection, inflammation, or other stimuli.”
Background
Glycogen synthase 3 (GSK-3) regulation of PD-1 expression and and its therapeutic implications
Krueger, J., Rudd, C. E., & Taylor, A. (2019) · Seminars in Immunology · doi:10.1016/j.smim.2019.101295 · Cited by 22
Checkpoint inhibitor immunotherapy for glioblastoma: current progress, challenges and future outlook
Gedeon, P. C., Champion, C. D., Rhodin, K. E., Woroniecka, K. I., Kemeny, H. R., Bramall, A. N., Bernstock, J. D., Choi, B. D., & Sampson, J. H. (2020) · Expert Review of Clinical Pharmacology · doi:10.1080/17512433.2020.1817737 · Cited by 21
Design, synthesis and biological evaluation of PD-1 derived peptides as inhibitors of PD-1/PD-L1 complex formation for cancer therapy
Bojko, M., Wegrzyn, K. E., Sikorska, E., Kocikowski, M., Parys, M., Battin, C., Steinberger, P., Kogut, M. M., Winnicki, M., Sieradzan, A. K., et al. (2022) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2022.106047 · Cited by 22
Improving immunotherapy for the treatment of hepatocellular carcinoma: learning from patients and preclinical models
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“It has been elucidated through mutagenetic studies that PD-1’s inhibitory effect on T cells is predominantly mediated via the activated ITSM 15 .”
The B7 Homologues and their Receptors in Hematologic Malignancies
Wilcox, R. A., Ansell, S. M., Lim, M. S., Zou, W., & Chen, L. (2012) · European Journal Of Haematology · doi:10.1111/j.1600-0609.2012.01766.x · Cited by 22
“Engagement of B7-H1 on tumor cells confers resistance to cytotoxic T-cell (CTL)mediated killing, thus functioning as a ‘molecular shield’ (43).”
Background
Progress and challenges in CRISPR-mediated therapeutic genome editing for monogenic diseases
Konishi, C. T., & Long, C. (2021) · Journal of Biomedical Research · doi:10.7555/jbr.34.20200105 · Cited by 26
Monitoring PD-1 Phosphorylation to Evaluate PD-1 Signaling during Antitumor Immune Responses
Bu, X., Juneja, V. R., Reynolds, C. G., Mahoney, K. M., Bu, M. T., McGuire, K. A., Maleri, S., Hua, P., Zhu, B., Klein, S. R., et al. (2021) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-21-0493 · Cited by 20
Vitamin D can reduce severity in COVID-19 through regulation of PD-L1
Aygün, H. (2022) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-022-02210-w · Cited by 20
“1 3 and negative signals transmitted to T cells by PD-1 and PD-L1 is critical for cellular immune responses (Riley 2009).”
BackgroundInfluential

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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