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Role of the PD-1 Pathway in the Immune Response
Open accessAbstract
Understanding immunoregulatory mechanisms is essential for the development of novel interventions to improve long-term allograft survival. Programmed death 1 (PD-1) and its ligands, PD-L1 and PD-L2, have emerged as critical inhibitory signaling pathways that regulate T cell response and maintain peripheral tolerance. PD-1 signaling inhibits alloreactive T cell activation, and can promote induced regulatory T cell development. Furthermore, the upregulation of PD-L1 on nonhematopoietic cells of the allograft may actively participate in the inhibition of immune responses and provide tissue-specific protection. In murine transplant models, this pathway has been shown to be critical for the induction and maintenance of graft tolerance. In this review, we discuss the current knowledge of the immunoregulatory functions of PD-1 and its ligands and their therapeutic potential in transplantation.
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“T cell proliferation and function can also be enhanced by blocking signalling through the inhibitory receptors such as PD-1 [77].”
From Senescence of T Lymphocytes: Implications for Enhancing Human Immunity (2016) · cites this paper as [77]
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“and this is an important strategic point because the use of PD-1/PD-L1 therapy has been reported to impair Treg cells in the renal allograft.173”
From Autoimmune diseases and immune-checkpoint inhibitors for cancer therapy: Review of the literature and personalized risk-based prevention strategy (2020) · cites this paper as [173]
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InfluentialEmerging trends and therapeutic applications of monoclonal antibodies
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“In line with this avidity requirement, there are currently no soluble agonists directed at VISTA, PD-1, or other checkpoint receptors in clinical trials (9).”
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“…is one of the major mechanisms responsible for the establishment of a tolerogenic microenvironment, which can play an important role as a therapeutic target in treatment of autoimmune and inflammatory diseases (Bour-Jordan et al., 2011; Riella et al., 2012; Bakdash et al., 2013; Hubo et al., 2013).”
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InfluentialPD-1 immunotherapy in pancreatic cancer: current status
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T-cell Exhaustion in Organ Transplantation
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“PD1 is a transmembrane receptor belonging to the CD28/CTLA-4 family that negatively interferes with TCR activation by recruiting protein tyrosine phosphatases, in particular SHP-2.(24) Both PD1 ligands, PDL1 and PDL2, inhibit TCR activation, although they differ in their interaction mechanisms with PD1.”
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BackgroundRecent progress in cancer immunotherapy approaches based on nanoparticle delivery devices
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Molecular Farming of Pembrolizumab and Nivolumab
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“Consequentially, the activation events of NF-кB and B-cell lymphoma-extra-large (Bcl-xL) are repressed, and thus the production of several cytokines, including interleukins (ILs), TNF-α and IFN-γ are inhibited [41,42].”
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BackgroundResultInfluentialPD-1 and LAG-3 Checkpoint Blockade: Potential Avenues for Therapy in B-Cell Lymphoma
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“The programmed death 1 (PD1) pathway has also emerged as an important physiologic immune checkpoint to maintain peripheral T cell tolerance and regulate adaptive immune responses particularly during chronic antigen exposure ( 14 ).”
BackgroundImmune Checkpoint Inhibitors: Fundamental Mechanisms, Current Status and Future Directions
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“PD-L1 cells and overall enhancement of their effector function through blockade of the many inhibitory mechanisms of PD-1 mentioned before [59].”
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BackgroundElevated levels of soluble PD-L1 are associated with reduced recurrence in papillary thyroid cancer
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BackgroundInflammation Determines the Capacity of Allogenic Endothelial Cells to Regulate Human Treg Expansion
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Ho, C., Chen, H., Hu, R., & Lee, P. (2019) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758835919843463 · Cited by 29
Nanotechnology-based in situ cancer vaccines: Mechanisms, design, and recent advances
Niu, G., Wang, H., Zhai, Y., Zhou, B., Kang, Y., Pei, Z., & Ji, X. (2024) · Nano Today · doi:10.1016/j.nantod.2024.102286 · Cited by 28
Sawaf, M., Dumortier, H., & Monneaux, F. (2016) · Journal of Immunology Research · doi:10.1155/2016/5767106 · Cited by 28
“The signal delivered through interaction between PD-1 on T FH and PD-L1 expressed by GC B cells is crucial for GC B cell survival [34].”
Rataj, F., Kraus, F. B. T., Chaloupka, M., Grassmann, S. A., Heise, C., Cadilha, B. L., Duewell, P., Endres, S., & Kobold, S. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01955 · Cited by 31
“PD-1 signaling mediates T cell suppression that prevents autoimmunity under physiological conditions and is therefore a key immune checkpoint on CD4+ and CD8+ T cells (21, 22).”
BackgroundPD-L1/PD-1 crosstalk in colorectal cancer: are we targeting the right cells?
Cantero-Cid, R., Casas-Martín, J., Hernández-Jiménez, E., Cubillos‐Zapata, C., Varela-Serrano, A., Ortiz, J. A., Casarrubios, M., Montalbán-Hernández, K. M., Villacañas-Gil, I., Guerra, L., et al. (2018) · BMC Cancer · doi:10.1186/s12885-018-4853-0 · Cited by 28
Islam, M. K., & Stanslas, J. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107870 · Cited by 31
Borges, T. J., Murakami, N., Lape, I. T., Gassen, R. B., Liu, K., Cai, S., Daccache, J., Safa, K., Shimizu, T., Ohori, S., et al. (2021) · JCI Insight · doi:10.1172/jci.insight.142909 · Cited by 28
“(TCR), and its expression is decreased once the antigen is cleared (2, 3).”
Self-citationDo inhibitory immune receptors play a role in the etiology of autoimmune disease?
Nordkamp, M. J. M. O., Koeleman, B. P. C., & Meyaard, L. (2013) · Clinical Immunology · doi:10.1016/j.clim.2013.11.007 · Cited by 29
Huang, L., Deng, X., Chang, F., Wu, X., Wu, Y., & Diao, Q. (2018) · Medicine · doi:10.1097/md.0000000000012858 · Cited by 28
Kamrani, S., Naseramini, R., Khani, P., Razavi, Z. S., Afkhami, H., Atashzar, M. R., Nasri, F., Alavimanesh, S., Saeidi, F., & Ronaghi, H. (2025) · Cancer Cell International · doi:10.1186/s12935-025-03741-x · Cited by 27
“PD-1 has two ligands: PD-L1 (B7-H1; CD274) and PD-L2 (B7-DC; CD273) [191].”
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T-cell co-stimulatory blockade in transplantation: two steps forward one step back!
Riella, L. V., & Sayegh, M. H. (2013) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2013.845661 · Cited by 28
“Similar picture is also seen in the family of co-inhibitory pathways, which are composed of programmed death ligand (PDL):programmed death-1 (PD1), B7:CTLA4, TIM3:Galectin9, among others [14,18-26].”
BackgroundSelf-citationRepositioning of Immunomodulators: A Ray of Hope for Alzheimer’s Disease?
Munafò, A., Burgaletto, C., Benedetto, G. D., Mauro, M. D., Mauro, R. D., Bernardini, R., & Cantarella, G. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.614643 · Cited by 27
Nanobodies Enhancing Cancer Visualization, Diagnosis and Therapeutics
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“Upon antigen presentation and TCR engagement, PD-1 expression is upregulated [88]; thereafter, PD-1 may bind to a PD-1 ligand (PD-L1 or PD-L2) [17,88,89].”
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An update on pathogenesis of systemic lupus erythematosus.
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Immune Checkpoint Inhibitors in the Cancer Patient with An Organ Transplant
Wanchoo, R., Riella, L. V., Uppal, N. N., Lopez, C. A., Nair, V. V., Devoe, C., & Jhaveri, K. D. (2017) · Journal of Onco-Nephrology · doi:10.5301/jo-n.5000006 · Cited by 26
“Pre-clinical studies have suggested the importance of PD-1 and its ligands in influencing allograft adaptive tolerance to transplants (27).”
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Prospects for NK Cell Therapy of Sarcoma
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“Programmed cell death protein 1 (PD-1) is a well-known checkpoint molecule, functioning as a “break” in the immune system [131].”
BackgroundChohan, M. H., Perry, M., Laurance-Young, P., Salih, V. M., & Foey, A. (2023) · British Journal of Biomedical Science · doi:10.3389/bjbs.2023.11065 · Cited by 25
“PD-1 ligation suppresses T-cell function via an inhibitory signal involving SHP-2 which inhibits CD28-mediated PI3K and Akt activity (35).”
Bandini, S., Ulivi, P., & Rossi, T. (2024) · Cells · doi:10.3390/cells13040337 · Cited by 27
“The PD-1 checkpoint is expressed on the surface of several activated immune cells, including macrophages, dendritic cells (DCs), Langerhans cells, B cells, and T cells, and plays a fundamental role in the regulation of T cell-mediated responses through programmed death signaling [17].”
BackgroundMLL3 enhances the transcription of PD-L1 and regulates anti-tumor immunity
Xiong, W., Deng, H., Huang, C., Zen, C., Jian, C., Ye, K., Zhong, Z., Zhao, X., & Zhu, L. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.10.027 · Cited by 25
Tähtinen, S., Blattner, C., Vähä-Koskela, M. J. V., Saha, D., Siurala, M., Parviainen, S., Utikal, J. S., Kanerva, A., Umansky, V., & Hemminki, A. (2016) · Journal of Immunotherapy · doi:10.1097/cji.0000000000000144 · Cited by 26
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
“This negative feedback regulation allows cancer cells to escape immune surveillance [23].”
BackgroundDecidua Basalis Mesenchymal Stem Cells Favor Inflammatory M1 Macrophage Differentiation In Vitro
Abumaree, M., Harthy, S. A., Subayyil, A. M. A., Alshabibi, M. A., Abomaray, F., Khatlani, T., Kalionis, B., El-Muzaini, M. F., Jumah, M. A., Jawdat, D. M., et al. (2019) · Cells · doi:10.3390/cells8020173 · Cited by 25
“…observation, we demonstrated that ICDBMSCs decreased macrophage expression of CD273 and CD274 (Figure 4D,E), which are ligands for the inhibitory programmed death 1 (PD-1) receptor that signal to inhibit the function of T cells and to induce development of immunosuppressive regulatory T cells [34].”
Liao, P., Wang, H., Tang, Y., Tang, Y.-J., & Liang, X. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02457 · Cited by 27
“PD-L1 expresses mainly on T cells, B cells, DCs and macrophages (95), while on some tumors surface, such as glioblastoma multiforme, NSCLC and some hematologic malignancies (96, 97).”
BackgroundSong, M., Sun, W., Liu, Q., Wang, Z., & Zhang, H. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1306232 · Cited by 24
Li, C. P. I., Fan, Y., & Chen, X. (2026) · npj Biofilms and Microbiomes · doi:10.1038/s41522-026-00912-0 · Cited by 29
“…T cells 58 (Tregs, immune cells that suppress excessive immune activation), upregulating programmed death-1 59 (PD-1, an inhibitory receptor on cells)/ programmed death-ligand 1 (PD-L1, its ligand) signaling, and inhibiting the expression of interleukin-2…”
Qiu, J., Tang, W., & Du, C. (2020) · Current Cancer Drug Targets · doi:10.2174/1568009620666200520084415 · Cited by 24
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Serafini, B., Benincasa, L., Rosicarelli, B., & Aloisi, F. (2024) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2024.578314 · Cited by 23
“…is expressed or inducible in different cell types, including antigen-presenting cells, lymphocytes and stromal cells; it engages its receptor PD-1 on the T cell surface to inhibit T cell activation (proliferation, cytokine production, cytolytic function) (Riella et al., 2012; Pauken et al., 2021).”
BackgroundTriggering of CD99 on monocytes by a specific monoclonal antibody regulates T cell activation
Laopajon, W., Pata, S., Takheaw, N., Surinkaew, S., Khummuang, S., & Kasinrerk, W. (2018) · Cellular Immunology · doi:10.1016/j.cellimm.2018.10.012 · Cited by 23
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Greisen, S. R., Aspari, M., & Deleuran, B. W. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.883733 · Cited by 25
“If the presented antigen resembles self or is of low affinity, upregulation of coinhibitory receptors (CIR), including programmed death-1 (PD-1) and cytotoxic T-lymphocyte-associated protein 4 (CTLA-4) will be more pronounced (5, 6).”
BackgroundApoptotic bodies inhibit inflammation by PDL1–PD1 ‐mediated macrophage metabolic reprogramming
Jiang, T., Xia, Y., Wang, W., Zhao, J., Liu, W., Liu, S., Shi, S., Li, B., He, X., & Jin, Y. J. (2023) · Cell Proliferation · doi:10.1111/cpr.13531 · Cited by 22
“26,27 In addition, exosomal PDL1 binds to PD1 on T cells, acting as an immunosuppressant that promotes wound healing.”
BackgroundKempe, K., Xiang, S. D., Wilson, P., Rahim, M. A., Ju, Y., Whittaker, M. R., Haddleton, D. M., Plebanski, M., Caruso, F., & Davis, T. P. (2017) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.6b15459 · Cited by 23
Metadata
- Authors
- Riella, L. V., Paterson, A. M., Sharpe, A. H., & Chandraker, A.
- Affiliations
- Brigham and Women's Hospital (US)
- Corresponding author
- Riella, L.V.
- Venue
- American Journal of Transplantation
- Publisher
- Elsevier BV
- Published
- 2012-10
- Volume
- 12
- Issue
- 10
- Pages
- 2575-2587
- ISSN
- 1600-6135 (ISSN-L)
- PMC
- PMC3784243
- OpenAlex
- W2144601357
- Cited by
- 444
- References
- 132
- Citations by year
- 2026: 25 · 2025: 25 · 2024: 39 · 2023: 35 · 2022: 33 · 2021: 40 · 2020: 38 · 2019: 36 · 2018: 42 · 2017: 50 · 2016: 25 · 2015: 22 · 2014: 21 · 2013: 13
- FWCI
- 1.65
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- American Journal of Transplantation (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- American Heart Association
- National Institute of Allergy and Infectious Diseases (R01AI051559, P01 AI 56299, R01 AI-51559, P01AI056299)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Surgery › Transplantation: Methods and Outcomes
- Keywords
- PD-1 pathway, PD-L1, PD-L2, allograft tolerance, immune regulation, regulatory T cells, peripheral tolerance, graft survival
- MeSH terms
- Graft Survival, Humans, Immune Tolerance, Lymphocyte Activation, Signal Transduction, Organ Transplantation, T-Lymphocytes, Regulatory, Programmed Cell Death 1 Receptor
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