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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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Stikvoort, A., Gaballa, A., Solders, M., Nederlof, I., Önfelt, B., Sundberg, B., Remberger, M., Sundin, M., Mattsson, J., & Uhlin, M. (2017) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2017.11.026 · Cited by 19
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“PD-1 is an inhibitory molecule that suppresses the proliferation of T-cells and the effector functions of activated T-cells through interaction with its ligand, the programmed death-ligand 1 (PD-L1).(4) PD-L1 exhibits a broad tissue distribution and can provide inhibitory signals to PD-1+ immune cells for suppressing…”
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“, 2004), provides inhibitory signals that control autoimmune responses by maintaining immune tolerance to self-anti-gens (Riella et al., 2012).”
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“PD-1 receptor can interact with two ligands, PD-L1 (CD274) and PD-L2 (CD273), which are also expressed on cell surface like immunoglobulin transmembrane receptors (63).”
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“Therefore, the successful implantation and transfer of ectopic endometrium outside the uterus is closely related to immune tolerance, especially the immune tolerance caused by PD-1/PD-L1 and IL-27 overexpression [42–44].”
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“…immunoglobulin suppressor of T cell activation (VISTA), B and T lymphocyte attenuator (BTLA), and signal regulatory protein alpha (SIRPα) are frequently upregulated on T cells and other immune cell subsets, and emerged as key immunosuppressive regulators to dampen anti-tumor immunity [2–8].”
PD-L1: Can it be a biomarker for the prognosis or a promising therapeutic target in cervical cancer?
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“PD-1 PD-1 is a checkpoint receptor that is upregulated in T cells after T-cell receptor stimulation (26).”
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Pluchart, H., Chanoine, S., Moro‐Sibilot, D., CHOUAID, C., Frey, G., Villa, J., Degano, B., Levra, M. G., Bedouch, P., & Toffart, A. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1016976 · Cited by 12
“Given the protective role of PD-(L) 1 signaling in immune tolerance (Riella et al., 2012), auto-immune diseases can appear or worsen with PD-(L)1 inhibitors.”
BackgroundImmune checkpoint inhibitors in kidney transplantation
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“Many preclinical studies have shown a crucial role of coinhibitory signals in protecting the allograft against rejection (reviewed in [25,46]).”
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“In contrast to CNI, mTORi offers multiple advantages such as anti-tumor activity 24 and preservation of Treg development 23 that is a key mediator of graft tolerance, which is strategically important because the use of PD-1/PD-L1 therapy was reported to impair Treg cells in the renal allograft 25 .”
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Programmed Death 1 (PD-1) and PD-1 Ligand (PD-L1) Expression in Chronic Apical Periodontitis
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“The PD-1 signaling has a critical role in limiting the effectiveness of antigen-specific T cells during other persisting infections and cancer (12).”
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Sarvari, J., Dowran, R., Hosseini, S. Y., Fattahi, M. R., & Erfani, N. (2018) · EXCLI journal · doi:10.17179/excli2018-1394 · Cited by 11
“3 (Riella et al., 2012).”
Soellradl, I., Kehrer, H., & Cejka, D. (2020) · Transplantation Proceedings · doi:10.1016/j.transproceed.2019.09.014 · Cited by 11
Franceschini, T., Vasuri, F., Muratori, P., Muratori, L., Guido, M., Lenzi, M., & D’Errico, A. (2021) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s00428-021-03122-5 · Cited by 11
Didié, M., Galla, S., Muppala, V., Dressel, R., & Zimmermann, W. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00955 · Cited by 11
“The PD-1/PD-L1 pathway plays an important role in immune regulation and may contribute to the immune escape of transplanted cells (23).”
BackgroundHimmelsbach, V., Koch, C., Trojan, J., & Finkelmeier, F. (2024) · Journal of Hepatocellular Carcinoma · doi:10.2147/jhc.s443218 · Cited by 10
Advancing Adjuvant Immunotherapy in Hepatocellular Carcinoma: A Comprehensive Review
Akabane, M., Chatzipanagiotou, O. P., Imaoka, Y., Schenk, A. D., & Pawlik, T. M. (2025) · ImmunoTargets and Therapy · doi:10.2147/itt.s528709 · Cited by 10
“156,157 This observation has led some experts to suggest anti-CTLA-4 therapies as a safer alternative for patients where preserving graft function is paramount.”
Harakal, J., Qiao, H., Wheeler, K. M., Rival, C. M., Paul, A., Hardy, D. M., Cheng, C. Y., Goldberg, E., & Tung, K. S. K. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.809247 · Cited by 10
“In addition, we showed that the Treg induction in uni-Vx is affected in mice with genetic deficiency in PD1 ligand and not in PD1, a finding consistent with the involvement of iTregs in post-transplantation tolerance (51).”
ResultIL-15 temporally reorients IL-10 biased B-1a cells toward IL-12 expression
Ghosh, A. K., Sinha, D., Mukherjee, S., Biswas, R., & Biswas, T. (2015) · Cellular and Molecular Immunology · doi:10.1038/cmi.2015.08 · Cited by 10
Wong, K., Shen, J., DâAmbruoso, S., Stefanoudakis, D., & Drakaki, A. (2019) · Transplantation Proceedings · doi:10.1016/j.transproceed.2019.08.002 · Cited by 10
Mastoridis, S., Martínez‐Llordella, M., & Fueyo, A. S. (2020) · World Journal of Transplantation · doi:10.5500/wjt.v10.i11.330 · Cited by 10
Kemal, Y., Çalışkan, S., Gün, S., & Kefeli, M. (2021) · Turkish Journal of Pathology · doi:10.5146/tjpath.2021.01558 · Cited by 10
“Immunotherapy with checkpoint inhibitors targeting Programmed death receptor-1 (PD-1) and Programmed death-ligand 1 (PD-L1) have been used effectively for the treatment of various tumors as a promising alternative for cancer management and found to be associated with the prognosis of the patients (7-12).”
BackgroundSako, Y., Hirono, S., & Yamaotsu, N. (2018) · SDRP Journal of Computational Chemistry & Molecular Modelling · doi:10.25177/jccmm.3.1.1 · Cited by 10
“tains self-tolerance and limits collateral tissue damage [3].”
BackgroundLiu, L., Zhang, Q., Chen, P., Guo, N., Song, A., Huang, X., Xia, W., Li, L., Moog, C., Wu, H., et al. (2019) · BMC Immunology · doi:10.1186/s12865-019-0319-7 · Cited by 12
“PD-1 signaling may also occur independently of T-cell or B-cell antigen receptor signaling [14].”
BackgroundShen, T. H., Zheng, S., Geng, L., Liu, Z., Xu, J., Lin, B., Qian, J., & Zheng, S. (2020) · Technology in Cancer Research & Treatment · doi:10.1177/1533033820979703 · Cited by 10
“Of the PD-L1-positive BTC patients enrolled in the KEYNOTE028 study, 17% had positive responses to pembrolizumab monotherapy.(16) The present study determined the potential positive effects of camrelizumab on treatment of Chinese patients with Shen et al 5”
BackgroundResultTherapeutic nexus of T cell immunometabolism in improving transplantation immunotherapy
Kazmi, S., Khan, M. A., Shamma, T., Altuhami, A., Assiri, A. M., & Broering, D. C. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.108621 · Cited by 9
Barbir, E., Abdulmoneim, S., Dudek, A. Z., & Kukla, A. (2024) · Transplant International · doi:10.3389/ti.2024.13322 · Cited by 9
Targeting Triple Negative Breast Cancer With Oncolytic Adenoviruses
Green-Tripp, G., Nattress, C. B., & Halldén, G. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.901392 · Cited by 9
Gao, Y., Duan, R., Li, H., Jiang, L., Tao, T., Liu, X., Zhu, L., Li, Z., Chen, B., Zheng, S. G., et al. (2023) · iScience · doi:10.1016/j.isci.2023.106729 · Cited by 9
“Overall, we constructed a transcriptional atlas of CDLNs to provide a basis for investigating the mechanisms of action of GMSCs. Immunosuppressive effect of GMSCs on T cell subsets To further analyze the T cell subsets, T cells were subdivided into nine subpopulations: (1) CD4+ naive T cells, (2) T helper 1 (Th1) cell…”
ResultInfluentialSekino, M., Iwadate, M., Yamaya, Y., Matsumoto, Y., Suzuki, S., Mizunuma, H., Nakano, K., Nakamura, I., & Suzuki, S. (2023) · Cancers · doi:10.3390/cancers15133449 · Cited by 9
“We used the data of blood samples and archival samples from all 33 patients with thyroid cancer who were newly diagnosed as having thyroid cancer and had undergone surgery or biopsy at Fukushima Medical University between January 2011 and January 2013 [27,28].”
MethodDurán, I., Castellano, D., Puente, J., Martín-Couce, L., Bello, E., Anido, U., Mas, J. M., & Costa, L. (2022) · Oncotarget · doi:10.18632/oncotarget.28183 · Cited by 11
“This results in an inhibitory effect on immunosuppressor factors, such as IL10, IL6, GAS6, ARG1, EZH2 or HIF1A; and activation of immunostimulatory molecules, including IFNG and IL2, over a plethora of cell types in the tumour microenvironment (Supplementary Figure 1, Supplementary Table 5, Table 5, Figure 3).”
BackgroundInfluentialWu, B., Fu, X., Huang, B. S., Tong, X., Zheng, H., Huang, S., & Lü, F. (2014) · Parasitology Research · doi:10.1007/s00436-014-3764-5 · Cited by 9
Cancer Imaging with Radiolabeled Monoclonal Antibodies
Harsini, S., & Rezaei, N. (2020) · Springer eBooks · doi:10.1007/978-3-030-30845-2_32 · Cited by 9
Xu, C., Sun, Z., Zhang, X., Zang, Q., Yang, Z., Li, L., Yang, X., He, Y., Ma, Z., & Chen, J. (2024) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2024.107376 · Cited by 8
BRD4 promotes immune escape of glioma cells by upregulating PD-L1 expression
Liu, Y., Cai, L., Wang, H., Yao, L., Wu, Y., Zhang, K., Su, Z., & Zhou, Y. (2024) · Journal of Neuro-Oncology · doi:10.1007/s11060-024-04889-8 · Cited by 8
“PD-L1 is a protein that plays a crucial role in regulating the immune system by binding to its receptor PD-1, thus inhibiting T cell activity and preventing the immune system from attacking the body’s own cells [21].”
Donor Variability and PD-1 Expression Limit BK Polyomavirus-specific T-cell Function and Therapy
Wilhelm, M., Kaur, A., Geng, A., Wernli, M., & Hirsch, H. H. (2025) · Transplantation · doi:10.1097/tp.0000000000005399 · Cited by 8
“55,56 Perhaps the most striking dilemma arises when solid organ transplantation is complicated by malignancies of poor prognosis, for which immune checkpoint inhibitors have shown significant benefit in nontransplant patients.”
Dushime, H., Moreno, S. G., Linard, C., Adrait, A., Couté, Y., Peltzer, J., Messiaen, S., Torres, C., Bensemmane, L., Lewandowski, D., et al. (2023) · Stem Cell Research & Therapy · doi:10.1186/s13287-023-03425-1 · Cited by 10
Pourali, G., Zafari, N., Velayati, M., Mehrabadi, S., Maftooh, M., Hassanian, S. M., Mobarhan, M. G., Ferns, G. A., Avan, A., & Khazaei, M. (2023) · Current Drug Targets · doi:10.2174/0113894501264450231129042256 · Cited by 9
Harnessing the immunotherapeutic potential of T-lymphocyte co-signaling molecules in transplantation
Ansari, A. W., Khan, M. A., Schmidt, R. E., & Broering, D. C. (2017) · Immunology Letters · doi:10.1016/j.imlet.2017.01.008 · Cited by 8
Sunshine, J. C., Sosman, J. A., Shetty, A. A., & Choi, J. N. (2020) · Journal of Immunotherapy · doi:10.1097/cji.0000000000000319 · Cited by 8
Chen, D., Wen, Y.-H., Wang, W., & Lin, W.-T. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12062157 · Cited by 8
Khalifian, S., Raimondi, G., Lee, W. A., & Brandacher, G. (2014) · Immunotherapy · doi:10.2217/imt.14.25 · Cited by 8
Zafar, S., Shehzadi, R., Dawood, H., Maqbool, M., Sarfraz, A., & Sarfraz, Z. (2024) · Therapeutic Advances in Medical Oncology · doi:10.1177/17588359231221339 · Cited by 7
“24,25 32 We see the landscape changing with immunotherapy playing a key role as a combination treatment.”
BackgroundTargeted Delivery of BMS-1166 for Enhanced Breast Cancer Immunotherapy
Yu, Z., Zhou, Z., & Zhao, Y. (2025) · International Journal of Nanomedicine · doi:10.2147/ijn.s497089 · Cited by 7
Deepak, H. B., Prince, S. E., & Deshpande, P. (2022) · Indian Journal of Pharmacology · doi:10.4103/ijp.ijp_1089_20 · Cited by 7
“[4] The best inhibitory pathway for T‑cell activation is CD80/CD86‑CTLA‑4.”
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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