Cited by 681Cancer Immunotherapy and BiomarkersT-cell and B-cell ImmunologyImmunotherapy and Immune Responses

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Regulation of PD-L1 expression in the tumor microenvironment

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Yi, Ming, Niu, Mengke, Xu, Linping, Luo, Suxia, Wu, Kongming·2021·Journal of Hematology & Oncology

DOI 10.1186/s13045-020-01027-5PMC PMC7792099

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Abstract

Programmed death-ligand 1 (PD-L1) on cancer cells engages with programmed cell death-1 (PD-1) on immune cells, contributing to cancer immune escape. For multiple cancer types, the PD-1/PD-L1 axis is the major speed-limiting step of the anti-cancer immune response. In this context, blocking PD-1/PD-L1 could restore T cells from exhausted status and eradicate cancer cells. However, only a subset of PD-L1 positive patients benefits from α-PD-1/PD-L1 therapies. Actually, PD-L1 expression is regulated by various factors, leading to the diverse significances of PD-L1 positivity. Understanding the mechanisms of PD-L1 regulation is helpful to select patients and enhance the treatment effect. In this review, we focused on PD-L1 regulators at the levels of transcription, post-transcription, post-translation. Besides, we discussed the potential applications of these laboratory findings in the clinic.

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Fig. 1 The regulators of PD-L1 expression. PD-L1 abundance is regulated by genomic alterations (amplification or translocation), epigenetic modifications (methylation of histone or CpG island, and histone acetylation), transcriptional regulation (inflammatory stimuli and oncogenic signals), post-transcriptional regulation (miRNA, the status of 3′- UTR, RAS, and Angiotensin II), and post-translational modification (ubiquitination, phosphorylation, glycosylation, palmitoylation). H3K4me3: tri-methylation of histone H3 on lysine 4; H3K27me3: tri-methylation of histone H3 on lysine 27; EGFR: epidermal growth factor receptor; IRF: interferon-responsive factor; IFN: interferon; DSB: double-strand break; GSK3β: glycogen synthase kinase 3β; PI3K: phosphoinositide 3-kinase; NF-κB: Nuclear factor kappa-B; HIF-1α: hypoxia-inducible factor-1α; ALK: Anaplastic lymphoma kinase; ER: endoplasmic reticulumCC BY · PubMed Central

Fig. 2 The current immune checkpoint inhibitor therapy could be further enhanced by regulating PD-L1 expression. Agents regulating PD-L1 expression might have a synergistic effect with the current immune checkpoint inhibitors. For example, targeting therapies such as CDK4/6 inhibitor upregulated PD-L1 expression and promoted immune escape. This treatment-induced immune evasion could be overcome by combination therapies containing α-PD-1/PD-L1 (the left panel). Besides, adjuvant treatment regulating PD-L1 expression might elevate the sensitivity to α-PD-1/PD-L1 or other immune checkpoint inhibitors. For instance, metformin downregulated PD-L1 by promoting endoplasmic-reticulum-associated degradation, and the combination therapy of metformin and α-CTLA-4 had a synergistic antitumor activity (the right panel). CDK: cyclin-dependent kinase; CTLA-4: cytotoxic T Lymphocyte antigen 4; ER: endoplasmic reticulumCC BY · PubMed Central

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PD-L1 is upregulated by EBV-driven LMP1 through NF-κB pathway and correlates with poor prognosis in natural killer/T-cell lymphoma
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miR-424(322) reverses chemoresistance via T-cell immune response activation by blocking the PD-L1 immune checkpoint
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Palmitoylation stabilizes PD-L1 to promote breast tumor growth
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Phosphorylated RB Promotes Cancer Immunity by Inhibiting NF-κB Activation and PD-L1 Expression
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The MLL1-H3K4me3 Axis-Mediated PD-L1 Expression and Pancreatic Cancer Immune Evasion
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The role of cancer-derived microRNAs in cancer immune escape
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Inhibition of ATM reverses EMT and decreases metastatic potential of cisplatin-resistant lung cancer cells through JAK/STAT3/PD-L1 pathway
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Glioblastoma-Derived IL6 Induces Immunosuppressive Peripheral Myeloid Cell PD-L1 and Promotes Tumor Growth
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Reactive oxygen species modulate macrophage immunosuppressive phenotype through the up-regulation of PD-L1
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Targeting DNA Methylation and EZH2 Activity to Overcome Melanoma Resistance to Immunotherapy
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PD-L1 expression is regulated by both DNA methylation and NF-kB during EMT signaling in non-small cell lung carcinoma
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MET Inhibitors Promote Liver Tumor Evasion of the Immune Response by Stabilizing PDL1
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EZH2 negatively regulates PD-L1 expression in hepatocellular carcinoma
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Endoplasmic reticulum stress‐induced exosomal miR‐27a‐3p promotes immune escape in breast cancer via regulating PD‐L1 expression in macrophages
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A novel bifunctional anti-PD-L1/TGF-β Trap fusion protein (M7824) efficiently reverts mesenchymalization of human lung cancer cells
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PD-L1 Is Upregulated by Simultaneous Amplification of the PD-L1 and JAK2 Genes in Non–Small Cell Lung Cancer
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Gut microbiome modulates efficacy of immune checkpoint inhibitors
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IL-6 promotes PD-L1 expression in monocytes and macrophages by decreasing protein tyrosine phosphatase receptor type O expression in human hepatocellular carcinoma
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Epstein−Barr virus-encoded EBNA2 alters immune checkpoint PD-L1 expression by downregulating miR-34a in B-cell lymphomas
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MAPK pathway activity plays a key role in PD‐L1 expression of lung adenocarcinoma cells
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IFNγ induces PD-L1 overexpression by JAK2/STAT1/IRF-1 signaling in EBV-positive gastric carcinoma
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miR-142-5p regulates tumor cell PD-L1 expression and enhances anti-tumor immunity
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MiR-873/PD-L1 axis regulates the stemness of breast cancer cells
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IL-27 induces the expression of IDO and PD-L1 in human cancer cells
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Glycosylation Changes in Brain Cancer
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Control of PD-L1 expression by miR-140/142/340/383 and oncogenic activation of the OCT4–miR-18a pathway in cervical cancer
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Inhibition of IL‐6‐JAK/Stat3 signaling in castration‐resistant prostate cancer cells enhances the NK cell‐mediated cytotoxicity via alteration of PD‐L1/NKG2D ligand levels
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MUC1-C integrates PD-L1 induction with repression of immune effectors in non-small-cell lung cancer
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Upregulation of PD-L1 via HMGB1-Activated IRF3 and NF-κB Contributes to UV Radiation-Induced Immune Suppression
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HDAC3 inhibition upregulates PD-L1 expression in B-cell lymphomas and augments the efficacy of anti-PD-L1 therapy
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miRNA-148a-3p Regulates Immunosuppression in DNA Mismatch Repair–Deficient Colorectal Cancer by Targeting PD-L1
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MYC expression correlates with PD-L1 expression in non-small cell lung cancer
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Functional loss of ARID1A is tightly associated with high PD‐L1 expression in gastric cancer
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Genomic Amplification of CD274 (PD-L1) in Small-Cell Lung Cancer
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Interferon regulatory factor 1 (IRF-1) and IRF-2 regulate PD-L1 expression in hepatocellular carcinoma (HCC) cells
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Oncofetal gene SALL4 reactivation by hepatitis B virus counteracts miR-200c in PD-L1-induced T cell exhaustion
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A regulatory role for the co-chaperone FKBP51s in PD-L1 expression in glioma
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Enhanced histone H3 acetylation of the PD-L1 promoter via the COP1/c-Jun/HDAC3 axis is required for PD-L1 expression in drug-resistant cancer cells
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Marked Global DNA Hypomethylation Is Associated with Constitutive PD-L1 Expression in Melanoma
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PD-L1 (CD274) promoter methylation predicts survival in colorectal cancer patients
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Italian Nivolumab Expanded Access Program in Nonsquamous Non–Small Cell Lung Cancer Patients: Results in Never-Smokers and EGFR-Mutant Patients
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Crosstalk of intracellular post-translational modifications in cancer
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MiR-140 Expression Regulates Cell Proliferation and Targets PD-L1 in NSCLC
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The miR‐3127‐5p/p‐ STAT 3 axis up‐regulates PD ‐L1 inducing chemoresistance in non‐small‐cell lung cancer
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TGF-β of lung cancer microenvironment upregulates B7H1 and GITRL expression in dendritic cells and is associated with regulatory T cell generation
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LPS promotes the expression of PD‐L1 in gastric cancer cells through NF‐κB activation
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PD‐L1 methylation regulates PD‐L1 expression and is associated with melanoma survival
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TNF-α and TGF-β Counter-Regulate PD-L1 Expression on Monocytes in Systemic Lupus Erythematosus
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Radiation alters PD-L1/NKG2D ligand levels in lung cancer cells and leads to immune escape from NK cell cytotoxicity via IL-6-MEK/Erk signaling pathway
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JAK2 and PD-L1 Amplification Enhance the Dynamic Expression of PD-L1 in Triple-negative Breast Cancer
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Romidepsin (FK228) regulates the expression of the immune checkpoint ligand PD-L1 and suppresses cellular immune functions in colon cancer
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Synergistic effects of IL-4 and TNFα on the induction of B7-H1 in renal cell carcinoma cells inhibiting allogeneic T cell proliferation
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Oral squamous cell carcinoma suppressed antitumor immunity through induction of PD-L1 expression on tumor-associated macrophages
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Epstein–Barr virus-encoded miR-BART5-5p upregulates PD-L1 through PIAS3/pSTAT3 modulation, worsening clinical outcomes of PD-L1-positive gastric carcinomas
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Synergistic inhibition of pancreatic cancer with anti-PD-L1 and c-Myc inhibitor JQ1
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Targeting glycosylation of PD-1 to enhance CAR-T cell cytotoxicity
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PD-L1 (CD274) and PD-L2 (PDCD1LG2) promoter methylation is associated with HPV infection and transcriptional repression in head and neck squamous cell carcinomas
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MicroRNA-497-5p down-regulation increases PD-L1 expression in clear cell renal cell carcinoma
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Cisplatin-mediated down-regulation of miR-145 contributes to up-regulation of PD-L1 via the c-Myc transcription factor in cisplatin-resistant ovarian carcinoma cells
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Correlation of MET gene amplification and TP53 mutation with PD-L1 expression in non-small cell lung cancer
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MYC inhibition increases PD-L1 expression induced by IFN-γ in hepatocellular carcinoma cells
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Control of pathogenic effector T-cell activities in situ by PD-L1 expression on respiratory inflammatory dendritic cells during respiratory syncytial virus infection
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EGFR or HER2 inhibition modulates the tumor microenvironment by suppression of PD-L1 and cytokines release
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PD-L1 expression is associated with ALK positivity and STAT3 activation, but not outcome in patients with systemic anaplastic large cell lymphoma
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Silibinin down-regulates PD-L1 expression in nasopharyngeal carcinoma by interfering with tumor cell glycolytic metabolism
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MiR-214 prevents the progression of diffuse large B-cell lymphoma by targeting PD-L1
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MET Receptor Tyrosine Kinase Regulates the Expression of Co-Stimulatory and Co-Inhibitory Molecules in Tumor Cells and Contributes to PD-L1-Mediated Suppression of Immune Cell Function
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C-Myc regulates PD-L1 expression in esophageal squamous cell carcinoma.
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TGF-Beta Treatment Modulates PD-L1 and CD40 Expression in Proximal Renal Tubular Epithelial Cells and Enhances CD8+ Cytotoxic T-Cell Responses
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MicroRNA-200a induces immunosuppression by promoting PTEN-mediated PD-L1 upregulation in osteosarcoma
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Increased PD-L1 expression in erlotinib-resistant NSCLC cells with MET gene amplification is reversed upon MET-TKI treatment
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PD-L1 Expression Is Regulated By NF-κB During EMT Signaling In Gastric Carcinoma
Xu, D., Li, J., Li, R., Lan, T., Xiao, C., & Gong, P. (2019) · OncoTargets and Therapy · doi:10.2147/ott.s224053 · Cited by 34
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Authors: Yi, M., Niu, M., Xu, L., Luo, S., & Wu, K.
Affiliations: Tongji Hospital (CN)
Zhengzhou University (CN)
Corresponding author: Luo, Suxia
Wu, Kongming
ORCID: Yi, Ming
Niu, Mengke
Luo, Suxia
Wu, Kongming
Venue: Journal of Hematology & Oncology
Publisher: Springer Science and Business Media LLC
Published: 2021-01-07
Volume: 14
Issue: 1
Pages: 10-10
ISSN: 1756-8722 (ISSN-L)
DOI: 10.1186/s13045-020-01027-5
PMC: PMC7792099
OpenAlex: W3118950316
Cited by: 681
References: 153
Citations by year: 2026: 114 · 2025: 108 · 2024: 169 · 2023: 130 · 2022: 113 · 2021: 47
FWCI: 13.99
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Journal of Hematology & Oncology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Natural Science Foundation of China (81874120, 82073370)
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 › Immunotherapy and Immune Responses
Keywords: PD-L1, PD-1/PD-L1 axis, tumor microenvironment, tumor immune evasion, transcriptional regulation, post-transcriptional regulation, post-translational regulation, T cell exhaustion, immune checkpoint inhibitors, predictive biomarkers
MeSH terms: Animals, Humans, Neoplasms, Protein Processing, Post-Translational, Transcriptional Activation, Gene Expression Regulation, Neoplastic, Tumor Escape, Epigenesis, Genetic, Tumor Microenvironment, B7-H1 Antigen

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Regulation of PD-L1 expression in the tumor microenvironment

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