Increased PD-L1 Restricts Liver Injury in Nonalcoholic Fatty Liver Disease - PubMed (original) (raw)

Increased PD-L1 Restricts Liver Injury in Nonalcoholic Fatty Liver Disease

Gang Dong et al. Oxid Med Cell Longev. 2022.

Abstract

PD-L1 is a critical checkpoint that protects tissues from autoimmune injury. Nevertheless, the role of PD-L1 in nonalcoholic fatty liver disease- (NAFLD-) induced liver damage is still unclear. In this study, we examined the role and mechanism of PD-L1 expression on NAFLD-induced liver damage in vitro and in vivo. PD-L1 expression in the livers from patients with NAFLD, and LO2 cells treated by FFA, was significantly increased. FFA triggers a large amount of ROS (generated from NOX4 and damaged mitochondria), promoting the ZNF24 expression and suppressing ZN24 sumoylation, both of which enhance the PD-L1 transcription and expression. The knockdown of PD-L1 increases CD8 + T cells' damage to FFA-treated LO2 cells, while its upregulation limits the liver injury in NAFLD models. Collectively, we demonstrate that FFA promotes PD-L1 expression through the ROS/ZNF24 pathway and suppresses UBE2I-mediated ZNF24 sumoylation to enhance its transcriptional activity of PD-L1. PD-L1 upregulation limits FFA-induced injury of hepatocytes in vitro and in vivo.

Copyright © 2022 Gang Dong et al.

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Conflict of interest statement

The authors have no conflicts of interest to declare.

Figures

Figure 1

Figure 1

PD-L1 expression levels in liver samples and FFA-treated LO2 cells. (a–d) PD-L1 expression and CD8+ T cells in the liver tissues determined by immunohistochemistry. (e) Intracellular lipid accumulation after FFA treatment (0.8 mM) for 24 hour measured by Oil Red staining. (f–i) Expression levels of PD-L1 detected by qRT-PCR, western blot, and immunofluorescence. ∗∗P < 0.01.

Figure 2

Figure 2

ROS mediated PD-L1 upregulation in FFA-treated LO2 cells. (a) Intracellular ROS in LO2 cells before and after FFA treatment measured by DCFH-DA. (b–d) Expression levels of NOX2 and NOX4 measured using qRT-PCR and western blot. (e) JC-1 probes were used to detect mitochondrial membrane potential. (f–j) Intracellular ROS in LO2 cells pretreated with siRNA against NOX4, MitoTEMPO (10 μ_M), or NAC (5 mM) followed by FFA treatment, measured by DCFH-DA, PD-L1 expression determined by western blot. ∗∗_P < 0.01.

Figure 3

Figure 3

ZNF24 promoted PD-L1 expression through binding to its promoter in FFA-treated LO2 cells. (a) A schematic of the target sites (wild and mutant) of ZNF24 in the promoter of PD-L1. (b–d) Dual-luciferase reporter assays performed in LO2 cells transfected with WT or MT plasmid containing ZNF24-binding sites in the PD-L1 promoter using Lipofectamine 2000 after ZNF24 overexpression. (e–g) ZNF24 expression after FFA treatment determined by qRT-PCR and western blot. (h and i) ZNF24 expression in LO2 cells pretreated with siRNA against NOX4, MitoTEMPO (10 μ_M), or NAC (5 mM) followed by FFA treatment, measured by western blot. (j and k) ZNF24 and PD-L1 expression in LO2 cells pretreated with siRNA against ZNF24, followed by FFA treatment detected by western blot. ∗∗_P < 0.01.

Figure 4

Figure 4

Identification of ZNF24–UBE2I protein interactions. (a and b) Analysis of protein interactions between ZNF24 and UBE2I using the BioGRID database, further confirmed by Co-IP assays. (c–f) UBE2I expression in LO2 cells treated by FFA or pretreated with siRNA against NOX4, MitoTEMPO (10 μ_M), or NAC (5 mM) followed by FFA treatment measured by western blot. (g and h) After FFA treatment, Sumo-1: ZNF24 and ZNF24 expression levels detected by western blot. (i and j) After UBE2I overexpression, Sumo-1: ZNF24, ZNF24, PD-L1, and UBE2I expression levels were determined by western blot. (k–m) Dual-luciferase reporter assays performed in LO2 cells transfected with WT plasmid containing ZNF24-binding sites in the PD-L1 promoter using Lipofectamine 2000 after ZNF24 overexpression with or without Sumo-1 overexpression. ∗∗_P < 0.01.

Figure 5

Figure 5

PD-L1 knockdown aggravated the damage of CD8 + T cells to FFA-treated LO2 cells. (a and b) Western blot determined the effect of siRNA against PD-L1. Coculturing of FFA-treated LO2 cells and CD8 + T cells in vitro. (c) mRNA expression levels of markers of T cell activation measured by qRT-PCR, (d) LO2 cell injury was evaluated by LDH assay, (e) AST or ALT in the supernatants measured by commercial assay kits. # represents that CD8 + T cells were incubated separately with LO2 cells, but supernatants were put together. ∗P < 0.05, ∗∗P < 0.01.

Figure 6

Figure 6

A NAFLD model was established. (a and b) The pathological changes of NAFLD were verified by H&E and Oil Red staining. (c–f) CD8+ T cells, PD-L1 expression, and hepatocyte apoptosis were detected by immunohistochemistry. (g) ALT and AST in the serum were detected using the commercial kit. ∗∗P < 0.01.

Figure 7

Figure 7

ROS/ZNF24/PD-L1 pathway activation in NAFLD models. (a) Intracellular ROS in hepatocytes in NAFLD significantly increased. (b) JC-1 probes were used to detect mitochondrial membrane potential. (c and d) NOX4 and ZNF24 expressions were determined by immunohistochemistry. (e and f) ROS/ZNF24/PD-L1 pathway activation examined by western blot.

Figure 8

Figure 8

PD-L1 limits liver injury in NAFLD models. (a and b) Western blot determined the effect of siRNA against PD-L1. (c) After PD-L1 knockdown, mRNA expression levels of markers of T cell activation measured by qRT-PCR. (d and e) Hepatocyte injury was evaluated by the Tunel assay and ALT/AST measurement. (f) Graph illustrating that both ROS/ZNF24 pathway activation and UBE2I-mediated ZNF24 sumoylation suppression induced by FFA promoted PD-L1 expression. ∗P < 0.05, ∗∗P < 0.01.

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