HOTAIR Knockdown Increases the Sensitivity of Hepatocellular Carcinoma Cells to Sorafenib by Disrupting miR-145-5p/HK2 Axis-Mediated Mitochondrial Function and Glycolysis

Background: Frequent drug resistance seriously limits the therapeutic efficacy of sorafenib in advanced hepatocellular carcinoma (HCC). Strategies to increase the response to sorafenib are limited, and the underlying mechanism to facilitate such an increase is not entirely underst...

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Main Authors: Meiyu Cheng, Bingrong Wang, Lina Duan, Yu Jin, Wenda Zhang, Na Li
Format: Article
Language:English
Published: IMR Press 2025-05-01
Series:Frontiers in Bioscience-Landmark
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Online Access:https://www.imrpress.com/journal/FBL/30/5/10.31083/FBL37368
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author Meiyu Cheng
Bingrong Wang
Lina Duan
Yu Jin
Wenda Zhang
Na Li
author_facet Meiyu Cheng
Bingrong Wang
Lina Duan
Yu Jin
Wenda Zhang
Na Li
author_sort Meiyu Cheng
collection DOAJ
description Background: Frequent drug resistance seriously limits the therapeutic efficacy of sorafenib in advanced hepatocellular carcinoma (HCC). Strategies to increase the response to sorafenib are limited, and the underlying mechanism to facilitate such an increase is not entirely understood. Homeobox (HOX) transcript antisense intergenic RNA (HOTAIR) expression is high in HCC, promoting the occurrence and progression of HCC. In this study, we explored the mechanism through which HOTAIR knockdown affects the response of HCC cells to the chemotherapeutic sorafenib. Methods: Cell viability and apoptosis were assessed using MTT assay, flow cytometry, and nuclear staining. Mitochondrial function and isolation were determined using flow cytometry and a mitochondrial isolation kit. Glycolysis was measured by glucose and lactic acid assay kits. The underlying mechanisms were explored through western blotting, quantitative reverse-transcription polymerase chain reaction (qRT-PCR), and chromatin immunoprecipitation (ChIP). Results: HOTAIR knockdown increased sorafenib-induced apoptosis in the HCC cells. HOTAIR and hexokinase 2 (HK2) expression levels were upregulated in human HCC tissues, demonstrating a significant correlation. The knockdown of HOTAIR or HK2 aggravated mitochondrial dysfunction and inhibited glycolysis. Further, HOTAIR knockdown promoted sorafenib-mediated HK2 mRNA downregulation, resulting in decreased HK2 protein levels in cells and mitochondria. This ultimately facilitated the mitochondrial apoptotic pathway. Moreover, it was demonstrated that HOTAIR regulated HK2 via polycomb repressive complex 2 (PRC2)-mediated epigenetic modification of miR-145-5p in HCC. Conclusions: HOTAIR knockdown increased the sensitivity of HCC cells to sorafenib by disrupting the miR-145-5p/HK2 axis-mediated mitochondrial function and glycolysis, suggesting new strategies for HCC treatment.
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spelling doaj-art-df34f0fd999b4a6491bb9d60a0eb07322025-08-20T02:32:27ZengIMR PressFrontiers in Bioscience-Landmark2768-67012025-05-013053736810.31083/FBL37368S2768-6701(25)01732-0HOTAIR Knockdown Increases the Sensitivity of Hepatocellular Carcinoma Cells to Sorafenib by Disrupting miR-145-5p/HK2 Axis-Mediated Mitochondrial Function and GlycolysisMeiyu Cheng0Bingrong Wang1Lina Duan2Yu Jin3Wenda Zhang4Na Li5Department of Pathophysiology, College of Basic Medical Sciences, Jilin University, 130021 Changchun, Jilin, ChinaDepartment of Pathophysiology, College of Basic Medical Sciences, Jilin University, 130021 Changchun, Jilin, ChinaDepartment of Pathophysiology, College of Basic Medical Sciences, Jilin University, 130021 Changchun, Jilin, ChinaDepartment of Pathophysiology, College of Basic Medical Sciences, Jilin University, 130021 Changchun, Jilin, ChinaDepartment of Pathology and Cancer Research Center, Yanbian University Medical College, 133002 Yanji, Jilin, ChinaDepartment of Pathophysiology, College of Basic Medical Sciences, Jilin University, 130021 Changchun, Jilin, ChinaBackground: Frequent drug resistance seriously limits the therapeutic efficacy of sorafenib in advanced hepatocellular carcinoma (HCC). Strategies to increase the response to sorafenib are limited, and the underlying mechanism to facilitate such an increase is not entirely understood. Homeobox (HOX) transcript antisense intergenic RNA (HOTAIR) expression is high in HCC, promoting the occurrence and progression of HCC. In this study, we explored the mechanism through which HOTAIR knockdown affects the response of HCC cells to the chemotherapeutic sorafenib. Methods: Cell viability and apoptosis were assessed using MTT assay, flow cytometry, and nuclear staining. Mitochondrial function and isolation were determined using flow cytometry and a mitochondrial isolation kit. Glycolysis was measured by glucose and lactic acid assay kits. The underlying mechanisms were explored through western blotting, quantitative reverse-transcription polymerase chain reaction (qRT-PCR), and chromatin immunoprecipitation (ChIP). Results: HOTAIR knockdown increased sorafenib-induced apoptosis in the HCC cells. HOTAIR and hexokinase 2 (HK2) expression levels were upregulated in human HCC tissues, demonstrating a significant correlation. The knockdown of HOTAIR or HK2 aggravated mitochondrial dysfunction and inhibited glycolysis. Further, HOTAIR knockdown promoted sorafenib-mediated HK2 mRNA downregulation, resulting in decreased HK2 protein levels in cells and mitochondria. This ultimately facilitated the mitochondrial apoptotic pathway. Moreover, it was demonstrated that HOTAIR regulated HK2 via polycomb repressive complex 2 (PRC2)-mediated epigenetic modification of miR-145-5p in HCC. Conclusions: HOTAIR knockdown increased the sensitivity of HCC cells to sorafenib by disrupting the miR-145-5p/HK2 axis-mediated mitochondrial function and glycolysis, suggesting new strategies for HCC treatment.https://www.imrpress.com/journal/FBL/30/5/10.31083/FBL37368hotairsorafenibmitochondrial functionhk2mir-145-5phcc
spellingShingle Meiyu Cheng
Bingrong Wang
Lina Duan
Yu Jin
Wenda Zhang
Na Li
HOTAIR Knockdown Increases the Sensitivity of Hepatocellular Carcinoma Cells to Sorafenib by Disrupting miR-145-5p/HK2 Axis-Mediated Mitochondrial Function and Glycolysis
Frontiers in Bioscience-Landmark
hotair
sorafenib
mitochondrial function
hk2
mir-145-5p
hcc
title HOTAIR Knockdown Increases the Sensitivity of Hepatocellular Carcinoma Cells to Sorafenib by Disrupting miR-145-5p/HK2 Axis-Mediated Mitochondrial Function and Glycolysis
title_full HOTAIR Knockdown Increases the Sensitivity of Hepatocellular Carcinoma Cells to Sorafenib by Disrupting miR-145-5p/HK2 Axis-Mediated Mitochondrial Function and Glycolysis
title_fullStr HOTAIR Knockdown Increases the Sensitivity of Hepatocellular Carcinoma Cells to Sorafenib by Disrupting miR-145-5p/HK2 Axis-Mediated Mitochondrial Function and Glycolysis
title_full_unstemmed HOTAIR Knockdown Increases the Sensitivity of Hepatocellular Carcinoma Cells to Sorafenib by Disrupting miR-145-5p/HK2 Axis-Mediated Mitochondrial Function and Glycolysis
title_short HOTAIR Knockdown Increases the Sensitivity of Hepatocellular Carcinoma Cells to Sorafenib by Disrupting miR-145-5p/HK2 Axis-Mediated Mitochondrial Function and Glycolysis
title_sort hotair knockdown increases the sensitivity of hepatocellular carcinoma cells to sorafenib by disrupting mir 145 5p hk2 axis mediated mitochondrial function and glycolysis
topic hotair
sorafenib
mitochondrial function
hk2
mir-145-5p
hcc
url https://www.imrpress.com/journal/FBL/30/5/10.31083/FBL37368
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