Basic Study
Copyright ©The Author(s) 2021. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Oct 28, 2021; 27(40): 6908-6926
Published online Oct 28, 2021. doi: 10.3748/wjg.v27.i40.6908
Transforming growth factor beta-1 upregulates glucose transporter 1 and glycolysis through canonical and noncanonical pathways in hepatic stellate cells
Ming-Yu Zhou, Ming-Liang Cheng, Tao Huang, Rui-Han Hu, Gao-Liang Zou, Hong Li, Bao-Fang Zhang, Juan-Juan Zhu, Yong-Mei Liu, Yang Liu, Xue-Ke Zhao
Ming-Yu Zhou, Ming-Liang Cheng, Tao Huang, Rui-Han Hu, Xue-Ke Zhao, Department of Internal Medicine, Guizhou Medical University, Guiyang 550001, Guizhou Province, China
Ming-Yu Zhou, Ming-Liang Cheng, Gao-Liang Zou, Hong Li, Bao-Fang Zhang, Juan-Juan Zhu, Yang Liu, Xue-Ke Zhao, Department of Infectious Diseases, Affiliated Hospital of Guizhou Medical University, Guiyang 550004, Guizhou Province, China
Yong-Mei Liu, Clinical Laboratory Center, Affiliated Hospital of Guizhou Medical University, Guiyang 550004, Guizhou Province, China
Author contributions: Zhao XK and Cheng ML designed the study; Zhou MY, Huang T and Hu RH performed most of the experiments and wrote the article; all authors contributed to the design and interpretation of the study; Zhou MY, Huang T and Hu RH contributed equally to this work; all authors approved the final version of the article.
Supported by National Natural Science Foundation of China, No. 82060116, No. 81860115 and No. 81960118; and Guizhou Science and Technology Support Project Fund, No. [2021] 058.
Institutional review board statement: This study was approved by the Institutional Review Board of the Affiliated Hospital of Guizhou Medical University.
Institutional animal care and use committee statement: All animal experiments conformed to the internationally accepted principles for the care and use of laboratory animals (license No. 2000719). All animal interventions were approved by the Institutional Animal Care and Use Committee (IACUC) of Guizhou Medical University.
Conflict-of-interest statement: The authors declare no conflicts of interest related to this study.
Data sharing statement: No additional data are available.
ARRIVE guidelines statement: The authors have read the ARRIVE Guidelines, and the manuscript was prepared and revised according to the ARRIVE Guidelines.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Xue-Ke Zhao, MD, PhD, Chief Physician, Professor, Department of Infectious Diseases, Affiliated Hospital of Guizhou Medical University, No. 28 Guiyi Road, Guiyang 550004, Guizhou Province, China. zhaoxueke1@163.com
Received: April 30, 2021
Peer-review started: April 30, 2021
First decision: July 2, 2021
Revised: July 19, 2021
Accepted: September 8, 2021
Article in press: September 8, 2021
Published online: October 28, 2021
Processing time: 180 Days and 3.8 Hours
ARTICLE HIGHLIGHTS
Research background

Liver fibrosis is a refractory disease that develops progressively and eventually evolves into liver cirrhosis or even liver cancer. Hepatic stellate cell (HSC) activation is the initiating factor for liver fibrosis, while aerobic glycolysis is one of the main metabolic characteristics. Transforming growth factor-β1 (TGF-β1) is the most important profibrotic factor in HSCs, and TGF-β1 drives metabolic reprogramming. Glucose transporter 1 (GLUT1) is the most widely distributed glucose transporter in mammals and is related to glycolytic metabolism. However, the role of GLUT1 in liver fibrosis and the relationship between GLUT1 and TGF-β1 remain unclear and require further investigation.

Research motivation

The results of this study might provide a basis for the application of GLUT1 in the treatment of liver fibrosis and provide an expanded basis for understanding the mechanism of action of TGF-β1 in metabolic reprogramming during liver fibrosis.

Research objectives

This study examined changes in GLUT1 expression in human and mouse fibrotic liver tissues and differences in extracellular acid production and in the expression levels of key glycolytic enzymes and GLUT1 during HSC activation induced by TGF-β1-related pathways. In addition, this study further explored the relationship between TGF-β1 pathways and GLUT1 expression and the potential underlying molecular mechanisms.

Research methods

IHC was employed to examine changes in GLUT1 expression in human and mouse fibrotic liver tissues. Immunofluorescence staining was performed to examine changes in GLUT1 and alpha-smooth muscle actin (α-SMA) expression in mouse fibrotic liver tissue. Primary mouse stellate cells were isolated. After activation of the cells by TGF-β1 stimulation, changes in extracellular acid production, key glycolytic enzymes and glucose consumption were examined. In addition, changes in GLUT1 expression were explored by activating/inhibiting the Smad2/3 pathway and inhibiting the expression of proteins related to the p38 and PI3K/AKT pathways. Finally, in mice with liver fibrosis, the effect of a GLUT1 inhibitor on liver fibrosis was investigated by performing Masson’s trichrome staining and Sirius red staining and analyzing serological inflammatory markers.

Research results

The expression of the GLUT1 protein was increased in both mouse and human fibrotic liver tissue.immunofluorescence staining revealed the colocalization of GLUT1 and α-SMA proteins, indicating that GLUT1 expression was related to the development of liver fibrosis. TGF-β1 induced an increase in aerobic glycolysis in HSCs and induced GLUT1 expression in HSCs by activating the canonical and noncanonical signaling pathways. The p38 MAPK pathway and the Smad pathway synergistically affected the induction of GLUT1 expression. GLUT1 inhibition eliminated the effect of TGF-β1 on the proliferation and migration of HSCs. A GLUT1 inhibitor was administered to a mouse model of liver fibrosis, and GLUT1 inhibition reduced the degree of liver inflammation.

Research conclusions

GLUT1 expression was upregulated in liver fibrosis, and the underlying mechanism was related to activation of the Smad2/3, p38 and PI3K/AKT pathways by TGF-β1, which directly induced GLUT1 expression and promoted glycolysis. GLUT1 inhibition eliminated TGF-β1-induced HSC activation, proliferation and migration, and GLUT1 inhibition exerted an antifibrotic effect.

Research perspectives

The results of this study reveal that the TGF-β1 pathway directly induces GLUT1 expression and aerobic glycolysis, thus promoting liver fibrosis. This study preliminarily clarified the mechanism underlying the interaction between TGF-β1 and GLUT1 in liver fibrosis, thus providing a deeper understanding of the mechanism of liver fibrosis and providing guidance for the selection of targets to treat liver fibrosis. The results from this study indicate that GLUT1 inhibitors may have certain prospective applications as therapeutic drugs for liver fibrosis.