Perivenous Stellate Cells Are the Main Source of Myofibroblasts and Cancer-Associated Fibroblasts Formed After Chronic Liver Injuries

Hepatology. 2021 Sep;74(3):1578-1594. doi: 10.1002/hep.31848.

Abstract

Background and aims: Studies of the identity and pathophysiology of fibrogenic HSCs have been hampered by a lack of genetic tools that permit specific and inducible fate-mapping of these cells in vivo. Here, by single-cell RNA sequencing of nonparenchymal cells from mouse liver, we identified transcription factor 21 (Tcf21) as a unique marker that restricted its expression to quiescent HSCs.

Approach and results: Tracing Tcf21+ cells by Tcf21-CreER (Cre-Estrogen Receptor fusion protein under the control of Tcf21 gene promoter) targeted ~10% of all HSCs, most of which were located at periportal and pericentral zones. These HSCs were quiescent under steady state but became activated on injuries, generating 62%-67% of all myofibroblasts in fibrotic livers and ~85% of all cancer-associated fibroblasts (CAFs) in liver tumors. Conditional deletion of Transforming Growth Factor Beta Receptor 2 (Tgfbr2) by Tcf21-CreER blocked HSC activation, compromised liver fibrosis, and inhibited liver tumor progression.

Conclusions: In conclusion, Tcf21-CreER-targeted perivenous stellate cells are the main source of myofibroblasts and CAFs in chronically injured livers. TGF-β signaling links HSC activation to liver fibrosis and tumorigenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Bile Ducts / surgery
  • Cancer-Associated Fibroblasts / cytology*
  • Carbon Tetrachloride / toxicity
  • Cell Lineage
  • Cholestasis
  • Chronic Disease
  • Hepatic Stellate Cells / cytology*
  • Hepatic Stellate Cells / metabolism
  • Hepatic Veins / pathology
  • Liver Cirrhosis / metabolism
  • Liver Cirrhosis / pathology
  • Liver Cirrhosis, Experimental / metabolism
  • Liver Cirrhosis, Experimental / pathology*
  • Liver Diseases / metabolism
  • Liver Diseases / pathology*
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Liver Neoplasms, Experimental / metabolism
  • Liver Neoplasms, Experimental / pathology*
  • Mice
  • Myofibroblasts / cytology*
  • Myofibroblasts / metabolism
  • Receptor, Transforming Growth Factor-beta Type II / genetics
  • Sequence Analysis, RNA
  • Single-Cell Analysis

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Tcf21 protein, mouse
  • Carbon Tetrachloride
  • Receptor, Transforming Growth Factor-beta Type II
  • Tgfbr2 protein, mouse