Hepatitis B and Hepatitis C Virus Infection Promote Liver Fibrogenesis through a TGF-β1-Induced OCT4/Nanog Pathway

J Immunol. 2022 Feb 1;208(3):672-684. doi: 10.4049/jimmunol.2001453. Epub 2022 Jan 12.

Abstract

Hepatitis B virus (HBV)/hepatitis C virus (HCV) coinfection accelerates liver fibrosis progression compared with HBV or HCV monoinfection. Octamer binding transcription factor 4 (OCT4) and Nanog are direct targets of the profibrogenic TGF-β1 signaling cascade. We leveraged a coculture model to monitor the effects of HBV and HCV coinfection on fibrogenesis in both sodium taurocholate cotransporting polypeptide-transfected Huh7.5.1 hepatoma cells and LX2 hepatic stellate cells (HSCs). We used CRISPR-Cas9 to knock out OCT4 and Nanog to evaluate their effects on HBV-, HCV-, or TGF-β1-induced liver fibrogenesis. HBV/HCV coinfection and HBx, HBV preS2, HCV Core, and HCV NS2/3 overexpression increased TGF-β1 mRNA levels in sodium taurocholate cotransporting polypeptide-Huh7.5.1 cells compared with controls. HBV/HCV coinfection further enhanced profibrogenic gene expression relative to HBV or HCV monoinfection. Coculture of HBV and HCV monoinfected or HBV/HCV coinfected hepatocytes with LX2 cells significantly increased profibrotic gene expression and LX2 cell invasion and migration. OCT4 and Nanog guide RNA independently suppressed HBV-, HCV-, HBV/HCV-, and TGF-β1-induced α-SMA, TIMP-1, and Col1A1 expression and reduced Huh7.5.1, LX2, primary hepatocyte, and primary human HSC migratory capacity. OCT4/Nanog protein expression also correlated positively with fibrosis stage in liver biopsies from patients with chronic HBV or HCV infection. In conclusion, HBV and HCV independently and cooperatively promote liver fibrogenesis through a TGF-β1-induced OCT4/Nanog-dependent pathway.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / biosynthesis
  • Adult
  • CRISPR-Cas Systems / genetics
  • Cell Line, Tumor
  • Cell Movement / physiology
  • Coinfection / pathology
  • Collagen Type I, alpha 1 Chain / biosynthesis
  • Female
  • Gene Knockout Techniques
  • Hepacivirus / metabolism
  • Hepatic Stellate Cells / pathology
  • Hepatic Stellate Cells / virology
  • Hepatitis B / pathology*
  • Hepatitis B virus / metabolism
  • Hepatitis C / pathology*
  • Hepatocytes / pathology
  • Hepatocytes / virology
  • Humans
  • Liver / pathology
  • Liver Cirrhosis / pathology*
  • Liver Cirrhosis / virology
  • Male
  • Nanog Homeobox Protein / genetics
  • Nanog Homeobox Protein / metabolism*
  • Octamer Transcription Factor-3 / genetics
  • Octamer Transcription Factor-3 / metabolism*
  • Organic Anion Transporters, Sodium-Dependent / metabolism
  • Symporters / metabolism
  • Tissue Inhibitor of Metalloproteinase-1 / biosynthesis
  • Transforming Growth Factor beta1 / metabolism*

Substances

  • ACTA2 protein, human
  • Actins
  • COL1A1 protein, human
  • Collagen Type I, alpha 1 Chain
  • NANOG protein, human
  • Nanog Homeobox Protein
  • Octamer Transcription Factor-3
  • Organic Anion Transporters, Sodium-Dependent
  • POU5F1 protein, human
  • Symporters
  • TIMP1 protein, human
  • Tissue Inhibitor of Metalloproteinase-1
  • Transforming Growth Factor beta1
  • sodium-bile acid cotransporter