Activation of p53 After Irradiation Impairs the Regenerative Capacity of the Mouse Liver

Hepatol Commun. 2022 Feb;6(2):411-422. doi: 10.1002/hep4.1815. Epub 2021 Sep 28.

Abstract

Radiation therapy is one of the treatment methods for hepatocellular carcinoma. However, radiation tolerance of the liver is low, and the detailed effect of radiation on liver regeneration has not been clarified. C57BL/6J mice or hepatocyte-specific p53 knockout (KO) mice (albumin [Alb]-Cre Trp53flox/flox ) were irradiated with a single fraction of 10 Gy localized to the upper abdomen. We performed 70% partial hepatectomy (PHx) 24 hours after irradiation. Liver regeneration was assessed by proliferation cell nuclear antigen (PCNA)- and Ki-67-positive hepatocyte ratios and liver-to-body weight ratio after PHx. To establish a fibrosis model, CCl4 was orally administered for 8 weeks. The murine hepatocyte cell line BNL CL.2 (CL2) was irradiated with 10 Gy. Irradiation activated p53, induced downstream p21 in the liver, and delayed liver regeneration after PHx. While PHx increased hepatocyte growth factor (HGF) levels and activated Met with or without irradiation in the regenerative liver, it activated Akt and extracellular kinase 1 and 2 (Erk 1/2) less in irradiated mice than in nonirradiated mice. In CL2 cells cultured with HGF, irradiation suppressed cell growth by decreasing phosphorylated Akt and Erk 1/2 levels, which was abolished by small interfering RNA-mediated p53 knockdown but not by p21 knockdown. Hepatocyte-specific knockout of p53 in mice abolished the irradiation-induced suppression of both liver regeneration and Akt and Erk 1/2 activation after PHx. In the fibrotic mouse model, the survival rate after PHx of irradiated p53 KO mice was higher than that of wild-type mice. Conclusion: p53 but not p21 is involved in the impaired regenerative ability of the irradiated liver.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Count
  • Cell Line
  • Cell Proliferation / radiation effects
  • Disease Models, Animal
  • Hepatocyte Growth Factor / physiology
  • Hepatocytes / radiation effects
  • Ki-67 Antigen / analysis
  • Liver Cirrhosis / metabolism
  • Liver Cirrhosis / pathology
  • Liver Regeneration / physiology
  • Liver Regeneration / radiation effects*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Proliferating Cell Nuclear Antigen / analysis
  • Proto-Oncogene Proteins c-akt / metabolism
  • Signal Transduction
  • Tumor Suppressor Protein p53 / physiology*
  • p21-Activated Kinases / analysis

Substances

  • Ki-67 Antigen
  • Proliferating Cell Nuclear Antigen
  • Tumor Suppressor Protein p53
  • Hepatocyte Growth Factor
  • Pak1 protein, mouse
  • Proto-Oncogene Proteins c-akt
  • p21-Activated Kinases
  • Mapk1 protein, mouse
  • Mapk3 protein, mouse
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3