Loss of immunity-supported senescence enhances susceptibility to hepatocellular carcinogenesis and progression in Toll-like receptor 2-deficient mice

Hepatology. 2013 Jan;57(1):171-82. doi: 10.1002/hep.25991.

Abstract

Hepatocellular carcinoma (HCC) is a complication at the endstage of chronic inflammatory liver diseases with dismal prognosis. Targeting of Toll-like receptor (TLR) 2 attenuates tumor metastases; we hypothesized that blocking TLR2 might also play a crucial role in reducing hepatocarcinogenesis. Surprisingly, we found that the genetic deletion of TLR2 increased susceptibility to diethylnitrosamine (DEN), a genotoxic carcinogen that can induce HCC. Indeed, TLR2-deficient mice showed a significant increase in carcinogenesis and progression of HCC as indicated by increases in tumor nodule size, tumor volume, and animal death. The enhanced susceptibility to DEN-induced HCC was associated with a broad-spectrum reduction in the immune response to DEN-induced liver injury. We found that TLR2 deficiency caused a decrease in the infiltration of macrophages and an attenuation of apoptosis signal regulating kinase 1 (ASK1) / p38 mitogen-activated protein kinase (p38 MAPK) / nuclear factor kappa B (NF-κB) signaling, which led to a decrease in the expression of interferon-gamma (IFN-γ), tumor necrosis factor alpha (TNF-α), interleukin (IL)-1α/β, IL-6, and Cxcl-2 as well as suppression of autophagy flux and increases in oxidative stress and p62 aggregation in liver tissue. The defects in immune networks resulted in suppressed p21- and p16/pRb-dependent senescence, which caused an increase in proliferation and a decrease in apoptotic and autophagy-associated cell death in mouse livers. Restoring cellular senescence and autophagy flux by treating TLR2-deficient mice with IFN-γ, a T helper 1 (Th1) cytokine and positive modulator of senescence and autophagy, could attenuate the carcinogenesis and progression of HCC associated with TLR2-deficient animals.

Conclusion: The loss of immune networks supporting cellular senescence and autophagy flux is attributed to enhanced susceptibility to DEN-induced hepatocellular carcinogenesis and progression in TLR2-deficient mice. These findings may be used to prevent the development of liver cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkylating Agents
  • Animals
  • Autophagy
  • Carcinoma, Hepatocellular / chemically induced
  • Carcinoma, Hepatocellular / immunology*
  • Carcinoma, Hepatocellular / metabolism
  • Cell Transformation, Neoplastic*
  • Cellular Senescence*
  • Cyclin-Dependent Kinase Inhibitor Proteins / metabolism
  • Diethylnitrosamine
  • Disease Progression
  • Female
  • Interferon-gamma / metabolism
  • Liver / immunology
  • Liver / metabolism
  • Liver Neoplasms / chemically induced
  • Liver Neoplasms / immunology*
  • Liver Neoplasms / metabolism
  • MAP Kinase Kinase Kinase 5 / metabolism
  • MAP Kinase Signaling System
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Reactive Oxygen Species / metabolism
  • Toll-Like Receptor 2 / metabolism*
  • Transcription Factor TFIIH
  • Transcription Factors / metabolism

Substances

  • Alkylating Agents
  • Cyclin-Dependent Kinase Inhibitor Proteins
  • Gtf2h1 protein, mouse
  • Reactive Oxygen Species
  • Tlr2 protein, mouse
  • Toll-Like Receptor 2
  • Transcription Factors
  • Transcription Factor TFIIH
  • Diethylnitrosamine
  • Interferon-gamma
  • MAP Kinase Kinase Kinase 5
  • Map3k5 protein, mouse