Hepatitis B virus X protein represses miRNA-148a to enhance tumorigenesis

J Clin Invest. 2013 Feb;123(2):630-45. doi: 10.1172/JCI64265. Epub 2013 Jan 16.

Abstract

MicroRNAs (miRNAs) have been shown to be dysregulated in virus-related cancers; however, miRNA regulation of virus-related cancer development and progression remains poorly understood. Here, we report that miR-148a is repressed by hepatitis B virus (HBV) X protein (HBx) to promote cancer growth and metastasis in a mouse model of hepatocellular carcinoma (HCC). Hematopoietic pre-B cell leukemia transcription factor-interacting protein (HPIP) is an important regulator of cancer cell growth. We used miRNA target prediction programs to identify miR-148a as a regulator of HPIP. Expression of miR-148a in hepatoma cells reduced HPIP expression, leading to repression of AKT and ERK and subsequent inhibition of mTOR through the AKT/ERK/FOXO4/ATF5 pathway. HBx has been shown to play a critical role in the molecular pathogenesis of HBV-related HCC. We found that HBx suppressed p53-mediated activation of miR-148a. Moreover, expression of miR-148a was downregulated in patients with HBV-related liver cancer and negatively correlated with HPIP, which was upregulated in patients with liver cancer. In cultured cells and a mouse xenograft model, miR-148a reduced the growth, epithelial-to-mesenchymal transition, invasion, and metastasis of HBx-expressing hepatocarcinoma cells through inhibition of HPIP-mediated mTOR signaling. Thus, miR-148a activation or HPIP inhibition may be a useful strategy for cancer treatment.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Carcinoma, Hepatocellular / etiology*
  • Carcinoma, Hepatocellular / genetics
  • Carcinoma, Hepatocellular / metabolism
  • Carcinoma, Hepatocellular / secondary
  • Co-Repressor Proteins
  • Down-Regulation
  • Epithelial-Mesenchymal Transition
  • Hep G2 Cells
  • Hepatitis B virus / pathogenicity
  • Humans
  • Liver Neoplasms / etiology*
  • Liver Neoplasms / genetics
  • Liver Neoplasms / metabolism
  • Liver Neoplasms, Experimental / etiology
  • Liver Neoplasms, Experimental / genetics
  • Liver Neoplasms, Experimental / metabolism
  • Male
  • Mice
  • Mice, Nude
  • MicroRNAs / antagonists & inhibitors
  • MicroRNAs / genetics*
  • Neoplasm Invasiveness
  • Signal Transduction
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / metabolism
  • Trans-Activators / physiology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transplantation, Heterologous
  • Viral Regulatory and Accessory Proteins

Substances

  • Co-Repressor Proteins
  • MIRN148 microRNA, human
  • MicroRNAs
  • Mirn148 microRNA, mouse
  • PBXIP1 protein, human
  • Trans-Activators
  • Transcription Factors
  • Viral Regulatory and Accessory Proteins
  • hepatitis B virus X protein
  • TOR Serine-Threonine Kinases