miR-22 promotes HBV-related hepatocellular carcinoma development in males

Clin Cancer Res. 2011 Sep 1;17(17):5593-603. doi: 10.1158/1078-0432.CCR-10-1734. Epub 2011 Jul 12.

Abstract

Purpose: Previous reports have shown that IL-1α-MyD88-IL-6 signaling is essential in promoting hepatocellular carcinoma (HCC) development in a diethylnitrosamine (DEN)-induced mouse model. We aimed to determine whether interleukin (IL)-1α regulates HCC development in humans.

Methods: HBV-associated HCC tissue, corresponding adjacent tissue, and normal tissue samples were obtained from 80 male and 36 female patients. IL-1α, ERα, IL-6, and MyD88 were quantified by using real-time PCR and Western blot. Stem-loop PCR was used to quantify miR-22 expression. Luciferase reporter assays were used to study transcriptional regulation.

Results: IL-1α was highly expressed in male tumor adjacent tissue compared with normal tissue (P = 0.025); however, this was not the case for female subjects. A linear relationship was observed between increased IL-1α and decreased ERα expression in male tumor adjacent tissue (r = -0.616, P = 0.004). Our results also indicated that estrogen (E2) was suppressed upon IL-1α secretion in ERα-overexpressed HCC cells. We detected high expression of miR-22 in male tumor adjacent tissue compared with controls (P = 0.027); furthermore, we showed that miR-22 downregulates ERα transcription by targeting the 3'-untranslated region. In the DEN-induced model, IL-1α was highly expressed in sprouting tumors and gradually decreased in conjunction with HCC development.

Conclusion: Overexpression of miR-22 in male tumor adjacent tissue was associated with downregulated ERα expression, potentially by attenuating the protective effect of estrogen and causing increased IL-1α expression. These results may explain the high incidence of HBV-associated HCC in the male population.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carcinoma, Hepatocellular / genetics
  • Carcinoma, Hepatocellular / metabolism*
  • Carcinoma, Hepatocellular / pathology
  • Carcinoma, Hepatocellular / virology
  • Cell Line, Tumor
  • Estrogen Receptor alpha / biosynthesis*
  • Female
  • Gene Expression Regulation, Neoplastic
  • Hepatitis B virus / pathogenicity*
  • Humans
  • Interleukin-1alpha / analysis
  • Interleukin-1alpha / biosynthesis*
  • Interleukin-6 / analysis
  • Interleukin-6 / biosynthesis
  • Liver Neoplasms / genetics
  • Liver Neoplasms / metabolism*
  • Liver Neoplasms / pathology
  • Male
  • Membrane Glycoproteins / analysis
  • Membrane Glycoproteins / biosynthesis
  • Mice
  • Mice, Inbred ICR
  • MicroRNAs / biosynthesis
  • MicroRNAs / metabolism*
  • RNA, Messenger / biosynthesis
  • Receptors, Interleukin-1 / analysis
  • Receptors, Interleukin-1 / biosynthesis
  • Sex Characteristics
  • Signal Transduction

Substances

  • ESR1 protein, human
  • Estrogen Receptor alpha
  • Interleukin-1alpha
  • Interleukin-6
  • MIRN22 microRNA, human
  • Membrane Glycoproteins
  • MicroRNAs
  • RNA, Messenger
  • Receptors, Interleukin-1
  • TIRAP protein, human