GNAS-activating mutations define a rare subgroup of inflammatory liver tumors characterized by STAT3 activation

J Hepatol. 2012 Jan;56(1):184-91. doi: 10.1016/j.jhep.2011.07.018. Epub 2011 Aug 9.

Abstract

Background & aims: Mosaic G-protein alpha-subunit (GNAS)-activating mutations are responsible for the McCune-Albright (MCA) syndrome. This oncogene that activates the adenylate cyclase is also mutated in various tumor types leading to the accumulation of cyclic-AMP. Identification of a hepatocellular adenoma (HCA) in two MCA patients led us to search for GNAS activation in benign and malignant hepatocellular carcinogenesis.

Methods: GNAS mutations were screened by sequencing 164 HCA, 245 hepatocellular carcinoma (HCC), and 17 fibrolamellar carcinomas. Tumors were characterized by quantitative RT-PCR, gene mutation screening and pathological reviewing. The consequences of wild type and mutant GNAS expression were analyzed in hepatocellular cell lines.

Results: A somatic GNAS-activating mutation was identified in 5 benign tumors and in 2 HCC. In benign tumors, GNAS mutations were exclusive from HNF1A, CTNNB1, and IL6ST mutations whereas one HCC demonstrated both CTNNB1 and GNAS mutations. Quantitative RT-PCR showed an activation of the IL-6 and interferon pathways in GNAS-mutated tumor tissues. Accordingly, pathological reviewing identified in GNAS-mutated tumors an inflammatory phenotype characterized by fibrosis and STAT3 activation. We further demonstrated in HCC cell lines that GNAS mutant expression induced inflammatory response and STAT3 activation.

Conclusions: We identified for the first time the association between two rare diseases, MCA syndrome and HCA occurrence, but also that somatic GNAS-activating mutations in sporadic benign and malignant liver tumors are characterized by an inflammatory phenotype. These results showed a cross-talk between cyclic-AMP and JAK/STAT pathways in liver tumors and they reinforce the role of STAT3 activation in liver tumorigenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenoma, Liver Cell / genetics
  • Adenoma, Liver Cell / metabolism
  • Adenoma, Liver Cell / pathology
  • Adult
  • Aged
  • Base Sequence
  • Carcinoma, Hepatocellular / genetics
  • Carcinoma, Hepatocellular / metabolism
  • Carcinoma, Hepatocellular / pathology
  • Chromogranins
  • DNA Mutational Analysis
  • DNA, Neoplasm / genetics
  • Female
  • Fibrous Dysplasia, Polyostotic / genetics
  • GTP-Binding Protein alpha Subunits, Gs / genetics*
  • Humans
  • Liver Neoplasms / classification
  • Liver Neoplasms / genetics*
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Male
  • Middle Aged
  • Models, Biological
  • Mutation*
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction

Substances

  • Chromogranins
  • DNA, Neoplasm
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • GNAS protein, human
  • GTP-Binding Protein alpha Subunits, Gs

Supplementary concepts

  • Fibrolamellar hepatocellular carcinoma