p28(GANK) prevents degradation of Oct4 and promotes expansion of tumor-initiating cells in hepatocarcinogenesis

Gastroenterology. 2012 Jun;142(7):1547-58.e14. doi: 10.1053/j.gastro.2012.02.042. Epub 2012 Feb 28.

Abstract

Background & aims: Hepatocellular carcinoma (HCC) is believed to arise from tumor-initiating cells (T-ICs), although little is known about their stem cell-like properties.

Methods: We quantified levels of p28(GANK) (Gankyrin), OV6, and Oct4 in 130 human HCC samples using immunohistochemistry. Magnetic-activated cell sorting was used to isolate OV6+ HCC cells. T-IC properties were evaluated by quantitative reverse-transcription polymerase chain reaction, flow cytometry, and spheroid formation. We used a coimmunoprecipitation assay to study interactions among p28(GANK), Oct4, and WWP2. Tumorigenicity and pulmonary metastasis were examined in nonobese diabetic and severe combined immunodeficient mice.

Results: In HCC samples, high levels of p28(GANK) correlated with expansion of OV6+ tumor cells; the combination of high levels of p28(GANK) and OV6 was associated with progression of HCC. p28(GANK) was predominantly expressed in liver T-ICs, isolated by magnetic sorting, and undifferentiated primary HCC spheroids. Increased levels of p28(GANK) in T-ICs increased their percentages in HCC samples, expression of stem cell genes, self-renewal potential, chemoresistance in vitro, and tumorigenicity and ability to develop into pulmonary metastases in mice. Conversely, knockdown of p28(GANK) reduced their T-IC properties. p28(GANK) likely activates liver T-ICs by impeding ubiquitination and degradation of the transcription factor Oct4 by WWP2. In support of this concept, levels of p28(GANK) correlated with those of Oct4 in HCC samples.

Conclusions: p28(GANK) activates and maintains liver T-ICs in HCCs by preventing degradation of Oct4. Inhibitors of p28(GANK) might therefore be developed to inactivate T-ICs and slow tumor progression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Differentiation / metabolism
  • Cell Line, Tumor
  • Disease Progression
  • Drug Resistance, Neoplasm
  • Gene Knockdown Techniques
  • Gene Silencing
  • Humans
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Liver Neoplasms / physiopathology*
  • Liver Neoplasms, Experimental / metabolism
  • Liver Neoplasms, Experimental / physiopathology*
  • Liver Neoplasms, Experimental / secondary
  • Lung Neoplasms / secondary
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / physiology*
  • Octamer Transcription Factor-3 / metabolism*
  • Prognosis
  • Proteasome Endopeptidase Complex / genetics
  • Proteasome Endopeptidase Complex / metabolism*
  • Proteolysis / drug effects
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism*
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Antigens, Differentiation
  • Octamer Transcription Factor-3
  • PSMD10 protein, human
  • Pou5f1 protein, mouse
  • Proto-Oncogene Proteins
  • oval cell marker OV-6
  • Wwp2 protein, mouse
  • Ubiquitin-Protein Ligases
  • Proteasome Endopeptidase Complex