Sorafenib down-regulates expression of HTATIP2 to promote invasiveness and metastasis of orthotopic hepatocellular carcinoma tumors in mice

Gastroenterology. 2012 Dec;143(6):1641-1649.e5. doi: 10.1053/j.gastro.2012.08.032. Epub 2012 Aug 23.

Abstract

Background & aims: Antiangiogenic agents can sometimes promote tumor invasiveness and metastasis, but little is known about the effects of the antiangiogenic drug sorafenib on progression of hepatocellular carcinoma (HCC).

Methods: Sorafenib was administered orally (30 mg · kg(-1) · day(-1)) to mice with orthotopic tumors grown from HCC-LM3, SMMC7721, or HepG2 cells. We analyzed survival times of mice, along with tumor growth, metastasis within liver and to lung, and induction of the epithelial-mesenchymal transition. Polymerase chain reaction arrays were used to determine the effects of sorafenib on gene expression patterns in HCC cells. We analyzed regulation of HIV-1 Tat interactive protein 2 (HTATIP2) by sorafenib and compared levels of this protein in tumor samples from 75 patients with HCC (21 who received sorafenib after resection and 54 who did not).

Results: Sorafenib promoted invasiveness and the metastatic potential of orthotopic tumors grown from SMMC7721 and HCC-LM3 cells but not from HepG2 cells. In gene expression analysis, HTATIP2 was down-regulated by sorafenib. HCC-LM3 cells that expressed small hairpin RNAs against HTATIP2 (knockdown) formed less invasive tumors in mice following administration of sorafenib than HCC-LM3 without HTATIP2 knockdown. Alternatively, HepG2 cells that expressed transgenic HTATIP2 formed more invasive tumors in mice following administration of sorafenib. Sorafenib induced the epithelial-mesenchymal transition in HCC cell lines, which was associated with expression of HTATIP2. Sorafenib regulated expression of HTATIP2 via Jun-activated kinase (JAK) and signal transducer and activator of transcription (STAT)3 signaling. Sorafenib therapy prolonged recurrence-free survival in patients who expressed lower levels of HTATIP2 compared with higher levels.

Conclusions: Sorafenib promotes invasiveness and the metastatic potential of orthotopic tumors from HCC cells in mice, down-regulating expression of HTATIP2 via JAK-STAT3 signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiogenesis Inhibitors / pharmacology
  • Animals
  • Carcinoma, Hepatocellular / pathology*
  • Carcinoma, Hepatocellular / physiopathology*
  • Cell Line, Tumor
  • Disease Models, Animal
  • Down-Regulation / drug effects*
  • Hep G2 Cells
  • Humans
  • Janus Kinases / physiology
  • Liver Neoplasms / pathology*
  • Liver Neoplasms / physiopathology*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Neoplasm Invasiveness / physiopathology
  • Neoplasm Metastasis / physiopathology
  • Niacinamide / analogs & derivatives*
  • Niacinamide / pharmacology
  • Phenylurea Compounds / pharmacology*
  • Repressor Proteins / physiology*
  • STAT3 Transcription Factor / physiology
  • Signal Transduction / physiology
  • Sorafenib
  • Transplantation, Heterologous
  • Tumor Suppressor Proteins / physiology*

Substances

  • Angiogenesis Inhibitors
  • Phenylurea Compounds
  • Repressor Proteins
  • STAT3 Transcription Factor
  • Tip30 protein, mouse
  • Tumor Suppressor Proteins
  • Niacinamide
  • Sorafenib
  • Janus Kinases