In vitro and in vivo inhibition of breast cancer cell growth by targeting the Hedgehog/GLI pathway with SMO (GDC-0449) or GLI (GANT-61) inhibitors

Oncotarget. 2016 Feb 23;7(8):9250-70. doi: 10.18632/oncotarget.7062.

Abstract

Aberrant Hedgehog (Hh)/glioma-associated oncogene (GLI) signaling has been implicated in cancer progression. Here, we analyzed GLI1, Sonic Hedgehog (Shh) and NF-κB expression in 51 breast cancer (ductal carcinoma) tissues using immunohistochemistry. We found a positive correlation between nuclear GLI1 expression and tumor grade in ductal carcinoma cases. Cytoplasmic Shh staining significantly correlated with a lower tumor grade. Next, the in vitro effects of two Hh signaling pathway inhibitors on breast cancer cell lines were evaluated using the Smoothened (SMO) antagonist GDC-0449 and the direct GLI1 inhibitor GANT-61. GDC-0449 and GANT-61 exhibited the following effects: a) inhibited breast cancer cell survival; b) induced apoptosis; c) inhibited Hh pathway activity by decreasing the mRNA expression levels of GLI1 and Ptch and inhibiting the nuclear translocation of GLI1; d) increased/decreased EGFR and ErbB2 protein expression, reduced p21-Ras and ERK1/ERK2 MAPK activities and inhibited AKT activation; and e) decreased the nuclear translocation of NF-κB. However, GANT-61 exerted these effects more effectively than GDC-0449. The in vivo antitumor activities of GDC-0449 and GANT-61 were analyzed in BALB/c mice that were subcutaneously inoculated with mouse breast cancer (TUBO) cells. GDC-0449 and GANT-61 suppressed tumor growth of TUBO cells in BALB/c mice to different extents. These findings suggest that targeting the Hh pathway using antagonists that act downstream of SMO is a more efficient strategy than using antagonists that act upstream of SMO for interrupting Hh signaling in breast cancer.

Keywords: Hedgehog/GLI pathway; breast cancer; inhibitors; tumor growth; tumor model.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus / drug effects
  • Anilides / therapeutic use*
  • Animals
  • Apoptosis / drug effects
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / pathology
  • Carcinoma, Ductal / drug therapy*
  • Carcinoma, Ductal / pathology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Enzyme Activation / drug effects
  • ErbB Receptors / biosynthesis
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Hedgehog Proteins / antagonists & inhibitors
  • Humans
  • MCF-7 Cells
  • Mammary Neoplasms, Experimental / drug therapy*
  • Mammary Neoplasms, Experimental / pathology
  • Mice
  • Mice, Inbred BALB C
  • NF-kappa B / biosynthesis
  • Patched-1 Receptor / biosynthesis
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins p21(ras) / metabolism
  • Pyridines / therapeutic use*
  • Pyrimidines / therapeutic use*
  • RNA, Messenger / biosynthesis
  • Receptor, ErbB-2 / biosynthesis
  • Signal Transduction / drug effects
  • Smoothened Receptor / antagonists & inhibitors*
  • Zinc Finger Protein GLI1 / antagonists & inhibitors*
  • Zinc Finger Protein GLI1 / biosynthesis

Substances

  • Anilides
  • GANT 61
  • Hedgehog Proteins
  • HhAntag691
  • NF-kappa B
  • PTCH1 protein, human
  • Patched-1 Receptor
  • Pyridines
  • Pyrimidines
  • RNA, Messenger
  • SHH protein, human
  • SMO protein, human
  • Smoothened Receptor
  • Zinc Finger Protein GLI1
  • EGFR protein, human
  • ERBB2 protein, human
  • ErbB Receptors
  • Receptor, ErbB-2
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases
  • Proto-Oncogene Proteins p21(ras)