Identification of the ZAK-MKK4-JNK-TGFβ signaling pathway as a molecular target for novel synthetic iminoquinone anticancer compound BA-TPQ

Curr Cancer Drug Targets. 2013 Jul;13(6):651-60. doi: 10.2174/15680096113139990040.

Abstract

Identification and validation of molecular targets are considered as key elements in new drug discovery and development. We have recently demonstrated that a novel synthetic iminoquinone analog, termed [7-(benzylamino)- 1,3,4,8-tetrahydropyrrolo [4,3, 2-de]quinolin-8(1H)-one] (BA-TPQ), has significant anti-breast cancer activity both in vitro and in vivo, but the underlying molecular mechanisms are not fully understood. Herein, we report the molecular studies for BA-TPQ's effects on JNK and its upstream and downstream signaling pathways. The compound up-regulates the JNK protein levels by increasing its phosphorylation and decreasing its polyubiquitination-mediated degradation. It activates ZAK at the MAPKKK level and MKK4 at the MAPKK level. It also up-regulates the TGFβ2 mRNA level, which can be abolished by the JNK-specific inhibitor SP600125, but not TGFβ pathway-specific inhibitor SD-208, indicating that both JNK and TGFβ signaling pathways are activated by BA-TPQ and that the JNK pathway activation precedes TGFβ activation. The pro-apoptotic and anti-growth effects of BA-TPQ are significantly blocked by both the JNK and TGFβ pathway inhibitors. In addition, BA-TPQ activates the ZAK-MKK4-JNK pathway in MCF7 cells, but not normal MCF10A cells, demonstrating its cancer-specific activities. In conclusion, our results demonstrate that BA-TPQ activates the ZAK-MKK4-JNK-TGFβ signaling cascade as a molecular target for its anticancer activity.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents / adverse effects
  • Antineoplastic Agents / antagonists & inhibitors
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / enzymology
  • Breast Neoplasms / metabolism
  • Cell Line
  • Cell Proliferation / drug effects
  • Female
  • Humans
  • JNK Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • JNK Mitogen-Activated Protein Kinases / chemistry
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • MAP Kinase Kinase 4 / antagonists & inhibitors
  • MAP Kinase Kinase 4 / metabolism
  • MAP Kinase Kinase Kinases
  • MAP Kinase Signaling System / drug effects*
  • MCF-7 Cells
  • Mammary Glands, Human / drug effects
  • Mammary Glands, Human / enzymology
  • Mammary Glands, Human / metabolism
  • Neoplasm Proteins / agonists
  • Neoplasm Proteins / antagonists & inhibitors*
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism
  • Neoplasms / drug therapy*
  • Neoplasms / metabolism
  • Phosphorylation / drug effects
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinases / chemistry
  • Protein Kinases / metabolism
  • Protein Stability / drug effects
  • Pyrroles / adverse effects
  • Pyrroles / antagonists & inhibitors
  • Pyrroles / pharmacology*
  • Quinolones / adverse effects
  • Quinolones / antagonists & inhibitors
  • Quinolones / pharmacology*
  • Transforming Growth Factor beta2 / agonists
  • Transforming Growth Factor beta2 / antagonists & inhibitors
  • Transforming Growth Factor beta2 / genetics
  • Transforming Growth Factor beta2 / metabolism
  • Ubiquitination / drug effects
  • Up-Regulation / drug effects*

Substances

  • 7-(benzylamino)-1,3,4,8-tetrahydropyrrolo(4,3,2-de)quinolin-8(1H)-one
  • Antineoplastic Agents
  • Neoplasm Proteins
  • Protein Kinase Inhibitors
  • Pyrroles
  • Quinolones
  • TGFB2 protein, human
  • Transforming Growth Factor beta2
  • Protein Kinases
  • JNK Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinases
  • MAP3K20 protein, human
  • MAP Kinase Kinase 4
  • MAP2K4 protein, human