Inhibition of c-Met downregulates TIGAR expression and reduces NADPH production leading to cell death

Oncogene. 2011 Mar 3;30(9):1127-34. doi: 10.1038/onc.2010.490. Epub 2010 Nov 8.

Abstract

c-Met represents an important emerging therapeutic target in cancer. In this study, we demonstrate the mechanism by which c-Met tyrosine kinase inhibition inhibits tumor growth in a highly invasive Asian-prevalent head and neck cancer, nasopharyngeal cancer (NPC). c-Met tyrosine kinase inhibitors (TKIs; AM7 and c-Met TKI tool compound SU11274) downregulated c-Met phosphorylation, resulting in marked inhibition of NPC cell growth and invasion. Strikingly, inhibition of c-Met resulted in significant downregulation of TP53-induced Glycolysis and Apoptosis Regulator (TIGAR) and subsequent depletion of intracellular NADPH. Importantly, overexpression of TIGAR ameliorated the effects of c-Met kinase inhibition, confirming the importance of TIGAR downregulation in the growth inhibitory activity of c-Met TKI. The effects of c-Met inhibition on TIGAR and NADPH levels were observed with two different c-Met TKIs (AM7 and SU11274) and with multiple cell lines. As NADPH provides a crucial reducing power required for cell survival and proliferation, our findings reveal a novel mechanistic action of c-Met TKI, which may represent a key effect of c-Met kinase inhibition. Our data provide the first evidence linking c-Met, TIGAR and NADPH regulation in human cancer cells suggesting that inhibition of a tyrosine kinase/TIGAR/NADPH cascade may have therapeutic applicability in human cancers.

Publication types

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

MeSH terms

  • Apoptosis
  • Apoptosis Regulatory Proteins
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival
  • Down-Regulation
  • Humans
  • Indoles / pharmacology*
  • Intracellular Signaling Peptides and Proteins / genetics*
  • NADP / biosynthesis*
  • Nasopharyngeal Neoplasms / drug therapy
  • Nasopharyngeal Neoplasms / metabolism*
  • Nasopharyngeal Neoplasms / pathology
  • Phosphoric Monoester Hydrolases
  • Phosphorylation
  • Piperazines / pharmacology*
  • Protein Kinase Inhibitors / pharmacology*
  • Proto-Oncogene Proteins c-met / antagonists & inhibitors*
  • Proto-Oncogene Proteins c-met / genetics
  • Proto-Oncogene Proteins c-met / metabolism
  • Pyrimidinones / pharmacology*
  • Quinolines / pharmacology*
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Sulfonamides / pharmacology*

Substances

  • ((3Z)-N-(3-chlorophenyl)-3-((3,5-dimethyl-4-((4-methylpiperazin-1-yl)carbonyl)-1H-pyrrol-2-yl)methylene)-N-methyl-2-oxo-2,3-dihydro-1H-indole-5-sulfonamide)
  • 5-(3-fluoro-4-((6-(methyloxy)-7-((3-(4-morpholinyl)propyl)oxy)-4-quinolinyl)oxy)phenyl)-3-methyl-2-(phenylmethyl)-4(3H)pyrimidinone
  • Apoptosis Regulatory Proteins
  • Indoles
  • Intracellular Signaling Peptides and Proteins
  • Piperazines
  • Protein Kinase Inhibitors
  • Pyrimidinones
  • Quinolines
  • Sulfonamides
  • NADP
  • Proto-Oncogene Proteins c-met
  • Phosphoric Monoester Hydrolases
  • TIGAR protein, human