Activation of Ras/PI3K/ERK pathway induces c-Myc stabilization to upregulate argininosuccinate synthetase, leading to arginine deiminase resistance in melanoma cells

Cancer Res. 2012 May 15;72(10):2622-33. doi: 10.1158/0008-5472.CAN-11-3605. Epub 2012 Mar 29.

Abstract

Melanomas and other cancers that do not express argininosuccinate synthetase (AS), the rate-limiting enzyme for arginine biosynthesis, are sensitive to arginine depletion with pegylated arginine deiminase (ADI-PEG20). However, ADI resistance eventually develops in tumors because of AS upregulation. Although it has been shown that AS upregulation involves c-Myc, the underlying mechanisms remain unknown. Here we show that ADI-PEG20 activates Ras signaling and the effector extracellular signal-regulated kinase (ERK) and phosphoinositide 3-kinase (PI3K)/AKT/GSK-3β kinase cascades, resulting in phosphorylation and stabilization of c-Myc by attenuation of its ubiquitin-mediated protein degradation mechanism. Inhibition of the induced cell signaling pathways using PI3K/AKT inhibitors suppressed c-Myc induction and enhanced ADI-mediated cell killing. Notably, in an animal model of AS-negative melanoma, combination therapy using a PI3K inhibitor plus ADI-PEG20 yielded additive antitumor effects as compared with either agent alone. Taken together, our findings offer mechanistic insight into arginine deprivation metabolism and ADI resistance, and they illustrate how combining inhibitors of the Ras/ERK and PI3K/AKT signaling pathways may improve ADI-PEG20 anticancer responses.

Publication types

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

MeSH terms

  • Animals
  • Argininosuccinate Synthase / biosynthesis*
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm*
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Female
  • Genes, ras
  • Humans
  • Hydrolases / pharmacology*
  • Hydrolases / therapeutic use
  • MAP Kinase Signaling System
  • Melanoma / drug therapy*
  • Melanoma / metabolism*
  • Mice
  • Mice, Nude
  • Phosphatidylinositol 3-Kinase
  • Polyethylene Glycols / pharmacology*
  • Polyethylene Glycols / therapeutic use
  • Protein Stability / drug effects
  • Proteolysis / drug effects
  • Proto-Oncogene Proteins c-myc / genetics*
  • Signal Transduction
  • Ubiquitin
  • Up-Regulation

Substances

  • MYC protein, human
  • Proto-Oncogene Proteins c-myc
  • Ubiquitin
  • Polyethylene Glycols
  • Phosphatidylinositol 3-Kinase
  • Extracellular Signal-Regulated MAP Kinases
  • Hydrolases
  • ADI PEG20
  • arginine deiminase
  • Argininosuccinate Synthase