Incomplete inhibition of phosphorylation of 4E-BP1 as a mechanism of primary resistance to ATP-competitive mTOR inhibitors

Oncogene. 2014 Mar 20;33(12):1590-600. doi: 10.1038/onc.2013.92. Epub 2013 Apr 1.

Abstract

The mammalian target of rapamycin (mTOR) regulates cell growth by integrating nutrient and growth factor signaling and is strongly implicated in cancer. But mTOR is not an oncogene, and which tumors will be resistant or sensitive to new adenosine triphosphate (ATP) competitive mTOR inhibitors now in clinical trials remains unknown. We screened a panel of over 600 human cancer cell lines to identify markers of resistance and sensitivity to the mTOR inhibitor PP242. RAS and phosphatidylinositol 3-kinase catalytic subunit alpha (PIK3CA) mutations were the most significant genetic markers for resistance and sensitivity to PP242, respectively; colon origin was the most significant marker for resistance based on tissue type. Among colon cancer cell lines, those with KRAS mutations were most resistant to PP242, whereas those without KRAS mutations most sensitive. Surprisingly, cell lines with co-mutation of PIK3CA and KRAS had intermediate sensitivity. Immunoblot analysis of the signaling targets downstream of mTOR revealed that the degree of cellular growth inhibition induced by PP242 was correlated with inhibition of phosphorylation of the translational repressor eIF4E-binding protein 1 (4E-BP1), but not ribosomal protein S6 (rpS6). In a tumor growth inhibition trial of PP242 in patient-derived colon cancer xenografts, resistance to PP242-induced inhibition of 4E-BP1 phosphorylation and xenograft growth was again observed in KRAS mutant tumors without PIK3CA co-mutation, compared with KRAS wild-type controls. We show that, in the absence of PIK3CA co-mutation, KRAS mutations are associated with resistance to PP242 and that this is specifically linked to changes in the level of phosphorylation of 4E-BP1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Adenosine Triphosphate / metabolism*
  • Animals
  • Antineoplastic Agents / pharmacology*
  • Binding, Competitive / drug effects*
  • Carrier Proteins / metabolism*
  • Cell Cycle Proteins
  • Cell Line, Tumor
  • Class I Phosphatidylinositol 3-Kinases
  • Colonic Neoplasms / pathology
  • Drug Resistance, Neoplasm / drug effects*
  • Eukaryotic Initiation Factors
  • Female
  • Humans
  • Indoles / pharmacology*
  • MAP Kinase Signaling System / drug effects
  • Mice
  • Mutation
  • Phosphatidylinositol 3-Kinases / genetics
  • Phosphoproteins / metabolism*
  • Phosphorylation / drug effects
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins p21(ras)
  • Purines / pharmacology*
  • Ribosomal Protein S6 / metabolism
  • TOR Serine-Threonine Kinases / antagonists & inhibitors*
  • TOR Serine-Threonine Kinases / metabolism
  • Xenograft Model Antitumor Assays
  • ras Proteins / genetics

Substances

  • Adaptor Proteins, Signal Transducing
  • Antineoplastic Agents
  • Carrier Proteins
  • Cell Cycle Proteins
  • Eif4ebp1 protein, mouse
  • Eukaryotic Initiation Factors
  • Indoles
  • KRAS protein, human
  • Phosphoproteins
  • Proto-Oncogene Proteins
  • Purines
  • Ribosomal Protein S6
  • Adenosine Triphosphate
  • Class I Phosphatidylinositol 3-Kinases
  • PIK3CA protein, human
  • TOR Serine-Threonine Kinases
  • Proto-Oncogene Proteins p21(ras)
  • ras Proteins
  • PP242