Systematic analysis of BRAF(V600E) melanomas reveals a role for JNK/c-Jun pathway in adaptive resistance to drug-induced apoptosis

Mol Syst Biol. 2015 Mar 26;11(3):797. doi: 10.15252/msb.20145877.

Abstract

Drugs that inhibit RAF/MEK signaling, such as vemurafenib, elicit profound but often temporary anti-tumor responses in patients with BRAF(V) (600E) melanoma. Adaptive responses to RAF/MEK inhibition occur on a timescale of hours to days, involve homeostatic responses that reactivate MAP kinase signaling and compensatory mitogenic pathways, and attenuate the anti-tumor effects of RAF/MEK inhibitors. We profile adaptive responses across a panel of melanoma cell lines using multiplex biochemical measurement, single-cell assays, and statistical modeling and show that adaptation involves at least six signaling cascades that act to reduce drug potency (IC50) and maximal effect (i.e., Emax ≪ 1). Among these cascades, we identify a role for JNK/c-Jun signaling in vemurafenib adaptation and show that RAF and JNK inhibitors synergize in cell killing. This arises because JNK inhibition prevents a subset of cells in a cycling population from becoming quiescent upon vemurafenib treatment, thereby reducing drug Emax. Our findings demonstrate the breadth and diversity of adaptive responses to RAF/MEK inhibition and a means to identify which steps in a signaling cascade are most predictive of phenotypic response.

Keywords: BRAFV600E melanomas; RAF and MEK inhibitors; adaptive responses; cell‐to‐cell variability; submaximal drug effect.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Apoptosis
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Drug Resistance, Neoplasm*
  • Drug Synergism
  • Humans
  • Indoles / pharmacology*
  • MAP Kinase Signaling System
  • Melanoma / drug therapy
  • Melanoma / genetics*
  • Mutation
  • Protein Kinase Inhibitors / pharmacology*
  • Proto-Oncogene Proteins B-raf / genetics*
  • Sulfonamides / pharmacology*
  • Vemurafenib

Substances

  • Indoles
  • Protein Kinase Inhibitors
  • Sulfonamides
  • Vemurafenib
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf