Differential inhibition of ex-vivo tumor kinase activity by vemurafenib in BRAF(V600E) and BRAF wild-type metastatic malignant melanoma

PLoS One. 2013 Aug 30;8(8):e72692. doi: 10.1371/journal.pone.0072692. eCollection 2013.

Abstract

Background: Treatment of metastatic malignant melanoma patients harboring BRAF(V600E) has improved drastically after the discovery of the BRAF inhibitor, vemurafenib. However, drug resistance is a recurring problem, and prognoses are still very bad for patients harboring BRAF wild-type. Better markers for targeted therapy are therefore urgently needed.

Methodology: In this study, we assessed the individual kinase activity profiles in 26 tumor samples obtained from patients with metastatic malignant melanoma using peptide arrays with 144 kinase substrates. In addition, we studied the overall ex-vivo inhibitory effects of vemurafenib and sunitinib on kinase activity status.

Results: Overall kinase activity was significantly higher in lysates from melanoma tumors compared to normal skin tissue. Furthermore, ex-vivo incubation with both vemurafenib and sunitinib caused significant decrease in phosphorylation of kinase substrates, i.e kinase activity. While basal phosphorylation profiles were similar in BRAF wild-type and BRAF(V600E) tumors, analysis with ex-vivo vemurafenib treatment identified a subset of 40 kinase substrates showing stronger inhibition in BRAF(V600E) tumor lysates, distinguishing the BRAF wild-type and BRAF(V600E) tumors. Interestingly, a few BRAF wild-type tumors showed inhibition profiles similar to BRAF(V600E) tumors. The kinase inhibitory effect of vemurafenib was subsequently analyzed in cell lines harboring different BRAF mutational status with various vemurafenib sensitivity in-vitro.

Conclusions: Our findings suggest that multiplex kinase substrate array analysis give valuable information about overall tumor kinase activity. Furthermore, intra-assay exposure to kinase inhibiting drugs may provide a useful tool to study mechanisms of resistance, as well as to identify predictive markers.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Cell Line, Tumor
  • Cluster Analysis
  • ErbB Receptors / antagonists & inhibitors
  • ErbB Receptors / metabolism
  • Female
  • Humans
  • Indoles / pharmacology*
  • Indoles / therapeutic use*
  • Male
  • Melanoma / drug therapy*
  • Melanoma / enzymology*
  • Melanoma / pathology
  • Middle Aged
  • Mutant Proteins / antagonists & inhibitors
  • Mutant Proteins / metabolism
  • Mutation / genetics
  • Neoplasm Metastasis
  • Protein Kinase Inhibitors / pharmacology
  • Protein Kinase Inhibitors / therapeutic use
  • Proto-Oncogene Proteins B-raf / antagonists & inhibitors*
  • Proto-Oncogene Proteins B-raf / genetics
  • Pyrroles / pharmacology
  • Pyrroles / therapeutic use
  • Receptor, Platelet-Derived Growth Factor beta / antagonists & inhibitors
  • Receptor, Platelet-Derived Growth Factor beta / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Skin / drug effects
  • Skin / enzymology
  • Skin / pathology
  • Skin Neoplasms / drug therapy*
  • Skin Neoplasms / enzymology*
  • Skin Neoplasms / pathology
  • Substrate Specificity / drug effects
  • Sulfonamides / pharmacology*
  • Sulfonamides / therapeutic use*
  • Sunitinib
  • Vemurafenib

Substances

  • Indoles
  • Mutant Proteins
  • Protein Kinase Inhibitors
  • Pyrroles
  • Sulfonamides
  • Vemurafenib
  • ErbB Receptors
  • Receptor, Platelet-Derived Growth Factor beta
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf
  • Sunitinib

Grants and funding

This work was supported by Grant No. 2011030 from the South-Eastern Norway Regional Health Authority to VNK, and grants received from Division of Medicine, Akershus University Hospital. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.