Modulation of melanoma cell phospholipid metabolism in response to heat shock protein 90 inhibition

Oncotarget. 2010 Jul;1(3):185-97. doi: 10.18632/oncotarget.125.

Abstract

Molecular chaperone heat shock protein 90 (Hsp90) inhibitors are promising targeted cancer therapeutic drugs, with the advantage that they deplete multiple oncogenic client proteins and modulate all the classical hallmarks of cancer. They are now in clinical trial and show potential for activity in melanoma and other malignancies. Here we explore the metabolic response to Hsp90 inhibition in human melanoma cells using magnetic resonance spectroscopy. We show that, concomitant with growth inhibition and re-differentiation, Hsp90 inhibition in human melanoma cells is associated with increased glycerophosphocholine content. This was seen with both the clinical geldanamycin-based Hsp90 drug 17-AAG and the structurally dissimilar Hsp90 inhibitor CCT018159. The effect was noted in both BRAF mutant SKMEL28 and BRAF wildtype CHL-1 melanoma cells. Elevated content of the -CH2+CH3 fatty acyl chains and cytoplasmic mobile lipid droplets was also observed in 17-AAG-treated SKMEL28 cells. Importantly, the phospholipase A2 inhibitor bromoenol lactone prevented the rise in glycerophosphocholine seen with 17-AAG, suggesting a role for phospholipase A2 activation in the Hsp90 inhibitor-induced metabolic response. Our findings provide a basis for using metabolic changes as non-invasive indicators of Hsp90 inhibition and potentially as biomarkers of anticancer activity with Hsp90 drugs in malignant melanoma and possibly in other cancers.

Keywords: Hsp90; MRS; melanoma; metabolism; phospholipid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents / therapeutic use
  • Benzoquinones / chemistry
  • Benzoquinones / pharmacology*
  • Benzoquinones / therapeutic use
  • Biomarkers, Pharmacological
  • Glycerylphosphorylcholine / metabolism
  • HSP90 Heat-Shock Proteins / antagonists & inhibitors*
  • Heterocyclic Compounds, 2-Ring / chemistry
  • Heterocyclic Compounds, 2-Ring / pharmacology
  • Humans
  • Lactams, Macrocyclic / chemistry
  • Lactams, Macrocyclic / pharmacology*
  • Lactams, Macrocyclic / therapeutic use
  • Lipid Metabolism / drug effects
  • Magnetic Resonance Spectroscopy
  • Melanoma / drug therapy*
  • Melanoma / metabolism*
  • Melanoma / pathology
  • Mutation / genetics
  • Naphthalenes / pharmacology
  • Phospholipase A2 Inhibitors
  • Proto-Oncogene Proteins B-raf / genetics
  • Proto-Oncogene Proteins B-raf / metabolism
  • Pyrazoles / chemistry
  • Pyrazoles / pharmacology
  • Pyrones / pharmacology
  • Skin Neoplasms / drug therapy*
  • Skin Neoplasms / metabolism*
  • Skin Neoplasms / pathology

Substances

  • Antineoplastic Agents
  • Benzoquinones
  • Biomarkers, Pharmacological
  • CCT018159
  • HSP90 Heat-Shock Proteins
  • Heterocyclic Compounds, 2-Ring
  • Lactams, Macrocyclic
  • Naphthalenes
  • Phospholipase A2 Inhibitors
  • Pyrazoles
  • Pyrones
  • tanespimycin
  • Glycerylphosphorylcholine
  • 6-(bromomethylene)tetrahydro-3-(1-naphthaleneyl)-2H-pyran-2-one
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf