A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors

Nature. 2003 Sep 25;425(6956):407-10. doi: 10.1038/nature01913.

Abstract

Heat shock protein 90 (Hsp90) is a molecular chaperone that plays a key role in the conformational maturation of oncogenic signalling proteins, including HER-2/ErbB2, Akt, Raf-1, Bcr-Abl and mutated p53. Hsp90 inhibitors bind to Hsp90, and induce the proteasomal degradation of Hsp90 client proteins. Although Hsp90 is highly expressed in most cells, Hsp90 inhibitors selectively kill cancer cells compared to normal cells, and the Hsp90 inhibitor 17-allylaminogeldanamycin (17-AAG) is currently in phase I clinical trials. However, the molecular basis of the tumour selectivity of Hsp90 inhibitors is unknown. Here we report that Hsp90 derived from tumour cells has a 100-fold higher binding affinity for 17-AAG than does Hsp90 from normal cells. Tumour Hsp90 is present entirely in multi-chaperone complexes with high ATPase activity, whereas Hsp90 from normal tissues is in a latent, uncomplexed state. In vitro reconstitution of chaperone complexes with Hsp90 resulted in increased binding affinity to 17-AAG, and increased ATPase activity. These results suggest that tumour cells contain Hsp90 complexes in an activated, high-affinity conformation that facilitates malignant progression, and that may represent a unique target for cancer therapeutics.

MeSH terms

  • Adenosine Triphosphatases / metabolism
  • Adenosine Triphosphate / metabolism
  • Antineoplastic Agents / metabolism*
  • Antineoplastic Agents / pharmacology*
  • Benzoquinones
  • Cell Line
  • Cysteine Endopeptidases / metabolism
  • HSP90 Heat-Shock Proteins / antagonists & inhibitors*
  • HSP90 Heat-Shock Proteins / chemistry*
  • HSP90 Heat-Shock Proteins / metabolism
  • Humans
  • Inhibitory Concentration 50
  • Lactams, Macrocyclic
  • Multienzyme Complexes / metabolism
  • Neoplasms / drug therapy
  • Neoplasms / metabolism*
  • Precipitin Tests
  • Proteasome Endopeptidase Complex
  • Protein Binding / drug effects
  • Protein Conformation
  • Rifabutin / analogs & derivatives*
  • Rifabutin / metabolism*
  • Rifabutin / pharmacology*
  • Substrate Specificity
  • Tumor Cells, Cultured

Substances

  • Antineoplastic Agents
  • Benzoquinones
  • HSP90 Heat-Shock Proteins
  • Lactams, Macrocyclic
  • Multienzyme Complexes
  • Rifabutin
  • tanespimycin
  • Adenosine Triphosphate
  • Cysteine Endopeptidases
  • Proteasome Endopeptidase Complex
  • Adenosine Triphosphatases