Levels of HdmX expression dictate the sensitivity of normal and transformed cells to Nutlin-3

Cancer Res. 2006 Mar 15;66(6):3169-76. doi: 10.1158/0008-5472.CAN-05-3832.

Abstract

Hdm2 and HdmX coordinately regulate the stability and function of p53. Each is overexpressed in subsets of many different types of malignancy, and most of these subsets maintain wild-type p53. Nutlins, newly discovered small-molecule inhibitors of the Hdm2-p53 interaction, offer a novel strategy for therapy of tumors with wild-type p53. We now show that Nutlin-3 efficiently induces apoptosis and diminishes long-term survival of human fibroblasts transformed in vitro by Hdm2 but not HdmX. The resistance of cells overexpressing HdmX to Nutlin-3 is due to its inability to disrupt the p53-HdmX interaction, resulting in continued suppression of p53 activity. Although HdmX overexpression yielded cells resistant to Nutlin-3, ablation of HdmX expression by short hairpin RNA sensitized tumor cells to Nutlin-3-mediated cell death or arrest. Furthermore, deletion of the COOH-terminal RING finger domain of HdmX completely reversed the resistance to Nutlin-3, probably reflecting the requirement of the RING finger for interaction with Hdm2. Thus, the relative abundance of Hdm2 and HdmX and the specificity of Nutlin-3 for Hdm2 influence the sensitivity of cells to p53-dependent apoptosis or arrest in response to Nutlin-3. Our findings establish Hdm2 and HdmX as independent therapeutic targets with respect to reactivating wild-type p53 as a means for cancer therapy.

Publication types

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

MeSH terms

  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Cell Cycle Proteins
  • Cell Transformation, Neoplastic / metabolism
  • Colonic Neoplasms / drug therapy
  • Colonic Neoplasms / metabolism
  • Doxorubicin / administration & dosage
  • Drug Screening Assays, Antitumor
  • Drug Synergism
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • HCT116 Cells
  • Humans
  • Imidazoles / administration & dosage
  • Imidazoles / pharmacology*
  • Nuclear Proteins / biosynthesis*
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Piperazines / administration & dosage
  • Piperazines / pharmacology*
  • Protein Structure, Tertiary
  • Proto-Oncogene Proteins / biosynthesis*
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-mdm2 / metabolism
  • RNA, Small Interfering / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Cell Cycle Proteins
  • Imidazoles
  • MDM4 protein, human
  • Nuclear Proteins
  • Piperazines
  • Proto-Oncogene Proteins
  • RNA, Small Interfering
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • nutlin 3
  • Doxorubicin
  • MDM2 protein, human
  • Proto-Oncogene Proteins c-mdm2