2-methoxyestradiol inhibits hypoxia-inducible factor 1alpha, tumor growth, and angiogenesis and augments paclitaxel efficacy in head and neck squamous cell carcinoma

Clin Cancer Res. 2004 Dec 15;10(24):8665-73. doi: 10.1158/1078-0432.CCR-04-1393.

Abstract

Purpose: Head and neck squamous cell carcinomas have been reported to overexpress hypoxia-inducible factor (HIF)-1alpha, a transcription factor that promotes expression of angiogenesis factors and resistance to programmed and therapy-induced cell death. 2-Methoxyestradiol (2ME2) is a natural compound with HIF-1alpha inhibitory activity that is currently being evaluated in phase 1 and 2 clinical trials for advanced solid tumors and multiple myeloma. To our knowledge, this is the first study to evaluate the effects of 2ME2 in head and neck squamous cell carcinoma.

Experimental design: In the present study, we investigated the effects of 2ME2 alone and in combination with paclitaxel, an active agent in recurrent or advanced head and neck squamous cell carcinoma.

Results: 2ME2 exhibited antiproliferative and cytotoxic effects in a panel of five head and neck squamous cell carcinoma cell lines in the 0.5 to 10 micromol/L range, including induction of G2-M blockade, caspase-3/7 activation, and apoptosis at 48 hours. 2ME2 resulted in decreased nuclear HIF-1alpha-binding activity and affected the expression of downstream genes, such as bid, a proapoptotic bcl-2 family member, and vascular endothelial growth factor, a proangiogenic cytokine. The up-regulation of Bid (57.5% at 12 hours, P < 0.0006) and inhibition of vascular endothelial growth factor secretion (57.7% at 24 hours, P < 0.015; and 50.3% at 48 hours, P < 0.0006) could be partially attributed to the effects on HIF-1alpha, because HIF-1alpha small interfering RNAs produced similar effects. Finally, in vivo, in a xenograft model of head and neck squamous cell carcinoma using UM-SCC-11A cells, 2ME2 exhibited antitumor and antiangiogenic activity, as measured by CD31 immunostaining.

Conclusions: These results provide support for the use of 2ME2 in combination with paclitaxel for the treatment of recurrent or advanced head and neck squamous cell carcinoma.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • 2-Methoxyestradiol
  • Animals
  • Antineoplastic Agents, Phytogenic / therapeutic use*
  • BH3 Interacting Domain Death Agonist Protein
  • Carcinoma, Squamous Cell / metabolism
  • Carcinoma, Squamous Cell / pathology
  • Carcinoma, Squamous Cell / prevention & control*
  • Carrier Proteins / metabolism
  • Caspase 3
  • Caspase 7
  • Caspases / metabolism
  • Cell Division / drug effects
  • Cell Hypoxia*
  • Drug Therapy, Combination
  • Enzyme Activation / drug effects
  • Estradiol / analogs & derivatives*
  • Estradiol / therapeutic use
  • Female
  • G2 Phase / drug effects
  • Head and Neck Neoplasms / metabolism
  • Head and Neck Neoplasms / pathology
  • Head and Neck Neoplasms / prevention & control*
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Mice
  • Mice, Inbred BALB C
  • Mice, SCID
  • Microcirculation
  • Paclitaxel / therapeutic use*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • RNA, Small Interfering / pharmacology
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Antineoplastic Agents, Phytogenic
  • BH3 Interacting Domain Death Agonist Protein
  • BID protein, human
  • Bid protein, mouse
  • Carrier Proteins
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Proto-Oncogene Proteins c-bcl-2
  • RNA, Small Interfering
  • Transcription Factors
  • Vascular Endothelial Growth Factor A
  • Estradiol
  • 2-Methoxyestradiol
  • CASP3 protein, human
  • CASP7 protein, human
  • Casp3 protein, mouse
  • Casp7 protein, mouse
  • Caspase 3
  • Caspase 7
  • Caspases
  • Paclitaxel