Basal and therapy-driven hypoxia-inducible factor-1α confers resistance to endocrine therapy in estrogen receptor-positive breast cancer

Oncotarget. 2015 Apr 20;6(11):8648-62. doi: 10.18632/oncotarget.3257.

Abstract

Resistance is an obstacle to endocrine therapy for breast cancer. We measured levels of hypoxia-inducible factor (HIF)-1α in 52 primary breast cancer patients before and after receiving neoadjuvant endocrine therapy with letrozole for at least 3 months. Pre-treatment levels of HIF-1α were associated with negative clinical outcome. Furthermore, levels of HIF-1α were increased in post-treatment residual tumors compared with those in pre-treatment biopsy samples. In animal studies, xenografts stably expressing HIF-1α were resistant to endocrine therapy with fulvestrant compared with the effects in control xenografts. Additionally, HIF-1α transcription was inhibited by zoledronic acid, a conventional drug for the treatment of postmenopausal osteoporosis, and was accompanied by a marked inhibition of the RAS/MAPK/ERK1/2 pathway. HIF-1α is a determinant of resistance to endocrine therapy and should be considered as a potential therapeutic target for overcoming endocrine resistance in estrogen receptor (ER)-positive breast cancer. In addition, zoledronic acid may overcome endocrine resistance in ER-positive human breast cancer by targeting HIF-1α transcription through inhibition of the RAS/MAPK/ERK1/2 pathway. Clinical studies on the administration of zoledronic acid as a second line treatment in patients who failed endocrine therapy should be considered to improve therapeutic outcomes in breast cancer patients.

Keywords: HIF-1a; breast cancer; endocrine resistance; estrogen receptor; zoledronic acid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents, Hormonal / pharmacology*
  • Antineoplastic Agents, Hormonal / therapeutic use
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology*
  • Cell Hypoxia
  • Cell Line, Tumor
  • Diphosphonates / pharmacology
  • Diphosphonates / therapeutic use*
  • Drug Resistance, Neoplasm / drug effects
  • Drug Resistance, Neoplasm / physiology*
  • Estradiol / analogs & derivatives
  • Estradiol / pharmacology
  • Estradiol / therapeutic use
  • Estrogens*
  • Female
  • Fulvestrant
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / antagonists & inhibitors
  • Hypoxia-Inducible Factor 1, alpha Subunit / biosynthesis
  • Hypoxia-Inducible Factor 1, alpha Subunit / physiology*
  • Imidazoles / pharmacology
  • Imidazoles / therapeutic use*
  • Letrozole
  • MAP Kinase Signaling System / drug effects
  • MAP Kinase Signaling System / physiology
  • Mice
  • Mice, Nude
  • Neoadjuvant Therapy
  • Neoplasm Proteins / analysis
  • Neoplasm Proteins / antagonists & inhibitors
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / physiology*
  • Neoplasms, Hormone-Dependent / drug therapy
  • Neoplasms, Hormone-Dependent / metabolism
  • Neoplasms, Hormone-Dependent / pathology*
  • Neovascularization, Pathologic / drug therapy
  • Nitriles / pharmacology
  • Nitriles / therapeutic use
  • Postmenopause
  • RNA Interference
  • RNA, Small Interfering / genetics
  • Receptors, Estrogen / analysis*
  • Transcription, Genetic / drug effects
  • Treatment Outcome
  • Triazoles / pharmacology
  • Triazoles / therapeutic use
  • Xenograft Model Antitumor Assays
  • Zoledronic Acid

Substances

  • Antineoplastic Agents, Hormonal
  • Diphosphonates
  • Estrogens
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Imidazoles
  • Neoplasm Proteins
  • Nitriles
  • RNA, Small Interfering
  • Receptors, Estrogen
  • Triazoles
  • Fulvestrant
  • Estradiol
  • Zoledronic Acid
  • Letrozole