Hydroxychloroquine inhibits autophagy to potentiate antiestrogen responsiveness in ER+ breast cancer

Clin Cancer Res. 2014 Jun 15;20(12):3222-32. doi: 10.1158/1078-0432.CCR-13-3227.

Abstract

Purpose: Estrogen receptor-α (ERα)-targeted therapies including tamoxifen (TAM) or Faslodex (ICI) are used to treat ER(+) breast cancers. Up to 50% of tumors will acquire resistance to these interventions. Autophagy has been implicated as a major driver of antiestrogen resistance. We have explored the ability of hydroxychloroquine (HCQ), which inhibits autophagy, to affect antiestrogen responsiveness.

Experimental design: TAM-resistant MCF7-RR and ICI-resistant/TAM cross-resistant LCC9 ER(+) breast cancer cells were injected into mammary fat pads of female athymic mice and treated with TAM and/or ICI in combination with oral low-dose HCQ.

Results: We show that HCQ can increase antiestrogen responsiveness in MCF7-RR and LCC9 cells and tumors, likely through the inhibition of autophagy. However, the combination of ICI+HCQ was less effective than HCQ alone in vivo, unlike the TAM+HCQ combination. Antiestrogen treatment stimulated angiogenesis in tumors but did not prevent HCQ effectiveness. The lower efficacy of ICI+HCQ was associated with ICI effects on cell-mediated immunity within the tumor microenvironment. The mouse chemokine KC (CXCL1) and IFNγ were differentially regulated by both TAM and ICI treatments, suggesting a possible effect on macrophage development/activity. Consistent with these observations, TAM+HCQ treatment increased tumor CD68(+) cells infiltration, whereas ICI and ICI+HCQ reduced peripheral tumor macrophage content. Moreover, macrophage elimination of breast cancer target cells in vitro was reduced following exposure to ICI.

Conclusion: HCQ restores antiestrogen sensitivity to resistant tumors. Moreover, the beneficial combination of TAM+HCQ suggests a positive outcome for ongoing neoadjuvant clinical trials using this combination for the treatment of ER(+) ductal carcinoma in situ lesions.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Autophagy / drug effects*
  • Blotting, Western
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cell Differentiation / drug effects
  • Cell Proliferation / drug effects
  • Drug Resistance, Neoplasm / drug effects*
  • Estradiol / analogs & derivatives*
  • Estradiol / pharmacology
  • Estrogen Antagonists / pharmacology
  • Estrogen Receptor Modulators / pharmacology*
  • Female
  • Fulvestrant
  • Humans
  • Hydroxychloroquine / pharmacology*
  • Immunoenzyme Techniques
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / pathology
  • Mice
  • Mice, Nude
  • Receptors, Estrogen / metabolism*
  • Tamoxifen / pharmacology*
  • Tumor Cells, Cultured
  • Xenograft Model Antitumor Assays

Substances

  • Estrogen Antagonists
  • Estrogen Receptor Modulators
  • Receptors, Estrogen
  • Tamoxifen
  • Fulvestrant
  • Hydroxychloroquine
  • Estradiol