Inhibition of ERα/ERK/P62 cascades induces "autophagic switch" in the estrogen receptor-positive breast cancer cells exposed to gemcitabine

Oncotarget. 2016 Jul 26;7(30):48501-48516. doi: 10.18632/oncotarget.10363.

Abstract

Several clinical trials revealed that estrogen receptor (ER) status had relevance to the response of mammary malignancy to chemotherapy. Autophagy has emerged as an important cellular mechanism of tumor cells in response to anticancer therapy. The aim of this study is to investigate whether gemcitabine induces autophagy, and more importantly, whether such autophagy is functional relevant to the therapeutic effects of gemcitabine in breast cancer cells in relation to the ER status. In our study, autophagy was induced both in ER+ MCF-7 and ER- MDA-MB-231 cells by gemcitabine markedly, while the autophagy plays distinct roles - cytoprotective in ER- MDA-MB-231 and cytotoxic in ER+ MCF-7 cells. Gemcitabine treatment leads to the activation of ERα-ERK-P62 signal pathway in MCF-7 cells which may augment the autophagic degradation, thus results in the excessive activation of autophagy and irreversible autophagic cell death eventually. Inhibition of ERα-ERK-P62 cascades in MCF-7 cells by small interfering RNA or PD98059 impairs the autophagic degradation, and leads to "autophagic switch" - from cytotoxic autophagy to cytoprotection. Moreover, stable overexpression of ERα in the ER- BCap37 breast cancer cell line enhances the gemcitabine-induced autophagy flux and switches the autophagic cytoprotection in ER- BCap37 to cytotoxicity effect in ER+ BCap37 cells. Our study firstly demonstrated that ER status influences gemcitabine efficacy via modulating the autophagy in breast cancer cells.

Keywords: P62; autophagy; breast cancer; estrogen receptor; gemcitabine.

MeSH terms

  • Antimetabolites, Antineoplastic / pharmacology*
  • Antimetabolites, Antineoplastic / therapeutic use
  • Autophagy / drug effects*
  • Beclin-1 / genetics
  • Beclin-1 / metabolism
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / pathology
  • Cytoprotection / drug effects
  • Deoxycytidine / analogs & derivatives*
  • Deoxycytidine / pharmacology
  • Deoxycytidine / therapeutic use
  • Estrogen Receptor alpha / metabolism
  • Female
  • Flavonoids / pharmacology
  • Gemcitabine
  • Humans
  • MCF-7 Cells
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Prohibitins
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Sequestosome-1 Protein / metabolism
  • Signal Transduction / drug effects*

Substances

  • Antimetabolites, Antineoplastic
  • BECN1 protein, human
  • Beclin-1
  • ESR1 protein, human
  • Estrogen Receptor alpha
  • Flavonoids
  • PHB2 protein, human
  • Prohibitins
  • RNA, Small Interfering
  • SQSTM1 protein, human
  • Sequestosome-1 Protein
  • Deoxycytidine
  • MAPK1 protein, human
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one
  • Gemcitabine