Luminal breast cancer cell lines overexpressing ZNF703 are resistant to tamoxifen through activation of Akt/mTOR signaling

PLoS One. 2013 Aug 26;8(8):e72053. doi: 10.1371/journal.pone.0072053. eCollection 2013.

Abstract

Background: Selective estrogen receptor modulators, such as tamoxifen, play a pivotal role in the treatment of luminal-type breast cancer. However, in clinical applications, nearly half of breast cancer patients are insensitive to tamoxifen, a small number of whom have early recurrence or disease progression when receiving tamoxifen. The underlying mechanism of this resistance has not been determined. ZNF703 is a novel oncogene in the 15% of breast cancers that harbor 8p12 amplifications. Therefore, the goal of our study was to explore the role of ZNF703 in tamoxifen resistance.

Methodology/principal findings: We used immunohistochemistry techniques to examine ZNF703 expression in stage I-III primary breast cancer specimens and found a positive expression rate of 91.3%. All patients were divided into either high or low ZNF703 expression groups. We found that high ZNF703 expression mainly occurred in ER+ and PR+ breast cancers. Furthermore, 4-hydroxytamoxifen had different modes of action in breast cancer cell lines with high or low ZNF703 expression. ZNF703 overexpression in MCF-7 breast cancer cells activated the Akt/mTOR signaling pathway, downregulated ERα, and reduced the antitumor effect of tamoxifen. Low-dose tamoxifen did not suppress, but rather, stimulated the growth of cells overexpressing ZNF703. ZNF703 knockdown in MDA-MB-134 and HCC1500 luminal B-type breast cancer cell lines by siRNA significantly decreased survival rates when cells were treated with tamoxifen. Furthermore, targeting ZNF703 with a mTOR inhibitor increased the inhibitory effects of tamoxifen in ZNF703-overexpressing cells.

Conclusion/significance: Our study suggests that ZNF703 expression levels may predict tamoxifen sensitivity. Tamoxifen should be administered with caution to those patients bearing tumors with ZNF703 overexpression. However, large clinical trials and prospective clinical studies are needed to verify these results.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents, Hormonal / pharmacology
  • Antineoplastic Agents, Hormonal / therapeutic use
  • Blotting, Western
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Drug Resistance, Neoplasm*
  • Female
  • Humans
  • Immunohistochemistry
  • MCF-7 Cells
  • Middle Aged
  • Proto-Oncogene Proteins c-akt / metabolism*
  • RNA Interference
  • Receptors, Estrogen / metabolism
  • Receptors, Progesterone / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / drug effects*
  • TOR Serine-Threonine Kinases / metabolism*
  • Tamoxifen / analogs & derivatives
  • Tamoxifen / pharmacology*
  • Tamoxifen / therapeutic use
  • Tissue Array Analysis

Substances

  • Antineoplastic Agents, Hormonal
  • Carrier Proteins
  • Receptors, Estrogen
  • Receptors, Progesterone
  • ZNF703 protein, human
  • Tamoxifen
  • afimoxifene
  • MTOR protein, human
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases

Grants and funding

This work was supported by grants from the National Science and Technology Major Project of the Ministry of Science and Technology of China (No.2012ZX09301001-007 to MYG) and National Natural Science Foundation of China (No. 81202087, 81202088 to KWS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.