IL-13Rα2 mediates PNR-induced migration and metastasis in ERα-negative breast cancer

Oncogene. 2015 Mar 19;34(12):1596-607. doi: 10.1038/onc.2014.53. Epub 2014 Apr 21.

Abstract

Emerging evidence has linked photoreceptor cell-specific nuclear receptor (PNR/NR2E3), an orphan nuclear hormone receptor, to human breast cancer. PNR was shown to be a transcriptional activator of estrogen receptor-α (ERα) in ERα-positive breast cancer cell lines and high-level expression of PNR correlates with favorable response of ERα-positive breast cancer patients to tamoxifen. Interestingly, gene expression microarray study shows that PNR regulates distinct genes from those regulated by ERα, suggesting that PNR could have ERα-independent functions. Herein, we investigated the function of PNR in ERα-negative breast cancer cells. Our results showed that PNR-induced cell migration and metastasis of ERα-negative breast cancer cells both in vitro and in vivo, and the effect was attributed to the upregulation of interleukin (IL)-13Rα2, a high-affinity receptor for IL-13 that regulates tumor growth, invasion and metastasis of various human cancers. Mechanistically, PNR activated transcription of IL-13Rα2 through direct recruitment to IL-13Rα2 promoter. Upon stimulation with IL-13, IL-13Rα2 increased the extracellular signal-regulated kinases 1 and 2 phosphorylation, which led to breast cancer migration and metastasis. The IL-13 triggered signal cascade was specific to IL-13Rα2, as the closely related IL-13Rα1 was not regulated by PNR. IL-13Rα2 is a novel tumor antigen that is overexpressed in a variety of solid tumor types. This study presents the first evidence that PNR could promote ERα-negative breast cancer metastasis through activation of IL-13Rα2-mediated signaling pathway.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology*
  • Cell Line, Tumor
  • Estrogen Receptor alpha / metabolism*
  • Female
  • Gene Expression Regulation, Neoplastic
  • HEK293 Cells
  • Humans
  • Interleukin-13 / metabolism
  • Interleukin-13 Receptor alpha2 Subunit / genetics*
  • Interleukin-13 Receptor alpha2 Subunit / metabolism
  • MCF-7 Cells
  • Mice
  • Neoplasm Metastasis
  • Neoplasm Transplantation
  • Orphan Nuclear Receptors / metabolism*
  • Signal Transduction / drug effects

Substances

  • Estrogen Receptor alpha
  • Interleukin-13
  • Interleukin-13 Receptor alpha2 Subunit
  • NR2E3 protein, human
  • Nr2e3 protein, mouse
  • Orphan Nuclear Receptors