Leptin receptor maintains cancer stem-like properties in triple negative breast cancer cells

Endocr Relat Cancer. 2013 Oct 14;20(6):797-808. doi: 10.1530/ERC-13-0329. Print 2013 Dec.

Abstract

Despite new therapies, breast cancer continues to be the second leading cause of cancer mortality in women, a consequence of recurrence and metastasis. In recent years, a population of cancer cells has been identified, called cancer stem cells (CSCs) with self-renewal capacity, proposed to underlie tumor recurrence and metastasis. We previously showed that the adipose tissue cytokine LEPTIN, increased in obesity, promotes the survival of CSCs in vivo. Here, we tested the hypothesis that the leptin receptor (LEPR), expressed in mammary cancer cells, is necessary for maintaining CSC-like and metastatic properties. We silenced LEPR via shRNA lentivirus transduction and determined that the expression of stem cell self-renewal transcription factors NANOG, SOX2, and OCT4 (POU5F1) is inhibited. LEPR-NANOG signaling pathway is conserved between species because we can rescue NANOG expression in human LEPR-silenced cells with the mouse LepR. Using a NANOG promoter GFP reporter, we showed that LEPR is enriched in NANOG promoter active (GFP+) cells. In lineage tracing studies, we showed that the GFP+ cells divide in a symmetric and asymmetric manner. LEPR-silenced MDA-MB-231 cells exhibit a mesenchymal to epithelial transition morphologically, increased E-CADHERIN and decreased VIMENTIN expression compared with control cells. Finally, LEPR-silenced cells exhibit reduced cell proliferation, self-renewal in tumor sphere assays, and tumor outgrowth in xenotransplant studies. Given the emergence of NANOG as a pro-carcinogenic protein in multiple cancers, these studies suggest that inhibition of LEPR may be a promising therapeutic approach to inhibit NANOG and thereby neutralize CSC functions.

Keywords: NANOG; breast cancer; cancer stem cell; leptin receptor; obesity.

Publication types

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

MeSH terms

  • Animals
  • Blotting, Western
  • Cell Proliferation
  • Female
  • Flow Cytometry
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Humans
  • Mesoderm / metabolism
  • Mesoderm / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nanog Homeobox Protein
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology*
  • Phosphorylation
  • RNA, Messenger / genetics
  • RNA, Small Interfering / genetics
  • Real-Time Polymerase Chain Reaction
  • Receptors, Leptin / antagonists & inhibitors
  • Receptors, Leptin / genetics
  • Receptors, Leptin / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Triple Negative Breast Neoplasms / metabolism
  • Triple Negative Breast Neoplasms / pathology*
  • Tumor Cells, Cultured
  • Wnt1 Protein / genetics
  • Wnt1 Protein / metabolism

Substances

  • Homeodomain Proteins
  • LEPR protein, human
  • NANOG protein, human
  • Nanog Homeobox Protein
  • RNA, Messenger
  • RNA, Small Interfering
  • Receptors, Leptin
  • Wnt1 Protein
  • Wnt1 protein, mouse