Dietary energy balance modulates epithelial-to-mesenchymal transition and tumor progression in murine claudin-low and basal-like mammary tumor models

Cancer Prev Res (Phila). 2012 Jul;5(7):930-42. doi: 10.1158/1940-6207.CAPR-12-0034. Epub 2012 May 15.

Abstract

Using novel murine models of claudin-low and basal-like breast cancer, we tested the hypothesis that diet-induced obesity (DIO) and calorie restriction (CR) differentially modulate progression of these aggressive breast cancer subtypes. For model development, we characterized two cell lines, "mesenchymal (M)-Wnt" and "epithelial (E)-Wnt," derived from MMTV-Wnt-1 transgenic mouse mammary tumors. M-Wnt, relative to E-Wnt, cells were tumor-initiating cell (TIC)-enriched (62% vs. 2.4% CD44(high)/CD24(low)) and displayed enhanced ALDEFLUOR positivity, epithelial-to-mesenchymal transition (EMT) marker expression, mammosphere-forming ability, migration, invasion, and tumorigenicity (P < 0.001; each parameter). M-Wnt and E-Wnt cells clustered with claudin-low and basal-like breast tumors, respectively, in gene expression profiles and recapitulated these tumors when orthotopically transplanted into ovariectomized C57BL/6 mice. To assess the effects of energy balance interventions on tumor progression and EMT, mice were administered DIO, control, or CR diets for 8 weeks before orthotopic transplantation of M-Wnt or E-Wnt cells (for each cell line, n = 20 mice per diet) and continued on their diets for 6 weeks while tumor growth was monitored. Relative to control, DIO enhanced M-Wnt (P = 0.01), but not E-Wnt, tumor progression; upregulated EMT- and TIC-associated markers including N-cadherin,fibronectin, TGFβ, Snail, FOXC2, and Oct4 (P < 0.05, each); and increased intratumoral adipocytes. Conversely, CR suppressed M-Wnt and E-Wnt tumor progression (P < 0.02, each) and inhibited EMT and intratumoral adipocyte accumulation. Thus, dietary energy balance interventions differentially modulate EMT and progression of claudin-low and basal-like tumors. EMT pathway components may represent targets for breaking the obesity-breast cancer link, particularly for preventing and/or controlling TIC-enriched subtypes such as claudin-low breast cancer.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism
  • Blotting, Western
  • Carcinoma, Basal Cell / etiology
  • Carcinoma, Basal Cell / metabolism
  • Carcinoma, Basal Cell / pathology*
  • Cell Adhesion
  • Cell Differentiation
  • Cell Movement
  • Cell Proliferation
  • Claudins / deficiency*
  • Diet*
  • Disease Progression
  • Energy Metabolism*
  • Epithelial-Mesenchymal Transition*
  • Female
  • Fluorescent Antibody Technique
  • Gene Expression Profiling
  • Humans
  • Immunoenzyme Techniques
  • Mammary Neoplasms, Animal / etiology
  • Mammary Neoplasms, Animal / metabolism
  • Mammary Neoplasms, Animal / pathology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neoplastic Stem Cells / pathology*
  • Oligonucleotide Array Sequence Analysis
  • Ovariectomy
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • Tumor Cells, Cultured
  • Wnt Proteins / genetics
  • Wnt Proteins / metabolism

Substances

  • Biomarkers, Tumor
  • Claudins
  • RNA, Messenger
  • Wnt Proteins