NMR-based metabolomic analysis identifies RON-DEK-β-catenin dependent metabolic pathways and a gene signature that stratifies breast cancer patient survival

PLoS One. 2022 Sep 6;17(9):e0274128. doi: 10.1371/journal.pone.0274128. eCollection 2022.

Abstract

Background: Advances in detection techniques and treatment have increased the diagnosis of breast cancer at early stages; however, recurrence occurs in all breast cancer subtypes, and both recurrent and de novo metastasis are typically treatment resistant. A growing body of evidence supports the notion that metabolic plasticity drives cancer recurrence. RON and DEK are proteins that promote cancer metastasis and synergize mechanistically to activate β-catenin, but the metabolic consequences are unknown.

Methods: To ascertain RON-DEK-β-catenin dependent metabolic pathways, we utilized an NMR-based metabolomics approach to determine steady state levels of metabolites. We also interrogated altered metabolic pathway gene expression for prognostic capacity in breast cancer patient relapse-free and distant metastasis-free survival and discover a metabolic signature that is likely associated with recurrence.

Results: RON-DEK-β-catenin loss showed a consistent metabolite regulation of succinate and phosphocreatine. Consistent metabolite alterations between RON and DEK loss (but not β-catenin) were found in media glucose consumption, lactate secretion, acetate secretion, and intracellular glutamine and glutathione levels. Consistent metabolite alterations between RON and β-catenin loss (and not DEK) were found only in intracellular lactate levels. Further pathway hits include β-catenin include glycolysis, glycosylation, TCA cycle/anaplerosis, NAD+ production, and creatine dynamics. Genes in these pathways epistatic to RON-DEK-β-catenin were used to define a gene signature that prognosticates breast cancer patient survival and response to chemotherapy.

Conclusions: The RON-DEK-β-catenin axis regulates the numerous metabolic pathways with significant associations to breast cancer patient outcomes.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Breast Neoplasms* / pathology
  • Cell Line, Tumor
  • Chromosomal Proteins, Non-Histone / genetics
  • Female
  • Humans
  • Lactates
  • Metabolic Networks and Pathways
  • Neoplasm Recurrence, Local
  • Oncogene Proteins / genetics
  • Poly-ADP-Ribose Binding Proteins / metabolism
  • beta Catenin / genetics
  • beta Catenin / metabolism

Substances

  • beta Catenin
  • Chromosomal Proteins, Non-Histone
  • DEK protein, human
  • Lactates
  • Oncogene Proteins
  • Poly-ADP-Ribose Binding Proteins