A feedback circuit comprising EHD1 and 14-3-3ζ sustains β-catenin/c-Myc-mediated aerobic glycolysis and proliferation in non-small cell lung cancer

Cancer Lett. 2021 Nov 1:520:12-25. doi: 10.1016/j.canlet.2021.06.023. Epub 2021 Jul 2.

Abstract

Mammalian Eps15 homology domain 1 (EHD1) participates in the development of non-small cell lung cancer (NSCLC). However, its role in mediating aerobic glycolysis remains unclear. Herein, microarray analysis revealed that EHD1 expression was significantly correlated with the glycolysis/gluconeogenesis pathway. Clinically, EHD1 expression was positively correlated with the maximum standard uptake value (SUVmax) in 18F-FDG PET/CT scans. Additionally, EHD1 knockdown inhibited aerobic glycolysis and proliferation in vitro and in vivo. Furthermore, Wnt/β-catenin signaling was identified as a critical EHD1-regulated pathway. Co-IP, native gel electrophoresis, and immunoblotting showed that EHD1 contributed to 14-3-3 dimerization via 14-3-3ζ and subsequent activation of β-catenin/c-Myc signaling. Analysis of the EHD1 regulatory region via ENCODE revealed the potential for c-Myc recruitment, leading to transcriptional activation of EHD1 and formation of an EHD1/14-3-3ζ/β-catenin/c-Myc positive feedback circuit. Notably, blocking this circuit with a Wnt/β-catenin inhibitor dramatically inhibited tumor growth in vivo. The positive correlations among EHD1, 14-3-3ζ, c-Myc, and LDHA were further confirmed in NSCLC tissues. Collectively, our study demonstrated that EHD1 activates a 14-3-3ζ/β-catenin/c-Myc regulatory circuit that synergistically promotes aerobic glycolysis and may constitute a promising therapeutic target for NSCLC.

Keywords: EHD1; Metabolic reprogramming; Positive feedback loop; Tumor proliferation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 14-3-3 Proteins / genetics*
  • A549 Cells
  • Animals
  • Carcinoma, Non-Small-Cell Lung / diagnostic imaging
  • Carcinoma, Non-Small-Cell Lung / genetics*
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Cell Movement / genetics
  • Cell Proliferation / genetics
  • Female
  • Gene Expression Regulation, Neoplastic / genetics
  • Heterografts
  • Humans
  • L-Lactate Dehydrogenase / genetics*
  • Male
  • Mice
  • Positron Emission Tomography Computed Tomography
  • Proto-Oncogene Proteins c-myc / genetics
  • Vesicular Transport Proteins / genetics*
  • Vesicular Transport Proteins / ultrastructure
  • Warburg Effect, Oncologic
  • Wnt Signaling Pathway / genetics
  • beta Catenin / genetics*

Substances

  • 14-3-3 Proteins
  • CTNNB1 protein, human
  • EHD1 protein, human
  • MYC protein, human
  • Proto-Oncogene Proteins c-myc
  • Vesicular Transport Proteins
  • YWHAZ protein, human
  • beta Catenin
  • L-Lactate Dehydrogenase
  • LDHA protein, human