Transcriptional suppression of AMPKα1 promotes breast cancer metastasis upon oncogene activation

Proc Natl Acad Sci U S A. 2020 Apr 7;117(14):8013-8021. doi: 10.1073/pnas.1914786117. Epub 2020 Mar 19.

Abstract

AMP-activated protein kinase (AMPK) functions as an energy sensor and is pivotal in maintaining cellular metabolic homeostasis. Numerous studies have shown that down-regulation of AMPK kinase activity or protein stability not only lead to abnormality of metabolism but also contribute to tumor development. However, whether transcription regulation of AMPK plays a critical role in cancer metastasis remains unknown. In this study, we demonstrate that AMPKα1 expression is down-regulated in advanced human breast cancer and is associated with poor clinical outcomes. Transcription of AMPKα1 is inhibited on activation of PI3K and HER2 through ΔNp63α. Ablation of AMPKα1 expression or inhibition of AMPK kinase activity leads to disruption of E-cadherin-mediated cell-cell adhesion in vitro and increased tumor metastasis in vivo. Furthermore, restoration of AMPKα1 expression significantly rescues PI3K/HER2-induced disruption of cell-cell adhesion, cell invasion, and cancer metastasis. Together, these results demonstrate that the transcription control is another layer of AMPK regulation and suggest a critical role for AMPK in regulating cell-cell adhesion and cancer metastasis.

Keywords: AMPK; cancer metastasis; cell adhesion; oncogenic signaling; ΔNp63α.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / antagonists & inhibitors
  • AMP-Activated Protein Kinases / genetics*
  • Animals
  • Breast / pathology
  • Breast Neoplasms / genetics*
  • Breast Neoplasms / mortality
  • Breast Neoplasms / pathology
  • Cell Adhesion / drug effects
  • Cell Adhesion / genetics
  • Cell Line, Tumor
  • Chromones / pharmacology
  • Disease-Free Survival
  • Down-Regulation
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Gene Knockdown Techniques
  • Humans
  • Lapatinib / pharmacology
  • Mice
  • Morpholines / pharmacology
  • Neoplasm Staging
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors / pharmacology
  • Prognosis
  • Receptor, ErbB-2 / antagonists & inhibitors
  • Receptor, ErbB-2 / metabolism
  • Tissue Array Analysis
  • Transcription Factors / metabolism*
  • Transcription, Genetic / drug effects
  • Transcriptional Activation
  • Tumor Suppressor Proteins / metabolism*
  • Xenograft Model Antitumor Assays

Substances

  • Chromones
  • Morpholines
  • Phosphoinositide-3 Kinase Inhibitors
  • TP63 protein, human
  • Transcription Factors
  • Tumor Suppressor Proteins
  • Lapatinib
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • ERBB2 protein, human
  • Receptor, ErbB-2
  • AMP-Activated Protein Kinases
  • PRKAA1 protein, human