SIK2 promotes reprogramming of glucose metabolism through PI3K/AKT/HIF-1α pathway and Drp1-mediated mitochondrial fission in ovarian cancer

Cancer Lett. 2020 Jan 28:469:89-101. doi: 10.1016/j.canlet.2019.10.029. Epub 2019 Oct 19.

Abstract

Salt-inducible kinase 2 (SIK2), which belongs to the AMP-activated protein kinase family, modulates various biological functions including fatty acid oxidation. However, the role of SIK2 in glucose metabolism reprogramming remains unclear in ovarian cancer (OC) cells. Here, we found that SIK2 significantly enhanced the Warburg effect of OC cells mainly through two mechanisms. On the one hand, SIK2 upregulated the expression of HIF-1α by activating the PI3K/AKT signaling pathway, which directly upregulated the transcription of major glycolytic genes to promote glycolysis. On the other hand, SIK2 promoted mitochondrial fission through phosphorylation of Drp1 at Ser616 site, which inhibited the mitochondrial oxidative phosphorylation. In addition, SIK2 promoted growth and metastasis of OC cells by promoting cell proliferation and inhibiting cell apoptosis, as well as enhancing the epithelial-mesenchymal transition. Moreover, the SIK2-mediated reprogramming of glucose metabolism played a critical role in growth and metastasis of OC cells. Collectively, our findings demonstrate that SIK2 is a crucial regulator of glucose metabolism in OC cells through activation of PI3K/AKT/HIF-1α pathway and Drp1 phosphorylation-mediated mitochondrial fission, which plays a critical oncogenic role in OC cells.

Keywords: Glycolysis; Mitochondrial dynamics; Oxidative phosphorylation; Salt-inducible kinase 2.

Publication types

  • Observational Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Cell Transformation, Neoplastic / genetics
  • Cell Transformation, Neoplastic / pathology
  • Dynamins / metabolism*
  • Epithelial-Mesenchymal Transition / genetics
  • Female
  • Follow-Up Studies
  • Gene Expression Regulation, Neoplastic
  • Gene Knockdown Techniques
  • Glucose / metabolism
  • Glycolysis / genetics*
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Kaplan-Meier Estimate
  • Mice
  • Mitochondrial Dynamics / genetics*
  • Ovarian Neoplasms / genetics
  • Ovarian Neoplasms / mortality
  • Ovarian Neoplasms / pathology*
  • Ovarian Neoplasms / surgery
  • Ovariectomy
  • Ovary / pathology
  • Ovary / surgery
  • Oxidative Phosphorylation
  • Phosphatidylinositol 3-Kinases / metabolism
  • Prognosis
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Proto-Oncogene Proteins c-akt / metabolism
  • Signal Transduction / genetics
  • Up-Regulation
  • Xenograft Model Antitumor Assays

Substances

  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • salt-inducible kinase-2, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • DNM1L protein, human
  • Dynamins
  • Glucose