EGF promotes PKM2 O-GlcNAcylation by stimulating O-GlcNAc transferase phosphorylation at Y976 and their subsequent association

J Biol Chem. 2022 Sep;298(9):102340. doi: 10.1016/j.jbc.2022.102340. Epub 2022 Aug 3.

Abstract

Epidermal growth factor (EGF) is one of the most well-characterized growth factors and plays a crucial role in cell proliferation and differentiation. Its receptor EGFR has been extensively explored as a therapeutic target against multiple types of cancers, such as lung cancer and glioblastoma. Recent studies have established a connection between deregulated EGF signaling and metabolic reprogramming, especially rewiring in aerobic glycolysis, which is also known as the Warburg effect and recognized as a hallmark in cancer. Pyruvate kinase M2 (PKM2) is a rate-limiting enzyme controlling the final step of glycolysis and serves as a major regulator of the Warburg effect. We previously showed that PKM2 T405/S406 O-GlcNAcylation, a critical mark important for PKM2 detetramerization and activity, was markedly upregulated by EGF. However, the mechanism by which EGF regulates PKM2 O-GlcNAcylation still remains uncharacterized. Here, we demonstrated that EGF promoted O-GlcNAc transferase (OGT) binding to PKM2 by stimulating OGT Y976 phosphorylation. As a consequence, we found PKM2 O-GlcNAcylation and detetramerization were upregulated, leading to a significant decrease in PKM2 activity. Moreover, distinct from PKM2, we observed that the association of additional phosphotyrosine-binding proteins with OGT was also enhanced when Y976 was phosphorylated. These proteins included STAT1, STAT3, STAT5, PKCδ, and p85, which are reported to be O-GlcNAcylated. Together, we show EGF-dependent Y976 phosphorylation is critical for OGT-PKM2 interaction and propose that this posttranslational modification might be important for substrate selection by OGT.

Keywords: O-GlcNAc transferase; O-GlcNAcylation; epidermal growth factor; phosphorylation; phosphotyrosine-binding protein; pyruvate kinase M2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Epidermal Growth Factor* / metabolism
  • ErbB Receptors / genetics
  • ErbB Receptors / metabolism
  • Humans
  • N-Acetylglucosaminyltransferases* / genetics
  • N-Acetylglucosaminyltransferases* / metabolism
  • Neoplasms / metabolism
  • Phosphorylation
  • Phosphotyrosine / metabolism
  • Pyruvate Kinase* / metabolism
  • STAT5 Transcription Factor / metabolism
  • Tyrosine* / metabolism

Substances

  • STAT5 Transcription Factor
  • Phosphotyrosine
  • Tyrosine
  • Epidermal Growth Factor
  • N-Acetylglucosaminyltransferases
  • OGT protein, human
  • Pyruvate Kinase
  • ErbB Receptors