JMJD5 regulates PKM2 nuclear translocation and reprograms HIF-1α-mediated glucose metabolism

Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):279-84. doi: 10.1073/pnas.1311249111. Epub 2013 Dec 16.

Abstract

JMJD5, a Jumonji C domain-containing dioxygenase, is important for embryonic development and cancer growth. Here, we show that JMJD5 is up-regulated by hypoxia and is crucial for hypoxia-induced cell proliferation. JMJD5 interacts directly with pyruvate kinase muscle isozyme (PKM)2 to modulate metabolic flux in cancer cells. The JMJD5-PKM2 interaction resides at the intersubunit interface region of PKM2, which hinders PKM2 tetramerization and blocks pyruvate kinase activity. This interaction also influences translocation of PKM2 into the nucleus and promotes hypoxia-inducible factor (HIF)-1α-mediated transactivation. JMJD5 knockdown inhibits the transcription of the PKM2-HIF-1α target genes involved in glucose metabolism, resulting in a reduction of glucose uptake and lactate secretion in cancer cells. JMJD5, along with PKM2 and HIF-1α, is recruited to the hypoxia response element site in the lactate dehydrogenase A and PKM2 loci and mediates the recruitment of the latter two proteins. Our data uncover a mechanism whereby PKM2 can be regulated by factor-binding-induced homo/heterooligomeric restructuring, paving the way to cell metabolic reprogram.

Keywords: Warburg effect; aerobic glycolysis; breast cancer; cancer metabolism.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Allosteric Site
  • Breast Neoplasms / metabolism
  • Carrier Proteins / metabolism*
  • Cell Line, Tumor
  • Cell Nucleus / metabolism
  • Cell Proliferation
  • Female
  • Gene Expression Regulation, Neoplastic*
  • Glucose / metabolism*
  • Glycolysis
  • HEK293 Cells
  • HeLa Cells
  • Histone Demethylases / metabolism*
  • Humans
  • Hypoxia
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Isoenzymes / metabolism
  • L-Lactate Dehydrogenase / metabolism
  • Lactate Dehydrogenase 5
  • Lactic Acid / metabolism
  • MCF-7 Cells
  • Membrane Proteins / metabolism*
  • Neoplasms / metabolism
  • Protein Binding
  • Protein Structure, Quaternary
  • Thyroid Hormone-Binding Proteins
  • Thyroid Hormones / metabolism*
  • Transcriptional Activation

Substances

  • Carrier Proteins
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Isoenzymes
  • Membrane Proteins
  • Thyroid Hormones
  • Lactic Acid
  • L-Lactate Dehydrogenase
  • Lactate Dehydrogenase 5
  • Histone Demethylases
  • KDM8 protein, human
  • Glucose