Nuclear Glycogenolysis Modulates Histone Acetylation in Human Non-Small Cell Lung Cancers

Cell Metab. 2019 Nov 5;30(5):903-916.e7. doi: 10.1016/j.cmet.2019.08.014. Epub 2019 Sep 12.

Abstract

Nuclear glycogen was first documented in the early 1940s, but its role in cellular physiology remained elusive. In this study, we utilized pure nuclei preparations and stable isotope tracers to define the origin and metabolic fate of nuclear glycogen. Herein, we describe a key function for nuclear glycogen in epigenetic regulation through compartmentalized pyruvate production and histone acetylation. This pathway is altered in human non-small cell lung cancers, as surgical specimens accumulate glycogen in the nucleus. We demonstrate that the decreased abundance of malin, an E3 ubiquitin ligase, impaired nuclear glycogenolysis by preventing the nuclear translocation of glycogen phosphorylase and causing nuclear glycogen accumulation. Re-introduction of malin in lung cancer cells restored nuclear glycogenolysis, increased histone acetylation, and decreased growth of cancer cells transplanted into mice. This study uncovers a previously unknown role for glycogen metabolism in the nucleus and elucidates another mechanism by which cellular metabolites control epigenetic regulation.

Keywords: E3 ubiquitin ligase; EPM2B; Lafora disease; NHLRC1; glycogen; glycogen phosphorylase; histone acetylation; malin; non-small cell lung cancer; nuclear metabolism.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • A549 Cells
  • Acetylation
  • Animals
  • Carbon / metabolism
  • Carcinoma, Non-Small-Cell Lung / metabolism*
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Cell Nucleus / metabolism*
  • Glycogen / biosynthesis
  • Glycogen Phosphorylase / metabolism
  • Glycogenolysis / genetics*
  • HEK293 Cells
  • Histones / metabolism*
  • Humans
  • Lung Neoplasms / metabolism*
  • Lung Neoplasms / pathology
  • Mice
  • Mice, Knockout
  • Mice, Nude
  • Transfection
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Histones
  • Carbon
  • Glycogen
  • NHLRC1 protein, human
  • NHLRC1 protein, mouse
  • Ubiquitin-Protein Ligases
  • Glycogen Phosphorylase