SQSTM1/p62-Directed Metabolic Reprogramming Is Essential for Normal Neurodifferentiation

Stem Cell Reports. 2019 Apr 9;12(4):696-711. doi: 10.1016/j.stemcr.2019.01.023. Epub 2019 Feb 28.

Abstract

Neurodegenerative disorders are an increasingly common and irreversible burden on society, often affecting the aging population, but their etiology and disease mechanisms are poorly understood. Studying monogenic neurodegenerative diseases with known genetic cause provides an opportunity to understand cellular mechanisms also affected in more complex disorders. We recently reported that loss-of-function mutations in the autophagy adaptor protein SQSTM1/p62 lead to a slowly progressive neurodegenerative disease presenting in childhood. To further elucidate the neuronal involvement, we studied the cellular consequences of loss of p62 in a neuroepithelial stem cell (NESC) model and differentiated neurons derived from reprogrammed p62 patient cells or by CRISPR/Cas9-directed gene editing in NESCs. Transcriptomic and proteomic analyses suggest that p62 is essential for neuronal differentiation by controlling the metabolic shift from aerobic glycolysis to oxidative phosphorylation required for neuronal maturation. This shift is blocked by the failure to sufficiently downregulate lactate dehydrogenase expression due to the loss of p62, possibly through impaired Hif-1α downregulation and increased sensitivity to oxidative stress. The findings imply an important role for p62 in neuronal energy metabolism and particularly in the regulation of the shift between glycolysis and oxidative phosphorylation required for normal neurodifferentiation.

Keywords: SQSTM1; hypoxia; mitochondria; mitophagy; neurodegeneration; neurodifferentiation; neuroepithelial-like stem cells; neuronal development; oxidative stress; p62.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Differentiation / genetics*
  • Cellular Reprogramming / genetics*
  • Energy Metabolism / genetics*
  • Gene Expression Profiling
  • Glycolysis
  • Humans
  • Mitophagy
  • Models, Biological
  • Neurodegenerative Diseases / etiology
  • Neurodegenerative Diseases / metabolism
  • Neurodegenerative Diseases / pathology
  • Neurons / cytology
  • Neurons / metabolism
  • Oxidative Phosphorylation
  • Oxidative Stress
  • Oxygen / metabolism
  • Sequestosome-1 Protein / genetics*
  • Sequestosome-1 Protein / metabolism

Substances

  • SQSTM1 protein, human
  • Sequestosome-1 Protein
  • Oxygen