Metabolomic Analysis Reveals Increased Aerobic Glycolysis and Amino Acid Deficit in a Cellular Model of Amyotrophic Lateral Sclerosis

Mol Neurobiol. 2016 May;53(4):2222-40. doi: 10.1007/s12035-015-9165-7. Epub 2015 May 12.

Abstract

Defects in energy metabolism are potential pathogenic mechanisms in amyotrophic lateral sclerosis (ALS), a rapidly fatal disease with no cure. The mechanisms through which this occurs remain elusive and their understanding may prove therapeutically useful. We used metabolomics and stable isotope tracers to examine metabolic changes in a well-characterized cell model of familial ALS, the motor neuronal NSC-34 line stably expressing human wild-type Cu/Zn superoxide dismutase (wtSOD1) or mutant G93A (G93ASOD1). Our findings indicate that wt and G93ASOD1 expression both enhanced glucose metabolism under serum deprivation. However, in wtSOD1 cells, this phenotype increased supply of amino acids for protein and glutathione synthesis, while in G93ASOD1 cells it was associated with death, aerobic glycolysis, and a broad dysregulation of amino acid homeostasis. Aerobic glycolysis was mainly due to induction of pyruvate dehydrogenase kinase 1. Our study thus provides novel insight into the role of deranged energy metabolism as a cause of poor adaptation to stress and a promoter of neural cell damage in the presence of mutant SOD1. Furthermore, the metabolic alterations we report may help explain why mitochondrial dysfunction and impairment of the endoplasmic reticulum stress response are frequently seen in ALS.

Keywords: Amino acids; Amyotrophic lateral sclerosis; Cu/Zn superoxide dismutase; Glutamate; Glutamine; Glycolysis; Motor neuron; NSC-34; Pyruvate dehydrogenase kinase 1; Serine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aerobiosis
  • Alanine / metabolism
  • Amino Acids / deficiency*
  • Amyotrophic Lateral Sclerosis / metabolism*
  • Animals
  • Caspase 3 / metabolism
  • Caspase 7 / metabolism
  • Cell Death
  • Cell Line
  • Culture Media, Serum-Free
  • Glucose / metabolism
  • Glutamine / metabolism
  • Glycolysis*
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Lactates / metabolism
  • Metabolome
  • Metabolomics / methods*
  • Mice
  • Models, Biological*
  • Mutant Proteins / metabolism
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / metabolism
  • Protein Serine-Threonine Kinases / metabolism
  • Pyruvate Dehydrogenase Acetyl-Transferring Kinase
  • Pyruvic Acid / metabolism
  • Superoxide Dismutase / genetics

Substances

  • Amino Acids
  • Culture Media, Serum-Free
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Lactates
  • Mutant Proteins
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Pyruvate Dehydrogenase Acetyl-Transferring Kinase
  • Glutamine
  • Pyruvic Acid
  • Superoxide Dismutase
  • Protein Serine-Threonine Kinases
  • Caspase 3
  • Caspase 7
  • Glucose
  • Alanine