S-sulfocysteine/NMDA receptor-dependent signaling underlies neurodegeneration in molybdenum cofactor deficiency

J Clin Invest. 2017 Dec 1;127(12):4365-4378. doi: 10.1172/JCI89885. Epub 2017 Nov 6.

Abstract

Molybdenum cofactor deficiency (MoCD) is an autosomal recessive inborn error of metabolism characterized by neurodegeneration and death in early childhood. The rapid and progressive neurodegeneration in MoCD presents a major clinical challenge and may relate to the poor understanding of the molecular mechanisms involved. Recently, we reported that treating patients with cyclic pyranopterin monophosphate (cPMP) is a successful therapy for a subset of infants with MoCD and prevents irreversible brain damage. Here, we studied S-sulfocysteine (SSC), a structural analog of glutamate that accumulates in the plasma and urine of patients with MoCD, and demonstrated that it acts as an N-methyl D-aspartate receptor (NMDA-R) agonist, leading to calcium influx and downstream cell signaling events and neurotoxicity. SSC treatment activated the protease calpain, and calpain-dependent degradation of the inhibitory synaptic protein gephyrin subsequently exacerbated SSC-mediated excitotoxicity and promoted loss of GABAergic synapses. Pharmacological blockade of NMDA-R, calcium influx, or calpain activity abolished SSC and glutamate neurotoxicity in primary murine neurons. Finally, the NMDA-R antagonist memantine was protective against the manifestation of symptoms in a tungstate-induced MoCD mouse model. These findings demonstrate that SSC drives excitotoxic neurodegeneration in MoCD and introduce NMDA-R antagonists as potential therapeutics for this fatal disease.

Keywords: Neurodegeneration; Neuroscience.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium Signaling*
  • Cysteine / analogs & derivatives*
  • Cysteine / metabolism
  • Disease Models, Animal
  • GABAergic Neurons / metabolism*
  • GABAergic Neurons / pathology
  • HEK293 Cells
  • Humans
  • Memantine / pharmacology
  • Metal Metabolism, Inborn Errors / drug therapy
  • Metal Metabolism, Inborn Errors / metabolism*
  • Metal Metabolism, Inborn Errors / pathology
  • Mice
  • Neurodegenerative Diseases / drug therapy
  • Neurodegenerative Diseases / genetics
  • Neurodegenerative Diseases / metabolism*
  • Neurodegenerative Diseases / pathology
  • Organophosphorus Compounds / pharmacology
  • Pterins / pharmacology
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Synapses / metabolism
  • Synapses / pathology
  • Tungsten Compounds / toxicity

Substances

  • Organophosphorus Compounds
  • Pterins
  • Receptors, N-Methyl-D-Aspartate
  • Tungsten Compounds
  • nulibry
  • S-sulphocysteine
  • Cysteine
  • tungstate
  • Memantine

Supplementary concepts

  • Molybdenum cofactor deficiency

Grants and funding

Funding period 2011-2013