Autonomous requirements of the Menkes disease protein in the nervous system

Am J Physiol Cell Physiol. 2015 Nov 15;309(10):C660-8. doi: 10.1152/ajpcell.00130.2015. Epub 2015 Aug 12.

Abstract

Menkes disease is a fatal neurodegenerative disorder arising from a systemic copper deficiency caused by loss-of-function mutations in a ubiquitously expressed copper transporter, ATP7A. Although this disorder reveals an essential role for copper in the developing human nervous system, the role of ATP7A in the pathogenesis of signs and symptoms in affected patients, including severe mental retardation, ataxia, and excitotoxic seizures, remains unknown. To directly examine the role of ATP7A within the central nervous system, we generated Atp7a(Nes) mice, in which the Atp7a gene was specifically deleted within neural and glial cell precursors without impairing systemic copper homeostasis, and compared these mice with the mottled brindle (mo-br) mutant, a murine model of Menkes disease in which Atp7a is defective in all cells. Whereas mo-br mice displayed neurodegeneration, demyelination, and 100% mortality prior to weaning, the Atp7a(Nes) mice showed none of these phenotypes, exhibiting only mild sensorimotor deficits, increased anxiety, and susceptibility to NMDA-induced seizure. Our results indicate that the pathophysiology of severe neurological signs and symptoms in Menkes disease is the result of copper deficiency within the central nervous system secondary to impaired systemic copper homeostasis and does not arise from an intrinsic lack of ATP7A within the developing brain. Furthermore, the sensorimotor deficits, hypophagia, anxiety, and sensitivity to NMDA-induced seizure in the Atp7a(Nes) mice reveal unique autonomous requirements for ATP7A in the nervous system. Taken together, these data reveal essential roles for copper acquisition in the central nervous system in early development and suggest novel therapeutic approaches in affected patients.

Keywords: Menkes disease; copper; nervous system; nutrition; transporter.

Publication types

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

MeSH terms

  • Adenosine Triphosphatases / genetics
  • Adenosine Triphosphatases / metabolism*
  • Animals
  • Cation Transport Proteins / genetics
  • Cation Transport Proteins / metabolism*
  • Copper / metabolism*
  • Copper-Transporting ATPases
  • Female
  • Gene Expression Regulation / physiology
  • Integrases
  • Male
  • Menkes Kinky Hair Syndrome / genetics
  • Menkes Kinky Hair Syndrome / metabolism*
  • Menkes Kinky Hair Syndrome / pathology
  • Mice
  • Mice, Knockout
  • Mutation

Substances

  • Atp7a protein, mouse
  • Cation Transport Proteins
  • Copper
  • Cre recombinase
  • Integrases
  • Adenosine Triphosphatases
  • Copper-Transporting ATPases