Neonatal hypoxia-ischemia differentially upregulates MAGUKs and associated proteins in PSD-93-deficient mouse brain

Stroke. 2003 Dec;34(12):2958-63. doi: 10.1161/01.STR.0000102560.78524.9D. Epub 2003 Nov 6.

Abstract

Background and purpose: Postsynaptic density (PSD)-93 and PSD-95 are the major membrane-associated guanylate kinases (MAGUKs) at excitatory synapses of the brain linking the N-methyl-d-aspartate receptor (NMDAR) with neuronal nitric oxide synthase (nNOS), which contributes to cell death after neonatal hypoxia-ischemia (HI). We investigated whether deletion of PSD-93 would dissociate the NMDAR from nNOS and be neuroprotective.

Methods: Postnatal day 7 wild-type (+/+), heterozygous (+/-), and homozygous (-/-) PSD-93 knockout mice were subjected to HI by permanent ligation of the right carotid artery, followed by exposure to 8% O2/92% N2 for 1 hour. Brains were scored 5 days later for damage with cresyl violet and iron stains. Western blot and coimmunoprecipitation were used to determine the expression and association of the major PSD proteins.

Results: There was no significant difference between PSD-93 (-/-) and (+/+) mice in mortality or degree of brain injury. In the absence of PSD-93, PSD-95 still interacted with NR2B and nNOS. Under physiological conditions, PSD-95, nNOS, NR2A, and NR2B were unaltered in the (-/-) pups. However, at 24 hours after HI, protein expression of PSD-95, nNOS, and NR2A but not NR2B was markedly higher in the (-/-) than in the (+/+) pups. In (+/+) pups, HI resulted in decreased expression of NR2A but not NR2B in cortex and decreased NR2A and NR2B expression in hippocampus, but this reduction was not observed in (-/-) pups.

Conclusions: PSD-93 is not essential for baseline synaptic function but may participate in regulation of NMDAR-associated signaling pathways after HI injury. Deletion of PSD-93 alone does not provide neuroprotection after neonatal HI, possibly a result, in part, of upregulation of PSD-95. MAGUKs may substitute for one another, allowing normal NMDAR function in the postnatal period.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Animals, Newborn
  • Blotting, Western
  • Brain / metabolism*
  • Brain / pathology
  • Discs Large Homolog 1 Protein
  • Disks Large Homolog 4 Protein
  • Guanylate Kinases
  • Heterozygote
  • Homozygote
  • Hypoxia-Ischemia, Brain / metabolism*
  • Hypoxia-Ischemia, Brain / pathology
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nerve Tissue Proteins / biosynthesis
  • Nerve Tissue Proteins / deficiency*
  • Nerve Tissue Proteins / metabolism
  • Neuropeptides / biosynthesis
  • Nitric Oxide Synthase / metabolism
  • Nitric Oxide Synthase Type I
  • Nucleoside-Phosphate Kinase / metabolism*
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Severity of Illness Index
  • Survival Rate
  • Up-Regulation*

Substances

  • Adaptor Proteins, Signal Transducing
  • Discs Large Homolog 1 Protein
  • Disks Large Homolog 4 Protein
  • Dlg1 protein, mouse
  • Dlg4 protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • NR2A NMDA receptor
  • NR2B NMDA receptor
  • Nerve Tissue Proteins
  • Neuropeptides
  • Receptors, N-Methyl-D-Aspartate
  • postsynaptic density proteins
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type I
  • Nos1 protein, mouse
  • Nucleoside-Phosphate Kinase
  • Dlg2 protein, mouse
  • Dlgh3 protein, mouse
  • Guanylate Kinases