Protein S protects neurons from excitotoxic injury by activating the TAM receptor Tyro3-phosphatidylinositol 3-kinase-Akt pathway through its sex hormone-binding globulin-like region

J Neurosci. 2010 Nov 17;30(46):15521-34. doi: 10.1523/JNEUROSCI.4437-10.2010.

Abstract

The anticoagulant factor protein S (PS) protects neurons from hypoxic/ischemic injury. However, molecular mechanisms mediating PS protection in injured neurons remain unknown. Here, we show mouse recombinant PS protects dose-dependently mouse cortical neurons from excitotoxic NMDA-mediated neuritic bead formation and apoptosis by activating the phosphatidylinositol 3-kinase (PI3K)-Akt pathway (EC(50) = 26 ± 4 nm). PS stimulated phosphorylation of Bad and Mdm2, two downstream targets of Akt, which in neurons subjected to pathological overstimulation of NMDA receptors (NMDARs) increased the antiapoptotic Bcl-2 and Bcl-X(L) levels and reduced the proapoptotic p53 and Bax levels. Adenoviral transduction with a kinase-deficient Akt mutant (Ad.Akt(K179A)) resulted in loss of PS-mediated neuronal protection, Akt activation, and Bad and Mdm2 phosphorylation. Using the TAM receptors tyrosine kinases Tyro3-, Axl-, and Mer-deficient neurons, we showed that PS protected neurons lacking Axl and Mer, but not Tyro3, suggesting a requirement of Tyro3 for PS-mediated protection. Consistent with these results, PS dose-dependently phosphorylated Tyro3 on neurons (EC(50) = 25 ± 3 nm). In an in vivo model of NMDA-induced excitotoxic lesions in the striatum, PS dose-dependently reduced the lesion volume in control mice (EC(50) = 22 ± 2 nm) and protected Axl(-/-) and Mer(-/-) transgenic mice, but not Tyro3(-/-) transgenic mice. Using different structural PS analogs, we demonstrated that the C terminus sex hormone-binding globulin-like (SHBG) domain of PS is critical for neuronal protection in vitro and in vivo. Thus, our data show that PS protects neurons by activating the Tyro3-PI3K-Akt pathway via its SHGB domain, suggesting potentially a novel neuroprotective approach for acute brain injury and chronic neurodegenerative disorders associated with excessive activation of NMDARs.

Publication types

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

MeSH terms

  • Animals
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Excitatory Amino Acid Agonists / toxicity
  • Gene Knockdown Techniques
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neurons / drug effects
  • Neurons / metabolism*
  • Neurons / pathology
  • Neuroprotective Agents / pharmacology
  • Phosphatidylinositol 3-Kinase / metabolism*
  • Protein S / physiology*
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Proto-Oncogene Proteins c-akt / physiology
  • Receptor Protein-Tyrosine Kinases / metabolism*
  • Sex Hormone-Binding Globulin / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology

Substances

  • Excitatory Amino Acid Agonists
  • Neuroprotective Agents
  • Protein S
  • Sex Hormone-Binding Globulin
  • Phosphatidylinositol 3-Kinase
  • Receptor Protein-Tyrosine Kinases
  • Tyro3 protein, mouse
  • Proto-Oncogene Proteins c-akt