Granulocyte-colony stimulating factor activates JAK2/PI3K/PDE3B pathway to inhibit corticosterone synthesis in a neonatal hypoxic-ischemic brain injury rat model

Exp Neurol. 2015 Oct:272:152-9. doi: 10.1016/j.expneurol.2015.03.019. Epub 2015 Mar 25.

Abstract

Objective: Our previous study demonstrated that granulocyte-colony stimulating factor (G-CSF)-induced neuroprotection is accompanied by an inhibition of corticosterone production in a neonatal hypoxic-ischemic (HI) rat model. The present study investigates how G-CSF inhibits corticosterone production, using adrenal cortical cells and HI rat pups.

Methods: Cholera toxin was used to induce corticosterone synthesis in a rodent Y1 adrenal cortical cell line by increasing cyclic adenosine monophosphate (cAMP). Both corticosterone and cAMP were quantitatively measured using a commercial enzyme-linked immunosorbent assay (ELISA). The downstream signaling components of the G-CSF receptor, including Janus Kinase 2 (JAK2)/Phosphatidylinositol-3-kinase (PI3K)/Protein kinase B (Akt) and Phosphodiesterase 3B (PDE3B), were detected by western blot. Sprague-Dawley rat pups at the age of 10days (P10) were subjected to unilateral carotid artery ligation followed by hypoxia for 2.5hours. Brain infarction volumes were determined using 2,3,5-triphenyltetrazolium chloride monohydrate (TTC) staining.

Results: G-CSF at 30ng/ml inhibited corticosterone synthesis but lost its inhibitory effect at higher doses. The inhibitory effect of G-CSF was conferred by interfering with cAMP signaling via the activation of the JAK2/PI3K/PDE3B signaling pathway. The degradation of cAMP by G-CSF signaling reduced corticosterone production. This mechanism was further verified in the neonatal HI brain injury rat model, in which inhibition of PDE3B reversed the protective effects of G-CSF.

Conclusion: Our data suggest that the neuroprotective G-CSF reduces corticosterone synthesis at the adrenal level by degrading intracellular cAMP via activation of the JAK2/PI3K/PDE3B pathway.

Keywords: Adrenal cortical cells; Cholera toxin; Corticosterone; Granulocyte colony stimulating factor; Hypothalamic-pituitary-adrenal axis; Hypoxia-ischemia; JAK2; PDE; Y1.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Body Weight / drug effects
  • Brain Infarction / drug therapy
  • Brain Infarction / etiology
  • Cell Line
  • Cell Survival / drug effects
  • Cholera Toxin / toxicity
  • Corticosterone / metabolism*
  • Cyclic AMP / metabolism
  • Cyclic Nucleotide Phosphodiesterases, Type 3 / metabolism
  • Disease Models, Animal
  • Enzyme Activation / drug effects
  • Enzyme Inhibitors / pharmacology
  • Enzyme Inhibitors / therapeutic use
  • Granulocyte Colony-Stimulating Factor / pharmacology*
  • Granulocyte Colony-Stimulating Factor / therapeutic use
  • Hypoxia-Ischemia, Brain / drug therapy
  • Hypoxia-Ischemia, Brain / metabolism*
  • Janus Kinase 2 / metabolism*
  • Nerve Degeneration / chemically induced
  • Nerve Degeneration / drug therapy
  • Nerve Degeneration / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / drug effects*

Substances

  • Enzyme Inhibitors
  • Granulocyte Colony-Stimulating Factor
  • Cholera Toxin
  • Cyclic AMP
  • Phosphatidylinositol 3-Kinases
  • Jak2 protein, rat
  • Janus Kinase 2
  • Cyclic Nucleotide Phosphodiesterases, Type 3
  • Pde3b protein, rat
  • Corticosterone