The role of serum/glucocorticoid-regulated kinase 1 in brain function following cerebral ischemia

J Cereb Blood Flow Metab. 2024 Jul;44(7):1145-1162. doi: 10.1177/0271678X231224508. Epub 2024 Jan 18.

Abstract

Cardiopulmonary arrest (CA) is a major cause of death/disability in the U.S. with poor prognosis and survival rates. Current therapeutic challenges are physiologically complex because they involve hypoperfusion (decreased cerebral blood flow), neuroinflammation, and mitochondrial dysfunction. We previously discovered novel serum/glucocorticoid-regulated kinase 1 (SGK1) is highly expressed in brain of neurons that are susceptible to ischemia (hippocampus and cortex). We inhibited SGK1 and utilized pharmacological (specific inhibitor, GSK650394) and neuron-specific genetic approaches (shRNA) in rodent models of CA to determine if SGK1 is responsible for hypoperfusion, neuroinflammation, mitochondrial dysfunctional, and neurological deficits after CA. Inhibition of SGK1 alleviated cortical hypoperfusion and neuroinflammation (via Iba1, GFAP, and cytokine array). Treatment with GSK650394 enhanced mitochondrial function (via Seahorse respirometry) in the hippocampus 3 and 7 days after CA. Neuronal injury (via MAP2, dMBP, and Golgi staining) in the hippocampus and cortex was observed 7 days after CA but ameliorated with SGK1-shRNA. Moreover, SGK1 mediated neuronal injury by regulating the Ndrg1-SOX10 axis. Finally, animals subjected to CA exhibited learning/memory, motor, and anxiety deficits after CA, whereas SGK1 inhibition via SGK1-shRNA improved neurocognitive function. The present study suggests the fundamental roles of SGK1 in brain circulation and neuronal survival/death in cerebral ischemia-related diseases.

Keywords: Serum/glucocorticoid-regulated kinase; cerebral ischemia; mitochondrial dysfunction; neuroinflammation; neurological deficits.

MeSH terms

  • Animals
  • Benzoates
  • Brain / metabolism
  • Brain Ischemia* / metabolism
  • Bridged Bicyclo Compounds, Heterocyclic
  • Cerebrovascular Circulation / drug effects
  • Cerebrovascular Circulation / physiology
  • Disease Models, Animal
  • Heart Arrest / complications
  • Hippocampus / metabolism
  • Immediate-Early Proteins* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / metabolism
  • Neurons / metabolism
  • Protein Serine-Threonine Kinases* / antagonists & inhibitors
  • Protein Serine-Threonine Kinases* / genetics
  • Protein Serine-Threonine Kinases* / metabolism
  • Rats

Substances

  • serum-glucocorticoid regulated kinase
  • Immediate-Early Proteins
  • Protein Serine-Threonine Kinases
  • 2-cyclopentyl-4-(5-phenyl-1H-pyrrolo(2,3-b)pyridin-3-yl)-benzoic acid
  • Benzoates
  • Bridged Bicyclo Compounds, Heterocyclic