Traumatic brain injury decreases AMP-activated protein kinase activity and pharmacological enhancement of its activity improves cognitive outcome

J Neurochem. 2016 Oct;139(1):106-19. doi: 10.1111/jnc.13726. Epub 2016 Aug 1.

Abstract

Prolonged metabolic suppression in the brain is a well-characterized secondary pathology of both experimental and clinical traumatic brain injury (TBI). AMP-activated kinase (AMPK) acts as a cellular energy sensor that, when activated, regulates various metabolic and catabolic pathways to decrease ATP consumption and increase ATP synthesis. As energy availability after TBI is suppressed, we questioned if increasing AMPK activity after TBI would improve cognitive outcome. TBI was delivered using the electromagnetic controlled cortical impact model on male Sprague-Dawley rats (275-300 g) and C57BL/6 mice (20-25 g). AMPK activity within the injured parietal cortex and ipsilateral hippocampus was inferred by western blots using phospho-specific antibodies. The consequences of acute manipulation of AMPK signaling on cognitive function were assessed using the Morris water maze task. We found that AMPK activity is decreased as a result of injury, as indicated by reduced AMPK phosphorylation and corresponding changes in the phosphorylation of its downstream targets: ribosomal protein S6 and Akt Substrate of 160 kDa (AS160). Increasing AMPK activity after injury using the drugs 5-amino-1-β-d-ribofuranosyl-imidazole-4-carboxamide or metformin did not affect spatial learning, but significantly improved spatial memory. Taken together, our results suggest that decreased AMPK activity after TBI may contribute to the cellular energy crisis in the injured brain, and that AMPK activators may have therapeutic utility. Increased phosphorylation of Thr172 activates AMP-activated protein kinase (AMPK) under conditions of low cellular energy availability. This leads to inhibition of energy consuming, while activating energy generating, processes. Hill et al., present data to indicate that TBI decreases Thr172 phosphorylation and that its stimulation by pharmacological agents offers neuroprotection and improves memory. These results suggest that decreased AMPK phosphorylation after TBI incorrectly signals the injured brain that excess energy is available, thereby contributing to the cellular energy crisis and memory impairments.

Keywords: glucose metabolism; hippocampus; memory retention; traumatic brain injury.

Publication types

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

MeSH terms

  • AMP-Activated Protein Kinases / drug effects*
  • AMP-Activated Protein Kinases / metabolism*
  • Aminoimidazole Carboxamide / analogs & derivatives
  • Aminoimidazole Carboxamide / pharmacology
  • Animals
  • Brain Injuries, Traumatic / metabolism*
  • Brain Injuries, Traumatic / psychology
  • Enzyme Activators / pharmacology*
  • Hippocampus / pathology
  • Male
  • Maze Learning / drug effects
  • Memory Disorders / etiology
  • Memory Disorders / prevention & control
  • Memory Disorders / psychology
  • Metformin / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Neuroprotective Agents / pharmacology
  • Nootropic Agents / pharmacology*
  • Parietal Lobe / pathology
  • Phosphorylation
  • Psychomotor Performance / drug effects
  • Rats
  • Rats, Sprague-Dawley
  • Ribonucleotides / pharmacology

Substances

  • Enzyme Activators
  • Neuroprotective Agents
  • Nootropic Agents
  • Ribonucleotides
  • Aminoimidazole Carboxamide
  • Metformin
  • AMP-Activated Protein Kinases
  • AICA ribonucleotide