Cholecystokinin octapeptide improves hippocampal glutamatergic synaptogenesis and postoperative cognition by inhibiting induction of A1 reactive astrocytes in aged mice

CNS Neurosci Ther. 2021 Nov;27(11):1374-1384. doi: 10.1111/cns.13718. Epub 2021 Aug 17.

Abstract

Aims: Delayed neurocognitive recovery (dNCR) is a common postoperative complication in geriatric surgical patients for which there is no efficacious therapy. Cholecystokinin octapeptide (CCK-8), an immunomodulatory peptide, regulates memory and learning. Here, we explored the effects and mechanism of action of CCK-8 on dNCR.

Methods: We applied laparotomy to establish a model of dNCR in aged mice. Morris water maze and fear conditioning tests were used to evaluate cognition. Immunofluorescence was used to detect the density of CCK-8, A1 reactive astrocytes, glutamatergic synapses, and activation of microglia in the hippocampus. Quantitative PCR was performed to determine mRNA levels of synapse-associated factors. A1 reactive astrocytes, activated microglia, and glutamatergic synapse-associated protein levels in the hippocampus were assessed by western blotting.

Results: Administration of CCK-8 suppressed the activation of microglia, the induction of A1 reactive astrocytes, and the expression of tumor necrosis factor alpha, complement 1q, and interleukin 1 alpha in the hippocampus. Furthermore, it promoted glutamatergic synaptogenesis and neurocognitive recovery in aged dNCR model mice.

Conclusion: Our findings indicated that CCK-8 alleviated cognitive impairment and promoted glutamatergic synaptogenesis by inhibiting the induction of A1 reactive astrocytes and the activation of microglia. CCK-8 is, therefore, a potential therapeutic target for dNCR.

Keywords: A1 reactive astrocyte; activated microglia; cholecystokinin octapeptide; delayed neurocognitive recovery; glutamatergic synaptogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / drug effects
  • Cognitive Dysfunction / drug therapy*
  • Cognitive Dysfunction / etiology
  • Cognitive Dysfunction / psychology*
  • Complement C1q / metabolism
  • Fear / psychology
  • Female
  • Glutamates / physiology*
  • Interleukin-1 / metabolism
  • Laparotomy
  • Macrophage Activation
  • Maze Learning
  • Mice
  • Mice, Inbred C57BL
  • Neurogenesis / drug effects*
  • Postoperative Complications / prevention & control*
  • Postoperative Complications / psychology*
  • Sincalide / therapeutic use*
  • Synapses
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Glutamates
  • Interleukin-1
  • Tumor Necrosis Factor-alpha
  • Complement C1q
  • Sincalide