Cannabidiol attenuates seizure susceptibility and behavioural deficits in adult CDKL5R59X knock-in mice

Eur J Neurosci. 2024 Jun;59(12):3337-3352. doi: 10.1111/ejn.16350. Epub 2024 Apr 23.

Abstract

Cyclin-dependent kinase-like 5 (CDKL5) deficiency disorder (CDD) is caused by a loss-of-function mutation in CDKL5 gene, encoding a serine-threonine kinase highly expressed in the brain. CDD manifests with early-onset epilepsy, autism, motor impairment and severe intellectual disability. While there are no known treatments for CDD, the use of cannabidiol has recently been introduced into clinical practice for neurodevelopmental disorders. Given the increased clinical utilization of cannabidiol, we examined its efficacy in the CDKL5R59X knock-in (R59X) mice, a CDD model based on a human mutation that exhibits both lifelong seizure susceptibility and behavioural deficits. We found that cannabidiol pre-treatment rescued the increased seizure susceptibility in response to the chemoconvulsant pentylenetetrazol (PTZ), attenuated working memory and long-term memory impairments, and rescued social deficits in adult R59X mice. To elucidate a potential mechanism, we compared the developmental hippocampal and cortical expression of common endocannabinoid (eCB) targets in R59X mice and their wild-type littermates, including cannabinoid type 1 receptor (CB1R), transient receptor potential vanilloid type 1 (TRPV1) and 2 (TRPV2), G-coupled protein receptor 55 (GPR55) and adenosine receptor 1 (A1R). Many of these eCB targets were developmentally regulated in both R59X and wild-type mice. In addition, adult R59X mice demonstrated significantly decreased expression of CB1R and TRPV1 in the hippocampus, and TRPV2 in the cortex, while TRPV1 was increased in the cortex. These findings support the potential for dysregulation of eCB signalling as a plausible mechanism and therapeutic target in CDD, given the efficacy of cannabidiol to attenuate hyperexcitability and behavioural deficits in this disorder.

Keywords: cannabidiol; cyclin‐dependent kinase‐like 5 deficiency disorder; endocannabinoid system; epilepsy; neurodevelopment.

MeSH terms

  • Animals
  • Behavior, Animal* / drug effects
  • Cannabidiol* / pharmacology
  • Cannabidiol* / therapeutic use
  • Cerebral Cortex / drug effects
  • Cerebral Cortex / metabolism
  • Disease Models, Animal
  • Endocannabinoids / metabolism
  • Epileptic Syndromes* / drug therapy
  • Epileptic Syndromes* / genetics
  • Epileptic Syndromes* / physiopathology
  • Gene Knock-In Techniques / methods
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Pentylenetetrazole
  • Protein Serine-Threonine Kinases* / genetics
  • Protein Serine-Threonine Kinases* / metabolism
  • Receptor, Cannabinoid, CB1 / genetics
  • Receptor, Cannabinoid, CB1 / metabolism
  • Receptors, Cannabinoid
  • Seizures* / drug therapy
  • Seizures* / genetics
  • Spasms, Infantile
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism

Substances

  • Cannabidiol
  • CDKL5 protein, mouse
  • CNR1 protein, mouse
  • Endocannabinoids
  • GPR55 protein, mouse
  • Pentylenetetrazole
  • Protein Serine-Threonine Kinases
  • Receptor, Cannabinoid, CB1
  • Receptors, Cannabinoid
  • TRPV Cation Channels
  • TRPV1 protein, mouse

Supplementary concepts

  • CDKL5 deficiency disorder