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Featured ArticleArticles, Neurobiology of Disease

Downregulation of the CB1 Cannabinoid Receptor and Related Molecular Elements of the Endocannabinoid System in Epileptic Human Hippocampus

Anikó Ludányi, Loránd Erőss, Sándor Czirják, János Vajda, Péter Halász, Masahiko Watanabe, Miklós Palkovits, Zsófia Maglóczky, Tamás F. Freund and István Katona
Journal of Neuroscience 19 March 2008, 28 (12) 2976-2990; DOI: https://doi.org/10.1523/JNEUROSCI.4465-07.2008
Anikó Ludányi
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Loránd Erőss
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Sándor Czirják
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János Vajda
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Péter Halász
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Masahiko Watanabe
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Miklós Palkovits
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Zsófia Maglóczky
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Tamás F. Freund
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István Katona
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Abstract

Endocannabinoid signaling is a key regulator of synaptic neurotransmission throughout the brain. Compelling evidence shows that its perturbation leads to development of epileptic seizures, thus indicating that endocannabinoids play an intrinsic protective role in suppressing pathologic neuronal excitability. To elucidate whether long-term reorganization of endocannabinoid signaling occurs in epileptic patients, we performed comparative expression profiling along with quantitative electron microscopic analysis in control (postmortem samples from subjects with no signs of neurological disorders) and epileptic (surgically removed from patients with intractable temporal lobe epilepsy) hippocampal tissue. Quantitative PCR measurements revealed that CB1 cannabinoid receptor mRNA was downregulated to one-third of its control value in epileptic hippocampus. Likewise, the cannabinoid receptor-interacting protein-1a mRNA was decreased, whereas 1b isoform levels were unaltered. Expression of diacylglycerol lipase-α, an enzyme responsible for 2-arachidonoylglycerol synthesis, was also reduced by ∼60%, whereas its related β isoform levels were unchanged. Expression level of N-acyl-phosphatidylethanolamine-hydrolyzing phospholipase D and fatty acid amide hydrolase, metabolic enzymes of anandamide, and 2-arachidonoylglycerol's degrading enzyme monoacylglycerol lipase did not change. The density of CB1 immunolabeling was also decreased in epileptic hippocampus, predominantly in the dentate gyrus, where quantitative electron microscopic analysis did not reveal changes in the ratio of CB1-positive GABAergic boutons, but uncovered robust reduction in the fraction of CB1-positive glutamatergic axon terminals. These findings show that a neuroprotective machinery involving endocannabinoids is impaired in epileptic human hippocampus and imply that downregulation of CB1 receptors and related molecular components of the endocannabinoid system may facilitate the deleterious effects of increased network excitability.

  • DGL
  • CRIP
  • cannabinoid
  • CB1
  • 2-AG
  • temporal lobe epilepsy
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The Journal of Neuroscience: 28 (12)
Journal of Neuroscience
Vol. 28, Issue 12
19 Mar 2008
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Downregulation of the CB1 Cannabinoid Receptor and Related Molecular Elements of the Endocannabinoid System in Epileptic Human Hippocampus
Anikó Ludányi, Loránd Erőss, Sándor Czirják, János Vajda, Péter Halász, Masahiko Watanabe, Miklós Palkovits, Zsófia Maglóczky, Tamás F. Freund, István Katona
Journal of Neuroscience 19 March 2008, 28 (12) 2976-2990; DOI: 10.1523/JNEUROSCI.4465-07.2008

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Downregulation of the CB1 Cannabinoid Receptor and Related Molecular Elements of the Endocannabinoid System in Epileptic Human Hippocampus
Anikó Ludányi, Loránd Erőss, Sándor Czirják, János Vajda, Péter Halász, Masahiko Watanabe, Miklós Palkovits, Zsófia Maglóczky, Tamás F. Freund, István Katona
Journal of Neuroscience 19 March 2008, 28 (12) 2976-2990; DOI: 10.1523/JNEUROSCI.4465-07.2008
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