Cited by 133Cannabis and Cannabinoid ResearchNeuroscience and Neuropharmacology ResearchReceptor Mechanisms and Signaling

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Multiple Forms of Endocannabinoid and Endovanilloid Signaling Regulate the Tonic Control of GABA Release

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Lee, S.-H., Ledri, M., Toth, B., Marchionni, I., Henstridge, C. M., Dudok, B., Kenesei, K., Barna, L., Szabo, S. I., Renkecz, T., Oberoi, M., Watanabe, M., Limoli, C. L., Horvai, G., Soltesz, I., Katona, I.·2015·Journal of Neuroscience

DOI 10.1523/jneurosci.4112-14.2015PMC PMC4495235

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Abstract

Persistent CB1 cannabinoid receptor activity limits neurotransmitter release at various synapses throughout the brain. However, it is not fully understood how constitutively active CB1 receptors, tonic endocannabinoid signaling, and its regulation by multiple serine hydrolases contribute to the synapse-specific calibration of neurotransmitter release probability. To address this question at perisomatic and dendritic GABAergic synapses in the mouse hippocampus, we used a combination of paired whole-cell patch-clamp recording, liquid chromatography/tandem mass spectrometry, stochastic optical reconstruction microscopy super-resolution imaging, and immunogold electron microscopy. Unexpectedly, application of the CB1 antagonist and inverse agonist AM251 [N-1-(2,4-dichlorophenyl)-5-(4-iodophenyl)-4-methyl-N-1-piperidinyl-1H-pyrazole-3-carboxamide], but not the neutral antagonist NESS0327 [8-chloro-1-(2,4-dichlorophenyl)-N-piperidin-1-yl-5,6-dihydro-4H-benzo[2,3]cyclohepta[2,4-b]pyrazole-3-carboxamine], significantly increased synaptic transmission between CB1-positive perisomatic interneurons and CA1 pyramidal neurons. JZL184 (4-nitrophenyl 4-[bis(1,3-benzodioxol-5-yl)(hydroxy)methyl]piperidine-1-carboxylate), a selective inhibitor of monoacylglycerol lipase (MGL), the presynaptic degrading enzyme of the endocannabinoid 2-arachidonoylglycerol (2-AG), elicited a robust increase in 2-AG levels and concomitantly decreased GABAergic transmission. In contrast, inhibition of fatty acid amide hydrolase (FAAH) by PF3845 (N-pyridin-3-yl-4-[[3-[5-(trifluoromethyl)pyridin-2-yl]oxyphenyl]methyl]piperidine-1-carboxamide) elevated endocannabinoid/endovanilloid anandamide levels but did not change GABAergic synaptic activity. However, FAAH inhibitors attenuated tonic 2-AG increase and also decreased its synaptic effects. This antagonistic interaction required the activation of the transient receptor potential vanilloid receptor TRPV1, which was concentrated on postsynaptic intracellular membrane cisternae at perisomatic GABAergic symmetrical synapses. Interestingly, neither AM251, JZL184, nor PF3845 affected CB1-positive dendritic interneuron synapses. Together, these findings are consistent with the possibility that constitutively active CB1 receptors substantially influence perisomatic GABA release probability and indicate that the synaptic effects of tonic 2-AG release are tightly controlled by presynaptic MGL activity and also by postsynaptic endovanilloid signaling and FAAH activity. SIGNIFICANCE STATEMENT: Tonic cannabinoid signaling plays a critical role in the regulation of synaptic transmission. However, the mechanistic details of how persistent CB1 cannabinoid receptor activity inhibits neurotransmitter release have remained elusive. Therefore, electrophysiological recordings, lipid measurements, and super-resolution imaging were combined to elucidate those signaling molecules and mechanisms that underlie tonic cannabinoid signaling. The findings indicate that constitutive CB1 activity has pivotal function in the tonic control of hippocampal GABA release. Moreover, the endocannabinoid 2-arachidonoylglycerol (2-AG) is continuously generated postsynaptically, but its synaptic effect is regulated strictly by presynaptic monoacylglycerol lipase activity. Finally, anandamide signaling antagonizes tonic 2-AG signaling via activation of postsynaptic transient receptor potential vanilloid TRPV1 receptors. This unexpected mechanistic diversity may be necessary to fine-tune GABA release probability under various physiological and pathophysiological conditions.

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Authors: Lee, S.-H., Ledri, M., Toth, B., Marchionni, I., Henstridge, C. M., Dudok, B., Kenesei, K., Barna, L., Szabo, S. I., Renkecz, T., Oberoi, M., Watanabe, M., Limoli, C. L., Horvai, G., Soltesz, I., & Katona, I.
Affiliations: University of California, Irvine (US)
HUN-REN Institute of Experimental Medicine (HU)
Semmelweis University (HU)
Budapest University of Technology and Economics (HU)
Hokkaido University (JP)
ORCID: Lee, S.-H.
Ledri, M.
Henstridge, C. M.
Dudok, B.
Kenesei, K.
Barna, L.
Renkecz, T.
Oberoi, M.
Watanabe, M.
Limoli, C. L.
Katona, I.
Venue: Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2015-07-08
Volume: 35
Issue: 27
Pages: 10039-10057
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.4112-14.2015
PMC: PMC4495235
OpenAlex: W1892287994
Cited by: 133
References: 115
Citations by year: 2026: 1 · 2025: 10 · 2024: 6 · 2023: 6 · 2022: 18 · 2021: 18 · 2020: 8 · 2019: 4 · 2018: 13 · 2017: 23 · 2016: 19 · 2015: 6
FWCI: 14.65
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
Locations: Journal of Neuroscience (publishedVersion, cc-by)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Padua Research Archive (University of Padova) (submittedVersion, other-oa)
Discovery Research Portal (University of Dundee) (submittedVersion)
eScholarship (California Digital Library) (submittedVersion)
Lund University Publications (Lund University) (submittedVersion)
Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
Padua Research Archive (University of Padova) (submittedVersion)
Funders: National Aeronautics and Space Administration (NNX10AD59G, NNX15AI22G)
Wellcome Trust (090946)
Magyar Tudományos Akadémia
National Institutes of Health (CA-62203, NS35915)
University of California, Irvine (CA-62203)
National Cancer Institute (CA 62203, P30CA062203)
National Institute of General Medical Sciences (GM-69337, T34GM069337)
National Institute of Neurological Disorders and Stroke (R29NS035915, R01NS035915, NS-35915, R37NS035915)
FP7 Ideas: European Research Council (243153)
Topics: Health Sciences › Medicine › Pharmacology (medical) › Cannabis and Cannabinoid Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
Keywords: endocannabinoid signaling, CB1 receptor, tonic inhibition, GABA release, 2-arachidonoylglycerol, anandamide, monoacylglycerol lipase, fatty acid amide hydrolase, TRPV1, presynaptic inhibition, hippocampus, CA1 pyramidal neurons
MeSH terms: Animals, Arachidonic Acids, Enzyme Inhibitors, Female, gamma-Aminobutyric Acid, Glycerides, Hippocampus, Male, Mice, Inbred C57BL, Mice, Transgenic, Neurons, Piperidines, Pyrazoles, Pyridines, Synapses, Signal Transduction, Receptor, Cannabinoid, CB1, TRPV Cation Channels, Mice, Inhibitory Postsynaptic Potentials, Cannabinoid Receptor Modulators, Endocannabinoids

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Multiple Forms of Endocannabinoid and Endovanilloid Signaling Regulate the Tonic Control of GABA Release

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