Cannabidiol inhibits endocannabinoid signaling in autaptic hippocampal neurons

Molecular Pharmacology

Volumn 94, Issue 1, 2018, Pages 743-748

  Straiker, Alex ^a   Dvorakova, Michaela ^a   Zimmowitch, Anaelle ^a   MacKie, Ken ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; BACLOFEN; CANNABIDIOL; ENDOCANNABINOID; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR;

ALLOSTERISM; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; DRUG MECHANISM; HIPPOCAMPUS; IN VITRO STUDY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ANIMAL; ANTAGONISTS AND INHIBITORS; METABOLISM; MOUSE; NERVE CELL;

ANIMALS; CANNABIDIOL; CANNABINOIDS; ENDOCANNABINOIDS; HIPPOCAMPUS; MICE; NEURONAL PLASTICITY; NEURONS; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; SIGNAL TRANSDUCTION;

EID: 85052148475     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.118.111864     Document Type: Article

References (41)

1. Adams R, Hunt M, and Clark JH (1940) Structure of cannabidiol, a product isolated from the marihuana extract of Minnesota wild hemp. J Am Chem Soc 62: 196-200.
2. Agurell S, Carlsson S, Lindgren JE, Ohlsson A, Gillespie H, and Hollister L (1981) Interactions of delta 1-tetrahydrocannabinol with cannabinol and cannabidiol following oral administration in man: assay of cannabinol and cannabidiol by mass fragmentography. Experientia 37:1090-1092.
3. Bekkers JM and Stevens CF (1991) Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci USA 88:7834-7838.
4. Dalton WS, Martz R, Lemberger L, Rodda BE, and Forney RB (1976) Influence of cannabidiol on delta-9-tetrahydrocannabinol effects. Clin Pharmacol Ther 19: 300-309.
5. Devinsky O, Cross JH, Laux L, Marsh E, Miller I, Nabbout R, Scheffer IE, Thiele EA, and Wright S; Cannabidiol in Dravet Syndrome Study Group (2017) Trial of cannabidiol for drug-resistant seizures in the Dravet syndrome. N Engl J Med 376: 2011-2020.
6. Devinsky O, Patel AD, Thiele EA, Wong MH, Appleton R, Harden CL, Greenwood S, Morrison G, and Sommerville K; GWPCARE1 Part A Study Group (2018) Randomized, dose-ranging safety trial of cannabidiol in Dravet syndrome. Neurology 90:e1204-e1211.
7. Drew GM, Lau BK, and Vaughan CW (2009) Substance P drives endocannabinoidmediated disinhibition in a midbrain descending analgesic pathway. J Neurosci 29: 7220-7229.
8. Elsohly MA and Slade D (2005) Chemical constituents of marijuana: the complex mixture of natural cannabinoids. Life Sci 78:539-548.
9. Furshpan EJ, MacLeish PR, O'Lague PH, and Potter DD (1976) Chemical transmission between rat sympathetic neurons and cardiac myocytes developing in microcultures: evidence for cholinergic, adrenergic, and dual-function neurons. Proc Natl Acad Sci USA 73:4225-4229.
10. Gaoni Y and Mechoulam R (1964) Isolation, structure and partial synthesis of an active constituent of hashish. J Am Chem Soc 86:1646-1647.
11. Haj-Dahmane S and Shen RY (2005) The wake-promoting peptide orexin-B inhibits glutamatergic transmission to dorsal raphe nucleus serotonin neurons through retrograde endocannabinoid signaling. J Neurosci 25:896-905.
12. Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin LS, de Costa BR, and Rice KC (1990) Cannabinoid receptor localization in brain. Proc Natl Acad Sci USA 87: 1932-1936.
13. Hiltunen AJ and Järbe TU (1986) Cannabidiol attenuates delta 9-tetrahydrocannabinollike discriminative stimulus effects of cannabinol. Eur J Pharmacol 125:301-304.
14. Jain T, Wager-Miller J, Mackie K, and Straiker A (2013) Diacylglycerol lipasea (DAGLa) and DAGLb cooperatively regulate the production of 2-arachidonoyl glycerol in autaptic hippocampal neurons. Mol Pharmacol 84:296-302.
15. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, and Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309-380.
16. Karniol IG and Carlini EA (1973) Pharmacological interaction between cannabidiol and delta 9-tetrahydrocannabinol. Psychopharmacology (Berl) 33:53-70.
17. Kim J, Isokawa M, Ledent C, and Alger BE (2002) Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci 22:10182-10191.
18. Kreitzer AC and Regehr WG (2001) Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
19. Laprairie RB, Bagher AM, Kelly ME, and Denovan-Wright EM (2015) Cannabidiol is a negative allosteric modulator of the cannabinoid CB1 receptor. Br J Pharmacol 172:4790-4805.
20. Levison SW and McCarthy KD (1991) Characterization and partial purification of AIM: a plasma protein that induces rat cerebral type 2 astroglia from bipotential glial progenitors. J Neurochem 57:782-794.
21. Maa E and Figi P (2014) The case for medical marijuana in epilepsy. Epilepsia 55: 783-786.
22. Maccarrone M, Maldonado R, Casas M, Henze T, and Centonze D (2017) Cannabinoids therapeutic use: what is our current understanding following the introduction of THC, THC:CBD oromucosal spray and others? Expert Rev Clin Pharmacol 10:443-455.
23. Maejima T, Hashimoto K, Yoshida T, Aiba A, and Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475.
24. McPartland JM, Duncan M, Di Marzo V, and Pertwee RG (2015) Are cannabidiol and D(9) -tetrahydrocannabivarin negative modulators of the endocannabinoid system? A systematic review. Br J Pharmacol 172:737-753.
25. Mechoulam R, Shani A, Edery H, and Grunfeld Y (1970) Chemical basis of hashish activity. Science 169:611-612.
26. O'Connell BK, Gloss D, and Devinsky O (2017) Cannabinoids in treatment-resistant epilepsy: a review. Epilepsy Behav 70:341-348.
27. Ohlsson A, Lindgren JE, Andersson S, Agurell S, Gillespie H, and Hollister LE (1986) Single-dose kinetics of deuterium-labelled cannabidiol in man after smoking and intravenous administration. Biomed Environ Mass Spectrom 13:77-83.
28. Papahatjis DP, Nikas SP, Andreou T, and Makriyannis A (2002) Novel 19,19-chain substituted Delta(8)-tetrahydrocannabinols. Bioorg Med Chem Lett 12:3583-3586.
29. Petitet F, Jeantaud B, Reibaud M, Imperato A, and Dubroeucq MC (1998) Complex pharmacology of natural cannabinoids: evidence for partial agonist activity of delta9-tetrahydrocannabinol and antagonist activity of cannabidiol on rat brain cannabinoid receptors. Life Sci 63:PL1-PL6.
30. Russo E and Guy GW (2006) A tale of two cannabinoids: the therapeutic rationale for combining tetrahydrocannabinol and cannabidiol. Med Hypotheses 66:234-246.
31. Straiker A, Hu SS, Long JZ, Arnold A, Wager-Miller J, Cravatt BF, and Mackie K (2009) Monoacylglycerol lipase limits the duration of endocannabinoid-mediated depolarization-induced suppression of excitation in autaptic hippocampal neurons. Mol Pharmacol 76:1220-1227.
32. Straiker A and Mackie K (2005) Depolarization-induced suppression of excitation in murine autaptic hippocampal neurones. J Physiol 569:501-517.
33. Straiker A and Mackie K (2007) Metabotropic suppression of excitation in murine autaptic hippocampal neurons. J Physiol 578:773-785.
34. Straiker A and Mackie K (2009) Cannabinoid signaling in inhibitory autaptic hippocampal neurons. Neuroscience 163:190-201.
35. Straiker A, Mitjavila J, Yin D, Gibson A, and Mackie K (2015) Aiming for allosterism: evaluation of allosteric modulators of CB1 in a neuronal model. Pharmacol Res 99:370-376.
36. Straiker A, Wager-Miller J, Hu SS, Blankman JL, Cravatt BF, and Mackie K (2011a) COX-2 and fatty acid amide hydrolase can regulate the time course of depolarization-induced suppression of excitation. Br J Pharmacol 164:1672-1683.
37. Straiker A, Wager-Miller J, Hutchens J, and Mackie K (2011b) Differential signalling in human cannabinoid CB1 receptors and their splice variants in autaptic hippocampal neurones. Br J Pharmacol 165:2660-2671.
38. Straiker AJ, Borden CR, and Sullivan JM (2002) G-protein alpha subunit isoforms couple differentially to receptors that mediate presynaptic inhibition at rat hippocampal synapses. J Neurosci 22:2460-2468.
39. Thomas A, Baillie GL, Phillips AM, Razdan RK, Ross RA, and Pertwee RG (2007) Cannabidiol displays unexpectedly high potency as an antagonist of CB1 and CB2 receptor agonists in vitro. Br J Pharmacol 150:613-623.
40. Thomas BF, Gilliam AF, Burch DF, Roche MJ, and Seltzman HH (1998) Comparative receptor binding analyses of cannabinoid agonists and antagonists. J Pharmacol Exp Ther 285:285-292.
41. Wilson RI and Nicoll RA (2001) Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592.