Cholecystokinin exerts an effect via the endocannabinoid system to inhibit GABAergic transmission in midbrain periaqueductal gray

Neuropsychopharmacology

Volumn 36, Issue 9, 2011, Pages 1801-1810

  Mitchell, Vanessa A ^a   Jeong, Hyo Jin ^a   Drew, Geoffrey M ^a   Vaughan, Christopher W ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

anxiety; cannabinoids; cholecystokinin; pain; periaqueductal gray; synaptic transmission

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; 4 [[2 [2 [[(2 ADAMANTYLOXY)CARBONYL]AMINO] 3 (1H INDOL 3 YL) 2 METHYLPROPIONAMIDO] 1 PHENYLETHYL]AMINO] 4 OXOBUTYRIC ACID MEGLUMINE; CHOLECYSTOKININ; CHOLECYSTOKININ OCTAPEPTIDE; DEVAZEPIDE; ENDOCANNABINOID; N METHYL DEXTRO ASPARTIC ACID; TETRAHYDROLIPSTATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BRAIN DEPTH RECORDING; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GABAERGIC TRANSMISSION; MALE; MESENCEPHALON; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PAIN; PATCH CLAMP; PERIAQUEDUCTAL GRAY MATTER; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; Q WAVE; RAT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALS; CHOLAGOGUES AND CHOLERETICS; CHOLECYSTOKININ; ENDOCANNABINOIDS; FEMALE; GAMMA-AMINOBUTYRIC ACID; MALE; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PERIAQUEDUCTAL GRAY; RATS; RATS, SPRAGUE-DAWLEY; SINCALIDE; SYNAPTIC TRANSMISSION;

EID: 79960329361     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2011.59     Document Type: Article

References (43)

1. Bertoglio LJ, Zangrossi Jr H (2005). Involvement of dorsolateral periaqueductal gray cholecystokinin-2 receptors in the regulation of a panic-related behavior in rats. Brain Res 1059: 46-51. (Pubitemid 41457325)
2. Bisogno T, Howell F, Williams G, Minassi A, Cascio MG, Ligresti A et al (2003). Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 163: 463-468. (Pubitemid 37429860)
3. Brack KE, Jeffery SM, Lovick TA (2006). Cardiovascular and respiratory responses to a panicogenic agent in anaesthetised female Wistar rats at different stages of the oestrous cycle. Eur J Neurosci 23: 3309-3318.
4. Brack KE, Lovick TA (2007). Neuronal excitability in the periaqueductal grey matter during the estrous cycle in female Wistar rats. Neuroscience 144: 325-335. (Pubitemid 44839030)
5. Carlberg M, Gundlach AL, Mercer LD, Beart PM (1992). Auto-radiographic localization of cholecystokinin A and B receptors in rat brain using [125I]d-Tyr25 (Nle28,31)-CCK 25-33S. Eur J Neurosci 4: 563-573.
6. Chen XH, Geller EB, Adler MW (1998). CCK(B) receptors in the periaqueductal grey are involved in electroacupuncture antinociception in the rat cold water tail-flick test. Neuro-pharmacology 37: 751-757. (Pubitemid 28313900)
7. Chhatwal JP, Gutman AR, Maguschak KA, Bowser ME, Yang Y, Davis M et al (2009). Functional interactions between endocan-nabinoid and CCK neurotransmitter systems may be critical for extinction learning. Neuropsychopharmacology 34: 509-521.
8. Connor M, Bagley EE, Mitchell VA, Ingram SL, Christie MJ, Humphrey PPA et al (2004). Cellular actions of somatostatin on rat peri-aqueductal grey neurons in vitro. Br J Pharmacol 142: 1273-1280. (Pubitemid 39178881)
9. Drew GM, Lau BK, Vaughan CW (2009). Substance P Drives endocannabinoid-mediated disinhibition in a midbrain descend-ing analgesic pathway. J Neurosci 29: 7220-7229.
10. Drew GM, Mitchell VA, Vaughan CW (2005). Postsynaptic actions of substance P on rat periaqueductal grey neurons in vitro. Neuropharmacology 49: 587-595. (Pubitemid 41208280)
11. Drew GM, Mitchell VA, Vaughan CW (2008). Glutamate spillover modulates GABAergic synaptic transmission in the rat midbrain periaqueductal grey via metabotropic glutamate receptors and endocannabinoid signaling. J Neurosci 28: 808-815. (Pubitemid 351158994)
12. Faris PL, Komisaruk BR, Watkins LR, Mayer DJ (1983). Evidence for the neuropeptide cholecystokinin as an antagonist of opiate analgesia. Science 219: 310-312. (Pubitemid 13222316)
13. Fields HL, Basbaum AI, Heinricher MM (2006). Central nervous systems mechanisms of pain modulation. In: Mc Mahon SB, Koltzenburg M (eds). Textbook of Pain, 5th edn. Elsevier, Churchill Livingston: Philadelphia, pp 125-142.
14. Finn DP, Jhaveri MD, Beckett SRG, Roe CH, Kendall DA, Marsden CA et al (2003). Effects of direct periaqueductal grey administration of a cannabinoid receptor agonist on nociceptive and aversive responses in rats. Neuropharmacology 45: 594-604. (Pubitemid 36980816)
15. Graeff FG, Silveira MC, Nogueira RL, Audi EA, Oliveira RM (1993). Role of the amygdala and periaqueductal gray in anxiety and panic. Behav Brain Res 58: 123-131. (Pubitemid 24024052)
16. Hohmann AG, Suplita RL, Bolton NM, Neely MH, Fegley D, Mangieri R et al (2005). An endocannabinoid mechanism for stress-induced analgesia. Nature 435: 1108-1112. (Pubitemid 40910518)
17. Jung KM, Mangieri R, Stapleton C, Kim J, Fegley D, Wallace M et al (2005). Stimulation of endocannabinoid formation in brain slice cultures through activation of group I metabotropic glutamate receptors. Mol Pharmacol 68: 1196-1202. (Pubitemid 41539977)
18. Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009). Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89: 309-380.
19. Keay KA, Bandler R (2001). Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neurosci Biobehav Rev 25: 669-678. (Pubitemid 34136896)
20. Kubota Y, Inagaki S, Shiosaka S, Cho HJ, Tateishi K, Hashimura E etal (1983). The distribution of cholecystokinin octapeptide-like structures in the lower brain stem of the rat: an immuno-histochemical analysis. Neuroscience 9: 587-604. (Pubitemid 13035010)
21. Kurrikoff K, Inno J, Matsui T, Vasar E (2008). Stress-induced analgesia in mice: evidence for interaction between endocanna-binoids and cholecystokinin. Eur J Neurosci 27: 2147-2155. (Pubitemid 351521482)
22. Lau BK, Vaughan CW (2008). Muscarinic modulation of synaptic transmission via endocannabinoid signalling in the rat midbrain periaqueductal gray. Mol Pharmacol 74: 1392-1398.
23. Li Y, Han JS (1989). Cholecystokinin-octapeptide antagonizes morphine analgesia in periaqueductal gray of the rat. Brain Res 480: 105-110. (Pubitemid 19050202)
24. Lichtman AH, Cook SA, Martin BR (1996). Investigation of brain sites mediating cannabinoid-induced antinociception in rats: evidence supporting periaqueductal gray involvement. J Pharmacol Exp Ther 276: 585-593.
25. Liu H, Chandler S, Beitz AJ, Shipley MT, Behbehani MM (1994). Characterization of the effect of cholecystokinin (CCK) on neurons in the periaqueductal gray of the rat: immuno-cytochemical and in vivo and in vitro electrophysiological studies. Brain Res 642: 83-94. (Pubitemid 24105692)
26. Lovick TA (2008). Pronociceptive action of cholecystokinin in the periaqueductal grey: a role in neuropathic and anxiety-induced hyperalgesic states. Neurosci Biobehav Rev 32: 852-862.
27. Luo B, Cheu JW, Siegel A (1998). Cholecystokinin B receptors in the periaqueductal gray potentiate defensive rage behavior elicited from the medial hypothalamus of the cat. Brain Res 796: 27-37. (Pubitemid 28343230)
28. Mercer LD, Beart PM (2004). Immunolocalization of CCK1R in rat brain using a new anti-peptide antibody. Neurosci Lett 359: 109-113. (Pubitemid 38446650)
29. Mercer LD, Beart PM, Horne MK, Finkelstein DI, Carrive P, Paxinos G (1996). On the distribution of cholecystokinin B receptors in monkey brain. Brain Res 738: 313-318. (Pubitemid 26378926)
30. Mitchell VA, Kawahara H, Vaughan CW (2009). Neurotensin inhibition of GABAergic transmission via m Glu R-induced endocannabinoid signalling in rat periaqueductal grey. J Physiol (Lond) 587: 2511-2520.
31. Moreira FA, Aguiar DC, Guimaraes FS (2007). Anxiolytic-like effect of cannabinoids injected into the rat dorsolateral periaqueductal gray. Neuropharmacology 52: 958-965. (Pubitemid 46227483)
32. Netto CF, Guimaraes FS (2004). Anxiogenic effect of cholecysto-kinin in the dorsal periaqueductal gray. Neuropsycho pharmacology 29: 101-107. (Pubitemid 38068019)
33. Noble F, Wank SA, Crawley JN, Bradwejn J, Seroogy KB, Hamon M et al (1999). International Union of Pharmacology. XXI. structure, distribution, and functions of cholecystokinin recep-tors. Pharmacol Rev 51: 745-781.
34. Osborne PB, Vaughan CW, Wilson HI, Christie MJ (1996). Opioid inhibition of rat periaqueductal grey neurones with identified projections to rostral ventromedial medulla in vitro. J Physiol (Lond) 490: 383-389. (Pubitemid 26032954)
35. Reichling DB, Basbaum AI (1990). Contribution of brain-stem GABAergic circuitry to descending antinociceptive controls.1. GABA-immunoreactive projection neurons in the periaqueductal gray and nucleus raphe magnus. J Comp Neurol 302: 370-377.
36. Resstel LB, Lisboa SF, Aguiar DC, Correa FM, Guimaraes FS (2008). Activation of CB1 cannabinoid receptors in the dorsolateral periaqueductal gray reduces the expression of contextual fear conditioning in rats. Psychopharmacology 198: 405-411.
37. Smeets RL, Fouraux MA, van Emst-de Vries SE, De Pont JJ, Willems PH (1998). Protein kinase C-mediated inhibition of transmembrane signalling through CCK(A) and CCK(B) receptors. Brit J Pharmacol 123: 1189-1197. (Pubitemid 28120518)
38. Tortorici V, Nogueira L, Salas R, Vanegas H (2003). Involvement of local cholecystokinin in the tolerance induced by morphine microinjections into the periaqueductal gray of rats. Pain 102: 9-16. (Pubitemid 36298857)
39. Uchigashima M, Narushima M, Fukaya M, Katona I, Kano M, Watanabe M (2007). Subcellular arrangement of molecules for 2-arachidonoyl-glycerol- mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J Neurosci 27: 3663-3676. (Pubitemid 46557660)
40. Vaughan CW, Christie MJ (1997). Presynaptic inhibitory action of opioids on synaptic transmission in the rat periaqueductal grey in vitro. J Physiol (Lond) 498: 463-472. (Pubitemid 27073390)
41. Vaughan CW, Connor M, Bagley EE, Christie MJ (2000). Actions of cannabinoids on membrane properties and synaptic trans-mission in rat periaqueductal gray neurons in vitro. Mol Pharmacol 57: 288-295. (Pubitemid 30084505)
42. Yang YM, Chung JM, Rhim H (2006). Cellular action of cholecystokinin-8S- mediated excitatory effects in the rat periaqueductal gray. Life Sci 79: 1702-1711. (Pubitemid 44374549)
43. Yang YM, Chung JM, Rhim H (2007). Cholecystokinin-8S-induced intracellular calcium signaling in acutely isolated periaqueductal gray neurons of the rat Biol Pharm Bull 30: 297-302.