Regulation of endocannabinoid release by G proteins: A paracrine mechanism of G protein-coupled receptor action

Molecular and Cellular Endocrinology

Volumn 353, Issue 1-2, 2012, Pages 29-36

  Gyombolai, Pál ^a   Pap, Dorottya ^a   Turu, Gábor ^a   Catt, Kevin J ^b   Bagdy, György ^a   Hunyady, László ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Angiotensin II; CB1; Endocannabinoid; GPCR

Indexed keywords

2 ARACHIDONOYLGLYCEROL; 4 AMINOBUTYRIC ACID; ANANDAMIDE; ANGIOTENSIN II; ANGIOTENSIN RECEPTOR; CALCIUM ION; CANNABINOID 1 RECEPTOR; CHOLECYSTOKININ; CORTICOTROPIN RELEASING FACTOR; DIACYLGLYCEROL; ENDOCANNABINOID; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; METABOTROPIC RECEPTOR; MUSCARINIC RECEPTOR; SEROTONIN 2A RECEPTOR; SEROTONIN 2C RECEPTOR;

4 AMINOBUTYRIC ACID RELEASE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC SYSTEM; HUMAN; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNE SYSTEM; METABOLIC REGULATION; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SUPRAOPTIC NUCLEUS; TRANSACTIVATION;

ANGIOTENSIN II; ANIMALS; ARACHIDONIC ACIDS; ENDOCANNABINOIDS; GLYCERIDES; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HUMANS; PARACRINE COMMUNICATION; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PIPERIDINES; PYRAZOLES; RATS; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, CANNABINOID, CB1;

EID: 84857794906     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.10.011     Document Type: Review

References (89)

1. Alger B.E., Kim J. Supply and demand for endocannabinoids. Trends Neurosci. 2011, 34:304-315.
2. Aso E., Renoir T., Mengod G., Ledent C., Hamon M., Maldonado R., Lanfumey L., Valverde O. Lack of CB1 receptor activity impairs serotonergic negative feedback. J. Neurochem. 2009, 109:935-944.
3. Bacci A., Huguenard J.R., Prince D.A. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 2004, 431:312-316.
4. Bagdy G. Role of the hypothalamic paraventricular nucleus in 5-HT1A, 5-HT2A and 5-HT2C receptor-mediated oxytocin, prolactin and ACTH/corticosterone responses. Behav. Brain Res. 1996, 73:277-280.
5. Bagdy G., Makara G.B. Hypothalamic paraventricular nucleus lesions differentially affect serotonin-1A (5-HT1A) and 5-HT2 receptor agonist-induced oxytocin, prolactin, and corticosterone responses. Endocrinology 1994, 134:1127-1131.
6. Bains J.S., Ferguson A.V. Paraventricular nucleus neurons projecting to the spinal cord receive excitatory input from the subfornical organ. Am. J. Physiol 1995, 268:R625-R633.
7. Basavarajappa B.S. Critical enzymes involved in endocannabinoid metabolism. Protein Pept. Lett. 2007, 14:237-246.
8. Berdyshev E.V., Schmid P.C., Krebsbach R.J., Schmid H.H. Activation of PAF receptors results in enhanced synthesis of 2-arachidonoylglycerol (2-AG) in immune cells. FASEB J. 2001, 15:2171-2178.
9. Best A.R., Regehr W.G. Serotonin evokes endocannabinoid release and retrogradely suppresses excitatory synapses. J. Neurosci. 2008, 28:6508-6515.
10. Bisogno T. Endogenous cannabinoids: structure and metabolism. J. Neuroendocrinol. 2008, 20(Suppl. 1):1-9.
11. Bockaert J., Claeysen S., Becamel C., Dumuis A., Marin P. Neuronal 5-HT metabotropic receptors: fine-tuning of their structure, signaling, and roles in synaptic modulation. Cell Tissue Res. 2006, 326:553-572.
12. Cadas H., Gaillet S., Beltramo M., Venance L., Piomelli D. Biosynthesis of an endogenous cannabinoid precursor in neurons and its control by calcium and cAMP. J. Neurosci. 1996, 16:3934-3942.
13. Chataigneau T., Feletou M., Thollon C., Villeneuve N., Vilaine J.P., Duhault J., Vanhoutte P.M. Cannabinoid CB1 receptor and endothelium-dependent hyperpolarization in guinea-pig carotid, rat mesenteric and porcine coronary arteries. Br. J. Pharmacol. 1998, 123:968-974.
14. Chen Q., Pan H.L. Signaling mechanisms of angiotensin II-induced attenuation of GABAergic input to hypothalamic presympathetic neurons. J. Neurophysiol. 2007, 97:3279-3287.
15. Chhatwal J.P., Gutman A.R., Maguschak K.A., Bowser M.E., Yang Y., Davis M., Ressler K.J. Functional interactions between endocannabinoid and CCK neurotransmitter systems may be critical for extinction learning. Neuropsychopharmacology 2009, 34:509-521.
16. De Petrocellis L., Di Marzo V. Non-CB1, non-CB2 receptors for endocannabinoids, plant cannabinoids, and synthetic cannabimimetics: focus on G-protein-coupled receptors and transient receptor potential channels. J. Neuroimmune. Pharmacol. 2010, 5:103-121.
17. Di S., Malcher-Lopes R., Halmos K.C., Tasker J.G. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J. Neurosci. 2003, 23:4850-4857.
18. Di S., Malcher-Lopes R., Marcheselli V.L., Bazan N.G., Tasker J.G. Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and gamma-aminobutyric acid inputs to hypothalamic magnocellular neurons. Endocrinology 2005, 146:4292-4301.
19. Foldy C., Lee S.Y., Szabadics J., Neu A., Soltesz I. Cell type-specific gating of perisomatic inhibition by cholecystokinin. Nat. Neurosci. 2007, 10:1128-1130.
20. Freund T.F., Katona I., Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol. Rev. 2003, 83:1017-1066.
21. Fukudome Y., Ohno-Shosaku T., Matsui M., Omori Y., Fukaya M., Tsubokawa H., Taketo M.M., Watanabe M., Manabe T., Kano M. Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2-mediated direct suppression and M1/M3-mediated indirect suppression through endocannabinoid signalling. Eur. J. Neurosci. 2004, 19:2682-2692.
22. Fulton D., Quilley J. Evidence against anandamide as the hyperpolarizing factor mediating the nitric oxide-independent coronary vasodilator effect of bradykinin in the rat. J. Pharmacol. Exp. Ther. 1998, 286:1146-1151.
23. Gebremedhin D., Lange A.R., Campbell W.B., Hillard C.J., Harder D.R. Cannabinoid CB1 receptor of cat cerebral arterial muscle functions to inhibit L-type Ca2+ channel current. Am. J. Physiol 1999, 276:H2085-H2093.
24. Haj-Dahmane S., Shen R.Y. The wake-promoting peptide orexin-B inhibits glutamatergic transmission to dorsal raphe nucleus serotonin neurons through retrograde endocannabinoid signaling. J. Neurosci. 2005, 25:896-905.
25. Hashimotodani Y., Ohno-Shosaku T., Kano M. Ca(2+)-assisted receptor-driven endocannabinoid release: mechanisms that associate presynaptic and postsynaptic activities. Curr. Opin. Neurobiol. 2007, 17:360-365.
26. Hashimotodani Y., Ohno-Shosaku T., Yamazaki M., Sakimura K., Kano M. Neuronal protease-activated receptor 1 drives synaptic retrograde signaling mediated by the endocannabinoid 2-arachidonoylglycerol. J. Neurosci. 2011, 31:3104-3109.
27. Hillard C.J., Ho W.S., Thompson J., Gauthier K.M., Wheelock C.E., Huang H., Hammock B.D. Inhibition of 2-arachidonoylglycerol catabolism modulates vasoconstriction of rat middle cerebral artery by the thromboxane mimetic, U-46619. Br. J. Pharmacol. 2007, 152:691-698.
28. Hirasawa M., Schwab Y., Natah S., Hillard C.J., Mackie K., Sharkey K.A., Pittman Q.J. Dendritically released transmitters cooperate via autocrine and retrograde actions to inhibit afferent excitation in rat brain. J. Physiol 2004, 559:611-624.
29. Hudson B.D., Hebert T.E., Kelly M.E. Ligand- and heterodimer-directed signaling of the CB(1) cannabinoid receptor. Mol. Pharmacol. 2010, 77:1-9.
30. Hunyady L., Catt K.J. Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol. Endocrinol. 2006, 20:953-970.
31. Ishac E.J., Jiang L., Lake K.D., Varga K., Abood M.E., Kunos G. Inhibition of exocytotic noradrenaline release by presynaptic cannabinoid CB1 receptors on peripheral sympathetic nerves. Br. J. Pharmacol. 1996, 118:2023-2028.
32. Jin X.H., Okamoto Y., Morishita J., Tsuboi K., Tonai T., Ueda N. Discovery and characterization of a Ca2+-independent phosphatidylethanolamine N-acyltransferase generating the anandamide precursor and its congeners. J. Biol. Chem. 2007, 282:3614-3623.
33. Kano M., Ohno-Shosaku T., Hashimotodani Y., Uchigashima M., Watanabe M. Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev. 2009, 89:309-380.
34. Kim J., Isokawa M., Ledent C., Alger B.E. Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J. Neurosci. 2002, 22:10182-10191.
35. Kola B., Farkas I., Christ-Crain M., Wittmann G., Lolli F., Amin F., Harvey-White J., Liposits Z., Kunos G., Grossman A.B., Fekete C., Korbonits M. The orexigenic effect of ghrelin is mediated through central activation of the endogenous cannabinoid system. PLoS One 2008, 3:e1797.
36. Kreitzer A.C., Regehr W.G. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 2001, 29:717-727.
37. Kurrikoff K., Inno J., Matsui T., Vasar E. Stress-induced analgesia in mice. Evidence for interaction between endocannabinoids and cholecystokinin. Eur. J. Neurosci. 2008, 27:2147-2155.
38. Lau B.K., Vaughan C.W. Muscarinic modulation of synaptic transmission via endocannabinoid signalling in the rat midbrain periaqueductal gray. Mol. Pharmacol. 2008, 74:1392-1398.
39. Lazary J., Juhasz G., Hunyady L., Bagdy G. Personalized medicine can pave the way for the safe use of CB receptor antagonists. Trends Pharmacol. Sci. 2011, 32:270-280.
40. Lazary J., Lazary A., Gonda X., Benko A., Molnar E., Hunyady L., Juhasz G., Bagdy G. Promoter variants of the cannabinoid receptor 1 gene (CNR1) in interaction with 5-HTTLPR affect the anxious phenotype. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2009, 150B:1118-1127.
41. Lee S.H., Soltesz I. Requirement for CB1 but not GABAB receptors in the cholecystokinin mediated inhibition of GABA release from cholecystokinin expressing basket cells. J. Physiol 2011, 589:891-902.
42. Leung D., Saghatelian A., Simon G.M., Cravatt B.F. Inactivation of N-acyl phosphatidylethanolamine phospholipase D reveals multiple mechanisms for the biosynthesis of endocannabinoids. Biochemistry 2006, 45:4720-4726.
43. Li D.P., Pan H.L. Angiotensin II attenuates synaptic GABA release and excites paraventricular-rostral ventrolateral medulla output neurons. J. Pharmacol. Exp. Ther. 2005, 313:1035-1045.
44. Liu J., Mirshahi F., Gao B., Khanolkar A.D., Sanyal A.J., Kunos G., Makriyannis A. Functional CB1 cannabinoid receptors in human vascular endothelial cells. Biochem. J. 2000, 346(Pt. 3):835-840.
45. Liu J., Wang L., Harvey-White J., Osei-Hyiaman D., Razdan R., Gong Q., Chan A.C., Zhou Z., Huang B.X., Kim H.Y., Kunos G. A biosynthetic pathway for anandamide. Proc. Natl. Acad. Sci. USA 2006, 103:13345-13350.
46. Maejima T., Hashimoto K., Yoshida T., Aiba A., Kano M. Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 2001, 31:463-475.
47. Malcher-Lopes R., Di S., Marcheselli V.S., Weng F.J., Stuart C.T., Bazan N.G., Tasker J.G. Opposing crosstalk between leptin and glucocorticoids rapidly modulates synaptic excitation via endocannabinoid release. J. Neurosci. 2006, 26:6643-6650.
48. Marinelli S., Pacioni S., Bisogno T., Di Marzo V., Prince D.A., Huguenard J.R., Bacci A. The endocannabinoid 2-arachidonoylglycerol is responsible for the slow self-inhibition in neocortical interneurons. J. Neurosci. 2008, 28:13532-13541.
49. Mato S., Aso E., Castro E., Martin M., Valverde O., Maldonado R., Pazos A. CB1 knockout mice display impaired functionality of 5-HT1A and 5-HT2A/C receptors. J. Neurochem. 2007, 103:2111-2120.
50. Mechoulam R., Fride E., Ben Shabat S., Meiri U., Horowitz M. Carbachol, an acetylcholine receptor agonist, enhances production in rat aorta of 2-arachidonoyl glycerol, a hypotensive endocannabinoid. Eur. J. Pharmacol. 1998, 362:R1-R3.
51. Miyakubo H., Hayashi Y., Tanaka J. Enhanced response of subfornical organ neurons projecting to the hypothalamic paraventricular nucleus to angiotensin II in spontaneously hypertensive rats. Auton. Neurosci. 2002, 95:131-136.
52. Narushima M., Uchigashima M., Fukaya M., Matsui M., Manabe T., Hashimoto K., Watanabe M., Kano M. Tonic enhancement of endocannabinoid-mediated retrograde suppression of inhibition by cholinergic interneuron activity in the striatum. J. Neurosci. 2007, 27:496-506.
53. Niederhoffer N., Szabo B. Involvement of CB1 cannabinoid receptors in the EDHF-dependent vasorelaxation in rabbits. Br. J. Pharmacol. 1999, 126:1383-1386.
54. Ohno-Shosaku T., Maejima T., Kano M. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 2001, 29:729-738.
55. Ohno-Shosaku T., Matsui M., Fukudome Y., Shosaku J., Tsubokawa H., Taketo M.M., Manabe T., Kano M. Postsynaptic M1 and M3 receptors are responsible for the muscarinic enhancement of retrograde endocannabinoid signalling in the hippocampus. Eur. J. Neurosci. 2003, 18:109-116.
56. Ohno-Shosaku T., Shosaku J., Tsubokawa H., Kano M. Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. Eur. J. Neurosci. 2002, 15:953-961.
57. Okamoto Y., Morishita J., Tsuboi K., Tonai T., Ueda N. Molecular characterization of a phospholipase D generating anandamide and its congeners. J. Biol. Chem. 2004, 279:5298-5305.
58. Okamoto Y., Wang J., Morishita J., Ueda N. Biosynthetic pathways of the endocannabinoid anandamide. Chem. Biodivers. 2007, 4:1842-1857.
59. Pacher, P., Batkai, S., Kunos, G., 2005. Cardiovascular pharmacology of cannabinoids. Handb. Exp. Pharmacol. 599-625.
60. Pacher P., Batkai S., Kunos G. The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol. Rev. 2006, 58:389-462.
61. Parrish J.C., Nichols D.E. Serotonin 5-HT(2A) receptor activation induces 2-arachidonoylglycerol release through a phospholipase c-dependent mechanism. J. Neurochem. 2006, 99:1164-1175.
62. Pertwee R.G., Howlett A.C., Abood M.E., Alexander S.P., Di Marzo V., Elphick M.R., Hansen H.S., Greasley P.J., Kunos G., Mackie K., Mechoulam R., Ross R.A. International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB and CB. Pharmacol. Rev. 2010, 62:588-631.
63. Rademacher D.J., Patel S., Ho W.S., Savoie A.M., Rusch N.J., Gauthier K.M., Hillard C.J. U-46619 but not serotonin increases endocannabinoid content in middle cerebral artery: evidence for functional relevance. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H2694-H2701.
64. Randall M.D., Alexander S.P., Bennett T., Boyd E.A., Fry J.R., Gardiner S.M., Kemp P.A., McCulloch A.I., Kendall D.A. An endogenous cannabinoid as an endothelium-derived vasorelaxant. Biochem. Biophys. Res. Commun. 1996, 229:114-120.
65. Randall M.D., Harris D., Kendall D.A., Ralevic V. Cardiovascular effects of cannabinoids. Pharmacol. Ther. 2002, 95:191-202.
66. Rozenfeld R., Gupta A., Gagnidze K., Lim M.P., Gomes I., Lee-Ramos D., Nieto N., Devi L.A. AT1R-CB(1)R heteromerization reveals a new mechanism for the pathogenic properties of angiotensin II. EMBO J. 2011, 30:2350-2363.
67. Shimizu T., Lu L., Yokotani K. Possible inhibitory roles of endogenous 2-arachidonoylglycerol during corticotropin-releasing factor-induced activation of central sympatho-adrenomedullary outflow in anesthetized rats. Eur. J. Pharmacol. 2010, 641:54-60.
68. Shimizu T., Lu L., Yokotani K. Endogenously generated 2-arachidonoylglycerol plays an inhibitory role in bombesin-induced activation of central adrenomedullary outflow in rats. Eur. J. Pharmacol. 2011, 658:123-131.
69. Shimizu T., Okada S., Yamaguchi N., Arai J., Wakiguchi H., Yokotani K. Brain phospholipase C/diacylglycerol lipase are involved in bombesin BB2 receptor-mediated activation of sympatho-adrenomedullary outflow in rats. Eur. J. Pharmacol. 2005, 514:151-158.
70. Shimizu T., Okada S., Yamaguchi-Shima N., Yokotani K. Brain phospholipase C-diacylglycerol lipase pathway is involved in vasopressin-induced release of noradrenaline and adrenaline from adrenal medulla in rats. Eur. J. Pharmacol. 2004, 499:99-105.
71. Shimizu T., Yokotani K. Bidirectional roles of the brain 2-arachidonoyl-sn-glycerol in the centrally administered vasopressin-induced adrenomedullary outflow in rats. Eur. J. Pharmacol. 2008, 582:62-69.
72. Simon G.M., Cravatt B.F. Endocannabinoid biosynthesis proceeding through glycerophospho-N-acyl ethanolamine and a role for alpha/beta-hydrolase 4 in this pathway. J. Biol. Chem. 2006, 281:26465-26472.
73. Simon G.M., Cravatt B.F. Characterization of mice lacking candidate N-acyl ethanolamine biosynthetic enzymes provides evidence for multiple pathways that contribute to endocannabinoid production in vivo. Mol. Biosyst. 2010, 6:1411-1418.
74. Sun Y.X., Tsuboi K., Okamoto Y., Tonai T., Murakami M., Kudo I., Ueda N. Biosynthesis of anandamide and N-palmitoylethanolamine by sequential actions of phospholipase A2 and lysophospholipase D. Biochem. J. 2004, 380:749-756.
75. Szidonya L., Cserzo M., Hunyady L. Dimerization and oligomerization of G-protein-coupled receptors: debated structures with established and emerging functions. J. Endocrinol. 2008, 196:435-453.
76. To C.T., Bagdy G. Anxiogenic effect of central CCK administration is attenuated by chronic fluoxetine or ipsapirone treatment. Neuropharmacology 1999, 38:279-282.
77. Tucci S.A., Rogers E.K., Korbonits M., Kirkham T.C. The cannabinoid CB1 receptor antagonist SR141716 blocks the orexigenic effects of intrahypothalamic ghrelin. Br. J. Pharmacol. 2004, 143:520-523.
78. Turu G., Simon A., Gyombolai P., Szidonya L., Bagdy G., Lenkei Z., Hunyady L. The role of diacylglycerol lipase in constitutive and angiotensin AT1 receptor-stimulated cannabinoid CB1 receptor activity. J. Biol. Chem. 2007, 282:7753-7757.
79. Turu G., Varnai P., Gyombolai P., Szidonya L., Offertaler L., Bagdy G., Kunos G., Hunyady L. Paracrine transactivation of the CB1 cannabinoid receptor by AT1 angiotensin and other Gq/11 protein-coupled receptors. J. Biol. Chem. 2009, 284:16914-16921.
80. Vandevoorde S., Lambert D.M. The multiple pathways of endocannabinoid metabolism: a zoom out. Chem. Biodivers. 2007, 4:1858-1881.
81. Varma N., Carlson G.C., Ledent C., Alger B.E. Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J. Neurosci. 2001, 21:RC188.
82. Vellani V., Petrosino S., De Petrocellis L., Valenti M., Prandini M., Magherini P.C., McNaughton P.A., Di Marzo V. Functional lipidomics. Calcium-independent activation of endocannabinoid/endovanilloid lipid signalling in sensory neurons by protein kinases C and A and thrombin. Neuropharmacology 2008, 55:1274-1279.
83. Ward, R.J., Pediani, J.D., Milligan, G., 2011. Hetero-multimerization of the cannabinoid CB1 receptor and the orexin OX1 receptor generates a unique complex in which both protomers are regulated by orexin A. J. Biol. Chem.
84. White R., Hiley C.R. A comparison of EDHF-mediated and anandamide-induced relaxations in the rat isolated mesenteric artery. Br. J. Pharmacol. 1997, 122:1573-1584.
85. Wilson R.I., Nicoll R.A. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 2001, 410:588-592.
86. Wilson R.I., Nicoll R.A. Endocannabinoid signaling in the brain. Science 2002, 296:678-682.
87. Yokotani K., Murakami Y., Okada S., Hirata M. Role of brain arachidonic acid cascade on central CRF1 receptor-mediated activation of sympatho-adrenomedullary outflow in rats. Eur. J. Pharmacol. 2001, 419:183-189.
88. Zampronio A.R., Kuzmiski J.B., Florence C.M., Mulligan S.J., Pittman Q.J. Opposing actions of endothelin-1 on glutamatergic transmission onto vasopressin and oxytocin neurons in the supraoptic nucleus. J. Neurosci. 2010, 30:16855-16863.
89. Zhang Z.H., Francis J., Weiss R.M., Felder R.B. The renin-angiotensin-aldosterone system excites hypothalamic paraventricular nucleus neurons in heart failure. Am. J. Physiol. Heart Circ. Physiol. 2002, 283:H423-H433.