Cannabinoid modulation of sensory neurotransmission via cannabinoid and vanilloid receptors: Roles in regulation of cardiovascular function

Life Sciences

Volumn 71, Issue 22, 2002, Pages 2577-2594

  Ralevic, Vera ^a   Kendall, David A ^a   Randall, Michael D ^a   Smart, Darren ^b  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Anandamide; Cannabinoids; Sensory nerves; Vanilloids; Vasorelaxation

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 3 ISOPROPYLAMINO 1 (7 METHYL 4 INDANYLOXY) 2 BUTANOL; 4 (1,1 DIMETHYLHEPTYL) 1',2',3',4',5',6' HEXAHYDRO 2,3' DIHYDROXY 6' (3 HYDROXYPROPYL)BIPHENYL; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; ANANDAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CAPSAICIN; CAPSAZEPINE; DEXANABINOL; METHANANDAMIDE; NEUROTRANSMITTER; OLVANIL; POTASSIUM CHANNEL; RECOMBINANT PROTEIN; RIMONABANT; RUTHENIUM RED; UNCLASSIFIED DRUG; VANILLOID RECEPTOR;

CARDIOVASCULAR FUNCTION; DRUG ACTIVITY; DRUG EFFECT; DRUG INHIBITION; DRUG POTENCY; EFFERENT NERVE; GAP JUNCTION; HOMEOSTASIS; HUMAN; HYPERPOLARIZATION; HYPOTENSION; NERVE ENDING; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSORY NERVE; SHORT SURVEY; SMOOTH MUSCLE; VASCULAR RESISTANCE; VASODILATATION;

EID: 0037131531     PISSN: 00243205     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0024-3205(02)02086-6     Document Type: Review

References (114)

1. Barja F., Mathison R., Huggel H. Substance P-containing nerve fibres in large peripheral blood vessels of the rat. Cell and Tissue Research. 229:1983;411-422.
2. Wharton J., Gulbenkian S., Mulderry P.K., Ghatei M.A., McGregor G.P., Bloom S.R., Polak J.M. Capsaicin induces a depletion of calcitonin gene-related peptide (CGRP)-immunoreactive nerves in the cardiovascular system of the guinea pig and rat. Journal of the Autonomic Nervous System. 16:1986;289-309.
3. Maggi C.A., Meli A. The sensory-efferent function of capsaicin-sensitive sensory neurons. General Pharmacology. 19(1):1988;1-43.
4. Holzer P. Peptidergic sensory neurons in the control of vascular functions: mechanisms and significance in the cutaneous and splanchnic vascular beds. Reviews in Physiology, Biochemistry and Pharmacology. 121:1992;49-146.
5. Lundberg J.M. Pharmacology of cotransmission in the autonomic nervous system: integrative aspects on amines, neuropeptides, adenosine triphosphate, amino acids and nitric oxide. Pharmacological Reviews. 48:1996;113-178.
6. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 389:1997;816-824.
7. Pertwee R. The evidence for the existence of cannabinoid receptors. General Pharmacology. 24:1993;811-824.
8. 2 receptors. Pharmacology and Therapeutics. 74:1997;129-180.
9. 1 cannabinoid receptors. Life Sciences. 65:1999;597-605.
10. Zygmunt P.M., Petersson J., Andersson D.A., Chuang H., Sørgård M., Di Marzo V., Julius D., Högestätt E.D. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature. 400:1999;452-457.
11. Smart D., Gunthorpe M.J., Jerman J.C., Nasir S., Gray J., Muir A.I., Chambers J.K., Randall A.D., Davis J.B. The endogenous lipid anandamide is a full agonist at the human vanilloid receptor (hVR1). British Journal of Pharmacology. 129(2):2000;227-230.
12. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science. 288:2000;306-313.
13. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., Harries M.H., Latcham J., Claphams C., Atkinson K., Hughes S.A., Rance K., Grau E., Harper A.J., Pugh P.L., Rogers D.C., Bingham S., Randall A.D., Sheardown S.A. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature. 405:2000;183-187.
14. Caterina M.J., Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annual Review of Neuroscience. 24:2001;487-517.
15. Szallasi A., Blumberg P.M. Vanilloid (capsaicin) receptors and mechanisms. Pharmacological Reviews. 51:1999;159-211.
16. Mezey E., Toth Z.E., Cortright D.N., Arzubi M.K., Krause J.E., Elde R., Guo A., Blumberg P.M., Szallasi A. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proceeding of the National Academy of Sciences USA. 97:2000;3655-3660.
17. Ralevic V., Kendall D.A., Randall M.D., Zygmunt P.M., Movahed P., Högestätt E.D. Vanilloid receptors on capsaicin-sensitive sensory nerves mediate relaxation to methanandamide in the rat isolated mesenteric arterial bed and small mesenteric arteries. British Journal of Pharmacology. 130:2000;1483-1488.
18. Malinowska B., Kwolek G., Gothert M. Anandamide and methanandamide induce both vanilloid VR1- and cannabinoid CB1 receptor-mediated changes in heart rate and blood pressure in anaesthetized rats. Naunyn-Schmiedebergs Archives of Pharmacology. 364:2001;562-569.
19. DiMarzo V., Bisogno T., Melck D., Ross R., Brockie H., Stevenson L., Pertwee R., DePetrocellis L. Interactions between synthetic vanilloids and the endogenous cannabinoid system. FEBS Letters. 436:1998;449-454.
20. Beltramo M., Piomelli D. Anandamide transport inhibition by the vanilloid agonist olvanil. European Journal of Pharmacology. 364:1999;75-78.
21. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., Gibson D., Mandelbaum A., Etinger A., Mechoulam R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science. 258:1992;1946-1949.
22. Ralevic V., Kendall D.A., Jerman J.C., Middlemiss D.N., Smart D. Cannabinoid activation of recombinant and endogenous vanilloid receptors. European Journal of Pharmacology. 424:2001;211-219.
23. Smart D., Jerman J.C., Gunthorpe M.J., Brough S.J., Ranson J., Cairns W., Hayes P.D., Randall A.D., Davis J.B. Characterisation using FLIPR of human vanilloid VR1 receptor pharmacology. European Journal of Pharmacology. 417:2001;51-58.
24. Pertwee R.G. Cannabinoid receptors and pain. Progress in Neurobiology. 63:2001;569-611.
25. Di Marzo V., Bisogno T., De Petrocellis L., Melck D., Orlando P., Wagner J.A., Kunos G. Biosynthesis and inactivation of the endocannabinoid 2-arachidonoylglycerol in circulating and tumoral macrophages. European Journal of Biochemistry. 264:1999;258-267.
26. Szolcsányi J. Are cannabinoids endogenous ligands for the VR1 capsaicin receptor. Trends in Pharmacological Sciences. 21(1):2000;41-42.
27. Szolcsanyi J. Anandamide and the question of its functional role for activation of capsaicin receptors. Trends in Pharmacological Sciences. 21:2000;203-204.
28. Zygmunt P.M., Julius D., Di Marzo V., Högestätt E.D. Anandamide - the other side of the coin. Trends in Pharmacological Sciences. 21(2):2000;43-44.
29. Smart D., Jerman J.C. Anandamide: an endogenous activator of the vanilloid receptor. Trends in Pharmacological Sciences. 21:2000;134.
30. DiMarzo V., Bisogno T., DePetrocellis L. Anandamide: some like it hot. Trends in Pharmacological Sciences. 22:2001;346-349.
31. Jerman J.C., Brough S.J., Prinjha R., Harries M.H., Davis J.B., Smart D. Characterization using FLIPR of rat vanilloid receptor (rVR1) pharmacology. British Journal of Pharmacology. 130:2000;916-922.
32. Ralevic V., Kendall D.A., Jerman J.C., Davis J.B., Middlemiss D.N., Smart D. Low pH modulation of recombinant vanilloid receptors and perivascular capsaicin-sensitive sensory neurotransmission. Autonomic Neuroscience. 88:2001;36-44.
33. Vellani V., Mapplebeck S., Moriondo A., Davis J.B., McNaughton P.A. Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. Journal of Physiology. 534:2001;813-825.
34. Olah Z., Karai L., Iadarola M.J. Anandamide activates vanilloid receptor 1 (VR1) at acidic pH in dorsal root ganglia neurons and cells ectopically expressing VR1. Journal of Biological Chemistry. 276:2001;31163-31170.
35. Hayes P., Meadows H.J., Gunthorpe M.J., Harries M.H., Duckworth M.D., Cairns W., Harrison D.C., Clarke C.E., Ellington K., Prinjha R.K., Barton A.J.L., Medhurst A.D., Smith G.D., Topp S., Murdock P., Sanger G.J., Terrett J., Jenkins O., Benham C.D., Randall A.D., Gloger I.S., Davis J.B. Cloning and functional expression of a human orthologue of rat vanilloid receptor-1. Pain. 88:2001;207-212.
36. Premkumar L.S., Ahern G.P. Induction of vanilloid receptor channel activity by protein kinase C. Nature. 408:2000;985-990.
37. DePetrocellis L., Harrison S., Bisogno T., Tognetto M., Brandi I., Smith G.D., Cremion C., Davis J.B., Geppetti P., DiMarzo V. The vanilloid receptor (VR1)-mediated effects of anandamide are potently enhanced by the cAMP-dependent protein kinase. Journal of Neurochemistry. 77:2001;1660-1663.
38. Sprague J., Harrison C., Rowbotham D.J., Smart D., Lambert D.G. Temperature-dependent activation of recombinant rat vanilloid VR1 receptors expressed in HEK293 cells by capsaicin and anandamide. European Journal of Pharmacology. 423:2001;121-125.
39. DePetrocellis L., Davis J.B., DiMarzo V. Palmitoylethanolamide enhances anandamide stimulation of human vanilloid VR1 receptors. FEBS Letters. 506:2001;253-256.
40. Bisogno T., Hanus L., DePetrocellis L., Tchilibon S., Ponde D.E., Brandi I., Moriello A.S., Davis J.B., Mechoulam R., DiMarzo V. Molecular targets for cannabidiol and its synthetic analogues. British Journal of Pharmacology. 134:2001;845-852.
41. Zygmunt P.M., Chuang H.H., Movahed P., Julius D., Högestätt E.D. The anandamide transport inhibitor AM404 activates vanilloid receptors. European Journal of Pharmacology. 396:2000;39-42.
42. Melck D., Bisogno T., DePetrocellis L., Chaung H.H., Julius D., Bifulco M., DiMarzo V. Unsaturated long-chain N-acyl-vanillyl-amides (N-VAMs): vanilloid receptor ligands that inhibit anandamide-facilitated transport and bind to CB1 cannabinoid receptors. Biochemical and Biophysical Research Communications. 262:1999;275-284.
43. DePetrocellis L., Bisogno T., Davis J.B., Pertwee R.G., DiMarzo V. Overlap between the ligand recognition properties of the anandamide transporter and the VR1 vanilloid receptor: inhibitors of anandamide uptake with negligible capsaicin-like activity. FEBS Letters. 483:2000;52-56.
44. DiMarzo V., Bisogno T., DePetrocellis L., Brandi I., Jefferson R.G., Winckler R.L., Davis J.B., Dasse O., Mahadevan A., Razdan R.K., Martin B.R. Highly selective CB1 cannabinoid receptor ligands and novel CB1/VR1 vanilloid receptor "hybrid" ligands. Biochemical and Biophysical Research Communications. 281:2001;444-451.
45. DiMarzo V., Breivogel C., Bisogno T., Melck D., Patrick G., Tao Q., Szallasi A., Razadan R.K., Martin B.R. Neurobehavioral activity in mice of N-vanillyl-arachidonyl-amide. European Journal of Pharmacology. 406:2000;363-374.
46. DiMarzo V., Lastres-Becker I., Bisogno T., DePetrocellis L., Milone A., Davis J.B., Fernandez-Ruiz J.J. Hypolocomotor effects in rats of capsaicin and two long chain capsaicin homologues. European Journal of Pharmacology. 420:2001;123-131.
47. Ross R.A., Gibson T.M., Brockie H.C., Leslie M., Pashmi G., Craib S.J., DiMarzo V., Pertwee R.G. Structure-activity relationship for the endogenous cannabinoid, anandamide, and certain of its analogues at vanilloid receptors in transfected cells and vas deferens. British Journal of Pharmacology. 132:2001;631-640.
48. Jung J., Hwang S.W., Kwak J., Lee S.-Y., Kang C.-J., Kim W.B., Kim D., Oh U. Capsaicin binds to the intracellular domain of the capsaicin-activated ion channel. Journal of Neuroscience. 19:1999;529-538.
49. DePetrocellis L., Bisogno T., Maccarone M., Dais J.B., Finazzi-Agro A., DiMarzo V. The activity of anandamide at vanilloid VR1 receptors requires facilitated transport across the cell membrane and is limited by intracellular metabolism. Journal of Biological Chemistry. 276:2001;12856-12863.
50. Craib S.J., Ellington H.C., Pertwee R.G., Ross R.A. A possible role of lipoxygenase in the activation of vanilloid receptors by anandamide in the guinea-pig bronchus. British Journal of Pharmacology. 134:2001;30-37.
51. Kunos G., Batkai S. Novel physiological functions of endocannabinoids as revealed through the use of mutant mice. Neurochemical Research. 26:2001;1015-1021.
52. Hwang S.W., Cho H., Kwak J., Lee S.-Y., Kang C.-J., Jung J., Cho S., Min K.H., Suh Y.-G., Kim D., Oh U. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proceeding of the National Academy of Sciences USA. 97:2000;6155-6160.
53. Piomelli D. The ligand that came from within. Trends in Pharmacological Sciences. 22:2001;17-19.
54. Szallasi A., DiMarzo V. New perspectives on enigmatic vanilloid receptors. Trends in Neurosciences. 23:2000;491-497.
55. Tucker R.C., Kagaya M., Page C.P., Spina D. The endogenous cannabinoid agonist, anandamide stimulates sensory nerves in guinea-pig airways. British Journal of Pharmacology. 132:2001;1127-1135.
56. Mang C.F., Erbelding D., Kilbinger H. Differential effects of anandamide on acetylcholine release in the guinea pig ileum mediated via vanilloid and non-CB1 cannabinoid receptors. British Journal of Pharmacology. 134:2001;161-167.
57. Gauldie S.D., McQueen D.S., Pertwee R., Chessell I.P. Anandamide activates peripheral nociceptors in normal and arthritic rat knee joints. British Journal of Pharmacology. 132:2001;617-621.
58. Szoke E., Balla Z., Csernoch L., Czeh G., Szolcsanyi J. Interacting effects of capsaicin and anandamide on intracellular calcium in sensory neurones. Neuroreport. 11:2000;1949-1952.
59. Al-Hayani A., Wease K.N., Ross R.A., Pertwee R.G., Davies S.N. The endogenous cannabinoid anandamide activates vanilloid receptors in the rat hippocampal slice. Neuropharmacology. 41:2001;1000-1005.
60. Maccarrone M., Lorenzon T., Bari M., Melino G., Finazzi-Agro A. Anandamide induces apoptosis in human cells via vanilloid receptors- evidence for a protective role of cannabinoid receptors. Journal of Biological Chemistry. 275:2000;31938-31945.
61. Jacobsson S.O.P., Wallin T., Fowler C.F. Inhibition of rat C6 glioma cell proliferation by endogenous and synthetic cannabinoids. Relative involvement of cannabinoid and vanilloid receptors. Journal of Pharmacology and Experimental Therapeutics. 299:2001;951-959.
62. Morisset V., Ahluwalia J., Nagy I., Urban L. Possible mechanisms of cannabinoid-induced antinociception in the spinal cord. European Journal of Pharmacology. 429:2001;93-100.
63. Tognetto M., Amadesi S., Harrison S., Creminon C., Trevisani M., Carreras M., Matera M., Geppetti P., Bianchi A. Anandamide excites central terminals of dorsal root ganglion neurons via vanilloid receptor-1 activation. Journal of Neuroscience. 21:2001;1104-1109.
64. Harris D., McCulloch A.I., Kendall D.A., Randall M.D. Characterization of vasorelaxant responses to anandamide in the rat mesenteric arterial bed. Journal of Physiology. 539:2002;893-902.
65. Randall M.D., Harris D., Darker I.T., Millns P.J., Kendall D.A. Endocannabinoids: endothelium-derived vasodilators. Vanhoutte P.M. Endothelium-dependent hyperpolarizations. 1999;149-155 Harcourt, Amsterdam.
66. Salio C, Fischer J, Franzoni MF, Conrathf M. Pre- and postsynaptic localizations of the CB1 cannabinoid receptor in the dorsal horn of the rat spinal cord. Neuroscience [in press].
67. Hohmann A.G., Herkenham M. Localization of central cannabinoid CB1 receptor messenger RNA in neuronal subpopulations of rat dorsal root ganglia: a double-label in situ hybridization study. Neuroscience. 90:1999;923-931.
68. Hohmann A.G., Herkenham M. Cannabinoid receptors undergo axonal flow in sensory nerves. Neuroscience. 92:1999;1171-1175.
69. Ahluwalia J., Urban L., Capogna M., Bevan S., Nagy I. Cannabinoid 1 receptors are expressed in nociceptive primary sensory neurons. Neuroscience. 100:2000;685-688.
70. Ross R.A., Coutts A.A., McFarlane S.M., Anavi-Goffer S., Irving A.J., Pertwee R.G., MacEwan D.J., Scott R.H. Actions of cannabinoid receptor ligands on rat cultured sensory neurones: implications for antinociception. Neuropharmacology. 40:2001;221-232.
71. Millns P.J., Chapman V., Kendall D.A. Cannabinoid inhibition of the capsaicin-induced calcium response in rat dorsal root ganglion neurones. British Journal of Pharmacology. 132:2001;969-971.
72. 2+ responses in adult rat dorsal root ganglion neurones. British Journal of Pharmacology. 2002;. [in press].
73. 2 receptors. Proceedings of the National Academy of Sciences. 96(24):1999;14136-14141.
74. Bouaboula M., Perrachon S., Canant X., Rinaldi-Carmona M., Portier M., Barth F., Calandra B., Pecceu F., Lupker J., Maffrand J.P., Le Fur G., Castelas P. A selective inverse agonist for central cannabinoid receptors inhibits mitogen-activated protein kinase activation stimulated by insulin or insulin-like growth factor 1: evidence for a new model of receptor/ligand interactions. Journal of Biological Chemistry. 272:1997;22330-22339.
75. MacLennan S.J., Reynen P.H., Kwan J., Bonhaus D.W. Evidence for inverse agonism of SR141716A at human recombinant cannabinoid CB1 and CB2 receptors. British Journal of Pharmacology. 124:1998;619-622.
76. 1 cannabinoid receptor activity. Molecular Pharmacology. 54:1998;1064-1072.
77. Coutts A.A., Brewster N., Ingram T., Razdan R.K., Pertwee R.G. Comparison of novel cannabinoid partial agonists and SR141716A in the guinea-pig small intestine. British Journal of Pharmacology. 129:2000;645-652.
78. 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. British Journal of Pharmacology. 123(5):1998;968-974.
79. White R., Hiley C.R. A comparison of EDHF-mediated and anandamide-induced relaxations in the rat isolated mesenteric artery. British Journal of Pharmacology. 122(8):1997;1573-1584.
80. Chaytor A.T., Martin P.E.M., Evans W.H., Randall M.D., Griffith T.M. The endothelial component of cannabinoid-induced relaxation in rabbit mesenteric artery depends on gap junctional communication. Journal of Physiology (Lond). 520(2):1999;539-550.
81. Richardson J.D., Kilo S., Hargreaves K.M. Cannabinoids reduce hyperalgesia and inflammation via interaction with peripheral CB1 receptors. Pain. 75(1):1998;111-119.
82. Kawasaki H., Takasaki K., Saito A., Goto K. Calcitonin gene-related peptide acts as a novel vasodilator neurotransmitter in mesenteric resistance vessels of the rat. Nature. 335:1988;165-167.
83. Ralevic V., Kendall D.A. Cannabinoid inhibition of capsaicin-sensitive sensory neurotransmission in the rat mesenteric arterial bed. European Journal of Pharmacology. 418:2001;117-125.
84. Duncan M., Kendall D.A., Ralevic V. Effect of WIN55,212, a cannabinoid receptor agonist, on sensory neurotransmission in the rat isolated mesenteric arterial bed. British Journal of Pharmacology. 2001;. [in press].
85. Duncan M., Kendall D.A., Ralevic V. CP55,940 inhibits capsaicin-sensitive sensory neurotransmission via CB1-like receptors in the rat isolated mesenteric arterial bed. British Journal of Pharmacology. 2002;. [in press].
86. 2+-induced relaxation. Journal of Pharmacology and Experimental Therapeutics. 289(1):1999;245-250.
87. 2+ induced relaxation in CB1 deficient mice. Hypertension. 39:2002;251-257.
88. Di Marzo V., Melck D., Bisogno T., De Petrocellis L. Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends in the Neurosciences. 21:1998;521-528.
89. Lake K.D., Martin B.R., Kunos G., Varga K. Cardiovascular effects of anandamide in anaesthetized and conscious normotensive rats. Hypertension. 29(5):1997;1204-1210.
90. Varga K., Lake K., Martin B.R., Kunos G. Novel antagonist implicates CB1 cannabinoid receptor in the hypotensive action of anandamide. European Journal of Pharmacology. 278(3):1995;279-283.
91. Varga K., Lake K.D., Huangfu D., Guyenet P.G., Kunos G. Mechanism of the hypotensive action of anandamide in anaesthetised rats. Hypertension. 28(4):1996;682-686.
92. 8-tetrahydrocannabinol-dimethylheptyl in rats. Journal of Cardiovascular Pharmacology. 28(2):1996;332-336.
93. Gardiner S.M., March J.E., Kemp P.A., Bennett T. Complex regional haemodynamic effects of anandamide in conscious rats. British Journal of Pharmacology. 2002;. [in press].
94. Zhou X.F., Livett B.G. Capsaicin-sensitive sensory neurons are involved in the plasma catecholamine response to selective stressors. Journal of Physiology. 433:1991;393-407.
95. 1 receptor knockout mice. Science. 283(5400):1999;401-404.
96. White R., Ho W.S.V., Bottrill F.E., Ford W.R., Hiley C.R. Mechanisms of anandamide-induced vasorelaxation in rat isolated coronary arteries. British Journal of Pharmacology. 134:2001;921-929.
97. Smith P.J.W., McQueen D.S. Anandamide induces cardiovascular and respiratory reflexes via vasosensory nerves in the anaesthetized rat. British Journal of Pharmacology. 134:2001;655-663.
98. Vanheel B., Van de Voorde J. Regional differences in anandamide-and methanandamide-induced membrane potential changes in rat mesenteric arteries. Journal of Pharmacology and Experimental Therapeutics. 296:2001;322-328.
99. 9-THC dilation of cerebral arterioles is blocked by indomethacin. American Journal of Physiology (Heart Circ). 38(6):1995;H1859-H1864.
100. Randall M.D., Harris D., Kendall D.A., Ralevic V. Cardiovascular effects of cannabinoids. Pharmacology and Therapeutics. 2002;. [in press].
101. Randall M.D., Alexander S.P.H., 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. Biochemical and Biophysical Research Communications. 229(1):1996;114-120.
102. Pratt P.F., Hillard C.J., Edgemond W.S., Campbell W.B. N-arachidonylethanolamide relaxation of bovine coronary artery is not mediated by CB1 cannabinoid receptor. American Journal of Physiology (Heart Circ). 43(1):1998;H375-H381.
103. Deutsch D.G., Goligorsky M.S., Schmid P.G., Krebsbach R.J., Schmid H.H.O., Das S.K., Dey S.K., Arreaza G., Thorup C., Stefano G., Moore L.C. Production and physiological actions of anandamide in the vasculature of the rat kidney. Journal of Clinical Investigation. 100(6):1997;1538-1546.
104. Maccarrone M., Bari M., Lorenzon T., Bisogno T., Di Marzo V., Finazzi-Agro A. Anandamide uptake by human endothelial cells and its regulation by nitric oxide. Journal of Biological Chemistry. 275(41):2000;13484-13492.
105. Plane F., Holland M., Waldron G.J., Garland C.J., Boyle J.P. Evidence that anandamide and EDHF act via different mechanisms in rat isolated mesenteric arteries. British Journal of Pharmacology. 121(8):1997;1509-1512.
106. Zygmunt P.M., Högestätt E.D., Waldeck K., Edwards G., Kirkup A.J., Weston A.H. Studies on the effects of anandamide in the rat hepatic artery. British Journal of Pharmacology. 122(8):1997;1679-1686.
107. Randall M.D., Kendall D.A. Anandamide and endothelium-derived hyperpolarizing factor act via a common vasorelaxant mechanism in rat mesentery. European Journal of Pharmacology. 346(1):1998;51-53.
108. Chen Y., McCarron R.M., Ohara Y., Bembry J., Azzam N., Lenz F.A., Shohmani E., Mechoulam R., Spatz M. Human brain capillary endothelium - 2-arachidonoglycerol (endocannabinoid) interacts with endothelin-1. Circulation Research. 87(4):2000;323-327.
109. Chaytor A.T., Evans W.H., Griffith T.M. Central role of heterocellular gap junctional communication in endothelium-dependent relaxations of rabbit arteries. Journal of Physiology (Lond). 508(2):1998;561-573.
110. +-relaxation. European Journal of Pharmacology. 401(1-2):2000;119-128.
111. Wagner J.A., Varga K., Jarai Z., Kunos G. Mesenteric vasodilation mediated by endothelial anandamide receptors. Hypertension. 33(1):1999;429-434.
112. 2 cannabinoid receptor-independent mechanism. Journal of Neuroscience. 22:2002;4720-4727.
113. Bonhaus D.W., Chang L.K., Kwan J., Martin G.R. Dual activation and inhibition of adenylyl cyclase by cannabinoid receptor agonists: evidence for agonist-specific trafficking of intracellular responses. Journal of Pharmacology and Experimental Therapeutics. 287(3):1998;884-888.
114. Gonsiorek W., Linn C., Fan X., Narula S., Lundell D., Hipkin R.W. Endocannabinoid 2-arachidonyl glycerol is a full agonist through human type 2 cannabinoid receptor: antagonism by anandamide. Molecular Pharmacology. 57(5):2000;1045-1050.