The analgesic effect of N-arachidonoyl-serotonin, a FAAH inhibitor and TRPV1 receptor antagonist, associated with changes in rostral ventromedial medulla and locus coeruleus cell activity in rats

Neuropharmacology

Volumn 55, Issue 7, 2008, Pages 1105-1113

  de Novellis, Vito ^a   Palazzo, Enza ^a   Rossi, Francesca ^a   De Petrocellis, Luciano ^b   Petrosino, Stefania ^b   Guida, Francesca ^a   Luongo, Livio ^a   Migliozzi, Annalucia ^a   Cristino, Luigia ^b   Marabese, Ida ^a   Starowicz, Katarzyna ^b   Di Marzo, Vincenzo ^b   Maione, Sabatino ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b CNR   (Italy)

Author keywords

Endocannabinoids; Pain; Periaqueductal grey; Rat; Rostral Ventromedial Medulla; TRPV1

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 5' IODORESINIFERATOXIN; CYCLOHEXYLCARBAMIC ACID 3' CARBAMOYLBIPHENYL 3 YL ESTER; ENDOCANNABINOID; FATTY ACID AMIDASE INHIBITOR; FORMALDEHYDE; KETANSERIN; N ARACHIDONOYLSEROTONIN; PHENTOLAMINE; RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG EFFECT; ENZYME INHIBITION; LOCUS CERULEUS; MALE; MEDULLA OBLONGATA; MICROINJECTION; NOCICEPTION; NONHUMAN; PAIN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; TAIL FLICK TEST; WISTAR RAT;

ADRENERGIC ANTAGONISTS; AMIDOHYDROLASES; ANALGESICS; ANIMALS; ARACHIDONIC ACIDS; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; FORMALDEHYDE; LOCUS COERULEUS; MALE; MEDULLA OBLONGATA; MICROINJECTIONS; OLEIC ACIDS; PAIN MEASUREMENT; PALMITIC ACIDS; RATS; REACTION TIME; SEROTONIN; SEROTONIN ANTAGONISTS; TRPV CATION CHANNELS;

EID: 54049133600     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2008.06.023     Document Type: Article

References (48)

1. Bajic D., Proudfit H.K., and Van Bockstaele E.J. Periaqueductal gray neurons monosynaptically innervate extranuclear noradrenergic dendrites in the rat pericoerulear region. J. Comp. Neurol. 427 (2000) 649-662
2. Bisogno T., Melck D., De Petrocellis L., Bobrov M.Y., Gretskaya N.M., Bezuglov V.V., Sitachitta N., Gerwick W.H., and Di Marzo V. Arachidonoylserotonin and other novel inhibitors of fatty acid amide hydrolase. Biochem. Biophys. Res. Commun. 248 (1998) 515-522
3. Bradshaw H.B., and Walker J.M. The expanding field of cannabimimetic and related lipid mediators. Br. J. Pharmacol. 144 (2005) 459-465
4. Brooks J.W., Pryce G., Bisogno T., Jaggar S.I., Hankey D.J., Brown P., Bridges D., Ledent C., Bifulco M., Rice A.S., Di Marzo V., and Baker D. Arvanil-induced inhibition of spasticity and persistent pain: evidence for therapeutic sites of action different from the vanilloid VR1 receptor and cannabinoid CB(1)/CB(2) receptors. Eur. J. Pharmacol. 439 (2002) 83-92
5. Carlson J.D., Selden N.R., and Heinricher M.M. Nocifensive reflex-related on- and off-cells in the pedunculopontine tegmental nucleus, cuneiform nucleus, and lateral dorsal tegmental nucleus. Brain Res. 1063 (2005) 187-194
6. Cedarbaum J.M., and Aghajanian G.K. Noradrenergic neurons of the locus coeruleus: inhibition by epinephrine and activation by the alpha-antagonist piperoxane. Brain Res. 112 (1976) 413-419
7. Cravatt B.F., Giang D.K., Mayfield S.P., Boger D.L., Lerner R.A., and Gilula N.B. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384 (1996) 83-87
8. Cristino L., de Petrocellis L., Pryce G., Baker D., Guglielmotti V., and Di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139 (2006) 1405-1415
9. De Novellis V., Mariani L., Palazzo E., Vita D., Marabese I., Scafuro M., Rossi F., and Maione S. Periaqueductal grey CB1 cannabinoid and metabotropic glutamate subtype 5 receptors modulate changes in rostral ventromedial medulla neuronal activities induced by subcutaneous formalin in the rat. Neuroscience 134 (2005) 269-281
10. Di Marzo V., Blumberg P.M., and Szallasi A. Endovanilloid signaling in pain. Curr. Opin. Neurobiol. 12 (2002) 372-379
11. Dubuisson D., and Dennis S.G. The formalin test: a quantitative study of the analgesic effect of morphine, meperidine and brain stem stimulation in rats and cats. Pain 4 (1977) 161-174
12. Ennis M., Behbehani M., Shipley M.T., Van Bockstaele E.J., and Aston-Jones G. Projections from the periaqueductal gray to the rostromedial pericoerulear region and nucleus locus coeruleus: anatomic and physiologic studies. J. Comp. Neurol. 306 (1991) 480-494
13. Fields H.L., Bry J., Hentall I., and Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heart. J. Neurosci. 3 (1983) 2545-2552
14. Fields H.L., Vanegas H., Hentall I.D., and Zorman G. Evidence that disinhibition of brain stem neurones contributes to morphine analgesia. Nature 306 (1983) 684-686
15. Fields H.L., Heinricher M.M., and Mason P. Neurotransmitters in nociceptive modulatory circuits. Annu. Rev. Neurosci. 14 (1991) 219-245
16. Freitas R.L., Ferreira C.M., Ribeiro S.J., Carvalho A.D., Elias-Filho D.H., Garcia-Cairasco N., and Coimbra N.C. Intrinsic neural circuits between dorsal midbrain neurons that control fear-induced responses and seizure activity and nuclei of the pain inhibitory system elaborating postictal antinociceptive processes: a functional neuroanatomical and neuropharmacological study. Exp. Neurol. 191 (2005) 225-242
17. Fu J., Oveisi F., Gaetani S., Lin E., and Piomelli D. Oleoylethanolamide, an endogenous PPAR-alpha agonist, lowers body weight and hyperlipidemia in obese rats. Neuropharmacology 48 (2005) 1147-1153
18. Holt S., Comelli F., Costa B., and Fowler C.J. Inhibitors of fatty acid amide hydrolase reduce carrageenan-induced hind paw inflammation in pentobarbital-treated mice: comparison with indomethacin and possible involvement of cannabinoid receptors. Br. J. Pharmacol. 146 (2005) 467-476
19. Iversen L., and Chapman V. Cannabinoids: a real prospect for pain relief?. Curr. Opin. Pharmacol. 2 (2002) 50-55
20. Jayamanne A., Greenwood R., Mitchell V.A., Aslan S., Piomelli D., and Vaughan C.W. Actions of the FAAH inhibitor URB597 in neuropathic and inflammatory chronic pain models. Br. J. Pharmacol. 147 (2006) 281-288
21. Kohno M., Hasegawa H., Inoue A., Muraoka M., Miyazaki T., Oka K., and Yasukawa M. Identification of N-arachidonylglycine as the endogenous ligand for orphan G-protein-coupled receptor GPR18. Biochem. Biophys. Res. Commun. 347 (2006) 827-832
22. Lichtman A.H., Shelton C.C., Advani T., and Cravatt B.F. Mice lacking fatty acid amide hydrolase exhibit a cannabinoid receptor-mediated phenotypic hypoalgesia. Pain 109 (2004) 319-327
23. Lichtman A.H., Leung D., Shelton C.C., Saghatelian A., Hardouin C., Boger D.L., and Cravatt B.F. Reversible inhibitors of fatty acid amide hydrolase that promote analgesia: evidence for an unprecedented combination of potency and selectivity. J. Pharmacol. Exp. Ther. 311 (2004) 441-448
24. Maione S., Bisogno T., de Novellis V., Palazzo E., Cristino L., Valenti M., Petrosino S., Guglielmotti V., Rossi F., and Di Marzo V. Elevation of endocannabinoid levels in the ventrolateral periaqueductal grey through inhibition of fatty acid amide hydrolase affects descending nociceptive pathways via both cannabinoid receptor type 1 and transient receptor potential vanilloid type-1 receptors. J. Pharmacol. Exp. Ther. 316 (2006) 969-982
25. Maione S., De Petrocellis L., de Novellis V., Moriello A.S., Petrosino S., Palazzo E., Rossi F.S., Woodward D.F., and Di Marzo V. Analgesic actions of N-arachidonoyl-serotonin, a fatty acid amide hydrolase inhibitor with antagonistic activity at vanilloid TRPV1 receptors. Br. J. Pharmacol. 150 (2007) 766-781
26. McGaraughty S., Chu K.L., Bitner R.S., Martino B., El Kouhen R., Han P., Nikkel A.L., Burgard E.C., Faltynek C.R., and Jarvis M.F. Capsaicin infused into the PAG affects rat tail flick responses to noxious heat and alters neuronal firing in the RVM. J. Neurophysiol. 90 (2003) 2702-2710
27. Meng I.D., and Johansen J.P. Antinociception and modulation of rostral ventromedial medulla neuronal activity by local microinfusion of a cannabinoid receptor agonist. Neuroscience 124 (2004) 685-693
28. Mezey E., Tóth Z.E., Cortright D.N., Arzubi M.K., Krause J.E., Elde R., Guo A., Blumberg P.M., and 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. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 3655-3660
29. Moreau J.L., and Fields H.L. Evidence for GABA involvement in midbrain control of medullary neurons that modulate nociceptive transmission. Brain Res. 397 (1986) 37-46
30. Ortar G., Cascio M.G., De Petrocellis L., Morera E., Rossi F., Schiano-Moriello A., Nalli M., de Novellis V., Woodward D.F., Maione S., and Di Marzo V. New N-arachidonoylserotonin analogues with potential "dual" mechanism of action against pain. J. Med. Chem. 50 (2007) 6554-6569
31. Palazzo E., de Novellis V., Marabese I., Cuomo D., Rossisca F., Berrino L., Rossi F., and Maione S. Interaction between vanilloid and glutamate receptors in the central modulation of nociception. Eur. J. Pharmacol. 439 (2002) 69-75
32. Palazzo E., Rossi F., and Maione S. Role of TRPV1 receptors in descending modulation of pain. Mol. Cell. Endocrinol 286 (2008) S79-S83
33. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, New York
34. Re G., Barbero R., Miolo A., and Di Marzo V. Palmitoylethanolamide, endocannabinoids and related cannabimimetic compounds in protection against tissue inflammation and pain: potential use in companion animals. Vet. J. 173 (2007) 21-30
35. Rea K., Roche M., and Finn D.P. Supraspinal modulation of pain by cannabinoids: the role of GABA and glutamate. Br. J. Pharmacol. 152 (2007) 633-648
36. Reiner K., Sukhotinsky I., and Devor M. Mesopontine tegmental anesthesia area projects independently to the rostromedial medulla and to the spinal cord. Neuroscience 146 (2007) 1355-1370
37. Sajedianfard J., Khatami S., Semnanian S., Naghdi N., and Jorjani M. In vivo measurement of noradrenaline in the locus coeruleus of rats during the formalin test: a microdialysis study. Eur. J. Pharmacol. 512 (2005) 153-156
38. Sandkuhler J., and Gebhart G.F. Relative contributions of the nucleus raphe magnus and adjacent medullary reticular formation to the inhibition by stimulation in the periaqueductal grey of a spinal nociceptive reflex in the pentobarbital-anaesthetized rat. Brain Res. 305 (1984) 77-87
39. Sasaki A., Takasaki I., Andoh T., Nojima H., Shiraki K., and Kuraishi Y. Roles of alpha-adrenoceptors and sympathetic nerve in acute herpetic pain induced by herpes simplex virus inoculation in mice. J. Pharmacol. Sci. 92 (2003) 329-336
40. Starowicz K., Nigam S., and Di Marzo V. Biochemistry and pharmacology of endovanilloids. Pharmacol. Ther. 114 (2007) 13-33
41. Starowicz K., Maione S., Cristino L., Palazzo E., Marabese I., Rossi F., de Novellis V., and Di Marzo V. Tonic endovanilloid facilitation of glutamate release in brainstem descending antinociceptive pathway. J. Neurosci. 27 (2007) 13739-13749
42. Suplita R.L., Farthing J.N., Gutierrez T., and Hohmann A.G. Inhibition of fatty-acid amide hydrolase enhances cannabinoid stress-induced analgesia: sites of action in the dorsolateral periaqueductal gray and rostral ventromedial medulla. Neuropharmacology 49 (2005) 1201-1209
43. Szallasi A., and Blumberg P.M. Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol. Rev. 51 (1999) 159-212
44. van der Stelt M., and Di Marzo V. Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur. J. Biochem. 271 (2004) 1827-1834
45. Tortorici V., and Morgan M.M. Comparison of morphine and kainic acid microinjections into identical PAG sites on the activity of RVM neurons. J. Neurophysiol. 88 (2002) 1707-1715
46. Ugedo L., Pineda J., Ruiz-Ortega J.A., and Martin-Ruiz R. Stimulation of Locus Coeruleus neurons by non-I1/I2-type imidazoline receptors: an in vivo and in vitro electrophysiological study. Br. J. Pharmacol. 125 (1998) 1685-1694
47. Zhang Z.H., Yang S.W., Chen J.Y., Xie Y.F., Qiao J.T., and Dafny N. Interaction of serotonin and norepinephrine in spinal antinociception. Brain Res. Bull. 38 (1995) 167-171
48. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110