Functional interaction between TRPV1 and μ-opioid receptors in the descending antinociceptive pathway activates glutamate transmission and induces analgesia

Journal of Neurophysiology

Volumn 101, Issue 5, 2009, Pages 2411-2422

  Maione, Sabatino ^a   Starowicz, Katarzyna ^b,c   Cristino, Luigia ^b   Guida, Francesca ^a   Palazzo, Enza ^a   Luongo, Livio ^a   Rossi, Francesca ^a   Marabese, Ida ^a   De Novellis, Vito ^a   Di Marzo, Vincenzo ^b,c  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b CNR   (Italy)

^c INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 5' IODO RESINIFERATOXIN; CAPSAICIN; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; GLUTAMIC ACID; MU OPIATE RECEPTOR; NALOXONE; RESINIFERATOXIN; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

4 AMINOBUTYRIC ACID RELEASE; ANALGESIA; ANIMAL EXPERIMENT; ANTINOCICEPTION; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; IMMUNOFLUORESCENCE; LATENT PERIOD; MALE; NOCICEPTION; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT;

ACTION POTENTIALS; ANIMALS; CAPSAICIN; DITERPENES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; GLUTAMIC ACID; HYPERALGESIA; MALE; MEDULLA OBLONGATA; MICROINJECTIONS; NALOXONE; PAIN MEASUREMENT; PAIN THRESHOLD; PERIAQUEDUCTAL GRAY; RATS; RATS, WISTAR; REACTION TIME; RECEPTORS, OPIOID, MU; TRPV CATION CHANNELS;

EID: 65649106202     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.91225.2008     Document Type: Article

References (55)

1. Basbaum AI, Fields HL. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7: 309-338, 1984.
2. Behbehani MM, Fields HL. Evidence that an excitatory connection between the periaqueductal gray and nucleus raphe magnus mediates stimulation produced analgesia. Brain Res 170: 85-93, 1979.
3. Biggs CS, Pearce BR, Fowler LJ, Whitton PS. The effect of sodium valproate on extracellular GABA and other amino acids in the rat ventral hippocampus: an in vivo microdialysis study. Brain Res 594: 138-142, 1992.
4. Chen Y, Willcockson HH, Valtschanoff JG. Increased expression of CGRP in sensory afferents of arthritic mice - effect of genetic deletion of the vanilloid receptor TRPV1. Neuropeptides 42: 551-556, 2008.
5. Chiou LC, Huang LY. Mechanism underlying increased neuronal activity in the rat ventrolateral periaqueductal grey by a mu-opioid. J Physiol 518: 551-559, 1999. (Pubitemid 29366749)
6. Commons KG, Aicher SA, Kow LM, Pfaff DW. Presynaptic and postsynaptic relations of mu-opioid receptors to gamma-aminobutyric acid-immunoreactive and medullary-projecting periaqueductal gray neurons. J Comp Neurol 419: 532-542, 2000. (Pubitemid 30185990)
7. Commons KG, van Bockstaele EJ, Pfaff DW. Frequent colocalization of mu opioid and NMDA-type glutamate receptors at postsynaptic sites in periaqueductal gray neurons. Comp Neurol 408: 549-559, 1999.
8. Cristino L, De Petrocellis L, Pryce G, Baker D, Guglielmotti V, di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139: 1405-1415, 2006.
9. Cristino L, Starowicz K, De Petrocellis L, Morishita J, Ueda N, Guglielmotti V, di Marzo V. Immunohistochemical localization of anabolic and catabolic enzymes for anandamide and other putative endovanilloids in the hippocampus and cerebellar cortex of the mouse brain. Neuroscience 151: 955-968, 2008.
10. De Petrocellis L, Harrison S, Bisogno T, Tognetto M, Brandi I, Smith GD, Creminon C, Davis JB, Geppetti P, Di Marzo V. The vanilloid receptor (VR1)-mediated effects of anandamide are potently enhanced by the cAMP-dependent protein kinase. J Neurochem 77: 1660-1663, 2001. (Pubitemid 32574501)
11. Endres-Becker J, Heppenstall PA, Mousa SA, Labuz D, Oksche A, Schäfer M, Stein C, Zöllner C. Mu-opioid receptor activation modulates transient receptor potential vanilloid 1 (TRPV1) currents in sensory neurons in a model of inflammatory pain. Mol Pharmacol 71: 12-18, 2007. (Pubitemid 46020973)
12. Fang FG, Haws CM, Drasner K, Williamson A, Fields HL. Opioid peptides (DAGO-enkephalin, dynorphin A(1-13), BAM 22P) microinjected into the rat brainstem: comparison of their antinociceptive effect and their effect on neuronal firing in the rostral ventromedial medulla. Brain Res 501: 116-128, 1989. (Pubitemid 19262558)
13. Fields H, Heinricher MM. Anatomy and physiology of a nociceptive modulatory system. Philos Trans R Soc Lond B Biol Sci 308: 361-374, 1985.
14. Fields HL, Bry J, Hentall I, Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci 3: 2545-2552, 1983. (Pubitemid 14187131)
15. Fields HL, Heinricher MM, Mason P. Neurotransmitters in nociceptive modulatory circuits. Annu Rev Neurosci 14: 219-245, 1991.
16. Fields HL, Malick A, Burstein R. Dorsal horn projection targets of ON and OFF cells in the rostral ventromedial medulla. J Neurophysiol 74: 1742-1759, 1995.
17. Fossum EN, Lisowski MJ, Macey TA, Ingram SL, Morgan MM. Microinjection of the vehicle dimethyl sulfoxide (DMSO) into the periaqueductal gray modulates morphine antinociception. Brain Res 1204: 53-58, 2008.
18. Gebhart GF, Sandkühler J, Thalhammer JG, Zimmermann M. Quantitative comparison of inhibition in spinal cord of nociceptive information by stimulation in periaqueductal gray or nucleus raphe magnus of the cat. J Neurophysiol 50: 1433-1445, 1983. (Pubitemid 14175700)
19. Gurtovenko AA, Anwar J. Modulating the structure and properties of cell membranes: the molecular mechanism of action of dimethyl sulfoxide. J Phys Chem B 111: 10453-10460, 2007. (Pubitemid 47441849)
20. Heinricher MM, Morgan MM, Tortorici V, Fields HL. Disinhibition of off-cells and antinociception produced by an opioid action within the rostral ventromedial medulla. Neuroscience 63: 279-288, 1994. (Pubitemid 24333967)
21. Heinricher MM, Neubert MJ. Neural basis for the hyperalgesic action of cholecystokinin in the rostral ventromedial medulla. J Neurophysiol 92: 1982-1989, 2004. (Pubitemid 39298656)
22. Heinricher MM, Tortorici V. Interference with GABA transmission in the rostral ventromedial medulla: disinhibition of off-cells as a central mechanism in nociceptive modulation. Neuroscience 63: 533-546, 1994. (Pubitemid 24357376)
23. Kalyuzhny AE, Arvidsson U, Wu W, Wessendorf MW. Mu-opioid and delta-opioid receptors are expressed in brainstem antinociceptive circuits - studies using immunocytochemistry and retrograde tract-tracing. J Neurosci 16: 6490-6503, 1996. (Pubitemid 26337372)
24. Kalyuzhny AE, Wessendorf MW. Relationship of mu- and delta-opioid receptors to GABAergic neurons in the central nervous system, including antinociceptive brainstem circuits. J Comp Neurol 392: 528-547, 1998.
25. Maione S, Bisogno T, de Novellis V, Palazzo E, Cristino L, Valenti M, Petrosino S, Guglielmotti V, Rossi F, 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: 969-982, 2006. (Pubitemid 43345268)
26. Maione S, Leyva J, Pallotta M, Berrino L, De Novellis V, Rossi F. Involvement of opioid receptors in N-methyl-D-aspartate-induced arterial hypertension in periaqueductal gray matter. Naunyn Schmiedebergs Arch Pharmacol 351: 87-92, 1995.
27. Maione S, Marabese I, Rossi F, Berrino L, Palazzo E, Trabce LA, Rossi F. Effects of persistent nociception on periaqueductal gray glycine release. Neuroscience 97: 311-316, 2000. (Pubitemid 30224769)
28. Marabese I, Rossi F, Palazzo E, de Novellis V, Starowicz K, Cristino L, Vita D, Gatta L, Guida F, Di Marzo V, Rossi F, Maione S. Periaqueductal gray metabotropic glutamate receptor subtype 7 and 8 mediate opposite effects on amino acid release, rostral ventromedial medulla cell activities, and thermal nociception. J Neurophysiol 98: 43-53, 2007. (Pubitemid 47084797)
29. McGaraughty S, Chu KL, Bitner RS, Martino B, El Kouhen R, Han P, Nikkel AL, Burgard EC, Faltynek CR, Jarvis MF. Capsaicin infused into the PAG affects rat tail flick responses to noxious heat and alters neuronal firing in the RVM. J Neurophysiol 90: 2702-2710, 2003. (Pubitemid 37266534)
30. Melzack R, Wall PD. On the nature of cutaneous sensory mechanisms. Brain 85: 331-356, 1962.
31. Mezey E, Toth ZE, Cortright DN, Arzubi MK, Krause JE, Elde R, Guo A, Blumberg PM, 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 USA 97: 3655-3660, 2000. (Pubitemid 30183358)
32. Millan MJ. Descending control of pain. Prog Neurobiol 66: 355-474, 2002. (Pubitemid 34606906)
33. Moreau JL, Fields HL. Evidences for GABA involvement in midbrain control of medullary neurons that modulate nociceptive transmission. Brain Res 397: 37-46, 1986. (Pubitemid 17184823)
34. Neubert MJ, Kincaid W, Heinricher MM. Nociceptive facilitating neurons in the rostral ventromedial medulla. Pain 110: 158-165, 2004. (Pubitemid 38953279)
35. Osborne PB, Vaughan CW, Wilson HI, Christie MJ. Opioid inhibition of rat periaqueductal grey neurones with identified projections to rostral ventromedial medulla in vitro. J Physiol 490: 383-389, 1996.
36. Palazzo E, de Novellis V, Marabese I, Cuomo D, Rossi F, Berrino L, Rossi F, Maione S. Interaction between vanilloid and glutamate receptors in the central modulation of nociception. Eur J Pharmacol 439: 69-75, 2002. (Pubitemid 34286608)
37. Palazzo E, Rossi F, Maione S. Role of TRPV1 receptors in descending modulation of pain. Mol Cell Endocrinol 286: 79-83, 2008.
38. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. London: Academic, 1986.
39. Rea K, Roche M, Finn DP. Supraspinal modulation of pain by cannabinoids: the role of GABA and glutamate. Br J Pharmacol 152: 633-648, 2007. (Pubitemid 350034981)
40. Reynolds DV. Surgery in the electrical analgesia induced by focal brain stimulation. Science 164: 444-445, 1969.
41. Rossi GC, Pasternak GW, Bodnar RJ. Mu and delta opioid synergy between the periaqueductal gray and the rostro-ventral medulla. Brain Res 665: 85-93, 1994.
42. Sandkühler J, Gebhart GF. Relative contributions of the nucleus raphe magnus and adjacent medullary reticular formation to the inhibition by stimulation in the periaqueductal gray of a spinal nociceptive reflex in the pentobarbital-anesthetized rat. Brain Res 305: 77-87, 1984. (Pubitemid 14117846)
43. Spinella M, Cooper ML, Bodnar RJ. Excitatory amino acid antagonists in the rostral ventromedial medulla inhibit mesencephalic morphine analgesia in rats. Pain 64: 545-552, 1996. (Pubitemid 26182881)
44. Starowicz K, Cristino L, di Marzo V. TRPV1 receptors in the central nervous system: potential for previously unforeseen therapeutic applications. Curr Pharm Des 14: 42-54, 2008.
45. Starowicz K, Maione S, Cristino L, Palazzo E, Marabese I, Rossi F, de Novellis V, di Marzo V. Tonic endovanilloid facilitation of glutamate release in brainstem descending antinociceptive pathways. J Neurosci 27: 13739-13749, 2007. (Pubitemid 350278253)
46. Sykes KT, White SR, Hurley RW, Mizoguchi H, Tseng LF, Hammond DL. Mechanisms responsible for the enhanced antinociceptive effects of microopioid receptor agonists in the rostral ventromedial medulla of male rats with persistent inflammatory pain. J Pharmacol Exp Ther 322: 813-821, 2007.
47. Tang T, Stevens BA, Cox BM. Opioid regulation of intracellular free calcium in cultured mouse dorsal root ganglion neurons. J Neurosci Res 44: 338-343, 1996. (Pubitemid 26152559)
48. Tortorici V, Morgan MM. Comparison of morphine and kainic acid microinjections into identical PAG sites on the activity of RVM neurons. J Neurophysiol 88: 1707-1715, 2002. (Pubitemid 35191175)
49. Tsou K, Jang CS. Studies on the sites of analgesic action of morphine by intracerebral micro-injection. Sci Sin 13: 1099-1109, 1964.
50. Vaughan CW, Christie MJ. Presynaptic inhibitory action of opioids on synaptic transmission in the rat periaqueductal grey in vitro. J Physiol 498: 463-472, 1997.
51. Vaughan CW, Ingram SL, Connor MA, Christie MJ. How opioids inhibit GABA-mediated neurotransmission. Nature 390: 611-614, 1997. (Pubitemid 28016195)
52. Vetter I, Wyse BD, Monteith GR, Roberts-Thomson SJ, Cabot PJ. The mu opioid agonist morphine modulates potentiation of capsaicin-evoked TRPV1 responses through a cyclic AMP-dependent protein kinase A pathway. Mol Pain 2: 22, 2006. (Pubitemid 44308920)
53. Williams FG, Beitz AJ. Ultrastructural morphometric analysis of enkephalin-immunoreactive terminals in the ventrocaudal periaqueductal gray: analysis of their relationship to periaqueductal gray-raphe magnus projection neurons. Neuroscience 38: 381-394, 1990. (Pubitemid 20332419)
54. Xu M, Kim CJ, Neubert MJ, Heinricher MM. NMDA receptor-mediated activation of medullary pro-nociceptive neurons is required for secondary thermal hyperalgesia. Pain 127: 253-262, 2007. (Pubitemid 46073411)
55. Yaksh TL, Yeung JC, Rudy TA. Systematic examination in the rat of brain sites sensitive to the direct application of morphine: observation of differential effects within the periaqueductal gray. Brain Res 114: 83-103, 1976.