Protein kinase C mediates the synergistic interaction between agonists acting at α2-adrenergic and delta-opioid receptors in spinal cord

Journal of Neuroscience

Volumn 29, Issue 42, 2009, Pages 13264-13273

  Overland, Aaron C ^a   Kitto, Kelley F ^a   Chabot Doré, Anne Julie ^b   Rothwell, Patrick E ^a   Fairbanks, Carolyn A ^a   Stone, Laura S ^b,c,d   Wilcox, George L ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; CALCITONIN GENE RELATED PEPTIDE; CLONIDINE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; DELTORPHIN II; PHOSPHOLIPASE C; PROTEIN KINASE C; TETRODOTOXIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME ACTIVATION; HUMAN; MALE; MOUSE; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL CORD DORSAL HORN; TAIL FLICK TEST;

ADRENERGIC ALPHA-AGONISTS; ANESTHETICS, LOCAL; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CLONIDINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG COMBINATIONS; DRUG SYNERGISM; ENZYME INHIBITORS; EVOKED POTENTIALS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HYPERALGESIA; INJECTIONS, SPINAL; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; OLIGOPEPTIDES; PATCH-CLAMP TECHNIQUES; POSTERIOR HORN CELLS; POTASSIUM; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, OPIOID, DELTA; SIGNAL TRANSDUCTION; SPINAL CORD; SUBSTANCE P; TETRODOTOXIN;

EID: 70350345550     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1907-09.2009     Document Type: Article

References (58)

1. Aantaa R, Marjamäki A, Scheinin M (1995) Molecular pharmacology of alpha 2-adrenoceptor subtypes. Ann Med 27:439-449.
2. American Pain Society (2008) Principles of analgesic use in the treatment of acute pain and cancer pain, Ed 6. Glenview, IL: American Pain Society.
3. Angst MS, Clark JD (2006) Opioid-induced hyperalgesia: a qualitative systematic review. Anesthesiology 104:570-587.
4. Arvidsson U, Dado RJ, Riedl M, Lee JH, Law PY, Loh HH, Elde R, Wessendorf MW (1995) delta-Opioid receptor immunoreactivity: distribution in brainstem and spinal cord, and relationship to biogenic amines and enkephalin. J Neurosci 15:1215-1235.
5. Bao L, Jin SX, Zhang C, Wang LH, Xu ZZ, Zhang FX, Wang LC, Ning FS, Cai HJ, Guan JS, Xiao HS, Xu ZQ, He C, Hökfelt T, Zhou Z, Zhang X (2003) Activation of delta opioid receptors induces receptor insertion and neuropeptide secretion. Neuron 37:121-133. (Pubitemid 36106439)
6. Cahill CM, Morinville A, Lee MC, Vincent JP, Collier B, Beaudet A (2001a) Prolonged morphine treatment targets delta opioid receptors to neuronal plasma membranes and enhances delta-mediated antinociception. J Neurosci 21:7598-7607. (Pubitemid 32904959)
7. Cahill CM, McClellan KA, Morinville A, Hoffert C, Hubatsch D, O'Donnell D, Beaudet A (2001b) Immunohistochemical distribution of delta opioid receptors in the rat CNS: evidence for somatodendritic labeling and antigen-specific cellular compartmentalization. J Comp Neurol 440:65-84.
8. Cahill CM, Morinville A, Hoffert C, O'Donnell D, Beaudet A (2003) Upregulation and trafficking of delta opioid receptor in a model of chronic inflammation: implications for pain control. Pain 101:199-208. (Pubitemid 36044668)
9. Cheng PY, Svingos AL, Wang H, Clarke CL, Jenab S, Beczkowska IW, Inturrisi CE, Pickel VM (1995) Ultrastructural immunolabeling shows prominent presynaptic vesicular localization of delta-opioid receptor within both enkephalin-and nonenkephalin-containing axon terminals in the superficial layers of the rat cervical spinal cord. J Neurosci 15:5976-5988.
10. Cheng PY, Liu-Chen LY, Pickel VM (1997) Dual ultrastructural immunocytochemical labeling of mu and delta opioid receptors in the superficial layers of the rat cervical spinal cord. Brain Res 778:367-380.
11. Connor M, Christie MD (1999) Opioid receptor signalling mechanisms. Clin Exp Pharmacol Physiol 26:493-499.
12. Cuello AC, Galfre G, Milstein C (1979) Detection of substance P in the central nervous system by a monoclonal antibody. Proc Natl Acad Sci U S A 76:3532-3536. (Pubitemid 9233178)
13. Dado RJ, Law PY, Loh HH, Elde R (1993) Immunofluorescent identification of a delta (delta)-opioid receptor on primary afferent nerve terminals. Neuroreport 5:341-344.
14. Dorn GW 2nd, Oswald KJ, McCluskey TS, Kuhel DG, Liggett SB (1997) Alpha 2A-adrenergic receptor stimulated calcium release is transduced by Gi-associated G(beta gamma)-mediated activation of phospholipase C. Biochemistry 36:6415-6423.
15. Fairbanks CA, Posthumus IJ, Kitto KF, Stone LS, Wilcox GL (2000) Moxonidine, a selective imidazoline/alpha(2) adrenergic receptor agonist, synergizes with morphine and deltorphin II to inhibit substance P-induced behavior in mice. Pain 84:13-20.
16. Fairbanks CA, Stone LS, Kitto KF, Nguyen HO, Posthumus IJ, Wilcox GL (2002) Alpha(2C)-Adrenergic receptors mediate spinal analgesia and adrenergic-opioid synergy. J Pharmacol Exp Ther 300:282-290.
17. Franco-Cereceda A, Henke H, Lundberg JM, Petermann JB, Hökfelt T, Fischer JA (1987) Calcitonin gene-related peptide (CGRP) in capsaicinsensitive substance P-immunoreactive sensory neurons in animals and man: distribution and release by capsaicin. Peptides 8:399-410. (Pubitemid 17065147)
18. Gendron L, Lucido AL, Mennicken F, O'Donnell D, Vincent JP, Stroh T, Beaudet A (2006) Morphine and pain-related stimuli enhance cell surface availability of somatic delta-opioid receptors in rat dorsal root ganglia. J Neurosci 26:953-962. (Pubitemid 43239576)
19. Guo XH, Fairbanks CA, Stone LS, Loh HH (2003) DPDPE-UK14,304 synergy is retained in mu opioid receptor knockout mice. Pain 104:209-217. (Pubitemid 36835890)
20. Han SK, Park JR, Park SA, Chun SW, Lee JC, Lee SY, Ryu PD, Park SJ (2007) Noradrenaline inhibits substantia gelatinosa neurons in mice trigeminal subnucleus caudalis via alpha(2) and beta adrenoceptors. Neurosci Lett 411:92-97.
21. Honoré P, Chapman V, Buritova J, Besson JM (1996) To what extent do spinal interactions between an alpha-2 adrenoceptor agonist and a mu opioid agonist influence noxiously evoked c-Fos expression in the rat? A pharmacological study. J Pharmacol Exp Ther 278:393-403. (Pubitemid 27167119)
22. Hylden JL, Wilcox GL (1980) Intrathecal morphine in mice: a new technique. Eur J Pharmacol 67:313-316. (Pubitemid 10007057)
23. Hylden JLK, Wilcox GL (1983) Pharmacological characterization of Substance P-induced nociception in mice: modulation by opioid and noradrenergic agonists at the spinal level. J Pharmacol Exp Ther 226:398-404.
24. Janssen PA, Niemegeers CJ, Dony JG (1963) The inhibitory effect of fentanyl and other morphine-like analgesics on the warm water induced tail withdrawl reflex in rats. Arzneimittelforschung 13:502-507.
25. Jordan BA, Devi LA (1999) G-protein-coupled receptor heterodimerization modulates receptor function. Nature 399:697-700.
26. Law PY, Wong YH, Loh HH (2000) Molecular mechanisms and regulation of opioid receptor signaling. Annu Rev Pharmacol Toxicol 40:389-430. (Pubitemid 30340688)
27. Millan MJ (1999) The induction of pain: an integrative review. Prog Neurobiol 57:1-164.
28. Millan MJ (2002) Descending control of pain. Prog Neurobiol 66:355-474.
29. Monasky MS, Zinsmeister AR, Stevens CW, Yaksh TL (1990) Interaction of intrathecal morphine and ST-91 on antinociception in the rat: dose-response analysis, antagonism and clearance. J Pharmacol Exp Ther 254:383-392.
30. Murase K, Randiæ M (1983) Electrophysiological properties of rat spinal dorsal horn neurones in vitro: calcium-dependent action potentials. J Physiol 334:141-153. (Pubitemid 13176088)
31. Omote K, Kitahata LM, Collins JG, Nakatani K, Nakagawa I (1990) The antinociceptive role of mu-and delta-opiate receptors and their interactions in the spinal dorsal horn of cats. Anesth Analg 71:23-28. (Pubitemid 20380565)
32. Ossipov MH, Harris S, Lloyd P, Messineo E (1990a) An isobolographic analysis of the antinociceptive effect of systemically and intrathecally administered combinations of clonidine and opiates. J Pharmacol Exp Ther 255:1107-1116.
33. Ossipov MH, Harris S, Lloyd P, Messineo E, Lin BS, Bagley J (1990b) Antinociceptive interaction between opioids and medetomidine: systemic additivity and spinal synergy. Anesthesiology 73:1227-1235.
34. Ossipov MH, Lozito R, Messineo E, Green J, Harris S, Lloyd P (1990c) Spinal antinociceptive synergy between clonidine and morphine, U69593, and DPDPE: isobolographic analysis. Life Sci 47:PL71-PL76.
35. Patwardhan AM, Berg KA, Akopain AN, Jeske NA, Gamper N, Clarke WP, Hargreaves KM (2005) Bradykinin-induced functional competence and trafficking of the delta-opioid receptor in trigeminal nociceptors. J Neurosci 25:8825-8832. (Pubitemid 41384450)
36. Pertovaara A (2006) Noradrenergic pain modulation. Prog Neurobiol 80:53-83.
37. Plenderleith MB, Haller CJ, Snow PJ (1990) Peptide coexistence in axon terminals within the superficial dorsal horn of the rat spinal cord. Synapse 6:344-350.
38. Rashid AJ, So CH, Kong MM, Furtak T, El-Ghundi M, Cheng R, O'Dowd BF, George SR (2007) D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci U S A 104:654-659. (Pubitemid 46123080)
39. Riedl MS, Schnell SA, Overland AC, Chabot-Doré AJ, Taylor AM, Ribeiro-da-Silva A, Elde RP, Wilcox GL, Stone LS (2009) Coexpression of alpha(2A)-adrenergic and delta-opioid receptors in substance P-containing terminals in rat dorsal horn. J Comp Neurol 513:385-398.
40. Roerig SC, Lei S, Kitto K, Hylden JK, Wilcox GL (1992) Spinal interactions between opioid and noradrenergic agonists in mice: multiplicativity involves delta and alpha-2 receptors. J Pharmacol Exp Ther 262:365-374.
41. Ryu PD, Gerber G, Murase K, Randic M (1988) Actions of calcitonin gene-related peptide on rat spinal dorsal horn neurons. Brain Res 441:357-361. (Pubitemid 18059984)
42. Stevens CW, Monasky MS, Yaksh TL (1988) Spinal infusion of opiate and alpha-2 agonists in rats: tolerance and cross-tolerance studies. J Pharmacol Exp Ther 244:63-70.
43. Stone LS, MacMillan LB, Kitto KF, Limbird LE, Wilcox GL (1997) The alpha2a adrenergic receptor subtype mediates spinal analgesia evoked by alpha2 agonists and is necessary for spinal adrenergic-opioid synergy. J Neurosci 17:7157-7165.
44. Stone LS, Broberger C, Vulchanova L, Wilcox GL, Hökfelt T, Riedl MS, Elde R (1998) Differential distribution of alpha2A and alpha2C adrenergic receptor immunoreactivity in the rat spinal cord. J Neurosci 18:5928-5937. (Pubitemid 28341368)
45. Sullivan AF, Dashwood MR, Dickenson AH (1987) Alpha 2-adrenoceptor modulation of nociception in rat spinal cord: location, effects and interactions with morphine. Eur J Pharmacol 138:169-177.
46. Tallarida RJ (1992) Statistical analysis of drug combinations for synergism. Pain 49:93-97.
47. Tallarida RJ (2002) The interaction index: a measure of drug synergism. Pain 98:163-168.
48. Trudeau LE, Emery DG, Haydon PG (1996) Direct modulation of the secretory machinery underlies PKA-dependent synaptic facilitation in hippocampal neurons. Neuron 17:789-797.
49. Vilardaga JP, Nikolaev VO, Lorenz K, Ferrandon S, Zhuang Z, Lohse MJ (2008) Conformational cross-talk between alpha2A-adrenergic and muopioid receptors controls cell signaling. Nat Chem Biol 4:126-131.
50. Wang HB, Guan JS, Bao L, Zhang X (2008) Distinct subcellular distribution of delta-opioid receptor fused with various tags in PC12 cells. Neurochem Res 33:2028-2034.
51. Wei ZY, Roerig SC (1998) Spinal morphine/clonidine antinociceptive synergism is regulated by protein kinase C, but not protein kinase A activity. J Pharmacol Exp Ther 287:937-943.
52. Wessendorf MW, Elde RP (1985) Characterization of an immunofluorescence technique for the demonstration of coexisting neurotransmitters within nerve fibers and terminals. J Histochem Cytochem 33:984-994.
53. Wigdor S, Wilcox GL (1987) Central and systemic morphine antinociception in the mouse: contribution of descending noradrenergic and serotonergic pathways. J Pharmacol Exp Ther 242:90-95. (Pubitemid 17112264)
54. Wilcox GL, Carlsson KH, Jochim A, Jurna I (1987) Mutual potentiation of antinociceptive effects of morphine and clonidine on motor and sensory responses in rat spinal cord. Brain Res 405:84-93. (Pubitemid 17034935)
55. Yoon SH, Lo TM, Loh HH, Thayer SA (1999) Delta-opioid-induced liberation of Gbetagamma mobilizes Ca2+ stores in NG108-15 cells. Mol Pharmacol 56:902-908.
56. Yoshimura M, Jessell TM (1989) Primary afferent-evoked synaptic responses and slow potential generation in rat substantia gelatinosa neurons in vitro. J Neurophysiol 62:96-108. (Pubitemid 19180544)
57. Yoshimura M, Jessell T (1990) Amino acid-mediated EPSPs at primary afferent synapses with substantia gelatinosa neurones in the rat spinal cord. J Physiol 430:315-335. (Pubitemid 20382826)
58. Zhang X, Bao L, Arvidsson U, Elde R, Hökfelt T (1998) Localization and regulation of the delta-opioid receptor in dorsal root ganglia and spinal cord of the rat and monkey: evidence for association with the membrane of large dense-core vesicles. Neuroscience 82:1225-1242. (Pubitemid 27502063)