Protein kinase Cε is required for spinal analgesic synergy between delta opioid and alpha-2A adrenergic receptor agonist pairs

Journal of Neuroscience

Volumn 33, Issue 33, 2013, Pages 13538-13546

  Schuster, Daniel J ^a   Kitto, Kelley F ^a   Overland, Aaron C ^b   Messing, Robert O ^c   Stone, Laura S ^d   Fairbanks, Carolyn A ^a,e   Wilcox, George L ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b San Diego   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^d MCGILL UNIVERSITY   (Canada)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2A ADRENERGIC RECEPTOR; ALPHA ADRENERGIC RECEPTOR STIMULATING AGENT; BRIMONIDINE; CLONIDINE; DELTA OPIATE RECEPTOR AGONIST; DELTORPHIN; ENDOMORPHIN 2; MORPHINE SULFATE; PROTEIN KINASE C ETA;

ANALGESIC ACTIVITY; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOUSE; NOCICEPTION; NONHUMAN; PEPTIDERGIC NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SPINAL ANESTHESIA; SPINAL CORD DORSAL HORN; SPINAL GANGLION; TAIL FLICK TEST;

ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ANALGESICS; ANESTHESIA, SPINAL; ANIMALS; CLONIDINE; DRUG SYNERGISM; ENZYME INHIBITORS; FEMALE; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGOPEPTIDES; PROTEIN KINASE C-EPSILON; QUINOXALINES; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, OPIOID, DELTA; SPINAL CORD;

EID: 84881535239     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4013-12.2013     Document Type: Article

References (48)

1. Aley KO, Messing RO, Mochly-Rosen D, Levine JD (2000) Chronic hyper-sensitivity for inflammatory nociceptor sensitization mediated by the ep-silon isozyme of protein kinase C. J Neurosci 20:4680-4685.
2. 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.
3. Beaudry H, Dubois D, Gendron L (2011) Activation of spinal mu- and delta-opioid receptors potently inhibits substance P release induced by peripheral noxious stimuli. J Neurosci 31:13068-13077.
4. Chakrabarti S, Liu NJ, Gintzler AR (2010) Formation of mu-/kappa-opioid receptor heterodimer is sex-dependent and mediates female-specific opioid analgesia. Proc Natl Acad Sci USA 107:20115-20119.
5. Chan AS, Law PY, Loh HH, Ho PN, Wu WM, Chan JS, Wong YH (2003) The first and third intracellular loops together with the carboxy terminal tail of the delta-opioid receptor contribute toward functional interaction with Galpha16. J Neurochem 87:697-708.
6. Chen L, Hahn H, Wu G, Chen CH, Liron T, Schechtman D, Cavallaro G, Banci L, Guo Y, Bolli R, Dorn GW 2nd, Mochly-Rosen D (2001) Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc Natl Acad Sci USA 98:11114-11119.
7. 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.
8. Dina OA, Khasar SG, Gear RW, Levine JD (2009) Activation of Gi induces mechanical hyperalgesia poststress or inflammation. Neuroscience 160:501-507.
9. 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.
10. Dorn GW 2nd, Souroujon MC, Liron T, Chen CH, Gray MO, Zhou HZ, Csukai M, Wu G, Lorenz JN, Mochly-Rosen D (1999) Sustained in vivo cardiac protection by a rationally designed peptide that causes e protein kinase C translocation. Proc Natl Acad Sci USA 96:12798-12803.
11. Fairbanks CA, Wilcox GL (1999) Spinal antinociceptive synergism between morphine and clonidine persists in mice made acutely or chronically tolerant to morphine. J Pharmacol Exp Ther 288:1107-1116.
12. 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.
13. Ferrari LF, Bogen O, Levine JD (2010) Nociceptor subpopulations involved in hyperalgesic priming. Neuroscience 165:896-901.
14. Forster JG, Rosenberg PH (2004) Small dose of clonidine mixed with low-dose ropivacaine and fentanyl for epidural analgesia after total knee arthroplasty. Br J Anaesth 93:670-677.
15. Gregoretti C, Moglia B, Pelosi P, Navalesi P (2009) Clonidine in perioperative medicine and intensive care unit: more than an anti-hypertensive drug. Curr Drug Targets 10:799-814.
16. Hucho TB, Dina OA, Levine JD (2005) Epac mediates a cAMP-to-PKC signaling in inflammatory pain: an isolectin B4(+) neuron-specific mechanism. J Neurosci 25:6119-6126.
17. Hylden JL, Wilcox GL (1980) Intrathecal morphine in mice: a new technique. Eur J Pharmacol 67:313-316.
18. Hylden JL, 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.
19. 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.
20. Johnson JA, Gray MO, Chen CH, Mochly-Rosen D (1996) A protein kinase C translocation inhibitor as an isozyme-selective antagonist of cardiac function. J Biol Chem 271:24962-24966.
21. Joseph EK, Levine JD (2010) Hyperalgesic priming is restricted to isolectin B4-positive nociceptors. Neuroscience 169:431-435.
22. Khasar SG, Lin YH, Martin A, Dadgar J, McMahon T, Wang D, Hundle B, Aley KO, Isenberg W, McCarter G, Green PG, Hodge CW, Levine JD, Messing RO (1999) A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice. Neuron 24:253-260.
23. Kondo I, Marvizon JC, Song B, Salgado F, Codeluppi S, Hua XY, Yaksh TL (2005) Inhibition by spinal mu- and delta-opioid agonists of afferent- evoked substance P release. J Neurosci 25:3651-3660.
24. Lee JW, Joshi S, Chan JS, Wong YH (1998) Differential coupling of mu-, delta-, and kappa-opioid receptors to G alpha16-mediated stimulation of phospholipase C. J Neurochem 70:2203-2211.
25. Li XY, Sun L, He J, Chen ZL, Zhou F, Liu XY, Liu RS (2010) The kappa-opioid receptor is upregulated in the spinal cord and locus ceruleus but downregulated in the dorsal root ganglia of morphine tolerant rats. Brain Res 1326:30-39.
26. Ma HT, Lin WW, Zhao B, Wu WT, Huang W, Li Y, Jones NL, Kruth HS (2006) Protein kinase C beta and delta isoenzymes mediate cholesterol accumulation in PMA-activated macrophages. Biochem Biophys Res Commun 349:214-220.
27. Olave MJ, Maxwell DJ (2002) An investigation of neurones that possess the alpha 2C-adrenergic receptor in the rat dorsal horn. Neuroscience 115: 31-40.
28. Ossipov MH, Lopez Y, Bian D, Nichols ML, Porreca F (1997) Synergistic antinociceptive interactions of morphine and clonidine in rats with nerve-ligation injury. Anesthesiology 86:196-204.
29. Overland AC, Kitto KF, Chabot-Doré AJ, Rothwell PE, Fairbanks CA, Stone LS, Wilcox GL (2009) Protein kinase C mediates the synergistic interaction between agonists acting atalpha2-adrenergic and delta-opioid receptors in spinal cord. J Neurosci 29:13264-13273.
30. Paech MJ, Pavy TJ, Orlikowski CE, Yeo ST, Banks SL, Evans SF, Henderson J (2004) Postcesarean analgesia with spinal morphine, clonidine, or their combination. Anesth Analg 98:1460-1466.
31. 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 Neu-rosci 25:8825-8832.
32. 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.
33. Rowan MP, Ruparel NB, Patwardhan AM, Berg KA, Clarke WP, Hargreaves KM (2009) Peripheral delta opioid receptors require priming for functional competence in vivo. Eur J Pharmacol 602:283-287.
34. Sánchez-Blázquez P, Garzon J (1998) Delta Opioid receptor subtypes activate inositol-signaling pathways in the production of antinociception. J Pharmacol Exp Ther 285:820-827.
35. Shin SW, Eisenach JC (2003) Intrathecal morphine reduces the visceromo-tor response to acute uterine cervical distension in an estrogen-independent manner. Anesthesiology 98:1467-1471; discussion 1466A.
36. Standifer KM, Rossi GC, Pasternak GW (1996) Differential blockadeof opi-oid analgesia by antisense oligodeoxynucleotides directed against various G protein alpha subunits. Mol Pharmacol 50:293-298.
37. 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.
38. Stone LS, Broberger C, Vulchanova L, Wilcox GL, Hokfelt 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.
39. 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.
40. Sweitzer SM, Wong SM, Peters MC, Mochly-Rosen D, Yeomans DC, Kendig JJ (2004) Protein kinase C epsilon and gamma: involvement in formalin-induced nociception in neonatal rats. J Pharmacol Exp Ther 309:616-625.
41. Tallarida R, Murray R (1987) Manual of pharmacological calculations with computer programs. New York: Springer.
42. Tallarida RJ, Porreca F, Cowan A (1989) Statistical analysis of drug-drug and site-site interactions with isobolograms. Life Sci 45:947-961.
43. Vulchanova L, Riedl MS, Shuster SJ, Stone LS, Hargreaves KM, Buell G, Surprenant A, North RA, Elde R (1998) P2X3 is expressed by DRG neurons that terminate in inner lamina II. Eur J Neurosci 10:3470-3478.
44. Wang HB, Zhao B, Zhong YQ, Li KC, Li ZY, Wang Q, Lu YJ, Zhang ZN, He SQ, Zheng HC, Wu SX, Hokfelt TG, Bao L, Zhang X (2010) Coexpres-sion of delta- and mu-opioid receptors in nociceptive sensory neurons. Proc Natl Acad Sci USA 107:13117-13122.
45. 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.
46. Wu DF, Chandra D, McMahon T, Wang D, Dadgar J, Kharazia VN, Liang YJ, Waxman SG, Dib-Hajj SD, Messing RO (2012) PKCepsilon phosphorylation of the sodium channel NaV1.8 increases channel function and produces mechanical hyperalgesia in mice. J Clin Invest 122: 1306-1315.
47. 2+ stores inNG108-15 cells. Mol Pharmacol 56:902-908.
48. Zhao B, Wang HB, Lu YJ, Hu JW, Bao L, Zhang X (2011) Transport of receptors, receptor signaling complexes and ion channels via neuropeptide-secretory vesicles. Cell Res 21:741-753.