The role of K-opioid receptor activation in mediating antinociception and addiction

Acta Pharmacologica Sinica

Volumn 31, Issue 9, 2010, Pages 1065-1070

  Wang, Yu Hua ^a,b   Sun, Jian Feng ^b   Tao, Yi Min ^b   Chi, Zhi Qiang ^b   Liu, Jing Gen ^b  

^a NANJING UNIVERSITY OF CHINESE MEDICINE   (China)

^b SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

addiction; antinociception; cocaine reward; desensitization; drug withdrawal; dynorphin; K opioid receptor; negative mood state; tolerance

Indexed keywords

3,4 DICHLORO N METHYL N [1 PHENYL 2 (1 PYRROLIDINYL)ETHYL]BENZENEACETAMIDE; CR 665; CR 845; CYCLAZOCINE; DYNORPHIN A [1-8][1 (N METHYLTYROSINE) 7 (N METHYLARGININE) 8 DEXTRO LEUCINE N ETHYLAMIDE]; ENADOLINE; KAPPA OPIATE RECEPTOR AGONIST; MORPHINAN DERIVATIVE; OPIATE AGONIST; OPIATE RECEPTOR; OPIATE RECEPTOR K; SPIRADOLINE; UNCLASSIFIED DRUG; ANALGESIC AGENT; KAPPA OPIATE RECEPTOR;

AGONIST; ANALGESIA; ANTINOCICEPTION; AVERSIVE BEHAVIOR; DIURESIS; DRUG DEPENDENCE; DYSPHORIA; HUMAN; MODULATION; NONHUMAN; PAIN; RELAPSE; REVIEW; SEDATION; SIDE EFFECT; STRESS; ADDICTION; ANIMAL; DRUG POTENTIATION; METABOLISM;

ANALGESICS; ANIMALS; HUMANS; PAIN; RECEPTORS, OPIOID, KAPPA; SUBSTANCE-RELATED DISORDERS;

EID: 77956358093     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2010.138     Document Type: Review

References (98)

1. Zukin RS, Eghbali M, Olive D, Unterwald EM, Tempel A. Characterization and visualization of rat and guinea pig brain kappa opioid receptors: evidence for kappa 1 and kappa 2 opioid receptors. Proc Natl Acad Sci USA 1988; 85: 4061-4065
2. Clark JA, Liu L, Price M, Hersh B, Edelson M, Pasternak GW. Kappa opiate receptor multiplicity: evidence for two U50,488-sensitive kappa 1 subtypes and a novel kappa 3 subtype. J Pharmacol Exp Ther 1989; 251: 461-468
3. Connor M, Kitchen I. Has the sun set on kappa3-opioid receptors? Br J Pharmacol 2006; 147: 349-350
4. Bruijnzeel AW. kappa-Opioid receptor signaling and brain reward function. Brain Res Rev 2009; 62: 127-146
5. Simonin F, Gaveriaux-Ruff C, Befort K, Matthes H, Lannes B, Micheletti G, et al. kappa-Opioid receptor in humans: cDNA and genomic cloning, chromosomal assignment, functional expression, pharmacology, and expression pattern in the central nervous system. Proc Natl Acad Sci USA 1995; 92: 7006-7010
6. Dhawan BN, Cesselin F, Raghubir R, Reisine T, Bradley PB, Portoghese PS, et al. International Union of Pharmacology. XII. Classification of opioid receptors. Pharmacol Rev 1996; 48: 567-592
7. Bruchas MR, Land BB, Chavkin C. The dynorphin/kappa opioid system as a modulator of stress-induced and pro-addictive behaviors. Brain Res 2010; 1314: 44-55.
8. Bruchas MR, Macey TA, Lowe JD, Chavkin C. Kappa opioid receptor activation of p38 MAPK is GRK3-and arrestin-dependent in neurons and astrocytes. J Biol Chem 2006; 281: 18081-18089
9. Bruchas MR, Yang T, Schreiber S, Defino M, Kwan SC, Li S, et al. Long-acting kappa opioid antagonists disrupt receptor signaling and produce noncompetitive effects by activating c-Jun N-terminal kinase. J Biol Chem 2007; 282: 29803-29811
10. McLennan GP, Kiss A, Miyatake M, Belcheva MM, Chambers KT, Pozek JJ, et al. Kappa opioids promote the proliferation of astrocytes via Gbetagamma and beta-arrestin 2-dependent MAPK-mediated pathways. J neurochem 2008; 107: 1753-1765
11. Camilleri M. Novel pharmacology: asimadoline, a kappa-opioid agonist, and visceral sensation. Neurogastroenterol Motil 2008; 20: 971-979
12. Knoll AT, Carlezon Jr. Dynorphin, stress, and depression. Brain Res 2010; 1314: 56-73.
13. Belcheva MM, Clark AL, Haas PD, Serna JS, Hahn JW, Kiss A, et al. Mu and kappa opioid receptors activate ERK/MAPK via different protein kinase C isoforms and secondary messengers in astrocytes. J Biol Chem 2005; 280: 27662-27669
14. Huang P, Steplock D, Weinman EJ, Hall RA, Ding Z, Li J, et al. kappa Opioid receptor interacts with Na(+)/H(+)-exchanger regulatory factor-1/Ezrin-radixin-moesin-binding phosphoprotein-50 (NHERF-1/EBP50) to stimulate Na(+)/H(+) exchange independent of G(i)/G(o) proteins. J Biol Chem 2004; 279: 25002-25009
15. Chen Y, Chen C, Liu-Chen LY. Dynorphin peptides differentially regulate the human kappa opioid receptor. Life Sci 2007; 80: 1439-1448
16. Liu-Chen LY. Agonist-induced regulation and trafficking of kappa opioid receptors. Life Sci 2004; 75: 511-536
17. McLaughlin JP, Myers LC, Zarek PE, Caron MG, Lefkowitz RJ, Czyzyk TA, et al. Prolonged kappa opioid receptor phosphorylation mediated by G-protein receptor kinase underlies sustained analgesic tolerance. J Biol Chem 2004; 279: 1810-1818
18. Meng F, Xie GX, Thompson RC, Mansour A, Goldstein A, Watson SJ, et al. Cloning and pharmacological characterization of a rat kappa opioid receptor. Proc Natl Acad Sci USA 1993; 90: 9954-9958
19. Kreibich A, Reyes BA, Curtis AL, Ecke L, Chavkin C, Van Bockstaele EJ, et al. Presynaptic inhibition of diverse afferents to the locus ceruleus by kappa-opiate receptors: a novel mechanism for regulating the central norepinephrine system. J Neurosci 2008; 28: 6516-6525
20. Shirayama Y, Ishida H, Iwata M, Hazama GI, Kawahara R, Duman RS. Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. J neurochem 2004; 90: 1258-1268
21. Winkler CW, Hermes SM, Chavkin CI, Drake CT, Morrison SF, Aicher S.A. Kappa opioid receptor (KOR) and GAD67 immunoreactivity are found in OFF and NEUTRAL cells in the rostral ventromedial medulla. J Neurophysiol 2006; 96: 3465-3473
22. Neugebauer V, Li W, Bird GC, Han JS. The amygdala and persistent pain. Neuroscientist 2004; 10: 221-234
23. Gutstein HB, Mansour A, Watson SJ, Akil H, Fields HL. Mu and kappa opioid receptors in periaqueductal gray and rostral ventromedial medulla. Neuroreport 1998; 9: 1777-1781
24. Clark CR, Birchmore B, Sharif NA, Hunter JC, Hill RG, Hughes J. PD117302: a selective agonist for the kappa-opioid receptor. Br J Pharmacol 1988; 93: 618-626
25. Lahti RA, Mickelson MM, McCall JM, Von Voigtlander PF. [3H] U-69593 a highly selective ligand for the opioid kappa receptor. Eur J Pharmacol 1985; 109: 281-284
26. Hunter JC, Leighton GE, Meecham KG, Boyle SJ, Horwell DC, Rees DC, et al. CI-977, a novel and selective agonist for the kappa-opioid receptor. Br J Pharmacol 1990; 101: 183-189
27. Lahti RA, VonVoigtlander PF, Barsuhn C. Properties of a selective kappa agonist, U-50,488H. Life Sci 1982; 31: 2257-2260
28. Pan ZZ. mu-Opposing actions of the kappa-opioid receptor. Trends Pharmacol Sci 1998; 19: 94-98
29. Mansour A, Hoversten MT, Taylor LP, Watson SJ, Akil H. The cloned mu, delta and kappa receptors and their endogenous ligands: evidence for two opioid peptide recognition cores. Brain Res 1995; 700: 89-98.
30. Land BB, Bruchas MR, Lemos JC, Xu M, Melief EJ, Chavkin C. The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J Neurosci 2008; 28: 407-414
31. Schwarzer C. 30 years of dynorphins-new insights on their functions in neuropsychiatric diseases. Pharmacol Ther 2009; 123: 353-370
32. Day R, Lazure C, Basak A, Boudreault A, Limperis P, Dong W, et al. Prodynorphin processing by proprotein convertase 2. Cleavage at single basic residues and enhanced processing in the presence of carboxypeptidase activity. J Biol Chem 1998; 273: 829-836
33. Yakovleva T, Bazov I, Cebers G, Marinova Z, Hara Y, Ahmed A, et al. Prodynorphin storage and processing in axon terminals and dendrites. FASEB J 2006; 20: 2124-2126
34. Shippenberg TS, Zapata A, Chefer VI. Dynorphin and the pathophysiology of drug addiction. Pharmacol Ther 2007; 116: 306-321
35. Mysels D, Sullivan MA. The kappa-opiate receptor impacts the pathophysiology and behavior of substance use. Am J Addict 2009; 18: 272-276
36. Chartoff EH, Potter D, Damez-Werno D, Cohen BM, Carlezon WA Jr. Exposure to the selective kappa-opioid receptor agonist salvinorin A modulates the behavioral and molecular effects of cocaine in rats. Neuropsychopharmacology 2008; 33: 2676-2687
37. Di Chiara G, Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 1988; 85: 5274-5278
38. Margolis EB, Hjelmstad GO, Bonci A, Fields HL. Kappa-opioid agonists directly inhibit midbrain dopaminergic neurons. J Neurosci 2003; 23: 9981-9986
39. Ukai M, Mizutani M, Kameyama T. Opioid peptides selective for receptor types modulate cocaine-induced behavioral responses in mice. Nihon Shinkei Seishin Yakurigaku Zasshi 1994; 14: 153-159
40. Crawford CA, McDougall SA, Bolanos CA, Hall S, Berger SP. The effects of the kappa agonist U-50,488 on cocaine-induced conditioned and unconditioned behaviors and Fos immunoreactivity. Psychopharmacology (Berl) 1995; 120: 392-399
41. Suzuki T, Shiozaki Y, Masukawa Y, Misawa M, Nagase H. The role of mu-and kappa-opioid receptors in cocaine-induced conditioned place preference. Jpn J Pharmacol 1992; 58: 435-442
42. Shippenberg TS, LeFevour A, Heidbreder C. kappa-Opioid receptor agonists prevent sensitization to the conditioned rewarding effects of cocaine. J Pharmacol Exp Ther 1996; 276: 545-554
43. Glick SD, Maisonneuve IM, Raucci J, Archer S. Kappa opioid inhibition of morphine and cocaine self-administration in rats. Brain Res 1995; 681: 147-152
44. Negus SS, Mello NK, Portoghese PS, Lin CE. Effects of kappa opioids on cocaine self-administration by rhesus monkeys. J Pharmacol Exp Ther 1997; 282: 44-55.
45. Mello NK, Negus SS. Effects of kappa opioid agonists on cocaine and food-maintained responding by rhesus monkeys. J Pharmacol Exp Ther 1998; 286: 812-824
46. Schenk S, Partridge B, Shippenberg TS. U69593, a kappa-opioid agonist, decreases cocaine self-administration and decreases cocaine-produced drug-seeking. Psychopharmacology (Berl) 1999; 144: 339-346
47. Schenk S, Partridge B, Shippenberg TS. Reinstatement of extinguished drug-taking behavior in rats: effect of the kappa-opioid receptor agonist, U69593. Psychopharmacology (Berl) 2000; 151: 85-90.
48. Maisonneuve IM, Archer S, Glick SD. U50,488, a kappa opioid receptor agonist, attenuates cocaine-induced increases in extracellular dopamine in the nucleus accumbens of rats. Neurosci Lett 1994; 181: 57-60.
49. Xu M, Petraschka M, McLaughlin JP, Westenbroek RE, Caron MG, Lefkowitz RJ, et al. Neuropathic pain activates the endogenous kappa opioid system in mouse spinal cord and induces opioid receptor tolerance. J Neurosci 2004; 24: 4576-4584
50. Nakazawa T, Furuya Y, Kaneko T, Yamatsu K. Spinal kappa receptormediated analgesia of E-2078, a systemically active dynorphin analog, in mice. J Pharmacol Exp Ther 1991; 256: 76-81.
51. DeHaven-Hudkins DL, Dolle RE. Peripherally restricted opioid agonists as novel analgesic agents. Curr Pharm Des 2004; 10: 743-757
52. Pan ZZ, Tershner SA, Fields HL. Cellular mechanism for anti-analgesic action of agonists of the kappa-opioid receptor. Nature 1997; 389: 382-385
53. Simonin F, Valverde O, Smadja C, Slowe S, Kitchen I, Dierich A, et al. Disruption of the kappa-opioid receptor gene in mice enhances sensitivity to chemical visceral pain, impairs pharmacological actions of the selective kappa-agonist U-50,488H and attenuates morphine withdrawal. EMBO J 1998; 17: 886-897
54. Kieffer BL, Gaveriaux-Ruff C. Exploring the opioid system by gene knockout. Prog Neurobiol 2002; 66: 285-306.
55. Aldrich JV, McLaughlin JP. Peptide kappa opioid receptor ligands: potential for drug development. AAPS J 2009; 11: 312-322
56. Riviere PJ. Peripheral kappa-opioid agonists for visceral pain. Br J Pharmacol 2004; 141: 1331-1334
57. Stein C, Clark JD, Oh U, Vasko MR, Wilcox GL, Overland AC, et al. Peripheral mechanisms of pain and analgesia. Brain Res Rev 2009; 60: 90-113.
58. Stein C, Lang LJ. Peripheral mechanisms of opioid analgesia. Curr Opin Pharmacol 2009; 9: 3-8.
59. Binder W, Machelska H, Mousa S, Schmitt T, Riviere PJ, Junien JL, et al. Analgesic and antiinflammatory effects of two novel kappa-opioid peptides. Anesthesiology 2001; 94: 1034-1044
60. Jolivalt CG, Jiang Y, Freshwater JD, Bartoszyk GD, Calcutt NA. Dynorphin A, kappa opioid receptors and the antinociceptive efficacy of asimadoline in streptozotocin-induced diabetic rats. Diabetologia 2006; 49: 2775-2785
61. Ko MC, Tuchman JE, Johnson MD, Wiesenauer K, Woods JH. Local administration of mu or kappa opioid agonists attenuates capsaicininduced thermal hyperalgesia via peripheral opioid receptors in rats. Psychopharmacology (Berl) 2000; 148: 180-185
62. Barber A, Bartoszyk GD, Bender HM, Gottschlich R, Greiner HE, Harting J, et al. A pharmacological profile of the novel, peripherallyselective kappa-opioid receptor agonist, EMD 61753. Br J Pharmacol 1994; 113: 1317-1327
63. Joshi SK, Su X, Porreca F, Gebhart GF. kappa -opioid receptor agonists modulate visceral nociception at a novel, peripheral site of action. J Neurosci 2000; 20: 5874-5879
64. Wang Y, Tang K, Inan S, Siebert D, Holzgrabe U, Lee DY, et al. Comparison of pharmacological activities of three distinct kappa ligands (Salvinorin A, TRK-820 and 3FLB) on kappa opioid receptors in vitro and their antipruritic and antinociceptive activities in vivo. J Pharmacol Exp Ther 2005; 312: 220-230
65. Pfeiffer A, Brantl V, Herz A, Emrich HM. Psychotomimesis mediated by kappa opiate receptors. Science 1986; 233: 774-776
66. Wadenberg ML. A review of the properties of spiradoline: a potent and selective kappa-opioid receptor agonist. CNS Drug Rev 2003; 9: 187-198
67. Bals-Kubik R, Ableitner A, Herz A, Shippenberg TS. Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J Pharmacol Exp Ther 1993; 264: 489-495
68. Mague SD, Pliakas AM, Todtenkopf MS, Tomasiewicz HC, Zhang Y, Stevens WC Jr, et al. Antidepressant-like effects of kappa-opioid receptor antagonists in the forced swim test in rats. J Pharmacol Exp Ther 2003; 305: 323-330
69. Carlezon WA Jr, Beguin C, DiNieri JA, Baumann MH, Richards MR, Todtenkopf MS, et al. Depressive-like effects of the kappa-opioid receptor agonist salvinorin A on behavior and neurochemistry in rats. J Pharmacol Exp Ther 2006; 316: 440-447
70. Carlezon WA Jr, Beguin C, Knoll AT, Cohen BM. Kappa-opioid ligands in the study and treatment of mood disorders. Pharmacol Ther 2009; 123: 334-343
71. Shippenberg TS, Herz A. Place preference conditioning reveals the involvement of D1-dopamine receptors in the motivational properties of mu-and kappa-opioid agonists. Brain Res 1987; 436: 169-172
72. Zhang Y, Butelman ER, Schlussman SD, Ho A, Kreek MJ. Effects of the plant-derived hallucinogen salvinorin A on basal dopamine levels in the caudate putamen and in a conditioned place aversion assay in mice: agonist actions at kappa opioid receptors. Psychopharmacology (Berl) 2005; 179: 551-558
73. Bruchas MR, Land BB, Aita M, Xu M, Barot SK, Li S, et al. Stressinduced p38 mitogen-activated protein kinase activation mediates kappa-opioid-dependent dysphoria. J Neurosci 2007; 27: 11614-11623
74. Sante AB, Nobre MJ, Brandao ML. Place aversion induced by blockade of mu or activation of kappa opioid receptors in the dorsal periaqueductal gray matter. Behav Pharmacol 2000; 11: 583-589
75. Redila VA, Chavkin C. Stress-induced reinstatement of cocaine seeking is mediated by the kappa opioid system. Psychopharmacology (Berl) 2008; 200: 59-70.
76. Valdez GR, Platt DM, Rowlett JK, Ruedi-Bettschen D, Spealman RD. Kappa agonist-induced reinstatement of cocaine seeking in squirrel monkeys: a role for opioid and stress-related mechanisms. J Pharmacol Exp Ther 2007; 323: 525-533
77. Carey AN, Borozny K, Aldrich JV, McLaughlin JP. Reinstatement of cocaine place-conditioning prevented by the peptide kappa-opioid receptor antagonist arodyn. Eur J Pharmacol 2007; 569: 84-89
78. Beardsley PM, Howard JL, Shelton KL, Carroll FI. Differential effects of the novel kappa opioid receptor antagonist, JDTic, on reinstatement of cocaine-seeking induced by footshock stressors vs cocaine primes and its antidepressant-like effects in rats. Psychopharmacology (Berl) 2005; 183: 118-126
79. Neumeyer JL, Bidlack JM, Zong R, Bakthavachalam V, Gao P, Cohen DJ, et al. Synthesis and opioid receptor affinity of morphinan and benzomorphan derivatives: mixed kappa agonists and mu agonists/antagonists as potential pharmacotherapeutics for cocaine dependence. J Med Chem 2000; 43: 114-122
80. Wang YJ, Tao YM, Li FY, Wang YH, Xu XJ, Chen J, et al. Pharmacological characterization of ATPM [(-)-3-aminothiazolo[5,4-b]-N- cyclopropylmethylmorphinan hydrochloride], a novel mixed kappa-agonist and mu-agonist/-antagonist that attenuates morphine antinociceptive tolerance and heroin self-administration behavior. J Pharmacol Exp Ther 2009; 329: 306-313
81. Gear RW, Miaskowski C, Gordon NC, Paul SM, Heller PH, Levine JD. The kappa opioid nalbuphine produces gender-and dose-dependent analgesia and antianalgesia in patients with postoperative pain. Pain 1999; 83: 339-345
82. Takemori AE, Loh HH, Lee NM. Suppression by dynorphin A and [des-Tyr1]dynorphin A peptides of the expression of opiate withdrawal and tolerance in morphine-dependent mice. J Pharmacol Exp Ther 1993; 266: 121-124
83. Vanderah TW, Gardell LR, Burgess SE, Ibrahim M, Dogrul A, Zhong CM, et al. Dynorphin promotes abnormal pain and spinal opioid antinociceptive tolerance. J Neurosci 2000; 20: 7074-7079
84. Koob GF, Volkow ND. Neurocircuitry of addiction. Neuropsychopharmacology; 35: 217-238
85. Tao YM, Li QL, Zhang CF, Xu XJ, Chen J, Ju YW, et al. LPK-26, a novel kappa-opioid receptor agonist with potent antinociceptive effects and low dependence potential. Eur J Pharmacol 2008; 584: 306-311
86. Specker S, Wananukul W, Hatsukami D, Nolin K, Hooke L, Kreek MJ, et al. Effects of dynorphin A(1-13) on opiate withdrawal in humans. Psychopharmacology (Berl) 1998; 137: 326-332
87. Greenwald MK, Stitzer ML, Haberny KA. Human pharmacology of the opioid neuropeptide dynorphin A(1-13). J Pharmacol Exp Ther 1997; 281: 1154-1163
88. Trigo JM, Martin-Garcia E, Berrendero F, Robledo P, Maldonado R. The endogenous opioid system: A common substrate in drug addiction. Drug Alcohol Depend 2009; 108: 183-194
89. Tomasiewicz HC, Todtenkopf MS, Chartoff EH, Cohen BM, Carlezon WA Jr. The kappa-opioid agonist U69,593 blocks cocaine-induced enhancement of brain stimulation reward. Biol Psychiatry 2008; 64: 982-988
90. Walsh SL, Geter-Douglas B, Strain EC, Bigelow GE. Enadoline and butorphanol: evaluation of kappa-agonists on cocaine pharmacodynamics and cocaine self-administration in humans. J Pharmacol Exp Ther 2001; 299: 147-158
91. Heidbreder CA, Goldberg SR, Shippenberg TS. The kappa-opioid receptor agonist U-69593 attenuates cocaine-induced behavioral sensitization in the rat. Brain Res 1993; 616: 335-338
92. Chefer VI, Moron JA, Hope B, Rea W, Shippenberg TS. Kappa-opioid receptor activation prevents alterations in mesocortical dopamine neurotransmission that occur during abstinence from cocaine. Neuroscience 2000; 101: 619-627
93. Gehrke BJ, Chefer VI, Shippenberg TS. Effects of acute and repeated administration of salvinorin A on dopamine function in the rat dorsal striatum. Psychopharmacology (Berl) 2008; 197: 509-517
94. McLaughlin JP, Land BB, Li S, Pintar JE, Chavkin C. Prior activation of kappa opioid receptors by U50,488 mimics repeated forced swim stress to potentiate cocaine place preference conditioning. Neuropsychopharmacology 2006; 31: 787-794
95. McLaughlin JP, Marton-Popovici M, Chavkin C. Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 2003; 23: 5674-5683
96. Mello NK, Negus SS. Interactions between kappa opioid agonists and cocaine. Preclinical studies. Ann N Y Acad Sci 2000; 909: 104-132
97. Archer S, Glick SD, Bidlack JM. Cyclazocine revisited. Neurochem Res 1996; 21: 1369-1373
98. Bowen CA, Negus SS, Zong R, Neumeyer JL, Bidlack JM, Mello NK. Effects of mixed-action kappa/mu opioids on cocaine self-administration and cocaine discrimination by rhesus monkeys. Neuropsychopharmacology 2003; 28: 1125-1139