Long-term antagonism of κ opioid receptors prevents escalation of and increased motivation for heroin intake

Journal of Neuroscience

Volumn 33, Issue 49, 2013, Pages 19384-19392

  Schlosburg, Joel E ^a   Whitfield Jr , Timothy W ^a   Park, Paula E ^a   Crawford, Elena F ^a   George, Olivier ^a   Vendruscolo, Leandro F ^a   Koob, George F ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNORPHIN; NORBINALTORPHIMINE; OPIATE RECEPTOR; PRODYNORPHIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; COMPULSION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NOCICEPTION; NONHUMAN; NUCLEUS ACCUMBENS; OPIATE ADDICTION; PRIORITY JOURNAL; RAT; REINFORCEMENT; VEIN CATHETERIZATION;

ANIMALS; ANXIETY; CATHETERIZATION; CONDITIONING, OPERANT; ENKEPHALINS; HEROIN DEPENDENCE; IMMUNOHISTOCHEMISTRY; MALE; MOTIVATION; NALTREXONE; NARCOTIC ANTAGONISTS; NUCLEUS ACCUMBENS; PROTEIN PRECURSORS; RATS; RATS, WISTAR; RECEPTORS, OPIOID, KAPPA; REINFORCEMENT SCHEDULE; SELF ADMINISTRATION; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 84888989742     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1979-13.2013     Document Type: Article

References (49)

1. Barbier E, Vendruscolo LF, Schlosburg JE, Edwards S, Juergens N, Park PE, Misra KK, Cheng K, Rice KC, Schank J, Schulteis G, Koob GF, Heilig M (2013) The NK1 Receptor Antagonist L822429 Reduces Heroin Reinforcement. Neuropsychopharmacology 38:976-984. CrossRef Medline
2. Bruchas MR, Yang T, Schreiber S, Defino M, Kwan SC, Li S, Chavkin C (2007) Long-acting kappa opioid antagonists disrupt receptor signaling and produce noncompetitive effects by activating c-Jun N-terminal kinase. J Biol Chem 282:29803-29811. CrossRef Medline
3. Bruchas MR, Land BB, Lemos JC, Chavkin C (2009) CRF1-R activation of the dynorphin/kappa opioid system in the mouse basolateral amygdala mediates anxiety-like behavior. PloS One 4:e8528. CrossRef Medline
4. Cappendijk SL, Hurd YL, Nylander I, van Ree JM, Terenius L (1999) A heroin-, but not a cocaine-expecting, self-administration state preferentially alters endogenous brain peptides. Eur J Pharmacol 365:175-182. CrossRef Medline
5. Carlezon WA Jr, Wise RA (1996) Rewarding actions of phencyclidine and related drugs in nucleus accumbens shell and frontal cortex. J Neurosci 16:3112-3122. Medline
6. Carlezon WA Jr, Duman RS, Nestler EJ (2005) The many faces of CREB. Trends Neurosci 28:436-445. CrossRef Medline
7. Chartoff E, Sawyer A, Rachlin A, Potter D, Pliakas A, Carlezon WA (2012) Blockade of kappa opioid receptors attenuates the development of depressive-like behaviors induced by cocaine withdrawal in rats. Neuropharmacology 62:167-176. CrossRef Medline
8. Chavkin C, James IF, Goldstein A (1982) Dynorphin is a specific endogenous ligand of the kappa opioid receptor. Science 215:413-415. CrossRef Medline
9. Clarke TK, Ambrose-Lanci L, Ferraro TN, Berrettini WH, Kampman KM, Dackis CA, Pettinati HM, O'Brien CP, Oslin DW, Lohoff FW (2012) Genetic association analyses of PDYN polymorphisms with heroin and cocaine addiction. Genes Brain Behav 11:415-423. CrossRef Medline
10. Edwards S, Vendruscolo LF, Schlosburg JE, Misra KK, Wee S, Park PE, Schulteis G, Koob GF (2012) Development of mechanical hypersensitivity in rats during heroin and ethanol dependence: alleviation by CRF(1) receptor antagonism. Neuropharmacology 62:1142-1151. CrossRef Medline
11. Gerra G, Leonardi C, Cortese E, D'Amore A, Lucchini A, Strepparola G, Serio G, Farina G, Magnelli F, Zaimovic A, Mancini A, Turci M, Manfredini M, Donnini C (2007) Human kappa opioid receptor gene (OPRK1) polymorphism is associated with opiate addiction. Am J Med Genet B Neuropsychiatr Genet 144B:771-775. CrossRef Medline
12. Horan P, Taylor J, Yamamura HI, Porreca F (1992) Extremely long-lasting antagonistic actions of nor-binaltorphimine (nor-BNI) in the mouse tailflick test. J Pharmacol Exp Ther 260:1237-1243. Medline
13. Jones DN, Holtzman SG (1992) Long term kappa-opioid receptor blockade following nor-binaltorphimine. Eur J Pharmacol 215:345-348. CrossRef Medline
14. Knoll AT, Meloni EG, Thomas JB, Carroll FI, Carlezon WA Jr (2007) Anxiolytic-like effects of kappa-opioid receptor antagonists in models of unlearned and learned fear in rats. J Pharmacol Exp Ther 323:838-845. CrossRef Medline
15. Koob GF (2008) A role for brain stress systems in addiction. Neuron 59:11-34. CrossRef Medline
16. Land BB, Bruchas MR, Schattauer S, Giardino WJ, Aita M, Messinger D, Hnasko TS, Palmiter RD, Chavkin C (2009) Activation of the kappa opioid receptor in the dorsal raphe nucleus mediates the aversive effects of stress and reinstates drug seeking. Proc Natl Acad Sci U S A 106:19168-19173. CrossRef Medline
17. Mague SD, Pliakas AM, Todtenkopf MS, Tomasiewicz HC, Zhang Y, Stevens WC Jr, Jones RM, Portoghese PS, Carlezon WA Jr (2003) Antidepressant-like effects of kappa-opioid receptor antagonists in the forced swim test in rats. J Pharmacol Exp Ther 305:323-330. CrossRef Medline
18. Margolis EB, Lock H, Chefer VI, Shippenberg TS, Hjelmstad GO, Fields HL (2006) Kappa opioids selectively control dopaminergic neurons projecting to the prefrontal cortex. Proc Natl Acad Sci U S A 103:2938-2942. CrossRef Medline
19. Munro TA, Berry LM, Van't Veer A, Béguin C, Carroll FI, Zhao Z, Carlezon WA Jr, Cohen BM (2012) Long-acting kappa opioid antagonists nor- BNI, GNTI and JDTic: pharmacokinetics in mice and lipophilicity. BMC Pharmacology 12:5. CrossRef Medline
20. Nealey KA, Smith AW, Davis SM, Smith DG, Walker BM (2011) kappaopioid receptors are implicated in the increased potency of intraaccumbens nalmefene in ethanol-dependent rats. Neuropharmacology 61:35-42. CrossRef Medline
21. Negus SS, Henriksen SJ, Mattox A, Pasternak GW, Portoghese PS, Takemori AE, Weinger MB, Koob GF (1993) Effect of antagonists selective for mu, delta and kappa opioid receptors on the reinforcing effects of heroin in rats. J Pharmacol Exp Ther 265:1245-1252. Medline
22. Newton SS, Thome J, Wallace TL, Shirayama Y, Schlesinger L, Sakai N, Chen J, Neve R, Nestler EJ, Duman RS (2002) Inhibition of cAMP response element-binding protein or dynorphin in the nucleus accumbens produces an antidepressant-like effect. J Neurosci 22:10883-10890. Medline
23. Nylander I, Vlaskovska M, Terenius L (1995) The effects of morphine treatment and morphine withdrawal on the dynorphin and enkephalin systems in Sprague-Dawley rats. Psychopharmacology (Berl) 118:391-400. CrossRef Medline
24. Pfeiffer A, Brantl V, Herz A, Emrich HM (1986) Psychotomimesis mediated by kappa opiate receptors. Science 233:774-776. CrossRef Medline
25. Potter DN, Damez-Werno D, Carlezon WA Jr, Cohen BM, Chartoff EH (2011) Repeated exposure to the kappa-opioid receptor agonist salvinorin A modulates extracellular signal-regulated kinase and reward sensitivity. Biol Psychiatry 70:744-753. CrossRef Medline
26. Redila VA, Chavkin C (2008) Stress-induced reinstatement of cocaine seeking is mediated by the kappa opioid system. Psychopharmacology (Berl) 200:59-70. CrossRef Medline
27. Rimoy GH, Wright DM, Bhaskar NK, Rubin PC (1994) The cardiovascular and CNS effects in the human of U-62066E. A selective opioid receptor agonist. Eur J Clin Pharmacol 46:203-207. Medline
28. Schank JR, Goldstein AL, Rowe KE, King CE, Marusich JA, Wiley JL, Carroll FI, Thorsell A, Heilig M (2012) The kappa opioid receptor antagonist JDTic attenuates alcohol seeking and withdrawal anxiety. Addict Biol 17:634-647. CrossRef Medline
29. Schindler AG, Messinger DI, Smith JS, Shankar H, Gustin RM, Schattauer SS, Lemos JC, Chavkin NW, Hagan CE, Neumaier JF, Chavkin C (2012) Stress produces aversion and potentiates cocaine reward by releasing endogenous dynorphins in the ventral striatum to locally stimulate serotonin reuptake. J Neurosci 32:17582-17596. CrossRef Medline
30. Shippenberg TS, Herz A (1986) Differential effects of mu and kappa opioid systems on motivational processes. NIDA Res Monogr 75:563-566. Medline
31. Shippenberg TS, Funada M, Schutz CG (2000) Dynorphin A (2-17) attenuates the unconditioned but not the conditioned effects of opiate withdrawal in the rat. Psychopharmacology (Berl) 151:351-358. CrossRef Medline
32. Sofuoglu M, Portoghese PS, Takemori AE (1992) Maintenance of acute morphine tolerance in mice by selective blockage of kappa opioid receptors with norbinaltorphimine. Eur J Pharmacol 210:159-162. CrossRef Medline
33. Solecki W, Ziolkowska B, Krowka T, Gieryk A, Filip M, Przewlocki R (2009) Alterations of prodynorphin gene expression in the rat mesocorticolimbic system during heroin self-administration. Brain Res 1255:113-121. CrossRef Medline
34. Suzuki T, Narita M, Takahashi Y, Misawa M, Nagase H (1992) Effects of nor-binaltorphimine on the development of analgesic tolerance to and physical dependence on morphine. Eur J Pharmacol 213:91-97. CrossRef Medline
35. Svingos AL, Chavkin C, Colago EE, Pickel VM (2001) Major coexpression of kappa-opioid receptors and the dopamine transporter in nucleus accumbens axonal profiles. Synapse 42:185-192. CrossRef Medline
36. Tjon GH, Voorn P, Vanderschuren LJ, de Vries TJ, Michiels NH, Jonker AJ, Klop H, Nestby P, Mulder AH, Schoffelmeer AN (1997) Delayed occurrence of enhanced striatal preprodynorphin gene expression in behaviorally sensitized rats: differential long-term effects of intermittent and chronic morphine administration. Neuroscience 76:167-176. Medline
37. Todtenkopf MS, Marcus JF, Portoghese PS, Carlezon WA Jr (2004) Effects of kappa-opioid receptor ligands on intracranial self-stimulation in rats. Psychopharmacology (Berl) 172:463-470. CrossRef Medline
38. United Nations Office for Drug Control and Crime Prevention (2012) World Drug Report 2012. Vienna: United Nations.
39. Valdez GR, Harshberger E (2012) Kappa opioid regulation of anxiety-like behavior during acute ethanol withdrawal. Pharmacol Biochem Behav 102:44-47. CrossRef Medline
40. Vendruscolo LF, Schlosburg JE, Misra KK, Chen SA, Greenwell TN, Koob GF (2011) Escalation patterns of varying periods of heroin access. Pharmacol Biochem Behav 98:570-574. CrossRef Medline
41. Walker BM, Koob GF (2008) Pharmacological evidence for a motivational role of kappa-opioid systems in ethanol dependence. Neuropsychopharmacology 33:643-652. CrossRef Medline
42. Walker BM, Zorrilla EP, Koob GF (2011) Systemic kappa-opioid receptor antagonism by nor-binaltorphimine reduces dependence-induced excessive alcohol self-administration in rats. Addict Biol 16:116-119. CrossRef Medline
43. Wee S, Koob GF (2010) The role of the dynorphin-kappa opioid system in the reinforcing effects of drugs of abuse. Psychopharmacology (Berl) 210: 121-135. CrossRef Medline
44. Wee S, Orio L, Ghirmai S, Cashman JR, Koob GF (2009) Inhibition of kappa opioid receptors attenuated increased cocaine intake in rats with extended access to cocaine. Psychopharmacology (Berl) 205:565-575. CrossRef Medline
45. Weissman BA,Zamir N (1987) Differential effects of heroin on opioid levels in the rat brain. Eur J Pharmacol 139:121-123. CrossRef Medline
46. Xi ZX, Fuller SA, Stein EA (1998) Dopamine release in the nucleus accumbens during heroin self-administration is modulated by kappa opioid receptors: an in vivo fast-cyclic voltammetry study. J Pharmacol Exp Ther 284:151-161. Medline
47. Yuferov V, Fussell D, LaForge KS, Nielsen DA, Gordon D, Ho A, Leal SM, Ott J, Kreek MJ (2004) Redefinition of the human kappa opioid receptor gene (OPRK1) structure and association of haplotypes with opiate addiction. Pharmacogenetics 14:793-804. CrossRef Medline
48. Zapata A, Shippenberg TS (2006) Endogenous kappa opioid receptor systems modulate the responsiveness of mesoaccumbal dopamine neurons to ethanol. Alcohol Clin Exp Res 30:592-597. CrossRef Medline
49. Zhou Y, Leri F, Grella SL, Aldrich JV, Kreek MJ (2013) Involvement of dynorphin and kappa opioid receptor in yohimbine-induced reinstatement of heroin seeking in rats. Synapse 67:358-361. CrossRef Medline