Depressive-like effects of the κ-opioid receptor agonist salvinorin A on behavior and neurochemistry in rats

Journal of Pharmacology and Experimental Therapeutics

Volumn 316, Issue 1, 2006, Pages 440-447

  Carlezon Jr , William A ^a   Béguin, Cécile ^a   DiNieri, Jennifer A ^a   Baumann, Michael H ^b   Richards, Michele R ^a   Todtenkopf, Mark S ^a   Rothman, Richard B ^b   Ma, Zhongze ^a   Lee, David Y W ^a   Cohen, Bruce M ^a   Carlezon, Bill ^a  

^a MCLEAN HOSPITAL   (United States)

^b NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; KAPPA OPIATE RECEPTOR AGONIST; SALVINORIN A; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DEPRESSION; DRUG EFFECT; DRUG EFFICACY; FORCED SWIMMING TEST; IMMOBILIZATION; LOCOMOTION; MALE; NEUROCHEMISTRY; NONHUMAN; NUCLEUS ACCUMBENS; OPEN FIELD TEST; PLANT LEAF; PRIORITY JOURNAL; RAT; SALVIA; SYMPTOMATOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN CHEMISTRY; DEPRESSION, CHEMICAL; DITERPENES; DOPAMINE; EXTRACELLULAR SPACE; MALE; MICRODIALYSIS; MOTOR ACTIVITY; PSYCHOTROPIC DRUGS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, KAPPA; SEROTONIN; SWIMMING;

EID: 29244488204     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.105.092304     Document Type: Article

References (40)

1. Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, Eisch AJ, Impey S, Storm DR, Neve RL, Yin JC, et al. (2002) CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci USA 99:11435-11440.
2. Baumann MH, Ayestas MA, Dersch CM, and Rothman RB (2001) 1-(m-Chlorophenyl) piperazine (mCPP) dissociates in vivo serotonin release from long-term serotonin depletion in rat brain. Neuropsychopharmacology 24:492-501.
3. Bucheler R, Gleiter CH, Schwoerer P, and Gaertner I (2005) Use of nonprohibited hallucinogenic plants: increasing relevance for public health? A case report and literature review on the consumption of Salvia divinorum (Diviner's Sage). Pharmacopsychiatry 38:1-5.
4. Carlezon WA Jr, Pliakas AM, Parrow AM, Detke MJ, Cohen BM, and Renshaw PF (2002) Antidepressant-like effects of cytidine in the forced swim test in rats. Biol Psychiatry 51:882-889.
5. Carlezon WA Jr, Thome J, Olson V, Lane-Ladd SB, Brodkin ES, Hiroi N, Duman RS, Neve RL, and Nestler EJ (1998) Regulation of cocaine reward by CREB. Science (Wash DC) 282:2272-2275.
6. Chappell PB, Leckman JF, Scahill LD, Hardin MT, Anderson G, and Cohen DJ (1993) Neuroendocrine and behavioral effects of the selective kappa agonist spiradoline in Tourette's syndrome: a pilot study. Psychiatry Res 47:267-280.
7. Chartoff EH, Papadopoulou M, Konradi C, and Carlezon WA Jr (2003) Dopamine-dependent increases in CREB phosphorylation during precipitated morphine withdrawal in primary cultures of rat striatum. J Neurochem 87:107-118.
8. Chavkin C, Sud S, Jin W, Stewart J, Zjawiony JK, Siebert DJ, Toth BA, Hufeisen SJ, and Roth BL (2004) Salvinorin A, an active component of the hallucinogenic sage Salvia divinorum is a highly efficacious kappa-opioid receptor agonist: structural and functional considerations. J Pharmacol Exp Ther 308:1197-1203.
9. Cryan JF, Markou A, and Lucki I (2002) Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23:238-245.
10. Detke MJ, Rickels M, and Lucki I (1995) Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology 121:66-72.
11. Devine DP, Leone P, Pocock D, and Wise RA (1993) Differential involvement of ventral tegmental mu, delta, and kappa opioid receptors in modulation of basal mesolimbic dopamine release: in vivo microdialysis studies. J Pharmacol Exp Ther 266:1236-1246.
12. DiChiara G and Imperato A (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85:5274-5278.
13. Donzanti BA, Althaus JS, Payson MM, and Von Voigtlander PF (1992) Kappa agonist-induced reduction in dopamine release: site of action and tolerance. Res Commun Chem Pathol Pharmacol 78:193-210.
14. Lee DY-W, Ma Z, Liu-Chen L-Y, Wang Y, Chen Y, Carlezon WA Jr, and Cohen BM (2005) Three new neoclerodane diterpenoids from the leaves of Salvia divinorum. Bioorg Med Chem 13:5635-5639.
15. Ma J, Ye N, Lange N, and Cohen BM (2003) Dynorphinergic GABA neurons are a target of both typical and atypical antipsychotic drugs in the nucleus accumbens shell, central amygdaloid nucleus and thalamic central medial nucleus. Neurosci 121:991-998.
16. Mague SD, Pliakas AM, Todtenkopf MS, Tomasiewicz HC, Zhang Y, Stevens WC Jr, Jones RM, Portoghese PS, and Carlezon WA Jr (2003) Antidepressant-like effects of κ-opioid receptor antagonists in the forced swim test in rats. J Pharmacol Exp Ther 305:323-330.
17. Maisonneuve IM, Archer S, and Glick SD (1994) U50,488, a κ-opioid receptor agonist, attenuates cocaine-induced increases in extracellular dopamine in the nucleus accumbens of rats. Neurosci Lett 181:57-60.
18. Margolis EB, Hjelmstad GO, Bonci A, and Fields HL (2003) Kappa-opioid agonists directly inhibit midbrain dopaminergic neurons. J Neurosci 23:9981-9986.
19. McLaughlin JP, Marton-Popovici M, and Chavkin C (2003) Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23:5674-5683.
20. Miliaressis E, Rompre PP, Laviolette P, Philippe L, and Coulombe D (1986) The curve-shift paradigm in self-stimulation. Physiol Behav 37:85-91.
21. Munro TA, Rizzacasa MA, Roth BL, Toth BA, and Yan F (2005) Studies toward the pharmacophore of salvinorin A, a potent kappa opioid receptor agonist. J Med Chem 48:345-348.
22. Nestler EJ and Carlezon WA Jr (2005) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry, in press.
23. Newton SS, Thome J, Wallace TL, Shirayama Y, Schlesinger L, Sakai N, Chen J, Neve R, Nestler EJ, and 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.
24. Pasquier DA, Kemper TL, Forbes WB, and Morgane PJ (1977) Dorsal raphe, substantia nigra and locus coeruleus: interconnections with each other and the neostriatum. Brain Res Bull 2:323-339.
25. Paxinos G and Watson C (1986) The Rat Brain in Stereotaxic Coordinates, 2nd ed., Academic Press, San Diego, CA.
26. Pfeiffer A, Brantl V, Herz A, and Emrich HM (1986) Psychotomimesis mediated by kappa opiate receptors. Science (Wash DC) 233:774-776.
27. Pliakas AM, Carlson R, Neve RL, Konradi C, Nestler EJ, and Carlezon WA Jr (2001) Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element binding protein expression in nucleus accumbens. J Neurosci 21:7397-7403.
28. Porsolt RD, Le Pichon M, and Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature (Lond) 266:730-732.
29. Roth BL, Baner K, Westkaemper R, Siebert D, Rice KC, Steinberg S, Ernsberger P, and Rothman RB (2002) Salvinorin A: a potent naturally occurring non-nitrogenous kappa opioid selective agonist. Proc Natl Acad Sci USA 99:11934-11939.
30. Rothman RB, Gorelick DA, Heishman SJ, Eichmiller PR, Hill BH, Norbeck J, and Liberto JG (2000) An open-label study of a functional opioid kappa antagonist in the treatment of opioid dependence. J Subst Abuse Treat 18:277-281.
31. Shaw-Lutchman TZ, Barrot M, Wallace T, Gilden L, Zachariou V, Impey S, Duman RS, Storm D, and Nestler EJ (2002) Regional and cellular mapping of cAMP response element-mediated transcription during naltrexone-precipitated morphine withdrawal. J Neurosci 22:3663-3672.
32. Shippenberg TS and Herz A (1987) Place preference conditioning reveals the involvement of D1-dopamine receptors in the motivational properties of mu- and kappa-opioid agonists. Brain Res 436:169-172.
33. Shippenberg TS and Rea W (1997) Sensitization to the behavioral effects of cocaine: modulation by dynorphin and kappa-opioid receptor agonists. Pharmacol Biochem Behav 57:449-455.
34. Spanagel R, Herz A, and Shippenberg TS (1992) Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc Natl Acad Sci USA 89:2046-2050.
35. Svingos AL, Colago EE, and Pickel VM (1999) Cellular sites for dynorphin activation of kappa-opioid receptors in the rat nucleus accumbens shell. J Neurosci 19:1804-1813.
36. Todtenkopf MS, Marcus JF, Portoghese PS, and Carlezon WA Jr (2004) Effects kappa opioid ligands on intracranial self-stimulation in rats. Psychopharmacology 172:463-470.
37. Walsh SL, Strain EC, Abreu ME, and Bigelow GE (2001) Enadoline, a selective kappa opioid agonist: comparison with butorphanol and hydromorphone in humans. Psychopharmacology 157:151-162.
38. Wise RA (1982) Neuroleptics and operant behavior: the anhedonia hypothesis. Behav Brain Sci 5:39-87.
39. Wise RA (1998) Drug-activation of brain reward pathways. Drug Alcohol Depend 51:13-22.
40. Zhang Y, Butelman ER, Schlussman SD, Ho A, and Kreek MJ (2005) 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 179:551-558.