The dysphoric component of stress is encoded by activation of the dynorphin κ-opioid system

Journal of Neuroscience

Volumn 28, Issue 2, 2008, Pages 407-414

  Land, Benjamin B ^a,b   Bruchas, Michael R ^a   Lemos, Julia C ^b   Xu, Mei ^a   Melief, Erica J ^a   Chavkin, Charles ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

opioid receptor; Aversion; Corticotropin releasing factor; Drug addiction; Dynorphin; Stress induced aversion

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; ANTALARMIN; ANTISAUVAGINE 30; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; DYNORPHIN; KAPPA OPIATE RECEPTOR; UROCORTIN III;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVERSION; AVERSIVE BEHAVIOR; BRAIN FUNCTION; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; DYSPHORIA; FOOTSHOCK; FORCED SWIMMING TEST; GENE DELETION; HIPPOCAMPUS; MALE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; STRESS;

3,4-DICHLORO-N-METHYL-N-(2-(1-PYRROLIDINYL)-CYCLOHEXYL)-BENZENEACETAMIDE, (TRANS)-ISOMER; ANALGESICS, NON-NARCOTIC; ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING, OPERANT; CORTICOTROPIN-RELEASING HORMONE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; DYNORPHINS; ENKEPHALINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NALTREXONE; NARCOTIC ANTAGONISTS; ODORS; PHOSPHORYLATION; PROTEIN PRECURSORS; RECEPTORS, OPIOID, KAPPA; STRESS; SWIMMING; UROCORTINS;

EID: 38349031157     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4458-07.2008     Document Type: Article

References (47)

1. Bale TL, Vale WW (2004) CRF and CRF receptors: role in stress responsivity and other behaviors. Annu Rev Pharmacol Toxicol 44:525-557.
2. Beardsley PM, Howard JL, Shelton KL, Carroll FI (2005) 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) 183:118-126.
3. Bruchas MR, Macey TA, Lowe JD, Chavkin C (2006) Kappa opioid receptor activation of p38 MAPK is GRK3-and arrestin-dependent in neurons and astrocytes. J Biol Chem 281:18081-18089.
4. Bruchas MR, Land BB, Aita M, Xu M, Barot SK, Li S, Chavkin C (2007) Stress-induced p38 mitogen activated protein kinase mediates κ-opioid dependent dysphoria. J Neurosci 27:11614-11623.
5. Cador M, Ahmed SH, Koob GF, Le Moal M, Stinus L (1992) Corticotropin-releasing factor induces a place aversion independent of its neuroendocrine role. Brain Res 597:304-309.
6. Carey AN, Borozny K, Aldrich JV, McLaughlin JP (2007) Reinstatement of cocaine place-conditioning prevented by the peptide kappa-opioid receptor antagonist arodyn. Eur J Phamacol 569:84-89.
7. Carlezon Jr WA, Beguin C, DiNieri JA, Baumann MH, Richards MR, Todtenkopf MS, Rothman RB, Ma Z, Lee DY, Cohen BM (2006) Depressive-like effects of the kappa-opioid receptor agonist salvinorin A on behavior and neurochemistry in rats. J Pharmacol Exp Ther 316:440-447.
8. Carrasco GA, Van de Kar LD (2003) Neuroendocrine pharmacology of stress. Eur J Pharmacol 463:235-272.
9. Chavkin C, James IF, Goldstein A (1982) Dynorphin is a specific endogenous ligand of the kappa opioid receptor. Science 215:413-415.
10. Contarino A, Papaleo F (2005) The corticotropin-releasing factor receptor-1 pathway mediates the negative affective states of opiate withdrawal. Proc Natl Acad Sci USA 102:18649-18654.
11. Erb S, Shaham Y, Stewart J (1998) The role of corticotropin-releasing factor and corticosterone in stress- and cocaine-induced relapse to cocaine seeking in rats. J Neurosci 18:5529-5536.
12. Fox HC, Bergquist KL, Hong KI, Sinha R (2007) Stress-induced and alcohol cue-induced craving in recently abstinent alcohol-dependent individuals. Alcohol Clin Exp Res 31:395-403.
13. Gabry KE, Chrousos GP, Rice KC, Mostafa RM, Sternberg E, Negrao AB, Webster EL, McCann SM, Gold PW (2002) Marked suppression of gastric ulcerogenesis and intestinal responses to stress by a novel class of drugs. Mol Psychiatry 7:474-483.
14. Gold PW, Chrousos GP (2002) Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs low CRH/NE states. Mol Psychiatry 7:254-275.
15. Griebel G, Simiand J, Steinberg R, Jung M, Gully D, Roger P, Geslin M, Scatton B, Maffrand JP, Soubrie P (2002) 4-(2-Chloro-4-methoxy-5-methylphenyl)- N-[(1S)-2-cyclopropyl-1-(3-fluoro-4-methylphenyl)ethyl]5-methyl-N-(2-propynyl) -1, 3-thiazol-2-amine hydrochloride (SSR125543A), a potent and selective corticotrophinreleasing factor(1) receptor antagonist. II. Characterization in rodent models of stress-related disorders. J Pharmacol Exp Ther 301:333-345.
16. Hammack SE, Schmid MJ, LoPresti ML, Der-Avakian A, Pellymounter MA, Foster AC, Watkins LR, Maier SF (2003) Corticotropin releasing hormone type 2 receptors in the dorsal raphe nucleus mediate the behavioral consequences of uncontrollable stress. J Neurosci 23:1019-1025.
17. Henry V, Vale W, Markou A (2006) The effect of lateral septum corticotropin-releasing factor receptor 2 activation on anxiety is modulated by stress. J Neurosci 26:9142-9152.
18. Keck ME, Ohl F, Holsboer F, Muller MB (2005) Listening to mutant mice: a spotlight on the role of CRF/CRF receptor systems in affective disorders. Neurosci Biobehav Rev 29:867-889.
19. Koob GF (2006) The neurobiology of addiction: a neuroadaptational view relevant for diagnosis. Addiction 101:23-30.
20. Koob GF, Kreek MJ (2007) Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am J Psychiatry 164:1149-1159.
21. Liu J, Yu B, Orozco-Cabal L, Grigoriadis DE, Rivier J, Vale WW, Shinnick-Gallagher P, Gallagher JP (2005) Chronic cocaine administration switches corticotropin-releasing factor2 receptor-mediated depression to facilitation of glutamatergic transmission in the lateral septum. J Neurosci 25:577-583.
22. Mague SD, Pliakas AM, Todtenkopf MS, Tomasiewicz HC, Zhang Y, Stevens Jr WC, Jones RM, Portoghese PS, Carlezon Jr WA (2003) Antidepressant-like effects of kappa-opioid receptor antagonists in the forced swim test in rats. J Pharmacol Exp Ther 305:323-330.
23. McLaughlin JP, Marton-Popovici M, Chavkin C (2003a) κ-Opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23:5674-5683.
24. McLaughlin JP, Xu M, Mackie K, Chavkin C (2003b) Phosphorylation of a carboxyl-terminal serine within the kappa-opioid receptor produces desensitization and internalization. J Biol Chem 278:34631-34640.
25. McLaughlin JP, Li S, Valdez J, Chavkin TA, Chavkin C (2006) Social defeat stress-induced behavioral responses are mediated by the endogenous kappa opioid system. Neuropsychopharmacology 31:1241-1248.
26. Narita M, Kaneko C, Miyoshi K, Nagumo Y, Kuzumaki N, Nakajima M, Nanjo K, Matsuzawa K, Yamazaki M, Suzuki T (2006) Chronic pain induces anxiety with concomitant changes in opioidergic function in the amygdala. Neuropsychopharmacology 31:739-750.
27. Nestler EJ, Carlezon Jr WA (2006) The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 59:1151-1159.
28. Nikolarakis KE, Almeida OF, Herz A (1986) Stimulation of hypothalamic beta-endorphin and dynorphin release by corticotropin-releasing factor (in vitro). Brain Res 399:152-155.
29. Paxinos G, Franklin KBJ (2004) The mouse brain in stereotaxic coordinates. San Diego: Elsevier.
30. Pfeiffer A, Brantl V, Herz A, Emrich HM (1986) Psychotomimesis mediated by kappa opiate receptors. Science 233:774-776.
31. Pliakas AM, Carlson RR, Neve RL, Konradi C, Nestler EJ, Carlezon Jr WA (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.
32. Porsolt RD, Le Pichon M, Jalfre M (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730-732.
33. Rivier J, Gulyas J, Kunitake K, DiGruccio M, Cantle JP, Perrin MH, Donaldson C, Vaughan J, Million M, Gourcerol G, Adelson DW, Rivier C, Tache Y, Vale W (2007) Stressin1-A, a potent corticotropin releasing factor receptor 1 (CRF1)-selective peptide agonist. J Med Chem 50:1668-1674.
34. Shaham Y, Funk D, Erb S, Brown TJ, Walker CD, Stewart J (1997) Corticotropin-releasing factor, but not corticosterone, is involved in stress-induced relapse to heroin-seeking in rats. J Neurosci 17:2605-2614.
35. Shaham Y, Erb S, Leung S, Buczek Y, Stewart J (1998) CP-154,526, a selective, non-peptide antagonist of the corticotropin-releasing factor1 receptor attenuates stress-induced relapse to drug seeking in cocaine- and heroin-trained rats. Psychopharmacology (Berl) 137:184-190.
36. Shippenberg TS, Herz A (1986) Differential effects of mu and kappa opioid systems on motivational processes. NIDA Res Monogr 75:563-566.
37. Song ZH, Takemori AE (1992) Stimulation by corticotropin-releasing factor of the release of immunoreactive dynorphin A from mouse spinal cords in vitro. Eur J Pharmacol 222:27-32.
38. Tache Y, Martinez V, Million M, Wang L (2001) Stress and the gastrointestinal tract III. Stress-related alterations of gut motor function: role of brain corticotropin-releasing factor receptors. Am J Physiol 280:G173-G177.
39. Tao R, Auerbach SB (2002) Opioid receptor subtypes differentially modulate serotonin efflux in the rat central nervous system. J Pharmacol Exp Ther 303:549-556.
40. Valdez GR, Platt DM, Rowlett JK, Ruedi-Bettschen D, Spealman RD (2007) Kappa agonist-induced reinstatment of cocaine seeking in squirrel monkeys: a role for opioid and stress-related mechanisms. J Pharmacol Exp Ther 323:525-533.
41. Volkow ND, Li TK (2004) Drug addiction: the neurobiology of behavior gone awry. Nat Rev Neurosci 5:963-970.
42. Wagner JJ, Terman GW, Chavkin C (1993) Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature 363:451-454.
43. Wang B, Shaham Y, Zitzman D, Azari S, Wise RA, You ZB (2005) Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin-releasing factor: a role in stress-induced relapse to drug seeking. J Neurosci 25:5389-5396.
44. Wang B, You ZB, Rice KC, Wise RA (2007) Stress-induced relapse to cocaine seeking: roles for the CRF(2) receptor and CRF-binding protein in the ventral tegmental area of the rat. Psychopharmacology (Berl) 193:283-294.
45. Wang J, Fang Q, Liu Z, Lu L (2005) Region-specific effects of brain corticotropin-releasing factor receptor type 1 blockade on footshockstress- or drug-priming-induced reinstatement of morphine conditioned place preference in rats. Psychopharmacology (Berl) 185:19-28.
46. Xu M, Bruchas MR, Ippolito DL, Gendron L, Chavkin C (2007) Sciatic nerve ligation-induced proliferation of spinal cord astrocytes is mediated by κ-opioid activation of p38 mitogen-activated protein kinase. J Neurosci 27:2570-2581.
47. Zobel AW, Nickel T, Kunzel HE, Ackl N, Sonntag A, Ising M, Holsboer F (2000) Effects of the high-affinity corticotropin-releasing hormone receptor 1 antagonist R121919 in major depression: the first 20 patients treated. J Psychiatr Res 34:171-181.