The role of kappa opioid receptors in stress-induced reinstatement of alcohol seeking in rats

Brain and Behavior

Volumn 4, Issue 3, 2014, Pages 356-367

  Funk, Douglas ^a   Coen, Kathleen ^a   Le A D ^a,b  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Alcohol self administration; Conditioned cue; CRF receptors; Kappa opioid receptors; Reinstatement; Stress

Indexed keywords

3, 4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL) CYCLOHEXYL] BENZENEACETAMIDE; ANTALARMIN; CORTICOTROPIN RELEASING FACTOR; KAPPA OPIATE RECEPTOR; UNCLASSIFIED DRUG; YOHIMBINE; 3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; ALCOHOL; CORTICOTROPIN RELEASING FACTOR RECEPTOR; NALTREXONE; NARCOTIC ANALGESIC AGENT; NARCOTIC ANTAGONIST; NORBINALTORPHIMINE; PYRIMIDINE DERIVATIVE; PYRROLE DERIVATIVE;

ALCOHOL CONSUMPTION; ALCOHOLISM; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CONTROLLED STUDY; DRINKING BEHAVIOR; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; STRESS; TRAINING; ADDICTION; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; ASSOCIATION; DRUG EFFECTS; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; LONG EVANS RAT; PHYSIOLOGICAL STRESS;

3,4-DICHLORO-N-METHYL-N-(2-(1-PYRROLIDINYL)-CYCLOHEXYL)-BENZENEACETAMIDE, (TRANS)-ISOMER; ANALGESICS, OPIOID; ANIMALS; BEHAVIOR, ADDICTIVE; BEHAVIOR, ANIMAL; CUES; DRUG-SEEKING BEHAVIOR; ETHANOL; MALE; NALTREXONE; NARCOTIC ANTAGONISTS; PYRIMIDINES; PYRROLES; RATS; RATS, LONG-EVANS; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RECEPTORS, OPIOID, KAPPA; SELF ADMINISTRATION; STRESS, PHYSIOLOGICAL; YOHIMBINE;

EID: 84896283479     PISSN: None     EISSN: 21623279     Source Type: Journal    
DOI: 10.1002/brb3.222     Document Type: Article

References (64)

1. Al-Hasani, R., J. G. McCall, A. M. Foshage, and M. R. Bruchas. 2013. Locus coeruleus kappa-opioid receptors modulate reinstatement of cocaine place preference through a noradrenergic mechanism. Neuropsychopharmacology 38:2484-2497.
2. Beardsley, P. M., J. L. Howard, K. L. Shelton, and F. I. Carroll. 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 183:118-126.
3. Beardsley, P. M., G. T. Pollard, J. L. Howard, and F. I. Carroll. 2010. Effectiveness of analogs of the kappa opioid receptor antagonist (3R)-7-hydroxy-N-((1S)-1-{[(3R, 4R)-4-(3- hydroxyphenyl)-3, 4-dimethyl-1-pipe ridinyl]methyl}-2- methylpropyl)- 1, 2, 3, 4-tetrahydro-3-isoquinolinecarboxami de (JDTic) to reduce U50, 488-induced diuresis and stress-induced cocaine reinstatement in rats. Psychopharmacology 210:189-198.
4. Berger, A. L., A. M. Williams, M. M. McGinnis, and B. M. Walker. 2013. Affective cue-induced escalation of alcohol self-administration and increased 22-kHz ultrasonic vocalizations during alcohol withdrawal: role of kappa-opioid receptors. Neuropsychopharmacology 38:647-654.
5. Broadbear, J. H., S. S. Negus, E. R. Butelman, B. R. de Costa, and J. H. Woods. 1994. Differential effects of systemically administered nor-binaltorphimine (nor-BNI) on kappa-opioid agonists in the mouse writhing assay. Psychopharmacology 115:311-319.
6. Brown, S. A., P. W. Vik, T. L. Patterson, I. Grant, and M. A. Schuckit. 1995. Stress, vulnerability and adult alcohol relapse. J. Stud. Alcohol 56:538-545.
7. Bruchas, M. R., B. B. Land, J. C. Lemos, and C. Chavkin. 2009. CRF1-R activation of the dynorphin/kappa opioid system in the mouse basolateral amygdala mediates anxiety-like behavior. PLoS ONE 4:e8528.
8. Canadian Council on Animal Care. 1993. Guide to the care and use of laboratory animals. 2nd ed. Vol. 1. Ottawa, ON, Canada.
9. Dawson, D. A., R. B. Goldstein, and B. F. Grant. 2007. Rates and correlates of relapse among individuals in remission from DSM-IV alcohol dependence: a 3-year follow-up. Alcohol. Clin. Exp. Res. 31:2036-2045.
10. Deehan, G. A., Jr, D. L. McKinzie, F. I. Carroll, W. J. McBride, and Z. A. Rodd. 2012. The long-lasting effects of JDTic, a kappa opioid receptor antagonist, on the expression of ethanol-seeking behavior and the relapse drinking of female alcohol-preferring (P) rats. Pharmacol. Biochem. Behav. 101:581-587.
11. Dityatev, A. E., and V. Y. Bolshakov. 2005. Amygdala, long-term potentiation, and fear conditioning. Neuroscientist 11:75-88.
12. Dunn, A. J., and A. H. Swiergiel. 2008. The role of corticotropin-releasing factor and noradrenaline in stress-related responses, and the inter-relationships between the two systems. Eur. J. Pharmacol. 583:186-193.
13. Endoh, T., H. Matsuura, C. Tanaka, and H. Nagase. 1992. Nor-binaltorphimine: a potent and selective kappa-opioid receptor antagonist with long-lasting activity in vivo. Arch. Int. Pharmacodyn. Ther. 316:30-42.
14. Feltenstein, M. W., and R. E. See. 2006. Potentiation of cue-induced reinstatement of cocaine-seeking in rats by the anxiogenic drug yohimbine. Behav. Brain Res. 174:1-8.
15. Funk, D., Z. Li, Y. Shaham, and A. D. Le. 2003. Effect of blockade of corticotropin-releasing factor receptors in the median raphe nucleus on stress-induced c-fos mRNA in the rat brain. Neuroscience 122:1-4.
16. Gianoulakis, C., J. P. de Waele, and J. Thavundayil. 1996. Implication of the endogenous opioid system in excessive ethanol consumption. Alcohol 13:19-23.
17. Grilli, M., E. Neri, S. Zappettini, F. Massa, A. Bisio, G. Romussi, et al. 2009. Salvinorin A exerts opposite presynaptic controls on neurotransmitter exocytosis from mouse brain nerve terminals. Neuropharmacology 57:523-530.
18. Holter, S. M., M. S. Henniger, A. W. Lipkowski, and R. Spanagel. 2000. Kappa-opioid receptors and relapse-like drinking in long-term ethanol-experienced rats. Psychopharmacology 153:93-102.
19. Jackson, K. J., J. P. McLaughlin, F. I. Carroll, and M. I. Damaj. 2012. Effects of the kappa opioid receptor antagonist, norbinaltorphimine, on stress and drug-induced reinstatement of nicotine-conditioned place preference in mice. Psychopharmacology 222:763-768.
20. Johansen, J. P., C. K. Cain, L. E. Ostroff, and J. E. LeDoux. 2011. Molecular mechanisms of fear learning and memory. Cell 147:509-524.
21. Jones, D. N., and S. G. Holtzman. 1992. Long term kappa-opioid receptor blockade following nor-binaltorphimine. Eur. J. Pharmacol. 215:345-348.
22. Karoly, H. C., and K. E. Hutchison. 2012. Does stress contribute to the incubation of craving? Biol. Psychiatry 71:e39.
23. Lam, M. P., and C. Gianoulakis. 2011. Effects of corticotropin-releasing hormone receptor antagonists on the ethanol-induced increase of dynorphin A1-8 release in the rat central amygdala. Alcohol 45:621-630.
24. Land, B. B., M. R. Bruchas, J. C. Lemos, M. Xu, E. J. Melief, and C. Chavkin. 2008. The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J. Neurosci. 28:407-414.
25. Le, A., and Y. Shaham. 2002a. Neurobiology of relapse to alcohol in rats. Pharmacol. Ther. 94:137-156.
26. Le, A. D., and Y. Shaham. 2002b. Neurobiology of relapse to alcohol in rats. Pharmacol. Ther. 94:137-156.
27. Le, A. D., B. Quan, W. Juzystch, P. J. Fletcher, N. Joharchi, and Y. Shaham. 1998. Reinstatement of alcohol-seeking by priming injections of alcohol and exposure to stress in rats. Psychopharmacology 135:169-174.
28. Le, A. D., S. Harding, W. Juzytsch, J. Watchus, U. Shalev, and Y. Shaham. 2000. The role of corticotrophin-releasing factor in stress-induced relapse to alcohol-seeking behavior in rats. Psychopharmacology 150:317-324.
29. Le, A. D., S. Harding, W. Juzytsch, D. Funk, and Y. Shaham. 2005. Role of alpha-2 adrenoceptors in stress-induced reinstatement of alcohol seeking and alcohol self-administration in rats. Psychopharmacology 179:366-373.
30. Le, A. D., D. Funk, S. Harding, W. Juzytsch, and P. J. Fletcher. 2009. The role of noradrenaline and 5-hydroxytryptamine in yohimbine-induced increases in alcohol-seeking in rats. Psychopharmacology 204:477-488.
31. Le, A. D., D. Funk, W. Juzytsch, K. Coen, B. M. Navarre, C. Cifani, et al. 2011. Effect of prazosin and guanfacine on stress-induced reinstatement of alcohol and food seeking in rats. Psychopharmacology 218:89-99.
32. Liu, X., and F. Weiss. 2002. Additive effect of stress and drug cues on reinstatement of ethanol seeking: exacerbation by history of dependence and role of concurrent activation of corticotropin-releasing factor and opioid mechanisms. J. Neurosci. 22:7856-7861.
33. Mague, S. D., A. M. Pliakas, M. S. Todtenkopf, H. C. Tomasiewicz, Y. Zhang, W. C. Stevens Jr, et al. 2003. Antidepressant-like effects of kappa-opioid receptor antagonists in the forced swim test in rats. J. Pharmacol. Exp. Ther. 305:323-330.
34. Mansour, A., H. Khachaturian, M. E. Lewis, H. Akil, and S. J. Watson. 1987. Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J. Neurosci. 7:2445-2464.
35. Mansour, A., C. A. Fox, S. Burke, F. Meng, R. C. Thompson, H. Akil, et al. 1994. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J. Comp. Neurol. 350:412-438.
36. Maren, S. 1996. Synaptic transmission and plasticity in the amygdala. An emerging physiology of fear conditioning circuits. Mol. Neurobiol. 13:1-22.
37. Marinelli, P. W., D. Funk, W. Juzytsch, S. Harding, K. C. Rice, Y. Shaham, et al. 2007a. The CRF1 receptor antagonist antalarmin attenuates yohimbine-induced increases in operant alcohol self-administration and reinstatement of alcohol seeking in rats. Psychopharmacology 195:345-355.
38. Marinelli, P. W., D. Funk, W. Juzytsch, Z. Li, and A. D. Le. 2007b. Effects of opioid receptor blockade on the renewal of alcohol seeking induced by context: relationship to c-fos mRNA expression. Eur. J. Neurosci. 26:2815-2823.
39. Marinelli, P. W., D. Funk, S. Harding, Z. Li, W. Juzytsch, and A. D. Le. 2009. Roles of opioid receptor subtypes in mediating alcohol-seeking induced by discrete cues and context. Eur. J. Neurosci. 30:671-678.
40. Marinelli, P. W., D. Funk, W. Juzytsch, and A. D. Le. 2010. Opioid receptors in the basolateral amygdala but not dorsal hippocampus mediate context-induced alcohol seeking. Behav. Brain Res. 211:58-63.
41. Mason, B. J., Y. Shaham, F. Weiss, and A. D. Le. 2009. Stress, alcohol craving, and relapse risk: mechanisms and viable treatment targets. Alcohol 43:541-543.
42. McLaughlin, J. P., M. Marton-Popovici, and C. Chavkin. 2003. k Opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J. Neurosci. 23:5674.
43. McLaughlin, J. P., B. B. Land, S. Li, J. E. Pintar, and C. Chavkin. 2006. Prior activation of kappa opioid receptors by U50, 488 mimics repeated forced swim stress to potentiate cocaine place preference conditioning. Neuropsychopharmacology 31:787-794.
44. Meister, B., M. J. Villar, S. Ceccatelli, and T. Hokfelt. 1990. Localization of chemical messengers in magnocellular neurons of the hypothalamic supraoptic and paraventricular nuclei: an immunohistochemical study using experimental manipulations. Neuroscience 37:603-633.
45. Nikolarakis, K. E., O. F. Almeida, and A. Herz. 1986. Stimulation of hypothalamic beta-endorphin and dynorphin release by corticotropin-releasing factor (in vitro). Brain Res. 399:152-155.
46. Pliakas, A. M., R. R. Carlson, R. L. Neve, C. Konradi, E. J. Nestler, and W. A. Carlezon 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.
47. Pradhan, A. A., K. Befort, C. Nozaki, C. Gaveriaux-Ruff, and B. L. Kieffer. 2011. The delta opioid receptor: an evolving target for the treatment of brain disorders. Trends Pharmacol. Sci. 32:581-590.
48. Redila, V. A., and C. Chavkin. 2008. Stress-induced reinstatement of cocaine seeking is mediated by the kappa opioid system. Psychopharmacology 200:59-70.
49. Reyes, B. A., G. Drolet, and E. J. Van Bockstaele. 2008. Dynorphin and stress-related peptides in rat locus coeruleus: contribution of amygdalar efferents. J. Comp. Neurol. 508:663-675.
50. Schank, J. R., A. L. Goldstein, K. E. Rowe, C. E. King, J. A. Marusich, J. L. Wiley, et al. 2012. The kappa opioid receptor antagonist JDTic attenuates alcohol seeking and withdrawal anxiety. Addict. Biol. 17:634-647.
51. Schindler, A. G., S. Li, and C. Chavkin. 2010. Behavioral stress may increase the rewarding valence of cocaine-associated cues through a dynorphin/kappa-opioid receptor-mediated mechanism without affecting associative learning or memory retrieval mechanisms. Neuropsychopharmacology 35:1932-1942.
52. Shirayama, Y., H. Ishida, M. Iwata, G. I. Hazama, R. Kawahara, and R. S. Duman. 2004. Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. J. Neurochem. 90:1258.
53. Sinha, R., and C. S. Li. 2007. Imaging stress- and cue-induced drug and alcohol craving: association with relapse and clinical implications. Drug Alcohol Rev. 26:25-31.
54. Smith, J. S., A. G. Schindler, E. Martinelli, R. M. Gustin, M. R. Bruchas, and C. Chavkin. 2012. Stress-induced activation of the dynorphin/kappa-opioid receptor system in the amygdala potentiates nicotine conditioned place preference. J. Neurosci. 32:1488-1495.
55. Sperling, R. E., S. M. Gomes, E. I. Sypek, A. N. Carey, and J. P. McLaughlin. 2010. Endogenous kappa-opioid mediation of stress-induced potentiation of ethanol-conditioned place preference and self-administration. Psychopharmacology 210:199-209.
56. Valdez, G. R., D. M. Platt, J. K. Rowlett, D. Ruedi-Bettschen, and R. D. Spealman. 2007. Kappa agonist-induced reinstatement of cocaine seeking in squirrel monkeys: a role for opioid and stress-related mechanisms. J. Pharmacol. Exp. Ther. 323:525-533.
57. Van Bockstaele, E. J., B. A. Reyes, and R. J. Valentino. 2010. The locus coeruleus: a key nucleus where stress and opioids intersect to mediate vulnerability to opiate abuse. Brain Res. 1314:162-174.
58. Walker, B. M., E. P. Zorrilla, and G. F. Koob. 2011. Systemic kappa-opioid receptor antagonism by nor-binaltorphimine reduces dependence-induced excessive alcohol self-administration in rats. Addict. Biol. 16:116-119.
59. Walker, B. M., G. R. Valdez, J. P. McLaughlin, and G. Bakalkin. 2012. Targeting dynorphin/kappa opioid receptor systems to treat alcohol abuse and dependence. Alcohol 46:359-370.
60. Weathington, J. M., and B. M. Cooke. 2012. Corticotropin-releasing factor receptor binding in the amygdala changes across puberty in a sex-specific manner. Endocrinology 153:5701-5705.
61. Yajima, F., T. Suda, N. Tomori, T. Sumitomo, Y. Nakagami, T. Ushiyama, et al. 1986. Effects of opioid peptides on immunoreactive corticotropin-releasing factor release from the rat hypothalamus in vitro. Life Sci. 39:181-186.
62. Young, E. J., and C. L. Williams. 2013. Differential activation of amygdala expression by positive and negatively valenced emotional learning conditions. Front Behav. Neurosci. 7:191.
63. Zhou, Y., F. Leri, S. L. Grella, J. V. Aldrich, and M. J. Kreek. 2013. Involvement of dynorphin and kappa opioid receptor in yohimbine-induced reinstatement of heroin seeking in rats. Synapse 67:358-361.
64. Zilles, K., M. Qu, and A. Schleicher. 1993. Regional distribution and heterogeneity of alpha-adrenoceptors in the rat and human central nervous system. J. Hirnforsch. 34:123-132.