Exposure to chronic mild stress prevents kappa opioid-mediated reinstatement of cocaine and nicotine place preference

Frontiers in Pharmacology

Volumn 4 AUG, Issue , 2013, Pages

  Al Hasani, Ream ^a   McCall, Jordan G ^a   Bruchas, Michael R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cocaine; Conditioned place preference; Kappa opioid receptor; Nicotine; Stress

Indexed keywords

COCAINE; KAPPA OPIATE RECEPTOR; NICOTINE;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BED; BEHAVIOR CONTROL; CAGE; CHRONIC STRESS; CONTROLLED STUDY; FORCED SWIMMING TEST; HUMAN; ILLUMINATION; MALE; MOUSE; NESTING; NONHUMAN; PLACE PREFERENCE; REGULATORY MECHANISM; REWARD; SLEEP QUALITY; SOCIAL STRESS; WATER DEPRIVATION; WHITE NOISE;

EID: 84881606775     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2013.00096     Document Type: Article

References (59)

1. Aguilar, M. A., Rodríguez-Arias, M., and Miñarro, J. (2009). Neurobiological mechanisms of the reinstatement of drug-conditioned place preference. Brain Res. Rev. 59, 253-277. doi: 10.1016/j.brainresrev.2008.08.002
2. Al-Hasani, R., and Bruchas, M. R. (2011). Molecular mechanisms of opioid receptor-dependent signaling and behavior. Anesthesiology 115, 1363-1381. doi: 10.1097/ALN.0b013e318238bba6
3. Al-Hasani, R., McCall, J. G., Foshage, A. M., and Bruchas, M. R. (2013). Locus coeruleus kappa opioid receptors modulate reinstatement of cocaine place preference through a noradrenergic mechanism. Neuropsychopharmacology doi: 10.1038/npp.2013.151 [Epub ahead of print].
4. Beardsley, P. M., Howard, J. L., Shelton, K. L., and Carroll, F. I. (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. doi: 10.1007/s00213-005-0167-4
5. Bergström, A., Jayatissa, M. N., Mørk, A., and Wiborg, O. (2008). Stress sensitivity and resilience in the chronic mild stress rat model of depression; an in situ hybridization study. Brain Res. 1196, 41-52. doi: 10.1016/j.brainres.2007.12.025
6. Bertrand, E., Smadja, C., Mauborgne, A., Roques, B. P., and Daugé, V. (1997). Social interaction increases the extracellular levels of [Met]enkephalin in the nucleus accumbens of control but not of chronic mild stressed rats. Neuroscience 80, 17-20.
7. Bilkei-Gorzo, A., Rácz, I., Michel, K., Darvas, M., Maldonado, R., and Zimmer, A. (2008). A common genetic predisposition to stress sensitivity and stress-induced nicotine craving. Biol. Psychiatry 63, 164-171. doi:10.1016/j.biopsych.2007.02.010
8. Bruchas, M. R., Land, B. B., Aita, M., Xu, M., Barot, S. K., Li, S., et al. (2007a). Stress-induced p38 mitogen-activated protein kinase activation mediates kappa-opioid-dependent dysphoria. J. Neurosci. 27, 11614-11623. doi: 10.1523/JNEUROSCI.3769-07.2007
9. Bruchas, M. R., Yang, T., Schreiber, S., Defino, M., Kwan, S. C., Li, S., et al. (2007b). 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. doi: 10.1074/jbc.M705540200
10. Bruchas, M. R., Land, B. B., and Chavkin, C. (2010). The dynorphin/kappa opioid system as a modulator of stress-induced and pro-addictive behaviors. Brain Res. 1314, 44-55. doi: 10.1016/j.brainres.2009.08.062
11. Bruchas, M. R., Macey, T. A., Lowe, J. D., and 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. doi: 10.1074/jbc.M513640200
12. Bruchas, M. R., Schindler, A. G., Shankar, H., Messinger, D. I., Miyatake, M., Land, B. B., et al. (2011). Selective p38α MAPK deletion in serotonergic neurons produces stress resilience in models of depression and addiction. Neuron 71, 498-511. doi: 10.1016/j.neuron.2011.06.011
13. Bruijnzeel, A. W. (2012). Tobacco addiction and the dysregulation of brain stress systems. Neurosci. Biobehav. Rev. 36, 1418-1441. doi: 10.1016/j.neubiorev.2012.02.015
14. Buczek, Y., Lê, A. D., Wang, A., Stewart, J., and Shaham, Y. (1999). Stress reinstates nicotine seeking but not sucrose solution seeking in rats. Psychopharmacology (Berl.) 144, 183-188.
15. Carlezon, W. A. Jr., Béguin, C., DiNieri, J. A., Baumann, M. H., Richards, M. R., Todtenkopf, M. S., et al. (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.
16. Chartoff, E., Sawyer, A., Rachlin, A., Potter, D., Pliakas, A., and Carlezon, W. A. (2012). Blockade of kappa opioid receptors attenuates the development of depressive-like behaviors induced by cocaine withdrawal in rats. Neuropharmacology 62, 167-176. doi: 10.1016/j.neuropharm.2011.06.014
17. Chen, Y., Chen, C., and Liu-Chen, L.-Y. (2007). Dynorphin peptides differentially regulate the human kappa opioid receptor. Life Sci. 80, 1439-1448. doi: 10.1016/j.lfs.2007.01.018
18. Covington, H. E. III, and Miczek, K. A. (2001). Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration "binges." Psychopharmacology (Berl.) 158, 388-398. doi: 10.1007/s002130100858
19. Ebner, S. R., Roitman, M. F., Potter, D. N., Rachlin, A. B., and Chartoff, E. H. (2010). Depressive-like effects of the kappa opioid receptor agonist salvinorin A are associated with decreased phasic dopamine release in the nucleus accumbens. Psychopharmacology (Berl.) 210, 241-252. doi: 10.1007/s00213-010-1836-5
20. Elizalde, N., Gil-Bea, F. J., Ramírez, M. J., Aisa, B., Lasheras, B., Del Rio, J., et al. (2008). Long-lasting behavioral effects and recognition memory deficit induced by chronic mild stress in mice: effect of antidepressant treatment. Psychopharmacology (Berl.) 199, 1-14. doi: 10.1007/s00213-007-1035-1
21. Gehrke, B. J., Chefer, V. I., and Shippenberg, T. S. (2008). Effects of acute and repeated administration of salvinorin A on dopamine function in the rat dorsal striatum. Psychopharmacology (Berl.) 197, 509-517. doi: 10.1007/s00213-007-1067-6
22. Giros, B., Jaber, M., Jones, S. R., Wightman, R. M., and Caron, M. G. (1996). Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379, 606-612. doi: 10.1038/379606a0
23. Graziane, N. M., Polter, A. M., Briand, L. A., Pierce, R. C., and Kauer, J. A. (2013). Kappa opioid receptors regulate stress-induced cocaine seeking and synaptic plasticity. Neuron 77, 942-954. doi: 10.1016/j.neuron.2012.12.034
24. Hill, M. N., Hellemans, K. G. C., Verma, P., Gorzalka, B. B., and Weinberg, J. (2012). Neurobiology of chronic mild stress: parallels to major depression. Neurosci. Biobehav. Rev. 36, 2085-2117. doi: 10.1016/j.neubiorev.2012.07.001
25. Jackson, K. J., McLaughlin, J. P., Carroll, F. I., and Damaj, M. I. (2013). Effects of the kappa opioid receptor antagonist, norbinaltorphimine, on stress and drug-induced reinstatement of nicotine-conditioned place preference in mice. Psychopharmacology (Berl.) 226, 763-768. doi: 10.1007/s00213-012-2716-y
26. Koob, G., and Kreek, M. J. (2007). Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am. J. Psychiatry 164, 1149-1159. doi: 10.1176/appi.ajp.2007.05030503
27. Koob, G. F. (2008). A role for brain stress systems in addiction. Neuron 59, 11-34. doi: 10.1016/j.neuron.2008.06.012
28. Land, B. B., Bruchas, M. R., Lemos, J. C., Xu, M., Melief, E. J., and Chavkin, C. (2008). The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J. Neurosci. 28, 407-414. doi: 10.1523/JNEUROSCI.4458-07.2008
29. Land, B. B., Bruchas, M. R., Schattauer, S., Giardino, W. J., Aita, M., Messinger, D., et al. (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. doi: 10.1073/pnas.0910705106
30. Leão, R. M., Cruz, F. C., Marin, M. T., and Planeta Cda, S. (2012). Stress induces behavioral sensitization, increases nicotine-seeking behavior and leads to a decrease of CREB in the nucleus accumbens. Pharmacol. Biochem. Behav. 101, 434-442. doi: 10.1016/j.pbb.2012.01.025
31. Lemos, J. C., Roth, C. A., Messinger, D. I., Gill, H. K., Phillips, P. E. M., and Chavkin, C. (2012a). Repeated stress dysregulates κ-opioid receptor signaling in the dorsal raphe through a p38α MAPK-dependent mechanism. J. Neurosci. 32, 12325-12336. doi: 10.1523/JNEUROSCI.2053-12.2012
32. Lemos, J. C., Wanat, M. J., Smith, J. S., Reyes, B. A. S., Hollon, N. G., Van Bockstaele, E. J., et al. (2012b). Severe stress switches CRF action in the nucleus accumbens from appetitive to aversive. Nature 490, 402-406. doi: 10.1038/nature11436
33. McEwen, B. S., and Gianaros, P. J. (2011). Stress- and allostasis-induced brain plasticity. Annu. Rev. Med. 62, 431-445. doi: 10.1146/annurev-med-052209-100430
34. McLaughlin, J. P., Land, B. B., Li, S., Pintar, J. E., and Chavkin, C. (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. doi: 10.1038/sj.npp.1300860
35. McLaughlin, J. P., 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.
36. McLaughlin, J. P., Myers, L. C., Zarek, P. E., Caron, M. G., Lefkowitz, R. J., Czyzyk, T. A., et al. (2004). Prolonged kappa opioid receptor phosphorylation mediated by G-protein receptor kinase underlies sustained analgesic tolerance. J. Biol. Chem. 279, 1810-1818. doi: 10.1074/jbc.M305796200
37. Peng, Y.-L., Liu, Y.-N., Liu, L., Wang, X., Jiang, C.-L., and Wang, Y.-X. (2012). Inducible nitric oxide synthase is involved in the modulation of depressive behaviors induced by unpredictable chronic mild stress. J. Neuroinflammation 9, 75. doi: 10.1186/1742-2094-9-75
38. Plaza-Zabala, A., Martín-García, E., de Lecea, L., Maldonado, R., and Berrendero, F. (2010). Hypocretins regulate the anxiogenic-like effects of nicotine and induce reinstatement of nicotine-seeking behavior. J. Neurosci. 30, 2300-2310. doi: 10.1523/JNEUROSCI.5724-09.2010
39. Potter, D. N., Damez-Werno, D., Carlezon, W. A. Jr., Cohen, B. M., and Chartoff, E. H. (2011). Repeted exposure to kappa-opioid receptor agonist salvinorin A modulates extracellular signal-regulated kinase and reward sensitivity. Biol. Psychiatry 70, 744-753. doi: 10.1016/j.biopsych.2011.05.021
40. Rasheed, N., Tyagi, E., Ahmad, A., Siripurapu, K. B., Lahiri, S., Shukla, R., et al. (2008). Involvement of monoamines and proinflammatory cytokines in mediating the anti-stress effects of Panax quinquefolium. J. Ethnopharmacol. 117, 257-262. doi: 10.1016/j.jep.2008.01.035
41. Redila, V. A., and Chavkin, C. (2008). Stress-induced reinstatement of cocaine seeking is mediated by the kappa opioid system. Psychopharmacology (Berl.) 200, 59-70. doi: 10.1007/s00213-008-1122-y
42. Reith, M. E. (1986). Effect of repeated administration of various doses of cocaine and WIN 35,065-2 on locomotor behavior of mice. Eur. J. Pharmacol. 130, 65-72. doi: 10.1016/0014-2999(86)90184-6
43. Schindler, A. G., Messinger, D. I., Smith, J. S., Shankar, H., Gustin, R. M., Schattauer, S. S., et al. (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. doi: 10.1523/JNEUROSCI.3220-2.2012
44. Smith, J. S., Schindler, A. G., Martinelli, E., Gustin, R. M., Bruchas, M. R., and Chavkin, C. (2012). Stress-induced activation of the dynorphin/κ-opioid receptor system in the amygdala potentiates nicotine conditioned place preference. J. Neurosci. 32, 1488-1495. doi: 10.1523/JNEUROSCI.2980-11.2012
45. Sora, I., Wichems, C., Takahashi, N., Li, X. F., Zeng, Z., Revay, R., et al. (1998). Cocaine reward models: conditioned place preference can be established in dopamine- and in serotonin-transporter knockout mice. Proc. Natl. Acad. Sci. U.S.A. 95, 7699-7704. doi: 10.1073/pnas.95.13.7699
46. Tolliver, B. K., Belknap, J. K., Woods, W. E., and Carney, J. M. (1994). Genetic analysis of sensitization and tolerance to cocaine. J. Pharmacol. Exp. Ther. 270, 1230-1238.
47. Tye, K. M., Mirzabekov, J. J., Warden, M. R., Ferenczi, E. A., Tsai, H.-C., Finkelstein, J., et al. (2013). Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493, 537-541. doi: 10.1038/nature11740
48. Tzschentke, T. M. (2007). Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict. Biol. 12, 227-462. doi: 10.1111/j.1369-1600.2007.00070.x
49. Van Bockstaele, E. J., Reyes, B. A. S., and Valentino, R. J. (2010). The locus coeruleus: a key nucleus where stress and opioids intersect to mediate vulnerability to opiate abuse. Brain Res. 1314, 162-174. doi: 10.1016/j.brainres.2009.09.036
50. Vancassel, S., Leman, S., Hanonick, L., Denis, S., Roger, J., Nollet, M., et al. (2008). n-3 polyunsaturated fatty acid supplementation reverses stress-induced modifications on brain monoamine levels in mice. J. Lipid Res. 49, 340-348. doi: 10.1194/jlr.M700328-JLR200
51. Walker, B. M., and Koob, G. F. (2008). Pharmacological evidence for a motivational role of kappa-opioid systems in ethanol dependence. Neuropsychopharmacology 33, 643-652. doi: 10.1038/sj.npp.1301438
52. Walker, B. M., Zorrilla, E. P., and Koob, G. F. (2011). Systemic κ-opioid recep - tor antagonism by nor-binaltorphi - mine reduces dependence-induced excessive alcohol self-administration in rats. Addict. Biol. 16, 116-119. doi: 10.1111/j.1369-1600.2010.00226.x
53. Wang, Y., Li, J.-G., Huang, P., Xu, W., and Liu-Chen, L.-Y. (2003). Differential effects of agonists on adenylyl cyclase superactivation mediated by the kappa opioid receptors: adenylyl cyclase superactivation is independent of agonist-induced phosphorylation, desensitization, internalization, and down-regulation. J. Pharmacol. Exp. Ther. 307, 1127-1134. doi: 10.1124/jpet.103.055814
54. Wee, S., and Koob, G. F. (2010). The role of the dynorphin-kappa opioid system in the reinforcing effects of drugs of abuse. Psychopharmacology (Berl.) 210, 121-135. doi: 10.1007/s00213-010-1825-8
55. Williams, J. T., Ingram, S. L., Henderson, G., Chavkin, C., von Zastrow, M., Schulz, S., et al. (2013). Regulation of μ-opioid receptors: desensitization, phosphorylation, internalization, and tolerance. Pharmacol. Rev. 65, 223-254. doi: 10.1124/pr.112.005942
56. Wise, R. A. (2004). Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483-494. doi: 10.1038/nrn1406
57. Yamada, H., and Bruijnzeel, A. W. (2011). Stimulation of α2-adrenergic receptors in the central nucleus of the amygdala attenuates stress-induced reinstatement of nicotine seeking in rats. Neuropharmacology 60, 303-311. doi: 10.1016/j.neuropharm.2010.09.013
58. Zhang, Y., Butelman, E. R., Schlussman, S. D., Ho, A., and Kreek, M. J. (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 (Berl.) 179, 551-558. doi: 10.1007/s00213-004-2087-0
59. Zhang, Y., Mantsch, J. R., Schlussman, S. D., Ho, A., and Kreek, M. J. (2002). Conditioned place preference after single doses or "binge" cocaine in C57BL/6J and 129/J mice. Pharmacol. Biochem. Behav. 73, 655-662. doi: 10.1016/S0091-3057(02)00859-6