Antagonism of κ opioid receptor in the nucleus accumbens prevents the depressive-like behaviors following prolonged morphine abstinence

Behavioural Brain Research

Volumn 291, Issue , 2015, Pages 334-341

  Zan, Gui Ying ^a   Wang, Qian ^b   Wang, Yu Jun ^a   Liu, Yao ^c   Hang, Ai ^d   Shu, Xiao Hong ^b   Liu, Jing Gen ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b DALIAN MEDICAL UNIVERSITY   (China)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

Depression; Morphine withdrawal; Nucleus accumbens; Prodynorphin; Opioid receptor

Indexed keywords

DYNORPHIN; MORPHINE; NORBINALTORPHIMINE; PRODYNORPHIN; ANTIDEPRESSANT AGENT; ENKEPHALIN; KAPPA OPIATE RECEPTOR; MESSENGER RNA; NALTREXONE; NARCOTIC AGENT; NARCOTIC ANTAGONIST; PREPROENKEPHALIN; PROTEIN PRECURSOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPRESSION; DOSE RESPONSE; DRUG DOSE ESCALATION; DRUG MECHANISM; DRUG WITHDRAWAL; GENE; GENE EXPRESSION REGULATION; LOCOMOTION; MALE; MORPHINE ADDICTION; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PRODYNORPHIN GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BLOCKING; UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DEPRESSIVE DISORDER; DISEASE MODEL; DRUG EFFECTS; METABOLISM; MOTOR ACTIVITY; PSYCHOLOGY; SUBSTANCE WITHDRAWAL SYNDROME;

ANIMALS; ANTIDEPRESSIVE AGENTS; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENKEPHALINS; MALE; MICE, INBRED C57BL; MORPHINE; MOTOR ACTIVITY; NALTREXONE; NARCOTIC ANTAGONISTS; NARCOTICS; NUCLEUS ACCUMBENS; PROTEIN PRECURSORS; RECEPTORS, OPIOID, KAPPA; RNA, MESSENGER; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 84930933872     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.05.053     Document Type: Article

References (69)

1. Cerdá M., Sagdeo A., Galea S. Comorbid forms of psychopathology: key patterns and future research directions. Epidemiol. Rev. 2008, 30:155-177.
2. Haertzen C.A., Meketon M.J., Hooks N.T. Subjective experiences produced by the withdrawal of opiates. Br. J. Addict. Alcohol Other Drugs 1970, 65:245-255.
3. Kanof P.D., Handelsman L., Aronson M.J., Ness R., Cochrane K.J., Rubinstein K.J. Clinical characteristics of naloxone-precipiated withdrawal in human opioid-dependent subjects. J. Exp. Ther. 1992, 260:355-363.
4. Kosten T.R., Rounsaville B.J., Kleber H.D. A 2.5-year follow-up of depression life crises and treatment effects on abstinence among opioid addicts. Arch. Gen. Psychiatry 1986, 43:733-738.
5. Childress A.R., Ehrman R., Mclellan A.T., MacRae J., Natale M., O'Brien C.P. Can induced moods trigger drug-related responses in opiate abuse patients. J. Subst. Abuse Treat. 1994, 11:17-23.
6. Shaham Y., Erb S., Stewart J. Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res. Brain Res. Rev. 2000, 33:13-33.
7. Anraku T., Ikegaya Y., Matsuki N., Nishiyama N. Withdrawal from chronic morphine administration causes prolonged enhancement of immobility in rat forced swimming test. Psychopharmacol. (Berl.) 2001, 157:217-220.
8. Goeldner C., Lutz P.E., Darcq E., Halter T., Clesse D., Ouagazzal A.M., et al. Impaired emotional-like behavior and serotonergic function during protracted abstinence from chronic morphine. Biol. Psychiatry 2011, 69:236-244.
9. Jia W., Liu R., Shi J., Wu B., Dang W., Du Y., et al. Differential regulation of MAPK phosphorylation in the dorsal hippocampus in response to prolonged morphine withdrawal induced depressive like symptoms in mice. Plos One 2013, 8:e66111.
10. Chartoff E., Sawyer A., Rachlin A., Potter D., Pliakas A., Carlezon W.A. Blockade of kappa opioid receptors attenuates the development of depressive-like behaviors induced by cocaine withdrawal in rats. Neuropharmacology 2012, 62:167-176.
11. Chavkin C., James I.F., Goldstein A. Dynorphin is a specific endogenous ligand of the kappa opioid receptor. Science 1982, 215:413-415.
12. Pfeiffer A., Brantl V., Herz A., Emrich H.M. Psychotomimesis mediated by kappa opiate receptors. Science 1986, 233:774-776.
13. Ukai M., Suzuki M., Mamiya T. Effects of U-50,488H, a kappa opioid receptor agonist, on the learned helplessness model of depression in mice. J. Neural. Transm. 2002, 109:1221-1225.
14. Carlezon W.A., Béguin C., DiNieri J.A., Baumann M.H., Richards M.R., Todtenkopf M.S., et al. Depressive-like effects of the kappa-opioid receptor agonist salvinorin a on behavior and neurochemistry in rats. J. Pharmacol. Exp. Ther. 2006, 316:440-447.
15. Todtenkopf M.S., Marcus J.F., Portoghese P.S., Carlezon W.A. Effects of -opioid receptor ligands on intracranial self-stimulation in rats. Psychopharmacol. (Berl.) 2004, 172:463-470.
16. Chavkin C. Dynorphin-still an extraordinarily potent opioid peptide. Mol. Pharmacol. 2013, 83:729-736.
17. Knoll A.T., Carlezon W.A. Dynorphin, stress, and depression. Brain Res. 2010, 1314:56-73.
18. Carlezon W.A., Béguin C., Knoll A.T., Cohen B.M. Kappa opioid ligands in the study and treatment of mood disorders. Pharmacol. Ther. 2009, 123:334-343.
19. Bruchas M.R., Schindler A.G., Shankar H., Messinger D.I., Miyatake M., Land B.B., et al. Selective p38α MAPK deletion in serotonergic neurons produces stress resilience in models of depression and addiction. Neuron 2011, 71:498-511.
20. Mague S.D., Pliakas A.M., Todtenkopf M.S., Tomasiewicz H.C., Zhang Y., Stevens W.C., et al. Antidepressant-like effects of kappa-opioid receptor antagonists in the forced swim test in rats. J. Pharmacol. Exp. Ther. 2003, 305:323-330.
21. McLaughlin J.P., Marton-Popovici M., Chavkin C. Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J. Neurosci. 2003, 23:5674-5683.
22. Beardsley P.M., Howard J.L., Shelton K.L., Carroll F.I. Differential effects of the novel kappa opioid receptor antagonist, JDTic, on reistatement of cocaine-seeking induced by footshock stressors vs cocaine primes and its antidepressant-like effects in rats. Psychopharmacol. (Berl.) 2005, 183:118-126.
23. Cohen A., Whitfield T.W., Kreifeldt M., Koebel P., Kieffer B.L., Contet C., et al. Virus-mediated shRNA knockdown of prodynorphin in the rat nucleus accumbens attenuates depression-like behavior and cocaine locomotor sensitization. Plos One 2014, 9:e97216.
24. Sivam S.P. Cocaine selectively increases striatonigral dynorphin levels by a dopaminergic mechanism. J. Pharmacol. Exp. Ther. 1989, 250:818-824.
25. Przewlocka B., Turchan J., Lason W., Przewlocki R. Ethanol withdrawal enhances the prodynorphin system activity in the rat nucleus accumbens. Neurosci. Lett. 1997, 238:13-16.
26. Lindholm S., Ploj K., Franck J., Nylander I. Repeated ethanol administration induces short-and long-term changes in enkephalin and dynorphin tissue concentrations in rat brain. Alcohol 2000, 22:165-171.
27. Solecki W., Ziolkowska B., Krowka T., Gieryk A., Filip M., Przewlocki R. Alterations of prodynorphin gene expression in the rat mesocorticolimbic system during heroin self-administration. Brain Res. 2009, 1255:113-121.
28. D'Addario C., Caputi F.F., Ekström T.J., Di Benedetto M., Maccarrone M., Romualdi P., et al. Ethanol induces epigenetic modulation of prodynorphin and pronociceptin gene expression in the rat amygdala complex. J. Mol. Neurosci. 2013, 49:312-319.
29. Gillett K., Harshberger E., Valdez G.R. Protracted withdrawal from ethanol and enhanced responsiveness stress: regulation via the dynorphin/kappa opioid receptor system. Alcohol 2013, 47:359-365.
30. Nylander I., Vlaskovska M., Terenius L. The effects of morphine treatment and morphine withdrawal on the dynorphin and enkephalin systems in sprague-dawley rats. Psychopharmacol. (Berl.) 1995, 118:391-400.
31. Nestler E.J., Carlezon W.A. The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 2006, 59:1151-1159.
32. Wise R.A. Dopamine and reward: the anhedonia hypothesis 30 years on. Neurotoxic. Res. 2008, 14:169-183.
33. Carlezon W.A., Thomas M.J. Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 2009, 56:122-132.
34. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., Monteggia L.M. Neurobiology of depression. Neuron 2002, 34:13-25.
35. Boadie Dunlop W., Charles Nemeroff B. The role of dopamine in the pathophysiology of depression. Arch. Gen. Psychiatry 2007, 64:327-337.
36. Wise R.A. Neuroleptics and operant behavior: the anhedonia hypothesis. Behav. Brain Sci. 1982, 5:39-87.
37. Muschamp J.W., Van't Veer A., Parsegian A., Gallo M.S., Chen M., Neve R.L., et al. Activation of creb in the nucleus accumbens shell produces anhedonia and resistance to extinction of fear in rats. J. Neurosci. 2011, 31:3095-3103.
38. Carlezon W.A., Thome J., Olson V.G., Lane-Ladd S.B., Brodkin E.S., Hiroi N., et al. Regulation of cocaine reward by creb. Science 1998, 282:2272-2275.
39. Newton S.S., Thome J., Wallace T.L., Shirayama Y., Schlesinger L., Sakai N., et al. Inhibition of camp response element-binding protein or dynorphin in the nucleus accumbens produces an antidepressant-like effect. J. Neurosci. 2002, 22:10883-10890.
40. Pliakas A.M., Carlson R.R., Neve R.L., Konradi C., Nestler E.J., Carlezon W.A. Jr 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. 2001, 21:7397-7403.
41. Liu Y., Zhou Q.X., Hou Y.Y., Lu B., Yu C., Chen J., et al. Actin polymerization-dependent increase in synaptic Arc/Arg3.1 expression in the amygdala is crucial for the expression of aversive memory associated with drug withdrawal. J. Neurosci. 2012, 32(12):5-12017.
42. Horan P., Taylor J., Yamamura H.I., Porreca F. Extremely long-lasting antagonistic actions of nor-binaltorphimine (nor-BNI) in the mouse tail-flick test. J. Pharmacol. Exp. Ther. 1992, 260:1237-1243.
43. Land B.B., Bruchas M.R., Schattauer S., Giardino W.J., Aita M., Messinger D., et al. Activation of the kappa opioid receptor inthe dorsal raphe nucleus mediates the aversive effects of stress andreinstates drug seeking. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:19168-19173.
44. Porsolt RD, Brossard G, Hautbois C, Roux S. Rodent models of depression: forced swimming and tail suspension behavioral despair tests in rats and mice. Current protocols in neuroscience2001,editorial board, Jacqueline N. Crawley .. [et al.] Chapter 8:Unit 8 10A.
45. Papp M., Willner P., Muscat R. An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacol. (Berl.) 1991, 104:255-259.
46. Kant G.J., Bauman R.A. Effects of chronic stress and time of day on preference for sucrose. Physiol. Behav. 1993, 54:499-502.
47. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-Delta Delta C(T) method. Methods 2001, 25:402-408.
48. Wong M.L., Medrano J.F. Real-time PCR for mRNA quantitation. BioTechniques 2005, 39:75-85.
49. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 2000, 132:365-386.
50. Porsolt R.D., Bertin A., Jalfre M. Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 1997, 229:327-336.
51. Der-Avakian A., Markou A. The neurobiology of anhedonia and other reward-related deficits. Trends Neurosci. 2012, 35:68-77.
52. Papaleo F., Kitchener P., Contarino A. Disruption of the CRF/CRF1 receptor stress system exacerbates the somatic signs of opiate withdrawal. Neuron 2007, 53:577-589.
53. Molina V.A., Heyser C.J., Spear L.P. Chronic variable stress or chronic morphine facilitates immobility in a forced swim test: reversal by naloxone. Psychopharmacol. (Berl.) 1994, 114:433-440.
54. Grasing K., Ghosh S. Selegiline prevents long-term changes in dopamine efflux and stress immobility during the second and third weeks of abstinence following opiate withdrawal. Neuropharmacology 1998, 37:1007-1017.
55. Schwarzer C. 30 years of dynorphins-new insights on their functions in neuropsychiatric diseases. Pharmacol. Ther. 2009, 123:353-370.
56. Carr G.V., Bangasser D.A., Bethea T., Young M., Valentino R.J., Lucki I. Antidepressant-like effects of kappa-opioid receptor antagonists in Wistar Kyoto rats. Neuropsychopharmacology 2010, 35:752-763.
57. McLaughlin J.P., Li S., Valdez J., Chavkin T.A., Chavkin C. Social defeat stress-induced behavioral responses are meadiated by the endogenous kappa opioid system. Neuropsychopharmacology 2006, 31:1241-1248.
58. Groenewegen H.J., Wright C.I., Beijer A.V., Voorn P. Convergence and segregation of ventral striatal inputs and outputs. Ann. N.Y. Acad. Sci. 1999, 877:49-63.
59. Chaudhri N., Sahuque L.L., Schairer W.W., Janak P.H. Separable roles of the nucleus accumbens core and shell in context- and cue-induced alcohol-seeking. Neuropsychopharmacology 2010, 35:783-791.
60. Bossert J.M., Poles G.C., Wihbey K.A., Koya E., Shaham Y. Differential effects of blockade of dopamine D1-family receptors in nucleus accumbens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues. J. Neurosci. 2007, 27:12655-12663.
61. Mansour A., Hoversten M.T., Taylor L.P., Watson S.J., Akil H. The cloned mu, delta and kappa receptors and their endogenous ligands: evidence for two opioid peptide recognition cores. Brain Res. 1995, 700:89-98.
62. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 1982, 9:321-353.
63. Zhang Y., Butelman E.R., Schlussman S.D., Ho A., Kreek M.J. Effects of the endogenous kappa opioid agonist dynorphin A(1-17) on cocaine-evoked increases in striatal dopamine levels and cocaine-induced place preference in C57BL/6J mice. Psychopharmacol. (Berl.) 2004, 172:422-429.
64. Di Chiara G., Imperato A. Opposite effects of mu and kappa opiate agonists on dopamine release in the nucleus accumbens and in the dorsal caudate of freely moving rats. J. Pharmacol. Exp. Ther. 1988, 244:1067-1080.
65. Spanagel R., Herz A., Shippenberg T.S. Opposing tonically active endogenous opioid systems modulate the mesolimbic dopaminergic pathway. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:2046-2050.
66. Murray E.A., Wise S.P., Drevets W.C. Localization of dysfunction in major depressive disorder: prefrontal cortex and amygdala. Biol. Psychiatry 2011, 69:e43-54.
67. Peluso M.A., Glahn D.C., Matsuo K., Monkul E.S., Najt P., Zamarripa F., et al. Amygdala hyperactivation in untreated depressed individuals. Psychiatry Res. 2009, 173:158-161.
68. Knoll A.T., Muschamp J.W., Sillivan S.E., Ferguson D., Dietz D.M., Meloni E.G., et al. Kappa opioid receptor signaling in the basolateral amygdala regulates conditioned fear and anxiety in rats. Biol. Psychiatry 2011, 70:425-433.
69. Bruchas M.R., Land B.B., Lemos J.C., Chavkin C. CRF1-R activation of the dynorphin/kappa opioid system in the mouse basolateral amygdale mediated anxiety-like behavior. PLoS One 2009, 4:e8528.