Kappa opioid receptor antagonism and chronic antidepressant treatment have beneficial activities on social interactions and grooming deficits during heroin abstinence

Addiction Biology

Volumn 22, Issue 4, 2017, Pages 1010-1021

  Lalanne, L ^a,b   Ayranci, G ^a,c   Filliol, D ^a   Gaveriaux Ruff C ^a   Befort, K ^a   Kieffer, B L ^a,c   Lutz, P E ^a,c  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b HÔPITAL CIVIL   (France)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

abstinence; addiction; heroin; kappa opioid receptor; serotonin; sociability

Indexed keywords

ANTIDEPRESSANT AGENT; DIAMORPHINE; FLUOXETINE; KAPPA OPIATE RECEPTOR; NORBINALTORPHIMINE; NALTREXONE; NARCOTIC ANTAGONIST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG ACTIVITY; DRUG EFFECT; DRUG EFFICACY; DRUG MEGADOSE; DRUG WITHDRAWAL; EMOTIONAL DISORDER; EXPERIMENTAL STUDY; EXPLORATORY RESEARCH; GROOMING; HEROIN DEPENDENCE; MALE; MOUSE; NONHUMAN; PILOT STUDY; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; SOCIAL AVOIDANCE BEHAVIOR; SOCIAL DISABILITY; SOCIAL INTERACTION; ANALOGS AND DERIVATIVES; ANIMAL; ANIMAL BEHAVIOR; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; PATHOPHYSIOLOGY; SOCIAL BEHAVIOR; TIME; TREATMENT OUTCOME;

ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; FLUOXETINE; GROOMING; HEROIN; HEROIN DEPENDENCE; MALE; MICE; MICE, INBRED C57BL; NALTREXONE; NARCOTIC ANTAGONISTS; RECEPTORS, OPIOID, KAPPA; SOCIAL BEHAVIOR; TIME; TREATMENT OUTCOME;

EID: 84961774486     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12392     Document Type: Article

References (59)

1. Al-Hasani R, McCall JG, Foshage AM, Bruchas MR (2013) Locus coeruleus kappa-opioid receptors modulate reinstatement of cocaine place preference through a noradrenergic mechanism. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology 38:2484–2497.
2. Almatroudi A, Husbands SM, Bailey CP, Bailey SJ (2015) Combined administration of buprenorphine and naltrexone produces antidepressant-like effects in mice. J Psychopharmacol 29:812–821.
3. th edn. American Psychiatric Association: Washington, DC.
4. Anraku T, Ikegaya Y, Matsuki N, Nishiyama N (2001) Withdrawal from chronic morphine administration causes prolonged enhancement of immobility in rat forced swimming test. Psychopharmacology (Berl) 157:217–220.
5. Ayranci G, Befort K, Lalanne L, Kieffer BL, Lutz PE (2015) Dissociation of heroin-induced emotional dysfunction from psychomotor activation and physical dependence among inbred mouse strains. Psychopharmacology (Berl) 232:1957–1971.
6. Bakken K, Landheim AS, Vaglum P (2007) Axis I and II disorders as long-term predictors of mental distress: a six-year prospective follow-up of substance-dependent patients. BMC Psychiatry 7:29.
7. Bilkei-Gorzo A, Mauer D, Michel K, Zimmer A (2014) Dynorphins regulate the strength of social memory. Neuropharmacology 77:406–413.
8. Blatchford KE, Diamond K, Westbrook RF, McNally GP (2005) Increased vulnerability to stress following opiate exposures: behavioral and autonomic correlates. Behav Neurosci 119:1034–1041.
9. Bruchas MR, Land BB, Aita M, Xu M, Barot SK, Li S, Chavkin C (2007a) Stress-induced p38 mitogen-activated protein kinase activation mediates kappa-opioid-dependent dysphoria. J Neurosci: Off J Soc Neurosci 27:11614–11623.
10. Bruchas MR, Land BB, Chavkin C (2010) The dynorphin/kappa opioid system as a modulator of stress-induced and pro-addictive behaviors. Brain Res 1314:44–55.
11. Bruchas MR, Schindler AG, Shankar H, Messinger DI, Miyatake M, Land BB, Lemos JC, Hagan CE, Neumaier JF, Quintana A, Palmiter RD, Chavkin C (2011) Selective p38alpha MAPK deletion in serotonergic neurons produces stress resilience in models of depression and addiction. Neuron 71:498–511.
12. Bruchas MR, Yang T, Schreiber S, Defino M, Kwan SC, Li S, Chavkin C (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.
13. Buda JJ, Carroll FI, Kosten TR, Swearingen D, Walters BB (2015) A double-blind, placebo-controlled trial to evaluate the safety, tolerability, and pharmacokinetics of single, escalating oral doses of JDTic. Neuropsychopharmacology: Off Publ Am College Neuropsychopharmacology 40:2059–2065.
14. Butelman ER, Negus SS, Ai Y, de Costa BR, Woods JH (1993) Kappa opioid antagonist effects of systemically administered nor-binaltorphimine in a thermal antinociception assay in rhesus monkeys. J Pharmacol Exp Ther 267:1269–1276.
15. Cole SL, Hofford RS, Evert DJ, Wellman PJ, Eitan S (2012) Social influences on morphine conditioned place preference in adolescent mice. Addict Biol 18:274–285.
16. Ehrich E, Turncliff R, Du Y, Leigh-Pemberton R, Fernandez E, Jones R, Fava M (2014) Evaluation of opioid modulation in major depressive disorder. Neuropsychopharmacology: Off Publ the Am College Neuropsychopharmacology 40:1448–1455.
17. Everitt BJ (2014) Neural and psychological mechanisms underlying compulsive drug seeking habits and drug memories—indications for novel treatments of addiction. Eur J Neurosci 40:2163–2182.
18. Fadda P, Scherma M, Fresu A, Collu M, Fratta W (2005) Dopamine and serotonin release in dorsal striatum and nucleus accumbens is differentially modulated by morphine in DBA/2 J and C57BL/6 J mice. Synapse 56:29–38.
19. Ferreira MD, Menescal-de-Oliveira L (2012) Opioidergic, GABAergic and serotonergic neurotransmission in the dorsal raphe nucleus modulates tonic immobility in guinea pigs. Physiol Behav 106:109–116.
20. George O, Koob GF, Vendruscolo LF (2014) Negative reinforcement via motivational withdrawal is the driving force behind the transition to addiction. Psychopharmacology (Berl) 231:3911–3917.
21. Gerra G, Borella F, Zaimovic A, Moi G, Bussandri M, Bubici C, Bertacca S (2004) Buprenorphine versus methadone for opioid dependence: predictor variables for treatment outcome. Drug Alcohol Depend 75:37–45.
22. Goeldner C, Lutz PE, Darcq E, Halter T, Clesse D, Ouagazzal AM, Kieffer BL (2011) Impaired emotional-like behavior and serotonergic function during protracted abstinence from chronic morphine. Biol Psychiatry 69:236–244.
23. Grasing K, Ghosh S (1998) Selegiline prevents long-term changes in dopamine efflux and stress immobility during the second and third weeks of abstinence following opiate withdrawal. Neuropharmacology 37:1007–1017.
24. Grella CE, Karno MP, Warda US, Niv N, Moore AA (2009) Gender and comorbidity among individuals with opioid use disorders in the NESARC study. Addict Behav 34:498–504.
25. Harris GC, Aston-Jones G (1993) Beta-adrenergic antagonists attenuate somatic and aversive signs of opiate withdrawal. Neuropsychopharmacology: Off PublAm College Neuropsychopharmacology 9:303–311.
26. Harris GC, Aston-Jones G (2001) Augmented accumbal serotonin levels decrease the preference for a morphine associated environment during withdrawal. Neuropsychopharmacology: Off Publ Am College Neuropsychopharmacology 24:75–85.
27. Hasin DS, O'Brien CP, Auriacombe M, Borges G, Bucholz K, Budney A, Compton WM, Crowley T, Ling W, Petry NM, Schuckit M, Grant BF (2013) DSM-5 criteria for substance use disorders: recommendations and rationale. Am J Psychiatry 170:834–851.
28. Hodgson SR, Hofford RS, Wellman PJ, Eitan S (2009) Different affective response to opioid withdrawal in adolescent and adult mice. Life Sci 84:52–60.
29. Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565–598.
30. Jia W, Liu R, Shi J, Wu B, Dang W, Du Y, Zhou Q, Wang J, Zhang R (2013) Differential regulation of MAPK phosphorylation in the dorsal hippocampus in response to prolonged morphine withdrawal-induced depressive-like symptoms in mice. PLoS One 8:e66111.
31. Karp JF, Butters MA, Begley AE, Miller MD, Lenze EJ, Blumberger DM, Mulsant BH, Reynolds CF 3rd (2014) Safety, tolerability, and clinical effect of low-dose buprenorphine for treatment-resistant depression in midlife and older adults. J Clin Psychiatry 75:e785–793.
32. Kest B, Hopkins E, Palmese CA, Adler M, Mogil JS (2002) Genetic variation in morphine analgesic tolerance: a survey of 11 inbred mouse strains. Pharmacol Biochem Behav 73:821–828.
33. Klein G, Juni A, Waxman AR, Arout CA, Inturrisi CE, Kest B (2008) A survey of acute and chronic heroin dependence in ten inbred mouse strains: evidence of genetic correlation with morphine dependence. Pharmacol Biochem Behav 90:447–452.
34. Knoll AT, Carlezon WA Jr (2010) Dynorphin, stress, and depression. Brain Res 1314:56–73.
35. Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology: Off Publ Am College Neuropsychopharmacology 35:217–238.
36. Lalanne L, Ayranci G, Kieffer BL, Lutz PE (2014) The kappa opioid receptor: from addiction to depression, and back. Front Psychiatry 5:170.
37. Land BB, Bruchas MR, Schattauer S, Giardino WJ, Aita M, Messinger D, Hnasko TS, Palmiter RD, Chavkin C (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.
38. Lutz PE, Ayranci G, Chu-Sin-Chung P, Matifas A, Koebel P, Filliol D, Befort K, Ouagazzal AM, Kieffer BL (2014) Distinct mu, delta, and kappa opioid receptor mechanisms underlie low sociability and depressive-like behaviors during heroin abstinence. Neuropsychopharmacology: Off Publ Am College Neuropsychopharmacology 39:2694–2705.
39. Lutz PE, Kieffer BL (2013) The multiple facets of opioid receptor function: implications for addiction. Curr Opin Neurobiol 23:473–479.
40. Lutz PE, Pradhan AA, Goeldner C, Kieffer BL (2011) Sequential and opposing alterations of 5-HT(1A) receptor function during withdrawal from chronic morphine. Eur neuropsychopharmacology: J Eur College Neuropsychopharmacology 21:835–840.
41. McLaughlin JP, Land BB, Li S, Pintar JE, Chavkin C (2006) Prior activation of kappa opioid receptors by U50,488 mimics repeated forced swim stress to potentiate cocaine place preference conditioning. Neuropsychopharmacology: Off Publ Am College Neuropsychopharmacology 31:787–794.
42. Melief EJ, Miyatake M, Carroll FI, Beguin C, Carlezon WA Jr, Cohen BM, Grimwood S, Mitch CH, Rorick-Kehn L, Chavkin C (2011) Duration of action of a broad range of selective kappa-opioid receptor antagonists is positively correlated with c-Jun N-terminal kinase-1 activation. Mol Pharmacol 80:920–929.
43. Metcalf MD, Coop A (2005) Kappa opioid antagonists: past successes and future prospects. AAPS J 7:E704–722.
44. Mogil JS, Wilson SG, Wan Y (2001) Assessing nociception in murine subjects. In: Kruger, L ed. Methods in Pain Research, pp. 11–39. CRC Press: Boca Raton, FL.
45. Munro TA, Berry LM, Van't Veer A, Beguin C, Carroll FI, Zhao Z, Carlezon WA Jr, Cohen BM (2012) Long-acting kappa opioid antagonists nor-BNI, GNTI and JDTic: pharmacokinetics in mice and lipophilicity. BMC Pharmacol 12:5.
46. Nunes EV, Levin FR (2006) Treating depression in substance abusers. Curr Psychiatry Rep 8:363–370.
47. Nylander I, Vlaskovska M, Terenius L (1995a) Brain dynorphin and enkephalin systems in Fischer and Lewis rats: effects of morphine tolerance and withdrawal. Brain Res 683:25–35.
48. Nylander I, Vlaskovska M, Terenius L (1995b) The effects of morphine treatment and morphine withdrawal on the dynorphin and enkephalin systems in Sprague-Dawley rats. Psychopharmacology (Berl) 118:391–400.
49. Patkar KA, Wu J, Ganno ML, Singh HD, Ross NC, Rasakham K, Toll L, McLaughlin JP (2013) Physical presence of nor-binaltorphimine in mouse brain over 21 days after a single administration corresponds to its long-lasting antagonistic effect on kappa-opioid receptors. J Pharmacol Exp Ther 346:545–554.
50. Picetti R, Caccavo JA, Ho A, Kreek MJ (2012) Dose escalation and dose preference in extended-access heroin self-administration in Lewis and Fischer rats. Psychopharmacology (Berl) 220:163–172.
51. Robles CF, McMackin MZ, Campi KL, Doig IE, Takahashi EY, Pride MC, Trainor BC (2014) Effects of kappa opioid receptors on conditioned place aversion and social interaction in males and females. Behav Brain Res 262:84–93.
52. Schindler AG, Messinger DI, Smith JS, Shankar H, Gustin RM, Schattauer SS, Lemos JC, Chavkin NW, Hagan CE, Neumaier JF, Chavkin C (2012) Stress produces aversion and potentiates cocaine reward by releasing endogenous dynorphins in the ventral striatum to locally stimulate serotonin reuptake. J Neurosci: Off J Soc Neurosci 32:17582–17596.
53. Schlussman SD, Zhang Y, Hsu NM, Allen JM, Ho A, Kreek MJ (2008) Heroin-induced locomotor activity and conditioned place preference in C57BL/6 J and 129P3/J mice. Neurosci Lett 440:284–288.
54. Simonin F, Valverde O, Smadja C, Slowe S, Kitchen I, Dierich A, Le Meur M, Roques BP, Maldonado R, Kieffer BL (1998) Disruption of the kappa-opioid receptor gene in mice enhances sensitivity to chemical visceral pain, impairs pharmacological actions of the selective kappa-agonist U-50,488H and attenuates morphine withdrawal. EMBO J 17:886–897.
55. Tao R, Auerbach SB (2005) mu-Opioids disinhibit and kappa-opioids inhibit serotonin efflux in the dorsal raphe nucleus. Brain Res 1049:70–79.
56. Vaught JL, Takemori AE (1979) Differential effects of leucine and methionine enkephalin on morphine-induced analgesia, acute tolerance and dependence. J Pharmacol Exp Ther 208:86–90.
57. Volkow ND, Baler RD, Goldstein RZ (2011) Addiction: pulling at the neural threads of social behaviors. Neuron 69:599–602.
58. Williams AM, Reis DJ, Powell AS, Neira LJ, Nealey KA, Ziegler CE, Kloss ND, Bilimoria JL, Smith CE, Walker BM (2012) The effect of intermittent alcohol vapor or pulsatile heroin on somatic and negative affective indices during spontaneous withdrawal in Wistar rats. Psychopharmacology (Berl) 223:75–88.
59. Zan GY, Wang Q, Wang YJ, Liu Y, Hang A, Shu XH, Liu JG (2015) Antagonism of kappa opioid receptor in the nucleus accumbens prevents the depressive-like behaviors following prolonged morphine abstinence. Behav Brain Res 291:334–341.