Dissociation of heroin-induced emotional dysfunction from psychomotor activation and physical dependence among inbred mouse strains

Psychopharmacology

Volumn 232, Issue 11, 2015, Pages 1957-1971

  Ayranci, G ^a,b,c   Befort, K ^a,b,c   Lalanne, L ^a,b,c,f   Kieffer, B L ^a,b,c,d   Lutz, P E ^a,b,c,e  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b CNRS   (France)

^c INSERM   (France)

^d DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f HÔPITAL CIVIL   (France)

Author keywords

Abstinence; Addiction; Depression; Heroin; Locomotion; Physical dependence; Sociability

Indexed keywords

DIAMORPHINE; NALOXONE;

ANIMAL; AROUSAL; DRUG EFFECTS; EMOTION; GENETICS; HEROIN DEPENDENCE; INBRED MOUSE STRAIN; MALE; MOTOR ACTIVITY; MOUSE; PSYCHOLOGY; SOCIAL BEHAVIOR; WITHDRAWAL SYNDROME;

ANIMALS; AROUSAL; EMOTIONS; HEROIN; HEROIN DEPENDENCE; MALE; MICE; MICE, INBRED STRAINS; MOTOR ACTIVITY; NALOXONE; SOCIAL BEHAVIOR; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 84940003527     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-014-3826-5     Document Type: Article

References (75)

1. Ahmed SH, Koob GF (1998) Transition from moderate to excessive drug intake: change in hedonic set point. Science 282:298-300
2. Andersen JM, Ripel A, Boix F, Normann PT, Morland J (2009) Increased locomotor activity induced by heroin in mice: pharmacokinetic demonstration of heroin acting as a prodrug for the mediator 6-monoacetylmorphine in vivo. J Pharmacol Exp Ther 331:153-161
3. 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 157:217-220
4. Bailey A, Metaxas A, Al-Hasani R, Keyworth HL, Forster DM, Kitchen I (2010) Mouse strain differences in locomotor, sensitisation and rewarding effect of heroin; association with alterations in MOP-r activation and dopamine transporter binding. Eur J Neurosci 31:742-753
5. Belknap JK, Riggan J, Cross S, Young ER, Gallaher EJ, Crabbe JC (1998) Genetic determinants of morphine activity and thermal responses in 15 inbred mouse strains. Pharmacol, Biochem Behav 59:353-360
6. Belzung C, Le Guisquet AM, Crestani F (2000) Flumazenil induces benzodiazepine partial agonist-like effects in BALB/c but not C57BL/6 mice. Psychopharmacology 148:24-32
7. Boix F, Andersen JM, Morland J (2013) Pharmacokinetic modeling of subcutaneous heroin and its metabolites in blood and brain of mice. Addict Biol 18:1-7
8. Buckman SG, Hodgson SR, Hofford RS, Eitan S (2009) Increased elevated plus maze open-arm time in mice during spontaneous morphine withdrawal. Behav Brain Res 197:454-456
9. Cole SL, Hofford RS, Evert DJ, Wellman PJ, Eitan S (2012) Social influences on morphine conditioned place preference in adolescent mice. Addiction Biology
10. Crawley JN (1985) Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9:37-44
11. Crawley J, Goodwin FK (1980) Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol, Biochem Behav 13:167-170
12. Cryan JF, Holmes A (2005) The ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4:775-790
13. Delfs JM, Zhu Y, Druhan JP, Aston-Jones G (2000) Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion. Nature 403:430-434
14. Deroche-Gamonet V, Belin D, Piazza PV (2004) Evidence for addiction-like behavior in the rat. Science 305:1014-1017
15. Ducci F, Roy A, Shen PH, Yuan Q, Yuan NP, Hodgkinson CA, Goldman LR, Goldman D (2009) Association of substance use disorders with childhood trauma but not African genetic heritage in an African American cohort. Am J Psychiatry 166:1031-1040
16. Dulawa SC, Holick KA, Gundersen B, Hen R (2004) Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 29:1321-1330
17. 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/2J and C57BL/6J mice. Synapse 56:29-38
18. File SE, Hyde JR (1978) Can social interaction be used to measure anxiety? Br J Pharmacol 62:19-24
19. 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
20. Goldman D, Oroszi G, Ducci F (2005) The genetics of addictions: uncovering the genes. Nat Rev Genet 6:521-532
21. Gorris LG, van Abeelen JH (1981) Behavioural effects of (-)naloxone in mice from four inbred strains. Psychopharmacology 74:355-359
22. Gowing L, Farrell MF, Ali R, White JM (2014) Alpha2-adrenergic agonists for the management of opioid withdrawal. Cochrane Database Syst Rev 3:CD002024
23. Grant BF, Stinson FS, Dawson DA, Chou SP, Dufour MC, Compton W, Pickering RP, Kaplan K (2004) Prevalence and co-occurrence of substance use disorders and independent mood and anxiety disorders: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Arch Gen Psychiatry 61:807-816
24. 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
25. Grasing K, Wang A, Schlussman S (1996) Behavioral measures of anxiety during opiate withdrawal. Behav Brain Res 80:195-201
26. 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
27. Harris GC, Aston-Jones G (2001) Augmented accumbal serotonin levels decrease the preference for a morphine associated environment during withdrawal. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 24:75-85
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. Hofford RS, Wellman PJ, Eitan S (2011) Social influences on plasma testosterone levels in morphine withdrawn adolescent mice and their drug-naive cage-mates. Psychoneuroendocrinology 36:728-736
30. Jaffe JH (1990) Trivializing dependence. Br J Addict 85:1425-1427, discussion 1429-31
31. 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
32. Kessler RC, Berglund P, Demler O, Jin R, Merikangas KR, Walters EE (2005) Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62:593-602
33. Kest B, Palmese CA, Hopkins E, Adler M, Juni A, Mogil JS (2002) Naloxone-precipitated withdrawal jumping in 11 inbred mouse strains: evidence for common genetic mechanisms in acute and chronic morphine physical dependence. Neuroscience 115:463-469
34. Klein G, Juni A, Arout CA, Waxman AR, Inturrisi CE, Kest B (2008a) Acute and chronic heroin dependence in mice: contribution of opioid and excitatory amino acid receptors. Eur J Pharmacol 586:179-188
35. Klein G, Juni A, Waxman AR, Arout CA, Inturrisi CE, Kest B (2008b) 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
36. Koek W, France CP, Javors MA (2012) Morphine-induced motor stimulation, motor incoordination, and hypothermia in adolescent and adult mice. Psychopharmacology 219:1027-1037
37. Koob GF (2008) A role for brain stress systems in addiction. Neuron 59:11-34
38. Koob GF, Le Moal M (2008) Review. Neurobiological mechanisms for opponent motivational processes in addiction. Philos Trans R Soc Lond B Biol Sci 363:3113-3123
39. Lalanne L, Ayranci G, Filliol D, Befort K, Lutz PE, Kieffer BL (2014) Low sociability induced by heroin protracted abstinence in mice is mediated by interactions between dynorphin-kappa opioid receptor and serotoninergic pathways. (In preparation)
40. Lalonde R, Strazielle C (2008) Relations between open-field, elevated plus-maze, and emergence tests as displayed by C57/BL6J and BALB/c mice. J Neurosci Methods 171:48-52
41. Le Merrer J, Befort K, Gardon O, Filliol D, Darcq E, Dembele D, Becker JA, Kieffer BL (2012) Protracted abstinence from distinct drugs of abuse shows regulation of a common gene network. Addiction Biology 17:1-12
42. Liu X, Gershenfeld HK (2001) Genetic differences in the tail-suspension test and its relationship to imipramine response among 11 inbred strains of mice. Biol Psychiatry 49:575-581
43. Lutz PE, Kieffer BL (2013) The multiple facets of opioid receptor function: implications for addiction. Curr Opin Neurobiol 23:473-479
44. 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 Neuropsychopharmacol: J Eur Coll Neuropsychopharmacol 21:835-840
45. Lutz PE, Reiss D, Ouagazzal AM, Kieffer BL (2013) A history of chronic morphine exposure during adolescence increases despair-like behaviour and strain-dependently promotes sociability in abstinent adult mice. Behav Brain Res 243:44-52
46. 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. Neuropsychopharmacol: Off Publ Am Coll of Neuropsychopharmacol 39:2694-2705
47. Mandillo S, Tucci V, Holter SM, Meziane H, Banchaabouchi MA, Kallnik M, Lad HV, Nolan PM, Ouagazzal AM, Coghill EL, Gale K, Golini E, Jacquot S, Krezel W, Parker A, Riet F, Schneider I, Marazziti D, Auwerx J, Brown SD, Chambon P, Rosenthal N, Tocchini-Valentini G, Wurst W (2008) Reliability, robustness, and reproducibility in mouse behavioral phenotyping: a cross-laboratory study. Physiol Genomics 34:243-255
48. Martin WR, Jasinski DR (1969) Physiological parameters of morphine dependence in man - tolerance, early abstinence, protracted abstinence. J Psychiatr Res 7:9-17
49. Matthes HW, Maldonado R, Simonin F, Valverde O, Slowe S, Kitchen I, Befort K, Dierich A, Le Meur M, Dolle P, Tzavara E, Hanoune J, Roques BP, Kieffer BL (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383:819-823
50. Miller BH, Schultz LE, Gulati A, Su AI, Pletcher MT (2010) Phenotypic characterization of a genetically diverse panel of mice for behavioral despair and anxiety. PLoS One 5:e14458
51. Moy SS, Nadler JJ, Young NB, Perez A, Holloway LP, Barbaro RP, Barbaro JR, Wilson LM, Threadgill DW, Lauder JM, Magnuson TR, Crawley JN (2007) Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav Brain Res 176:4-20
52. Murphy NP, Lam HA, Maidment NT (2001) A comparison of morphine-induced locomotor activity and mesolimbic dopamine release in C57BL6, 129Sv and DBA2 mice. J Neurochem 79:626-635
53. Nadler JJ, Moy SS, Dold G, Trang D, Simmons N, Perez A, Young NB, Barbaro RP, Piven J, Magnuson TR, Crawley JN (2004) Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav 3:303-314
54. Norcross M, Mathur P, Enoch AJ, Karlsson RM, Brigman JL, Cameron HA, Harvey-White J, Holmes A (2008) Effects of adolescent fluoxetine treatment on fear-, anxiety- or stress-related behaviors in C57BL/6J or BALB/cJ mice. Psychopharmacology 200:413-424
55. Nunes EV, Sullivan MA, Levin FR (2004) Treatment of depression in patients with opiate dependence. Biol Psychiatry 56:793-802
56. Papaleo F, Kieffer BL, Tabarin A, Contarino A (2007) Decreased motivation to eat in mu-opioid receptor-deficient mice. Eur J Neurosci 25:3398-3405
57. Peles E, Schreiber S, Naumovsky Y, Adelson M (2007) Depression in methadone maintenance treatment patients: rate and risk factors. J Affect Disord 99:213-220
58. Porsolt RD, Bertin A, Jalfre M (1977) Behavioral despair in mice: a primary screening test for antidepressants. Arch Int Pharmacodyn Ther 229:327-336
59. Pothion S, Bizot JC, Trovero F, Belzung C (2004) Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav Brain Res 155:135-146
60. Renard CE, Dailly E, David DJ, Hascoet M, Bourin M (2003) Monoamine metabolism changes following the mouse forced swimming test but not the tail suspension test. Fundam Clin Pharmacol 17:449-455
61. Rouibi K, Contarino A (2012) Increased motivation to eat in opiate-withdrawn mice. Psychopharmacology 221:675-684
62. Sarter M, Bodewitz G, Stephens DN (1988) Attenuation of scopolamine-induced impairment of spontaneous alteration behaviour by antagonist but not inverse agonist and agonist beta-carbolines. Psychopharmacology (Berl) 94:491-495
63. Schlussman SD, Zhang Y, Hsu NM, Allen JM, Ho A, Kreek MJ (2008) Heroin-induced locomotor activity and conditioned place preference in C57BL/6J and 129P3/J mice. Neurosci Lett 440:284-288
64. Schlussman SD, Cassin J, Zhang Y, Levran O, Ho A, Kreek MJ (2011) Regional mRNA expression of the endogenous opioid and dopaminergic systems in brains of C57BL/6J and 129P3/J mice: strain and heroin effects. Pharmacol, Biochem Behav 100:8-16
65. Schlussman SD, Buonora M, Brownstein AJ, Zhang Y, Ho A, Kreek MJ (2013) Regional mRNA expression of GABAergic receptor subunits in brains of C57BL/6J and 129P3/J mice: strain and heroin effects. Brain Res 1523:49-58
66. Steru L, Chermat R, Thierry B, Simon P (1985) The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology 85:367-370
67. Szumlinski KK, Lominac KD, Frys KA, Middaugh LD (2005) Genetic variation in heroin-induced changes in behaviour: effects of B6 strain dose on conditioned reward and locomotor sensitization in 129-B6 hybrid mice. Genes Brain Behav 4:324-336
68. Tang X, Sanford LD (2005) Home cage activity and activity-based measures of anxiety in 129P3/J, 129X1/SvJ and C57BL/6J mice. Physiol Behav 84:105-115
69. Tarabar AF, Nelson LS (2003) The resurgence and abuse of heroin by children in the United States. Curr Opin Pediatr 15:210-215
70. Vannoni E, Voikar V, Colacicco G, Sanchez MA, Lipp HP, Wolfer DP (2014) Spontaneous behavior in the social homecage discriminates strains, lesions and mutations in mice. J Neurosci Methods 234:26-37
71. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R (1987) Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 93:358-364
72. Xu K, Lichtermann D, Lipsky RH, Franke P, Liu X, Hu Y, Cao L, Schwab SG, Wildenauer DB, Bau CH, Ferro E, Astor W, Finch T, Terry J, Taubman J, Maier W, Goldman D (2004) Association of specific haplotypes of D2 dopamine receptor gene with vulnerability to heroin dependence in 2 distinct populations. Arch Gen Psychiatry 61:597-606
73. Zanos P, Georgiou P, Wright SR, Hourani SM, Kitchen I, Winsky-Sommerer R, Bailey A (2014) The oxytocin analogue carbetocin prevents emotional impairment and stress-induced reinstatement of opioid-seeking in morphine-abstinent mice. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 39:855-65
74. Zhang D, Zhou X, Wang X, Xiang X, Chen H, Hao W (2007) Morphine withdrawal decreases responding reinforced by sucrose self-administration in progressive ratio. Addict Biol 12:152-7
75. Ziauddeen H, Chamberlain SR, Nathan PJ, Koch A, Maltby K, Bush M, Tao WX, Napolitano A, Skeggs AL, Brooke AC, Cheke L, Clayton NS, Sadaf Farooqi I, O'Rahilly S, Waterworth D, Song K, Hosking L, Richards DB, Fletcher PC, Bullmore ET (2013) Effects of the mu-opioid receptor antagonist GSK1521498 on hedonic and consummatory eating behaviour: a proof of mechanism study in binge-eating obese subjects. Mol Psychiatry 18:1287-1293