Effects of repeated social defeat on adolescent mice on cocaine-induced CPP and self-administration in adulthood: integrity of the blood–brain barrier

Addiction Biology

Volumn 22, Issue 1, 2017, Pages 129-141

  Rodríguez Arias, Marta ^a,d   Montagud Romero, Sandra ^a,d   Rubio Araiz, Ana ^c,d   Aguilar, María A ^a,d   Martín García, Elena ^b,d   Cabrera, Roberto ^b,d   Maldonado, Rafael ^b,d   Porcu, Francesca ^c,d   Colado, María Isabel ^c,d   Miñarro, José ^a,d  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Blood brain barrier; cocaine; conditioned place preference; self administration; social defeat

Indexed keywords

COCAINE; COLLAGEN TYPE 4; IMMUNOGLOBULIN G; LAMININ;

ADOLESCENT; ARTICLE; BEHAVIOR ASSESSMENT; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DRUG SELF ADMINISTRATION; HIPPOCAMPUS; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PLACE PREFERENCE; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REPEAT SOCIAL DEFEAT; SOCIAL ASPECTS AND RELATED PHENOMENA; SOCIAL INTERACTION; ANIMAL; ANIMAL BEHAVIOR; ANIMAL MODEL; CONDITIONED REFLEX; DRUG EFFECTS; MENTAL STRESS; METABOLISM; SOCIAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; BLOOD-BRAIN BARRIER; COCAINE; CONDITIONING, CLASSICAL; MALE; MICE; MODELS, ANIMAL; SELF ADMINISTRATION; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84941710968     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12301     Document Type: Article

References (63)

1. Adriani W, Chiarotti F, Laviola G (1998) Elevated novelty seeking and peculiar d-amphetamine sensitization in periadolescent mice compared with adult mice. Behav Neurosci 112:1152–1166.
2. Andersen SL, Lyss PJ, Dumont NL, Teicher MH (1999) Enduring neurochemical effects of early maternal separation on limbic structures. Ann N Y Acad Sci 877:756–759.
3. Andersen SL, Gazzara RA (1993) The ontogeny of apomorphine-induced alterations of neostriatal dopamine release: effects on spontaneous release. J Neurochem 61:2247–2255.
4. Andersen SL, Teicher MH (2009) Desperately driven and no brakes: developmental stress exposure and subsequent risk for substance abuse. Neurosci Biobehav Rev 33:516–524.
5. Andersen SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27:3–18.
6. Arenas MC, Daza-Losada M, Vidal-Infer A, Aguilar MA, Miñarro J, Rodríguez-Arias M (2014) Capacity of novelty-induced locomotor activity and the hole-board test to predict sensitivity to the conditioned rewarding effects of cocaine. Physiol Behav 133:152–160.
7. Audet MC, Jacobson-Pick S, Wann BP, Anisman H (2011) Social defeat promotes specific cytokine variations within the prefrontal cortex upon subsequent aggressive or endotoxin challenges. Brain Behav Immun 25:1197–1205.
8. Baarendse PJ, Limpens JH, Vanderschuren LJ (2014) Disrupted social development enhances the motivation for cocaine in rats. Psychopharmacology (Berl) 231:1695–1704.
9. Badanich KA, Adler KJ, Kirstein CL (2006) Adolescents differ from adults in cocaine conditioned place preference and cocaine-induced dopamine in the nucleus accumbens septi. Eur J Pharmacol 550:95–106.
10. Bartolomucci A, Palanza P, Parmigiani S, Pederzani T, Merlot E, Neveu PJ, Dantzer R (2003) Chronic psychosocial stress down-regulates central cytokines mRNA. Brain Res Bull 62:173–178.
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 p38α MAPK deletion in serotonergic neurons produces stress resilience in models of depression and addiction. Neuron 71:498–511.
12. Burke AR, Watt MJ, Forster GL (2011) Adolescent social defeat increases adult amphetamine conditioned place preference and alters D2 dopamine receptor expression. Neuroscience 197:269–279.
13. Burke AR, Renner KJ, Forster GL, Watt MJ (2010) Adolescent social defeat alters neural, endocrine and behavioral responses to amphetamine in adult male rats. Brain Res 1352:147–156.
14. Buwalda B, de Boer SF, Schmidt ED, Felszeghy K, Nyakas C, Sgoifo A, Van der Vegt BJ, Tilders FJ, Bohus B, Koolhaas JM (1999) Long-lasting deficient dexamethasone suppression of hypothalamic–pituitary–adrenocortical activation following peripheral CRF challenge in socially defeated rats. J Neuroendocrinol 11:513–520.
15. Buwalda B, Kole MH, Veenema AH, Huininga M, de Boer SF, Korte SM, Koolhaas JM (2005) Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci Biobehav Rev 29:83–97.
16. Covington HE 3rd, Miczek KA (2001) Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration “binges”. Psychopharmacology (Berl) 158:388–398.
17. Daza-Losada M, Rodríguez-Arias M, Aguilar MA, Miñarro J (2009) Acquisition and reinstatement of MDMA-induced conditioned place preference in mice pre-treated with MDMA or cocaine during adolescence. Addict Biol 14:447–456.
18. Ding Y, Lin K, Li B, Ma L (2005) Enhanced cocaine self-administration in adult rats with adolescent isolation experience. Pharmacol Biochem Behav 82:673–677.
19. Dunbar RI (2010) The social role of touch in humans and primates: behavioural function and neurobiological mechanisms. Neurosci Biobehav Rev 34:260–268.
20. Franklin Kbj, Paxinos G (1997) The Mouse Brain in Stereotaxic Coordinates. Academic Press Inc: San Diego, California.
21. Gan X, Zhang L, Berger O, Stins MF, Way D, Taub DD, Chang SL, Kim KS, House SD, Weinand M, Witte M, Graves MC, Fiala M (1999) Cocaine enhances brain endothelial adhesion molecules and leukocyte migration. Clin Immunol 91:68–76.
22. García-Pardo MP, Rodríguez-Arias M, Maldonado C, Manzanedo C, Miñarro J, Aguilar MA (2014) Effects of acute social stress on the conditioned place preference induced by MDMA in adolescent and adult mice. Behav Pharmacol 25:532–546.
23. Gasche Y, Copin JC, Sugawara T, Fujimura M, Chan PH (2001) Matrix metalloproteinase inhibition prevents oxidative stress-associated blood–brain barrier disruption after transient focal cerebral ischemia. J Cereb Blood Flow Metab 21:1393–1400.
24. Gottschall PE, Deb S (1996) Regulation of matrix metalloproteinase expressions in astrocytes, microglia and neurons. Neuroimmunomodulation 3:69–75.
25. Hall FS, Wilkinson LS, Humby T, Inglis W, Kendall DA, Marsden CA, Robbins TW (1998) Isolation rearing in rats: pre- and postsynaptic changes in striatal dopaminergic systems. Pharmacol Biochem Behav 59:859–872.
26. Han X, Albrechet-Souza L, Doyle MR, Shimamoto A, DeBold JF, Miczek KA (2015) Social stress and escalated drug self-administration in mice II. Cocaine and dopamine in the nucleus accumbens. Psychopharmacology (Berl) 232:1003–1010.
27. Hanke ML, Powell ND, Stiner LM, Bailey MT, Sheridan JF (2012) β-Adrenergic blockade decreases the immunomodulatory effects of social disruption stress. Brain Behav Immun 26:1150–1159.
28. Hawkins BT, Davis TP (2005) The blood–brain barrier/neurovascular unit in health and disease. Pharmacol Rev 57:173–185.
29. Howes SR, Dalley JW, Morrison CH, Robbins TW, Everitt BJ (2000) Leftward shift in the acquisition of cocaine self-administration in isolation-reared rats: relationship to extracellular levels of dopamine, serotonin and glutamate in the nucleus accumbens and amygdala–striatal FOS expression. Psychopharmacology (Berl) 151:55–63.
30. Kabbaj M, Norton CS, Kollack-Walker S, Watson SJ, Robinson TE, Akil H (2001) Social defeat alters the acquisition of cocaine self-administration in rats: role of individual differences in cocaine-taking behavior. Psychopharmacology (Berl) 158:382–387.
31. Katsu M, Niizuma K, Yoshioka H, Okami N, Sakata H, Chan PH (2010) Hemoglobin-induced oxidative stress contributes to matrix metalloproteinase activation and blood–brain barrier dysfunction in vivo. J Cereb Blood Flow Metab 30:1939–1950.
32. Kessler RC, McLaughlin KA, Green JG, Gruber MJ, Sampson NA, Zaslavsky AM, Aguilar-Gaxiola S, Alhamzawi AO, Alonso J, Angermeyer M, Benjet C, Bromet E, Chatterji S, de Girolamo G, Demyttenaere K, Fayyad J, Florescu S, Gal G, Gureje O, Haro JM, Hu CY, Karam EG, Kawakami N, Lee S, Lépine JP, Ormel J, Posada-Villa J, Sagar R, Tsang A, Ustün TB, Vassilev S, Viana MC, Williams DR (2010) Childhood adversities and adult psychopathology in the WHO World Mental Health Surveys. Br J Psychiatry 197:378–385.
33. Kim EK, Choi EJ (2010) Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta 1802:396e405.
34. Kovalenko IL, Galyamina AG, Smagin DA, Michurina TV, Kudryavtseva NN, Enikolopov G (2014) Extended effect of chronic social defeat stress in childhood on behaviors in adulthood. PLoS Onee-pub ahead of print 25 March 2014 DOI: 10.1371/journal.pone.0091762.
35. Laviola G, Pascucci T, Pieretti S (2001) Striatal dopamine sensitization to d-amphetamine in periadolescent but not in adult rats. Pharmacol Biochem Behav 68:115–124.
36. Lee H, Park JW, Kim SP, Lo EH, Lee SR (2009) Doxycycline inhibits matrix metalloproteinase-9 and laminin degradation after transient global cerebral ischemia. Neurobiol Dis 34:189–198.
37. McCormick CM, Thomas CM, Sheridan CS, Nixon F, Flynn JA, Mathews IZ (2012) Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces deficits in spatial location memory in adulthood. Hippocampus 22:1300–1312.
38. Martini M, Valverde O (2012) A single episode of maternal deprivation impairs the motivation for cocaine in adolescent mice. Psychopharmacology (Berl) 219:149–158.
39. McQuaid RJ, Audet MC, Jacobson-Pick S, Anisman H (2013) Environmental enrichment influences brain cytokine variations elicited by social defeat in mice. Psychoneuroendocrinology 38:987–996.
40. Miczek KA, Covington HE 3rd, Nikulina EM Jr, Hammer RP (2004) Aggression and defeat: persistent effects on cocaine self-administration and gene expression in peptidergic and aminergic mesocorticolimbic circuits. Neurosci Biobehav Rev 27:787–802.
41. Montagud-Romero S, Daza-Losada M, Vidal-Infer A, Maldonado C, Aguilar MA, Miñarro J, Rodríguez-Arias M (2014) The novelty-seeking phenotype modulates the long-lasting effects of intermittent ethanol administration during adolescence. PLoS Onee-pub ahead of print 21 March 2014 DOI: 10.1371/journal.pone.0092576.
42. Novick AM, Miiller LC, Forster GL, Watt MJ (2013) Adolescent social defeat decreases spatial working memory performance in adulthood. Behav Brain Funct 9:39.
43. Patki G, Solanki N, Atrooz F, Ansari A, Allam F, Jannise B, Maturi J, Salim S (2014) Novel mechanistic insights into treadmill exercise based rescue of social defeat-induced anxiety-like behavior and memory impairment in rats. Physiol Behav 130:135–144.
44. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD (2006) Blood–brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 1:223–236.
45. Rodríguez-Arias M, Miñarro J, Aguilar MA, Pinazo J, Simón VM (1998) Effects of risperidone and SCH 23390 on isolation-induced aggression in male mice. Eur Neuropsychopharmacol 8:95–103.
46. Rodríguez-Arias M, Castillo A, Daza-Losada M, Aguilar MA, Miñarro J (2009) Effects of extended cocaine conditioning in the reinstatement of place preference. Physiol Behav 96:620–30.
47. Rodriguez-Arias M, Navarrete F, Blanco-Gandia MC, Arenas MC, Bartoll-Andrés A, Aguilar MA, Rubio G, Miñarro J, Manzanares J (2015) Social defeat in adolescent mice increases vulnerability to alcohol consumption. Addict Biol. in press, DOI: 10.1111/adb.12184.
48. Shaftel SS, Carlson TJ, Olschowka JA, Kyrkanides S, Matousek SB, O'Banion MK (2007) Chronic interleukin-1beta expression in mouse brain leads to leukocyte infiltration and neutrophil-independent blood brain barrier permeability without overt neurodegeneration. J Neurosci 27:9301–9309.
49. Shimamoto A, Holly EN, Boyson CO, DeBold JF, Miczek KA (2015) Individual differences in anhedonic and accumbal dopamine responses to chronic social stress and their link to cocaine self-administration in female rats. Psychopharmacology (Berl) 232:825–834.
50. Soria G, Mendizábal V, Touriño C, Robledo P, Ledent C, Parmentier M, Maldonado R, Valverde O (2005) Lack of CB1 cannabinoid receptor impairs cocaine self-administration. Neuropsychopharmacology 30:1670–1680.
51. Sterlemann V, Rammes G, Wolf M, Liebl C, Ganea K, Müller Mb, Schmidt MV (2010). Chronic social stress during adolescence induces cognitive impairment in aged mice. Hippocampus 20:540–549.
52. Tian W, Kyriakides TR (2009) Matrix metalloproteinase-9 deficiency leads to prolonged foreign body response in the brain associated with increased IL-1beta levels and leakage of the blood–brain barrier. Matrix Biol 28:148–59.
53. Tornatzky W, Miczek KA (1993) Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiol Behav 53:983–993.
54. Urrutia A, Rubio-Araiz A, Gutierrez-Lopez MD, ElAli A, Hermann DM, O'Shea E, Hermann DM, O'Shea E, Colado MI (2013) A study on the effect of JNK inhibitor, SP600125, on the disruption of blood–brain barrier induced by methamphetamine. Neurobiol Dis 50:49–58.
55. Vecil GG, Larsen PH, Corley SM, Herx LM, Besson A, Goodyer CG, Yong VW (2000) Interleukin-1 is a key regulator of matrix metalloproteinase-9 expression in human neurons in culture and following mouse brain trauma in vivo. J Neurosci Res 61:212–224.
56. Vidal J, Bie J, Granneman RA, Wallinga AE, Koolhaas JM, Buwalda B (2007) Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity. Physiol Behav 92:824–830.
57. Vidal-Infer A, Arenas MC, Daza-Losada M, Aguilar MA, Miñarro J, Rodríguez-Arias M (2012) High novelty-seeking predicts greater sensitivity to the conditioned rewarding effects of cocaine. Pharmacol Biochem Behav 102:124–132.
58. Watt MJ, Burke AR, Renner KJ, Forster GL (2009) Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults. Behav Neurosci 123:564–576.
59. Weidt A, Hofmann SE, Konig B (2012) Not only mate choice matters: fitness consequences of social partner choice in female house mice. Anim Behav 75:801–808.
60. Wohleb ES, Powell ND, Godbout JP, Sheridan JF (2013) Stress-induced recruitment of bone marrow derived monocytes to the brain promotes anxiety-like behavior. J Neurosci 33:13820–13833.
61. Wohleb ES, Hanke ML, Corona AW, Powell ND, Stiner LM, Bailey MT, Nelson RJ, Godbout JP, Sheridan JF (2011) β-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. J Neurosci 31:6277–6288.
62. Yao H, Kim K, Duan M, Hayashi T, Guo M, Morgello S, Prat A, Wang J, Su TP, Buch S (2011) Cocaine hijacks sigma 1 receptor to initiate induction of activated leukocyte cell adhesion molecule: implication for increased monocyte adhesion and migration in the CNS. J Neurosci 31:5942–5955.
63. Yap JJ, Chartoff EH, Holly EN, Potter DN, Carlezon WA Jr, Miczek KA (2015) Social defeat stress-induced sensitization and escalated cocaine self-administration: the role of ERK signaling in the rat ventral tegmental area. Psychopharmacology (Berl) 232:1555–1569.