Prolonged abstinence from developmental cocaine exposure dysregulates BDNF and its signaling network in the medial prefrontal cortex of adult rats

International Journal of Neuropsychopharmacology

Volumn 17, Issue 4, 2014, Pages 625-634

  Giannotti, Giuseppe ^a,b   Caffino, Lucia ^a,b   Calabrese, Francesca ^a,b   Racagni, Giorgio ^a,b,c   Riva, Marco A ^a,b   Fumagalli, Fabio ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b Presidency of the Council of Ministers   (Italy)

^c IRCCS ISTITUTO CENTRO SAN GIOVANNI DI DIO FATEBENEFRATELLI   (Italy)

Author keywords

Adolescence; cocaine; neurotrophins; prefrontal cortex

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM RESPONSIVE FACTOR; COCAINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA 124; MICRORNA 132; MITOGEN ACTIVATED PROTEIN KINASE 1; NEURONAL PER ARNT SIM DOMAIN PROTEIN 4; NEUROTROPHIN; PROTEIN KINASE B; S6 KINASE; TISSUE PLASMINOGEN ACTIVATOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DOPAMINE UPTAKE INHIBITOR; MESSENGER RNA; MICRORNA;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EXPOSURE; DRUG WITHDRAWAL; ENZYME ACTIVATION; MEDIAL PREFRONTAL CORTEX; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; AGE; ANIMAL; DRUG EFFECTS; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AGE FACTORS; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; COCAINE; DOPAMINE UPTAKE INHIBITORS; MALE; MICRORNAS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84896388752     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145713001454     Document Type: Article

References (46)

1. Alvaro-Bartolome M, La Harpe R, Callado LF, Meana JJ, Garcia-Sevilla JA (2011) Molecular adaptations of apoptotic pathways and signaling partners in the cerebral cortex of human cocaine addicts and cocaine-treated rats. Neuroscience 196:1-15.
2. Andersen SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27:3-18.
3. Barbon A, Fumagalli F, Caracciolo L, Madaschi L, Lesma E, Mora C, Carelli S, Slotkin TA, Racagni G, Di Giulio AM, Gorio A, Barlati S (2010) Acute spinal cord injury persistently reduces R/G RNA editing of AMPA receptors. J Neurochem 114:397-407.
4. Berglind WJ, See RE, Fuchs RA, Ghee SM, Whitfield TW Jr., Miller SW, McGinty JF (2007) A BDNF infusion into the medial prefrontal cortex suppresses cocaine seeking in rats. Eur J Neurosci 26:757-766.
5. Berglind WJ, Whitfield TW Jr., LaLumiere RT, Kalivas PW, McGinty JF (2009) A single intra-PFC infusion of BDNF prevents cocaine-induced alterations in extracellular glutamate within the nucleus accumbens. J Neurosci 29:3715-3719.
6. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K (2010) The Arc of synaptic memory. Exp Brain Res 200:125-140.
7. Caffino L, Racagni G, Fumagalli F (2011) Stress and cocaine interact to modulate Arc/Arg3.1 expression in rat brain. Psychopharmacol (Berl) 218:241-248.
8. Caffino L, Calabrese F, Giannotti G, Barbon A, Verheij MM, Racagni G, Fumagalli F (2013) Stress rapidly dysregulates the glutamatergic synapse in the prefrontal cortex of cocaine-withdrawn adolescent rats. Addict Biol. doi: 10.1111/adb.12089. [Epub ahead of print].
9. Casey BJ, Getz S, Galvan A (2008) The adolescent brain. Dev Rev 28:62-77.
10. Chandrasekar V, Dreyer JL (2009) microRNAs miR-124, let-7d and miR-181a regulate cocaine-induced plasticity. Mol Cell Neurosci 42:350-362.
11. Chapman RH, Stern JM (1978) Maternal stress and pituitary-adrenal manipulations during pregnancy in rats: effects on morphology and sexual behaviour of male offspring. J Comp Physiol Psychol 92:1074-1083.
12. Chourbaji S, Brandwein C, Vogt MA, Dormann C, Hellweg R, Gass P (2008) Nature vs. nurture: can enrichment rescue the behavioural phenotype of BDNF heterozygous mice? Behav Brain Res 192:254-258.
13. Chourbaji S, Brandwein C, Gass P (2011) Altering BDNF expression by genetics and/or environment: impact for emotional and depression-like behaviour in laboratory mice. Neurosci Biobehav Rev 35:599-611.
14. Chourbaji S, Hortnagl H, Molteni R, Riva MA, Gass P, Hellweg R (2012) The impact of environmental enrichment on sex-specific neurochemical circuitries-effects on brain-derived neuro-trophic factor and the serotonergic system. Neuroscience 220:267-276.
15. Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52:445-459.
16. Collins SL, Izenwasser S (2004) Chronic nicotine differentially alters cocaine-induced locomotor activity in adolescent vs. adult male and female rats. Neuropharmacol 46:349-362.
17. Ernst M, Romeo RD, Andersen SL (2009) Neurobiology of the development of motivated behaviours in adolescence: a window into a neural systems model. Pharmacol Biochem Behav 93:199-211.
18. Filip M, Faron-Gorecka A, Kusmider M, Golda A, Frankowska M, Dziedzicka-Wasylewska M (2006) Alterations in BDNF and trkB mRNAs following acute or sensitizing cocaine treatments and withdrawal. Brain Res 1071:218-225.
19. Fumagalli F, Bedogni F, Frasca A, Di Pasquale L, Racagni G, Riva MA (2006) Corticostriatal up-regulation of activity-regulated cytoskeletal- associated protein expression after repeated exposure to cocaine. Mol Pharmacol 70:1726-1734.
20. Fumagalli F, Di Pasquale L, Caffino L, Racagni G, Riva MA (2007) Repeated exposure to cocaine differently modulates BDNF mRNA and protein levels in rat striatum and prefrontal cortex. Eur J Neurosci 26:2756-2763.
21. Fumagalli F, Caffino L, Racagni G, Riva MA (2009a) Repeated stress prevents cocaine-induced activation of BDNF signaling in rat prefrontal cortex. Eur Neuropsychopharmacol 19:402-408.
22. Fumagalli F, Franchi C, Caffino L, Racagni G, Riva MA, Cervo L (2009b) Single session of cocaine intravenous self-administration shapes goal-oriented behaviours and up-regulates Arc mRNA levels in rat medial prefrontal cortex. Int J Neuropsychopharmacol 12:423-429.
23. Fumagalli F, Calabrese F, Luoni A, Bolis F, Racagni G, Riva MA (2012) Modulation of BDNF expression by repeated treatment with the novel antipsychotic lurasidone under basal condition and in response to acute stress. Int J Neuropsychopharmacol 15:235-246.
24. Fumagalli F, Moro F, Caffino L, Orru A, Cassina C, Giannotti G, Di Clemente A, Racagni G, Fumagalli F, Cervo L (2013) Region-specific effects on BDNF expression after contingent or non-contingent cocaine i.v. self-administration in rats. Int J Neuropsychopharmacol 16:913-918.
25. Gong R, Park CS, Abbassi NR, Tang SJ (2006) Roles of glutamate receptors and the mammalian target of rapamycin (mTOR) signaling pathway in activity-dependent dendritic protein synthesis in hippocampal neurons. J Biol Chem 281:18802-18815.
26. Graham DL, Edwards S, Bachtell RK, DiLeone RJ, Rios M, Self DW (2007) Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat Neurosci 10:1029-1037.
27. Grimm JW, Lu L, Hayashi T, Hope BT, Su TP, Shaham Y (2003) Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J Neurosci 23:742-747.
28. Hearing MC, Miller SW, See RE, McGinty JF (2008) Relapse to cocaine seeking increases activity-regulated gene expression differentially in the prefrontal cortex of abstinent rats. Psychopharmacol (Berl) 198:77-91.
29. Hearing MC, Schwendt M, McGinty JF (2011) Suppression of activity-regulated cytoskeleton-associated gene expression in the dorsal striatum attenuates extinction of cocaine-seeking. Int J Neuropsychopharmacol 14:784-795.
30. Hoeffer CA, Klann E (2010) mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci 33:67-75.
31. Horger BA, Iyasere CA, Berhow MT, Messer CJ, Nestler EJ, Taylor JR (1999) Enhancement of locomotor activity and conditioned reward to cocaine by brain-derived neurotrophic factor. J Neurosci 19:4110-4122.
32. Kelley AE, Schochet T, Landry CF (2004) Risk taking and novelty seeking in adolescence: introduction to part I. Ann N Y Acad Sci 1021:27-32.
33. Lu L, Dempsey J, Liu SY, Bossert JM, Shaham Y (2004) A single infusion of brain-derived neurotrophic factor into the ventral tegmental area induces long-lasting potentiation of cocaine seeking after withdrawal. J Neurosci 24:1604-1611.
34. McGinty JF, Whitfield TW Jr., Berglind WJ (2010) Brain-derived neurotrophic factor and cocaine addiction. Brain Res 1314:183-193.
35. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippo-campal plasticity. Science 306:487-491.
36. Panja D, Bramham CR (2013) BDNF mechanisms in late LTP formation: a synthesis and breakdown. Neuropharmacol doi: pii: S0028-3908(13)00292-X. 10.1016/j.neuropharm.2013. 06.024. [Epub ahead of print].
37. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, 5th edn. New York: Academic Press.
38. Pruunsild P, Sepp M, Orav E, Koppel I, Timmusk T (2011) Identification of cis-elements and transcription factors regulating neuronal activity-dependent transcription of human BDNF gene. J Neurosci 31:3295-3308.
39. Rial Verde EM, Lee-Osbourne J, Worley PF, Malinow R, Cline HT (2006) Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52:461-474.
40. Saarelainen T, Hendolin P, Lucas G, Koponen E, Sairanen M, MacDonald E, Agerman K, Haapasalo A, Nawa H, Aloyz R, Ernfors P, Castren E (2003) Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioural effects. J Neurosci 23:349-357.
41. Sadri-Vakili G, Kumaresan V, Schmidt HD, Famous KR, Chawla P, Vassoler FM, Overland RP, Xia E, Bass CE, Terwilliger EF, Pierce RC, Cha JH (2010) Cocaine-induced chromatin remodeling increases brain-derived neurotrophic factor transcription in the rat medial prefrontal cortex, which alters the reinforcing efficacy of cocaine. J Neurosci 30:11735-11744.
42. Spear LP (2000) The adolescent brain and age-related behavioural manifestations. Neurosci Biobehav Rev 24:417-463.
43. Swiech L, Perycz M, Malik A, Jaworski J (2008) Role of mTOR in physiology and pathology of the nervous system. Biochim Biophys Acta 1784:116-132.
44. Twining RC, Bolan M, Grigson PS (2009) Yoked delivery of cocaine is aversive and protects against the motivation for drug in rats. Behav Neurosci 123:913-925.
45. Wang X, Luo YX, He YY, Li FQ, Shi HS, Xue LF, Xue YX, Lu L (2010) Nucleus accumbens core mammalian target of rapamycin signaling pathway is critical for cue-induced reinstatement of cocaine seeking in rats. J Neurosci 30:12632-12641.
46. Whitfield TW Jr., Shi X, Sun WL, McGinty JF (2011) The suppressive effect of an intra-prefrontal cortical infusion of BDNF on cocaine-seeking is Trk receptor and extracellular signal-regulated protein kinase mitogen-activated protein kinase dependent. J Neurosci 31:834-842.