Molecular mechanisms mediating a deficit in recall of fear extinction in adult mice exposed to cocaine in utero

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Kabir, Zeeba D ^a   Katzman, Aaron C ^b   Kosofsky, Barry E ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; COCAINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MESSENGER RNA; METHYL CPG BINDING PROTEIN 2;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BRAIN DERIVED NEUROTROPHIC FACTOR GENE; CONDITIONING; CONTROLLED STUDY; EMBRYO; EXON; HIPPOCAMPUS; LEARNING; MALE; MEDIAL PREFRONTAL CORTEX; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; PREFRONTAL CORTEX; PRENATAL DRUG EXPOSURE; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; RECALL; REINFORCEMENT;

ALTERNATIVE SPLICING; ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; COCAINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EXONS; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; HIPPOCAMPUS; MALE; MEMORY; MENTAL RECALL; METHYL-CPG-BINDING PROTEIN 2; MICE; PREFRONTAL CORTEX; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTOR, TRKB; RNA, MESSENGER;

EID: 84892945154     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084165     Document Type: Article

References (48)

1. Crandall JE, Hackett HE, Tobet SA, Kosofsky BE, Bhide PG (2004) Cocaine exposure decreases GABA neuron migration from the ganglionic eminence to the cerebral cortex in embryonic mice. Cereb Cortex 14: 665-675. doi:10.1093/cercor/bhh027. PubMed: 15054047.
2. Gressens P, Kosofsky BE, Evrard P (1992) Cocaine-induced disturbances of corticogenesis in the developing murine brain. Neurosci Lett 140: 113-116. doi:10.1016/0304-3940(92)90694-3. PubMed: 1407688.
3. Lidow MS, Song ZM (2001) Primates exposed to cocaine in utero display reduced density and number of cerebral cortical neurons. J Comp Neurol 435: 263-275. doi:10.1002/cne.1028. PubMed: 11406810.
4. Morrow BA, Elsworth JD, Roth RH (2005) Prenatal exposure to cocaine selectively disrupts the development of parvalbumin containing local circuit neurons in the medial prefrontal cortex of the rat. Synapse 56: 1-11. doi:10.1002/syn.20121. PubMed: 15700288.
5. Warner TD, Behnke M, Eyler FD, Padgett K, Leonard C et al. (2006) Diffusion tensor imaging of frontal white matter and executive functioning in cocaine-exposed children. Pediatrics 118: 2014-2024. doi:10.1542/peds.2006-0003. PubMed: 17079574.
6. Garavan H, Morgan RE, Mactutus CF, Levitsky DA, Booze RM et al. (2000) Prenatal cocaine exposure impairs selective attention: evidence from serial reversal and extradimensional shift tasks. Behav Neurosci 114: 725-738. doi:10.1037/0735-7044.114.4.725. PubMed: 10959532.
7. Romano AG, Harvey JA (1996) Prenatal exposure to cocaine disrupts discrimination learning in adult rabbits. Pharmacol Biochem Behav 53: 617-621. doi:10.1016/0091-3057(95)02061-6. PubMed: 8866963.
8. Singer LT, Eisengart LJ, Minnes S, Noland J, Jey A et al. (2005) Prenatal cocaine exposure and infant cognition. Infant Behav Dev 28: 431-444. doi:10.1016/j.infbeh.2005.03.002. PubMed: 19079636.
9. Wilkins AS, Genova LM, Posten W, Kosofsky BE (1998) Transplacental cocaine exposure. 1: A rodent model. Neurotoxicol Teratol 20: 215-226. doi:10.1016/S0892-0362(97)00125-6. PubMed: 9638679.
10. Kabir ZD, Lourenco F, Byrne ME, Katzman A, Lee F et al. (2012) Brain-derived neurotrophic factor genotype impacts the prenatal cocaine-induced mouse phenotype. Dev Neurosci 34: 184-197. doi: 10.1159/000337712. PubMed: 22572518.
11. Andero R, Ressler KJ (2012) Fear extinction and BDNF: translating animal models of PTSD to the clinic. Genes Brain Behav 11: 503-512. doi:10.1111/j.1601-183X.2012.00801.x. PubMed: 22530815.
12. Peters J, Kalivas PW, Quirk GJ (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16: 279-288. doi: 10.1101/lm.1041309. PubMed: 19380710.
13. Quirk GJ, Mueller D (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33: 56-72. doi:10.1038/sj.npp.1301555. PubMed: 17882236.
14. Sotres-Bayon F, Quirk GJ (2010) Prefrontal control of fear: more than just extinction. Curr Opin Neurobiol 20: 231-235. doi:10.1016/j.conb.2010.02. 005. PubMed: 20303254.
15. Sotres-Bayon F, Cain CK, LeDoux JE (2006) Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol Psychiatry 60: 329-336. doi:10.1016/j.biopsych.2005.10.012. PubMed: 16412988.
16. Rosenkranz JA, Moore H, Grace AA (2003) The prefrontal cortex regulates lateral amygdala neuronal plasticity and responses to previously conditioned stimuli. J Neurosci 23: 11054-11064. PubMed: 14657162.
17. Quirk GJ, Likhtik E, Pelletier JG, Paré D (2003) Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 23: 8800-8807. PubMed: 14507980.
18. Sotres-Bayon F, Sierra-Mercado D, Pardilla-Delgado E, Quirk GJ (2012) Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron 76: 804-812. doi:10.1016/j.neuron.2012.09.028. PubMed: 23177964.
19. Peters J, Dieppa-Perea LM, Melendez LM, Quirk GJ (2010) Induction of fear extinction with hippocampal-infralimbic BDNF. Science 328: 1288-1290. doi:10.1126/science.1186909. PubMed: 20522777.
20. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T (2007) Mouse and rat BDNF gene structure and expression revisited. J Neurosci Res 85: 525-535. doi:10.1002/jnr.21139. PubMed: 17149751.
21. Lu Y, Ji Y, Ganesan S, Schloesser R, Martinowich K et al. (2011) TrkB as a potential synaptic and behavioral tag. J Neurosci 31: 11762-11771. doi:10.1523/JNEUROSCI.2707-11.2011. PubMed: 21849537.
22. Chen WG, West AE, Tao X, Corfas G, Szentirmay MN et al. (2003) Upstream stimulatory factors are mediators of Ca2+-responsive transcription in neurons. J Neurosci 23: 2572-2581. PubMed: 12684442.
23. Tabuchi A, Sakaya H, Kisukeda T, Fushiki H, Tsuda M (2002) Involvement of an upstream stimulatory factor as well as cAMPresponsive element-binding protein in the activation of brain-derived neurotrophic factor gene promoter I. J Biol Chem 277: 35920-35931. doi:10.1074/jbc.M204784200. PubMed: 12114522.
24. Tao X, Finkbeiner S, Arnold DB, Shaywitz AJ, Greenberg ME (1998) Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20: 709-726. doi: 10.1016/S0896-6273(00) 81010-7. PubMed: 9581763.
25. Tian F, Marini AM, Lipsky RH (2010) NMDA receptor activation induces differential epigenetic modification of Bdnf promoters in hippocampal neurons. Amino Acids 38: 1067-1074. doi:10.1007/s00726-009-0315-y. PubMed: 19565326.
26. Li T, Talvenheimo J, Zeni L, Rosenfeld R, Stearns G et al. (2002) Changes in protein conformation and dynamics upon complex formation of brain-derived neurotrophic factor and its receptor: investigation by isotope-edited Fourier transform IR spectroscopy. Biopolymers 67: 10-19. doi:10.1002/bip.10038. PubMed: 11842409.
27. Lu B (2003) Pro-region of neurotrophins: role in synaptic modulation. Neuron 39: 735-738. doi:10.1016/S0896-6273(03)00538-5. PubMed: 12948441.
28. Greenberg ME, Xu B, Lu B, Hempstead BL (2009) New insights in the biology of BDNF synthesis and release: implications in CNS function. J Neurosci 29: 12764-12767. doi:10.1523/JNEUROSCI.3566-09.2009. PubMed: 19828787.
29. Holson RR, Pearce B (1992) Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. Neurotoxicol Teratol 14: 221-228. doi:10.1016/0892-0362(92)90020-B. PubMed: 1635542.
30. Giordano TP 3rd, Satpute SS, Striessnig J, Kosofsky BE, Rajadhyaksha AM (2006) Up-regulation of dopamine D(2)L mRNA levels in the ventral tegmental area and dorsal striatum of amphetamine-sensitized C57BL/6 mice: role of Ca(v)1.3 L-type Ca(2+) channels. J Neurochem 99: 1197-1206. doi:10.1111/j.1471-4159.2006. 04186.x.
31. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST et al. (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 320: 1224-1229. doi:10.1126/science.1153252. PubMed: 18511691.
32. Chen WG, Chang Q, Lin Y, Meissner A, West AE et al. (2003) Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302: 885-889. doi:10.1126/science.1086446. PubMed: 14593183.
33. Tsankova NM, Kumar A, Nestler EJ (2004) Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J Neurosci 24: 5603-5610. doi:10.1523/JNEUROSCI.0589-04.2004. PubMed: 15201333.
34. Paz R, Barsness B, Martenson T, Tanner D, Allan AM (2007) Behavioral teratogenicity induced by nonforced maternal nicotine consumption. Neuropsychopharmacology 32: 693-699. doi:10.1038/sj.npp.1301066. PubMed: 16554741.
35. Eiden RD, Foote A, Schuetze P (2007) Maternal cocaine use and caregiving status: group differences in caregiver and infant risk variables. Addict Behav 32: 465-476. doi:10.1016/j.addbeh. 2006.05.013. PubMed: 16837139.
36. Lester BM, Lin H, Degarmo DS, Fisher PA, Lagasse LL et al. (2012) Neurobehavioral disinhibition predicts initiation of substance use in children with prenatal cocaine exposure. Drug Alcohol Depend 126: 80-86. doi:10.1016/j.drugalcdep.2012.04.014. PubMed: 22608010.
37. Lester BM, Lagasse LL (2010) Children of addicted women. J Addict Dis 29: 259-276. doi:10.1080/10550881003684921. PubMed: 20407981.
38. Delaney-Black V, Chiodo LM, Hannigan JH, Greenwald MK, Janisse J et al. (2011) Prenatal and postnatal cocaine exposure predict teen cocaine use. Neurotoxicol Teratol 33: 110-119. doi:10.1016/j.ntt.2010.06.011. PubMed: 20609384.
39. Frank DA, Rose-Jacobs R, Crooks D, Cabral HJ, Gerteis J et al. (2011) Adolescent initiation of licit and illicit substance use: Impact of intrauterine exposures and post-natal exposure to violence. Neurotoxicol Teratol 33: 100-109. doi:10.1016/j.ntt.2010.06.002. PubMed: 20600847.
40. Fisher PA, Lester BM, DeGarmo DS, Lagasse LL, Lin H et al. (2011) The combined effects of prenatal drug exposure and early adversity on neurobehavioral disinhibition in childhood and adolescence. Dev Psychopathol 23: 777-788. doi:10.1017/S0954579411000290. PubMed: 21756431.
41. Herry C, Ferraguti F, Singewald N, Letzkus JJ, Ehrlich I et al. (2010) Neuronal circuits of fear extinction. Eur J Neurosci 31: 599-612. doi: 10.1111/j.1460-9568.2010.07101.x. PubMed: 20384807.
42. Wilkins AS, Jones K, Kosofsky BE (1998) Transplacental cocaine exposure. 2: Effects of cocaine dose and gestational timing. Neurotoxicol Teratol 20: 227-238. doi:10.1016/S0892-0362(97)00127-X. PubMed: 9638680.
43. Corcoran KA, Quirk GJ (2007) Activity in prelimbic cortex is necessary for the expression of learned, but not innate, fears. J Neurosci 27: 840-844. doi:10.1523/JNEUROSCI.5327-06.2007. PubMed: 17251424.
44. Hong EJ, McCord AE, Greenberg ME (2008) A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 60: 610-624. doi:10.1016/j.neuron.2008.09.024. PubMed: 19038219.
45. 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. doi:10.1111/j.1460-9568.2007.05918.x. PubMed: 18001273.
46. Sobreviela T, Pagcatipunan M, Kroin JS, Mufson EJ (1996) Retrograde transport of brain-derived neurotrophic factor (BDNF) following infusion in neo- and limbic cortex in rat: relationship to BDNF mRNA expressing neurons. J Comp Neurol 375: 417-444. doi:10.1002/(SICI)1096-9861(19961118)375:3. PubMed: 8915840.
47. Bredy TW, Wu H, Crego C, Zellhoefer J, Sun YE et al. (2007) Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learn Mem 14: 268-276. doi:10.1101/lm.500907. PubMed: 17522015.
48. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM et al. (2001) Calcium regulation of neuronal gene expression. Proc Natl Acad Sci U S A 98: 11024-11031. doi:10.1073/pnas.191352298. PubMed: 11572963.