Extracellular Signal-Regulated Kinase 1/2 Involvement in the Enhancement of Contextual Fear Conditioning by Nicotine

Behavioral Neuroscience

Volumn 121, Issue 5, 2007, Pages 1119-1124

  Raybuck, Jonathan D ^a   Gould, Thomas J ^a  

^a TEMPLE UNIVERSITY   (United States)

Author keywords

acetylcholine; contextual fear conditioning; ERK 1 2; learning; nicotine

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NICOTINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; C57BL 6 MOUSE; CONDITIONING; CONTROLLED STUDY; FEAR; MALE; MOUSE; NONHUMAN;

AMINOACETONITRILE; ANIMALS; CONDITIONING (PSYCHOLOGY); ENZYME INHIBITORS; FEAR; MALE; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NICOTINE; NICOTINIC AGONISTS;

EID: 35148857014     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.121.5.1119     Document Type: Article

References (70)

1. Ahi J., Radulovic J., and Spiess J. The role of hippocampal signaling cascades in consolidation of fear memory. Behavioral Brain Research 149 (2004) 17-31
2. Atkins C., Selcher J., Petraitis J., Traskos J., and Sweatt J. The MAPK cascade is required for mammalian associative learning. Nature Neuroscience 1 (1998) 602-609
3. Bardgett M.E., Boeckman R., Krochmal D., Fernando H., Ahrens R., and Csernansky J.G. NMDA receptor blockade and hippocampal neuronal loss impair fear conditioning and position habit reversal in C57Bl/6 mice. Brain Research Bulletin 60 1-2 (2003) 131-142
4. ++ permeability. Biochemical Society Transcripts 22 3 (1994) 294S
5. Berkeley J.L., and Levey A.I. Cell-specific extracellular signal-regulated kinase activation by multiple G protein-coupled receptor families in hippocampus. Molecular Pharmacology 63 (2003) 128-135
6. Bliss T.V., and Collingridge G.L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361 (1993, January 7) 31-39
7. Brunzell D.H., Russell D.S., and Picciotto M.R. In vivo nicotine treatment regulates mesocorticolimbic CREB and ERK signaling in C57Bl/6J mice. Journal of Neurochemistry 84 (2003) 1431-1441
8. Chen M.J., Nguyen T.V., Pike C.J., and Russo-Neustadt A.A. Norepinephrine induces BDNF and activates the PI-3K and MAPK cascades in embryonic hippocampal neurons. Cell Signaling 19 (2007) 114-128
9. Ciamei A., Averson M., Cestari V., and Castellano C. Effects of MK-801 and nicotine combination on memory consolidation in CD1 mice. Psychopharmacology 154 (2002) 126-130
10. Cohen B.H. Explaining psychological statistics. 2nd ed. (2001), Wiley, New York
11. Coogan A.N., O'Leary D.M., and O'Connor J.J. P42/44 MAP kinase inhibitor PD098059 attenuates multiple forms of synaptic plasticity in rat dentate gyrus in vitro. Journal of Neurophysiology 81 (1999) 103-110
12. Csernansky J.G., Martin M., Shah R., Bertchume A., Colvin J., and Dong H. Cholinesterase inhibitors ameliorate behavioral deficits induced by MK-801 in mice. Neuropsychopharmacology 30 (2005) 2135-2143
13. Dajas-Bailador F.A., Soliakov L., and Wonnacott S. Intracellular Ca2+ signals evoked by stimulation of nicotinic acetylcholine receptors in SH-SY5Y cells: Contribution of voltage-operated Ca2+ channels and Ca2+ stores. Journal of Neurochemistry 80 (2002) 520-530
14. Davis J.A., and Gould T.J. The effects of DHBE and MLA on nicotine-induced enhancement of contextual fear conditioning in C57BL/6 mice. Psychopharmacology (Berlin) 184 (2006) 345-352
15. Davis J.A., Porter J., and Gould T.J. Nicotine enhances both foreground and background contextual fear conditioning. Neuroscience Letters 394 (2005) 202-205
16. English J.D., and Sweatt J.D. Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. Journal of Biological Chemistry 271 (1996) 24329-24332
17. English J.D., and Sweatt J.D. A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. Journal of Biological Chemistry 272 (1997) 19103-19106
18. Errico M., Crozier R.A., Plummer M.R., and Cowen D.S. 5-HT(7) receptors activate the mitogen activated protein kinase extracellular signal related kinase in cultured rat hippocampal neurons. Neuroscience 102 (2001) 361-367
19. Favata M.F., Horiuchi K.Y., Manos E.J., Daulerio A.J., Stradley D.A., Feeser W.S., et al. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. Journal of Biological Chemistry 273 (1998) 18623-18632
20. Fedele E., Varnier G., Ansaldo M.A., and Raiteri M. Nicotine administration stimulates the in vivo N-methyl-D-aspartate receptor/nitric oxide/cyclic GMP pathway in rat hippocampus through glutamate release. British Journal of Pharmacology 125 (1998) 1042-1048
21. Feiro O., and Gould T.J. The interactive effects of nicotinic and muscarinic cholinergic receptor inhibition on fear conditioning in young and aged C57BL/6 mice. Pharmacology, Biochemistry, and Behavior 80 (2005) 251-262
22. Florian C., Mons N., and Roullet P. CREB antisense oligodeoxynucleotide administration into the dorsal hippocampal CA3 region impairs long- but not short-term spatial memory in mice. Learning & Memory 13 (2006) 465-472
23. Fujii S., Ji Z., Morita N., and Sumikawa K. Acute and chronic nicotine exposure differentially facilitate the induction of LTP. Brain Research 846 (1999) 137-143
24. Gould T.J., Feiro O., and Moore D. Nicotine enhances trace cued fear conditioning but not delay cued fear conditioning in C57BL/6 mice. Behavioral Brain Research 155 (2004) 167-173
25. Gould T.J., and Higgins J.S. Nicotine enhances contextual fear conditioning in C57BL/6J mice at 1 and 7 days post-training. Neurobiology of Learning and Memory 80 (2003) 147-157
26. Gould T.J., and Lewis M.C. Coantagonism of glutamate receptors and nicotinic acetylcholinergic receptors disrupts fear conditioning and latent inhibition of fear conditioning. Learning Memory 12 (2005) 389-398
27. Gould T.J., and Lommock J.A. Nicotine enhances contextual fear conditioning and ameliorates ethanol-induced deficits in contextual fear conditioning. Behavioral Neuroscience 117 (2003) 1276-1282
28. Gould T.J., McCarthy M.M., and Keith R.A. MK-801 disrupts acquisition of contextual fear conditioning but enhances memory consolidation of cued fear conditioning. Behavioural Pharmacology 13 (2002) 287-294
29. Gould T.J., and Wehner J.M. Nicotine enhancement of contextual fear conditioning. Behavioral Brain Research 102 (1999) 31-39
30. Grady S.R., Marks M.J., and Collins A.C. Desensitization of nicotine-stimulated [3H]dopamine release from mouse striatal synaptosomes. Journal of Neurochemistry 62 (1994) 1390-1398
31. Grady S.R., Murphy K.L., Cao J., Marks M.J., McIntosh J.M., and Collins A.C. Characterization of nicotinic agonist-induced [(3)H]dopamine release from synaptosomes prepared from four mouse brain regions. Journal Pharmacology and Experimental Therapeutics 301 (2002) 651-660
32. Graves L., Dalvi A., Lucki I., Blendy J.A., and Abel T. Behavioral analysis of CREB alphadelta mutation on a B6/129 F1 hybrid background. Hippocampus 12 (2002) 18-26
33. Hu M., Liu Q.S., Chang K.T., and Berg D.K. Nicotinic regulation of CREB activation in hippocampal neurons by glutamatergic and nonglutamatergic pathways. Molecular and Cellular Neurosciences 21 (2002) 616-625
34. Impey S., Obrietan K., Wong S.T., Poser S., Yano S., Wayman G., et al. Cross talk between ERK and PKA is required for Ca2+ stimulation of CREB-dependent transcription and ERK nuclear translocation. Neuron 21 (1998) 869-883
35. Impey S., Smith D.M., Obrietan K., Donahue R., Wade C., and Storm D.R. Stimulation of cAMP response element (CRE)-mediated transcription during contextual learning. Nature Neuroscience 1 (1998) 595-601
36. Izquierdo I., and McGaugh J.L. Behavioural pharmacology and its contribution to the molecular basis of memory consolidation. Behavioural Pharmacology 11 7-8 (2000) 517-534
37. Ji J.Z., Wang X.M., and Li B.M. Deficit in long-term contextual fear memory induced by blockade of beta-adrenoceptors in hippocampal CA1 region. European Journal of Neuroscience 17 (2003) 1947-1952
38. Levin E.D., Bettegowda C., Weaver T., and Christopher N.C. Nicotine-dizocilpine interactions and working and reference memory performance of rats in the radial-arm maze. Pharmacology, Biochemistry and Behavior 61 (1998) 335-340
39. Logue S.F., Paylor R., and Wehner J.M. Hippocampal lesions cause learning deficits in inbred mice in the Morris water maze and conditioned-fear task. Behavioral Neuroscience 111 (1997) 104-113
40. Matsuyama S., Matsumoto A., Enomoto T., and Nishizaki T. Activation of nicotinic acetylcholine receptors induces long-term potentiation in vivo in the intact mouse dentate gyrus. European Journal of Neuroscience 12 (2000) 3741-3747
41. Maxwell S.E., and Delaney H.D. Designing experiments and analyzing data: A model comparison perspective. 2nd ed. (2003), Erlbaum, Mahwah, NJ
42. McGehee D.S., Heath M.J., Gelber S., Devay P., and Role L.W. Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269 (1995, September 22) 1692-1696
43. Melik E., Babar-Melik E., Ozgunen T., and Binokay S. Median raphe nucleus mediates forming long-term but not short-term contextual fear conditioning in rats. Behavioral Brain Research 112 (2000) 145-150
44. Nakayama H., Numakawa T., Ikeuchi T., and Hatanaka H. Nicotine-induced phosphorylation of extracellular signal-regulated protein kinase and CREB in PC12h cells. Journal of Neurochemistry 79 (2001) 489-498
45. Nowak L., Bregestovski P., Ascher P., Herbet A., and Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307 (1984, February 2) 462-465
46. Petersen D.R., Norris K.J., and Thompson J.A. A comparative study of the disposition of nicotine and its metabolites in three inbred strains of mice. Drug Metabolism and Disposition 12 (1984) 725-731
47. Pezze M.A., Heidbreder C.A., Feldon J., and Murphy C.A. Selective responding of nucleus accumbens core and shell dopamine to aversively conditioned contextual and discrete stimuli. Neuroscience 108 (2001) 91-102
48. Phillips R.G., and LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 106 (1992) 274-285
49. Radcliffe K.A., Fisher J.L., Gray R., and Dani J.A. Nicotinic modulation of glutamate and GABA synaptic transmission of hippocampal neurons. Annals of the New York Academy of the Sciences 868 (1999) 591-610
50. Rao T.S., Correa L.D., Adams P., Santori E.M., and Sacaan A.I. Pharmacological characterization of dopamine, norepinephrine and serotonin release in the rat prefrontal cortex by neuronal nicotinic acetylcholine receptor agonists. Brain Research 990 (2003) 203-208
51. Riedel G., Platt B., and Micheau J. Glutamate receptor function in learning and memory. Behavioral Brain Research 140 (2003, March 18) 1-47
52. Risso F., Grilli M., Parodi M., Bado M., Raiteri M., and Marchi M. Nicotine exerts a permissive role on NMDA receptor function in hippocampal noradrenergic terminals. Neuropharmacology 47 (2004) 65-71
53. Roberts A.J., Krucker T., Levy C.L., Slanina K.A., Sutcliffe J.G., and Hedlund P.B. Mice lacking 5-HT receptors show specific impairments in contextual learning. European Journal of Neuroscience 19 (2004) 1913-1922
54. Rosen L.B., Ginty D.D., Weber M.J., and Greenberg M.E. Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12 (1994) 1207-1221
55. Runyan J.D., and Dash P.K. Intra-medial prefrontal administration of SCH-23390 attenuates ERK phosphorylation and long-term memory for trace fear conditioning in rats. Neurobiology of Learning and Memory 82 (2004) 65-70
56. Sananbenesi F., Fischer A., Schrick C., Spiess J., and Radulovic J. Phosphorylation of hippocampal Erk-1/2, Elk-1, and p90-Rsk-1 during contextual fear conditioning: Interactions between Erk-1/2 and Elk-1. Molecular and Cellular Neurosciences 21 (2002) 463-476
57. Sananbenesi F., Fischer A., Schrick C., Spiess J., and Radulovic J. Mitogen-activated protein kinase signaling in the hippocampus and its modulation by corticotropin-releasing factor receptor 2: A possible link between stress and fear memory. Neuropharmacology 44 (2003) 1089-1099
58. Sawada S., Ohno-Shosaku T., and Yamamoto C. Augmenting action of nicotine on population spikes in the dentate gyrus of the guinea pig. Neuroscience Research 20 (1994) 317-322
59. Seguela P., Wadiche J., Dineley-Miller K., Dani J.A., and Patrick J.W. Molecular cloning, functional properties, and distribution of rat brain alpha 7: A nicotinic cation channel highly permeable to calcium. Journal of Neuroscience 13 (1993) 596-604
60. Selcher J.C., Atkins C.M., Trzaskos J.M., Paylor R., and Sweatt J.D. A necessity for MAP kinase activation in mammalian spatial learning. Learning & Memory 6 (1999) 478-490
61. Shalin S., Zirrgiebel U., Honsa K., Julien J., Miller F., Kaplan D., and Sweatt J. Neuronal MEK is important for normal fear conditioning in mice. Journal of Neuroscience Research 75 (2004) 760-770
62. Singer S., Rossi S., Verzosa S., Hashim A., Lonow R., Cooper T., et al. Nicotine-induced changes in neurotransmitter levels in brain areas associated with cognitive function. Neurochemical Research 29 (2004) 1779-1792
63. Soares J.C., Fornari R.V., and Oliveira M.G. Role of muscarinic M1 receptors in inhibitory avoidance and contextual fear conditioning. Neurobiology of Learning and Memory 86 (2006) 188-196
64. Sweatt J.D. The neuronal MAP kinase cascade: A biochemical signal integration system subserving synaptic plasticity and memory. Journal of Neurochemistry 76 (2001) 1-10
65. Valjent E., Pages C., Herve D., Girault J.A., and Caboche J. Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain. European Journal of Neuroscience 19 (2004) 1826-1836
66. Wang J., Chen Y.B., Zhu X.N., and Chen R.Z. Activation of p42/44 mitogen-activated protein kinase pathway in long-term potentiation induced by nicotine in hippocampal CA1 region in rats. Acta Pharmacologia Sinica 22 (2001) 685-690
67. Wehner J.M., Keller J.J., Keller A.B., Picciotto M.R., Paylor R., Booker T.K., et al. Role of neuronal nicotinic receptors in the effects of nicotine and ethanol on contextual fear conditioning. Neuroscience 129 (2004) 11-24
68. Winder D.G., Martin K.C., Muzzio I.A., Rohrer D., Chruscinski A., Kobilka B., and Kandel E.R. ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24 (1999) 715-726
69. Wood M.A., Kaplan M.P., Park A., Blanchard E.J., Oliveira A.M., Lombardi T.L., and Abel T. Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learning & Memory 12 (2005) 111-119
70. Yamazaki Y., Jia Y., Niu R., and Sumikawa K. Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus. European Journal of Neuroscience 23 (2006) 1819-1828