Extracellular signal-regulated kinase signaling in the ventral tegmental area mediates cocaine-induced synaptic plasticity and rewarding effects

Journal of Neuroscience

Volumn 31, Issue 31, 2011, Pages 11244-11255

  Pan, Bin ^a   Zhong, Peng ^a   Sun, Dalong ^a   Liu, Qing song ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COCAINE DEPENDENCE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG DEPENDENCE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GABAERGIC SYSTEM; IN VIVO STUDY; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REWARD; SYNAPTIC INHIBITION; TRAINING; VENTRAL TEGMENTUM;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BENZOXAZINES; BIOPHYSICS; CALCIUM CHANNEL BLOCKERS; COCAINE; CONDITIONING, OPERANT; DOPAMINE UPTAKE INHIBITORS; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GABA ANTAGONISTS; MALE; MORPHOLINES; NAPHTHALENES; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PICROTOXIN; PIPERIDINES; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; REWARD; SIGNAL TRANSDUCTION; SYNAPSES; VENTRAL TEGMENTAL AREA;

EID: 79961216486     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1040-11.2011     Document Type: Article

References (77)

1. Argilli E, Sibley DR, Malenka RC, England PM, Bonci A (2008) Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area. J Neurosci 28:9092-9100
2. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609
3. Berhow MT, Hiroi N, Nestler EJ (1996) Regulation of ERK (extracellular signal-regulated kinase), part of the neurotrophin signal transduction cascade, in the rat mesolimbic dopamine system by chronic exposure to morphine or cocaine. J Neurosci 16:4707-4715
4. Bolshakov VY, Carboni L, Cobb MH, Siegelbaum SA, Belardetti F (2000) Dual MAP kinase pathways mediate opposing forms of long-term plasticity at CA3-CA1 synapses. Nat Neurosci 3:1107-1112
5. Bouaboula M, Poinot-Chazel C, Bourrieacute; B, Canat X, Calandra B, Rinaldi-Carmona M, Le Fur G, Casellas P (1995) Activation of mitogenactivated protein kinases by stimulation of the central cannabinoid receptor CB1. Biochem J 312:637-641
6. Brami-Cherrier K, Valjent E, Garcia M, Pages C, Hipskind RA, Caboche J. (2002) Dopamine induces a PI3-kinase-independent activation of Akt in striatal neurons: a new route to cAMP response element-binding protein phosphorylation. J Neurosci 22:8911-8921
7. Chevaleyre V, Castillo PE (2003) Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38:461-472
8. Chevaleyre V, Castillo PE (2004) Endocannabinoid-mediated metaplasticity in the hippocampus. Neuron 43:871-881
9. Chevaleyre V, Heifets BD, Kaeser PS, Südhof TC, Purpura DP, Castillo PE (2007) Endocannabinoid-mediated long-term plasticity requires cAMP/ PKA signaling and RIM1alpha. Neuron 54:801-812
10. Chiu CQ, Puente N, Grandes P, Castillo PE (2010) Dopaminergic modulation of endocannabinoid-mediated plasticity at GABAergic synapses in the prefrontal cortex. J Neurosci 30:7236-7248
11. Corbillé AG, Valjent E, Marsicano G, Ledent C, Lutz B, Hervé D, Girault JA (2007) Role of cannabinoid type 1 receptors in locomotor activity and striatal signaling in response to psychostimulants. J Neurosci 27:6937-6947
12. Davis MI, Ronesi J, Lovinger DM (2003) A predominant role for inhibition of the adenylate cyclase/protein kinase A pathway in ERK activation by cannabinoid receptor 1 in N1E-115 neuroblastoma cells. J Biol Chem 278:48973-48980
13. Derkinderen P, Ledent C, Parmentier M, Girault JA (2001) Cannabinoids activate p38 mitogen-activated protein kinases through CB1 receptors in hippocampus. J Neurochem 77:957-960
14. Derkinderen P, Valjent E, Toutant M, Corvol JC, Enslen H, Ledent C, Trzaskos J, Caboche J, Girault JA (2003) Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J Neurosci 23:2371-2382
15. English JD, Sweatt JD (1996) Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J Biol Chem 271:24329-24332
16. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106
17. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, Feeser WS, Van Dyk DE, Pitts WJ, Earl RA, Hobbs F, Copeland RA, Magolda RL, Scherle PA, Trzaskos JM (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273:18623-18632
18. Gallagher SM, Daly CA, Bear MF, Huber KM (2004) Extracellular signalregulated protein kinase activation is required for metabotropic glutamate receptor-dependent long-term depression in hippocampal area CA1. J Neurosci 24:4859-4864
19. Gerdeman GL, Ronesi J, Lovinger DM (2002) Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5:446-451
20. Gerdeman GL, Partridge JG, Lupica CR, Lovinger DM (2003) It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci 26:184-192
21. Girault JA, Valjent E, Caboche J, Hervé D (2007) ERK2: a logical AND gate critical for drug-induced plasticity? Curr Opin Pharmacol 7:77-85
22. Grueter BA, Gosnell HB, Olsen CM, Schramm-Sapyta NL, Nekrasova T, Landreth GE, Winder DG (2006) Extracellular-signal regulated kinase 1-dependent metabotropic glutamate receptor 5-induced long-term depression in the bed nucleus of the stria terminalis is disrupted by cocaine administration. J Neurosci 26:3210-3219
23. Heifets BD, Castillo PE (2009) Endocannabinoid signaling and long-term synaptic plasticity. Annu Rev Physiol 71:283-306
24. Howlett AC (2005) Cannabinoid receptor signaling. Handb Exp Pharmacol 2005:53-79
25. Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98:739-755
26. Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565-598
27. Jiang W, Zhang Y, Xiao L, Van Cleemput J, Ji SP, Bai G, Zhang X (2005) Cannabinoids promote embryonic and adult hippocampus neurogenesis and produce anxiolytic-and antidepressant-like effects. J Clin Invest 115:3104-3116
28. Johnson SW, North RA (1992) Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450:455-468
29. Jones S, Kauer JA (1999) Amphetamine depresses excitatory synaptic transmission via serotonin receptors in the ventral tegmental area. J Neurosci 19:9780-9787
30. Kalivas PW, Churchill L, Klitenick MA (1993) GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neuroscience 57:1047-1060
31. Katona I, Sperlagh B, Sík A, Kafalvi A, Vizi ES, Mackie K, Freund TF. (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544-4558
32. Kauer JA (2004) Learning mechanisms in addiction: synaptic plasticity in the ventral tegmental area as a result of exposure to drugs of abuse. Annu Rev Physiol 66:447-475
33. Kelleher RJ 3rd, Govindarajan A, Jung HY, Kang H, Tonegawa S (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467-479
34. Kellogg R, Mackie K, Straiker A (2009) Cannabinoid CB1 receptordependent long-term depression in autaptic excitatory neurons. J Neurophysiol 102:1160-1171
35. Lammel S, Hetzel A, Hackel O, Jones I, Liss B, Roeper J (2008) Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57:760-773
36. Liu QS, Pu L, Poo, MM (2005) Repeated cocaine exposure in vivo facilitates LTP induction in midbrain dopamine neurons. Nature 437:1027-1031
37. 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
38. Lu L, Hope BT, Dempsey J, Liu SY, Bossert JM, Shaham Y (2005) Central amygdala ERK signaling pathway is critical to incubation of cocaine craving. Nat Neurosci 8:212-219
39. Lu L, Koya E, Zhai H, Hope BT, Shaham Y (2006) Role of ERK in cocaine addiction. Trends Neurosci 29:695-703
40. Lu L, Wang X, Wu P, Xu C, Zhao M, Morales M, Harvey BK, Hoffer BJ, Shaham Y (2009) Role of ventral tegmental area glial cell line-derived neurotrophic factor in incubation of cocaine craving. Biol Psychiatry 66:137-145
41. Lupica CR, Riegel AC (2005) Endocannabinoid release from midbrain dopamine neurons: a potential substrate for cannabinoid receptor antagonist treatment of addiction. Neuropharmacology 48:1105-1116
42. Luu P, Malenka RC (2008) Spike timing-dependent long-term potentiation in ventral tegmental area dopamine cells requires PKC. J Neurophysiol 100:533-538
43. Margolis EB, Lock H, Hjelmstad GO, Fields HL (2006) The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? J Physiol 577:907-924
44. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534
45. Mato S, Lafourcade M, Robbe D, Bakiri Y, Manzoni OJ (2008) Role of the cyclic-AMP/PKA cascade and of P/Q-type Ca channels in endocannabinoid-mediated long-term depression in the nucleus accumbens. Neuropharmacology 54:87-94
46. Matsumoto M, Hikosaka O (2009) Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459:837-841
47. Matyas F, Urban GM, Watanabe M, Mackie K, Zimmer A, Freund TF, Katona I (2008) Identification of the sites of 2-arachidonoylglycerol synthesis and action imply retrograde endocannabinoid signaling at both GABAergic and glutamatergic synapses in the ventral tegmental area. Neuropharmacology 54:95-107
48. Miller CA, Marshall JF (2005) Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron 47:873-884
49. Nakielny S, Cohen P, Wu J, Sturgill T (1992) MAP kinase activator from insulin-stimulated skeletal muscle is a protein threonine/tyrosine kinase. EMBO J 11:2123-2129
50. Neve KA, Seamans JK, Trantham-Davidson H (2004) Dopamine receptor signaling. J Recept Signal Transduct Res 24:165-205
51. Orio L, Edwards S, George O, Parsons LH, Koob GF (2009) A role for the endocannabinoid system in the increased motivation for cocaine in extended-access conditions. J Neurosci 29:4846-4857
52. Pan B, Hillard CJ, Liu QS (2008a) Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J Neurosci 28:1385-1397
53. Pan B, Hillard CJ, Liu QS (2008b) D2 dopamine receptor activation facilitates endocannabinoid-mediated long-term synaptic depression of GABAergic synaptic transmission in midbrain dopamine neurons via cAMP-protein kinase A signaling. J Neurosci 28:14018-14030
54. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. New York: Academic. Pierce RC, Pierce-Bancroft AF, Prasad BM (1999) Neurotrophin-3 contributes to the initiation of behavioral sensitization to cocaine by activating the Ras/mitogen-activated protein kinase signal transduction cascade. J Neurosci 19:8685-8695
55. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ (2002) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci U S A 99:8384-8388
56. Roberson ED, English JD, Adams JP, Selcher JC, Kondratick C, Sweatt JD (1999) The mitogen-activated protein kinase cascade couples PKA and PKC to cAMP response element binding protein phosphorylation in area CA1 of hippocampus. J Neurosci 19:4337-4348
57. Ronesi J, Lovinger DM (2005) Induction of striatal long-term synaptic depression by moderate frequency activation of cortical afferents in rat. J Physiol 562:245-256
58. Ronesi J, Gerdeman GL, Lovinger DM (2004) Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J Neurosci 24:1673-1679
59. Rush AM, Wu J, Rowan MJ, Anwyl R (2002) Group I metabotropic glutamate receptor (mGluR)-dependent long-term depression mediated via p38 mitogen-activated protein kinase is inhibited by previous highfrequency stimulation and activation of mGluRs and protein kinase C in the rat dentate gyrus in vitro. J Neurosci 22:6121-6128
60. Rutkowska M (2004) The effect of AM 251, a cannabinoid CB1 receptor antagonist, on food intake in rats. Acta Pol Pharm 61:401-403
61. Stork PJ, Schmitt JM (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12:258-266
62. Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311-317
63. Thiemann G, Di Marzo V, Molleman A, Hasenohrl RU. (2008) The CB1 cannabinoid receptor antagonist AM251 attenuates amphetamine-induced behavioural sensitization while causingmonoaminechanges in nucleus accumbens and hippocampus. Pharmacol Biochem Behav 89:384-391
64. Tsou K, Mackie K, Sañudo-Peña MC, Walker JM (1999) Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience 93:969-975
65. Ungless MA, Magill PJ, Bolam JP (2004) Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303:2040-2042
66. Valjent E, Corvol JC, Pages C, Besson MJ, Maldonado R, Caboche J (2000) Involvement of the extracellular signal-regulated kinase cascade for cocaine-rewarding properties. J Neurosci 20:8701-8709
67. Valjent E, Pages C, Herve D, Girault JA, Caboche J (2004) Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain. Eur J Neurosci 19:1826-1836
68. Valjent E, Pascoli V, Svenningsson P, Paul S, Enslen H, Corvol JC, Stipanovich A, Caboche J, Lombroso PJ, Nairn AC, Greengard P, Herve D, Girault JA (2005) Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci U S A 102:491-496
69. Valjent E, Aubier B, Corbillé AG, Brami-Cherrier K, Caboche J, Topilko P, Girault JA, Hervé D (2006) Plasticity-associated gene Krox24/Zif268 is required for long-lasting behavioral effects of cocaine. J Neurosci 26:4956-4960
70. Wartmann M, Campbell D, Subramanian A, Burstein SH, Davis RJ (1995) The MAP kinase signal transduction pathway is activated by the endogenous cannabinoid anandamide. FEBS Lett 359:133-136
71. Wiskerke J, Pattij T, Schoffelmeer AN, De Vries TJ (2008) The role of CB1 receptors in psychostimulant addiction. Addict Biol 13:225-238
72. Xi ZX, Gilbert JG, Peng XQ, Pak AC, Li X, Gardner EL (2006) Cannabinoid CB1 receptor antagonist AM251 inhibits cocaine-primed relapse in rats: role of glutamate in the nucleus accumbens. J Neurosci 26:8531-8536
73. Xia Y, Driscoll JR, Wilbrecht L, Margolis EB, Fields HL, Hjelmstad GO (2011) Nucleus accumbens medium spiny neurons target non-dopaminergic neurons in the ventral tegmental area. J Neurosci 31:7811-7816
74. Yan Z, Feng J, Fienberg AA, Greengard P (1999) D2 dopamine receptors induce mitogen-activated protein kinase and cAMP response elementbinding protein phosphorylation in neurons. Proc Natl Acad Sci U S A 96:11607-11612
75. Yin HH, Davis MI, Ronesi JA, Lovinger DM (2006) The role of protein synthesis in striatal long-term depression. J Neurosci 26:11811-11820
76. Zhang TA, Placzek AN, Dani JA (2010) In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area. Neuropharmacology 59:431-436
77. Zhu PJ, Lovinger DM (2007) Persistent synaptic activity produces longlasting enhancement of endocannabinoid modulation and alters longterm synaptic plasticity. J Neurophysiol 97:4386-4389.