CREB involvement in the regulation of striatal prodynorphin by nicotine

Psychopharmacology

Volumn 221, Issue 1, 2012, Pages 143-153

  McCarthy, Michael J ^a   Duchemin, Anne Marie ^a   Neff, Norton H ^a   Hadjiconstantinou, Maria ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Dopamine D1 receptors; DynCRE3; Dynorphin; Nicotine; pCREB; Prodynorphin; Prodynorphin gene transcription; Striatum

Indexed keywords

8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; ADENYLATE CYCLASE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOPAMINE 1 RECEPTOR; DYNORPHIN; MECAMYLAMINE; MESSENGER RNA; NICOTINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; GEL MOBILITY SHIFT ASSAY; GENE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PRODYNORPHIN GENE; PROMOTER REGION; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

ADENYLATE CYCLASE; ANIMALS; BENZAZEPINES; CORPUS STRIATUM; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DYNORPHINS; ENKEPHALINS; MALE; MECAMYLAMINE; MICE; NICOTINE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PRECURSORS; RESPONSE ELEMENTS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84859635817     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-011-2559-y     Document Type: Article

References (73)

1. Anderson M, Konradi C, Cenci MA (2001) cAMP response elementbinding protein is required for dopamine-dependent gene expression in the intact but not the dopamine-denervated striatum. J Neurosci 15:9930-9943 (Pubitemid 34184077)
2. Angulo JA, McEwen BS (1994) Molecular aspects of neuropeptide regulation and function in the corpus striatum and nucleus accumbens. Brain Res Rev 19:1-28 (Pubitemid 24024082)
3. Bals-Kubik R, Herz A, Shippenberg TS (1989) Evidence that the aversive effects of opioid antagonists and agonists are centrally mediated. Psychopharmacology 98:203-206 (Pubitemid 19137732)
4. Bals-Kubik R, Ableitner A, Herz A, Shippenberg TS (1993) Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J Pharmacol Exp Ther 264:489-495 (Pubitemid 23309241)
5. Beninger RJ, Miller R (1998) Dopamine D1-like receptors and rewardrelated incentive learning. Neurosci Behav Rev 22:335-345 (Pubitemid 28194390)
6. Brami-Cherrier K, Valjent E, Hervé D, Darragh J, Corvol J-C, Pages C, Simon AJ, Girault J-A, Caboche J (2005) Parsing the molecular and behavioral effects of cocaine inmitogen- and stress-activated protein kinase-1-deficient mice. J Neurosci 25:11444-11454 (Pubitemid 43083716)
7. Bruijnzeel AW (2009) Kappa-opioid receptor signaling and brain reward function. Brain Res Rev 62:127-146
8. Brunzell DH, Russell DS, Picciotto MR (2003) In vivo nicotine treatment regulates mesocorticolimbic CREB and ERK signaling in C57B1/6J mice. J Neurochem 84:1431-1441 (Pubitemid 36343609)
9. Brunzell DH, Mineur YS, Neve RL, Picciotto MR (2009) Nucleus accumbens CREB activity is necessary for nicotine conditioned place preference. Neuropsychopharmacology 34:1993-2001
10. Carlezon WA Jr, Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N, Duman RS, Neve RL, Nestler EJ (1998) Regulation of cocaine reward by CREB. Science 282:2272-2275 (Pubitemid 29004079)
11. Carlezon WA Jr, Duman RS, Nestler EJ (2005) The many faces of CREB. Trends Neurosci 28:436-445 (Pubitemid 40982557)
12. Carlezon WA Jr, Begiun C, DiNieri JA, Bauman MH, Richards MR, Todtenkopf MS, Rothman RB, Ma Z, Lee DY, Cohen BM (2006) Depressive-like effects of the kappa-opioid receptor agonist salvinorin A on behavior and neurochemistry in rats. J Pharmacol Exp Ther 316:440-447 (Pubitemid 41832624)
13. Carrión AM, Mellström B, Luckman SM, Naranjo JR (1998) Stimulus-specific hierarchy of enhancer elements within the rat prodynorphin promoter. J Neurochem 70:914-921 (Pubitemid 28113623)
14. Cole DG, Kobierski LA, Konradi C, Hyman SE (1994) 6- Hydroxydopamine lesions of rat substantia nigra up-regulate dopamine-induced phosphorylation of the cAMP-response element binding protein in striatal neurons. Proc Natl Acad Sci USA 91:9631-9635
15. Cole RL, Konradi C, Douglass J, Hyman SE (1995) Neuronal adaptation to amphetamine and dopamine: molecular mechanisms of prodynorphin gene regulation in rat striatum. Neuron 14:813-823
16. Collins-Hicok J, Lin L, Spiro G, Laybourn PJ, Tschumper R, Rapacz B, McMurray CT (1994) Induction of the rat prodynorphin gene through Gs-coupled receptors may involve phosphorylationdependent derepression and activation. Mol Cell Biol 14:2837-2848
17. Dinieri JA, Nemeth CL, Parsegian A, Carle T, Gurevich VV, Gurevich E, Neve RL, Nestler EJ, Carlezon WA Jr (2009) Altered sensitivity to rewarding and aversive drugs in mice with inducible disruption of cAMP response element-binding protein function within the nucleus accumbens. J Neurosci 29:1855-1859
18. Douglass J, McKinzie AA, Pollock KM (1994) Identification of multiple DNA elements regulating basal and protein kinase Ainduced transcriptional expression of the rat prodynorphin gene. Mol Endocrinol 8:333-344 (Pubitemid 24108361)
19. Duchemin AM, Zhang H, Neff NH, Hadjiconstantinou M (2009) Increased expression of VMAT2 in dopaminergic neurons during nicotine withdrawal. Neurosci Lett 467:182-186
20. Fasano S, Brambilla R (2002) Cellular mechanisms of striatumdependent behavioral plasticity and drug addiction. Curr Mol Med 2:649-665 (Pubitemid 35256296)
21. Foulds J, Stapelton JA, Bell N, Swettenham J, Jarvis MJ, Russell MAH (1997) Mood and physiological effects of subcutaneous nicotine in smokers and never smokers. Drug Alcohol Depend 44:105-115 (Pubitemid 27129503)
22. Fudala PJ, Teoh KW, Iwamoto ET (1985) Pharmacologic characterization of nicotine-induced conditioned place preference. Pharmacol Biochem Behav 22:237-241 (Pubitemid 15132106)
23. Gerfen CR, Surmeier DJ (2011) Modulation of striatal projection systems by dopamine. Annu Rev Neurosci 34:441-466. doi:10.1146/annurev-neuro-061010- 113641
24. Gommans J, Stolerman IP, Shoaib M (2000) Antagonism of the discriminative and aversive stimulus properties of nicotine in C57BL/6j mice. Neuropharmacology 39:2840-2847
25. Hagiwara M, Brindle P, Harootunian A, Armstrong R, Rivier J, Vale W, Tsien R, Montminy MR (1993) Coupling of hormonal stimulation and transcription via cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol Cell Biol 13:4852-4859 (Pubitemid 23220391)
26. Heisman SJ, Henningfiled JF (2000) Tolerance to repeated nicotine administration on performance, subjective, and physiological responses in nonsmokers. Psychopharmacology 152:321-333
27. Iadarola MJ, Messersmith DJ (1994) Molecular biology of dynorphin gene expression in relationship to spinal cord processing of pain. In: Urban L (ed) The cellular mechanisms of sensory processing. Springer, Berlin, pp 313-336
28. i βγ subunits in nucleus accumbens/ventral tegmental cocultures: the role of dopamine D1/D2 and adenosine A receptors. J Pharmacol Exp Ther 322:23-29
29. Isola R, Zhang H, Tejwani GA, Neff NH, Hadjiconstantinou M (2009) Acute nicotine changes dynorphin and prodynorphin mRNA in the striatum. Psychopharmacology 201:507-516
30. Izenwasser S, Buzas B, CoxBM(1993) Differential regulation of adenylyl cyclase activity by mu and delta opioids in rat caudate-putamen and nucleus accumbens. J Pharmacol Exp Ther 267:145-152 (Pubitemid 23325001)
31. Jackson KJ, Walters CL, Damaj MI (2009) β2 subunit-containing nicotinic receptors mediate acute nicotine-induced activation of calcium/calmodulin-dependent protein kinase II-dependent pathways in vivo. J Pharmacol Exp Ther 330:541-549
32. Kiba H, Jayaraman A (1994) Nicotine induced c-fos expression in the striatum is mediated mostly by dopamine D1 receptor and is dependent on NMDA stimulation. Mol Brain Res 23:1-13 (Pubitemid 24090976)
33. Kivinummi T, Kaste K, Rantamäki T, Castrén E, Ahtee L (2011) Alterations in BDNF and phospho-CREB levels following chronic oral nicotine treatment and its withdrawal in dopaminergic brain areas of mice. Neurosci Lett 491:108-112
34. Konradi C, Heckers S (1995) Haloperidol-induced Fos expression in striatum is dependent upon transcription factor cyclic AMP response element binding protein. Neuroscience 65:1051-1061
35. Livingstone PD, Wonnacott S (2009) Nicotinic acetylcholine receptors and the ascending dopamine pathways. Biochem Pharmacol 78:744-755
36. Mayr B, Montminy M (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2:599-609 (Pubitemid 33674011)
37. McCarthy MJ, Zhang H, Neff NH, Hadjiconstantinou M (2010) Nicotine withdrawal and κ-opioid receptors. Psychopharmacology 210:221-229
38. McGinty JF, Shi XD, Schwendt M, Saylor A, Toda S (2008) Regulation of psychostimulant-induced signaling and gene expression in the striatum. J Neurochem 104:1440-1449 (Pubitemid 351316778)
39. McPherson CS, Lawrence AJ (2007) The nuclear transcription factor CREB: involvement in addiction, deletion models and looking forward. Curr Neuropharmacol 5:202-212 (Pubitemid 351863862)
40. Messersmith DJ, Gu J, Dubner R, Douglass J, Iadarola MJ (1994) Basal and inducible transcriptional activity of an upstream AP-1/ CRE element (DYNCRE3) in the prodynorphin promoter. Mol Cell Neurosci 5:238-245 (Pubitemid 24172506)
41. Messersmith DJ, Kim DJ, Gu R, Dubner R, Iadarola MJ (1996) c-Jun activation of the DYNCRE3 site in the prodynorphin promoter. Mol Brain Res 40:15-21 (Pubitemid 26241781)
42. Messersmith DJ, Kim DJ, Iadarola MJ (1998) Transcription factor regulation of prodynorphin gene expression following rat hind paw inflammation. Mol Brain Res 53:259-269 (Pubitemid 28085461)
43. Moratalla R, Xu M, Tonegawa S, Graybiel AM (1996) Cellular responses to psychomotor stimulant and neuroleptic drugs are abnormal in mice lacking the D1 dopamine receptor. Proc Natl Acad Sci USA 93:14928-14933 (Pubitemid 26419072)
44. Mucha RF, Hertz A (1985) Motivational properties of κ- and μ-opioid receptor agonists studied with place and taste preference conditioning procedure. Psychopharmacology 86:274-280 (Pubitemid 15064950)
45. Muschamp JW, Van't Veer A, Parsegian A, Gallo MS, Chen M, Neve RL, Meloni EG, Carlezon WA Jr (2011) Activation of CREB in the nucleus accumbens shell produces anhedonia and resistance to extinction of fear in rats. J Neurosci 31:3095-3103
46. Naranjo JR, Mellström B, Archaval M, Sassone-Corsi P (1991) Molecular pathways of pain: Fos/Jun-mediated activation of a noncanonical AP-1 site in the prodynorphin gene. Neuron 6:607-617
47. Nestler EJ (2004) Molecular mechanisms of drug addiction. Neuropharmacology 47:24-32
48. Newton SS, Thomas J, Wallase TL, Shirayama Y, Schlesinger L, Sakai N, Chen J, Neve RL, Nestler EJ, Duman RS (2002) Inhibition of cAMP response element-binding protein or dynorphin in the nucleus accumbens produces an antidepressant-like effect. J Neurosci 22:10883-10890 (Pubitemid 36005163)
49. Nisell M, Nomikos GG, Chergiu K, Grillner P, Svensson TH (1997) Chronic nicotine enhances basal and nicotine-induced Fos immunoreactivity preferentially in the medial prefrontal cortex of the rat. Neuropsychopharmacology 17:151-161 (Pubitemid 27365956)
50. Panagis G, Nissel M, Nomikos GG, Chergui K, Svensson TH (1996) Nicotine injections into the ventral tegmental area increase locomotion and Fos-like immunoreactivity in the nucleus accumbens of the rat. Brain Res 730:133-142 (Pubitemid 26305333)
51. Pandey SC (2004) The gene transcription factor cyclic AMPresponsive element binding protein: role in positive and negative affective states of alcohol addiction. Pharmacol Ther 104:47-58
52. Pandey SC, Roy A, Xu T, Mittal N (2001) Effects of protracted nicotine exposure and withdrawal on the expression and phosphorylation of the CREB gene transcription factor in rat brain. J Neurochem 77:943-952 (Pubitemid 32466791)
53. Pascual MM, Pastor V, Bernabeu RO (2009) Nicotine-conditioned place preference induced CREB phosphorylation and Fos expression in the adult rat brain. Psychopharmacology 207:57-71
54. Pescatore KA, Glowa JR, Riley AL (2005) Strain differences in the acquisition of nicotine-induced conditioned taste aversion. Pharmacol Biochem Behav 82:751-757 (Pubitemid 43184054)
55. Pfeiffer A, Brandl V, Herz A, Emrich HM (1986) Psychomimesis mediated by kappa opiate receptors. Science 223:774-776 (Pubitemid 16016229)
56. Pliakas AM, Carlsson RR, Neve RL, Konradi C, Nestler EJ, Carlezon WA Jr (2001) Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens. J Neurosci 21:7397-7403 (Pubitemid 32846987)
57. Pluzarev O, Pandey SC (2004) Modulation of CREB expression and phosphorylation in the rat nucleus accumbens during nicotine exposure and withdrawal. J Neurosci Res 77:884-891 (Pubitemid 39187071)
58. Pozzi L, Hakansson K, Usiello A, Borgkvist A, Lindskog M, Greengard P, Fisone G (2003) Opposite regulation of typical and atypical antipsychotics of ERK1/2, CREB and Elk-1 phosphorylation in mouse dorsal striatum. J Neurochem 86:451-459 (Pubitemid 36842444)
59. Rissinger FO, Oakes RA (1995) Nicotine-induced conditioned place preference and conditioned place aversion in mice. Pharmacol Biochem Behav 51:457-461
60. Salminen O, Seppä T, Gäddnäs H, Ahtee L (1999) The effects of acute nicotine on the metabolism of dopamine and the expression of Fos protein in striatal and limbic brain areas of rats during chronic nicotine infusion and its withdrawal. J Neurosci 19:8145-8151 (Pubitemid 30225810)
61. Shaywitz AJ, Greenberg ME (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68:821-861 (Pubitemid 29449210)
62. Shoaib M, Gommans J, Morley A, Stolerman IP, Graillhe R, Changeux JP (2002) The role of nicotine receptor beta-2 subunit in nicotine discrimination and conditioned taste aversion. Neuropharmacology 42:530-539 (Pubitemid 34304245)
63. Simpson JN, McGinty JF (1994) Forskolin increases phosphorylated- CREB and fos immunoreactivity in rat striatum. NeuroReport 10:1213-1216 (Pubitemid 24199798)
64. Simpson JN, McGinty JF (1995) Forskolin induces preproenkephalin and preprodynorphin mRNA in rat striatum by in situ hybridization histochemistry. Synapse 19:151-159
65. Steiner H, Gerfen CR (1998) Role of dynorphin and enkephalin in the regulation of striatal output pathways and behavior. Exp Brain Res 123:60-76 (Pubitemid 28495297)
66. Sun W-L, Zhou L, Hazim R, Quinones-Jenab V, Jenab S (2007) Effects of acute nicotine on Erk and DARPP-32 phosphorylation pathways in the caudate-putamen of Fischer rats. Brain Res 178:12-19 (Pubitemid 47625354)
67. Todtenkopf MS, Marcus JF, Portoghese PS, Carlezon WA Jr (2004) Effects of kappa-opioid receptor ligands on intracranial selfstimulation in rats. Psychopharmacology 172:463-470 (Pubitemid 38650984)
68. Walters CL, Blendy JA (2001) Different requirement for cAMP response element binding protein in positive and negative reinforcing properties of drugs of abuse. J Neurosci 21:9438-9444 (Pubitemid 33096887)
69. Walters CL, Cleck JN, Kuo Y-C, Blendy JA (2005) μ-Opioid receptor and CREB activation are required for nicotine reward. Neuron 46:933-943 (Pubitemid 40805353)
70. Wee S, Koob GF (2010) The role of the dynorphin-κ opioid system in the reinforcing effects of drugs of abuse. Psychopharmacology 210:121-135
71. Wickens JR, Budd CS, Hyland BI, Arbuthnott GW (2007) Striatal contributions to reward and decision making: making sense of regional variations in a reiterated processing matrix. Ann NY Acad Sci 1104:192-212 (Pubitemid 47092742)
72. Xu M, Moratalla R, Gold LH, Hiro N, Coob GF, Graybiel AM, Tonegawa S (1994) Dopamine D1 receptor mutant mice are deficient in striatal expression of dynorphin and in dopaminemediated behavioral responses. Cell 79:729-742 (Pubitemid 24363815)
73. Zhang L, Lou D, Jiao H, Zhang D, Wang X, Xia Y, Zhang J, Xu M (2004) Cocaine-induced intracellular signaling and gene expression are oppositely regulated by the dopamine D1 and D3 receptors. J Neurosci 24:3344-3354 (Pubitemid 38451900)