Type 1 equilibrative nucleoside transporter regulates ethanol drinking through accumbal N-methyl-D-aspartate receptor signaling

Biological Psychiatry

Volumn 69, Issue 11, 2011, Pages 1043-1051

  Nam, Hyung Wook ^a   Lee, Moonnoh R ^a   Zhu, Yu ^a   Wu, Jinhua ^a   Hinton, David J ^a   Choi, Sun ^a   Kim, Taehyun ^a   Hammack, Nora ^a   Yin, Jerry C P ^c   Choi, Doo Sup ^a,b  

^a MAYO GRADUATE SCHOOL   (United States)

^b Mayo Clinic College of Medicine   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Alcoholism; CGP37849; CREB; ENT1; NMDA glutamate receptor; nucleus accumbens

Indexed keywords

BETA GALACTOSIDASE; CALCIUM; CALMODULIN; CYCLIC AMP; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROGRANIN; PROTEIN KINASE C GAMMA; PROTEIN KINASE TYK2;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE DELETION; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

2-AMINO-5-PHOSPHONOVALERATE; ALCOHOL DRINKING; ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER 1; ETHANOL; EXCITATORY AMINO ACID ANTAGONISTS; GLUTAMIC ACID; MALE; MICE; MICE, KNOCKOUT; MICRODIALYSIS; NUCLEUS ACCUMBENS; PROTEIN KINASE C; RECEPTORS, N-METHYL-D-ASPARTATE; SELF ADMINISTRATION; SIGNAL TRANSDUCTION;

EID: 79955772672     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2011.02.013     Document Type: Article

References (60)

1. H.J. Harwood, D. Fountain, and G. Livermore Economic costs of alcohol abuse and alcoholism Recent Dev Alcohol 14 1998 307 330
2. A.H. Mokdad, J.S. Marks, D.F. Stroup, and J.L. Gerberding Actual causes of death in the United States JAMA 291 2000 1238 1245
3. L. Asatryan, H.W. Nam, M.R. Lee, M.M. Thakkar, M.S. Dar, and D.L. Davies Implication of the purinergic system in alcohol use disorders Alcohol Clin Exp Res 35 2011 584 594
4. T.V. Dunwiddie, and S.A. Masino The role and regulation of adenosine in the central nervous system Annu Rev Neurosci 24 2001 31 55 (Pubitemid 32695222)
5. B.B. Fredholm, J.F. Chen, S.A. Masino, and J.M. Vaugeois Actions of adenosine at its receptors in the CNS: Insights from knockouts and drugs Annu Rev Pharmacol Toxicol 45 2005 385 412 (Pubitemid 40261811)
6. S. Ferr, B.B. Fredholm, M. Morelli, P. Popoli, and K. Fuxe Adenosine-dopamine receptor-receptor interactions as an integrative mechanism in the basal ganglia Trends Neurosci 20 1997 482 487 (Pubitemid 27421712)
7. L.E. Nagy, I. Diamond, D.J. Casso, C. Franklin, and A.S. Gordon Ethanol increases extracellular adenosine by inhibiting adenosine uptake via the nucleoside transporter J Biol Chem 265 1990 1946 1951
8. C.L. Ruby, C. Adams, E.J. Knight, H.W. Nam, and D.S. Choi An essential role for adenosine signaling in alcohol abuse Curr Drug Abuse Rev 3 2010 163 174
9. R.I. Melendez, and P.W. Kalivas Last call for adenosine transporters Nat Neurosci 7 2004 795 796 (Pubitemid 38989498)
10. D.S. Choi, M.G. Cascini, W. Mailliard, H. Young, P. Paredes, and T. McMahon The type 1 equilibrative nucleoside transporter regulates ethanol intoxication and preference Nat Neurosci 7 2004 855 861 (Pubitemid 38989509)
11. J. Chen, H.W. Nam, M.R. Lee, D.J. Hinton, S. Choi, and T. Kim Altered glutamatergic neurotransmission in the striatum regulates ethanol sensitivity and intake in mice lacking ENT1 Behav Brain Res 208 2010 636 642
12. F.E. Parkinson, W. Xiong, C.R. Zamzow, T. Chestley, T. Mizuno, and M.L. Duckworth Transgenic expression of human equilibrative nucleoside transporter 1 in mouse neurons J Neurochem 109 2009 562 572
13. J.L. Short, J. Drago, and A.J. Lawrence Comparison of ethanol preference and neurochemical measures of mesolimbic dopamine and adenosine systems across different strains of mice Alcohol Clin Exp Res 30 2006 606 620
14. R.L. Bell, M.W. Kimpel, J.N. McClintick, W.N. Strother, L.G. Carr, and T. Liang Gene expression changes in the nucleus accumbens of alcohol-preferring rats following chronic ethanol consumption Pharmacol Biochem Behav 94 2009 131 147
15. R. Sharma, S. Engemann, P. Sahota, and M.M. Thakkar Role of adenosine and wake-promoting basal forebrain in insomnia and associated sleep disruptions caused by ethanol dependence J Neurochem 115 2010 782 794
16. N. Gass, H.M. Ollila, S. Utge, T. Partonen, E. Kronholm, and S. Pirkola Contribution of adenosine related genes to the risk of depression with disturbed sleep J Affect Disord 126 2010 134 139
17. J-.H. Kim, V.M. Karpyak, J.M. Biernacka, H.W. Nam, and U. Preuss Functional role of the polymorphic 647 T/C variant of ENT1 (SLC29A1) and its association with alcohol withdrawal seizure PLoS ONE 6 2011 e16331
18. O. Levran, D. Londono, K. O'Hara, M. Randesi, J. Rotrosen, and P. Casadonte Heroin addiction in African Americans: A hypothesis-driven association study Genes Brain Behav 8 2009 531 540
19. J. Harvey, and M.G. Lacey A postsynaptic interaction between dopamine D1 and NMDA receptors promotes presynaptic inhibition in the rat nucleus accumbens via adenosine release J Neurosci 17 1997 5271 5280
20. J. Wu, M.R. Lee, S. Choi, T. Kim, and D.S. Choi ENT1 regulates ethanol-sensitive EAAT2 expression and function in astrocytes Alcohol Clin Exp Res 34 2010 1110 1117
21. M.R. Lee, D.J. Hinton, J. Wu, P.K. Mishra, J.D. Port, S.I. Macura, and D.S. Choi Acamprosate reduces ethanol drinking behaviors and alters the metabolite profile in mice lacking ENT1 Neurosci Lett 490 2011 90 95
22. J. Hu, J. Qian, O. Borisov, S. Pan, Y. Li, and T. Liu Optimized proteomic analysis of a mouse model of cerebellar dysfunction using amine-specific isobaric tags Proteomics 6 2006 4321 4334 (Pubitemid 44277034)
23. T. Liu, V. D'Mello, L. Deng, J. Hu, M. Ricardo, and S. Pan A multiplexed proteomics approach to differentiate neurite outgrowth patterns J Neurosci Methods 158 2006 22 29 (Pubitemid 44528758)
24. D.S. Choi, D. Wang, J. Dadgar, W.S. Chang, and R.O. Messing Conditional rescue of protein kinase C epsilon regulates ethanol preference and hypnotic sensitivity in adult mice J Neurosci 22 2002 9905 9911 (Pubitemid 35332875)
25. K.K. Szumlinski, K.D. Lominac, M.J. Kleschen, E.B. Oleson, M.H. Dehoff, and M.K. Schwarz Behavioral and neurochemical phenotyping of Homer1 mutant mice: Possible relevance to schizophrenia Genes Brain Behav 4 2005 273 288 (Pubitemid 41002403)
26. S.G. Amara, and A.C. Fontana Excitatory amino acid transporters: Keeping up with glutamate Neurochem Int 41 2002 313 318
27. F.A. Chaudhry, K.P. Lehre, M. van Lookeren Campagne, O.P. Ottersen, N.C. Danbolt, and J. Storm-Mathisen Glutamate transporters in glial plasma membranes: Highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry Neuron 15 1995 711 720
28. B.E. Lonze, and D.D. Ginty Function and regulation of CREB family transcription factors in the nervous system Neuron 35 2002 605 623 (Pubitemid 35229980)
29. M. Bantscheff, M. Boesche, D. Eberhard, T. Matthieson, G. Sweetman, and B. Kuster Robust and sensitive iTRAQ quantification on an LTQ Orbitrap mass spectrometer Mol Cell Proteomics 7 2008 1702 1713
30. C.L. Han, C.W. Chien, W.C. Chen, Y.R. Chen, C.P. Wu, H. Li, and Y.J. Chen A multiplexed quantitative strategy for membrane proteomics: Opportunities for mining therapeutic targets for autosomal dominant polycystic kidney disease Mol Cell Proteomics 7 2008 1983 1997
31. Z. Xia, and D.R. Storm The role of calmodulin as a signal integrator for synaptic plasticity Nat Rev Neurosci 6 2005 267 276 (Pubitemid 40469981)
32. A.M. Sanchez-Perez, and V. Felipo Serines 890 and 896 of the NMDA receptor subunit NR1 are differentially phosphorylated by protein kinase C isoforms Neurochem Int 47 2005 84 91 (Pubitemid 40848697)
33. C.W. Mahoney, K. Seki, and K.P. Huang Phosphorylation of MARCKS, neuromodulin, and neurogranin by protein kinase C exhibits differential responses to diacylglycerols Cell Signal 7 1995 679 685
34. D.D. Gerendasy, and J.G. Sutcliffe RC3/neurogranin, a postsynaptic calpacitin for setting the response threshold to calcium influxes Mol Neurobiol 15 1997 131 163 (Pubitemid 127719576)
35. J. Wu, K.P. Huang, and F.L. Huang Participation of NMDA-mediated phosphorylation and oxidation of neurogranin in the regulation of Ca2+- and Ca2+/calmodulin-dependent neuronal signaling in the hippocampus J Neurochem 86 2003 1524 1533 (Pubitemid 37174269)
36. I. Dominguez-Gonzalez, S.N. Vazquez-Cuesta, A. Algaba, and F.J. Diez-Guerra Neurogranin binds to phosphatidic acid and associates to cellular membranes Biochem J 404 2007 31 43 (Pubitemid 46788082)
37. K.P. Huang, F.L. Huang, T. Jager, J. Li, K.G. Reymann, and D. Balschun Neurogranin/RC3 enhances long-term potentiation and learning by promoting calcium-mediated signaling J Neurosci 24 2004 10660 10669 (Pubitemid 39557639)
38. T. Krucker, G.R. Siggins, R.K. McNamara, K.A. Lindsley, A. Dao, and D.W. Allison Targeted disruption of RC3 reveals a calmodulin-based mechanism for regulating metaplasticity in the hippocampus J Neurosci 22 2002 5525 5535 (Pubitemid 35386474)
39. M.B. Kennedy Signal transduction molecules at the glutamatergic postsynaptic membrane Brain Res Brain Res Rev 26 1998 243 257 (Pubitemid 28318080)
40. K. Seki, H.C. Chen, and K.P. Huang Dephosphorylation of protein kinase C substrates, neurogranin, neuromodulin, and MARCKS, by calcineurin and protein phosphatases 1 and 2A Arch Biochem Biophys 316 1995 673 679
41. G.Y. Wu, K. Deisseroth, and R.W. Tsien Activity-dependent CREB phosphorylation: Convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway Proc Natl Acad Sci U S A 98 2001 2808 2813 (Pubitemid 32209565)
42. C. Chen, M. Kano, A. Abeliovich, L. Chen, S. Bao, and J.J. Kim Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKC gamma mutant mice Cell 83 1995 1233 1242 (Pubitemid 26007813)
43. V. Vengeliene, D. Bachteler, W. Danysz, and R. Spanagel The role of the NMDA receptor in alcohol relapse: A pharmacological mapping study using the alcohol deprivation effect Neuropharmacology 48 2005 822 829 (Pubitemid 40489039)
44. K. Sato, A. Suematsu, T. Nakashima, S. Takemoto-Kimura, K. Aoki, and Y. Morishita Regulation of osteoclast differentiation and function by the CaMK-CREB pathway Nat Med 12 2006 1410 1416 (Pubitemid 44924500)
45. J.H. Krystal, I.L. Petrakis, G. Mason, L. Trevisan, and D.C. D'Souza N-methyl-D-aspartate glutamate receptors and alcoholism: Reward, dependence, treatment, and vulnerability Pharmacol Ther 99 2003 79 94 (Pubitemid 36694751)
46. B.J. Bowers, E.H. Owen, A.C. Collins, A. Abeliovich, S. Tonegawa, and J.M. Wehner Decreased ethanol sensitivity and tolerance development in gamma-protein kinase C null mutant mice is dependent on genetic background Alcohol Clin Exp Res 23 1999 387 397 (Pubitemid 29144829)
47. R.A. Harris, S.J. McQuilkin, R. Paylor, S. Tonegawa, and J.M. Wehner Mutant mice lacking the gamma isoform of protein kinase C show decreased behavioral actions of ethanol and altered function of gamma-aminobutyrate type A receptors Proc Natl Acad Sci U S A 92 1995 3658 3662
48. A. Represa, J.C. Deloulme, M. Sensenbrenner, Y. Ben-Ari, and J. Baudier Neurogranin: Immunocytochemical localization of a brain-specific protein kinase C substrate J Neurosci 10 1990 3782 3792
49. D.D. Gerendasy, S.R. Herron, P.A. Jennings, and J.G. Sutcliffe Calmodulin stabilizes an amphiphilic alpha-helix within RC3/neurogranin and GAP-43/neuromodulin only when Ca2+ is absent J Biol Chem 270 1995 6741 6750
50. A.M. Zhabotinsky, R.N. Camp, I.R. Epstein, and J.E. Lisman Role of the neurogranin concentrated in spines in the induction of long-term potentiation J Neurosci 26 2006 7337 7347 (Pubitemid 44315201)
51. C. Boucheron, S. Alfos, V. Enderlin, M. Husson, V. Pallet, R. Jaffard, and P. Higueret Age-related effects of ethanol consumption on triiodothyronine and retinoic acid nuclear receptors, neurogranin and neuromodulin expression levels in mouse brain Neurobiol Aging 27 2006 1326 1334 (Pubitemid 44067308)
52. A. Krazem, N. Mons, P. Higueret, and R. Jaffard Chronic ethanol consumption restores the age-related decrease in neurogranin mRNA level in the hippocampus of mice Neurosci Lett 338 2003 62 66 (Pubitemid 36136037)
53. M.R. Martzen, and J.R. Slemmon The dendritic peptide neurogranin can regulate a calmodulin-dependent target J Neurochem 64 1995 92 100
54. S.M. Anderson, K.R. Famous, G. Sadri-Vakili, V. Kumaresan, H.D. Schmidt, and C.E. Bass CaMKII: A biochemical bridge linking accumbens dopamine and glutamate systems in cocaine seeking Nat Neurosci 11 2008 344 353 (Pubitemid 351311801)
55. X.Y. Liu, L.M. Mao, G.C. Zhang, C.J. Papasian, E.E. Fibuch, and H.X. Lan Activity-dependent modulation of limbic dopamine D3 receptors by CaMKII Neuron 61 2009 425 438
56. F.A. Witzmann, J. Li, W.N. Strother, W.J. McBride, L. Hunter, and D.W. Crabb Innate differences in protein expression in the nucleus accumbens and hippocampus of inbred alcohol-preferring and -nonpreferring rats Proteomics 3 2003 1335 1344 (Pubitemid 36929556)
57. W.J. McBride, J.A. Schultz, M.W. Kimpel, J.N. McClintick, M. Wang, J. You, and Z.A. Rodd Differential effects of ethanol in the nucleus accumbens shell of alcohol-preferring (P), alcohol-non-preferring (NP) and Wistar rats: A proteomics study Pharmacol Biochem Behav 92 2009 304 313
58. R. Spanagel, and F. Kiefer Drugs for relapse prevention of alcoholism: Ten years of progress Trends Pharmacol Sci 29 2008 109 115
59. S.C. Pandey, A. Roy, H. Zhang, and T. Xu Partial deletion of the cAMP response element-binding protein gene promotes alcohol-drinking behaviors J Neurosci 24 2004 5022 5030 (Pubitemid 38697836)
60. B.J. Everitt, and T.W. Robbins Neural systems of reinforcement for drug addiction: From actions to habits to compulsion Nat Neurosci 8 2005 1481 1489 (Pubitemid 41573659)