Enhancement of alcohol drinking in mice depends on alterations in RNA editing of serotonin 2C receptors

International Journal of Neuropsychopharmacology

Volumn 17, Issue 5, 2014, Pages 739-751

  Watanabe, Yoshihisa ^a   Yoshimoto, Kanji ^b   Tatebe, Harutsugu ^b   Kita, Masakazu ^b   Nishikura, Kazuko ^c   Kimura, Minoru ^d   Tanaka, Masaki ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^c WISTAR INSTITUTE   (United States)

^d TAMAGAWA UNIVERSITY   (Japan)

Author keywords

Alcohol drinking; dorsal raphe nucleus; nucleus accumbens; RNA editing; serotonin 2C receptor

Indexed keywords

ADENOSINE; ADENOSINE DEAMINASE; ALCOHOL; G PROTEIN COUPLED RECEPTOR; INOSINE; MESSENGER RNA; SEROTONIN 2C RECEPTOR;

ALCOHOL CONSUMPTION; ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; DRINKING BEHAVIOR; FEMALE; LONG TERM EXPOSURE; MALE; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; REWARD; RNA EDITING; WILD TYPE; ANIMAL; C3H MOUSE; C57BL MOUSE; DBA MOUSE; GENETICS; IMMUNOBLOTTING; ISOMERISM; METABOLISM; RAPHE NUCLEUS; SPECIES DIFFERENCE;

ADENOSINE DEAMINASE; ALCOHOL DRINKING; ANIMALS; IMMUNOBLOTTING; ISOMERISM; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED DBA; NUCLEUS ACCUMBENS; RAPHE NUCLEI; RECEPTOR, SEROTONIN, 5-HT2C; RNA EDITING; RNA, MESSENGER; SPECIES SPECIFICITY;

EID: 84898059288     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145713001545     Document Type: Article

References (52)

1. Abramowski D, Rigo M, Duc D, Hoyer D, Staufenbiel M (1995) Localization of the 5-hydroxytryptamine2C receptor protein in human and rat brain using specific antisera. Neuropharmacol 34:1635-1645
2. Berg KA, Cropper JD, Niswender CM, Sanders-Bush E, Emeson RB, Clarke WP (2001) RNA-editing of the 5-HT(2C) receptor alters agonist-receptor-effector coupling specificity. Br J Pharmacol 134:386-392
3. Buckholtz NS, Zhou DF, Freedman DX (1988) Serotonin2 agonist administration down-regulates rat brain serotonin2 receptors. Life Sci 42:2439-2445
4. Buckland PR, D'Souza U, Maher NA, McGuffin P (1997) The effects of antipsychotic drugs on the mRNA levels of serotonin 5HT2A and 5HT2C receptors. Brain Res Mol Brain Res 48:45-52
5. Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H, Sanders-Bush E, Emeson RB (1997) Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387:303-308
6. Clemett DA, Punhani T, Duxon MS, Blackburn TP, Fone KC (2000) Immunohistochemical localisation of the 5-HT2C receptor protein in the rat CNS. Neuropharmacol 39:123-132
7. Crabbe JC (2002) Alcohol and genetics: New models. Am J Med Genet 114:969-974
8. De Deurwaerdere P, Spampinato U (1999) Role of serotonin(2A) and serotonin(2B/2C) receptor subtypes in the control of accumbal and striatal dopamine release elicited in vivo by dorsal raphe nucleus electrical stimulation. J Neurochem 73:1033-1042
9. De Deurwaerdere P, Navailles S, Berg KA, Clarke WP, Spampinato U (2004) Constitutive activity of the serotonin2C receptor inhibits in vivo dopamine release in the rat striatum and nucleus accumbens. J Neurosci 24:3235-3241
10. Du Y, Davisson MT, Kafadar K, Gardiner K (2006) A-To-I pre-mRNA editing of the serotonin 2C receptor: Comparisons among inbred mouse strains. Gene 382:39-46
11. Englander MT, Dulawa SC, Bhansali P, Schmauss C (2005) How stress and fluoxetine modulate serotonin 2C receptor pre-mRNA editing. J Neurosci 25:648-651
12. Fitzgerald LW, Iyer G, Conklin DS, Krause CM, Marshall A, Patterson JP, Tran DP, Jonak GJ, Hartig PR (1999) Messenger RNA editing of the human serotonin 5-HT2C receptor. Neuropsychopharmacol 21:82S-90S.
13. Flomen R, Knight J, Sham P, Kerwin R, Makoff A (2004) Evidence that RNA editing modulates splice site selection in the 5-HT2C receptor gene. Nucleic Acids Res 32:2113-2122
14. Giorgetti M, Tecott LH (2004) Contributions of 5-HT(2C) receptors to multiple actions of central serotonin systems. Eur J Pharmacol 488:1-9
15. Gurevich I, Englander MT, Adlersberg M, Siegal NB, Schmauss C (2002a) Modulation of serotonin 2C receptor editing by sustained changes in serotonergic neurotransmission. J Neurosci 22:10529-10532
16. Gurevich I, Tamir H, Arango V, Dwork AJ, Mann JJ, Schmauss C (2002b) Altered editing of serotonin 2C receptor pre-mRNA in the prefrontal cortex of depressed suicide victims. Neuron 34:349-356
17. Hackler EA, Airey DC, Shannon CC, Sodhi MS, Sanders-Bush E (2006) 5-HT(2C) receptor RNA editing in the amygdala of C57BL/6J, DBA/2J, and BALB/cJ mice. Neurosci Res 55:96-104
18. Hartner JC, Schmittwolf C, Kispert A, Muller AM, Higuchi M, Seeburg PH (2004) Liver disintegration in the mouse embryo caused by deficiency in the RNA-editing enzyme ADAR1. J Biol Chem 279:4894-4902
19. Herrick-Davis K, Grinde E, Niswender CM (1999) Serotonin 5-HT2C receptor RNA editing alters receptor basal activity: Implications for serotonergic signal transduction. J Neurochem 73:1711-1717
20. Iwamoto K, Bundo M, Kato T (2009) Serotonin receptor 2C and mental disorders: Genetic, expression and RNA editing studies. RNA Biol 6:248-253
21. Kapasova Z, Szumlinski KK (2008) Strain differences in alcohol-induced neurochemical plasticity: A role for accumbens glutamate in alcohol intake. Alcohol Clin Exp Res 32:617-631
22. Kawahara Y, Grimberg A, Teegarden S, Mombereau C, Liu S, Bale TL, Blendy JA, Nishikura K (2008) Dysregulated editing of serotonin 2C receptor mRNAs results in energy dissipation and loss of fat mass. J Neurosci 28:12834-12844
23. Koob GF, Sanna PP, Bloom FE (1998a) Neuroscience of addiction. Neuron 21:467-476
24. Koob GF, Roberts AJ, Schulteis G, Parsons LH, Heyser CJ, Hyytia P, Merlo-Pich E, Weiss F (1998b) Neurocircuitry targets in ethanol reward and dependence. Alcohol Clin Exp Res 22:3-9
25. Kwak S, Nishimoto Y, Yamashita T (2008) Newly identified ADAR-mediated A-To-I editing positions as a tool for ALS research. RNA Biol 5:193-197
26. Lumeng L, Murphy J, McBride W, Li T-K (1995) Genetic Influences on alcohol preference in animals. In: The genetics of alcoholism (Begleiter H, Kissin B, eds), pp 165-201. New York: Oxford University Press
27. Maas S, Kawahara Y, Tamburro KM, Nishikura K (2006) A-To-I RNA editing and human disease. RNA Biol 3:1-9
28. McClearn GE (1968) The use of strain rank orders in assessing equivalence of techniques. Behav Res Meth Instrum 1:49-51
29. McKenna DJ, Nazarali AJ, Himeno A, Saavedra JM (1989) Chronic treatment with (+/-)DOI, a psychotomimetic 5-HT2 agonist, downregulates 5-HT2 receptors in rat brain. Neuropsychopharmacol 2:81-87
30. Miyazaki KW, Miyazaki K, Doya K (2012) Activation of dorsal raphe serotonin neurons is necessary for waiting for delayed rewards. J Neurosci 32:10451-10457
31. Mombereau C, Kawahara Y, Gundersen BB, Nishikura K, Blendy JA (2010) Functional relevance of serotonin 2C receptor mRNA editing in antidepressant-And anxiety-like behaviours. Neuropharmacol 59:468-473
32. Muller CP, Huston JP (2006) Determining the region-specific contributions of 5-HT receptors to the psychostimulant effects of cocaine. Trends Pharmacol Sci 27:105-112
33. Navailles S, Moison D, Ryczko D, Spampinato U (2006) Region-dependent regulation of mesoaccumbens dopamine neurons in vivo by the constitutive activity of central serotonin2C receptors. J Neurochem 99:1311-1319
34. Navailles S, Moison D, Cunningham KA, Spampinato U (2008) Differential regulation of the mesoaccumbens dopamine circuit by serotonin2C receptors in the ventral tegmental area and the nucleus accumbens: An in vivo microdialysis study with cocaine. Neuropsychopharmacol 33:237-246
35. Nishikura K (2006) Editor meets silencer: Crosstalk between RNA editing and RNA interference. Nat Rev Mol Cell Biol 7:919-931
36. Niswender CM, Copeland SC, Herrick-Davis K, Emeson RB, Sanders-Bush E (1999) RNA editing of the human serotonin 5-hydroxytryptamine 2C receptor silences constitutive activity. J Biol Chem 274:9472-9478
37. Pistis M, Muntoni AL, Gessa G, Diana M (1997) Effects of acute, chronic ethanol and withdrawal on dorsal raphe neurons: Electrophysiological studies. Neuroscience 79:171-176
38. Robison AJ, Nestler EJ (2011) Transcriptional and epigenetic mechanisms of addiction. Nature Reviews Neuroscience 12:623-637
39. Sheppard JR, Albersheim P, McClearn GE (1968) Enzyme activities and ethanol preference in mice. Biochem Genet 2:205-212
40. Sommer B, Kohler M, Sprengel R, Seeburg PH (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:11-19
41. Van Bockstaele EJ, Biswas A, Pickel VM (1993) Topography of serotonin neurons in the dorsal raphe nucleus that send axon collaterals to the rat prefrontal cortex and nucleus accumbens. Brain Res 624:188-198
42. Van Oekelen D, Luyten WH, Leysen JE (2003) 5-HT2A and 5-HT2C receptors and their atypical regulation properties. Life Sci 72:2429-2449
43. Wang Q, O'Brien PJ, Chen CX, Cho DS, Murray JM, Nishikura K (2000a) Altered G protein-coupling functions of RNA editing isoform and splicing variant serotonin2C receptors. J Neurochem 74:1290-1300
44. Wang Q, O'Brien PJ, Chen CX, Cho DS, Murray JM, Nishikura K (2000b) Altered G protein-coupling functions of RNA editing isoform and splicing variant serotonin2C receptors. J Neurochem 74:1290-1300
45. Wang Q, Miyakoda M, Yang W, Khillan J, Stachura DL, Weiss MJ, Nishikura K (2004) Stress-induced apoptosis associated with null mutation of ADAR1 RNA editing deaminase gene. J Biol Chem 279:4952-4961
46. Watanabe Y, Ikegawa M, Naruse Y, Tanaka M (2009) A novel splicing variant form suppresses the activity of full-length signal transducer and activator of transcription 5A. FEBS J 276:6312-6323
47. Werry TD, Loiacono R, Sexton PM, Christopoulos A (2008) RNA editing of the serotonin 5HT2C receptor and its effects on cell signalling, pharmacology and brain function. Pharmacol Ther 119:7-23
48. Yoshimoto K, Komura S (1989) Genetic differences in the effects of voluntary ethanol consumption on brain monoamine levels in inbred strains of mice, C57BL/6J, C3H/He and DBA/2Cr. Alcohol Alcohol 24:225-229
49. Yoshimoto K, McBride WJ (1992) Regulation of nucleus accumbens dopamine release by the dorsal raphe nucleus in the rat. Neurochem Res 17:401-407
50. Yoshimoto K, McBride WJ, Lumeng L, Li TK (1992a) Ethanol enhances the release of dopamine and serotonin in the nucleus accumbens of HAD and LAD lines of rats. Alcohol Clin Exp Res 16:781-785
51. Yoshimoto K, McBride WJ, Lumeng L, Li TK (1992b) Alcohol stimulates the release of dopamine and serotonin in the nucleus accumbens. Alcohol 9:17-22
52. Yoshimoto K, Watanabe Y, Tanaka M, Kimura M (2012) Serotonin2C receptors in the nucleus accumbens are involved in enhanced alcohol-drinking behaviour. Eur J Neurosci 35:1368-1380