Central neuropeptide y modulates binge-like ethanol drinking in C57BL/6J mice via Y1 and Y2 receptors

Neuropsychopharmacology

Volumn 37, Issue 6, 2012, Pages 1409-1421

  Sparrow, Angela M ^a   Lowery Gionta, Emily G ^a   Pleil, Kristen E ^b   Li, Chia ^b   Sprow, Gretchen M ^a   Cox, Benjamin R ^a   Rinker, Jennifer A ^a   Jijon, Ana M ^b   Peňl, José ^b   Navarro, Montserrat ^a   Kash, Thomas L ^b   Thiele, Todd E ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

amygdala; binge like; ethanol; neuropeptide Y; Y1 receptor; Y2 receptor

Indexed keywords

N [2 [1,2 DIHYDRO 3,5(4H) DIOXO 1,2 DIPHENYL 1,2,4 TRIAZOL 4 YL]ETHYL] N2 [[1 [2 [4 [5,11 DIHYDRO 6(6H) OXODIBENZ[B,E]AZEPIN 11 YL] 1 PIPERAZINYL] 2 OXOETHYL]CYCLOPENTYL]ACETYL]ARGININAMIDE; NALPHA (DIPHENYLACETYL) N (4 HYDROXYBENZYL) DEXTRO ARGININAMIDE; NEUROPEPTIDE Y; NEUROPEPTIDE Y1 RECEPTOR; NEUROPEPTIDE Y1 RECEPTOR AGONIST; NEUROPEPTIDE Y2 RECEPTOR; NEUROPEPTIDE Y2 RECEPTOR AGONIST; OPIATE AGONIST; UNCLASSIFIED DRUG;

ALCOHOL ABSTINENCE; ALCOHOLISM; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; DRINKING BEHAVIOR; GABAERGIC TRANSMISSION; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; TISSUE SLICE;

ALCOHOL DRINKING; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; ARGININE; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CONDITIONING, OPERANT; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; GENE EXPRESSION REGULATION; INHIBITORY POSTSYNAPTIC POTENTIALS; INJECTIONS, INTRAVENTRICULAR; MALE; MICE; MICE, INBRED C57BL; NEURONS; NEUROPEPTIDE Y; PEPTIDE FRAGMENTS; RECEPTORS, NEUROPEPTIDE Y;

EID: 84859768964     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2011.327     Document Type: Article

References (68)

1. Bacchi F, Mathe AA, Jimenez P, Stasi L, Arban R, Gerrard P et al (2006). Anxiolytic-like effect of the selective neuropeptide Y Y2 receptor antagonist BIIE0246 in the elevated plus-maze. Peptides 27: 3202-3207. (Pubitemid 44738169)
2. Badia-Elder NE, Stewart RB, Powrozek TA, Murphy JM, Li TK (2003). Effects of neuropeptide Y on sucrose and ethanol intake and on anxiety-like behavior in high alcohol drinking (HAD) and low alcohol drinking (LAD) rats. Alcohol Clin Exp Res 27: 894-899. (Pubitemid 36759377)
3. Badia-Elder NE, Stewart RB, Powrozek TA, Roy KF, Murphy JM, Li TK (2001). Effect of neuropeptide Y (NPY) on oral ethanol intake in Wistar, alcohol-preferring (P), and-nonpreferring (NP) rats. Alcohol Clin Exp Res 25: 386-390. (Pubitemid 32221818)
4. Brumovsky P, Stanic D, Shuster S, Herzog H, Villar M, Hokfelt T (2005). Neuropeptide Y2 receptor protein is present in peptidergic and nonpeptidergic primary sensory neurons of the mouse. J Comp Neurol 489: 328-348. (Pubitemid 41026233)
5. Bulwa ZB, Sharlin JA, Clark PJ, Bhattacharya TK, Kilby CN, Wang Y et al (2011). Increased consumption of ethanol and sugar water in mice lacking the dopamine D2 long receptor. Alcohol 45: 631-639.
6. Chen X, DiMaggio DA, Han SP, Westfall TC (1997). Autoreceptorinduced inhibition of neuropeptide Y release from PC-12 cells is mediated by Y2 receptors. Am J Physiol 273(4 Pt 2): H1737-H1744.
7. Criado JR, Liu T, Ehlers CL, Mathe AA (2011). Prolonged chronic ethanol exposure alters neuropeptide Y and corticotropinreleasing factor levels in the brain of adult Wistar rats. Pharmacol Biochem Behav 99: 104-111.
8. Doods H, Gaida W, Wieland HA, Dollinger H, Schnorrenberg G, Esser F et al (1999). BIIE0246: a selective and high affinity neuropeptide Y Y(2) receptor antagonist. Eur J Pharmacol 384: R3-R5. (Pubitemid 30006963)
9. Doods HN, Wieland HA, Engel W, Eberlein W, Willim KD, Entzeroth M et al (1996). BIBP 3226, the first selective neuropeptide Y1 receptor antagonist: a review of its pharmacological properties. Regul Peptides 65: 71-77. (Pubitemid 26273589)
10. Ehlers CL, Li TK, Lumeng L, Hwang BH, Somes C, Jimenez P et al (1998). Neuropeptide Y levels in ethanol-naive alcohol-preferring and nonpreferring rats and in Wistar rats after ethanol exposure. Alcohol Clin Exp Res 22: 1778-1782. (Pubitemid 28536170)
11. Feletou M, Levens NR (2005). Neuropeptide Y2 receptors as drug targets for the central regulation of body weight. Curr Opin Investig Drugs 6: 1002-1011. (Pubitemid 41535784)
12. Finn DA, Snelling C, Fretwell AM, Tanchuck MA, Underwood L, Cole M et al (2007). Increased drinking during withdrawal from intermittent ethanol exposure is blocked by the CRF receptor antagonist d-Phe-CRF(12-41). Alcohol Clin Exp Res 31: 939-949. (Pubitemid 46776166)
13. Franklin KBJ, Paxinos G (1997). The Mouse Brain in Stereotaxic Coordinates. Academic Press: San Diego, CA.
14. Funk CK, Dell LE, Crawford EF, Koob GF (2006). Corticotropinreleasing factor within the central nucleus of the amygdala mediates enhanced ethanol self-administration in withdrawn, ethanol-dependent rats. J Neurosci 26: 11324-11332. (Pubitemid 44772162)
15. Gehlert DR, Cippitelli A, Thorsell A, Le AD, Hipskind PA, Hamdouchi C et al (2007). 3-(4-Chloro-2-morpholin-4-ylthiazol-5-yl)-8-(1-ethylpropyl)-2,6- dimethyl-imidazo[1,2-b]pyridazine: a novel brain-penetrant, orally available corticotropinreleasing factor receptor 1 antagonist with efficacy in animal models of alcoholism. J Neurosci 27: 2718-2726. (Pubitemid 46393604)
16. Gerald C, Walker MW, Criscione L, Gustafson EL, Batzlhartmann C, Smith KE et al (1996). A receptor subtype involved in neuropeptide-Y-induced food intake. Nature 382: 168-171. (Pubitemid 26242883)
17. Gilpin NW, Misra K, Herman MA, Cruz MT, Koob GF, Roberto M (2011). Neuropeptide Y opposes alcohol effects on gammaaminobutyric acid release in amygdala and blocks the transition to alcohol dependence. Biol Psychiatry 69: 1091-1099.
18. Gilpin NW, Misra K, Koob GF (2008). Neuropeptide Y in the central nucleus of the amygdala suppresses dependence-induced increases in alcohol drinking. Pharmacol Biochem Behav 90: 475-480.
19. Gmel G, Bissery A, Gammeter R, Givel JC, Calmes JM, Yersin B et al (2006). Alcohol-attributable injuries in admissions to a swiss emergency room-an analysis of the link between volume of drinking, drinking patterns, and preattendance drinking. Alcohol Clin Exp Res 30: 501-509. (Pubitemid 43341356)
20. Gupta T, Syed YM, Revis AA, Miller SA, Martinez M, Cohn KA et al (2008). Acute effects of acamprosate and MPEP on ethanol Drinking-in-the-Dark in male C57BL/6J mice. Alcohol Clin Exp Res 32: 1992-1998.
21. Haubensak W, Kunwar PS, Cai H, Ciocchi S, Wall NR, Ponnusamy R et al (2010). Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468: 270-276.
22. Hayes DM, Knapp DJ, Breese GR, Thiele TE (2005). Comparison of basal NPY and CRF levels between the high ethanol drinking C57BL/6J and low ethanol drinking DBA/2J inbred mouse strains. Alcohol Clin Exp Res 29: 721-729. (Pubitemid 40686540)
23. Hendrickson LM, Zhao-Shea R, Tapper AR (2009). Modulation of ethanol drinking-in-the-dark by mecamylamine and nicotinic acetylcholine receptor agonists in C57BL/6J mice. Psychopharmacology (Berl) 204: 563-572.
24. Hingson R, Heeren T, Winter M, Wechsler H (2005). Magnitude of alcohol-related mortality and morbidity among U.S. college students ages 18-24: changes from 1998 to 2001. Annu Rev Public Health 26: 259-279. (Pubitemid 40547384)
25. Hingson RW, Heeren T, Winter MR (2006). Age of alcoholdependence onset: associations with severity of dependence and seeking treatment. Pediatrics 118: e755-e763. (Pubitemid 46090003)
26. Kamdar NK, Miller SA, Syed YM, Bhayana R, Gupta T, Rhodes JS (2007). Acute effects of naltrexone and GBR 12909 on ethanol drinking-in-the-dark in C57BL/6J mice. Psychopharmacology (Berl) 192: 207-217. (Pubitemid 46669212)
27. Kash TL, Winder DG (2006). Neuropeptide Y and corticotropinreleasing factor bi-directionally modulate inhibitory synaptic transmission in the bed nucleus of the stria terminalis. Neuropharmacology 51: 1013-1022. (Pubitemid 44528607)
28. Kaur S, Ryabinin AE (2010). Ghrelin receptor antagonism decreases alcohol consumption and activation of perioculomotor urocortincontaining neurons. Alcohol Clin Exp Res 34: 1525-1534.
29. King PJ, Widdowson PS, Doods HN, Williams G (1999). Regulation of neuropeptide Y release by neuropeptide Y receptor ligands and calcium channel antagonists in hypothalamic slices. J Neurochem 73: 641-646. (Pubitemid 29339837)
30. King PJ, Williams G, Doods H, Widdowson PS (2000). Effect of a selective neuropeptide Y Y(2) receptor antagonist, BIIE0246 on neuropeptide Y release. Eur J Pharmacol 396: R1-R3. (Pubitemid 30261560)
31. Koob GF (2003). Alcoholism: allostasis and beyond. Alcohol Clin Exp Res 27: 232-243. (Pubitemid 36236646)
32. Koob GF, Le Moal M (2001). Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24: 97-129.
33. Kopp J, Xu ZQ, Zhang X, Pedrazzini T, Herzog H, Kresse A et al (2002). Expression of the neuropeptide Y Y1 receptor in the CNS of rat and of wild-type and Y1 receptor knock-out mice. Focus on immunohistochemical localization. Neuroscience 111: 443-532. (Pubitemid 34521893)
34. Linsenbardt DN, Boehm 2nd SL (2009). Agonism of the endocannabinoid system modulates binge-like alcohol intake in male C57BL/6J mice: involvement of the posterior ventral tegmental area. Neuroscience 164: 424-434.
35. Lowery EG, Spanos M, Navarro M, Lyons AM, Hodge CW, Thiele TE (2010). CRF-1 antagonist and CRF-2 agonist decrease binge-like ethanol drinking in C57BL/6J mice independent of the HPA axis. Neuropsychopharmacology 35: 1241-1252.
36. Lyons AM, Thiele TE (2010). Neuropeptide Y conjugated to saporin alters anxiety-like behavior when injected into the central nucleus of the amygdala or basomedial hypothalamus in BALB/cJ mice. Peptides 31: 2193-2199.
37. Melon L, Boehm 2nd SL (2011). GABA(A) receptors in the posterior, but not anterior, ventral tegmental area mediate Ro15-4513-induced attenuation of binge-like ethanol consumption in C57BL/6J female mice. Behav Brain Res 220: 230-237.
38. Miller JW, Naimi TS, Brewer RD, Jones SE (2007). Binge drinking and associated health risk behaviors among high school students. Pediatrics 119: 76-85. (Pubitemid 46397844)
39. Moore EM, Boehm 2nd SL (2009). Site-specific microinjection of baclofen into the anterior ventral tegmental area reduces bingelike ethanol intake in male C57BL/6J mice. Behav Neurosci 123: 555-563.
40. Mullins D, Kirby D, Hwa J, Guzzi M, Rivier J, Parker E (2001). Identification of potent and selective neuropeptide Y Y(1) receptor agonists with orexigenic activity in vivo. Mol Pharmacol 60: 534-540. (Pubitemid 32781561)
41. Nakhate KT, Dandekar MP, Kokare DM, Subhedar NK (2009). Involvement of neuropeptide Y Y(1) receptors in the acute, chronic and withdrawal effects of nicotine on feeding and body weight in rats. Eur J Pharmacol 609: 78-87.
42. Navarro M, Cubero I, Knapp DJ, Breese GR, Thiele TE (2008). Decreased immunoreactivity of the melanocortin neuropeptide alpha-melanocyte-stimulating hormone (alpha-MSH) after chronic ethanol exposure in Sprague-Dawley rats. Alcohol Clin Exp Res 32: 266-276.
43. Naveilhan P, Neveu I, Arenas E, Ernfors P (1998). Complementary and overlapping expression of Y1, Y2 and Y5 receptors in the developing and adult mouse nervous system. Neuroscience 87: 289-302. (Pubitemid 28351185)
44. Okoro CA, Brewer RD, Naimi TS, Moriarty DG, GilesWH, Mokdad AH (2004). Binge drinking and health-related quality of life: do popular perceptions match reality? Am J Prev Med 26: 230-233. (Pubitemid 38338673)
45. Palmiter RD, Erickson JC, Hollopeter G, Baraban SC, Schwartz MW (1998). Life without neuropeptide Y. Recent Prog Horm Res 53: 163-199. (Pubitemid 128472741)
46. Pandey SC, Ugale R, Zhang H, Tang L, Prakash A (2008). Brain chromatin remodeling: a novel mechanism of alcoholism. J Neurosci 28: 3729-3737.
47. Pinto S, Roseberry AG, Liu H, Diano S, Shanabrough M, Cai X et al (2004). Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304: 110-115. (Pubitemid 38451468)
48. Qian J, Colmers WF, Saggau P (1997). Inhibition of synaptic transmission by neuropeptide Y in rat hippocampal area CA1: modulation of presynaptic Ca2+ entry. J Neurosci 17: 8169-8177. (Pubitemid 27461041)
49. Rhodes JS, Best K, Belknap JK, Finn DA, Crabbe JC (2005). Evaluation of a simple model of ethanol drinking to intoxication in C57BL/6J mice. Physiol Behav 84: 53-63. (Pubitemid 40092065)
50. Roberto M, Madamba SG, Stouffer DG, Parsons LH, Siggins GR (2004). Increased GABA release in the central amygdala of ethanol-dependent rats. J Neurosci 24: 10159-10166. (Pubitemid 39492041)
51. Roy A, Pandey SC (2002). The decreased cellular expression of neuropeptide Y protein in rat brain structures during ethanol withdrawal after chronic ethanol exposure. Alcohol Clin Exp Res 26: 796-803. (Pubitemid 34666138)
52. Sajja RK, Rahman S (2011). Lobeline and cytisine reduce voluntary ethanol drinking behavior in male C57BL/6J mice. Prog Neuropsychopharmacol Biol Psychiatry 35: 257-264.
53. Sakharkar AJ, Zhang H, Tang L, Shi G, Pandey SC et al. Histone deacetylases (HDAC)-induced histone modifications in the amygdala: a role in rapid tolerance to the anxiolytic effects of ethanol. Alcohol Clin Exp Res; (e-pub ahead of print 25 July 2011).
54. Shepherd JP, Sutherland I, Newcombe RG (2006). Relations between alcohol, violence and victimization in adolescence. J Adolesc 29: 539-553. (Pubitemid 44070571)
55. Slawecki CJ, Jimenez-Vasquez P, Mathe AA, Ehlers CL (2005). Effect of ethanol on brain neuropeptides in adolescent and adult rats. J Stud Alcohol 66: 46-52. (Pubitemid 40381600)
56. Smith-White MA, Hardy TA, Brock JA, Potter EK (2001). Effects of a selective neuropeptide Y Y2 receptor antagonist, BIIE0246, on Y2 receptors at peripheral neuroeffector junctions. Br J Pharmacol 132: 861-868. (Pubitemid 32193643)
57. Sorensen G, Lindberg C, Wortwein G, Bolwig TG, Woldbye DP (2004). Differential roles for neuropeptide Y Y1 and Y5 receptors in anxiety and sedation. J Neurosci Res 77: 723-729. (Pubitemid 39194614)
58. Sparta DR, Sparrow AM, Lowery EG, Fee JR, Knapp DJ, Thiele TE (2008). Blockade of the corticotropin releasing factor type 1 receptor attenuates elevated ethanol drinking associated with drinking in the dark procedures. Alcohol Clin Exp Res 32: 259-265.
59. Thiele TE, Cubero I, van Dijk G, Mediavilla C, Bernstein IL (2000). Ethanol-induced c-Fos expression in catecholamine-and neuropeptide Y-producing neurons in rat brainstem. Alcohol Clin Exp Res 24: 802-809. (Pubitemid 30421730)
60. Thiele TE, Koh MT, Pedrazzini T (2002). Voluntary alcohol consumption is controlled via the neuropeptide Y Y1 receptor. J Neurosci 22: RC208.
61. Thiele TE, Naveilhan P, Ernfors P (2004). Assessment of ethanol consumption and water drinking by NPY Y2 receptor knockout mice. Peptides 25: 975-983. (Pubitemid 38760285)
62. Thiele TE, Sparta DR, Fee JR, Navarro M, Cubero I (2003). Central neuropeptide Y alters ethanol-induced sedation, but not ethanol intake, in C57BL/6 mice. Alcohol 31: 155-160. (Pubitemid 38018981)
63. Thorsell A, Rimondini R, Heilig M (2002). Blockade of central neuropeptide Y (NPY) Y2 receptors reduces ethanol selfadministration in rats. Neurosci Lett 332: 1-4.
64. Valdez GR, Roberts AJ, Chan K, Davis H, Brennan M, Zorrilla EP et al (2002). Increased ethanol self-administration and anxietylike behavior during acute ethanol withdrawal and protracted abstinence: regulation by corticotropin-releasing factor. Alcohol Clin Exp Res 26: 1494-1501. (Pubitemid 35192310)
65. Wahlestedt C, Yanaihara N, Hakanson R (1986). Evidence for different pre-and post-junctional receptors for neuropeptide Y and related peptides. Regul Peptides 13: 307-301.
66. Walker BM, Drimmer DA, Walker JL, Liu T, Mathe AA, Ehlers CL (2010). Effects of prolonged ethanol vapor exposure on forced swim behavior, and neuropeptide Y and corticotropin-releasing factor levels in rat brains. Alcohol 44: 487-493.
67. Zhang H, Pandey SC (2003). Effects of PKA modulation on the expression of neuropeptide Y in rat amygdaloid structures during ethanol withdrawal. Peptides 24: 1397-1402. (Pubitemid 38045547)
68. Zhang H, Sakharkar AJ, Shi G, Ugale R, Prakash A, Pandey SC (2010). Neuropeptide Y signaling in the central nucleus of amygdala regulates alcohol-drinking and anxiety-like behaviors of alcohol-preferring rats. Alcohol Clin Exp Res 34: 451-461.