Effect of chronic ethanol on enkephalin in the hypothalamus and extra-hypothalamic areas

Alcoholism: Clinical and Experimental Research

Volumn 34, Issue 5, 2010, Pages 761-770

  Chang, Guo Qing ^a   Barson, Jessica R ^a   Karatayev, Olga ^a   Chang, Si Yi ^a   Chen, Yu Wei ^b   Leibowitz, Sarah F ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

Corticolimbic; Dynorphin; Enkephalin; Ethanol; Hypothalamus

Indexed keywords

ALCOHOL; DYNORPHIN; ENKEPHALIN; MESSENGER RNA; WATER;

ADULT ANIMAL; ALCOHOL CONSUMPTION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONTROLLED STUDY; GENE EXPRESSION; HISTOCHEMISTRY; HYPOTHALAMUS; IN SITU HYBRIDIZATION; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; VENTRAL TEGMENTUM;

ALCOHOL DRINKING; AMYGDALA; ANIMALS; DYNORPHINS; ENKEPHALINS; ETHANOL; HYPOTHALAMUS; MALE; NUCLEUS ACCUMBENS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; VENTRAL TEGMENTAL AREA;

ANIMALIA; RATTUS;

EID: 77951579363     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2010.01148.x     Document Type: Article

References (93)

1. Arjune D, Bowen WD, Bodnar RJ (1991) Ingestive behavior following central [D-Ala2, Leu5, Cys6]-enkephalin (DALCE), a short-acting agonist and long-acting antagonist at the delta opioid receptor. Pharmacol Biochem Behav 39 : 429 436.
2. 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)
3. Barson JR, Carr AJ, Soun JE, Sobhani NC, Leibowitz SF, Hoebel BG (2009a) Opioids in the nucleus accumbens stimulate ethanol intake. Physiol Behav 98 : 453 459.
4. Barson JR, Carr AJ, Soun JE, Sobhani NC, Rada P, Leibowitz SF, Hoebel BG (2009b) Opioids in the hypothalamic paraventricular nucleus stimulate ethanol intake. Alcohol Clin Exp Res 34 : 214 222.
5. Barton C, Lin L, York DA, Bray GA (1995) Differential effects of enterostatin, galanin and opioids on high-fat diet consumption. Brain Res 702 : 55 60.
6. Berman Y, Devi L, Carr KD (1994) Effects of chronic food restriction on prodynorphin-derived peptides in rat brain regions. Brain Res 664 : 49 53. (Pubitemid 24347594)
7. Berman YL, Devi L, Spangler R, Kreek MJ, Carr KD (1997) Chronic food restriction and streptozotocin-induced diabetes differentially alter prodynorphin mRNA levels in rat brain regions. Mol Brain Res 46 : 25 30. (Pubitemid 27214352)
8. Bilkei-Gorzo A, Michel K, Noble F, Roques BP, Zimmer A (2007) Preproenkephalin knockout mice show no depression-related phenotype. Neuropsychopharmacology 32 : 2330 2337. (Pubitemid 47587681)
9. Bilkei-Gorzo A, Otto M, Zimmer A (2008) Environmental modulation of anxiety-related neuronal activity and behaviors. Behav Brain Res 186 : 289 292. (Pubitemid 350122757)
10. Blednov YA, Walker D, Martinez M, Harris RA (2006) Reduced alcohol consumption in mice lacking preprodynorphin. Alcohol 40 : 73 86. (Pubitemid 46329324)
11. Cador M, Kelley AE, Le Moal M, Stinus L (1986) Ventral tegmental area infusion of substance P, neurotensin and enkephalin: differential effects on feeding behavior. Neuroscience 18 : 659 669. (Pubitemid 16062904)
12. Chang G-Q, Gaysinskaya V, Karatayev O, Leibowitz SF (2008) Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci 28 : 12107 12119.
13. Chang G-Q, Karatayev O, Ahsan R, Avena NM, Lee C, Lewis MJ, Hoebel BG, Leibowitz SF (2007a) Effect of ethanol on hypothalamic opioid peptides, enkephalin, and dynorphin: relationship with circulating triglycerides. Alcohol Clin Exp Res 31 : 249 259. (Pubitemid 46155224)
14. Chang GQ, Karatayev O, Ahsan R, Gaysinskaya V, Marwil Z, Leibowitz SF (2007b) Dietary fat stimulates endogenous enkephalin and dynorphin in the paraventricular nucleus: role of circulating triglycerides. Am J Physiol Endocrinol Metab 292 : E561 E570. (Pubitemid 46220581)
15. Chang GQ, Karatayev O, Davydova Z, Leibowitz SF (2004) Circulating triglycerides impact on orexigenic peptides and neuronal activity in hypothalamus. Endocrinology 145 : 3904 3912. (Pubitemid 39037579)
16. Cowen MS, Lawrence AJ (2001) Alterations in central preproenkephalin mRNA expression after chronic free-choice ethanol consumption by fawn-hooded rats. Alcohol Clin Exp Res 25 : 1126 1133.
17. Devine DP, Leone P, Pocock D, Wise RA (1993) Differential involvement of ventral tegmental mu, delta and kappa opioid receptors in modulation of basal mesolimbic dopamine release: in vivo microdialysis studies. J Pharmacol Exp Ther 266 : 1236 1246. (Pubitemid 24175764)
18. Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137 : 75 114. (Pubitemid 35346430)
19. Di Chiara G, Bassareo V (2007) Reward system and addiction: what dopamine does and doesn't do. Curr Opin Pharmacol 7 : 69 76. (Pubitemid 46238042)
20. Di Chiara G, Imperato A (1985) Ethanol preferentially stimulates dopamine release in the nucleus accumbens of freely moving rats. Eur J Pharmacol 115 : 131 132. (Pubitemid 16233374)
21. Foster KL, McKay PF, Seyoum R, Milbourne D, Yin W, Sarma PV, Cook JM, June HL (2004) GABA(A) and opioid receptors of the central nucleus of the amygdala selectively regulate ethanol-maintained behaviors. Neuropsychopharmacology 29 : 269 284. (Pubitemid 38175146)
22. Garzon M, Pickel VM (2002) Ultrastructural localization of enkephalin and mu-opioid receptors in the rat ventral tegmental area. Neuroscience 114 : 461 474. (Pubitemid 35245425)
23. Giacchino JL, Henriksen SJ (1998) Opioid effects on activation of neurons in the medial prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 22 : 1157 1178.
24. Glass MJ, Billington CJ, Levine AS (2000) Naltrexone administered to central nucleus of amygdala or PVN: neural dissociation of diet and energy. Am J Physiol Regul Integr Comp Physiol 279 : R86 R92.
25. de Gortari P, Mendez M, Rodriguez-Keller I, Perez-Martinez L, Joseph-Bravob P (2000) Acute ethanol administration induces changes in TRH and proenkephalin expression in hypothalamic and limbic regions of rat brain. Neurochem Int 37 : 483 496. (Pubitemid 30386986)
26. Gosnell BA (1988) Involvement of mu opioid receptors in the amygdala in the control of feeding. Neuropharmacology 27 : 319 326.
27. Gustafsson L, Ploj K, Nylander I (2005) Effects of maternal separation on voluntary ethanol intake and brain peptide systems in female Wistar rats. Pharmacol Biochem Behav 81 : 506 516. (Pubitemid 40966796)
28. Hayward MD, Pintar JE, Low MJ (2002) Selective reward deficit in mice lacking beta-endorphin and enkephalin. J Neurosci 22 : 8251 8258.
29. Hebb AL, Zacharko RM, Gauthier M, Trudel F, Laforest S, Drolet G (2004) Brief exposure to predator odor and resultant anxiety enhances mesocorticolimbic activity and enkephalin expression in CD-1 mice. Eur J Neurosci 20 : 2415 2429. (Pubitemid 39472403)
30. Herz A (1997) Endogenous opioid systems and alcohol addiction. Psychopharmacology (Berl) 129 : 99 111. (Pubitemid 27033665)
31. Heyser CJ, Roberts AJ, Schulteis G, Koob GF (1999) Central administration of an opiate antagonist decreases oral ethanol self-administration in rats. Alcohol Clin Exp Res 23 : 1468 1476. (Pubitemid 29468443)
32. Hoebel BG, Avena NM, Rada P (2007) Accumbens dopamine-acetylcholine balance in approach and avoidance. Curr Opin Pharmacol 7 : 617 627. (Pubitemid 350177561)
33. Jamensky NT, Gianoulakis C (1997) Content of dynorphins and kappa-opioid receptors in distinct brain regions of C57BL/6 and DBA/2 mice. Alcohol Clin Exp Res 21 : 1455 1464. (Pubitemid 27517930)
34. Jenck F, Gratton A, Wise RA (1987a) Opioid receptor subtypes associated with ventral tegmental facilitation of lateral hypothalamic brain stimulation reward. Brain Res 423 : 34 38. (Pubitemid 17157151)
35. Jenck F, Quirion R, Wise RA (1987b) Opioid receptor subtypes associated with ventral tegmental facilitation and periaqueductal gray inhibition of feeding. Brain Res 423 : 39 44. (Pubitemid 17157152)
36. Kelley AE (1999) Functional specificity of ventral striatal compartments in appetitive behaviors. Ann N Y Acad Sci 877 : 71 90.
37. Kim EM, Quinn JG, Levine AS, O'Hare E (2004) A bi-directional mu-opioid-opioid connection between the nucleus of the accumbens shell and the central nucleus of the amygdala in the rat. Brain Res 1029 : 135 139. (Pubitemid 39467744)
38. Koob GF (1992) Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 13 : 177 184.
39. Koob GF (2009) Brain stress systems in the amygdala and addiction. Brain Res 1293 : 61 75.
40. Koob GF, Bloom FE (1988) Cellular and molecular mechanisms of drug dependence. Science 242 : 715 721.
41. Kovacs KM, Szakall I, O'Brien D, Wang R, Vinod KY, Saito M, Simonin F, Kieffer BL, Vadasz C (2005) Decreased oral self-administration of alcohol in kappa-opioid receptor knock-out mice. Alcohol Clin Exp Res 29 : 730 738. (Pubitemid 40686541)
42. Lam MP, Marinelli PW, Bai L, Gianoulakis C (2008) Effects of acute ethanol on opioid peptide release in the central amygdala: an in vivo microdialysis study. Psychopharmacology (Berl) 201 : 261 271.
43. Land BB, Bruchas MR, Lemos JC, Xu M, Melief EJ, Chavkin C (2008) The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J Neurosci 28 : 407 414.
44. Latimer LG, Duffy P, Kalivas PW (1987) Mu opioid receptor involvement in enkephalin activation of dopamine neurons in the ventral tegmental area. J Pharmacol Exp Ther 241 : 328 337. (Pubitemid 17119379)
45. Leibowitz SF (2007) Overconsumption of dietary fat and alcohol: mechanisms involving lipids and hypothalamic peptides. Physiol Behav 91 : 513 521.
46. Leibowitz SF, Akabayashi A, Wang J, Alexander JT, Dourmashkin JT, Chang GQ (2007) Increased caloric intake on a fat-rich diet: role of ovarian steroids and galanin in the medial preoptic and paraventricular nuclei and anterior pituitary of female rats. J Neuroendocrinol 19 : 753 766. (Pubitemid 47386876)
47. Levine AS, Olszewski PK, Mullett MA, Pomonis JD, Grace MK, Kotz CM, Billington CJ (2004) Intra-amygdalar injection of DAMGO: effects on c-Fos levels in brain sites associated with feeding behavior. Brain Res 1015 : 9 14.
48. Li XW, Li TK, Froehlich JC (1998) Enhanced sensitivity of the nucleus accumbens proenkephalin system to alcohol in rats selectively bred for alcohol preference. Brain Res 794 : 35 47.
49. Lindholm S, Ploj K, Franck J, Nylander I (2000) Repeated ethanol administration induces short- and long-term changes in enkephalin and dynorphin tissue concentrations in rat brain. Alcohol 22 : 165 171. (Pubitemid 32015909)
50. Lucas LR, Pompei P, Ono J, McEwen BS (1998) Effects of adrenal steroids on basal ganglia neuropeptide mRNA and tyrosine hydroxylase radioimmunoreactive levels in the adrenalectomized rat. J Neurochem 71 : 833 843. (Pubitemid 28480433)
51. Marinelli PW, Bai L, Quirion R, Gianoulakis C (2005) A microdialysis profile of Met-enkephalin release in the rat nucleus accumbens following alcohol administration. Alcohol Clin Exp Res 29 : 1821 1828. (Pubitemid 41579131)
52. Mathieu-Kia AM, Besson MJ (1998) Repeated administration of cocaine, nicotine and ethanol: effects on preprodynorphin, preprotachykinin A and preproenkephalin mRNA expression in the dorsal and the ventral striatum of the rat. Brain Res Mol Brain Res 54 : 141 151.
53. McBride WJ, Murphy JM, Lumeng L, Li TK (1990) Serotonin, dopamine and GABA involvement in alcohol drinking of selectively bred rats. Alcohol 7 : 199 205. (Pubitemid 20268902)
54. McFarland K, Lapish CC, Kalivas PW (2003) Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. J Neurosci 23 : 3531 3537. (Pubitemid 36531996)
55. McLaughlin JP, Marton-Popovici M, Chavkin C (2003) Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J Neurosci 23 : 5674 5683. (Pubitemid 36807845)
56. Mendez M, Morales-Mulia M (2006) Ethanol exposure differentially alters pro-enkephalin mRNA expression in regions of the mesocorticolimbic system. Psychopharmacology (Berl) 189 : 117 124. (Pubitemid 44607265)
57. Mucha RF, Iversen SD (1986) Increased food intake after opioid microinjections into nucleus accumbens and ventral tegmental area of rat. Brain Res 397 : 214 224.
58. Naleid AM, Grace MK, Chimukangara M, Billington CJ, Levine AS (2007) Paraventricular opioids alter intake of high-fat but not high-sucrose diet depending on diet preference in a binge model of feeding. Am J Physiol Regul Integr Comp Physiol 293 : R99 R105. (Pubitemid 47092167)
59. Noel MB, Wise RA (1995) Ventral tegmental injections of a selective mu or delta opioid enhance feeding in food-deprived rats. Brain Res 673 : 304 312.
60. Nylander I, Vlaskovska M, Terenius L (1995) Brain dynorphin and enkephalin systems in Fischer and Lewis rats: effects of morphine tolerance and withdrawal. Brain Res 683 : 25 35.
61. Oliva JM, Manzanares J (2007) Gene transcription alterations associated with decrease of ethanol intake induced by naltrexone in the brain of Wistar rats. Neuropsychopharmacology 32 : 1358 1369. (Pubitemid 46788846)
62. Ookuma K, Barton C, York DA, Bray GA (1997) Effect of enterostatin and kappa-opioids on macronutrient selection and consumption. Peptides 18 : 785 791. (Pubitemid 27400205)
63. Patterson-Buckendahl P, Kubovcakova L, Krizanova O, Pohorecky LA, Kvetnansky R (2005) Ethanol consumption increases rat stress hormones and adrenomedullary gene expression. Alcohol 37 : 157 166.
64. Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press
65. Phillips AG, LePiane FG (1982) Reward produced by microinjection of (D-Ala2),Met5-enkephalinamide into the ventral tegmental area. Behav Brain Res 5 : 225 229.
66. Ploj K, Roman E, Gustavsson L, Nylander I (2000) Basal levels and alcohol-induced changes in nociceptin/orphanin FQ, dynorphin, and enkephalin levels in C57BL/6J mice. Brain Res Bull 53 : 219 226.
67. Ragnauth A, Schuller A, Morgan M, Chan J, Ogawa S, Pintar J, Bodnar RJ, Pfaff DW (2001) Female preproenkephalin-knockout mice display altered emotional responses. Proc Natl Acad Sci USA 98 : 1958 1963. (Pubitemid 32165605)
68. Reagan LP, Rosell DR, Wood GE, Spedding M, Munoz C, Rothstein J, McEwen BS (2004) Chronic restraint stress up-regulates GLT-1 mRNA and protein expression in the rat hippocampus: reversal by tianeptine. Proc Natl Acad Sci USA 101 : 2179 2184. (Pubitemid 38229035)
69. Sawchenko PE (1998) Toward a new neurobiology of energy balance, appetite, and obesity: the anatomists weigh in. J Comp Neurol 402 : 435 441.
70. See RE (2005) Neural substrates of cocaine-cue associations that trigger relapse. Eur J Pharmacol 526 : 140 146.
71. Shaw SG, Vives F, Mora F (1984) Opioid peptides and self-stimulation of the medial prefrontal cortex in the rat. Psychopharmacology (Berl) 83 : 288 292. (Pubitemid 14083655)
72. Shippenberg TS, Zapata A, Chefer VI (2007) Dynorphin and the pathophysiology of drug addiction. Pharmacol Ther 116 : 306 321. (Pubitemid 47454747)
73. Shirayama Y, Chaki S (2006) Neurochemistry of the nucleus accumbens and its relevance to depression and antidepressant action in rodents. Curr Neuropharmacol 4 : 277 291. (Pubitemid 44524464)
74. Shirayama Y, Ishida H, Iwata M, Hazama GI, Kawahara R, Duman RS (2004) Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. J Neurochem 90 : 1258 1268. (Pubitemid 39167359)
75. Silvestre JS, Pallares M, Nadal R, Ferre N (2002) Opposite effects of ethanol and ketamine in the elevated plus-maze test in Wistar rats undergoing a chronic oral voluntary consumption procedure. J Psychopharmacol 16 : 305 312. (Pubitemid 35470574)
76. Soderpalm B, Lof E, Ericson M (2009) Mechanistic studies of ethanol's interaction with the mesolimbic dopamine reward system. Pharmacopsychiatry 42 (Suppl. 1 S87 S94.
77. Steketee JD (2003) Neurotransmitter systems of the medial prefrontal cortex: potential role in sensitization to psychostimulants. Brain Res Brain Res Rev 41 : 203 228.
78. Tanaka E, North RA (1994) Opioid actions on rat anterior cingulate cortex neurons in vitro. J Neurosci 14 (3 Pt 1 1106 1113. (Pubitemid 24081907)
79. Volkow ND, Wang GJ, Ma Y, Fowler JS, Wong C, Ding YS, Hitzemann R, Swanson JM, Kalivas P (2005) Activation of orbital and medial prefrontal cortex by methylphenidate in cocaine-addicted subjects but not in controls: relevance to addiction. J Neurosci 25 : 3932 3939. (Pubitemid 40570426)
80. Walker BM, Koob GF (2008) Pharmacological evidence for a motivational role of kappa-opioid systems in ethanol dependence. Neuropsychopharmacology 33 : 643 652.
81. Weafer J, Fillmore MT (2008) Individual differences in acute alcohol impairment of inhibitory control predict ad libitum alcohol consumption. Psychopharmacology (Berl) 201 : 315 324.
82. Weiss F, Porrino LJ (2002) Behavioral neurobiology of alcohol addiction: recent advances and challenges. J Neurosci 22 : 3332 3337. (Pubitemid 37465737)
83. Wiedenmayer CP, Noailles PA, Angulo JA, Barr GA (2002) Stress-induced preproenkephalin mRNA expression in the amygdala changes during early ontogeny in the rat. Neuroscience 114 : 7 11.
84. Will MJ, Franzblau EB, Kelley AE (2004) The amygdala is critical for opioid-mediated binge eating of fat. Neuroreport 15 : 1857 1860.
85. Williams G, Bing C, Cai XJ, Harrold JA, King PJ, Liu XH (2001) The hypothalamus and the control of energy homeostasis: different circuits, different purposes. Physiol Behav 74 : 683 701. (Pubitemid 34076616)
86. Wilson MA, Junor L (2008) The role of amygdalar mu-opioid receptors in anxiety-related responses in two rat models. Neuropsychopharmacology 33 : 2957 2968.
87. Wise RA, Hoffman DC (1992) Localization of drug reward mechanisms by intracranial injections. Synapse 10 : 247 263.
88. Wittmann W, Schunk E, Rosskothen I, Gaburro S, Singewald N, Herzog H, Schwarzer C (2009) Prodynorphin-derived peptides are critical modulators of anxiety and regulate neurochemistry and corticosterone. Neuropsychopharmacology 34 : 775 785.
89. Yeomans MR (2004) Effects of alcohol on food and energy intake in human subjects: evidence for passive and active over-consumption of energy. Br J Nutr 92 (Suppl. 1 S31 S34.
90. Yeomans MR, Gray RW (2002) Opioid peptides and the control of human ingestive behaviour. Neurosci Biobehav Rev 26 : 713 728.
91. Yoshimoto K, McBride WJ, Lumeng L, Li TK (1992) Alcohol stimulates the release of dopamine and serotonin in the nucleus accumbens. Alcohol 9 : 17 22.
92. Zarrindast MR, Babapoor-Farrokhran S, Rezayof A (2008) Involvement of opioidergic system of the ventral hippocampus, the nucleus accumbens or the central amygdala in anxiety-related behavior. Life Sci 82 : 1175 1181.
93. Zhang M, Gosnell BA, Kelley AE (1998) Intake of high-fat food is selectively enhanced by mu opioid receptor stimulation within the nucleus accumbens. J Pharmacol Exp Ther 285 : 908 914. (Pubitemid 28237478)