Urocortin-1 within the centrally-projecting edinger-westphal nucleus is critical for ethanol preference

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Giardino, William J ^a   Cocking, Davelle L ^a   Kaur, Simranjit ^a   Cunningham, Christopher L ^a   Ryabinin, Andrey E ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; TAP WATER; UROCORTIN I; CORTICOTROPIN RELEASING FACTOR RECEPTOR; CRF RECEPTOR TYPE 2; UROCORTIN; WATER;

ALCOHOL CONSUMPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVERSIVE BEHAVIOR; BOTTLE FEEDING; CELL NUCLEUS; CONTROLLED STUDY; DRINKING; EDINGER WESTPHAL NUCLEUS; ELECTROLYSIS; GENE DELETION; GENE EXPRESSION; GENE INACTIVATION; MOUSE; NONHUMAN; PROTEIN FUNCTION; ANIMAL; C57BL MOUSE; CHEMISTRY; DECISION MAKING; FOOD PREFERENCE; GENETICS; MOUSE MUTANT; NERVE CELL; PHYSIOLOGY;

MUS;

ANIMALS; CHOICE BEHAVIOR; ETHANOL; FOOD PREFERENCES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; UROCORTINS; WATER;

EID: 80055032657     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026997     Document Type: Article

References (90)

1. Koob GF, Le Moal M, (2008) Review. Neurobiological mechanisms for opponent motivational processes in addiction. Philos Trans R Soc Lond B Biol Sci 363: 3113-3123.
2. Koob GF, Roberts AJ, Schulteis G, Parsons LH, Heyser CJ, et al. (1998) Neurocircuitry targets in ethanol reward and dependence. Alcohol Clin Exp Res 22: 3-9.
3. Koob GF, (2003) Alcoholism: allostasis and beyond. Alcohol Clin Exp Res 27: 232-243.
4. Crabbe JC, Phillips TJ, Harris RA, Arends MA, Koob GF, (2006) Alcohol-related genes: contributions from studies with genetically engineered mice. Addict Biol 11: 195-269.
5. Chang SL, Patel NA, Romero AA, (1995) Activation and desensitization of Fos immunoreactivity in the rat brain following ethanol administration. Brain Res 679: 89-98.
6. Ryabinin AE, Criado JR, Henriksen SJ, Bloom FE, Wilson MC, (1997) Differential sensitivity of c-Fos expression in hippocampus and other brain regions to moderate and low doses of alcohol. Mol Psychiatry 2: 32-43.
7. Knapp DJ, Braun CJ, Duncan GE, Qian Y, Fernandes A, et al. (2001) Regional specificity of ethanol and NMDA action in brain revealed with FOS-like immunohistochemistry and differential routes of drug administration. Alcohol Clin Exp Res 25: 1662-1672.
8. Murphy NP, Sakoori K, Okabe C, (2006) Lack of evidence of a role for the neurosteroid allopregnanolone in ethanol-induced reward and c-fos expression in DBA/2 mice. Brain Res 1094: 107-118.
9. Topple AN, Hunt GE, McGregor IS, (1998) Possible neural substrates of beer-craving in rats. Neurosci Lett 252: 99-102.
10. Bachtell RK, Wang YM, Freeman P, Risinger FO, Ryabinin AE, (1999) Alcohol drinking produces brain region-selective changes in expression of inducible transcription factors. Brain Res 847: 157-165.
11. Weitemier AZ, Woerner A, Backstrom P, Hyytia P, Ryabinin AE, (2001) Expression of c-Fos in Alko alcohol rats responding for ethanol in an operant paradigm. Alcohol Clin Exp Res 25: 704-710.
12. Ryabinin AE, Bachtell RK, Freeman P, Risinger FO, (2001) ITF expression in mouse brain during acquisition of alcohol self-administration. Brain Res 890: 192-195.
13. Ryabinin AE, Galvan-Rosas A, Bachtell RK, Risinger FO, (2003) High alcohol/sucrose consumption during dark circadian phase in C57BL/6J mice: involvement of hippocampus, lateral septum and urocortin-positive cells of the Edinger-Westphal nucleus. Psychopharmacology (Berl) 165: 296-305.
14. Bachtell RK, Weitemier AZ, Galvan-Rosas A, Tsivkovskaia NO, Risinger FO, et al. (2003) The Edinger-Westphal-lateral septum urocortin pathway and its relationship to alcohol consumption. J Neurosci 23: 2477-2487.
15. Sharpe AL, Tsivkovskaia NO, Ryabinin AE, (2005) Ataxia and c-Fos expression in mice drinking ethanol in a limited access session. Alcohol Clin Exp Res 29: 1419-1426.
16. Kaur S, Ryabinin AE, (2010) Ghrelin receptor antagonism decreases alcohol consumption and activation of perioculomotor urocortin-containing neurons. Alcohol Clin Exp Res 34: 1525-1534.
17. Anacker AM, Loftis JM, Kaur S, Ryabinin AE, (2011) Prairie voles as a novel model of socially facilitated excessive drinking. Addict Biol 16: 92-107.
18. Cavani JA, Reiner A, Cuthbertson SL, Bittencourt JC, Toledo CA, (2003) Evidence that urocortin is absent from neurons of the Edinger-Westphal nucleus in pigeons. Braz J Med Biol Res 36: 1695-1700.
19. Weitemier AZ, Tsivkovskaia NO, Ryabinin AE, (2005) Urocortin 1 distribution in mouse brain is strain-dependent. Neuroscience 132: 729-740.
20. Ryabinin AE, Tsivkovskaia NO, Ryabinin SA, (2005) Urocortin 1-containing neurons in the human Edinger-Westphal nucleus. Neuroscience 134: 1317-1323.
21. Kozicz T, Bittencourt JC, May PJ, Reiner A, Gamlin PD, et al. (2011) The Edinger-Westphal nucleus: a historical, structural, and functional perspective on a dichotomous terminology. J Comp Neurol 519: 1413-1434.
22. Bachtell RK, Tsivkovskaia NO, Ryabinin AE, (2002) Strain differences in urocortin expression in the Edinger-Westphal nucleus and its relation to alcohol-induced hypothermia. Neuroscience 113: 421-434.
23. Spangler E, Cote DM, Anacker AM, Mark GP, Ryabinin AE, (2009) Differential sensitivity of the perioculomotor urocortin-containing neurons to ethanol, psychostimulants and stress in mice and rats. Neuroscience 160: 115-125.
24. Vaughan J, Donaldson C, Bittencourt J, Perrin MH, Lewis K, et al. (1995) Urocortin, a mammalian neuropeptide related to fish urotensin I and to corticotropin-releasing factor. Nature 378: 287-292.
25. Lewis K, Li C, Perrin MH, Blount A, Kunitake K, et al. (2001) Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proc Natl Acad Sci U S A 98: 7570-7575.
26. Valdez GR, Roberts AJ, Chan K, Davis H, Brennan M, et al. (2002) Increased ethanol self-administration and anxiety-like behavior during acute ethanol withdrawal and protracted abstinence: regulation by corticotropin-releasing factor. Alcohol Clin Exp Res 26: 1494-1501.
27. Le AD, Harding S, Juzytsch W, Fletcher PJ, Shaham Y, (2002) The role of corticotropin-releasing factor in the median raphe nucleus in relapse to alcohol. J Neurosci 22: 7844-7849.
28. Turek VF, Tsivkovskaia NO, Hyytia P, Harding S, Le AD, et al. (2005) Urocortin 1 expression in five pairs of rat lines selectively bred for differences in alcohol drinking. Psychopharmacology (Berl) 181: 511-517.
29. Fonareva I, Spangler E, Cannella N, Sabino V, Cottone P, et al. (2009) Increased perioculomotor urocortin 1 immunoreactivity in genetically selected alcohol preferring rats. Alcohol Clin Exp Res 33: 1956-1965.
30. Kiianmaa K, Hyytia P, Samson HH, Engel JA, Svensson L, et al. (2003) New neuronal networks involved in ethanol reinforcement. Alcohol Clin Exp Res 27: 209-219.
31. Ryabinin AE, Weitemier AZ, (2006) The urocortin 1 neurocircuit: ethanol-sensitivity and potential involvement in alcohol consumption. Brain Res Rev 52: 368-380.
32. Turek VF, Bennett B, Ryabinin AE, (2008) Differences in the urocortin 1 system between long-sleep and short-sleep mice. Genes Brain Behav 7: 113-119.
33. Bachtell RK, Weitemier AZ, Ryabinin AE, (2004) Lesions of the Edinger-Westphal nucleus in C57BL/6J mice disrupt ethanol-induced hypothermia and ethanol consumption. Eur J Neurosci 20: 1613-1623.
34. Weitemier AZ, Ryabinin AE, (2005) Lesions of the Edinger-Westphal nucleus alter food and water consumption. Behav Neurosci 119: 1235-1243.
35. Kozicz T, (2003) Neurons colocalizing urocortin and cocaine and amphetamine-regulated transcript immunoreactivities are induced by acute lipopolysaccharide stress in the Edinger-Westphal nucleus in the rat. Neuroscience 116: 315-320.
36. Zigman JM, Jones JE, Lee CE, Saper CB, Elmquist JK, (2006) Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol 494: 528-548.
37. Gaszner B, Korosi A, Palkovits M, Roubos EW, Kozicz T, (2007) Neuropeptide Y activates urocortin 1 neurons in the nonpreganglionic Edinger-Westphal nucleus. J Comp Neurol 500: 708-719.
38. Xu L, Bloem B, Gaszner B, Roubos EW, Kozicz T, (2009) Sex-specific effects of fasting on urocortin 1, cocaine- and amphetamine-regulated transcript peptide and nesfatin-1 expression in the rat Edinger-Westphal nucleus. Neuroscience 162: 1141-1149.
39. Xu L, Scheenen WJ, Leshan RL, Patterson CM, Elias CF, et al. (2011) Leptin signaling modulates the activity of urocortin 1 neurons in the mouse nonpreganglionic Edinger-Westphal nucleus. Endocrinology 152: 979-988.
40. Vetter DE, Li C, Zhao L, Contarino A, Liberman MC, et al. (2002) Urocortin-deficient mice show hearing impairment and increased anxiety-like behavior. Nat Genet 31: 363-369.
41. Coste SC, Kesterson RA, Heldwein KA, Stevens SL, Heard AD, et al. (2000) Abnormal adaptations to stress and impaired cardiovascular function in mice lacking corticotropin-releasing hormone receptor-2. Nat Genet 24: 403-409.
42. Kaur S, Li J, Stenzel-Poore M, Ryabinin AE, Corticotropin-releasing factor acting on corticotropin-releasing factor receptor type 1 is critical for binge alcohol drinking in mice. Alcohol Clin Exp Res in press.
43. Pastor R, McKinnon CS, Scibelli AC, Burkhart-Kasch S, Reed C, et al. (2008) Corticotropin-releasing factor-1 receptor involvement in behavioral neuroadaptation to ethanol: a urocortin1-independent mechanism. Proc Natl Acad Sci U S A 105: 9070-9075.
44. Yoneyama N, Crabbe JC, Ford MM, Murillo A, Finn DA, (2008) Voluntary ethanol consumption in 22 inbred mouse strains. Alcohol 42: 149-160.
45. Cunningham CL, Niehus DR, Malott DH, Prather LK, (1992) Genetic differences in the rewarding and activating effects of morphine and ethanol. Psychopharmacology (Berl) 107: 385-393.
46. Cunningham CL, Gremel CM, Groblewski PA, (2006) Drug-induced conditioned place preference and aversion in mice. Nat Protoc 1: 1662-1670.
47. Cunningham CL, Henderson CM, (2000) Ethanol-induced conditioned place aversion in mice. Behav Pharmacol 11: 591-602.
48. Cunningham CL, Ferree NK, Howard MA, (2003) Apparatus bias and place conditioning with ethanol in mice. Psychopharmacology (Berl) 170: 409-422.
49. Blednov YA, Walker D, Harris RA, (2004) Blockade of the leptin-sensitive pathway markedly reduces alcohol consumption in mice. Alcohol Clin Exp Res 28: 1683-1692.
50. Koylu EO, Couceyro PR, Lambert PD, Kuhar MJ, (1998) Cocaine- and amphetamine-regulated transcript peptide immunohistochemical localization in the rat brain. J Comp Neurol 391: 115-132.
51. Dayas CV, McGranahan TM, Martin-Fardon R, Weiss F, (2008) Stimuli linked to ethanol availability activate hypothalamic CART and orexin neurons in a reinstatement model of relapse. Biol Psychiatry 63: 152-157.
52. Dandekar MP, Singru PS, Kokare DM, Lechan RM, Thim L, et al. (2008) Importance of cocaine- and amphetamine-regulated transcript peptide in the central nucleus of amygdala in anxiogenic responses induced by ethanol withdrawal. Neuropsychopharmacology 33: 1127-1136.
53. King BJ, Furlong TM, McNally GP, (2010) Cocaine and amphetamine related transcript (CART) inhibits context induced reinstatement of reward seeking. Behav Neurosci 124: 423-427.
54. Maciewicz R, Phipps BS, Grenier J, Poletti CE, (1984) Edinger-Westphal nucleus: cholecystokinin immunocytochemistry and projections to spinal cord and trigeminal nucleus in the cat. Brain Res 299: 139-145.
55. Tanaka H, Yoshida T, Miyamoto N, Motoike T, Kurosu H, et al. (2003) Characterization of a family of endogenous neuropeptide ligands for the G protein-coupled receptors GPR7 and GPR8. Proc Natl Acad Sci U S A 100: 6251-6256.
56. Dun SL, Brailoiu GC, Mizuo K, Yang J, Chang JK, et al. (2005) Neuropeptide B immunoreactivity in the central nervous system of the rat. Brain Res 1045: 157-163.
57. Foo KS, Brismar H, Broberger C, (2008) Distribution and neuropeptide coexistence of nucleobindin-2 mRNA/nesfatin-like immunoreactivity in the rat CNS. Neuroscience 156: 563-579.
58. Kozicz T, Yanaihara H, Arimura A, (1998) Distribution of urocortin-like immunoreactivity in the central nervous system of the rat. J Comp Neurol 391: 1-10.
59. Bittencourt JC, Vaughan J, Arias C, Rissman RA, Vale WW, et al. (1999) Urocortin expression in rat brain: evidence against a pervasive relationship of urocortin-containing projections with targets bearing type 2 CRF receptors. J Comp Neurol 415: 285-312.
60. Vasconcelos LA, Donaldson C, Sita LV, Casatti CA, Lotfi CF, et al. (2003) Urocortin in the central nervous system of a primate (Cebus apella): sequencing, immunohistochemical, and hybridization histochemical characterization. J Comp Neurol 463: 157-175.
61. Cservenka A, Spangler E, Cote DM, Ryabinin AE, (2010) Postnatal developmental profile of urocortin 1 and cocaine- and amphetamine-regulated transcript in the perioculomotor region of C57BL/6J mice. Brain Res 1319: 33-43.
62. Heilig M, Koob GF, (2007) A key role for corticotropin-releasing factor in alcohol dependence. Trends Neurosci 30: 399-406.
63. Koob GF, (2010) The role of CRF and CRF-related peptides in the dark side of addiction. Brain Res 1314: 3-14.
64. Merlo Pich E, Lorang M, Yeganeh M, Rodriguez de Fonseca F, Raber J, et al. (1995) Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awake rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci 15: 5439-5447.
65. Zorrilla EP, Valdez GR, Weiss F, (2001) Changes in levels of regional CRF-like-immunoreactivity and plasma corticosterone during protracted drug withdrawal in dependent rats. Psychopharmacology (Berl) 158: 374-381.
66. Sommer WH, Rimondini R, Hansson AC, Hipskind PA, Gehlert DR, et al. (2008) Upregulation of voluntary alcohol intake, behavioral sensitivity to stress, and amygdala crhr1 expression following a history of dependence. Biol Psychiatry 63: 139-145.
67. Roberto M, Cruz MT, Gilpin NW, Sabino V, Schweitzer P, et al. (2010) Corticotropin releasing factor-induced amygdala gamma-aminobutyric Acid release plays a key role in alcohol dependence. Biol Psychiatry 67: 831-839.
68. Lodge DJ, Lawrence AJ, (2003) The CRF1 receptor antagonist antalarmin reduces volitional ethanol consumption in isolation-reared fawn-hooded rats. Neuroscience 117: 243-247.
69. Sparta DR, Sparrow AM, Lowery EG, Fee JR, Knapp DJ, et al. (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.
70. Lowery EG, Spanos M, Navarro M, Lyons AM, Hodge CW, et al. (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.
71. Sabino V, Cottone P, Koob GF, Steardo L, Lee MJ, et al. (2006) Dissociation between opioid and CRF1 antagonist sensitive drinking in Sardinian alcohol-preferring rats. Psychopharmacology (Berl) 189: 175-186.
72. Funk CK, Zorrilla EP, Lee MJ, Rice KC, Koob GF, (2007) Corticotropin-releasing factor 1 antagonists selectively reduce ethanol self-administration in ethanol-dependent rats. Biol Psychiatry 61: 78-86.
73. Chu K, Koob GF, Cole M, Zorrilla EP, Roberts AJ, (2007) Dependence-induced increases in ethanol self-administration in mice are blocked by the CRF1 receptor antagonist antalarmin and by CRF1 receptor knockout. Pharmacol Biochem Behav 86: 813-821.
74. Gehlert DR, Cippitelli A, Thorsell A, Le AD, Hipskind PA, et al. (2007) 3-(4-Chloro-2-morpholin-4-yl-thiazol-5-yl)-8-(1-ethylpropyl)-2,6-dimethyl- imidazo[1,2-b]pyridazine: a novel brain-penetrant, orally available corticotropin-releasing factor receptor 1 antagonist with efficacy in animal models of alcoholism. J Neurosci 27: 2718-2726.
75. Gilpin NW, Richardson HN, Koob GF, (2008) Effects of CRF1-receptor and opioid-receptor antagonists on dependence-induced increases in alcohol drinking by alcohol-preferring (P) rats. Alcohol Clin Exp Res 32: 1535-1542.
76. Richardson HN, Zhao Y, Fekete EM, Funk CK, Wirsching P, et al. (2008) MPZP: a novel small molecule corticotropin-releasing factor type 1 receptor (CRF1) antagonist. Pharmacol Biochem Behav 88: 497-510.
77. Sparta DR, Ferraro FM 3rd, Fee JR, Knapp DJ, Breese GR, et al. (2009) The alcohol deprivation effect in C57BL/6J mice is observed using operant self-administration procedures and is modulated by CRF-1 receptor signaling. Alcohol Clin Exp Res 33: 31-42.
78. Sharpe AL, Coste SC, Burkhart-Kasch S, Li N, Stenzel-Poore MP, et al. (2005) Mice deficient in corticotropin-releasing factor receptor type 2 exhibit normal ethanol-associated behaviors. Alcohol Clin Exp Res 29: 1601-1609.
79. Sharpe AL, Phillips TJ, (2009) Central urocortin 3 administration decreases limited-access ethanol intake in nondependent mice. Behav Pharmacol 20: 346-351.
80. Bale TL, Contarino A, Smith GW, Chan R, Gold LH, et al. (2000) Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress. Nat Genet 24: 410-414.
81. Henry B, Vale W, Markou A, (2006) The effect of lateral septum corticotropin-releasing factor receptor 2 activation on anxiety is modulated by stress. J Neurosci 26: 9142-9152.
82. Zhao Y, Valdez GR, Fekete EM, Rivier JE, Vale WW, et al. (2007) Subtype-selective corticotropin-releasing factor receptor agonists exert contrasting, but not opposite, effects on anxiety-related behavior in rats. J Pharmacol Exp Ther 323: 846-854.
83. Funk CK, Koob GF, (2007) A CRF(2) agonist administered into the central nucleus of the amygdala decreases ethanol self-administration in ethanol-dependent rats. Brain Res 1155: 172-178.
84. Pastor R, Reed C, Burkhart-Kasch S, Li N, Sharpe AL, et al. (2011) Ethanol concentration-dependent effects and the role of stress on ethanol drinking in corticotropin-releasing factor type 1 and double type 1 and 2 receptor knockout mice. Psychopharmacology (Berl).
85. Chalmers DT, Lovenberg TW, De Souza EB, (1995) Localization of novel corticotropin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1 receptor mRNA expression. J Neurosci 15: 6340-6350.
86. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, et al. (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428: 191-212.
87. Neufeld-Cohen A, Evans AK, Getselter D, Spyroglou A, Hill A, et al. (2010) Urocortin-1 and-2 double-deficient mice show robust anxiolytic phenotype and modified serotonergic activity in anxiety circuits. Mol Psychiatry 15: 426-441, 339.
88. Neufeld-Cohen A, Tsoory MM, Evans AK, Getselter D, Gil S, et al. (2010) A triple urocortin knockout mouse model reveals an essential role for urocortins in stress recovery. Proc Natl Acad Sci U S A 107: 19020-19025.
89. Giardino WJ, Mark GP, Stenzel-Poore MP, Ryabinin AE, Dissociation of corticotropin-releasing factor receptor subtype involvement in sensitivity to locomotor effects of methamphetamine and cocaine Psychopharmacology (Berl) in press.
90. Giardino WJ, Pastor R, Anacker AM, Spangler E, Cote DM, et al. (2011) Dissection of corticotropin-releasing factor system involvement in locomotor sensitivity to methamphetamine. Genes Brain Behav 10: 78-89.