Role of orexin-1 receptor mechanisms on compulsive food consumption in a model of binge eating in female rats

Neuropsychopharmacology

Volumn 37, Issue 9, 2012, Pages 1999-2011

  Piccoli, Laura ^a,d   Micioni Di Bonaventura, Maria Vittoria ^b   Cifani, Carlo ^b   Costantini, Vivian J A ^a,d   Massagrande, Mario ^a,d   Montanari, Dino ^a,d   Martinelli, Prisca ^a,d   Antolini, Marinella ^a,d   Ciccocioppo, Roberto ^b   Massi, Maurizio ^b   Merlo Pich, Emilio ^c   Di Fabio, Romano ^a,d   Corsi, Mauro ^a,d  

^a GSK   (Italy)

^b UNIVERSITY OF CAMERINO   (Italy)

^c GLAXOSMITHKLINE   (United States)

^d Aptuit Inc   (United States)

Author keywords

binge eating; compulsive food consumption; female rats; orexin 1 receptor antagonist; orexin 2 receptor antagonist

Indexed keywords

GSK 1059865; JNJ 10397049; OREXIN 1 RECEPTOR; PROTEIN INHIBITOR; SB 649868; TOPIRAMATE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; AREA UNDER THE CURVE; BINGE EATING DISORDER; CONTROLLED STUDY; DIET RESTRICTION; DRUG MECHANISM; DRUG SCREENING; FEMALE; FOOD INTAKE; MALE; MAXIMUM PLASMA CONCENTRATION; NONHUMAN; POLYSOMNOGRAPHY; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REVIEW; STRESS;

EID: 84863986943     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.48     Document Type: Review

References (81)

1. American Psychiatric Association (2000). Diagnostic and Statistic Manual of Mental Disorders, IV-TR. American Psychiatric Association: Washington, DC.
2. Appolinario JC, Godoy-Matos A, Fontenelle LF, Carraro L, Cabral M, Vieira A et al (2000). An open-label trial of sibutramine in obese patients with binge-eating disorder. J Clin Psychiatry 63: 8-30.
3. Arunlakshana O, Schild HO (1959). Some quantitative uses of drug antagonists. Br J Pharmacol Chemother 14: 48-58.
4. Avena NM, Bocarsly ME (2011). Dysregulation of brain reward systems in eating disorders: neurochemical information from animal models of binge eating, bulimia nervosa, and anorexia nervosa. Neuropharmacology; e-pub ahead of print 27 November 2011.
5. Avena NM, Rada P, Hoebel BG (2008). Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32: 20-39.
6. Bello NT, Hajnal A (2010). Dopamine and binge eating behaviors. Pharmacol Bioichem Behav 97: 25-33.
7. Bonci A, Borgland S (2009). Role of orexin/hypocretin and CRF in the formation of drug-dependent synaptic plasticity in the mesolimbic system. Neuropharmacology 56: 107-111.
8. Borgland SL, Taha SA, Sarti F, Fields HL, Bonci A (2006). Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49: 589-601.
9. Boutrel B, Kenny PJ, Specio SE, Martin-Fardon R, Markou A, Koob GF et al (2005). Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc Natl Acad Sci USA 102: 19168-19173.
10. Brandish PE, Hill LA, Zheng W, Scolnick EM (2003). Scintillation proximity assay of inositol phosphates in cells extracts: highthroughput measurement of G-protein-coupled receptor activation. Anal Biochem 313: 311-318.
11. Brisbare-Roch C, Dingemanse J, Koberstein R, Hoever P, Aissaoui H, Flores S et al (2007). Promotion of sleep by targeting the orexin system in rats, dogs and humans. Nat Med 13: 50-155.
12. Broft AI, Berner LA, Martinez D, Walsh BT (2011). Bulimia nervosa and evidence for striatal dopamine dysregulation: a conceptual review. Physiol Behav 104: 122-127.
13. Carter WP, Hudson JI, Lalonde JK, Pindyck L, Mcelroy SL, Pope Jr HG (2003). Pharmacologic treatment of binge eating disorder. Int J Eat Disord 34(Suppl): S74-S88.
14. Cason AM, Smith RJ, Tahsili-Fahadan P, Moorman DE, Sartor GC, Aston-Jones G (2010). Role of orexin/hypocretin in reward seeking and addiction: implications for obesity. Physiol Behav 100: 419-428.
15. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C et al (1999). Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 98: 437-451.
16. Cifani C, Polidori C, Melotto S, Ciccocioppo R, Massi MA (2009). Preclinical model of binge-eating elicited by yo-yo dieting and stressful exposure to food: effect of sibutramine, fluoxetine, topiramate and midazolam. Psychopharmacology 204: 113-125.
17. Corwin R, Avena NM, Boggiano MM (2011). Feeling and reward: perspective from three rat models of binge eating. Physiol Behav 104: 87-97.
18. Crowther JH, Sanftner J, Bonifazi DZ, Shepherd KL (2001). The role of daily hassles in binge eating. Int J Eat Disord 29: 449-454.
19. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE et al (1998). The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95: 322-327.
20. Devlin MJ, Yanovski SZ, Wilson GT (2000). Obesity: what mental health professionals need to know. Am J Psychiatry 157: 854-866.
21. Di Fabio R, Pellacani A, Faedo S, Roth A, Piccoli L, Gerrard P et al (2011). Discovery process and pharmacological characterization of a novel dual orexin 1 and orexin 2 receptor antagonist useful for treatment of sleep disorders. Biorg Med Chem Lett 21: 5562-5567.
22. Dugovic C, Shelton JE, Aluisio LE, Fraser IC, Jiang X, Sutton SW et al (2009). Blockade of orexin-1 receptors attenuates orexin-2 receptor antagonism-induced sleep promotion in the rat. J Pharmacol Exp Ther 330: 142-151.
23. Fassino S, Leombruni P, Pierò A, Abbate-Daga G, Giacomo Rovera G (2003). Mood, eating attitudes, and anger in obese women with and without binge eating disorder. J Psychosom Res 54: 559-566.
24. Foulds Mathes W, Brownley KA, Mo X, Bulik CM (2009). The biology of binge eating. Appetite 52: 545-553.
25. Freeman LM, Gil KM (2004). Daily stress, coping, and dietary restraint in binge eating. Int J Eat Disord 36: 204-212.
26. Gearhardt AN, Corbin WR, Brownell KD (2011a). Food addiction: an examination of the diagnostic criteria for dependence. J Addict Med 3: 1-7.
27. Gearhardt AN, Yokum S, Orr PT, Stice E, Corbin WR, Brownell KD (2011b). Neural correlates of food addiction. Arch Gen Psychiatry 68: 808-816.
28. Gold MS, Frost-Pineda K, JacobsWS (2003). Overeating, binge eating, and eating disorders as addictions. Psychiatr Ann 33: 112-116.
29. Gozzi A, Turrini G, Piccoli L, Massagrande M, Amantini D, Antolini M et al (2011). Functional magnetic resonance imaging reveals different neural substrates for the effects of orexin-1 and orexin-2 receptor antagonists. PLoS One 6: e16406.
30. Grucza RA, Przybeck TR, Cloninger CR (2007). Prevalence and correlates of binge eating disorder in a community sample. Compr Psychiatry 48: 124-131.
31. Harris GC, Aston-Jones G (2006). Arousal and reward: a dichotomy in orexin function. Trends Neurosci 29: 571-577.
32. Harris GC, Wimmer M, Aston-Jones G (2005). A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437: 556-559.
33. Haynes AC, Jackson B, Chapman H, Tadayyon M, Johns A, Porter RA et al (2000). A selective orexin-1 receptor antagonist reduces food consumption in male and female rats. Regul Pept 96: 45-51.
34. Heath AC (1998). Binge-eating and bulimia: potential insights into etiology and pathophysiology through genetic epidemiologic studies. Biol Psychiatry 44: 1208-1209.
35. Hoebel BG (1985). Brain neurotransmitters in food and drug reward. Am J Clin Nutr 42(Suppl): 1133-1150.
36. Hollander JA, Lu Q, Cameron MD, Kamenecka TM, Kenny PJ (2008). Insular hypocretin transmission regulates nicotine reward. Proc Natl Acad Sci USA 105: 19480-19485.
37. Hudson JI, Hiripi E, Pope Jr HG, Kessler RC (2007). The prevalence and correlates of eating disorders in the national comorbidity survey replication. Biol Psychiatry 61: 348-358.
38. Ifland JR, Preuss HG, Marcus MT, Rourke KM, Taylor WC, Burau K et al (2009). Refined food addiction: a classic substance use disorder. Med Hypotheses 72: 518-526.
39. Kenakin T, Jenkinson S, Watson C (2006). Determining the potency and molecular mechanism of action of unsurmountable antagonists. J Pharmacol Exp Ther 319: 710-723.
40. Kenny PJ (2011). Common cellular and molecular mechanisms in obesity and drug addiction. Nat Rev Neurosci 12: 638-651.
41. Koob GF (2008). A role for brain stress system in addiction. Neuron 59: 11-34.
42. Kuwaki T (2011). Orexin links emotional stress to autonomic functions. Auton Neurosci 161: 20-27.
43. Javaras KN, Pope HG, Lalonde JK, Roberts JL, Nillni YI, Laird NM et al (2008). Co-occurrence of binge eating disorder with psychiatric and medical disorders. J Clin Psychiatry 269: 266-273.
44. Johnson PL, Truitt W, Fitz SD, Minick PE, Dietrich A, Sanghani S et al (2010). A key role for orexin in panic anxiety. Nat Med 16: 111-115.
45. Johnson PM, Kenny PJ (2010). Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13: 635-641.
46. Jupp B, Krivdic B, Krstew E, Lawrence AJ (2011). The orexin1 receptor antagonist SB-334867 dissociates the motivational properties of alcohol and sucrose in rats. Brain Res 1391: 54-59.
47. Lawrence AJ, Cowen MS, Yang HJ, Chen F, Oldfield B (2006). The orexin system regulates alcohol-seeking in rats. Br J Pharmacol 148: 752-759.
48. Lu XY, Bagnol D, Burke S, Akil H, Watson SJ (2000). Differential distribution and regulation of OX1 and OX2 orexin/hypocretin receptor messenger RNA in the brain upon fasting. Horm Behav 37: 335-344.
49. Malherbe P, Borroni E, Pinard E, Wettstein JG, Knoflach F (2009). Biochemical and electrophysiological characterization of almorexant, a dual orexin 1 receptor (OX1)/orexin 2 receptor (OX2) antagonist: comparison with selective OX1 and OX2 antagonists. Mol Pharmacol 76: 618-631.
50. Marcus JN, Aschkenasi CJ, Lee CE, Chemelli RM, Saper CB, Yanagisawa M et al (2001). Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 435: 6-25.
51. Martin-Fardon R, Zorrilla EP, Ciccocioppo R, Weiss F (2010). Role of innate and drug-induced dysregulation of brain stress and arousal systems in addiction: focus on corticotropin-releasing factor, nociceptin/orphanin FQ, and orexin/hypocretin. Brain Res 1314: 145-161.
52. McAtee LC, Sutton SW, Rudolph DA, Li X, Aluisio LE, Phuong VK et al (2004). Novel substituted 4-phenyl-[1,3]dioxanes: potent and selective orexin receptor 2 (OX2R) antagonists. Bioorg Med Chem Lett 14: 4225-4229.
53. McElroy SL, Guerdjikova AI, Martens B, Keck Jr PE, Pope HG, Hudson JI (2009). Role of antiepileptic drugs in the management of eating disorders. CNS Drugs 23: 139-156.
54. McElroy SL, Hudson JI, Capece JA, Beyers K, Fisher AC, Rosenthal NR (2007). Topiramate for the treatment of binge eating disorder associated with obesity: a placebo controlled study. Biol Psychiatry 61: 1039-1048.
55. Nair SG, Golden SA, Shaham Y (2008). Differential effects of the hypocretin 1 receptor antagonist SB 334867 on high-fat food self-administration and reinstatement of food seeking in rats. Br J Pharmacol 154: 406-416.
56. Pelchat ML, Johnson A, Chan R, Valdez J, Ragland JD (2004). Images of desire: food-craving activation during fMRI. Neuro-Image 23: 1486-1493.
57. Perello M, Sakata I, Birnbaum S, Chuang JC, Osborne-Lawrence S, Rovinsky SA et al (2010). Ghrelin increases the rewarding value of high fat diet in an orexin-dependent manner. Biol Psych 67: 880-886.
58. Polivy J, Zeitlin SB, Herman CP, Beal AL (1994). Food restriction and binge eating: a study of former prisoner of war. J Abnorm Psychol 103: 409-411.
59. Read KD, Braggio S (2010). Assessing brain free fraction in early drug discovery. Expert Opin Drug Metab Toxicol 6: 337-344.
60. Richards JK, Simms JA, Steensland P, Taha SA, Borgland SL, Bonci A et al (2008). Inhibition of orexin-1/hypocretin-1 receptors inhibits yohimbine-induced reinstatement of ethanol and sucrose seeking in Long-Evans rats. Psychopharmacology 199: 109-117.
61. Rodgers RJ, Halford JC, Nunes de Souza RL, Canto de Souza AL, Piper DC, Arch JR et al (2001). SB-334867, a selective orexin-1 receptor antagonist, enhances behavioural satiety and blocks the hyperphagic effect of orexin-A in rats. Eur J Neurosci 13: 1444-1452.
62. Sakamoto F, Yamada S, Ueta Y (2004). Centrally administered orexin-A activates corticotropin-releasing factor containing neurons in the hypothalamic paraventricular nucleus and central amygdaloid nucleus of rats: possible involvement of central orexins on stress-activated central CRF neurons. Reg Pept 118: 183-191.
63. Sakurai T (2007). The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 8: 171-181.
64. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H et al (1998). Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92: 573-585.
65. Sharf R, Sarhan M, Brayton CE, Guarnieri DJ, Taylor JR, DiLeone RJ (2010). Orexin signaling via OX1R mediates operant responding for food reinforcement. Biol Psychiatry 67: 753-760.
66. Shoblock JR, Welty N, Aluisio L, Fraser I, Motley ST, Morton K et al (2011). Selective blockade of the orexin-2 receptor attenuates ethanol self-administration, place preference, and reinstatement. Psychopharmacology 215: 191-203.
67. Smith RJ, Tahsili-Fahadan P, Aston-Jones G (2010). Orexin/hypocretin is necessary for context-driven cocaine-seeking. Neuropharmacology 58: 179-184.
68. Stice E, Agras WS, Telch FC, Halmi KA, Mitchell JE, Wilson T (2001). Subtyping binge eating-disordered women along dieting and negative affect dimensions. Int J Eat Disord 30: 11-27.
69. Trivedi P, Yu H, MacNeil DJ, Van der Ploeg LH, Guan XM (1998). Distribution of orexin receptor mRNA in the rat brain. FEBS Lett 438: 71-75.
70. Uramura K, Funahashi H, Muroya S, Shioda S, Takigawa M, Yada T (2001). Orexin-a activates phospholipase C and protein kinase C mediated Ca2+ signaling in dopamine neurons of the ventral tegmental area. NeuroReport 12: 1885-1889.
71. Volkow ND, Wise RA (2005). How can drug addiction help us understand obesity? Nat Neurosci 8: 555-560.
72. Yager J (2008). Binge eating disorder: the search for better treatments. Am J Psychiatry 165: 4-6.
73. Yanovski SZ (2003). Binge eating disorder and obesity in 2003: could treating an eating disorder have a positive effect on the obesity epidemic? Int J Eat Disord 34(Suppl): S117-S120.
74. Walsh BT, Devlin MJ (1998). Eating disorders: progress and problems. Science 280: 1387-1390.
75. Wang GJ, Geliebter A, Volkow ND, Telang FW, Logan J, Jayne MC et al (2011). Enhanced striatal dopamine release during food stimulation during binge eating disorder. Obesity 19: 1601-1608.
76. Wardle J, Steptoe A, Oliver G, Lipsey Z (2000). Stress, dietary restraint and food intake. J Psychosom Res 48: 195-202.
77. Waters A, Hill A, Waller G (2001). Internal and external antecedents of binge eating episodes in a group of women with bulimia nervosa. Int J Eat Disord 29: 17-22.
78. Wilfley DE, Crow SJ, Hudson JI, Mitchell JE, Berkowitz RI, Blakesley V et al (2008). Sibutramine eating disorder research group. Efficacy of sibutramine for the treatment of binge eating disorder: a randomized multicenter placebo-controlled doubleblind study. Am J Psychiatry 165: 51-58.
79. Willie JT, Chemelli RM, Sinton CM, Yanagisawa M (2001). To eat or to sleep? Orexin in the regulation of feeding and wakefulness. Annu Rev Neurosci 24: 429-458.
80. Wolff GE, Crosby RD, Roberts JA, Wittrock DA (2000). Differences in daily stress, mood, coping, and eating behavior in binge eating and nonbinge eating college women. Addict Behav 25: 205-216.
81. Zheng H, Patterson LM, Berthoud HR (2007). Orexin signaling in the ventral tegmental area is required for high-fat appetite induced by opioid stimulation of the nucleus accumbens. J Neurosci 27: 11075-11082.