Rev-erbα modulates the hypothalamic orexinergic system to influence pleasurable feeding behaviour in mice

Addiction Biology

Volumn 22, Issue 2, 2017, Pages 411-422

  Feillet, Céline A ^b   Bainier, Claire ^a   Mateo, Maria ^a   Blancas Velázquez, Aurea ^a   Salaberry, Nora L ^a   Ripperger, Jürgen A ^b   Albrecht, Urs ^b   Mendoza, Jorge ^a  

^a Institut des Neurosciences Cellulaires et Intégratives UPR3212   (France)

^b UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

circadian; compulsive; food reward; orexin; palatable; Rev Erb

Indexed keywords

1 (2 METHYL 6 BENZOXAZOLYL) 3 (1,5 NAPHTHYRIDIN 4 YL)UREA; NUCLEAR RECEPTOR NR1D1; OREXIN; NR1D1 PROTEIN, MOUSE; OREXIN RECEPTOR; OREXIN RECEPTOR ANTAGONIST;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CATECHOLAMINERGIC SYSTEM; CONTROLLED STUDY; DRUG EFFECT; FEEDING BEHAVIOR; FOOD INTAKE; FOOD PREFERENCE; HYPOTHALAMUS; IN VITRO STUDY; IN VIVO STUDY; MALE; MOTIVATION; MOUSE; NONHUMAN; OREXINERGIC SYSTEM; ORX GENE; PALATABILITY; PLEASURE; PROMOTER REGION; PROTEIN EXPRESSION; REWARD; SIGNAL TRANSDUCTION; ANIMAL; CIRCADIAN RHYTHM; DRUG EFFECTS; EATING; GENETICS; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; CIRCADIAN RHYTHM; EATING; FEEDING BEHAVIOR; HYPOTHALAMUS; MALE; MICE; MICE, KNOCKOUT; NEURONS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; OREXIN RECEPTOR ANTAGONISTS; OREXIN RECEPTORS; OREXINS; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION;

EID: 84949667792     PISSN: 13556215     EISSN: 13691600     Source Type: Journal    
DOI: 10.1111/adb.12339     Document Type: Article

References (50)

1. Abarca C, Albrecht U, Spanagel R (2002) Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc Natl Acad Sci U S A 99:9026–9030.
2. Akiyama M, Yuasa T, Hayasaka N, Horikawa K, Sakurai T, Shibata S (2004) Reduced food anticipatory activity in genetically orexin (hypocretin) neuron-ablated mice. Eur J Neurosci 20:3054–3062.
3. Alcaraz-Iborra M, Carvajal F, Lerma-Cabrera JM, Valor LM, Cubero I (2014) Binge-like consumption of caloric and non-caloric palatable substances in ad libitum-fed C57BL/6 J mice: pharmacological and molecular evidence of orexin involvement. Behav Brain Res 272:93–99.
4. Avena NM, Bocarsly ME, Hoebel BG (2012) Animal models of sugar and fat bingeing: relationship to food addiction and increased body weight. Methods Mol Biol 829:351–365.
5. Baird JP, Choe A, Loveland JL, Beck J, Mahoney CE, Lord JS, Grigg LA (2009) Orexin-A hyperphagia: hindbrain participation in consummatory feeding responses. Endocrinology 150:1202–1216.
6. Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330:1349–1354.
7. Berridge KC, Ho CY, Richard JM, DiFeliceantonio AG (2010) The tempted brain eats: pleasure and desire circuits in obesity and eating disorders. Brain Res 1350:43–64.
8. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev 28:309–369.
9. 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.
10. 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.
11. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, Ditacchio L, Atkins AR, Glass CK, Liddle C, Auwerx J, Downes M, Panda S, Evans RM (2012) Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 485:123–127.
12. Choi DL, Davis JF, Fitzgerald ME, Benoit SC (2010) The role of orexin-A in food motivation, reward-based feeding behavior and food-induced neuronal activation in rats. Neuroscience 167:11–20.
13. Chung S, Lee EJ, Yun S, Choe HK, Park SB, Son HJ, Kim KS, Dluzen DE, Lee I, Hwang O, Son GH, Kim K (2014) Impact of circadian nuclear receptor REV-ERBα on midbrain dopamine production and mood regulation. Cell 157:858–868.
14. Clegg DJ, Air EL, Woods SC, Seeley RJ (2002) Eating elicited by orexin-a, but not melanin-concentrating hormone, is opioid mediated. Endocrinology 143:2995–3000.
15. Deboer T, Overeem S, Visser NA, Duindam H, Frölich M, Lammers GJ, Meijer JH (2004) Convergence of circadian and sleep regulatory mechanisms on hypocretin-1. Neuroscience 129:727–732.
16. Delezie J, Dumont S, Dardente H, Oudart H, Gréchez-Cassiau A, Klosen P, Teboul M, Delaunay F, Pévet P, Challet E (2012) The nuclear receptor REV-ERBα is required for the daily balance of carbohydrate and lipid metabolism. FASEB J 26:3321–3335.
17. Everett LJ, Lazar MA (2014) Nuclear receptor Rev-erbα: up, down, and all around. Trends Endocrinol Metab 25:586–592.
18. Fadel J, Deutch AY (2002) Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience 111:379–387.
19. Gondard E, Anaclet C, Akaoka H, Guo RX, Zhang M, Buda C, Franco P, Kotani H, Lin JS (2013) Enhanced histaminergic neurotransmission and sleep-wake alterations, a study in histamine H3-recpetor knock-out mice. Neuropsychopharmachology 38:1015–1031.
20. Hampp G, Ripperger JA, Houben T, Schmutz I, Blex C, Perreau-Lenz S, Brunk I, Spanagel R, Ahnert-Hilger G, Meijer JH, Albrecht U (2008) Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr Biol 18:678–683.
21. Harris GC, Wimmer M, Aston-Jones G (2005) A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437:556–559.
22. Holtz NA, Zlebnik NE, Caroll ME (2012) Differential orexin/hypocretin expression in addiction-prone and-resistant rats selectively bred for high (HiS) and low (LoS) saccharin intake. Neurosci Lett 522:12–15.
23. Jager J, O'Brien WT, Manlove J, Krizman EN, Fang B, Gerhart-Hines Z, Robinson MB, Klein PS, Lazar MA (2014) Behavioral changes and dopaminergic dysregulation in mice lacking the nuclear receptor Rev-erbα. Mol Endocrinol 28:490–498.
24. Kelley AE, Baldo BA, Pratt WE, Will MJ (2005) Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav 86:773–795.
25. Lenoir M, Serre F, Cantin L, Ahmed SH (2007) Intense sweetness surpasses cocaine reward. PLoS One 2:e698.
26. Lewis SR, Ahmed S, Dym C, Khaimova E, Kest B, Bodnar RJ (2005) Inbred mouse strain survey of sucrose intake. Physiol Behav 85:546–556.
27. Liu L, Duff K (2008) A technique for serial collection of cerebrospinal fluid from the cisterna magna in mouse. JoVE 21:DOI: 10.3791/960.
28. Logan RW, Williams WP 3rd, McClung CA (2014) Circadian rhythms and addiction: mechanistic insights and future directions. Behav Neurosci 128:387–412.
29. Mahler SV, Moorman DE, Smith RJ, James MH, Aston-Jones G (2014) Motivational activation: a unifying hypothesis of orexin/hypocretin function. Nat Neurosci 17:1298–1303.
30. Matsuo E, Mochizuki A, Nakayama K, Nakamura S, Yamamoto T, Shioda S, Sakurai T, Yanagisawa M, Shiuchi T, Minokoshi Y, Inoue T (2011) Decreased intake of sucrose solutions in orexin knockout mice. J Mol Neurosci 43:217–224.
31. McClung CA, Sidiropoulou K, Vitaterna M, Takahashi JS, White FJ, Cooper DC, Nestler EJ (2005) Regulation of dopaminergic transmission and cocaine reward by the Clock gene. Proc Natl Acad Sci U S A 102:9377–9381.
32. Mendoza J, Clesse D, Pévet P, Challet E (2010) Food-reward signalling in the suprachiasmatic clock. J Neurochem 112:1489–1499.
33. Mieda M, Williams SC, Sinton CM, Richardson JA, Sakurai T, Yanagisawa M (2004) Orexin neurons function in an efferent pathway of a food-entrainable circadian oscillator in eliciting food-anticipatory activity and wakefulness. J Neurosci 24:10493–10501.
34. 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.
35. Nieh EH, Matthews GA, Allsop SA, Presbrey KN, Leppla CA, Wichmann R, Neve R, Wildes CP, Tye KM (2015) Decoding neural circuits that control compulsive sucrose seeking. Cell 160:528–541.
36. Paxinos G, Franklin KBJ (2001) The Mouse Brain in Stereotaxic Coordinates, Second edn. Academic Press: San Diego.
37. Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecth U, Schibler U (2002) The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110:251–260.
38. Sakurai T (2014) The role of orexin in motivated behaviours. Nat Rev Neurosci 15:719–731.
39. Sakurai T, Mieda M (2011) Connectomics of orexin-producing neurons: interface of systems of emotion, energy homeostasis and arousal. Trends Pharmacol Sci 32:451–462.
40. Sanchis-Segura C, Spanagel R (2006) Behavioural assessment of drug reinforcement and addictive features in rodents: an overview. Addict Biol 11:2–38.
41. Saper CB, Chou TC, Elmquist JK (2002) The need to feed: homeostatic and hedonic control of eating. Neuron 36:199–211.
42. Sharf R, Sarhan M, Brayton CE, Guarnieri DJ, Taylor JR, DiLeone RJ (2010) Orexin signaling via the orexin 1 receptor mediates operant responding for food reinforcement. Biol Psychiatry 67:753–760.
43. Solt LA, Wang Y, Banerjee S, Hughes T, Kojetin DJ, Lundasen T, Shin Y, Liu J, Cameron MD, Noel R, Yoo SH, Takahashi JS, Butler AA, Kamenecka TM, Burris TP (2012) Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 485:62–68.
44. Spanagel R, Pendyala G, Abarca C, Zghoul T, Sanchis-Segura C, Magnone MC, Lascorz J, Depner M, Holzberg D, Soyka M, Schreiber S, Matsuda F, Lathrop M, Schumann G, Albrecht U (2005) The clock gene Per2 influences the glutamatergic system and modulates alcohol consumption. Nat Med 11:35–42.
45. Takahashi JS, Hong HK, Ko CH, McDearmon EL (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 9:764–775.
46. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, Eckel RH, Takahashi JS, Bass J (2005) Obesity and metabolic syndrome in circadian Clock mutant mice. Science 308:1043–1045.
47. Yi CX, Serlie MJ, Ackermans MT, Foppen E, Buijs RM, Sauerwein HP, Fliers E, Kalsbeek A (2009) A major role for perifornical orexin neurons in the control of glucose metabolism in rats. Diabetes 58:1998–2005.
48. Yoshida Y, Fujiki N, Nakajima T, Ripley B, Matsumura H, Yoneda H, Mignot E, Nishino S (2001) Fluctuation of extracellular hypocretin-1 (orexin A) levels in the rat in relation to the light–dark cycle and sleep-wake activities. Eur J Neurosci 14:1075–1081.
49. Zeitzer JM, Buckmaster CL, Parker KJ, Hauck CM, Lyons DM, Mignot E (2003) Circadian and homeostatic regulation of hypocretin in a primate model: implications for the consolidation of wakefulness. J Neurosci 23:3555–3560.
50. Zhang S, Zeitzer JM, Yoshida Y, Wisor JP, Nishino S, Edgar DM, Mignot E (2004) Lesions of the suprachiasmatic nucleus eliminate the daily rhythm of hypocretin-1 release. Sleep 27:619–627.