Ghrelin mediates stress-induced food-reward behavior in mice

Journal of Clinical Investigation

Volumn 121, Issue 7, 2011, Pages 2684-2692

  Chuang, Jen Chieh ^a   Perello, Mario ^a   Sakata, Ichiro ^a   Osborne Lawrence, Sherri ^a   Savitt, Joseph M ^b   Lutter, Michael ^a,c   Zigman, Jeffrey M ^a,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GHRELIN; GHRELIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CATECHOLAMINE NERVE CELL; CONTROLLED STUDY; FOOD; FOOD REWARD BEHAVIOR; LIPID DIET; MAJOR DEPRESSION; MALE; MENTAL STRESS; MOUSE; NONHUMAN; PLACE PREFERENCE; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; REWARD;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); EATING; FEEDING BEHAVIOR; FOOD; GHRELIN; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; RECEPTORS, GHRELIN; REWARD; SOCIAL DOMINANCE; STRESS, PSYCHOLOGICAL;

EID: 79959997891     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI57660     Document Type: Article

References (71)

1. Oliver G, Wardle J. Perceived effects of stress on food choice. Physiol Behav. 1999;66(3):511-515. (Pubitemid 29219448)
2. Gibson EL. Emotional influences on food choice: sensory, physiological and psychological pathways. Physiol Behav. 2006;89(1):53-61.
3. Dallman MF. Stress-induced obesity and the emotional nervous system. Trends Endocrinol Metab. 2010;21(3):159-165.
4. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th Ed., Text Revision. Washington, DC, USA: American Psychiatric Association; 2000.
5. Novick JS, et al. Clinical and demographic features of atypical depression in outpatients with major depressive disorder: preliminary findings from STAR*D. J Clin Psychiatry. 2005;66(8):1002-1011. (Pubitemid 41191792)
6. Richardson LP, et al. A longitudinal evaluation of adolescent depression and adult obesity. Arch Pediatr Adolesc Med. 2003;157(8):739-745. (Pubitemid 36988004)
7. Vieweg WV, et al. Posttraumatic stress disorder and body mass index in military veterans. Preliminary findings. Prog Neuropsychopharmacol Biol Psychiatry. 2006;30(6):1150-1154. (Pubitemid 44202363)
8. Pecoraro N, Reyes F, Gomez F, Bhargava A, Dallman MF. Chronic stress promotes palatable feeding, which reduces signs of stress: feedforward and feedback effects of chronic stress. Endocrinology. 2004;145(8):3754-3762. (Pubitemid 39037562)
9. Melhorn SJ, et al. Meal patterns and hypothalamic NPY expression during chronic social stress and recovery. Am J Physiol Regul Integr Comp Physiol. 2010; 299(3):R813-R822.
10. Pankevich DE, Teegarden SL, Hedin AD, Jensen CL, Bale TL. Caloric restriction experience reprograms stress and orexigenic pathways and promotes binge eating. J Neurosci. 2010;30(48):16399-16407.
11. Teegarden SL, Bale TL. Effects of stress on dietary preference and intake are dependent on access and stress sensitivity. Physiol Behav. 2008; 93(4-5):713-723. (Pubitemid 351381069)
12. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature. 1999;402(6762):656-660. (Pubitemid 129516334)
13. Sakata I, et al. Characterization of a novel ghrelin cell reporter mouse. Regul Pept. 2009;155(1-3):91-98.
14. Sakata I, et al. Ghrelin-producing cells exist as two types of cells, closed- and opened-type cells, in the rat gastrointestinal tract. Peptides. 2002;23(3):531-536. (Pubitemid 34143270)
15. Dornonville de la Cour C, et al. A-like cells in the rat stomach contain ghrelin and do not operate under gastrin control. Regul Pept. 2001;99(2-3):141-150.
16. Nakazato M, et al. A role for ghrelin in the central regulation of feeding. Nature. 2001;409(6817):194-198. (Pubitemid 32144284)
17. Tschop M, Smiley DL, Heiman ML. Ghrelin induces adiposity in rodents. Nature. 2000; 407(6806):908-913.
18. Wren AM, et al. Ghrelin enhances appetite and increases food intake in humans. J Clin Endocrinol Metab. 2001;86(12):5992.
19. Disse E, et al. Peripheral ghrelin enhances sweet taste food consumption and preference, regardless of its caloric content. Physiol Behav. 2010;101(2):277-281.
20. Egecioglu E, et al. Ghrelin increases intake of rewarding food in rodents. Addict Biol. 2010;15(3):304-311.
21. Perello M, et al. Ghrelin increases the rewarding value of high-fat diet in an orexin-dependent manner. Biol Psychiatry. 2010;67(9):880-886.
22. Shimbara T, et al. Central administration of ghrelin preferentially enhances fat ingestion. Neurosci Lett. 2004;369(1):75-79. (Pubitemid 39369506)
23. Disse E, et al. Systemic ghrelin and reward: effect of cholinergic blockade. Physiol Behav. 2011; 102(5):481-484.
24. Skibicka KP, Hansson C, Egecioglu E, Dickson SL. Role of ghrelin in food reward: impact of ghrelin on sucrose self-administration and mesolimbic dopamine and acetylcholine receptor gene expression [published online ahead of print February 11, 2011]. Addict Biol. doi:10.1111/j.1369-1600.2010.00294.x.
25. Malik S, McGlone F, Bedrossian D, Dagher A. Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab. 2008;7(5):400-409. (Pubitemid 351598026)
26. Lutter M, et al. The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nat Neurosci. 2008;11(7):752-753. (Pubitemid 351896679)
27. Asakawa A, et al. A role of ghrelin in neuroendocrine and behavioral responses to stress in mice. Neuroendocrinology. 2001;74(3):143-147. (Pubitemid 32786213)
28. Kristenssson E, et al. Acute psychological stress raises plasma ghrelin in the rat. Regul Pept. 2006;134(2-3):114-117.
29. Ochi M, et al. Effect of chronic stress on gastric emptying and plasma ghrelin levels in rats. Life Sci. 2008;82(15-16):862-868.
30. Rouach V, et al. The acute ghrelin response to a psychological stress challenge does not predict the post-stress urge to eat. Psychoneuroendocrinology. 2007;32(6):693-702. (Pubitemid 47017588)
31. Chuang JC, Zigman JM. Ghrelin's roles in stress, mood, and anxiety regulation. Int J Pept. 2010;2010(pii):460549.
32. Berton O, et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science. 2006;311(5762):864-868. (Pubitemid 43228853)
33. Nestler EJ, Hyman SE. Animal models of neuropsychiatric disorders. Nat Neurosci. 2010;13(10):1161-1169.
34. Chuang JC, et al. Chronic social defeat stress disrupts regulation of lipid synthesis. J Lipid Res. 2010;51(6):1344-1353.
35. Chuang JC, et al. A beta3-adrenergic-leptin-melanocortin circuit regulates behavioral and metabolic changes induced by chronic stress. Biol Psychiatry. 2010;67(11):1075-1082.
36. Abizaid A, et al. Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest. 2006;116(12):3229-3239. (Pubitemid 44878637)
37. Zigman JM, Jones JE, Lee CE, Saper CB, Elmquist JK. Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol. 2006;494(3):528-548. (Pubitemid 41791000)
38. Nestler EJ, Carlezon WA Jr. The mesolimbic dopamine reward circuit in depression. Biol Psychiatry. 2006;59(12):1151-1159. (Pubitemid 44192421)
39. Krishnan V, et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell. 2007;131(2):391-404. (Pubitemid 47576141)
40. Jerlhag E, Egecioglu E, Dickson SL, Douhan A, Svensson L, Engel JA. Ghrelin administration into tegmental areas stimulates locomotor activity and increases extracellular concentration of dopamine in the nucleus accumbens. Addict Biol. 2007;12(1):6-16. (Pubitemid 46405994)
41. Jerlhag E, Egecioglu E, Dickson SL, Andersson M, Svensson L, Engel JA. Ghrelin stimulates locomotor activity and accumbal dopamine-overflow via central cholinergic systems in mice: implications for its involvement in brain reward. Addict Biol. 2006;11(1):45-54. (Pubitemid 46696736)
42. Naleid AM, Grace MK, Cummings DE, Levine AS. Ghrelin induces feeding in the mesolimbic reward pathway between the ventral tegmental area and the nucleus accumbens. Peptides. 2005;26(11):2274-2279. (Pubitemid 41584095)
43. Skibicka KP, Hansson C, Alvarez-Crespo M, Friberg PA, Dickson SL. Ghrelin directly targets the ventral tegmental area to increase food motivation. Neuroscience. 2011;180:129-137.
44. Shuto Y, et al. Hypothalamic growth hormone secretagogue receptor regulates growth hormone secretion, feeding, and adiposity. J Clin Invest. 2002;109(11):1429-1436. (Pubitemid 34596168)
45. Zigman JM, et al. Mice lacking ghrelin receptors resist the development of diet-induced obesity. J Clin Invest. 2005;115(12):3564-3572. (Pubitemid 43121844)
46. Savitt JM, Jang SS, Mu W, Dawson VL, Dawson TM. Bcl-x is required for proper development of the mouse substantia nigra. J Neurosci. 2005;25(29):6721-6728. (Pubitemid 41023139)
47. Andrews ZB, et al. Ghrelin promotes and protects nigrostriatal dopamine function via a UCP2-dependent mitochondrial mechanism. J Neurosci. 2009;29(45):14057-14065.
48. Willesen MG, Kristensen P, Romer J. Co-localization of growth hormone secretagogue receptor and NPY mRNA in the arcuate nucleus of the rat. Neuroendocrinology. 1999;70(5):306-316.
49. Hokfelt T, Martensson R, Bjorklund A, Kleinau S, Goldstein M. Distributional maps of tyrosine-hydroxylase-immunoreactive neurons in the rat brain. In: Bjorklund A, Hokfelt T, eds. Handbook of Chemical Neuroanatomy. Vol 2: Classical Transmitters in the CNS, Part I. Amsterdam, The Netherlands: Elsevier Science Publishers B.V.; 1984:277-379.
50. Longo KA, et al. Improved insulin sensitivity and metabolic flexibility in ghrelin receptor knockout mice. Regul Pept. 2008;150(1-3):55-61.
51. Zhao TJ, et al. Ghrelin secretion stimulated by {beta}1-adrenergic receptors in cultured ghrelinoma cells and in fasted mice. Proc Natl Acad Sci U S A. 2010;107(36):15868-15873.
52. Mundinger TO, Cummings DE, Taborsky GJ Jr. Direct stimulation of ghrelin secretion by sympathetic nerves. Endocrinology. 2006;147(6):2893-2901. (Pubitemid 43764624)
53. Sgoifo A, et al. Social stress, autonomic neural activation, and cardiac activity in rats. Neurosci Biobehav Rev. 1999;23(7):915-923. (Pubitemid 29502397)
54. Barnes TD, Kubota Y, Hu D, Jin DZ, Graybiel AM. Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature. 2005;437(7062):1158-1161. (Pubitemid 41509353)
55. Mohankumar SM, et al. Chronic estradiol exposure induces oxidative stress in the hypothalamus to decrease hypothalamic dopamine and cause hyperprolactinemia. Am J Physiol Regul Integr Comp Physiol. 2011;300(3):R693- R699.
56. Cooper ML, Russell M, Frone MR. Work stress and alcohol effects: a test of stress-induced drinking. J Health Soc Behav. 1990;31(3):260-276. (Pubitemid 20308733)
57. Kandel DB, et al. Psychiatric disorders associated with substance use among children and adolescents: findings from the Methods for the Epidemiology of Child and Adolescent Mental Disorders (MECA) Study. J Abnorm Child Psychol. 1997;25(2):121-132. (Pubitemid 27169355)
58. King CA, Ghaziuddin N, McGovern L, Brand E, Hill E, Naylor M. Predictors of comorbid alcohol and substance abuse in depressed adolescents. J Am Acad Child Adolesc Psychiatry. 1996;35(6):743-751. (Pubitemid 26174608)
59. Reed PL, Anthony JC, Breslau N. Incidence of drug problems in young adults exposed to trauma and posttraumatic stress disorder: do early life experiences and predispositions matter? Arch Gen Psychiatry. 2007;64(12):1435-1442. (Pubitemid 350223562)
60. Breslau N, Davis GC, Schultz LR. Posttraumatic stress disorder and the incidence of nicotine, alcohol, and other drug disorders in persons who have experienced trauma. Arch Gen Psychiatry. 2003; 60(3):289-294. (Pubitemid 36307440)
61. Sinha R. The role of stress in addiction relapse. Curr Psychiatry Rep. 2007;9(5):388-395. (Pubitemid 47559360)
62. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J. The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl). 2003;168(1-2):3-20. (Pubitemid 36851158)
63. Sanchez CJ, Sorg BA. Conditioned fear stimuli reinstate cocaine-induced conditioned place preference. Brain Res. 2001;908(1):86-92. (Pubitemid 32703664)
64. Addolorato G, et al. Relationship between ghrelin levels, alcohol craving, and nutritional status in current alcoholic patients. Alcohol Clin Exp Res. 2006;30(11):1933-1937. (Pubitemid 44630097)
65. Jerlhag E, et al. Requirement of central ghrelin signaling for alcohol reward. Proc Natl Acad Sci U S A. 2009;106(27):11318-11323.
66. Jerlhag E, Egecioglu E, Dickson SL, Engel JA. Ghrelin receptor antagonism attenuates cocaine- and amphetamine-induced locomotor stimulation, accumbal dopamine release, and conditioned place preference. Psychopharmacology (Berl). 2010;211(4):415-422.
67. Tessari M, et al. Correlation between serum ghrelin levels and cocaine-seeking behaviour triggered by cocaine-associated conditioned stimuli in rats. Addict Biol. 2007;12(1):22-29. (Pubitemid 46406004)
68. Davis KW, Wellman PJ, Clifford PS. Augmented cocaine conditioned place preference in rats pretreated with systemic ghrelin. Regul Pept. 2007;140(3):148-152. (Pubitemid 46418913)
69. Wellman PJ, Davis KW, Nation JR. Augmentation of cocaine hyperactivity in rats by systemic ghrelin. Regul Pept. 2005;125(1-3):151-154. (Pubitemid 39593719)
70. Jerlhag E, Engel JA. Ghrelin receptor antagonism attenuates nicotine-induced locomotor stimulation, accumbal dopamine release and conditioned place preference in mice [published online ahead of print February 8, 2011]. Drug Alcohol Depend. doi:10.1016/j.drugalcdep.2011.01.010.
71. Kurrasch DM, Huang J, Wilkie TM, Repa JJ. Quantitative real-time polymerase chain reaction measurement of regulators of G-protein signaling mRNA levels in mouse tissues. Methods Enzymol. 2004;389:3-15. (Pubitemid 39119058)