Central ghrelin signaling mediates the metabolic response of C57BL/6 male mice to chronic social defeat stress

Endocrinology

Volumn 154, Issue 3, 2013, Pages 1080-1091

  Patterson, Z R ^a   Khazall, R ^a   MacKay, H ^a   Anisman, H ^a   Abizaid, A ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AGOUTI PROTEIN; HISTIDYL DEXTRO TRYPTOPHYLALANYLTRYPTOPHYL DEXTRO PHENYLALANYLLYSINAMIDE; NEUROPEPTIDE Y;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CALORIC INTAKE; CHRONIC STRESS; CONTROLLED STUDY; DISEASE ASSOCIATION; HORMONE METABOLISM; HYPERINSULINEMIA; HYPERLEPTINEMIA; LIPID STORAGE; LONG TERM EXPOSURE; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOCIAL STRESS; WEIGHT GAIN; WILD TYPE;

ADIPOSE TISSUE, BROWN; AGING; ANIMALS; BEHAVIOR, ANIMAL; ENERGY INTAKE; GHRELIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; OBESITY; RECEPTORS, GHRELIN; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL; WEIGHT GAIN;

EID: 84874614457     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1834     Document Type: Article

References (62)

1. McEwen BS. Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol Rev. 2007;87:873-904.
2. Ulrich-Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci. 2009;10:397-409.
3. Di S, Malcher-Lopes R, Halmos KC, Tasker JG. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: A fast feedback mechanism. J Neurosci. 2003;23:4850-4857.
4. Di S, Malcher-Lopes R, Marcheselli VL, Bazan NG, Tasker JG. Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and α-aminobutyric acid inputs to hypothalamic magnocellular neurons. Endocrinology. 2005;146: 4292-4301.
5. Jones MT, Hillhouse EW, Burden JL. Structure-activity relationships of corticosteroid feedback at the hypothalamic level. J Endocrinol. 1977;74:415-424.
6. Sapolsky RM, Krey LC, McEwen BS. Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. Proc Natl Acad Sci U S A. 1984;81:6174-6177.
7. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 2000;21:55-89.
8. Diorio D, Viau V, Meaney MJ. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitaryadrenal responses to stress. J Neurosci. 1993;13:3839-3847.
9. Radley JJ, Williams B, Sawchenko PE. Noradrenergic innervation of the dorsal medial prefrontal cortex modulates hypothalamo-pituitary-adrenal responses to acute emotional stress. J Neurosci. 2008; 28:5806-5816.
10. Cole MA, Kim PJ, Kalman BA, Spencer RL. Dexamethasone suppression of corticosteroid secretion: Evaluation of the site of action by receptor measures and functional studies. Psychoneuroendocrinology. 2000;25:151-167.
11. Mahmoud SN, Scaccianoce S, Scraggs PR, Nicholson SA, Gillham B, Jones MT. Characteristics of corticosteroid inhibition of adrenocorticotrophin release from the anterior pituitary gland of the rat. J Endocrinol. 1984;102:33-42.
12. Frasure-Smith N, Lesperance F. Reflections on depression as a cardiac risk factor. Psychosom Med. 2005;67(suppl)1:S19-S25.
13. Black PH. The inflammatory consequences of psychologic stress: Relationship to insulin resistance, obesity, atherosclerosis and diabetes mellitus, type II. Med Hypotheses. 2006;67:879-891.
14. Boudaba C, Szabo K, Tasker JG. Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J Neurosci. 1996;16:7151-7160.
15. Herman JP, Tasker JG, Ziegler DR, Cullinan WE. Local circuit regulation of paraventricular nucleus stress integration: Glutamate-GABAconnections. Pharmacol Biochem Behav. 2002;71:457-468.
16. Dornonville de la Cour C, Bjorkqvist M, Sandvik AK, et al. A-like cells in the rat stomach contain ghrelin and do not operate under gastrin control. Regul Pept. 2001;99:141-150.
17. Nakazato M, Murakami N, Date Y, et al. A role for ghrelin in the central regulation of feeding. Nature. 2001;409:194-198.
18. Date Y, Shimbara T, Koda S, et al. Peripheral ghrelin transmits orexigenic signals through the noradrenergic pathway from the hindbrain to the hypothalamus. Cell Metab. 2006;4:323-331.
19. Tschop M, Smiley DL, Heiman ML. Ghrelin induces adiposity in rodents. Nature. 2000;407:908-913.
20. Theander-Carrillo C, Wiedmer P, Cettour-Rose P, et al. Ghrelin action in the brain controls adipocyte metabolism. J Clin Invest. 2006;116:1983-1993.
21. Delhanty PJ, Sun Y, Visser JA, et al. Unacylated ghrelin rapidly modulates lipogenic and insulin signaling pathway gene expression in metabolically active tissues of GHSR deleted mice. PLoS One. 2010;5:e11749.
22. Currie PJ, Mirza A, Fuld R, Park D, Vasselli Jr. Ghrelin is an orexigenic and metabolic signaling peptide in the arcuate and paraventricular nuclei.AmJ Physiol Regul Integr Comp Physiol. 2005;289: R353-R358.
23. Howard AD, Feighner SD, Cully DF, et al. A receptor in pituitary and hypothalamus that functions in growth hormone release. Science. 1996;273:974-977.
24. Kirchner H, Gutierrez JA, Solenberg PJ, et al. GOAT links dietary lipids with the endocrine control of energy balance. Nat Med. 2009; 15:741-745.
25. Asakawa A, Inui A, Kaga T, et al.Arole of ghrelin in neuroendocrine and behavioral responses to stress in mice. Neuroendocrinology. 2001;74:143-147.
26. Kristenssson E, Sundqvist M, Astin M, et al. Acute psychological stress raises plasma ghrelin in the rat. Regul Pept. 2006;134:114-117.
27. Ochi M, Tominaga K, Tanaka F, et al. Effect of chronic stress on gastric emptying and plasma ghrelin levels in rats. Life Sci. 2008; 82:862-868.
28. Zheng J, Dobner A, Babygirija R, Ludwig K, Takahashi T. Effects of repeated restraint stress on gastric motility in rats. Am J Physiol Regul Integr Comp Physiol. 2009;296:R1358-R1365.
29. Pfluger PT, Kirchner H, Gunnel S, et al. Simultaneous deletion of ghrelin and its receptor increases motor activity and energy expenditure. Am J Physiol Gastrointest Liver Physiol. 2008;294:G610-G618.
30. Bartolomucci A, Pederzani T, Sacerdote P, Panerai AE, Parmigiani S, Palanza P. Behavioral and physiological characterization of male mice under chronic psychosocial stress. Psychoneuroendocrinology. 2004;29:899-910.
31. Bartolomucci A, Cabassi A, Govoni P, et al. Metabolic consequences and vulnerability to diet-induced obesity in male mice under chronic social stress. PLoS One. 2009;4:e4331.
32. Paxinos G, Franklin, KBG. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA; Academic Press; 1997
33. Palkovits M. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res. 1973;59:449-450.
34. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3:1101-1108.
35. Chuang JC, Cui H, Mason BL, et al. Chronic social defeat stress disrupts regulation of lipid synthesis. J Lipid Res. 2010;51:1344-1353.
36. Chuang JC, Perello M, Sakata I, et al. Ghrelin mediates stress-induced food-reward behavior in mice. J Clin Invest. 2011;121:2684-2692.
37. Chuang JC, Krishnan V, Yu HG, et al. A β(3)-adrenergic- leptinmelanocortin circuit regulates behavioral and metabolic changes induced by chronic stress. Biol Psychiatry. 2010;67(11):1075- 1082.
38. Tamashiro KL, Hegeman MA, Nguyen MM, et al. Dynamic body weight and body composition changes in response to subordination stress. Physiol Behav. 2007;91:440-448.
39. Foster MT, Solomon MB, Huhman KL, Bartness TJ. Social defeat increases food intake, body mass, and adiposity in Syrian hamsters. Am J Physiol Regul Integr Comp Physiol. 2006;290:R1284-R1293.
40. Schmidt MV, Czisch M, Sterlemann V, Reinel C, Samann P, Muller MB. Chronic social stress during adolescence in mice alters fat distribution in late life: Prevention by antidepressant treatment. Stress. 2009;12:89-94.
41. Lin L, Saha PK, Ma X, et al. Ablation of ghrelin receptor reduces adiposity and improves insulin sensitivity during aging by regulating fat metabolism in white and brown adipose tissues. Aging Cell. 2011;10:996-1010.
42. Spencer SJ, Xu L, Clarke MA, et al. Ghrelin regulates the hypothalamic-pituitary-adrenal axis and restricts anxiety after acute stress. Biol Psychiatry. 2012;72:457-465.
43. Schmid DA, Held K, Ising M, Uhr M, Weikel JC, Steiger A. Ghrelin stimulates appetite, imagination of food, GH, ACTH, and cortisol, but does not affect leptin in normal controls. Neuropsychopharmacology. 2005;30:1187-1192.
44. Tassone F, Broglio F, Destefanis S, et al. Neuroendocrine and metabolic effects of acute ghrelin administration in human obesity. J Clin Endocrinol Metab. 2003;88:5478-5483.
45. Lutter M, Sakata I, Osborne-Lawrence S, et al. The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nat Neurosci. 2008;11:752-753.
46. Alvarez-Crespo M, Skibicka KP, Farkas I, et al. The amygdala as a neurobiological target for ghrelin in rats: Neuroanatomical, electrophysiological and behavioral evidence. PLoS One. 2012;7:e46321.
47. Kanehisa M, Akiyoshi J, Kitaichi T, et al. Administration of antisense DNA for ghrelin causes an antidepressant and anxiolytic response in rats. Prog Neuropsychopharmacol Biol Psychiatry. 2006; 30:1403-1407.
48. Kanoski SE, Fortin SM, Ricks KM, Grill HJ. Ghrelin signaling in the ventral hippocampus stimulates learned and motivational aspects of feeding via PI3K-Akt signaling [published online ahead of print August 13, 2012]. Biol Psychiatry. doi: 10.1016/j.biopsych. 2012.07.002
49. Patterson ZR, Ducharme R, Anisman H, Abizaid A. Altered metabolic and neurochemical responses to chronic unpredictable stressors in ghrelin receptor-deficient mice. Eur J Neurosci. 2010;32(4): 632-639.
50. 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;494:528-548.
51. Faulconbridge LF, Cummings DE, Kaplan JM, Grill HJ. Hyperphagic effects of brainstem ghrelin administration. Diabetes. 2003;52:2260-2265.
52. Currie PJ, Khelemsky R, Rigsbee EM, et al. Ghrelin is an orexigenic peptide and elicits anxiety-like behaviors following administration into discrete regions of the hypothalamus. Behav Brain Res. 2012; 226:96-105.
53. Abizaid A, Liu Z, Andrews Z. Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest. 2006;116(12):3229-3239.
54. Razzoli M, Domenici E, Carboni L, et al. A role for BDNF/TrkB signaling in behavioral and physiological consequences of social defeat stress. Genes Brain Behav. 2011;10:424-433.
55. Perello M, Sakata I, Birnbaum S, et al. Ghrelin increases the rewarding value of high-fat diet in an orexin-dependent manner. Biol Psychiatry. 2010;67:880-886.
56. 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.
57. King SJ, Isaacs AM, O'Farrell E, Abizaid A. Motivation to obtain preferred foods is enhanced by ghrelin in the ventral tegmental area. Horm Behav. 2011;60:572-580.
58. Chao H, Digruccio M, Chen P, Li C. Type 2 corticotropin-releasing factor receptor in the ventromedial nucleus of hypothalamus is critical in regulating feeding and lipid metabolism in white adipose tissue. Endocrinology. 2012;153:166-176.
59. Scott MM, Perello M, Chuang JC, et al. Hindbrain ghrelin receptor signaling is sufficient to maintain fasting glucose. PLoS One. 2012; 7:e44089.
60. Depoortere I, Thijs T, Peeters T. The contractile effect of the ghrelin receptor antagonist, D-Lys3-GHRP-6, in rat fundic strips is mediated through5-HTreceptors. Eur J Pharmacol. 2006;537:160-165.
61. Patel K, Dixit VD, Lee JH, et al. Identification of ghrelin receptor blocker, D-[Lys3] GHRP-6 as a CXCR4 receptor antagonist. Int J Biol Sci. 2012;8:108-117.
62. Anisman H, Matheson K. Stress, depression, and anhedonia: Caveats concerning animal models. Neurosci Biobehav Rev. 2005;29:525- 546.