Ghrelin modulates the fMRI BOLD response of homeostatic and hedonic brain centers regulating energy balance in the rat

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Sárvári, Miklós ^a   Kocsis, Pál ^b   Deli, Levente ^b   Gajári, Dávid ^b   Dávid, Szabolcs ^b   Pozsgay, Zsófia ^b   Hegedus, Nikolett ^b   Tihanyi, Károly ^b   Liposits, Zsolt ^a,c  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b GEDEON RICHTER LTD   (Hungary)

^c PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN PEPTIDE; ENDOCANNABINOID; G PROTEIN COUPLED RECEPTOR; GHRELIN; GHRELIN RECEPTOR; RIMONABANT; CANNABINOID 1 RECEPTOR; ESTRADIOL;

ANIMAL EXPERIMENT; ARTICLE; BOLD SIGNAL; BRAIN; CONTROLLED STUDY; ENERGY BALANCE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HOMEOSTASIS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; LATERAL HYPOTHALAMUS; LIMBIC CORTEX; LIMBIC SYSTEM; MALE; NONHUMAN; NUCLEUS ACCUMBENS; OVARIECTOMY; PREFRONTAL CORTEX; RAT; SUPRACHIASMATIC NUCLEUS; TELENCEPHALON; THALAMUS VENTRAL NUCLEUS; ANIMAL; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; REWARD; SIGNAL TRANSDUCTION; TIME; WISTAR RAT;

ANIMALS; BRAIN; ESTRADIOL; FEEDING BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION; GHRELIN; HOMEOSTASIS; HYPOTHALAMUS; LIMBIC SYSTEM; MAGNETIC RESONANCE IMAGING; MALE; NUCLEUS ACCUMBENS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PREFRONTAL CORTEX; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; REWARD; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; TIME FACTORS;

EID: 84901329458     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097651     Document Type: Article

References (73)

1. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, et al. (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402: 656-660. (Pubitemid 129516334)
2. van der Lely AJ, Tschop M, Heiman ML, Ghigo E (2004) Biological, physiological, pathophysiological, and pharmacological aspects of ghrelin. Endocr Rev 25: 426-457. (Pubitemid 38780667)
3. Howard AD, Feighner SD, Cully DF, Arena JP, Liberator PA, et al. (1996) A receptor in pituitary and hypothalamus that functions in growth hormone release. Science 273: 974-977. (Pubitemid 26275178)
4. 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. (Pubitemid 41791000)
5. Mitchell V, Bouret S, Beauvillain JC, Schilling A, Perret M, et al. (2001) Comparative distribution of mRNA encoding the growth hormone secreta-gogue-receptor (GHS-R) in Microcebus murinus (Primate, lemurian) and rat forebrain and pituitary. J Comp Neurol 429: 469-489. (Pubitemid 32010051)
6. Harrold JA, Dovey T, Cai XJ, Halford JC, Pinkney J (2008) Autoradiographic analysis of ghrelin receptors in the rat hypothalamus. Brain Res 1196: 59-64.
7. Kojima M, Kangawa K (2002) Ghrelin, an orexigenic signaling molecule from the gastrointestinal tract. Curr Opin Pharmacol 2: 665-668. (Pubitemid 35476917)
8. Cowley MA, Smith RG, Diano S, Tschop M, Pronchuk N, et al. (2003) The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 37: 649-661. (Pubitemid 36262986)
9. Horvath TL, Abizaid A, Dietrich MO, Li Y, Takahashi JS, et al. (2012) Ghrelin-immunopositive hypothalamic neurons tie the circadian clock and visual system to the lateral hypothalamic arousal center. Mol Metab 1: 79-85.
10. Menyhert J, Wittmann G, Hrabovszky E, Szlavik N, Keller E, et al. (2006) Distribution of ghrelin-immunoreactive neuronal networks in the human hypothalamus. Brain Res 1125: 31-36. (Pubitemid 44838545)
11. Kojima M, Kangawa K (2005) Ghrelin: structure and function. Physiol Rev 85: 495-522. (Pubitemid 40404635)
12. Kojima M, Kangawa K (2013) Ghrelin discovery: a decade after. Endocr Dev 25: 1-4.
13. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, et al. (2001) A role for ghrelin in the central regulation of feeding. Nature 409: 194-198. (Pubitemid 32144284)
14. Tschop M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407: 908-913.
15. Shuto Y, Shibasaki T, Otagiri A, Kuriyama H, Ohata H, et al. (2002) Hypothalamic growth hormone secretagogue receptor regulates growth hormone secretion, feeding, and adiposity. J Clin Invest 109: 1429-1436. (Pubitemid 34596168)
16. Zigman JM, Nakano Y, Coppari R, Balthasar N, Marcus JN, et al. (2005) Mice lacking ghrelin receptors resist the development of diet-induced obesity. J Clin Invest 115: 3564-3572. (Pubitemid 43121844)
17. Willesen MG, Kristensen P, Romer J (1999) Co-localization of growth hormone secretagogue receptor and NPY mRNA in the arcuate nucleus of the rat. Neuroendocrinology 70: 306-316.
18. Zeltser LM, Seeley RJ, Tschop MH (2012) Synaptic plasticity in neuronal circuits regulating energy balance. Nat Neurosci 15: 1336-1342.
19. Castaneda TR, Tong J, Datta R, Culler M, Tschop MH (2010) Ghrelin in the regulation of body weight and metabolism. Front Neuroendocrinol 31: 44-60.
20. Cummings DE, Naleid AM, Figlewicz Lattemann DP (2007) Ghrelin: a link between energy homeostasis and drug abuse? Addict Biol 12: 1-5. (Pubitemid 46406005)
21. Naleid AM, Grace MK, Cummings DE, Levine AS (2005) Ghrelin induces feeding in the mesolimbic reward pathway between the ventral tegmental area and the nucleus accumbens. Peptides 26: 2274-2279. (Pubitemid 41584095)
22. Dickson SL, Egecioglu E, Landgren S, Skibicka KP, Engel JA, et al. (2011) The role of the central ghrelin system in reward from food and chemical drugs. Mol Cell Endocrinol 340: 80-87.
23. Egecioglu E, Jerlhag E, Salome N, Skibicka KP, Haage D, et al. (2010) Ghrelin increases intake of rewarding food in rodents. Addict Biol 15: 304-311.
24. Jerlhag E, Egecioglu E, Dickson SL, Andersson M, Svensson L, et al. (2006) Ghrelin stimulates locomotor activity and accumbal dopamine-overflow via central cholinergic systems in mice: implications for its involvement in brain reward. Addict Biol 11: 45-54. (Pubitemid 46696736)
25. Menzies JR, Skibicka KP, Leng G, Dickson SL (2013) Ghrelin, reward and motivation. Endocr Dev 25: 101-111.
26. Perello M, Sakata I, Birnbaum S, Chuang JC, Osborne-Lawrence S, et al. (2010) Ghrelin increases the rewarding value of high-fat diet in an orexin-dependent manner. Biol Psychiatry 67: 880-886.
27. Skibicka KP, Hansson C, Egecioglu E, Dickson SL (2012) Role of ghrelin in food reward: impact of ghrelin on sucrose self-administration and mesolimbic dopamine and acetylcholine receptor gene expression. Addict Biol 17: 95-107.
28. Jerlhag E, Egecioglu E, Landgren S, Salome N, Heilig M, et al. (2009) Requirement of central ghrelin signaling for alcohol reward. Proc Natl Acad Sci U S A 106: 11318-11323.
29. Jerlhag E, Egecioglu E, Dickson SL, Engel JA (2010) Ghrelin receptor antagonism attenuates cocaine- and amphetamine-induced locomotor stimulation, accumbal dopamine release, and conditioned place preference. Psychopharmacology (Berl) 211: 415-422.
30. Vengeliene V (2013) The role of ghrelin in drug and natural reward. Addict Biol 18: 897-900.
31. Hansson C, Shirazi RH, Naslund J, Vogel H, Neuber C, et al. (2012) Ghrelin influences novelty seeking behavior in rodents and men. PLoS One 7: e50409.
32. Cardona Cano S, Merkestein M, Skibicka KP, Dickson SL, Adan RA (2012) Role of ghrelin in the pathophysiology of eating disorders: implications for pharmacotherapy. CNS Drugs 26: 281-296.
33. Helmling S, Jarosch F, Klussmann S (2006) The promise of ghrelin antagonism in obesity treatment. Drug News Perspect 19: 13-20.
34. Cowley MA (2003) Hypothalamic melanocortin neurons integrate signals of energy state. Eur J Pharmacol 480: 3-11. (Pubitemid 37410356)
35. Kanoski SE, Fortin SM, Ricks KM, Grill HJ (2013) Ghrelin signaling in the ventral hippocampus stimulates learned and motivational aspects of feeding via PI3K-Akt signaling. Biol Psychiatry 73: 915-923.
36. Kola B, Boscaro M, Rutter GA, Grossman AB, Korbonits M (2006) Expanding role of AMPK in endocrinology. Trends Endocrinol Metab 17: 205-215. (Pubitemid 43974977)
37. Velasquez DA, Martinez G, Romero A, Vazquez MJ, Boit KD, et al. (2011) The central Sirtuin 1/p53 pathway is essential for the orexigenic action of ghrelin. Diabetes 60: 1177-1185.
38. Romero-Pico A, Vazquez MJ, Gonzalez-Touceda D, Folgueira C, Skibicka KP, et al. (2013) Hypothalamic kappa-opioid receptor modulates the orexigenic effect of ghrelin. Neuropsychopharmacology 38: 1296-1307.
39. Kola B, Farkas I, Christ-Crain M, Wittmann G, Lolli F, et al. (2008) The orexigenic effect of ghrelin is mediated through central activation of the endogenous cannabinoid system. PLoS One 3: e1797.
40. Farkas I, Vastagh C, Sarvari M, Liposits Z (2013) Ghrelin decreases firing activity of gonadotropin-releasing hormone (GnRH) neurons in an estrous cycle and endocannabinoid signaling dependent manner. PLoS One 8: e78178.
41. Clegg DJ, Brown LM, Zigman JM, Kemp CJ, Strader AD, et al. (2007) Estradiol-dependent decrease in the orexigenic potency of ghrelin in female rats. Diabetes 56: 1051-1058. (Pubitemid 46525056)
42. Lage R, Vazquez MJ, Varela L, Saha AK, Vidal-Puig A, et al. (2010) Ghrelin effects on neuropeptides in the rat hypothalamus depend on fatty acid metabolism actions on BSX but not on gender. FASEB J 24: 2670-2679.
43. Sarvari M, Hrabovszky E, Kallo I, Solymosi N, Toth K, et al. (2011) Estrogens regulate neuroinflammatory genes via estrogen receptors alpha and beta in the frontal cortex of middle-aged female rats. J Neuroinflammation 8: 82.
44. Watson GPaC (1998) The rat brain in stereotaxic coordinates: Academic Press.
45. Kocsis P, Gajari D, Deli L, Gocze KZ, Pozsgay Z, et al. (2013) Effect of tolperisone on the resting brain and on evoked responses, an phMRI BOLD study. Brain Res Bull 99: 34-40.
46. Seoane LM, Tovar S, Baldelli R, Arvat E, Ghigo E, et al. (2000) Ghrelin elicits a marked stimulatory effect on GH secretion in freely-moving rats. Eur J Endocrinol 143: R7-9.
47. Banks WA, Tschop M, Robinson SM, Heiman ML (2002) Extent and direction of ghrelin transport across the blood-brain barrier is determined by its unique primary structure. J Pharmacol Exp Ther 302: 822-827. (Pubitemid 34787253)
48. Date Y, Toshinai K, Koda S, Miyazato M, Shimbara T, et al. (2005) Peripheral interaction of ghrelin with cholecystokinin on feeding regulation. Endocrinology 146: 3518-3525. (Pubitemid 41058123)
49. Wellman PJ, Clifford PS, Rodriguez JA, Hughes S, Di Francesco C, et al. (2012) Brain reinforcement system function is ghrelin dependent: studies in the rat using pharmacological fMRI and intracranial self-stimulation. Addict Biol 17: 908-919.
50. Kuo YT, Parkinson JR, Chaudhri OB, Herlihy AH, So PW, et al. (2007) The temporal sequence of gut peptide CNS interactions tracked in vivo by magnetic resonance imaging. J Neurosci 27: 12341-12348. (Pubitemid 350085464)
51. Tzschentke TM, Schmidt WJ (2000) Functional relationship among medial prefrontal cortex, nucleus accumbens, and ventral tegmental area in locomotion and reward. Crit Rev Neurobiol 14: 131-142. (Pubitemid 32756782)
52. Oades RD, Halliday GM (1987) Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res 434: 117-165. (Pubitemid 17064083)
53. Dahlstroem A, Fuxe K, Olson L, Ungerstedt U (1964) Ascending Systems of Catecholamine Neurons from the Lower Brain Stem. Acta Physiol Scand 62: 485-486.
54. Abizaid A, Liu ZW, Andrews ZB, Shanabrough M, Borok E, et al. (2006) Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest 116: 3229-3239. (Pubitemid 44878637)
55. Wellman PJ, Hollas CN, Elliott AE (2008) Systemic ghrelin sensitizes cocaine-induced hyperlocomotion in rats. Regul Pept 146: 33-37.
56. Carlini VP, Monzon ME, Varas MM, Cragnolini AB, Schioth HB, et al. (2002) Ghrelin increases anxiety-like behavior and memory retention in rats. Biochem Biophys Res Commun 299: 739-743. (Pubitemid 36034549)
57. Carlini VP, Ghersi M, Schioth HB, de Barioglio SR (2010) Ghrelin and memory: differential effects on acquisition and retrieval. Peptides 31: 1190-1193.
58. Diano S, Farr SA, Benoit SC, McNay EC, da Silva I, et al. (2006) Ghrelin controls hippocampal spine synapse density and memory performance. Nat Neurosci 9: 381-388. (Pubitemid 43290968)
59. Guan XM, Yu H, Palyha OC, McKee KK, Feighner SD, et al. (1997) Distribution of mRNA encoding the growth hormone secretagogue receptor in brain and peripheral tissues. Brain Res Mol Brain Res 48: 23-29. (Pubitemid 27298124)
60. Bennett PA, Thomas GB, Howard AD, Feighner SD, van der Ploeg LH, et al. (1997) Hypothalamic growth hormone secretagogue-receptor (GHS-R) expression is regulated by growth hormone in the rat. Endocrinology 138: 4552-4557. (Pubitemid 27460886)
61. Lopez M, Lage R, Saha AK, Perez-Tilve D, Vazquez MJ, et al. (2008) Hypothalamic fatty acid metabolism mediates the orexigenic action of ghrelin. Cell Metab 7: 389-399. (Pubitemid 351618114)
62. Kola B, Hubina E, Tucci SA, Kirkham TC, Garcia EA, et al. (2005) Cannabinoids and ghrelin have both central and peripheral metabolic and cardiac effects via AMP-activated protein kinase. J Biol Chem 280: 25196-25201. (Pubitemid 40934612)
63. Olszewski PK, Li D, Grace MK, Billington CJ, Kotz CM, et al. (2003) Neural basis of orexigenic effects of ghrelin acting within lateral hypothalamus. Peptides 24: 597-602. (Pubitemid 36829349)
64. Bermudez-Silva FJ, Cardinal P, Cota D (2012) The role of the endocannabinoid system in the neuroendocrine regulation of energy balance. J Psychopharmacol 26: 114-124.
65. Horvath TL, Diano S, Tschop M (2003) Ghrelin in hypothalamic regulation of energy balance. Current Topics in Medicinal Chemistry 3: 921-927.
66. Tucci SA, Rogers EK, Korbonits M, Kirkham TC (2004) The cannabinoid CB1 receptor antagonist SR141716 blocks the orexigenic effects of intrahypothalamic ghrelin. Br J Pharmacol 143: 520-523. (Pubitemid 39524268)
67. Mechoulam R, Parker LA (2013) The endocannabinoid system and the brain. Annu Rev Psychol 64: 21-47.
68. Katona I, Freund TF (2012) Multiple functions of endocannabinoid signaling in the brain. Annu Rev Neurosci 35: 529-558.
69. Andrews ZB (2011) The extra-hypothalamic actions of ghrelin on neuronal function. Trends Neurosci 34: 31-40.
70. Jung KM, Clapper JR, Fu J, D'Agostino G, Guijarro A, et al. (2012) 2-arachidonoylglycerol signaling in forebrain regulates systemic energy metabolism. Cell Metab 15: 299-310.
71. Malik S, McGlone F, Bedrossian D, Dagher A (2008) Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab 7: 400-409. (Pubitemid 351598026)
72. Kroemer NB, Krebs L, Kobiella A, Grimm O, Pilhatsch M, et al. (2013) Fasting levels of ghrelin covary with the brain response to food pictures. Addict Biol 18: 855-862.
73. Jones RB, McKie S, Astbury N, Little TJ, Tivey S, et al. (2012) Functional neuroimaging demonstrates that ghrelin inhibits the central nervous system response to ingested lipid. Gut 61: 1543-1551.