Metabolic status regulates ghrelin function on energy homeostasis

Neuroendocrinology

Volumn 93, Issue 1, 2011, Pages 48-57

  Briggs, Dana I ^a   Andrews, Zane B ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Arcuate nucleus; Body weight regulation; Calorie restriction; Diet induced obesity; Food intake; Glucose homeostasis; Growth hormone secretagogue receptor; Neuropeptide Y; Pro opiomelanocortin

Indexed keywords

ACYLTRANSFERASE; AGOUTI RELATED PROTEIN; GHRELIN; GHRELIN O ACYLTRANSFERASE; GLUCOSE; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ARTICLE; CALORIC RESTRICTION; CELL FUNCTION; ENERGY BALANCE; FATTY ACID OXIDATION; FOOD INTAKE; GLUCOSE BLOOD LEVEL; MITOCHONDRION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL;

ACYLTRANSFERASES; AGOUTI-RELATED PROTEIN; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; CALORIC RESTRICTION; DIET; EATING; ENERGY METABOLISM; GHRELIN; HOMEOSTASIS; HYPOTHALAMUS; MICE; MICE, KNOCKOUT; MODELS, NEUROLOGICAL; NEURONS; NEUROPEPTIDE Y;

EID: 79951682389     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000322589     Document Type: Article

References (69)

1. Gropp E, Shanabrough M, Borok E, Xu AW, Janoschek R, Buch T, Plum L, Balthasar N, Hampel B, Waisman A, Barsh GS, Horvath TL, Bruning JC: Agouti-related peptide-expressing neurons are mandatory for feeding. Nat Neurosci 2005;8:1289-1291. (Pubitemid 41630413)
2. Luquet S, Perez FA, Hnasko TS, Palmiter RD: Npy/agrp neurons are essential for feeding in adult mice but can be ablated in neonates. Science 2005;310:683-685. (Pubitemid 41528162)
3. Tschop M, Smiley DL, Heiman ML: Ghrelin induces adiposity in rodents. Nature 2000;407:908-913.
4. Howard AD, Feighner SD, Cully DF, Arena JP, Liberator PA, Rosenblum CI, Hamelin M, Hreniuk DL, Palyha OC, Anderson J, Paress PS, Diaz C, Chou M, Liu KK, McKee KK, Pong SS, Chaung LY, Elbrecht A, Dashkevicz M, Heavens R, Rigby M, Sirinathsinghji DJ, Dean DC, Melillo DG, Patchett AA, Nargund R, Griffin PR, DeMartino JA, Gupta SK, Schaeffer JM, Smith RG, Van der Ploeg LH: A receptor in pituitary and hypothalamus that functions in growth hormone release. Science 1996;273:974-977. (Pubitemid 26275178)
5. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K: Ghrelin is a growthhormone-releasing acylated peptide from stomach. Nature 1999;402:656-660. (Pubitemid 129516334)
6. Date Y, Kojima M, Hosoda H, Sawaguchi A, Mondal MS, Suganuma T, Matsukura S, Kangawa K, Nakazato M: Ghrelin, a novel growth hormone-releasing acylated peptide, is synthesized in a distinct endocrine cell type in the gastrointestinal tracts of rats and humans. Endocrinology 2000;141:4255-4261.
7. Cowley MA, Smith RG, Diano S, Tschop M, Pronchuk N, Grove KL, Strasburger CJ, Bidlingmaier M, Esterman M, Heiman ML, Garcia-Segura LM, Nillni EA, Mendez P, Low MJ, Sotonyi P, Friedman JM, Liu H, Pinto S, Colmers WF, Cone RD, Horvath TL: The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 2003;37:649-661. (Pubitemid 36262986)
8. Gutierrez JA, Solenberg PJ, Perkins DR, Willency JA, Knierman MD, Jin Z, Witcher DR, Luo S, Onyia JE, Hale JE: Ghrelin octanoylation mediated by an orphan lipid transferase. Proc Natl Acad Sci USA 2008;105:6320-6325. (Pubitemid 351758344)
9. Yang J, Brown MS, Liang G, Grishin N V, Goldstein JL: Identification of the acyltransferase that octanoylates ghrelin, an appetitestimulating pept ide hormone. Cell 2008;132:387-396. (Pubitemid 351192001)
10. Sakata I, Yang J, Lee CE, Osborne-Lawrence S, Rovinsky SA, Elmquist JK, Zigman JM: Colocalization of ghrelin O-acyltransferase and ghrelin in gastric mucosal cells. Am J Physiol Endocrinol Metab 2009;297: E134-E141.
11. Kirchner H, Gutierrez JA, Solenberg PJ, Pfluger PT, Czyzyk TA, Willency JA, Schurmann A, Joost HG, Jandacek RJ, Hale JE, Heiman ML, Tschop MH: Goat links dietary lipids with the endocrine control of energy balance. Nat Med 2009;15:741-745.
12. Zhu X, Cao Y, Voogd K, Steiner DF: On the processing of proghrelin to ghrelin. J Biol Chem 2006;281:38867-38870. (Pubitemid 46042013)
13. Murakami N, Hayashida T, Kuroiwa T, Nakahara K, Ida T, Mondal MS, Nakazato M, Kojima M, Kangawa K: Role for central ghrelin in food intake and secretion profile of stomach ghrelin in rats. J Endocrinol 2002;174:283-288. (Pubitemid 34965767)
14. Guan XM, Yu H, Palyha OC, McKee KK, Feighner SD, Sirinathsinghji DJ, Smith RG, Van der Ploeg LH, Howard AD: Distribution of mRNA encoding the growth hormone secretagogue receptor in brain and peripheral tissues. Brain Res Mol Brain Res 1997;48:23-29. (Pubitemid 27298124)
15. 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. (Pubitemid 41791000)
16. Tannenbaum GS, Lapointe M, Beaudet A, Howard AD: Expression of growth hormone secretagogue-receptors by growth hormone - releasing hormone neurons in the mediobasal hypothalamus. Endocrinology 1998;139:4420-4423. (Pubitemid 28513733)
17. 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;70:306-316.
18. Shuto Y, Shibasaki T, Otagiri A, Kuriyama H, Ohata H, Tamura H, Kamegai J, Sugihara H, Oikawa S, Wakabayashi I: Hypothalamic growth hormone secretagogue receptor regulates growth hormone secretion, feeding, and adiposity. J Clin Invest 2002;109:1429-1436. (Pubitemid 34596168)
19. Andrews ZB, Liu ZW, Walllingford N, Erion DM, Borok E, Friedman JM, Tschop MH, Shanabrough M, Cline G, Shulman GI, Coppola A, Gao XB, Horvath TL, Diano S: UCP2 mediates ghrelin's action on NPY/AGRP neurons by lowering free radicals. Nature 2008;454:846-851.
20. Hewson AK, Dickson SL: Systemic administration of ghrelin induces Fos and EGR-1 proteins in the hypothalamic arcuate nucleus of fasted and fed rats. J Neuroendocrinol 2000;12:1047-1049.
21. Wang L, Saint-Pierre DH, Tache Y: Peripheral ghrelin selectively increases fos expression in neuropeptide y - synthesizing neurons in mouse hypothalamic arcuate nucleus. Neurosci Lett 2002;325:47-51. (Pubitemid 34521976)
22. Kamegai J, Tamura H, Shimizu T, Ishii S, Sugihara H, Wakabayashi I: Central effect of ghrelin, an endogenous g row t h hormone secretagogue, on hypothalamic peptide gene expression. Endocrinology 2000;141:4797-4800. (Pubitemid 32055162)
23. Kamegai J, Tamura H, Shimizu T, Ishii S, Sugihara H, Wakabayashi I: Chronic central infusion of ghrelin increases hypothalamic neuropeptide y and agouti-related protein mR NA levels and body weight in rats. Diabetes 2001;50:2438-2443. (Pubitemid 33642759)
24. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, Matsukura S: A role for ghrelin in the central regulation of feeding. Nature 2001;409:194-198. (Pubitemid 32144284)
25. Chen HY, Trumbauer ME, Chen AS, Weingarth DT, Adams JR, Frazier EG, Shen Z, Marsh DJ, Feighner SD, Guan XM, Ye Z, Nargund R P, Smith RG, Van der Ploeg LH, Howard AD, MacNeil DJ, Qian S: Orexigenic act ion of periphera l gh relin is med iated by neuropeptide y and agouti-related protein. Endocrinology 2004;145:2607-2612.
26. Luquet S, Phillips CT, Palmiter RD: NPY/AGRP neurons are not essential for feeding responses to glucoprivation. Peptides 2007;28:214-225. (Pubitemid 46176250)
27. Tong Q, Ye CP, Jones JE, Elmquist JK, Lowell BB: Synaptic release of GABA by AGRP neurons is required for normal regulation of energy balance. Nat Neurosci 2008.
28. Lutter M, Sakata I, Osborne-Lawrence S, Rovinsky SA, Anderson JG, Jung S, Birnbau m S, Yanagisawa M, Elmquist J K, Nestler EJ, Zigman JM: The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nat Neurosci 2008;11:752-753. (Pubitemid 351896679)
29. Zhao TJ, Liang G, Li RL, Xie X, Sleeman MW, Murphy AJ, Valenzuela DM, Yancopoulos GD, Goldstein JL, Brown MS: Ghrelin O-acyltransferase (GOAT) is essential for growth hormone-mediated survival of calorie-restricted mice. Proc Natl Acad Sci USA 2010;107:7467-7472.
30. Liu J, Prudom CE, Nass R, Pezzoli SS, Oliveri MC, Johnson ML, Veldhuis P, Gordon DA, Howard AD, Witcher DR, Geysen HM, Gaylinn BD, Thorner MO: Novel ghrelin assays provide evidence for independent regulation of ghrelin acylation and secretion in healthy young men. J Clin Endocrinol Metab 2008;93:1980-1987. (Pubitemid 351656547)
31. Hassouna R, Zizzari P, Tolle V: The ghrelin/obestatin balance in the physiological and pathological control of growth hormone secretion, body composition and food intake. J Neuroendocrinol 2010;22:793-804.
32. Anderson KA, Ribar TJ, Lin F, Noeldner PK, Green MF, Muehlbauer MJ, Witters LA, Kemp BE, Means AR: Hypothalamic CAMKK2 contributes to the regulation of energy balance. Cell Metab 2008;7:377-388. (Pubitemid 351598022)
33. Andersson U, Filipsson K, Abbott CR, Woods A, Smith K, Bloom SR, Carling D, Small CJ: AMP-activated protein kinase plays a role in the control of food intake. J Biol Chem 2004;279:12005-12008. (Pubitemid 38445761)
34. Lopez M, Lage R, Saha AK, Perez-Tilve D, Vazquez MJ, Varela L, Sangiao-Alvarellos S, Tovar S, Raghay K, Rodriguez-Cuenca S, Deoliveira RM, Castaneda T, Datta R, Dong JZ, Culler M, Sleeman MW, Alvarez CV, Gallego R, Lelliott CJ, Carling D, Tschop MH, Dieguez C, Vidal-Puig A: Hypothalamic fatty acid metabolism mediates the orexigenic action of ghrelin. Cell Metab 2008;7:389-399. (Pubitemid 351618114)
35. Kola B, Hubina E, Tucci SA, Kirkham TC, Garcia EA, Mitchell SE, Williams LM, Hawley SA, Hardie DG, Grossman AB, Korbonits M: Cannabinoids and ghrelin have both central and peripheral metabolic and cardiac effects via AMP-activated protein kinase. J Biol Chem 2005;280:25196-25201. (Pubitemid 40934612)
36. Kohno D, Sone H, Minokoshi Y, Yada T: Ghrelin raises [Ca2+]i via AMPK in hypothalamic arcuate nucleus NPY neurons. Biochem Biophys Res Commun 2008;366:388-392. (Pubitemid 50010409)
37. Steinberg GR, Kemp BE: AMPK in health and disease. Physiol Rev 2009;89:1025-1078.
38. Obici S, Feng Z, Arduini A, Conti R, Rossetti L: Inhibition of hypothalamic carnitine palmitoyltransferase-1 decreases food intake and glucose production. Nat Med 2003;9:756-761. (Pubitemid 36749226)
39. Wolfgang MJ, Lane MD: The role of hypothalamic malonyl-CoA in energy homeostasis. J Biol Chem 2006;281:37265-37269. (Pubitemid 46042029)
40. Ochoa JJ, Quiles JL, Ibanez S, Martinez E, Lopez-Frias M, Huertas JR, Mataix J: Aging-related oxidative stress depends on dietary lipid source in rat postmitotic tissues. J Bioenerg Biomembr 2003;35:267-275. (Pubitemid 38115224)
41. Sun Y, Asnicar M, Saha PK, Chan L, Smith RG: Ablation of ghrelin improves the diabetic but not obese phenotype of ob/ob mice. Cell Metab 2006;3:379-386.
42. Sun Y, Butte NF, Garcia JM, Smith RG: Characterization of adult ghrelin and ghrelin receptor knockout mice under positive and negative energy balance. Endocrinology 2008;149:843-850. (Pubitemid 351159337)
43. Sun Y, Asnicar M, Smith RG: Central and peripheral roles of ghrelin on glucose homeostasis. Neuroendocrinology 2007;86:215-228. (Pubitemid 350073609)
44. Perreault M, Istrate N, Wang L, Nichols AJ, Tozzo E, Stricker-Krongrad A: Resistance to the orexigenic effect of ghrelin in dietaryinduced obesity in mice: reversal upon weight loss. Int J Obes Relat Metab Disord 2004;28:879-885. (Pubitemid 39005688)
45. Banks WA: The blood-brain barrier as a cause of obesity. Curr Pharm des 2008;14:1606-1614. (Pubitemid 352002988)
46. Bouret SG, Gorski JN, Patterson CM, Chen S, Levin BE, Simerly RB: Hypothalamic neural projections are permanently disrupted in diet-induced obese rats. Cell Metab 2008;7:179-185. (Pubitemid 351181005)
47. Sipols AJ, Baskin DG, Schwartz MW: Effect of intracerebroventricular insulin infusion on diabetic hyperphagia and hypothalamic neuropeptide gene expression. Diabetes 1995;44:147-151.
48. Martin TL, Alquier T, Asakura K, Furukawa N, Preitner F, Kahn BB: Diet-induced obesity alters AMP kinase activity in hypothalamus and skeletal muscle. J Biol Chem 2006;281:18933-18941. (Pubitemid 44035396)
49. Briggs DI, Enriori PJ, Lemus MB, Cowley MA, Andrews ZB: Diet-induced obesity causes ghrelin resistance in arcuate NPY/AGRP neurons. Endocrinology 2010;151:4745-4755.
50. Banks WA, Burney BO, Robinson SM: Effects of triglycerides, obesity, and starvation on ghrelin transport across the blood-brain barrier. Peptides 2008;29:2061-2065.
51. Holst B, Cygankiewicz A, Jensen TH, Ankersen M, Schwartz TW: High constitutive signaling of the ghrelin receptor - identification of a potent inverse agonist. Mol Endocrinol 2003;17:2201-2210. (Pubitemid 37352532)
52. Petersen PS, Woldbye DP, Madsen AN, Egerod KL, Jin C, Lang M, Rasmussen M, Beck-Sickinger AG, Holst B: In vivo characterization of high basal signaling from the ghrelin receptor. Endocrinology 2009;150:4920-4930.
53. Schwartz MW, Sipols AJ, Marks JL, Sanacora G, White JD, Scheurink A, Kahn SE, Baskin DG, Woods SC, Figlewicz DP, et al: Inhibition of hypothalamic neuropeptide y gene expression by insulin. Endocrinology 1992;130:3608-3616.
54. Minokoshi Y, Alquier T, Furukawa N, Kim YB, Lee A, Xue B, Mu J, Foufelle F, Ferre P, Birnbaum MJ, Stuck BJ, Kahn BB: Amp-kinase regulates food intake by responding to hormonal and nutrient signals in the hypotha lamus. Nature 2004;428:569-574. (Pubitemid 38480541)
55. Flanagan DE, Evans ML, Monsod TP, Rife F, Heptulla RA, Tamborlane W V, Sherwin RS: The influence of insulin on circulating ghrelin. Am J Physiol Endocrinol Metab 2003;284: E313-E316. (Pubitemid 36120103)
56. McCowen KC, Maykel JA, Bistrian BR, Ling PR: Circulating ghrelin concentrations are lowered by intravenous glucose or hyperinsulinemic euglycemic conditions in rodents. J Endocrinol 2002;175: R7-R11. (Pubitemid 35414401)
57. Luque RM, Kineman RD: Impact of obesity on the growth hormone axis: evidence for a direct inhibitory effect of hyperinsulinemia on pituitary function. Endocrinology 2006;147:2754-2763. (Pubitemid 43764612)
58. Theander-Carrillo C, Wiedmer P, Cettour-Rose P, Nogueiras R, Perez-Tilve D, Pfluger P, Castaneda TR, Muzzin P, Schurmann A, Szanto I, Tschop MH, Rohner-Jeanrenaud F: Ghrelin action in the brain controls adipocyte metabolism. J Clin Invest 2006;116:1983-1993. (Pubitemid 44033322)
59. Zarjevski N, Cusin I, Vettor R, Rohner-Jeanrenaud F, Jeanrenaud B: Chronic intracerebroventricular neuropeptide-Y administration to normal rats mimics hormonal and metabolic changes of obesity. Endocrinology 1993;133:1753-1758. (Pubitemid 23295205)
60. Tschop M, Statnick MA, Suter TM, Heiman ML: GH-releasing peptide-2 increases fat mass in mice lacking NPY: indication for a crucial mediating role of hypothalamic agouti-related protein. Endocrinology 2002;143:558-568. (Pubitemid 34107210)
61. Shrestha YB, Wickwire K, Giraudo S: Effect of reducing hypothalamic ghrelin receptor gene expression on energy balance. Peptides 2009;30:1336-1341.
62. Wortley KE, Anderson KD, Garcia K, Murray JD, Malinova L, Liu R, Moncrieffe M, Thabet K, Cox HJ, Yancopoulos GD, Wiegand SJ, Sleeman MW: Genetic deletion of ghrelin does not decrease food intake but inf luences metabolic fuel preference. Proc Natl Acad Sci USA 2004;101:8227-8232. (Pubitemid 38698082)
63. Wortley KE, del Rincon JP, Murray JD, Garcia K, Iida K, Thorner MO, Sleeman MW: Absence of ghrelin protects against early-onset obesity. J Clin Invest 2005;115:3573-3578. (Pubitemid 43121845)
64. Zigman JM, Nakano Y, Coppari R, Balthasar N, Marcus JN, Lee CE, Jones JE, Deysher AE, Waxman AR, White RD, Williams TD, Lachey JL, Seeley RJ, Lowell BB, Elmquist JK: Mice lacking ghrelin receptors resist the development of diet-induced obesity. J Clin Invest 2005;115:3564-3572. (Pubitemid 43121844)
65. Sun Y, Wang P, Zheng H, Smith RG: Ghrelin stimulation of growth hormone release and appetite is mediated through the growth hormone secretagogue receptor. Proc Natl Acad Sci USA 2004;101:4679-4684. (Pubitemid 38437470)
66. Pfluger PT, Kirchner H, Gunnel S, Schrott B, Perez-Tilve D, Fu S, Benoit SC, Horvath T, Joost HG, Wortley KE, Sleeman MW, Tschop MH: Simultaneous deletion of ghrelin and its receptor increases motor activity and energy expenditure. Am J Physiol Gastrointest Liver Physiol 2008;294: G610-G618. (Pubitemid 351468766)
67. Goldstone AP, Thomas EL, Brynes AE, Castroman G, Edwards R, Ghatei MA, Frost G, Holland AJ, Grossman AB, Korbonits M, Bloom SR, Bell JD: Elevated fasting plasma ghrelin in Prader-Willi syndrome adults is not solely explained by their reduced visceral adiposity and insulin resistance. J Clin Endocrinol Metab 2004;89:1718-1726. (Pubitemid 38507925)
68. Vestergaard ET, Gormsen LC, Jessen N, Lund S, Hansen TK, Moller N, Jorgensen JO: Ghrelin infusion in humans induces acute insulin resistance and lipolysis independent of growth hormone signaling. Diabetes 2008;57:3205-3210.
69. Pacifico L, Poggiogalle E, Costantino F, Anania C, Ferraro F, Chiarelli F, Chiesa C: Acylated and nonacylated ghrelin levels and their associations with insulin resistance in obese and normal weight children with metabolic syndrome. Eur J Endocrinol 2009;161:861-870.