Meal Anticipatory Rise in Acylated Ghrelin at Dark Onset is Blunted After Long-Term Fasting in Rats

Journal of Neuroendocrinology

Volumn 23, Issue 9, 2011, Pages 804-814

  Zizzari, P ^a   Hassouna, R ^a   Longchamps, R ^a   Epelbaum, J ^a   Tolle, V ^a  

^a INSERM   (France)

Author keywords

Activity; Acylated ghrelin; Fasting; Feeding; Ghrelin O acyl transferase

Indexed keywords

ACYLTRANSFERASE; AGOUTI RELATED PROTEIN; GHRELIN; NEUROPEPTIDE; NEUROPEPTIDE Y;

ACYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; ENERGY CONSERVATION; ENERGY RESOURCE; FEEDING; FEEDING BEHAVIOR; LIGHT DARK CYCLE; LOCOMOTION; MALE; MEAL; MOTIVATION; NONHUMAN; NUTRITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ACYLATION; AGOUTI-RELATED PROTEIN; ANIMALS; ANTICIPATION, PSYCHOLOGICAL; BEHAVIOR, ANIMAL; BIOLOGICAL MARKERS; CIRCADIAN RHYTHM; DARKNESS; EATING; FASTING; FATTY ACIDS, NONESTERIFIED; GHRELIN; HUMANS; MALE; MOTOR ACTIVITY; NEUROPEPTIDE Y; PHOTOPERIOD; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80051575440     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02183.x     Document Type: Article

References (52)

1. 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: 656-660.
2. Tomasetto C, Karam SM, Ribieras S, Masson R, Lefèbvre O, Staub A, Alexander G, Chenard MP, Rio MC. Identification and characterization of a novel gastric peptide hormone: the motilin-related peptide. Gastroenterology 2000; 119: 395-405.
3. Tschöp M, Smiley DL, Heiman ML. Ghrelin induces adiposity in rodents. Nature 2000; 407: 908-913.
4. 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.
5. Yang J, Brown MS, Liang G, Grishin NV, Goldstein JL. Identification of the acyltransferase that octanoylates ghrelin, an appetite-stimulating peptide hormone. Cell 2008; 132: 387-396.
6. Tolle V, Zizzari P, Tomasetto C, Rio MC, Epelbaum J, Bluet-Pajot MT. In vivo and in vitro effects of ghrelin/motilin-related peptide on growth hormone secretion in the rat. Neuroendocrinology 2001; 73: 54-61.
7. Hosoda H, Kojima M, Matsuo H, Kangawa K. Ghrelin and des-acyl ghrelin: two major forms of rat ghrelin peptide in gastrointestinal tissue. Biochem Biophys Res Commun 2000; 279: 909-913.
8. Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 2001; 50: 1714-1719.
9. 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.
10. Tolle V, Bassant M-H, Zizzari P, Poindessous-Jazat F, Tomasetto C, Epelbaum J, Bluet-Pajot M-T. Ultradian rhythmicity of ghrelin secretion in relation with GH, feeding behavior, and sleep-wake patterns in rats. Endocrinology 2002; 143: 1353-1361.
11. Zizzari P, Hassouna R, Grouselle D, Epelbaum J, Tolle V. Physiological roles of preproghrelin-derived peptides in GH secretion and feeding. Peptides 2011; [Epub ahead of print].
12. Drazen DL, Vahl TP, D'Alessio DA, Seeley RJ, Woods SC. Effects of a fixed meal pattern on ghrelin secretion: evidence for a learned response independent of nutrient status. Endocrinology 2006; 147: 23-30.
13. Sugino T, Hasegawa Y, Kikkawa Y, Yamaura J, Yamagishi M, Kurose Y, Kojima M, Kangawa K, Terashima Y. A transient ghrelin surge occurs just before feeding in a scheduled meal-fed sheep. Biochem Biophys Res Commun 2002; 295: 255-260.
14. Sugino T, Yamaura J, Yamagishi M, Ogura A, Hayashi R, Kurose Y, Kojima M, Kangawa K, Hasegawa Y, Terashima Y. A transient surge of ghrelin secretion before feeding is modified by different feeding regimens in sheep. Biochem Biophys Res Commun 2002; 298: 785-788.
15. Verbaeys I, Tolle V, Swennen Q, Zizzari P, Buyse J, Epelbaum J, Cokelaere M. Scheduled feeding results in adipogenesis and increased acylated ghrelin. Am J Physiol Endocrinol Metab 2011; 300: E1103-E1111.
16. Blum ID, Patterson Z, Khazall R, Lamont EW, Sleeman MW, Horvath TL, Abizaid A. Reduced anticipatory locomotor responses to scheduled meals in ghrelin receptor deficient mice. Neuroscience 2009; 164: 351-359.
17. LeSauter J, Hoque N, Weintraub M, Pfaff DW, Silver R. Stomach ghrelin-secreting cells as food-entrainable circadian clocks. Proc Natl Acad Sci USA 2009; 106: 13582-13587.
18. Seoane LM, Al-Massadi O, Caminos JE, Tovar SA, Dieguez C, Casanueva FF. Sensory stimuli directly acting at the central nervous system regulate gastric ghrelin secretion. an ex vivo organ culture study. Endocrinology 2007; 148: 3998-4006.
19. Toshinai K, Mondal MS, Nakazato M, Date Y, Murakami N, Kojima M, Kangawa K, Matsukura S. Upregulation of Ghrelin expression in the stomach upon fasting, insulin-induced hypoglycemia, and leptin administration. Biochem Biophys Res Commun 2001; 281: 1220-1225.
20. Ariyasu H, Takaya K, Hosoda H, Iwakura H, Ebihara K, Mori K, Ogawa Y, Hosoda K, Akamizu T, Kojima M, Kangawa K, Nakao K. Delayed short-term secretory regulation of ghrelin in obese animals: evidenced by a specific RIA for the active form of ghrelin. Endocrinology 2002; 143: 3341-3350.
21. Foster-Schubert KE, Overduin J, Prudom CE, Liu J, Callahan HS, Gaylinn BD, Thorner MO, Cummings DE. Acyl and total ghrelin are suppressed strongly by ingested proteins, weakly by lipids, and biphasically by carbohydrates. J Clin Endocrinol Metab 2008; 93: 1971-1979.
22. Gahete MD, Córdoba-Chacón J, Salvatori R, Castaño JP, Kineman RD, Luque RM. Metabolic regulation of ghrelin O-acyl transferase (GOAT) expression in the mouse hypothalamus, pituitary, and stomach. Mol Cell Endocrinol 2010; 317: 154-160.
23. Kirchner H, Gutierrez JA, Solenberg PJ, Pfluger PT, Czyzyk TA, Willency JA, Schürmann A, Joost H-G, Jandacek RJ, Hale JE, Heiman ML, Tschöp MH. GOAT links dietary lipids with the endocrine control of energy balance. Nat Med 2009; 15: 741-745.
24. Liu X, York DA, Bray GA. Regulation of ghrelin gene expression in stomach and feeding response to a ghrelin analogue in two strains of rats. Peptides 2004; 25: 2171-2177.
25. Zizzari P, Longchamps R, Epelbaum J, Bluet-Pajot MT. Obestatin partially affects ghrelin stimulation of food intake and growth hormone secretion in rodents. Endocrinology 2007; 148: 1648-1653.
26. Armstrong S, Coleman G, Singer G. Food and water deprivation: changes in rat feeding, drinking, activity and body weight. Neurosci Biobehav Rev 1980; 4: 377-402.
27. Bluet-Pajot MT, Durand D, Drouva SV, Mounier F, Pressac M, Kordon C. Further evidence that thyrotropin-releasing hormone participate in the regulation of growth hormone secretion in the rat. Neuroendocrinology 1986; 44: 70-75.
28. Ezan E, Laplante E, Bluet-Pajot MT, Mounier F, Mamas S, Grouselle D, Grognet JM, Kordon C. An enzyme immunoassay for rat growth hormone: validation and application to the determination of plasma levels and in vitro release. J Immunoassay 1997; 18: 335-356.
29. Burton-Freeman B, Gietzen DW, Schneeman BO. Meal pattern analysis to investigate the satiating potential of fat, carbohydrate, and protein in rats. Am J Physiol 1997; 273: R1916-R1922.
30. Langhans W, Scharrer E. Role of fatty acid oxidation in control of meal pattern. Behav Neural Biol 1987; 47: 7-16.
31. Prudom C, Liu J, Patrie J, Gaylinn BD, Foster-Schubert KE, Cummings DE, Thorner MO, Geysen HM. Comparison of competitive radioimmunoassays and two-site sandwich assays for the measurement and interpretation of plasma ghrelin levels. J Clin Endocrinol Metab 2010; 95: 2351-2358.
32. Solomon TP, Chambers ES, Jeukendrup AE, Toogood AA, Blannin AK. The effect of feeding frequency on insulin and ghrelin responses in human subjects. Br J Nutr 2008; 100: 810-819.
33. Bagnasco M, Kalra PS, Kalra SP. Ghrelin and leptin pulse discharge in fed and fasted rats. Endocrinology 2002; 143: 726-729.
34. Verhagen LA, Egecioglu E, Luijendijk MC, Hillebrand JJ, Adan RA, Dickson SL. Acute and chronic suppression of the central ghrelin signaling system reveals a role in food anticipatory activity. Eur Neuropsychopharmacol 2011; 21: 384-392.
35. Davis JF, Choi DL, Clegg DJ, Benoit SC. Signaling through the ghrelin receptor modulates hippocampal function and meal anticipation in mice. Physiol Behav 2011; 103: 39-43.
36. Szentirmai E, Kapas L, Sun Y, Smith RG, Krueger JM. Restricted feeding-induced sleep, activity, and body temperature changes in normal and preproghrelin-deficient mice. Am J Physiol Regul Integr Comp Physiol 2010; 298: R467-R477.
37. Arvaniti K, Huang Q, Richard D. Effects of leptin and corticosterone on the expression of corticotropin-releasing hormone, agouti-related protein, and proopiomelanocortin in the brain of ob/ob mouse. Neuroendocrinology 2001; 73: 227-236.
38. Mizuno TM, Mobbs CV. Hypothalamic agouti-related protein messenger ribonucleic acid is inhibited by leptin and stimulated by fasting. Endocrinology 1999; 140: 814-817.
39. Ahima RS, Kelly J, Elmquist JK, Flier JS. Distinct physiologic and neuronal responses to decreased leptin and mild hyperleptinemia. Endocrinology 1999; 140: 4923-4931.
40. Korner J, Savontaus E, Chua SC Jr, Leibel RL, Wardlaw SL. Leptin regulation of Agrp and Npy mRNA in the rat hypothalamus. J Neuroendocrinol 2001; 13: 959-966.
41. Tolle V, Low MJ. In vivo evidence for inverse agonism of Agouti-related peptide in the central nervous system of proopiomelanocortin-deficient mice. Diabetes 2008; 57: 86-94.
42. Lawrence CB, Snape AC, Baudoin FM-H, Luckman SM. Acute central ghrelin and GH secretagogues induce feeding and activate brain appetite centers. Endocrinology 2002; 143: 155-162.
43. Toshinai K, Date Y, Murakami N, Shimada M, Mondal MS, Shimbara T, Guan J-L, Wang Q-P, Funahashi H, Sakurai T, Shioda S, Matsukura S, Kangawa K, Nakazato M. Ghrelin-induced food intake is mediated via the orexin pathway. Endocrinology 2003; 144: 1506-1512.
44. Bertile F, Oudart H, Criscuolo F, Le Maho Y, Raclot T. Hypothalamic gene expression in long-term fasted rats: relationship with body fat. Biochem Biophys Res Commun 2003; 303: 1106-1113.
45. Perello M, Sakata I, Birnbaum S, Chuang JC, Osborne-Lawrence S, Rovinsky SA, Woloszyn J, Yanagisawa M, Lutter M, Zigman JM. Ghrelin increases the rewarding value of high-fat diet in an orexin-dependent manner. Biol Psychiatry 2010; 67: 880-886.
46. 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.
47. Tannenbaum GS, Martin JB, Colle E. Ultradian growth hormone rhythm in the rat: effects of feeding, hyperglycemia, and insulin-induced hypoglycemia. Endocrinology 1976; 99: 720-727.
48. Zizzari P, Halem H, Taylor J, Dong JZ, Datta R, Culler MD, Epelbaum J, Bluet-Pajot MT. Endogenous ghrelin regulates episodic growth hormone (GH) secretion by amplifying GH Pulse amplitude: evidence from antagonism of the GH secretagogue-R1a receptor. Endocrinology 2005; 146: 3836-3842.
49. Zhao T-J, 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.
50. González CR, Vázquez MJ, López M, Diéguez C. Influence of chronic undernutrition and leptin on GOAT mRNA levels in rat stomach mucosa. J Mol Endocrinol 2008; 41: 415-421.
51. Reimer RA, Maurer AD, Lau DCW, Auer RN. Long-term dietary restriction influences plasma ghrelin and GOAT mRNA level in rats. Physiol Behav 2010; 99: 605-610.
52. Stengel A, Goebel M, Wang L, Tache Y, Sachs G, Lambrecht NW. Differential distribution of ghrelin-O-acyltransferase (GOAT) immunoreactive cells in the mouse and rat gastric oxyntic mucosa. Biochem Biophys Res Commun 2010; 392: 67-71.