Sensing of fatty acids for octanoylation of ghrelin involves a gustatory G-protein

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Janssen, Sara ^a   Laermans, Jorien ^a   Iwakura, Hiroshi ^b   Tack, Jan ^a   Depoortere, Inge ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3,3,14,14 TETRAMETHYLHEXADECANEDIOIC ACID; ALPHA GUSTDUCIN; ALPHA TRANSDUCIN; G PROTEIN COUPLED RECEPTOR 120; G PROTEIN COUPLED RECEPTOR 40; GHRELIN; GUANINE NUCLEOTIDE BINDING PROTEIN; LINOLEIC ACID; NUCLEOTIDE BINDING PROTEIN; OCTANOIC ACID; SMALL INTERFERING RNA; TRIOCTANOIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOSENSOR; CELLULAR DISTRIBUTION; CHEMICAL MODIFICATION; CONTROLLED STUDY; DOWN REGULATION; GENE INACTIVATION; HORMONE ACTION; HORMONE BLOOD LEVEL; HORMONE RELEASE; HORMONE SYNTHESIS; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LIPID DIET; MALE; MOUSE; NONHUMAN; OCTANOYLATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STOMACH EMPTYING; UPREGULATION; WILD TYPE;

AGOUTI-RELATED PROTEIN; ALPHA-LINOLENIC ACID; ANIMALS; BODY WEIGHT; CAPRYLATES; CELL LINE; DIET; FATTY ACIDS; FEEDING BEHAVIOR; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GHRELIN; HETEROTRIMERIC GTP-BINDING PROTEINS; HUMANS; MALE; MICE; MICE, INBRED C57BL; PALMITIC ACIDS; PROTEIN TRANSPORT; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; TASTE;

MUS;

EID: 84863084353     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040168     Document Type: Article

References (46)

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.
2. Dezaki K, Sone H, Yada T, (2008) Ghrelin is a physiological regulator of insulin release in pancreatic islets and glucose homeostasis. Pharmacol Ther 118: 239-249.
3. Depoortere I, (2009) Targeting the ghrelin receptor to regulate food intake. Regul Pept 156: 13-23.
4. 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.
5. Kamegai J, Tamura H, Shimizu T, Ishii S, Sugihara H, et al. (2001) Chronic central infusion of ghrelin increases hypothalamic neuropeptide Y and Agouti-related protein mRNA levels and body weight in rats. Diabetes 50: 2438-2443.
6. Tschop M, Smiley DL, Heiman ML, (2000) Ghrelin induces adiposity in rodents. Nature 407: 908-913.
7. Theander-Carrillo C, Wiedmer P, Cettour-Rose P, Nogueiras R, Perez-Tilve D, et al. (2006) Ghrelin action in the brain controls adipocyte metabolism. J Clin Invest 116: 1983-1993.
8. Choi K, Roh SG, Hong YH, Shrestha YB, Hishikawa D, et al. (2003) The role of ghrelin and growth hormone secretagogues receptor on rat adipogenesis. Endocrinology 144: 754-759.
9. Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, et al. (2001) A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes 50: 1714-1719.
10. Zhao TJ, Sakata I, Li RL, Liang G, Richardson JA, et al. (2010) Ghrelin secretion stimulated by {beta}1-adrenergic receptors in cultured ghrelinoma cells and in fasted mice. Proc Natl Acad Sci U S A 107: 15868-15873.
11. Overduin J, Frayo RS, Grill HJ, Kaplan JM, Cummings DE, (2005) Role of the duodenum and macronutrient type in ghrelin regulation. Endocrinology 146: 845-850.
12. Foster-Schubert KE, Overduin J, Prudom CE, Liu J, Callahan HS, et al. (2008) Acyl and total ghrelin are suppressed strongly by ingested proteins, weakly by lipids, and biphasically by carbohydrates. J Clin Endocrinol Metab 93: 1971-1979.
13. Callahan HS, Cummings DE, Pepe MS, Breen PA, Matthys CC, et al. (2004) Postprandial suppression of plasma ghrelin level is proportional to ingested caloric load but does not predict intermeal interval in humans. J Clin Endocrinol Metab 89: 1319-1324.
14. Hosoda H, Kojima M, Matsuo H, Kangawa K, (2000) Ghrelin and des-acyl ghrelin: two major forms of rat ghrelin peptide in gastrointestinal tissue. Biochem Biophys Res Commun 279: 909-913.
15. Gutierrez JA, Solenberg PJ, Perkins DR, Willency JA, Knierman MD, et al. (2008) Ghrelin octanoylation mediated by an orphan lipid transferase. Proc Natl Acad Sci U S A 105: 6320-6325.
16. Yang J, Brown MS, Liang G, Grishin NV, Goldstein JL, (2008) Identification of the acyltransferase that octanoylates ghrelin, an appetite-stimulating peptide hormone. Cell 132: 387-396.
17. Nishi Y, Hiejima H, Hosoda H, Kaiya H, Mori K, et al. (2005) Ingested medium-chain fatty acids are directly utilized for the acyl modification of ghrelin. Endocrinology 146: 2255-2264.
18. Briscoe CP, Tadayyon M, Andrews JL, Benson WG, Chambers JK, et al. (2003) The orphan G protein-coupled receptor GPR40 is activated by medium and long chain fatty acids. J Biol Chem 278: 11303-11311.
19. Tanaka T, Yano T, Adachi T, Koshimizu TA, Hirasawa A, et al. (2008) Cloning and characterization of the rat free fatty acid receptor GPR120: in vivo effect of the natural ligand on GLP-1 secretion and proliferation of pancreatic beta cells. Naunyn Schmiedebergs Arch Pharmacol 377: 515-522.
20. Edfalk S, Steneberg P, Edlund H, (2008) Gpr40 is expressed in enteroendocrine cells and mediates free fatty acid stimulation of incretin secretion. Diabetes 57: 2280-2287.
21. Hirasawa A, Tsumaya K, Awaji T, Katsuma S, Adachi T, et al. (2005) Free fatty acids regulate gut incretin glucagon-like peptide-1 secretion through GPR120. Nat Med 11: 90-94.
22. Tanaka T, Katsuma S, Adachi T, Koshimizu TA, Hirasawa A, et al. (2008) Free fatty acids induce cholecystokinin secretion through GPR120. Naunyn Schmiedebergs Arch Pharmacol 377: 523-527.
23. Liou AP, Lu X, Sei Y, Zhao X, Pechhold S, et al. (2011) The G-protein-coupled receptor GPR40 directly mediates long-chain fatty acid-induced secretion of cholecystokinin. Gastroenterology 140: 903-912.
24. Matsumura S, Eguchi A, Mizushige T, Kitabayashi N, Tsuzuki S, et al. (2009) Colocalization of GPR120 with phospholipase-Cbeta2 and alpha-gustducin in the taste bud cells in mice. Neurosci Lett 450: 186-190.
25. Wong GT, Gannon KS, Margolskee RF, (1996) Transduction of bitter and sweet taste by gustducin. Nature 381: 796-800.
26. He W, Yasumatsu K, Varadarajan V, Yamada A, Lem J, et al. (2004) Umami taste responses are mediated by alpha-transducin and alpha-gustducin. J Neurosci 24: 7674-7680.
27. Janssen S, Laermans J, Verhulst PJ, Thijs T, Tack J, et al. (2011) Bitter taste receptors and alpha-gustducin regulate the secretion of ghrelin with functional effects on food intake and gastric emptying. Proc Natl Acad Sci U S A 108: 2094-2099.
28. Hass N, Schwarzenbacher K, Breer H, (2007) A cluster of gustducin-expressing cells in the mouse stomach associated with two distinct populations of enteroendocrine cells. Histochem Cell Biol 128: 457-471.
29. Sutherland K, Young RL, Cooper NJ, Horowitz M, Blackshaw LA, (2007) Phenotypic characterization of taste cells of the mouse small intestine. American journal of physiology Gastrointestinal and liver physiology 292: G1420-1428.
30. Bezencon C, le Coutre J, Damak S, (2007) Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chemical senses 32: 41-49.
31. Young RL, Sutherland K, Pezos N, Brierley SM, Horowitz M, et al. (2009) Expression of taste molecules in the upper gastrointestinal tract in humans with and without type 2 diabetes. Gut 58: 337-346.
32. Verhulst PJ, De Smet B, Saels I, Thijs T, Ver Donck L, et al. (2008) Role of ghrelin in the relationship between hyperphagia and accelerated gastric emptying in diabetic mice. Gastroenterology 135: 1267-1276.
33. Kitazawa T, De Smet B, Verbeke K, Depoortere I, Peeters TL, (2005) Gastric motor effects of peptide and non-peptide ghrelin agonists in mice in vivo and in vitro. Gut 54: 1078-1084.
34. Iwakura H, Li Y, Ariyasu H, Hosoda H, Kanamoto N, et al. (2010) Establishment of a novel ghrelin-producing cell line. Endocrinology 151: 2940-2945.
35. Hara T, Hirasawa A, Sun Q, Sadakane K, Itsubo C, et al. (2009) Novel selective ligands for free fatty acid receptors GPR120 and GPR40. Naunyn Schmiedebergs Arch Pharmacol 380: 247-255.
36. Cao H, Gerhold K, Mayers JR, Wiest MM, Watkins SM, et al. (2008) Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell 134: 933-944.
37. Schwartz GJ, Fu J, Astarita G, Li X, Gaetani S, et al. (2008) The lipid messenger OEA links dietary fat intake to satiety. Cell Metab 8: 281-288.
38. Gillum MP, Zhang D, Zhang XM, Erion DM, Jamison RA, et al. (2008) N-acylphosphatidylethanolamine, a gut- derived circulating factor induced by fat ingestion, inhibits food intake. Cell 135: 813-824.
39. Kirchner H, Gutierrez JA, Solenberg PJ, Pfluger PT, Czyzyk TA, et al. (2009) GOAT links dietary lipids with the endocrine control of energy balance. Nat Med 15: 741-745.
40. Gahete MD, Cordoba-Chacon J, Salvatori R, Castano JP, Kineman RD, et al. (2010) Metabolic regulation of ghrelin O-acyl transferase (GOAT) expression in the mouse hypothalamus, pituitary, and stomach. Mol Cell Endocrinol 317: 154-160.
41. Depoortere I, De Winter B, Thijs T, De Man J, Pelckmans P, et al. (2005) Comparison of the gastroprokinetic effects of ghrelin, GHRP-6 and motilin in rats in vivo and in vitro. Eur J Pharmacol 515: 160-168.
42. Fukuda H, Mizuta Y, Isomoto H, Takeshima F, Ohnita K, et al. (2004) Ghrelin enhances gastric motility through direct stimulation of intrinsic neural pathways and capsaicin-sensitive afferent neurones in rats. Scand J Gastroenterol 39: 1209-1214.
43. Laugerette F, Passilly-Degrace P, Patris B, Niot I, Febbraio M, et al. (2005) CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J Clin Invest 115: 3177-3184.
44. Shah BP, Liu P, Yu T, Hansen DR, Gilbertson TA, (2011) TRPM5 is critical for linoleic acid-induced CCK secretion from the enteroendocrine cell line, STC-1. Am J Physiol Cell Physiol 302: C210-219.
45. Fukuwatari T, Kawada T, Tsuruta M, Hiraoka T, Iwanaga T, et al. (1997) Expression of the putative membrane fatty acid transporter (FAT) in taste buds of the circumvallate papillae in rats. FEBS Lett 414: 461-464.
46. Widmayer P, Kuper M, Kramer M, Konigsrainer A, Breer H, (2011) Altered expression of gustatory-signaling elements in gastric tissue of morbidly obese patients. Int J Obes (Lond).