Dietary caprylic acid (C8:0) does not increase plasma acylated ghrelin but decreases plasma unacylated ghrelin in the rat

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Lemarié, Fanny ^a   Beauchamp, Erwan ^a   Dayot, Stéphanie ^a   Duby, Cécile ^a   Legrand, Philippe ^a   Rioux, Vincent ^a  

^a AGROCAMPUS OUEST   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GHRELIN; GROWTH HORMONE; MESSENGER RNA; OCTANOIC ACID; SOMATOMEDIN C; OCTANOIC ACID DERIVATIVE;

ACYLATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC RESTRICTION; CHEMICAL MODIFICATION; CONTROLLED STUDY; DIETARY INTAKE; FAT MASS; FOOD INTAKE; GROWTH HORMONE RELEASE; HORMONE BLOOD LEVEL; HYPOPHYSIS; INTESTINE; LIPID DIET; LIPID HYDROLYSIS; MALE; NONHUMAN; OBESITY; OCTANOYLATION; PROTEIN EXPRESSION; RAT; STOMACH; TISSUE SPECIFICITY; WEIGHT GAIN; WEIGHT REDUCTION; ACETYLATION; ADIPOSE TISSUE; ANIMAL; BLOOD; BODY WEIGHT; DIETARY SUPPLEMENT; DRUG EFFECTS; GENETICS; METABOLISM; PROTEIN PROCESSING; SPRAGUE DAWLEY RAT;

ACETYLATION; ADIPOSE TISSUE; ANIMALS; BODY WEIGHT; CAPRYLATES; DIETARY SUPPLEMENTS; GHRELIN; GROWTH HORMONE; INSULIN-LIKE GROWTH FACTOR I; MALE; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84941313018     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133600     Document Type: Article

References (78)

1. Jensen RG, Ferris AM, Lammi-Keefe CJ, Henderson RA. Lipids of bovine and human milks: A comparison. J Dairy Sci. 1990; 73: 223-40. PMID: 2184172.
2. Takeuchi H, Sekine S, Kojima K, Aoyama T. The application of medium-chain fatty acids: edible oil with a suppressing effect on body fat accumulation. Asia Pac J Clin Nutr. 2008; 17 Suppl 1: 320-323. PMID: 18296368.
3. Bach AC, Babayan VK. Medium-chain triglycerides: An update. Am J Clin Nutr. 1982; 36: 950-62. PMID: 6814231.
4. Clark SB, Brause B, Holt PR. Lipolysis and Absorption of Fat in the Rat Stomach. Gastroenterology. 1969; 56: 214-222. doi:10.1016/S0016-5085(69)80120-4 PMID: 5764591.
5. Perret JP. [Gastric lipolysis of maternal milk triglycerides, and gastric absorption of medium chain fatty acids in the young rabbit (author's transl)]. J Physiol (Paris). 1980; 76: 159-166.
6. Lai HC, Ney DM. Gastric digestion modifies absorption of butterfat into lymph chylomicrons in rats. J Nutr. 1998; 128: 2403-2410. PMID: 9868188.
7. You YQ, Ling PR, Qu JZ, Bistrian BR. Effects of medium-chain triglycerides, long-chain triglycerides, or 2-monododecanoin on fatty acid composition in the portal vein, intestinal lymph, and systemic circulation in rats. JPEN J Parenter Enter Nutr. 2008; 32: 169-75.
8. Ooyama K, Kojima K, Aoyama T, Takeuchi H. Decrease of food intake in rats after ingestion of medium-chain triacylglycerol. J Nutr Sci Vitaminol Tokyo. 2009; 55: 423-7. PMID: 19926929.
9. Papamandjaris AA, MacDougall DE, Jones PJ. Medium chain fatty acid metabolism and energy expenditure: obesity treatment implications. Life Sci. 1998; 62: 1203-15. PMID: 9570335.
10. Bach AC, Ingenbleek Y, Frey A. The usefulness of dietary medium-chain triglycerides in body weight control: fact or fancy? J Lipid Res. 1996; 37: 708-26. PMID: 8732772.
11. Geliebter A, Torbay N, Bracco EF, Hashim SA, Van Itallie TB. Overfeeding with medium-chain triglyceride diet results in diminished deposition of fat. Am J Clin Nutr. 1983; 37: 1-4. PMID: 6849272.
12. Baba N, Bracco EF, Hashim SA. Role of brown adipose tissue in thermogenesis induced by overfeeding a diet containing medium chain triglyceride. Lipids. 1987; 22: 442-4. PMID: 3613876.
13. Han J, Hamilton JA, Kirkland JL, Corkey BE, Guo W. Medium-chain oil reduces fat mass and down-regulates expression of adipogenic genes in rats. Obes Res. 2003; 11: 734-44. PMID: 12805394.
14. Tsuji H, Kasai M, Takeuchi H, Nakamura M, Okazaki M, Kondo K. Dietary medium-chain triacylglycerols suppress accumulation of body fat in a double-blind, controlled trial in healthy men and women. J Nutr. 2001; 131: 2853-9. PMID: 11694608.
15. St-Onge MP, Bosarge A, Goree LL, Darnell B. Medium chain triglyceride oil consumption as part of a weight loss diet does not lead to an adverse metabolic profile when compared to olive oil. J Am Coll Nutr. 2008; 27: 547-52. PMID: 18845704.
16. Hu FB, Stampfer MJ, Manson JE, Ascherio A, Colditz GA, Speizer FE, et al. Dietary saturated fats and their food sources in relation to the risk of coronary heart disease in women. Am J Clin Nutr. 1999; 70: 1001-8. PMID: 10584044.
17. 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: 656-60. PMID: 10604470.
18. 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. doi:10.1006/bbrc.2000.4039PMID: 11162448.
19. Howard AD, Feighner SD, Cully DF, Arena JP, Liberator PA, Rosenblum CI, et al. A receptor in pituitary and hypothalamus that functions in growth hormone release. Science. 1996; 273: 974-7. PMID: 8688086.
20. Wang Q, Liu C, Uchida A, Chuang J-C, Walker A, Liu T, et al. Arcuate AgRP neurons mediate orexigenic and glucoregulatory actions of ghrelin. Mol Metab. 2014; 3: 64-72. doi:10.1016/j.molmet.2013.10.001 PMID: 24567905.
21. Delporte C. Structure and physiological actions of ghrelin. Scientifica. 2013; 2013: 518909. doi:10.1155/2013/518909 PMID: 24381790.
22. Zhao T-J, Liang G, Li RL, Xie X, Sleeman MW, Murphy AJ, et al. Ghrelin O-acyltransferase (GOAT) is essential for growth hormone-mediated survival of calorie-restricted mice. Proc Natl Acad Sci. 2010; 107: 7467-7472. doi:10.1073/pnas.1002271107 PMID: 20231469.
23. Gutierrez JA, Solenberg PJ, Perkins DR, Willency JA, Knierman MD, Jin Z, et al. Ghrelin octanoylation mediated by an orphan lipid transferase. Proc Natl Acad Sci U S A. 2008; 105: 6320-5.
24. 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: 387-96. doi:10.1016/j.cell.2008.01.017 PMID: 18267071.
25. Nishi Y, Hiejima H, Hosoda H, Kaiya H, Mori K, Fukue Y, et al. Ingested medium-chain fatty acids are directly utilized for the acyl modification of ghrelin. Endocrinology. 2005; 146: 2255-64. PMID: 15677766.
26. Kirchner H, Gutierrez JA, Solenberg PJ, Pfluger PT, Czyzyk TA, Willency JA, et al. GOAT links dietary lipids with the endocrine control of energy balance. Nat Med. 2009; 15: 741-5. doi:10.1038/nm.1997 PMID: 19503064.
27. Barnett BP, Hwang Y, Taylor MS, Kirchner H, Pfluger PT, Bernard V, et al. Glucose and weight control in mice with a designed ghrelin O-acyltransferase inhibitor. Science. 2010; 330: 1689-92. doi:10.1126/science.1196154 PMID: 21097901.
28. Hosoda H, Kangawa K. Standard sample collections for blood ghrelin measurements. Methods Enzymol. 2012; 514: 113-126. doi:10.1016/B978-0-12-381272-8.00008-8 PMID: 22975050.
29. Chen C-Y, Lee W-J, Chong K, Lee S-D, Liao Y-D. Impact of intracerebroventricular obestatin on plasma acyl ghrelin, des-acyl ghrelin and nesfatin-1 levels, and on gastric emptying in rats. Mol Med Rep. 2012; 6: 191-196. doi:10.3892/mmr.2012.901 PMID: 22562076.
30. Legrand P, Beauchamp E, Catheline D, Pedrono F, Rioux V. Short Chain Saturated Fatty Acids Decrease Circulating Cholesterol and Increase Tissue PUFA Content in the Rat. Lipids. 2010; 45: 975-86. doi:10.1007/s11745-010-3481-5PMID: 20924709.
31. Guillou H, Martin P, Jan S, D'Andrea S, Roulet A, Catheline D, et al. Comparative effect of fenofibrate on hepatic desaturases in wild-type and peroxisome proliferator-activated receptor alpha-deficient mice. Lipids. 2002; 37: 981-9. PMID: 12530558.
32. Rioux V, Catheline D, Bouriel M, Legrand P. Dietary myristic acid at physiologically relevant levels increases the tissue content of C20:5 n-3 and C20:3 n-6 in the rat. Reprod Nutr Dev. 2005; 45: 599-612. PMID: 16188210.
33. Ezanno H, Beauchamp E, Catheline D, Legrand P, Rioux V. Beneficial impact of a mix of dairy fat with rapeseed oil on n-6 and n-3 PUFA metabolism in the rat: A small enrichment in dietary alpha-linolenic acid greatly increases its conversion to DHA in the liver: Better conversion of dietary ALA to DHA when mixed with butterfat. Eur J Lipid Sci Technol. 2015; 117:281-290 doi:10.1002/ejlt.201400304.
34. Rioux V, Pedrono F, Blanchard H, Duby C, Boulier-Monthean N, Bernard L, et al. Trans-vaccenate is Delta13-desaturated by FADS3 in rodents. J Lipid Res. 2013; 54: 3438-52. doi:10.1194/jlr.M042572 PMID: 24070791.
35. Yamauchi T, Waki H, Kamon J, Murakami K, Motojima K, Komeda K, et al. Inhibition of RXR and PPARγ ameliorates diet-induced obesity and type 2 diabetes. J Clin Invest. 2001; 108: 1001-1013. PMID: 11581301.
36. Kubota N, Terauchi Y, Miki H, Tamemoto H, Yamauchi T, Komeda K, et al. PPARγ mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell. 1999; 4: 597-609. PMID: 10549291.
37. Knockaert L, Berson A, Ribault C, Prost P-E, Fautrel A, Pajaud J, et al. Carbon tetrachloride-mediated lipid peroxidation induces early mitochondrial alterations in mouse liver. Lab Invest. 2011; 92: 396-410. doi:10.1038/labinvest.2011.193 PMID: 22157718.
38. Castaneda TR, Tong J, Datta R, Culler M, Tschöp MH. Ghrelin in the regulation of body weight and metabolism. Front Neuroendocrinol. 2010; 31: 44-60. doi:10.1016/j.yfrne.2009.10.008 PMID: 19896496.
39. Chia DJ. Mechanisms of growth hormone-mediated gene regulation. Mol Endocrinol. 2014; Available: http://press.endocrine.org/doi/abs/10.1210/me.2014-1099.
40. 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. PMID: 16679295.
41. Leidy HJ, Dougherty KA, Frye BR, Duke KM, Williams NI. Twenty-four-hour Ghrelin Is Elevated after Calorie Restriction and Exercise Training in Non-obese Women. Obesity. 2007; 15: 446-455. doi:10.1038/oby.2007.542PMID: 17299118.
42. Legrand P, Morise A, Kalonji E. Update of French nutritional recommendations for fatty acids. World Rev Nutr Diet. 2011; 102: 137-43. doi:10.1159/000327800 PMID: 21865827.
43. Zammit VA. Mechanisms of regulation of the partition of fatty acids between oxidation and esterification in the liver. Prog Lipid Res. 1984; 23: 39-67. PMID: 6152703.
44. Carriere F, Barrowman JA, Verger R, Laugier R. Secretion and contribution to lipolysis of gastric and pancreatic lipases during a test meal in humans. Gastroenterology. 1993; 105: 876-888. PMID: 8359655.
45. Gargouri Y, Pieroni G, Rivière C, Lowe PA, Saunière JF, Sarda L, et al. Importance of human gastric lipase for intestinal lipolysis: An in vitro study. Biochim Biophys Acta. 1986; 879: 419-423. PMID: 3778930.
46. Egelrud T, Ollvecrona T, Helander H. Studies on gastric absorption of lipids in the suckling rat. Scand J Gastroenterol. 1971; 6: 329-333. PMID: 5561179.
47. Rioux V, Catheline D, Legrand P. In rat hepatocytes, myristic acid occurs through lipogenesis, palmitic shortening and lauric acid elongation. Animal. 2007; 1: 820-826. doi:10.1017/S1751731107000122PMID: 22444745.
48. Nishi Y, Mifune H, Yabuki A, Tajiri Y, Hirata R, Tanaka E, et al. Changes in Subcellular Distribution of n-Octanoyl or n-Decanoyl Ghrelin in Ghrelin-Producing Cells. Front Endocrinol. 2013; 4: 84. doi:10.3389/fendo.2013.00084.
49. Fukumori R, Sugino T, Shingu H, Moriya N, Kobayashi H, Hasegawa Y, et al. Ingestion of medium chain fatty acids by lactating dairy cows increases concentrations of plasma ghrelin. Domest Anim Endocrinol. 2013; 45: 216-223. doi:10.1016/j.domaniend.2013.09.005 PMID: 24209506.
50. Patterson M, Murphy KG, le Roux CW, Ghatei MA, Bloom SR. Characterization of ghrelin-like immunoreactivity in human plasma. J Clin Endocrinol Metab. 2005; 90: 2205-2211. doi:10.1210/jc.2004-1641 PMID: 15657369.
51. Delhanty PJD, Huisman M, Julien M, Mouchain K, Brune P, Themmen APN, et al. The acylated (AG) to unacylated (UAG) ghrelin ratio in esterase inhibitor-treated blood is higher than previously described. Clin Endocrinol (Oxf). 2015; 82: 142-146. doi:10.1111/cen.12489.
52. Lee H-M, Wang G, Englander EW, Kojima M, Greeley GH Jr. Ghrelin, a new gastrointestinal endocrine peptide that stimulates insulin secretion: enteric distribution, ontogeny, influence of endocrine, and dietary manipulations. Endocrinology. 2002; 143: 185-190. PMID: 11751608.
53. Cummings DE, Foster-Schubert KE, Overduin J. Ghrelin and Energy Balance: Focus on Current Controversies. Curr Drug Targets. 2005; 6: 153-169. doi:10.2174/1389450053174569 PMID: 15777186.
54. Gong Z, Yoshimura M, Aizawa S, Kurotani R, Zigman JM, Sakai T, et al. G protein-coupled receptor 120 signaling regulates ghrelin secretion in vivo and in vitro. Am J Physiol-Endocrinol Metab. 2014; 306: E28-E35. doi:10.1152/ajpendo.00306.2013 PMID: 24222669.
55. Chen W, Enriori PJ. Ghrelin: A journey from GH secretagogue to regulator of metabolism. Transl Gastrointest Cancer. 2014; 4: 14-27.
56. Takagi K, Legrand R, Asakawa A, Amitani H, François M, Tennoune N, et al. Anti-ghrelin immunoglobulins modulate ghrelin stability and its orexigenic effect in obese mice and humans. Nat Commun. 2013; 4. doi:10.1038/ncomms3685.
57. Goebel-Stengel M, Hofmann T, Elbelt U, Teuffel P, Ahnis A, Kobelt P, et al. The ghrelin activating enzyme ghrelin-O-acyltransferase (GOAT) is present in human plasma and expressed dependent on body mass index. Peptides. 2013; 43: 13-19. doi:10.1016/j.peptides.2013.02.011 PMID: 23454172.
58. Janssen S, Laermans J, Iwakura H, Tack J, Depoortere I. Sensing of Fatty Acids for Octanoylation of Ghrelin Involves a Gustatory G-Protein. PLoS ONE. 2012; 7: e40168. doi:10.1371/journal.pone.0040168 PMID: 22768248.
59. Nishi Y, Hiejima H, Mifune H, Sato T, Kangawa K, Kojima M. Developmental changes in the pattern of ghrelin's acyl modification and the levels of acyl-modified ghrelins in murine stomach. Endocrinology. 2005; 146: 2709-2715. doi:10.1210/en.2004-0645 PMID: 15746259.
60. Nishi Y, Mifune H, Kojima M. Ghrelin acylation by ingestion of medium-chain fatty acids. Methods Enzymol. 2012; 514: 303-315. doi:10.1016/B978-0-12-381272-8.00019-2 PMID: 22975061.
61. 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 mRNA levels and body weight in rats. Diabetes. 2001; 50: 2438-2443. PMID: 11679419.
62. Tschöp M, Smiley DL, Heiman ML. Ghrelin induces adiposity in rodents. Nature. 2000; 407: 908-913. doi:10.1038/35038090 PMID: 11057670.
63. Albarran-Zeckler RG, Sun Y, Smith RG. Physiological roles revealed by ghrelin and ghrelin receptor deficient mice. Peptides. 2011; 32: 2229-2235. doi:10.1016/j.peptides.2011.07.003 PMID: 21781995.
64. St-Onge MP, Jones PJ. Physiological effects of medium-chain triglycerides: potential agents in the prevention of obesity. J Nutr. 2002; 132: 329-32. PMID: 11880549.
65. Nagao K, Yanagita T. Medium-chain fatty acids: functional lipids for the prevention and treatment of the metabolic syndrome. Pharmacol Res Off J Ital Pharmacol Soc. 2010; 61: 208-212. doi:10.1016/j.phrs.2009.11.007.
66. Crozier G, Bois-Joyeux B, Chanez M, Girard J, Peret J. Metabolic effects induced by long-term feeding of medium-chain triglycerides in the rat. Metabolism. 1987; 36: 807-814. PMID: 3298941.
67. Ferreira L, Lisenko K, Barros B, Zangeronimo M, Pereira L, Sousa R. Influence of medium-chain triglycerides on consumption and weight gain in rats: A systematic review. J Anim Physiol Anim Nutr. 2014; 98: 1-8. doi:10.1111/jpn.12030.
68. Briggs DI, Andrews ZB. A recent update on the role of ghrelin in glucose homeostasis. Curr Diabetes Rev. 2011; 7: 201-207. PMID: 21539509.
69. Yi C-X, Heppner KM, Kirchner H, Tong J, Bielohuby M, Gaylinn BD, et al. The GOAT-ghrelin system is not essential for hypoglycemia prevention during prolonged calorie restriction. PloS One. 2012; 7: e32100. doi:10.1371/journal.pone.0032100 PMID: 22363801.
70. Zhang Y, Fang F, Goldstein JL, Brown MS, Zhao T-J. Reduced autophagy in livers of fasted, fatdepleted, ghrelin-deficient mice: reversal by growth hormone. Proc Natl Acad Sci U S A. 2015; 112: 1226-1231. doi:10.1073/pnas.1423643112 PMID: 25583513.
71. Kumar R, Salehi A, Rehfeld JF, Höglund P, Lindström E, Håkanson R. Proghrelin peptides: Desacyl ghrelin is a powerful inhibitor of acylated ghrelin, likely to impair physiological effects of acyl ghrelin but not of obestatin A study of pancreatic polypeptide secretion from mouse islets. Regul Pept. 2010; 164: 65-70. doi:10.1016/j.regpep.2010.06.005 PMID: 20619300.
72. Inhoff T, Mönnikes H, Noetzel S, Stengel A, Goebel M, Dinh QT, et al. Desacyl ghrelin inhibits the orexigenic effect of peripherally injected ghrelin in rats. Peptides. 2008; 29: 2159-2168. doi:10.1016/j.peptides.2008.09.014 PMID: 18938204.
73. Han J, Farmer SR, Kirkland JL, Corkey BE, Yoon R, Pirtskhalava T, et al. Octanoate attenuates adipogenesis in 3T3-L1 preadipocytes. J Nutr. 2002; 132: 904-10. PMID: 11983812.
74. Sarda P, Lepage G, Roy CC, Chessex P. Storage of medium-chain triglycerides in adipose tissue of orally fed infants. Am J Clin Nutr. 1987; 45: 399-405. PMID: 3812339.
75. Bays HE, González-Campoy JM, Bray GA, Kitabchi AE, Bergman DA, Schorr AB, et al. Pathogenic potential of adipose tissue and metabolic consequences of adipocyte hypertrophy and increased visceral adiposity. Expert Rev Cardiovasc Ther. 2008; 6: 343-368. doi:10.1586/14779072.6.3.343 PMID: 18327995.
76. Thompson NM, Gill DAS, Davies R, Loveridge N, Houston PA, Robinson ICAF, et al. Ghrelin and desoctanoyl ghrelin promote adipogenesis directly in vivo by a mechanism independent of the type 1a growth hormone secretagogue receptor. Endocrinology. 2004; 145: 234-242. doi:10.1210/en.2003-0899 PMID: 14551228.
77. Toshinai K, Yamaguchi H, Sun Y, Smith RG, Yamanaka A, Sakurai T, et al. Des-Acyl Ghrelin Induces Food Intake by a Mechanism Independent of the Growth Hormone Secretagogue Receptor. Endocrinology. 2006; 147: 2306-2314doi:10.1210/en.2005-1357 PMID: 16484324.
78. Astrup A, Dyerberg J, Elwood P, Hermansen K, Hu FB, Jakobsen MU, et al. The role of reducing intakes of saturated fat in the prevention of cardiovascular disease: Where does the evidence stand in 2010? Am J Clin Nutr. 2011; 93: 684-8. doi:10.3945/ajcn.110.004622 PMID: 21270379.