Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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Naringenin stimulates cholecystokinin secretion in STC-1 cells

  • Park, Min (Division of Metabolism and Functionality Research, Korea Food Research Institute) ;
  • Kim, Kyong (Division of Metabolism and Functionality Research, Korea Food Research Institute) ;
  • Lee, Yu Mi (Division of Metabolism and Functionality Research, Korea Food Research Institute) ;
  • Rhyu, Mee Ra (Division of Metabolism and Functionality Research, Korea Food Research Institute) ;
  • Kim, Hye Young (Division of Metabolism and Functionality Research, Korea Food Research Institute)
  • Received : 2013.08.07
  • Accepted : 2013.12.05
  • Published : 2014.04.01
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Abstract

BACKGROUND/OBJECTIVES: Cholecystokinin (CCK), a hormone or neuropeptide, is secreted in response to intraluminal nutrients by enteroendocrine I-cells of the intestine and has important physiological actions related to appetite regulation and satiety. The stimulation on CCK secretion from the intestine is of potential relevance for body weight management. Naringenin (4',5,7-trihydroxyflavanone) and its glycoside naringin (naringenin 7-rhamnoglucoside) have been reported to have many biological functions. In the current study, we investigated the question of whether naringenin and naringin could stimulate CCK secretion and then examined the mechanisms involved in CCK release. MATERIALS/METHODS: STC-1 cells were used as a model of enteroendocrine cells. CCK release and changes in intracellular $Ca^{2+}$ ($[Ca^{2+}]_i$) were measured after incubation of cells with naringenin and naringin for 1 h. RESULTS: Naringenin caused significant (P < 0.05) stimulation of CCK secretion, but naringin did not. In addition, regarding the secretory mechanisms, naringenin-induced CCK secretion involved increases in $[Ca^{2+}]_i$, influx of extracellular $Ca^{2+}$, at least in part, and activation of TRP channels, including TRPA1. CONCLUSION: Findings of this study suggest that naringenin could have a role in appetite regulation and satiety.

Keywords

References

  1. Hand KV, Bruen CM, O'Halloran F, Giblin L, Green BD. Acute and chronic effects of dietary fatty acids on cholecystokinin expression, storage and secretion in enteroendocrine STC-1 cells. Mol Nutr Food Res 2010;54 Suppl 1:S93-103. https://doi.org/10.1002/mnfr.200900343
  2. Dockray GJ. Chapter 4-Gastrointestinal hormones: gastrin, cholecystokinin, somatostatin, and ghrelin. In: Johnson LR, Barret KE, Gishan FK, Merchant JL, Said HM, Wood JD, editors. Physiology of the Gastrointestinal Tract. Vol. 1. New York (NY): Elsevier Academic Press; 2006. p.91-120.
  3. Chen MC, Wu SV, Reeve JR Jr, Rozengurt E. Bitter stimuli induce $Ca^{2+}$ signaling and CCK release in enteroendocrine STC-1 cells: role of L-type voltage-sensitive $Ca^{2+}$ channels. Am J Physiol Cell Physiol 2006;291:C726-39. https://doi.org/10.1152/ajpcell.00003.2006
  4. Purhonen AK, Louhivuori LM, Kiehne K, Kerman KE, Herzig KH. TRPA1 channel activation induces cholecystokinin release via extracellular calcium. FEBS Lett 2008;582:229-32. https://doi.org/10.1016/j.febslet.2007.12.005
  5. Erlund I. Review of the flavonoids quercetin, hesperetin, and naringenin. Dietary sources, bioactivities, bioavailability, and epidemiology. Nutr Res 2004;24:851-74. https://doi.org/10.1016/j.nutres.2004.07.005
  6. Li XH, Xiong ZL, Lu S, Zhang Y, Li FM. Pharmacokinetics of naringin and its metabolite naringenin in rats after oral administration of Rhizoma drynariae extract assayed by UPLC-MS/MS. Chin J Nat Med 2010;8:40-6. https://doi.org/10.3724/SP.J.1009.2010.00040
  7. Van Acker FA, Schouten O, Haenen GR, van der Vijgh WJ, Bast A. Flavonoids can replace alpha-tocopherol as an antioxidant. FEBS Lett 2000;473:145-8. https://doi.org/10.1016/S0014-5793(00)01517-9
  8. Guthrie N, Carroll KK. Inhibition of mammary cancer by citrus flavonoids. Adv Exp Med Biol 1998;439:227-36. https://doi.org/10.1007/978-1-4615-5335-9_16
  9. Mulvihill EE, Huff MW. Antiatherogenic properties of flavonoids: implications for cardiovascular health. Can J Cardiol 2010;26 Suppl A:17A-21A. https://doi.org/10.1016/S0828-282X(10)71056-4
  10. Borradaile NM, de Dreu LE, Huff MW. Inhibition of net HepG2 cell apolipoprotein B secretion by the citrus flavonoid naringenin involves activation of phosphatidylinositol 3-kinase, independent of insulin receptor substrate-1 phosphorylation. Diabetes 2003;52: 2554-61. https://doi.org/10.2337/diabetes.52.10.2554
  11. Mulvihill EE, Allister EM, Sutherland BG, Telford DE, Sawyez CG, Edwards JY, Markle JM, Hegele RA, Huff MW. Naringenin prevents dyslipidemia, apolipoprotein B overproduction, and hyperinsulinemia in LDL receptor-null mice with diet-induced insulin resistance. Diabetes 2009;58:2198-210. https://doi.org/10.2337/db09-0634
  12. Choi JS, Yokozawa T, Oura H. Improvement of hyperglycemia and hyperlipemia in streptozotocin-diabetic rats by a methanolic extract of Prunus davidiana stems and its main component, prunin. Planta Med 1991;57:208-11. https://doi.org/10.1055/s-2006-960075
  13. Ortiz-Andrade RR, Sanchez-Salgado JC, Navarrete-Vazquez G, Webster SP, Binnie M, Garcia-Jimenez S, Leon-Rivera I, CigarroaVazquez P, Villalobos-Molina R, Estrada-Soto S. Antidiabetic and toxicological evaluations of naringenin in normoglycaemic and NIDDM rat models and its implications on extra-pancreatic glucose regulation. Diabetes Obes Metab 2008;10:1097-104. https://doi.org/10.1111/j.1463-1326.2008.00869.x
  14. Kannappan S, Anuradha CV. Naringenin enhances insulin-stimulated tyrosine phosphorylation and improves the cellular actions of insulin in a dietary model of metabolic syndrome. Eur J Nutr 2010; 49:101-9. https://doi.org/10.1007/s00394-009-0054-6
  15. Benavente-Garcia O, Castillo J. Update on uses and properties of citrus flavonoids: new findings in anticancer, cardiovascular, and anti-inflammatory activity. J Agric Food Chem 2008;56:6185-205. https://doi.org/10.1021/jf8006568
  16. Jung UJ, Lee MK, Jeong KS, Choi MS. The hypoglycemic effects of hesperidin and naringin are partly mediated by hepatic glucoseregulating enzymes in C57BL/KsJ-db/db mice. J Nutr 2004;134: 2499-503. https://doi.org/10.1093/jn/134.10.2499
  17. Jung UJ, Lee MK, Park YB, Kang MA, Choi MS. Effect of citrus flavonoids on lipid metabolism and glucose-regulating enzyme mRNA levels in type-2 diabetic mice. Int J Biochem Cell Biol 2006;38: 1134-45. https://doi.org/10.1016/j.biocel.2005.12.002
  18. Pu P, Gao DM, Mohamed S, Chen J, Zhang J, Zhou XY, Zhou NJ, Xie J, Jiang H. Naringin ameliorates metabolic syndrome by activating AMP-activated protein kinase in mice fed a high-fat diet. Arch Biochem Biophys 2012;518:61-70. https://doi.org/10.1016/j.abb.2011.11.026
  19. Kim HY, Park M, Kim K, Lee YM, Rhyu MR. Hesperetin stimulates cholecystokinin secretion in enteroendocrine STC-1 cells. Biomol Ther (Seoul) 2013;21:121-5. https://doi.org/10.4062/biomolther.2012.077
  20. Zhu BW, Li DM, Zhou DY, Han S, Yang JF, Li T, Ye WX, Greeley GH. Structural analysis and CCK-releasing activity of a sulphated polysaccharide from abalone (Haliotis Discus Hannai Ino) viscera. Food Chem 2011;125:1273-8. https://doi.org/10.1016/j.foodchem.2010.10.065
  21. Le Neve B, Foltz M, Daniel H, Gouka R. The steroid glycoside H.g.-12 from Hoodia gordonii activates the human bitter receptor TAS2R14 and induces CCK release from HuTu-80 cells. Am J Physiol Gastrointest Liver Physiol 2010;299:G1368-75. https://doi.org/10.1152/ajpgi.00135.2010

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