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Effect of Korean pine nut oil on hepatic iron, copper, and zinc status and expression of genes and proteins related to iron absorption in diet-induced obese mice

  • Shin, Sunhye (Major of Food and Nutrition, Division of Applied Food System, Seoul Women's University) ;
  • Lim, Yeseo (Department of Food and Nutrition, College of Human Ecology, Seoul National University) ;
  • Chung, Jayong (Department of Food and Nutrition, College of Human Ecology, Kyung Hee University) ;
  • Park, Soyoung (Department of Food and Nutrition, College of Human Ecology, Seoul National University) ;
  • Han, Sung Nim (Department of Food and Nutrition, College of Human Ecology, Seoul National University)
  • Received : 2021.06.21
  • Accepted : 2021.09.16
  • Published : 2021.10.31

Abstract

Purpose: Body adiposity is negatively correlated with hepatic iron status, and Korean pine nut oil (PNO) has been reported to reduce adiposity. Therefore, we aimed to study the effects of PNO on adiposity, hepatic mineral status, and the expression of genes and proteins involved in iron absorption. Methods: Five-week-old male C57BL/6 mice were fed a control diet containing 10% kcal from PNO (PC) or soybean oil (SBO; SC), or a high-fat diet (HFD) containing 35% kcal from lard and 10% kcal from PNO (PHFD) or SBO (SHFD). Hepatic iron, copper, and zinc content; and expression of genes and proteins related to iron absorption were measured. Results: HFD-fed mice had a higher white fat mass (2-fold; p < 0.001), lower hepatic iron content (25% lower; p < 0.001), and lower hepatic Hamp (p = 0.028) and duodenal Dcytb mRNA levels (p = 0.037) compared to the control diet-fed mice. Hepatic iron status was negatively correlated with body weight (r = -0.607, p < 0.001) and white fat mass (r = -0.745, p < 0.001). Although the PHFD group gained less body weight (18% less; p < 0.05) and white fat mass (18% less; p < 0.05) than the SHFD group, the hepatic iron status impaired by the HFD feeding did not improve. The expression of hepatic and duodenal ferroportin protein was not affected by the fat amount or the oil type. PNO-fed mice had significantly lower Slc11a2 (p = 0.022) and Slc40a1 expression (p = 0.027) compared to SBO-fed mice. However, the PC group had a higher Heph expression than the SC group (p < 0.05). The hepatic copper and zinc content did not differ between the four diet groups, but hepatic copper content adjusted by body weight was significantly lower in the HFD-fed mice compared to the control diet-fed mice. Conclusion: HFD-induced obesity decreased hepatic iron storage by affecting the regulation of genes related to iron absorption; however, the 18% less white fat mass in the PHFD group was not enough to improve the iron status compared to the SHFD group. The hepatic copper and zinc status was not altered by the fat amount or the oil type.

Keywords

Acknowledgement

This work was supported by the grant from National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (NRF-2010-0024878).

References

  1. Lecube A, Carrera A, Losada E, Hernandez C, Simo R, Mesa J. Iron deficiency in obese postmenopausal women. Obesity (Silver Spring) 2006; 14(10): 1724-1730. https://doi.org/10.1038/oby.2006.198
  2. Moayeri H, Bidad K, Zadhoush S, Gholami N, Anari S. Increasing prevalence of iron deficiency in overweight and obese children and adolescents (Tehran Adolescent Obesity Study). Eur J Pediatr 2006; 165(11): 813-814. https://doi.org/10.1007/s00431-006-0178-0
  3. Amato A, Santoro N, Calabro P, Grandone A, Swinkels DW, Perrone L, et al. Effect of body mass index reduction on serum hepcidin levels and iron status in obese children. Int J Obes 2010; 34(12): 1772-1774. https://doi.org/10.1038/ijo.2010.204
  4. Chung J, Kim MS, Han SN. Diet-induced obesity leads to decreased hepatic iron storage in mice. Nutr Res 2011; 31(12): 915-921. https://doi.org/10.1016/j.nutres.2011.09.014
  5. Park CY, Chung J, Koo KO, Kim MS, Han SN. Hepatic iron storage is related to body adiposity and hepatic inflammation. Nutr Metab (Lond) 2017; 14: 14. https://doi.org/10.1186/s12986-017-0169-3
  6. Chung H, Wu D, Smith D, Meydani SN, Han SN. Lower hepatic iron storage associated with obesity in mice can be restored by decreasing body fat mass through feeding a low-fat diet. Nutr Res 2016; 36(9): 955-963. https://doi.org/10.1016/j.nutres.2016.06.003
  7. Sandstrom B. Micronutrient interactions: effects on absorption and bioavailability. Br J Nutr 2001; 85 Suppl 2: S181-S185. https://doi.org/10.1079/BJN2000312
  8. Anderson GJ, Frazer DM, McLaren GD. Iron absorption and metabolism. Curr Opin Gastroenterol 2009; 25(2): 129-135. https://doi.org/10.1097/MOG.0b013e32831ef1f7
  9. Collins JF, Prohaska JR, Knutson MD. Metabolic crossroads of iron and copper. Nutr Rev 2010; 68(3): 133-147. https://doi.org/10.1111/j.1753-4887.2010.00271.x
  10. Solomons NW, Jacob RA. Studies on the bioavailability of zinc in humans: effects of heme and nonheme iron on the absorption of zinc. Am J Clin Nutr 1981; 34(4): 475-482. https://doi.org/10.1093/ajcn/34.4.475
  11. Haschke F, Ziegler EE, Edwards BB, Fomon SJ. Effect of iron fortification of infant formula on trace mineral absorption. J Pediatr Gastroenterol Nutr 1986; 5(5): 768-773. https://doi.org/10.1097/00005176-198609000-00018
  12. Kennedy ML, Failla ML, Smith JC Jr. Influence of genetic obesity on tissue concentrations of zinc, copper, manganese and iron in mice. J Nutr 1986; 116(8): 1432-1441. https://doi.org/10.1093/jn/116.8.1432
  13. Pasman WJ, Heimerikx J, Rubingh CM, van den Berg R, O'Shea M, Gambelli L, et al. The effect of Korean pine nut oil on in vitro CCK release, on appetite sensations and on gut hormones in post-menopausal overweight women. Lipids Health Dis 2008; 7: 10. https://doi.org/10.1186/1476-511X-7-10
  14. Park S, Lim Y, Shin S, Han SN. Impact of Korean pine nut oil on weight gain and immune responses in high-fat diet-induced obese mice. Nutr Res Pract 2013; 7(5): 352-358. https://doi.org/10.4162/nrp.2013.7.5.352
  15. Le NH, Shin S, Tu TH, Kim CS, Kang JH, Tsuyoshi G, et al. Diet enriched with korean pine nut oil improves mitochondrial oxidative metabolism in skeletal muscle and brown adipose tissue in diet-induced obesity. J Agric Food Chem 2012; 60(48): 11935-11941. https://doi.org/10.1021/jf303548k
  16. Zhu S, Park S, Lim Y, Shin S, Han SN. Korean pine nut oil replacement decreases intestinal lipid uptake while improves hepatic lipid metabolism in mice. Nutr Res Pract 2016; 10(5): 477-486. https://doi.org/10.4162/nrp.2016.10.5.477
  17. Park S, Shin S, Lim Y, Shin JH, Seong JK, Han SN. Korean pine nut oil attenuated hepatic triacylglycerol accumulation in high-fat diet-induced obese mice. Nutrients 2016; 8(1): 59. https://doi.org/10.3390/nu8010059
  18. Nemeth E, Ganz T. Regulation of iron metabolism by hepcidin. Annu Rev Nutr 2006; 26(1): 323-342. https://doi.org/10.1146/annurev.nutr.26.061505.111303
  19. Ouchi N, Ohashi K, Shibata R, Murohara T. Adipocytokines and obesity-linked disorders. Nagoya J Med Sci 2012; 74(1-2): 19-30.
  20. McClung JP, Karl JP. Iron deficiency and obesity: the contribution of inflammation and diminished iron absorption. Nutr Rev 2009; 67(2): 100-104. https://doi.org/10.1111/j.1753-4887.2008.00145.x
  21. Sonnweber T, Ress C, Nairz M, Theurl I, Schroll A, Murphy AT, et al. High-fat diet causes iron deficiency via hepcidin-independent reduction of duodenal iron absorption. J Nutr Biochem 2012; 23(12): 1600-1608. https://doi.org/10.1016/j.jnutbio.2011.10.013
  22. Steele TM, Frazer DM, Anderson GJ. Systemic regulation of intestinal iron absorption. IUBMB Life 2005; 57(7): 499-503. https://doi.org/10.1080/15216540500149904
  23. Kuo YM, Su T, Chen H, Attieh Z, Syed BA, McKie AT, et al. Mislocalisation of hephaestin, a multicopper ferroxidase involved in basolateral intestinal iron transport, in the sex linked anaemia mouse. Gut 2004; 53(2): 201-206. https://doi.org/10.1136/gut.2003.019026
  24. Arredondo M, Munoz P, Mura CV, Nunez MT. DMT1, a physiologically relevant apical Cu1+ transporter of intestinal cells. Am J Physiol Cell Physiol 2003; 284(6): C1525-C1530. https://doi.org/10.1152/ajpcell.00480.2002
  25. Espinoza A, Le Blanc S, Olivares M, Pizarro F, Ruz M, Arredondo M. Iron, copper, and zinc transport: inhibition of divalent metal transporter 1 (DMT1) and human copper transporter 1 (hCTR1) by shRNA. Biol Trace Elem Res 2012; 146(2): 281-286. https://doi.org/10.1007/s12011-011-9243-2
  26. Liuzzi JP, Cousins RJ. Mammalian zinc transporters. Annu Rev Nutr 2004; 24(1): 151-172. https://doi.org/10.1146/annurev.nutr.24.012003.132402
  27. Wyman S, Simpson RJ, McKie AT, Sharp PA. Dcytb (Cybrd1) functions as both a ferric and a cupric reductase in vitro. FEBS Lett 2008; 582(13): 1901-1906. https://doi.org/10.1016/j.febslet.2008.05.010
  28. Dupic F, Fruchon S, Bensaid M, Loreal O, Brissot P, Borot N, et al. Duodenal mRNA expression of iron related genes in response to iron loading and iron deficiency in four strains of mice. Gut 2002; 51(5): 648-653. https://doi.org/10.1136/gut.51.5.648
  29. Frazer DM, Wilkins SJ, Becker EM, Murphy TL, Vulpe CD, McKie AT, et al. A rapid decrease in the expression of DMT1 and Dcytb but not Ireg1 or hephaestin explains the mucosal block phenomenon of iron absorption. Gut 2003; 52(3): 340-346. https://doi.org/10.1136/gut.52.3.340