DOI QR코드

DOI QR Code

Impact of Korean pine nut oil on weight gain and immune responses in high-fat diet-induced obese mice

  • Park, Soyoung ;
  • Lim, Yeseo ;
  • Shin, Sunhye ;
  • Han, Sung Nim
  • Received : 2013.03.29
  • Accepted : 2013.05.20
  • Published : 2013.10.01

Abstract

Korean pine nut oil (PNO) has been reported to have favorable effects on lipid metabolism and appetite control. We investigated whether PNO consumption could influence weight gain, and whether the PNO-induced effect would result in an improvement of immune function in high-fat diet (HFD)-induced obese mice. C57BL/6 mice were fed control diets with 10% energy fat from either PNO or soybean oil (SBO), or HFDs with 45% energy fat from 10% PNO or SBO and 35% lard, 20% PNO or SBO and 25% lard, or 30% PNO or SBO and 15% lard for 12 weeks. The proliferative responses of splenocytes upon stimulation with concanavalin A (Con A) or lipopolysaccharide (LPS), Con A-stimulated production of interleukin (IL)-2 and interferon (IFN)-${\gamma}$, and LPS-stimulated production of IL-6, IL-$1{\beta}$, and prostaglandin $E_2$ ($PGE_2$) by splenocytes were determined. Consumption of HFDs containing PNO resulted in significantly less weight gain (17% less, P < 0.001), and lower weight gain was mainly due to less white adipose tissue (18% less, P = 0.001). The reduction in weight gain did not result in the overall enhancement in splenocyte proliferation. Overall, PNO consumption resulted in a higher production of IL-$1{\beta}$ (P = 0.04). Replacement of SBO with PNO had no effect on the production of IL-2, IFN-${\gamma}$, IL-6, or $PGE_2$ in mice fed with either the control diets or HFDs. In conclusion, consumption of PNO reduced weight gain in mice fed with HFD, but this effect did not result in the overall improvement in immune responses.

Keywords

Pine nut oil;obesity;high-fat diet;immune response;inflammatory cytokine

References

  1. Hughes GM, Boyland EJ, Williams NJ, Mennen L, Scott C, Kirkham TC, Harrold JA, Keizer HG, Halford JC. The effect of Korean pine nut oil ($PinnoThin^{TM}$) on food intake, feeding behaviour and appetite: a double-blind placebo-controlled trial. Lipids Health Dis 2008;7:6. https://doi.org/10.1186/1476-511X-7-6
  2. Rural Development Administration, National Academy of Agricultural Science. Food Composition Table. 8th rev. ed. Suwon: National Academy of Agricultural Science; 2011.
  3. Wolff RL, Pedrono F, Pasquier E, Marpeau AM. General characteristics of Pinus spp. seed fatty acid compositions, and importance of delta5-olefinic acids in the taxonomy and phylogeny of the genus. Lipids 2000;35:1-22. https://doi.org/10.1007/s11745-000-0489-y
  4. Asset G, Baugé E, Wolff RL, Fruchart JC, Dallongeville J. Pinus pinaster oil affects lipoprotein metabolism in apolipoprotein E-deficient mice. J Nutr 1999;129:1972-8. https://doi.org/10.1093/jn/129.11.1972
  5. Asset G, Staels B, Wolff RL, Baugé E, Madj Z, Fruchart JC, Dallongeville J. Effects of Pinus pinaster and Pinus koraiensis seed oil supplementation on lipoprotein metabolism in the rat. Lipids 1999;34:39-44. https://doi.org/10.1007/s11745-999-335-2
  6. Sugano M, Ikeda I, Wakamatsu K, Oka T. Influence of Korean pine (Pinus koraiensis)-seed oil containing cis-5,cis-9,cis-12- octadecatrienoic acid on polyunsaturated fatty acid metabolism, eicosanoid production and blood pressure of rats. Br J Nutr 1994;72:775-83. https://doi.org/10.1079/BJN19940079
  7. Pasman WJ, Heimerikx J, Rubingh CM, van den Berg R, O'Shea M, Gambelli L, Hendriks HF, Einerhand AW, Scott C, Keizer HG, Mennen LI. 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
  8. Galli C, Calder PC. Effects of fat and fatty acid intake on inflammatory and immune responses: a critical review. Ann Nutr Metab 2009;55:123-39. https://doi.org/10.1159/000228999
  9. Kapoor R, Huang YS. Gamma linolenic acid: an antiinflammatory omega-6 fatty acid. Curr Pharm Biotechnol 2006;7:531-4. https://doi.org/10.2174/138920106779116874
  10. Milner JJ, Beck MA. The impact of obesity on the immune response to infection. Proc Nutr Soc 2012;71:298-306. https://doi.org/10.1017/S0029665112000158
  11. Tanaka T, Hattori T, Kouchi M, Hirano K, Satouchi K. Methyleneinterrupted double bond in polyunsaturated fatty acid is an essential structure for metabolism by the fatty acid chain elongation system of rat liver. Biochim Biophys Acta 1998;1393: 299-306. https://doi.org/10.1016/S0005-2760(98)00084-8
  12. Chuang LT, Tsai PJ, Lee CL, Huang YS. Uptake and incorporation of pinolenic acid reduces n-6 polyunsaturated fatty acid and downstream prostaglandin formation in murine macrophage. Lipids 2009;44:217-24. https://doi.org/10.1007/s11745-008-3276-0
  13. Matsuo N, Osada K, Kodama T, Lim BO, Nakao A, Yamada K, Sugano M. Effects of gamma-linolenic acid and its positional isomer pinolenic acid on immune parameters of Brown-Norway rats. Prostaglandins Leukot Essent Fatty Acids 1996;55:223-9. https://doi.org/10.1016/S0952-3278(96)90002-2
  14. Weber DJ, Rutala WA, Samsa GP, Santimaw JE, Lemon SM. Obesity as a predictor of poor antibody response to hepatitis B plasma vaccine. JAMA 1985;254:3187-9. https://doi.org/10.1001/jama.1985.03360220053027
  15. Nieman DC, Henson DA, Nehlsen-Cannarella SL, Ekkens M, Utter AC, Butterworth DE, Fagoaga OR. Influence of obesity on immune function. J Am Diet Assoc 1999;99:294-9. https://doi.org/10.1016/S0002-8223(99)00077-2
  16. Ahmed T, Das SK, Golden JK, Saltzman E, Roberts SB, Meydani SN. Calorie restriction enhances T-cell-mediated immune response in adult overweight men and women. J Gerontol A Biol Sci Med Sci 2009;64A:1107-13. https://doi.org/10.1093/gerona/glp101
  17. Tanaka S, Isoda F, Ishihara Y, Kimura M, Yamakawa T. T lymphopaenia in relation to body mass index and TNF-alpha in human obesity: adequate weight reduction can be corrective. Clin Endocrinol (Oxf) 2001;54:347-54.
  18. Sato Mito N, Suzui M, Yoshino H, Kaburagi T, Sato K. Long term effects of high fat and sucrose diets on obesity and lymphocyte proliferation in mice. J Nutr Health Aging 2009;13:602-6. https://doi.org/10.1007/s12603-009-0170-2
  19. Ferramosca A, Savy V, Einerhand AWC, Zara V. Pinus koraiensis seed oil ($PinnoThin^{TM}$) supplementation reduces body weight gain and lipid concentration in liver and plasma of mice. J Anim Feed Sci 2008;17:621-30. https://doi.org/10.22358/jafs/66690/2008
  20. Tanaka T, Takimoto T, Morishige J, Kikuta Y, Sugiura T, Satouchi K. Non-methylene-interrupted polyunsaturated fatty acids: effective substitute for arachidonate of phosphatidylinositol. Biochem Biophys Res Commun 1999;264:683-8. https://doi.org/10.1006/bbrc.1999.1559
  21. Lamas O, Marti A, Martinez JA. Obesity and immunocompetence. Eur J Clin Nutr 2002;56 Suppl 3:S42-5.
  22. Moriguchi S, Kato M, Sakai K, Yamamoto S, Shimizu E. Decreased mitogen response of splenic lymphocytes in obese Zucker rats is associated with the decreased expression of glucose transporter 1 (GLUT-1). Am J Clin Nutr 1998;67:1124-9. https://doi.org/10.1093/ajcn/67.6.1124
  23. Mito N, Hosoda T, Kato C, Sato K. Change of cytokine balance in diet-induced obese mice. Metabolism 2000;49:1295-300. https://doi.org/10.1053/meta.2000.9523
  24. Han SN, Jeon KJ, Kim MS, Kim HK, Lee AJ. Obesity with a body mass index under 30 does not significantly impair the immune response in young adults. Nutr Res 2011;31:362-9. https://doi.org/10.1016/j.nutres.2011.04.002
  25. Jolly CA. Dietary restriction and immune function. J Nutr 2004; 134:1853-6. https://doi.org/10.1093/jn/134.8.1853
  26. Joseph SB, Miner KT, Croft M. Augmentation of naive, Th1 and Th2 effector CD4 responses by IL-6, IL-1 and TNF. Eur J Immunol 1998;28:277-89. https://doi.org/10.1002/(SICI)1521-4141(199801)28:01<277::AID-IMMU277>3.0.CO;2-8
  27. Fritsche KL, Johnston PV. Effect of dietary $\alpha$-linolenic acid on growth, metastasis, fatty acid profile and prostaglandin production of two murine mammary adenocarcinomas. J Nutr 1990;120: 1601-9. https://doi.org/10.1093/jn/120.12.1601
  28. Ben-Sasson SZ, Hu-Li J, Quiel J, Cauchetaux S, Ratner M, Shapira I, Dinarello CA, Paul WE. IL-1 acts directly on CD4 T cells to enhance their antigen-driven expansion and differentiation. Proc Natl Acad Sci U S A 2009;106:7119-24. https://doi.org/10.1073/pnas.0902745106
  29. Marshall LA, Johnston PV. Modulation of tissue prostaglandin synthesizing capacity by increased ratios of dietary alpha-linolenic acid to linoleic acid. Lipids 1982;17:905-13. https://doi.org/10.1007/BF02534586
  30. Fritsche KL, Johnston PV. Modulation of eicosanoid production and cell-mediated cytotoxicity by dietary α-linolenic acid in BALB/c mice. Lipids 1989;24:305-11. https://doi.org/10.1007/BF02535168
  31. Winnik S, Lohmann C, Richter EK, Schafer N, Song WL, Leiber F, Mocharla P, Hofmann J, Klingenberg R, Boren J, Becher B, Fitzgerald GA, Luscher TF, Matter CM, Beer JH. Dietary $\alpha$ -linolenic acid diminishes experimental atherogenesis and restricts T cell-driven inflammation. Eur Heart J 2011;32:2573-84. https://doi.org/10.1093/eurheartj/ehq501

Cited by

  1. Essential oil of Pinus koraiensis inhibits cell proliferation and migration via inhibition of p21-activated kinase 1 pathway in HCT116 colorectal cancer cells vol.14, pp.1, 2014, https://doi.org/10.1186/1472-6882-14-275
  2. Anti-atherosclerosis effect of pine nut oil in high-cholesterol and high-fat diet fed rats and its mechanism studies in human umbilical vein endothelial cells vol.24, pp.1, 2015, https://doi.org/10.1007/s10068-015-0043-x
  3. Korean pine nut oil replacement decreases intestinal lipid uptake while improves hepatic lipid metabolism in mice vol.10, pp.5, 2016, https://doi.org/10.4162/nrp.2016.10.5.477
  4. Pinolenic Acid Downregulates Lipid Anabolic Pathway in HepG2 Cells vol.51, pp.7, 2016, https://doi.org/10.1007/s11745-016-4149-6
  5. Effects of Pine Nut (Pinus koraiensis) Meal Protein Peptides on Memory Function of Mice vol.881-883, pp.1662-8985, 2014, https://doi.org/10.4028/www.scientific.net/AMR.881-883.815
  6. Time-restricted feeding of a high-fat diet in male C57BL/6 mice reduces adiposity but does not protect against increased systemic inflammation vol.43, pp.10, 2018, https://doi.org/10.1139/apnm-2017-0706

Acknowledgement

Supported by : National Research Foundation (NRF)