Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
권호 표지
DOI QR코드

DOI QR Code

Korean pine nut oil replacement decreases intestinal lipid uptake while improves hepatic lipid metabolism in mice

  • Zhu, Shuang (Department of Food and Nutrition, College of Human Ecology, Seoul National University) ;
  • Park, Soyoung (Department of Food and Nutrition, College of Human Ecology, Seoul National University) ;
  • Lim, Yeseo (Department of Food and Nutrition, College of Human Ecology, Seoul National University) ;
  • Shin, Sunhye (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 : 2015.12.31
  • Accepted : 2016.05.17
  • Published : 2016.10.01
Download PDF
⟨ Previous Next ⟩

Abstract

BACKGROUND/OBJECTIVES: Consumption of pine nut oil (PNO) was shown to reduce weight gain and attenuate hepatic steatosis in mice fed a high-fat diet (HFD). The aim of this study was to examine the effects of PNO on both intestinal and hepatic lipid metabolism in mice fed control or HFD. MATERIALS/METHODS: Five-week-old C57BL/6 mice were fed control diets containing 10% energy fat from either Soybean Oil (SBO) or PNO, or HFD containing 15% energy fat from lard and 30% energy fat from SBO or PNO for 12 weeks. Expression of genes related to intestinal fatty acid (FA) uptake and channeling (Cd36, Fatp4, Acsl5, Acbp), intestinal chylomicron synthesis (Mtp, ApoB48, ApoA4), hepatic lipid uptake and channeling (Lrp1, Fatp5, Acsl1, Acbp), hepatic triacylglycerol (TAG) lipolysis and FA oxidation (Atgl, Cpt1a, Acadl, Ehhadh, Acaa1), as well as very low-density lipoprotein (VLDL) assembly (ApoB100) were determined by real-time PCR. RESULTS: In intestine, significantly lower Cd36 mRNA expression (P<0.05) and a tendency of lower ApoA4 mRNA levels (P = 0.07) was observed in PNO-fed mice, indicating that PNO consumption may decrease intestinal FA uptake and chylomicron assembly. PNO consumption tended to result in higher hepatic mRNA levels of Atgl (P = 0.08) and Cpt1a (P = 0.05). Significantly higher hepatic mRNA levels of Acadl and ApoB100 were detected in mice fed PNO diet (P<0.05). These results suggest that PNO could increase hepatic TAG metabolism; mitochondrial fatty acid oxidation and VLDL assembly. CONCLUSIONS: PNO replacement in the diet might function in prevention of excessive lipid uptake by intestine and improve hepatic lipid metabolism in both control diet and HFD fed mice.

Keywords

References

  1. de Wit N, Derrien M, Bosch-Vermeulen H, Oosterink E, Keshtkar S, Duval C, de Vogel-van den Bosch J, Kleerebezem M, Muller M, van der Meer R. Saturated fat stimulates obesity and hepatic steatosis and affects gut microbiota composition by an enhanced overflow of dietary fat to the distal intestine. Am J Physiol Gastrointest Liver Physiol 2012;303:G589-99. https://doi.org/10.1152/ajpgi.00488.2011
  2. Abumrad NA, Davidson NO. Role of the gut in lipid homeostasis. Physiol Rev 2012;92:1061-85. https://doi.org/10.1152/physrev.00019.2011
  3. Nguyen P, Leray V, Diez M, Serisier S, Le Bloc'h J, Siliart B, Dumon H. Liver lipid metabolism. J Anim Physiol Anim Nutr (Berl) 2008;92:272-83. https://doi.org/10.1111/j.1439-0396.2007.00752.x
  4. Kim S, Sohn I, Ahn JI, Lee KH, Lee YS, Lee YS. Hepatic gene expression profiles in a long-term high-fat diet-induced obesity mouse model. Gene 2004;340:99-109. https://doi.org/10.1016/j.gene.2004.06.015
  5. Fabbrini E, Sullivan S, Klein S. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 2010;51:679-89. https://doi.org/10.1002/hep.23280
  6. Turpin SM, Hoy AJ, Brown RD, Rudaz CG, Honeyman J, Matzaris M, Watt MJ. Adipose triacylglycerol lipase is a major regulator of hepatic lipid metabolism but not insulin sensitivity in mice. Diabetologia 2011;54:146-56. https://doi.org/10.1007/s00125-010-1895-5
  7. Green CJ, Hodson L. The influence of dietary fat on liver fat accumulation. Nutrients 2014;6:5018-33. https://doi.org/10.3390/nu6115018
  8. Lee JW, Lee KW, Lee SW, Kim IH, Rhee C. Selective increase in pinolenic acid (all-cis-5,9,12-18:3) in Korean pine nut oil by crystallization and its effect on LDL-receptor activity. Lipids 2004;39:383-7. https://doi.org/10.1007/s11745-004-1242-2
  9. Ferramosca A, Savy V, Einerhand AW, Zara V. Pinus koraiensis seed oil (PinnoThinTM) 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
  10. 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
  11. 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;7:352-8. https://doi.org/10.4162/nrp.2013.7.5.352
  12. Le NH, Shin S, Tu TH, Kim CS, Kang JH, Tsuyoshi G, Teruo K, Han SN, Yu R. 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;60:11935-41. https://doi.org/10.1021/jf303548k
  13. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957;226:497-509.
  14. Petit V, Arnould L, Martin P, Monnot MC, Pineau T, Besnard P, Niot I. Chronic high-fat diet affects intestinal fat absorption and postprandial triglyceride levels in the mouse. J Lipid Res 2007;48:278-87. https://doi.org/10.1194/jlr.M600283-JLR200
  15. Huang W, Liu R, Ou Y, Li X, Qiang O, Yu T, Tang CW. Octreotide promotes weight loss via suppression of intestinal MTP and apoB48 expression in diet-induced obesity rats. Nutrition 2013;29:1259-65. https://doi.org/10.1016/j.nut.2013.01.013
  16. Iqbal J, Hussain MM. Intestinal lipid absorption. Am J Physiol Endocrinol Metab 2009;296:E1183-94. https://doi.org/10.1152/ajpendo.90899.2008
  17. Black DD. Development and physiological regulation of intestinal lipid absorption. I. Development of intestinal lipid absorption: cellular events in chylomicron assembly and secretion. Am J Physiol Gastrointest Liver Physiol 2007;293:G519-24. https://doi.org/10.1152/ajpgi.00189.2007
  18. Lu S, Yao Y, Cheng X, Mitchell S, Leng S, Meng S, Gallagher JW, Shelness GS, Morris GS, Mahan J, Frase S, Mansbach CM, Weinberg RB, Black DD. Overexpression of apolipoprotein A-IV enhances lipid secretion in IPEC-1 cells by increasing chylomicron size. J Biol Chem 2006;281:3473-83. https://doi.org/10.1074/jbc.M502501200
  19. Stan S, Delvin E, Lambert M, Seidman E, Levy E. Apo A-IV: an update on regulation and physiologic functions. Biochim Biophys Acta 2003;1631:177-87. https://doi.org/10.1016/S1388-1981(03)00004-0
  20. Mortimer BC, Beveridge DJ, Martins IJ, Redgrave TG. Intracellular localization and metabolism of chylomicron remnants in the livers of low density lipoprotein receptor-deficient mice and apoEdeficient mice. Evidence for slow metabolism via an alternative apoE-dependent pathway. J Biol Chem 1995;270:28767-76. https://doi.org/10.1074/jbc.270.48.28767
  21. Nestel PJ, Havel RJ, Bezman A. Sites of initial removal of chylomicron triglyceride fatty acids from the blood. J Clin Invest 1962;41:1915-21. https://doi.org/10.1172/JCI104648
  22. Lillis AP, Van Duyn LB, Murphy-Ullrich JE, Strickland DK. LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol Rev 2008;88:887-918. https://doi.org/10.1152/physrev.00033.2007
  23. Masson O, Chavey C, Dray C, Meulle A, Daviaud D, Quilliot D, Muller C, Valet P, Liaudet-Coopman E. LRP1 receptor controls adipogenesis and is up-regulated in human and mouse obese adipose tissue. PLoS One 2009;4:e7422. https://doi.org/10.1371/journal.pone.0007422
  24. Willnow TE. Mechanisms of hepatic chylomicron remnant clearance. Diabet Med 1997;14 Suppl 3:S75-80. https://doi.org/10.1002/(SICI)1096-9136(199708)14:3+3.3.CO;2-0
  25. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 2005;115:1343-51. https://doi.org/10.1172/JCI23621
  26. Hardwick JP, Osei-Hyiaman D, Wiland H, Abdelmegeed MA, Song BJ. PPAR/RXR regulation of fatty acid metabolism and fatty acid omega-hydroxylase (CYP4) isozymes: implications for prevention of lipotoxicity in fatty liver disease. PPAR Res 2009;2009:952734.
  27. Adiels M, Olofsson SO, Taskinen MR, Boren J. Overproduction of very low-density lipoproteins is the hallmark of the dyslipidemia in the metabolic syndrome. Arterioscler Thromb Vasc Biol 2008;28:1225-36. https://doi.org/10.1161/ATVBAHA.107.160192
  28. Grenier-Larouche T, Labbé SM, Noll C, Richard D, Carpentier AC. Metabolic inflexibility of white and brown adipose tissues in abnormal fatty acid partitioning of type 2 diabetes. Int J Obes Suppl 2012;2:S37-42. https://doi.org/10.1038/ijosup.2012.21
  29. Bjorndal B, Burri L, Staalesen V, Skorve J, Berge RK. Different adipose depots: their role in the development of metabolic syndrome and mitochondrial response to hypolipidemic agents. J Obes 2011;2011:490650.
  30. Ong KT, Mashek MT, Bu SY, Greenberg AS, Mashek DG. Adipose triglyceride lipase is a major hepatic lipase that regulates triacylglycerol turnover and fatty acid signaling and partitioning. Hepatology 2011;53:116-26. https://doi.org/10.1002/hep.24006
  31. Guo Y, Jolly RA, Halstead BW, Baker TK, Stutz JP, Huffman M, Calley JN, West A, Gao H, Searfoss GH, Li S, Irizarry AR, Qian HR, Stevens JL, Ryan TP. Underlying mechanisms of pharmacology and toxicity of a novel PPAR agonist revealed using rodent and canine hepatocytes. Toxicol Sci 2007;96:294-309. https://doi.org/10.1093/toxsci/kfm009
  32. van der Leij FR, Bloks VW, Grefhorst A, Hoekstra J, Gerding A, Kooi K, Gerbens F, te Meerman G, Kuipers F. Gene expression profiling in livers of mice after acute inhibition of beta-oxidation. Genomics 2007;90:680-9. https://doi.org/10.1016/j.ygeno.2007.08.004
  33. Millar JS, Stone SJ, Tietge UJ, Tow B, Billheimer JT, Wong JS, Hamilton RL, Farese RV Jr, Rader DJ. Short-term overexpression of DGAT1 or DGAT2 increases hepatic triglyceride but not VLDL triglyceride or apoB production. J Lipid Res 2006;47:2297-305. https://doi.org/10.1194/jlr.M600213-JLR200
  34. Miccoli R, Bianchi C, Penno G, Del Prato S. Insulin resistance and lipid disorders. Future Lipidol 2008;3:651-64. https://doi.org/10.2217/17460875.3.6.651
  35. Heath RB, Karpe F, Milne RW, Burdge GC, Wootton SA, Frayn KN. Selective partitioning of dietary fatty acids into the VLDL TG pool in the early postprandial period. J Lipid Res 2003;44:2065-72. https://doi.org/10.1194/jlr.M300167-JLR200
  36. Geerling JJ, Boon MR, van der Zon GC, van den Berg SA, van den Hoek AM, Lombès M, Princen HM, Havekes LM, Rensen PC, Guigas B. Metformin lowers plasma triglycerides by promoting VLDL-triglyceride clearance by brown adipose tissue in mice. Diabetes 2014;63:880-91. https://doi.org/10.2337/db13-0194
  37. Cooper AD. Hepatic uptake of chylomicron remnants. J Lipid Res 1997;38:2173-92.

Cited by

  1. Acyl-CoA dehydrogenase long chain expression is associated with esophageal squamous cell carcinoma progression and poor prognosis vol.11, pp.None, 2016, https://doi.org/10.2147/ott.s171963
  2. Dietary sn-2 palmitic triacylglycerols reduced faecal lipids, calcium contents and altered lipid metabolism in Sprague-Dawley rats vol.70, pp.4, 2019, https://doi.org/10.1080/09637486.2018.1541968
  3. Tomato seed oil attenuates hyperlipidemia and modulates gut microbiota in C57BL/6J mice vol.11, pp.5, 2020, https://doi.org/10.1039/d0fo00133c
  4. 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 vol.54, pp.5, 2021, https://doi.org/10.4163/jnh.2021.54.5.435