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Absorption of Dietary Cholesterol Oxidation Products and Their Downstream Metabolic Effects Are Reduced by Dietary Apple Polyphenols

  • Original Article
  • Published:
Lipids

Abstract

Exogenous and endogenous cholesterol oxidation products (COPs) perturb various metabolic processes, and thereby they may induce various homeostasis-related disorders. Here, we observed that procyanidin-rich dietary apple polyphenol (APP) from unripe apples alleviates the perturbation of lipid metabolism by decreasing the exogenous COP levels in rats. Dietary COPs may be the greatest source of COPs found in the human body. Rats (4 weeks of age) were fed AIN-purified diets containing 0.3% COPs supplemented with 0.5 or 2.5% APP for 3 weeks. Dietary APP alleviated the growth inhibition action of the exogenous COPs. The modulations of the liver lipid profile by COPs remained unchanged. However, serum total cholesterol, high-density lipoprotein cholesterol, and triglyceride levels increased following the intake of dietary APP. Further, dietary APP inhibited the increase in lipid peroxide levels in the liver and serum by COPs. The activity of hepatic Δ6 desaturase was lowered by dietary APP in a dose-dependent manner, although exogenous COPs generally increased the activity of this enzyme. In keeping with this observation, Δ6 desaturation indices in the phospholipids and cholesteryl esters of the liver and serum lipids were lower in the APP-fed groups than those in the control group. Dietary APP also promoted the excretion of exogenous COPs, cholesterol, and acidic steroids in feces. Therefore, the inhibition of intestinal absorption of COPs may partly contribute to the alleviation of the perturbation of lipid metabolism and lipid peroxidation levels. Thus, APP may be an important removal agent of exogenous toxic material such as COPs contained in processed or fast foods.

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Abbreviations

APP:

Apple polyphenol

COP:

Cholesterol oxidation product

FID:

Flame ionization detector

GLC:

Gas–liquid chromatography

HDL:

High-density lipoprotein

HMG-CoA:

3-Hydroxy-3-methylglutarylcoenzyme A

HPLC:

High-performance liquid chromatography

6-Keto-PGF1α :

6-Ketoprostaglandin F1α

mRNA:

Messenger RNA

PC:

Phosphatidylcholine

PE:

Phosphatidylethanoleamine

PGI2 :

Prostacyclin

SOD:

Superoxide dismutase

TBARS:

Thiobarbituric acid reactive substances

References

  1. Paniangvait P, King AJ, Jones AD, German BG (1995) Cholesterol oxides in foods of animal origin. J Food Sci 60:1159–1174

    Article  CAS  Google Scholar 

  2. Lake RJ, Scholes P (1997) Quality and consumption of oxidized lipids from deep-frying fats and oils in New Zealand. J Am Oil Chem 74:1065–1068

    CAS  Google Scholar 

  3. Lake RJ, Scholes P (1997) Consumption of cholesterol oxides from fast foods fried in beef fat in New Zealand. J Am Oil Chem 74:1069–1075

    CAS  Google Scholar 

  4. Osada K, Sasaki E, Sugano M (1994) Lymphatic absorption of oxidized cholesterol in rats. Lipids 29:555–559

    Article  PubMed  CAS  Google Scholar 

  5. Osada K, Kodama T, Cui L, Ito Y, Sugano M (1994) Effects of dietary oxidized cholesterol on lipid metabolism in differently aged rats. Biosci Biotechnol Biochem 58:1062–1069

    Article  CAS  Google Scholar 

  6. Osada K, Kodama T, Noda S, Yamada K, Sugano M (1995) Oxidized cholesterol modulates age-related change in lipid metabolism in rats. Lipids 30:405–413

    Article  PubMed  CAS  Google Scholar 

  7. Osada K, Kodama T, Yamada K, Nakamura S, Sugano M (1998) Dietary oxidized cholesterol modulates cholesterol metabolism in rats fed high-cholesterol diet. Lipids 33:757–764

    Article  PubMed  CAS  Google Scholar 

  8. Smith LL, Johonson BH (1989) Biological activities of oxysterols. Free Radic Biol Med 7:285–352

    Article  PubMed  CAS  Google Scholar 

  9. Osada K, Inoue T, Nakamura S, Sugano M (1999) Dietary soybean protein moderates the deleterious disturbance of lipid metabolism caused by exogenous oxidized cholesterol in rats. Biochim Biophys Acta 1427:337–350

    PubMed  CAS  Google Scholar 

  10. Matsumoto N, Okushio K, Hara Y (1998) Effect of black tea polyphenols on plasma lipids in cholesterol-fed rats. J Nutr Sci Vitaminol 44:337–342

    PubMed  CAS  Google Scholar 

  11. Vidal R, Hernandez-Vallejo S, Pauquai T, Texier O, Rousset M, Chambaz J, Demignot S, Lacorte JM (2005) Apple procyanidins decrease cholesterol esterification and lipoprotein secretion in Caco-2/TC7 enterocytes. J Lipid Res 46:258–268

    Article  PubMed  CAS  Google Scholar 

  12. Ikeda I, Imasato Y, Sasaki E, Nakayama M, Nagao H, TakeoT, Yayabe F, Sugano M (1992) Tea catechins decrease micellar solubility and intestinal absorption of cholesterol in rat. Biochim Biophys Acta 1127:141–146

    PubMed  CAS  Google Scholar 

  13. Yang TT, Koo MW (2000) Chinese green tea lowers cholesterol level through an increase in fecal lipid excretion. Life Sci 66:411–423

    Article  PubMed  CAS  Google Scholar 

  14. Leth T, Jusrensen U (1998) Analysis of flavonoids in fruits, vegetables and beverages by HPLC-UV and LC-MS and estimation of the total daily flavonoids intake in Denmark. In: Amado R, Andersson H, Bardocz S, Serra F (eds) Polyphenols in food. Office for official publications of the European communities, Luxembourg, pp 39–40

    Google Scholar 

  15. Macheix JJ, Fleuriet A, Billot J (1990) Changes and metabolism of phenolic compounds in fruits. In: Macheix JJ, Fleuriet A, Billot J (eds) Fruit phenolics. CRC, Boca Raton, pp 149–237

    Google Scholar 

  16. Ohnishi-Kameyama M, Yanagida A, Kanda K, Nagata T (1997) Identification of catechin oligomers from apple (Malus pumila cv. Fuji) in matrix-associated laser desorption/ionization time-of-flight mass spectrometry and fast-atom bombardment mass spectrometry. Rapid Commun Mass Spectrom 11:31–36

    Article  PubMed  CAS  Google Scholar 

  17. American Institute of Nutrition (1997) Report of the AIN Ad Hoc committee on standard for nutritional studies. J Nutr 107:1340–1348

    Google Scholar 

  18. Sevensson L (1988) The effect of dietary partially hydrogenated marine oils on desaturation of fatty acids in rats. Lipids 18:171–178

    Article  Google Scholar 

  19. Lowry OH, Rosebsough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  20. Oyanagui Y (1984) Reevaluation of assay methods and establishment of kit for superoxide dismutase activity. Anal Biochem 142:290–296

    Article  PubMed  CAS  Google Scholar 

  21. Yagi K (1976) A simple fluorometric assay for lipoperoxides in blood plasma. Biochem Med 15:212–216

    Article  PubMed  CAS  Google Scholar 

  22. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  PubMed  CAS  Google Scholar 

  23. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–506

    PubMed  CAS  Google Scholar 

  24. Kawakami Y, Tsurugasaki W, Yoshida Y, Igarashi Y, Nakamura S, Osada K (2004) Regulative actions of dietary soy isoflavone on biological antioxidative system and lipid metabolism in rats. J Agric Food Chem 52:1764–1768

    Article  PubMed  CAS  Google Scholar 

  25. Ikeda I, Tomari Y, Sugano M (1989) Interrelated effects of dietary fiber and fat on lymphatic cholesterol and triglyceride absorption in rats. J Nutr 119:1383–1387

    PubMed  CAS  Google Scholar 

  26. Sugano M, Yamada Y, Yoshida K, Hashimoto Y, Matsuo T, Kimoto M (1988) The hypocholesterolemic action of the undigested fraction of soybean protein in rats. Atherosclerosis 172:115–112

    Article  Google Scholar 

  27. Osada K, Kodama T, Yamada K, Sugano M (1993) Oxidation of cholesterol by heating. J Agric Food Chem 41:1198–1202

    Article  CAS  Google Scholar 

  28. Bruckner GG, Lokesh B, German B, Kinsella JE (1984) Biosynthesis of prostanoids, tissue fatty acid composition and thrombotic parameters in rats fed diets enriched with docosahexaenoic (22:6n-3) or eicosapentaenoic (20:5n-3) acid. Thromb Res 34:479–497

    Article  PubMed  CAS  Google Scholar 

  29. Duncan DB (1955) Multiple range and multiple F test. Biometrics 11:1–42

    Article  Google Scholar 

  30. Nakatsugawa K, Kaneda T (1980) Absorption of methyl linolate hydroperoxides in rabbit. J Jpn Oil Chem Soc 30:74–77

    Google Scholar 

  31. Nakatsugawa K, Kaneda T (1983) Absorption and metabolism of methyllinolate hydroperoxides in rat. J Jpn Oil Chem Soc 32:361–366

    CAS  Google Scholar 

  32. Kandutsch AA, Heiniger HJ, Chen HW (1977) Effects of 25-hydroxycholesterol and 7-ketocholesterol, inhibitor of sterol synthesis, administered orally to mice. Biochim Biophys Acta 486:260–272

    PubMed  CAS  Google Scholar 

  33. Koba K, Wakamatsu K, Obata K, Sugano M (1993) Effects of dietary proteins on linoleic acid desaturation and membrane fluidity in rats liver microsomes. Lipids 28:457–464

    Article  PubMed  CAS  Google Scholar 

  34. Hochgraf E, Mokady S, Cogan U (1997). Dietary oxidized linoleic acid modifies lipid composition of rat liver microsomes and increases their fluidity. J Nutr 127:681–686

    PubMed  CAS  Google Scholar 

  35. Lahous Z, Astruc ME, Crastes de Paulet A (1988) Serum-induced arachidonic acid release and prostaglandin biosynthesis are potentiated by oxygenated sterols in NRK 49F cells. Biochim Biophys Acta 958:396–404

    Google Scholar 

  36. Lahous Z, Vial H, Michel F, Crastes de Paulet A, Astruc ME (1991) Oxysterol activation of arachidonic acid release and prostaglandin E2 biosynthesis in NRK 49F cells is partially dependent on protein kinase C activity. Cell Signal 3:559–567

    Article  Google Scholar 

  37. Ruzaidi A, Amin I, Nawalyah AG, Hamid M, Faizul HA (2005) The effect of Malaysian cocoa extract on glucose levels and lipid profiles in diabetic rats. J Ethnopharmacol 98:55–60

    Article  PubMed  CAS  Google Scholar 

  38. Kobayashi M, Unno T, Suzuki Y, Nozawa A, Sagesaka Y, Kakuda T, Ikeda I (2005) Heat-epimerized tea catechin disease prevention. In: Rodriguez H, Cutler RG (eds) Critical reviews of oxidative stress and aging, advances in basic science, diagnostics and intervention, vol 1. World Scientific, Singapore, pp 640–660

  39. Osada K, Suzuki T, Sami M, Ohta Y, Kanda T, Ikeda M (2006) Dose-dependent hypocholesterolemic actions of dietary apple polyphenol in rats fed cholesterol. Lipids 41:133–140

    Article  CAS  PubMed  Google Scholar 

  40. Bagchi D, Preuss HG (2002) Oligomeric proanthocyanidins in human health and disease prevention. In: Rodriguez H, Cutler RG (eds) Critical reviews of oxidative stress and aging, advances in basic science, diagnostics and intervention, vol 1. World Scientific, Singapore, pp 640–660

  41. Shoji T, Masumoto S, Moriichi N, Akiyama H, Kanda T, Ohtake Y, Goda Y (2006) Apple procyanidin oligomers absorption in rats after oral administration: analysis of procyanidins in plasma using the porter method and high-performance liquid chromatography/tandem mass spectrometry. J Agric Food Chem 54:884–892

    Article  PubMed  CAS  Google Scholar 

  42. Anderson JW, Gustafson NJ (1988) Hypocholesterolemic effects of oat and bean products. Am J Clin Nutr 48:749–753

    PubMed  CAS  Google Scholar 

  43. Ogata S, Fujimoto K, Iwakiri R, Matsunaga C, Ogawa Y, Koyama T, Sakai T (1997) Effect of polydextrose on absorption of triglyceride and cholesterol in mesenteric lymph-fistula rats. Proc Soc Exp Biol Med 215:53-58

    PubMed  CAS  Google Scholar 

  44. Hamada T, Goto H, Yamahira T, Sugawara T, Imaizumi K, Ikeda I (2006) Solubility in and affinity for the bile salt micelle of plant sterols are important determinants of their intestinal absorption in rats. Lipids 41:551–556

    Article  PubMed  CAS  Google Scholar 

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Author information

Author notes

  1. Yamato Ogino

    Present address: Fukushima Laboratory, TOAEIYO Co. Ltd, 1 Tanaka, Yuno-aza, Izaka-cho, Fukushima, 960-0280, Japan

Authors and Affiliations

  1. Faculty of Agriculture and Life Science, Hirosaki University, 3 Bunkyo-cho, Hirosaki, Aomori, 036-8561, Japan

    Yamato Ogino, Kyoichi Osada & Shingo Nakamura

  2. Fundamental Research Laboratory, Asahi Breweries Ltd, 1-21 Midori 1-chome, Moriya, Ibaraki, 302-0106, Japan

    Yutaka Ohta & Tomomasa Kanda

  3. Faculty of Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka, 821-8581, Japan

    Michihiro Sugano

Authors
  1. Yamato Ogino
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  2. Kyoichi Osada
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  3. Shingo Nakamura
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  4. Yutaka Ohta
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  6. Michihiro Sugano
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Correspondence to Kyoichi Osada.

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Ogino, Y., Osada, K., Nakamura, S. et al. Absorption of Dietary Cholesterol Oxidation Products and Their Downstream Metabolic Effects Are Reduced by Dietary Apple Polyphenols. Lipids 42, 151–161 (2007). https://doi.org/10.1007/s11745-006-3008-2

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  • DOI: https://doi.org/10.1007/s11745-006-3008-2

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