Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2015, Article ID 958217, 17 pages
http://dx.doi.org/10.1155/2015/958217
Research Article

Flaxseed Oil Containing α-Linolenic Acid Ester of Plant Sterol Improved Atherosclerosis in ApoE Deficient Mice

1Department of Nutrition and Food Hygiene, Hubei Key Laboratory of Food Nutrition and Safety, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
2Key Laboratory of Environment and Health, Ministry of Education & Ministry of Environmental Protection and State Key Laboratory of Environmental Health (Incubating), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
3Oil Crops Research Institute, Chinese Academy of Agricultural Sciences, Hubei Key Laboratory of Oil Crops Lipid Chemistry and Nutrition, Hubei University of Technology, Wuhan 430030, China
4School of Food and Pharmaceutical Engineering, Hubei University of Technology, Wuhan 430030, China

Received 17 September 2014; Accepted 5 January 2015

Academic Editor: David Vauzour

Copyright © 2015 Hao Han et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. S. Go, D. Mozaffarian, V. L. Roger et al., “Heart disease and stroke statistics—2014 update: a report from the American Heart Association,” Circulation, vol. 129, no. 3, pp. e28–e292, 2014. View at Publisher · View at Google Scholar
  2. A. Kitamura, H. Noda, M. Nakamura et al., “Association between non-high-density lipoprotein cholesterol levels and the incidence of coronary heart disease among Japanese: the Circulatory Risk in Communities Study (CIRCS),” Journal of Atherosclerosis and Thrombosis, vol. 18, no. 6, pp. 445–463, 2011. View at Google Scholar · View at Scopus
  3. J. L. Witztum and D. Steinberg, “Role of oxidized low density lipoprotein in atherogenesis,” The Journal of Clinical Investigation, vol. 88, no. 6, pp. 1785–1792, 1991. View at Publisher · View at Google Scholar · View at Scopus
  4. M. B. Madsen, A.-M. Jensen, and E. B. Schmidt, “The effect of a combination of plant sterol-enriched foods in mildly hypercholesterolemic subjects,” The American Journal of Clinical Nutrition, vol. 26, no. 6, pp. 792–798, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. Expert Panel on Detection-Evaluation- and Treatment of High Blood Cholesterol in Adults, “Executive summary of the third report of The National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III),” JAMA, vol. 285, no. 19, pp. 2486–2497, 2001. View at Publisher · View at Google Scholar
  6. European Atherosclerosis Society Consensus Panel on Phytosterols, “European Atherosclerosis Society Consensus Panel on Phytosterols, Plant sterols and plant stanols in the management of dyslipidaemia and prevention of cardiovascular disease,” Atherosclerosis, vol. 232, no. 2, pp. 346–360, 2014. View at Google Scholar
  7. D. R. Chirovsky, V. Fedirko, Y. Cui, V. Sazonov, and P. Barter, “Prospective studies on the relationship between high-density lipoprotein cholesterol and cardiovascular risk: a systematic review,” European Journal of Cardiovascular Prevention and Rehabilitation, vol. 16, no. 4, pp. 404–423, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Morrison and J. E. Hokanson, “The independent relationship between triglycerides and coronary heart disease,” Vascular Health and Risk Management, vol. 5, no. 1, pp. 89–95, 2009. View at Google Scholar · View at Scopus
  9. I. Demonty, N. Ebine, X. Jia, and P. J. H. Jones, “Fish oil fatty acid esters of phytosterols alter plasma lipids but not red blood cell fragility in hamsters,” Lipids, vol. 40, no. 7, pp. 695–702, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Noakes, P. M. Clifton, A. M. E. Doornbos, and E. A. Trautwein, “Plant sterol ester-enriched milk and yoghurt effectively reduce serum cholesterol in modestly hypercholesterolemic subjects,” European Journal of Nutrition, vol. 44, no. 4, pp. 214–222, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. D. Hanke, P. Zahradka, S. K. Mohankumar, J. L. Clark, and C. G. Taylor, “A diet high in α-linolenic acid and monounsaturated fatty acids attenuates hepatic steatosis and alters hepatic phospholipid fatty acid profile in diet-induced obese rats,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 89, no. 6, pp. 391–401, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Rodriguez-Leyva, C. M. Dupasquier, R. McCullough, and G. N. Pierce, “The cardiovascular effects of flaxseed and its omega-3 fatty acid, alpha-linolenic acid,” The Canadian Journal of Cardiology, vol. 26, no. 9, pp. 489–496, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Kromhout, E. J. Giltay, and J. M. Geleijnse, “n-3 fatty acids and cardiovascular events after myocardial infarction,” The New England Journal of Medicine, vol. 363, no. 21, pp. 2015–2026, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. M. H. Moghadasian, B. M. McManus, D. V. Godin, B. Rodrigues, and J. J. Frohlich, “Proatherogenic and antiatherogenic effects of probucol and phytosterols in apolipoprotein E-deficient mice: possible mechanisms of action,” Circulation, vol. 99, no. 13, pp. 1733–1739, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Nakashima, A. S. Plump, E. W. Raines, J. L. Breslow, and R. Ross, “ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 14, no. 1, pp. 133–140, 1994. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Qianchun, Z. Pin, H. Qingde et al., “Chemical synthesis of phytosterol esters of polyunsaturated fatty acids with ideal oxidative stability,” European Journal of Lipid Science and Technology, vol. 113, no. 4, pp. 441–449, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. J. J. Eady, T. Orta, M. F. Dennis, M. R. L. Stratford, and J. H. Peacock, “Glutathione determination by the Tietze enzymatic recycling assay and its relationship to cellular radiation response,” British Journal of Cancer, vol. 72, no. 5, pp. 1089–1095, 1995. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Ohkawa, N. Ohishi, and K. Yagi, “Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction,” Analytical Biochemistry, vol. 95, no. 2, pp. 351–358, 1979. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Yusuf, S. Hawken, S. Ounpuu et al., “Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study,” The Lancet, vol. 364, no. 9438, pp. 937–952, 2004. View at Google Scholar
  20. V. Escurriol, M. Cofán, C. Moreno-Iribas et al., “Phytosterol plasma concentrations and coronary heart disease in the prospective Spanish EPIC cohort,” The Journal of Lipid Research, vol. 51, no. 3, pp. 618–624, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. J. G. Canto and A. E. Iskandrian, “Major risk factors for cardiovascular disease: debunking the ‘only 50%’ myth,” The Journal of the American Medical Association, vol. 290, no. 7, pp. 947–949, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. Q. Deng, X. Yu, J. Xu et al., “Effect of flaxseed oil fortified with vitamin E and phytosterols on antioxidant defense capacities and lipids profile in rats,” Journal of Food Science, vol. 77, no. 6, pp. H135–H140, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Yang, P. J. Espenshade, M. E. Wright et al., “Crucial step in cholesterol homeostasis: Sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER,” Cell, vol. 110, no. 4, pp. 489–500, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. J. L. Goldstein, R. B. Rawson, and M. S. Brown, “Mutant mammalian cells as tools to delineate the sterol regulatory element-binding protein pathway for feedback regulation of lipid synthesis,” Archives of Biochemistry and Biophysics, vol. 397, no. 2, pp. 139–148, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. K. M. Boberg, J.-E. Akerlund, and I. Bjorkhem, “Effect of sitosterol on the rate-limiting enzymes in cholesterol synthesis and degradation,” Lipids, vol. 24, no. 1, pp. 9–12, 1989. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. T. Liang, W. T. Wong, L. Guan et al., “Effect of phytosterols and their oxidation products on lipoprotein profiles and vascular function in hamster fed a high cholesterol diet,” Atherosclerosis, vol. 219, no. 1, pp. 124–133, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Castrillo and P. Tontonoz, “Nuclear receptors in macrophage biology: at the crossroads of lipid metabolism and inflammation,” Annual Review of Cell and Developmental Biology, vol. 20, pp. 455–480, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. K. N. Maxwell, R. E. Soccio, E. M. Duncan, E. Sehayek, and J. L. Breslow, “Novel putative SREBP and LXR target genes identified by microarray analysis in liver of cholesterol-fed mice,” Journal of Lipid Research, vol. 44, no. 11, pp. 2109–2119, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. N. Tanaka, X. Zhang, E. Sugiyama et al., “Eicosapentaenoic acid improves hepatic steatosis independent of PPARα activation through inhibition of SREBP-1 maturation in mice,” Biochemical Pharmacology, vol. 80, no. 10, pp. 1601–1612, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. S. D. Clarke, “Nonalcoholic steatosis and steatohepatitis. I. Molecular mechanism for polyunsaturated fatty acid regulation of gene transcription,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 281, no. 4, pp. G865–G869, 2001. View at Google Scholar · View at Scopus
  31. P. P. Devarshi, N. M. Jangale, A. E. Ghule, S. L. Bodhankar, and A. M. Harsulkar, “Beneficial effects of flaxseed oil and fish oil diet are through modulation of different hepatic genes involved in lipid metabolism in streptozotocin-nicotinamide induced diabetic rats,” Genes and Nutrition, vol. 8, no. 3, pp. 329–342, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. K. Nomaguchi, M. Tanaka, E. Misawa et al., “Aloe vera phytosterols act as ligands for PPAR and improve the expression levels of PPAR target genes in the livers of mice with diet-induced obesity,” Obesity Research and Clinical Practice, vol. 5, no. 3, pp. e190–e201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. E. Misawa, M. Tanaka, K. Nomaguchi et al., “Oral ingestion of Aloe vera phytosterols alters hepatic gene expression profiles and ameliorates obesity-associated metabolic disorders in Zucker diabetic fatty rats,” Journal of Agricultural and Food Chemistry, vol. 60, no. 11, pp. 2799–2806, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. J. D. Horton, J. L. Goldstein, and M. S. Brown, “SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver,” The Journal of Clinical Investigation, vol. 109, no. 9, pp. 1125–1131, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Schoonjans, B. Staels, and J. Auwerx, “The peroxisome proliferator activated receptors (PPARs) and their effects on lipid metabolism and adipocyte differentiation,” Biochimica et Biophysica Acta—Lipids and Lipid Metabolism, vol. 1302, no. 2, pp. 93–109, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Libby, “Inflammation in atherosclerosis,” Nature, vol. 420, no. 6917, pp. 868–874, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Libby, “Role of inflammation in atherosclerosis associated with rheumatoid arthritis,” The American Journal of Medicine, vol. 121, no. 10, pp. S21–S31, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Yadav, V. Saini, and S. Arora, “MCP-1: chemoattractant with a role beyond immunity: a review,” Clinica Chimica Acta, vol. 411, no. 21-22, pp. 1570–1579, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Libby, P. M. Ridker, and G. K. Hansson, “Inflammation in atherosclerosis: from pathophysiology to practice,” Journal of the American College of Cardiology, vol. 54, no. 23, pp. 2129–2138, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. P. J. H. Jones, I. Demonty, Y. M. Chan, Y. Herzog, and D. Pelled, “Fish-oil esters of plant sterols differ from vegetable-oil sterol esters in triglycerides lowering, carotenoid bioavailability and impact on plasminogen activator inhibitor-1 (PAI-1) concentrations in hypercholesterolemic subjects,” Lipids in Health and Disease, vol. 6, article 28, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. L. S. Rallidis, G. Paschos, G. K. Liakos, A. H. Velissaridou, G. Anastasiadis, and A. Zampelas, “Dietary alpha-linolenic acid decreases C-reactive protein, serum amyloid A and interleukin-6 in dyslipidaemic patients,” Atherosclerosis, vol. 167, no. 2, pp. 237–242, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. L. S. Rallidis, G. Paschos, M. L. Papaioannou et al., “The effect of diet enriched with α-linolenic acid on soluble cellular adhesion molecules in dyslipidaemic patients,” Atherosclerosis, vol. 174, no. 1, pp. 127–132, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Ferrucci, A. Cherubini, S. Bandinelli et al., “Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers,” Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 2, pp. 439–446, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. D. Pastori, R. Carnevale, and P. Pignatelli, “Is there a clinical role for oxidative stress biomarkers in atherosclerotic diseases?” Internal and Emergency Medicine, vol. 9, no. 2, pp. 123–131, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. A. A. Baskar, K. S. Al Numair, M. Gabriel Paulraj, M. A. Alsaif, M. A. Muamar, and S. Ignacimuthu, “β-sitosterol prevents lipid peroxidation and improves antioxidant status and histoarchitecture in rats with 1,2-dimethylhydrazine-induced colon cancer,” Journal of Medicinal Food, vol. 15, no. 4, pp. 335–343, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. N. M. Jangale, P. P. Devarshi, A. A. Dubal et al., “Dietary flaxseed oil and fish oil modulates expression of antioxidant and inflammatory genes with alleviation of protein glycation status and inflammation in liver of streptozotocin-nicotinamide induced diabetic rats,” Food Chemistry, vol. 141, no. 1, pp. 187–195, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. J. F. Keaney Jr., “Oxidative stress and the vascular wall: NADPH oxidases take center stage,” Circulation, vol. 112, no. 17, pp. 2585–2588, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Kaneto, N. Katakami, M. Matsuhisa, and T.-A. Matsuoka, “Role of reactive oxygen species in the progression of type 2 diabetes and atherosclerosis,” Mediators of Inflammation, vol. 2010, Article ID 453892, 11 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. P. A. Barry-Lane, C. Patterson, M. Van Der Merwe et al., “p47phox is required for atherosclerotic lesion progression in ApoE-/- mice,” The Journal of Clinical Investigation, vol. 108, no. 10, pp. 1513–1522, 2001. View at Publisher · View at Google Scholar · View at Scopus