Botanical oils enriched in n-6 and n-3 FADS2 products are equally effective in preventing atherosclerosis and fatty liver

Journal of Lipid Research

Volumn 56, Issue 6, 2015, Pages 1191-1205

  Shewale, Swapnil V ^a   Boudyguina, Elena ^a   Zhu, Xuewei ^a   Shen, Lulu ^a,c   Hutchins, Patrick M ^b   Barkley, Robert M ^b   Murphy, Robert C ^a,b   Parks, John S ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c JIANGSU NORMAL UNIVERSITY   (China)

Author keywords

Fatty acid desaturase 2; Inflammation; Lipoproteins metabolism; Macrophages monocytes; Mass spectrometry; Supplementary fatty acid metabolism; Very low density lipoprotein

Indexed keywords

ACYL COENZYME A DESATURASE; ACYL COENZYME A DESATURASE 2; ARGINASE 1; BORAGE OIL; ECHIUM OIL; FISH OIL; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERLEUKIN 10; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; LOW DENSITY LIPOPROTEIN CHOLESTEROL; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PALM OIL; UNCLASSIFIED DRUG; VEGETABLE OIL; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL; GAMMA LINOLENIC ACID; LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ATHEROSCLEROSIS; BORAGO; CHEMOTAXIS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DOWN REGULATION; ECHIUM; ECHIUM PLANTAGINEUM; ELAEIS GUINEENSIS; FATTY LIVER; FEMALE; GENE EXPRESSION; HEART PROTECTION; IN VIVO STUDY; LIPID COMPOSITION; LIPOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ANIMAL; ATHEROGENIC DIET; BLOOD; CHEMISTRY; DIET THERAPY; DRUG EFFECTS; GENETICS; HUMAN; KNOCKOUT MOUSE; LIVER; METABOLISM;

ANIMALS; ATHEROSCLEROSIS; CHOLESTEROL, VLDL; DIET, ATHEROGENIC; ECHIUM; FATTY ACID DESATURASES; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; FATTY LIVER; FISH OILS; GAMMA-LINOLENIC ACID; HUMANS; LIVER; MICE; MICE, KNOCKOUT; PLANT OILS; RECEPTORS, LDL;

EID: 84937110167     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M059170     Document Type: Review

References (69)

1. Lloyd-Jones, D., R. Adams, M. Carnethon, G. De Simone, T. B. Ferguson, K. Flegal, E. Ford, K. Furie, A. Go, K. Greenlund, et al. 2009. Heart disease and stroke statistics-2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 119: 480-486.
2. Mozaffarian, D., R. Micha, and S. Wallace. 2010. Effects on coronary heart disease of increasing polyunsaturated fat in place of saturated fat: a systematic review and meta-analysis of randomized controlled trials. PLoS Med. 7: e1000252.
3. Bigger, J. T., Jr., and T. El-Sherif. 2001. Polyunsaturated fatty acids and cardiovascular events: a fish tale. Circulation. 103: 623-625.
4. Calder, P. C., and R. F. Grimble. 2002. Polyunsaturated fatty acids, inflammation and immunity. Eur. J. Clin. Nutr. 56 (Suppl 3) : S14-S19.
5. Kang, J. X., and A. Leaf. 1996. Antiarrhythmic effects of polyunsaturated fatty acids. Recent studies. Circulation. 94: 1774-1780.
6. Parks, J. S., J. Kaduck-Sawyer, B. C. Bullock, and L. L. Rudel. 1990. Effect of dietary fish oil on coronary artery and aortic atherosclerosis in African green monkeys. Arteriosclerosis. 10: 1102-1112.
7. Hu, F. B., L. Bronner, W. C. Willett, M. J. Stampfer, K. M. Rexrode, C. M. Albert, D. Hunter, and J. E. Manson. 2002. Fish and omega-3 fatty acid intake and risk of coronary heart disease in women. JAMA. 287: 1815-1821.
8. Horrobin, D. F. 1993. Fatty acid metabolism in health and disease: the role of delta-6-desaturase. Am. J. Clin. Nutr. 57: 732S-736S; discussion 736S-737S.
9. Degirolamo, C., K. L. Kelley, M. D. Wilson, and L. L. Rudel. 2010. Dietary n-3 LCPUFA from fish oil but not alpha-linolenic acidderived LCPUFA confers atheroprotection in mice. J. Lipid Res. 51: 1897-1905.
10. Harris, W. S., D. Mozaffarian, E. Rimm, P. Kris-Etherton, L. L. Rudel, L. J. Appel, M. M. Engler, M. B. Engler, and F. Sacks. 2009. Omega-6 fatty acids and risk for cardiovascular disease: a science advisory from the American Heart Association Nutrition Subcommittee of the Council on Nutrition, Physical Activity, and Metabolism; Council on Cardiovascular Nursing; and Council on Epidemiology and Prevention. Circulation. 119: 902-907.
11. Degirolamo, C., G. S. Shelness, and L. L. Rudel. 2009. LDL cholesteryl oleate as a predictor for atherosclerosis: evidence from human and animal studies on dietary fat. J. Lipid Res. 50 (Suppl) : S434-S439.
12. Farvid, M. S., M. Ding, A. Pan, Q. Sun, S. E. Chiuve, L. M. Steffen, W. C. Willett, and F. B. Hu. 2014. Dietary linoleic acid and risk of coronary heart disease: a systematic review and meta-analysis of prospective cohort studies. Circulation. 130: 1568-1578.
13. Harris, W. S., and G. C. Shearer. 2014. Omega-6 fatty acids and cardiovascular disease: friend or foe? Circulation. 130: 1562-1564.
14. Chopra, J., and R. O. Webster. 1988. PGE1 inhibits neutrophil adherence and neutrophil-mediated injury to cultured endothelial cells. Am. Rev. Respir. Dis. 138: 915-920.
15. Jones, D. A., and F. A. Fitzpatrick. 1990. "Suicide" inactivation of thromboxane A2 synthase. Characteristics of mechanism-based inactivation with isolated enzyme and intact platelets. J. Biol. Chem. 265: 20166-20171.
16. Zhang, P., E. Boudyguina, M. D. Wilson, A. K. Gebre, and J. S. Parks. 2008. Echium oil reduces plasma lipids and hepatic lipogenic gene expression in apoB100-only LDL receptor knockout mice. J. Nutr. Biochem. 19: 655-663.
17. Brown, A. L., X. Zhu, S. Rong, S. Shewale, J. Seo, E. Boudyguina, A. K. Gebre, M. A. Alexander-Miller, and J. S. Parks. 2012. Omega-3 fatty acids ameliorate atherosclerosis by favorably altering monocyte subsets and limiting monocyte recruitment to aortic lesions. Arterioscler. Thromb. Vasc. Biol. 32: 2122-2130.
18. Rudel, L. L., K. Kelley, J. K. Sawyer, R. Shah, and M. D. Wilson. 1998. Dietary monounsaturated fatty acids promote aortic atherosclerosis in LDL receptor-null, human ApoB100-overexpressing transgenic mice. Arterioscler. Thromb. Vasc. Biol. 18: 1818-1827.
19. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
20. Bi, X., X. Zhu, C. Gao, S. Shewale, Q. Cao, M. Liu, E. Boudyguina, A. K. Gebre, M. D. Wilson, A. L. Brown, et al. 2014. Myeloid cell-specific ATP-binding cassette transporter A1 deletion has minimal impact on atherogenesis in atherogenic diet-fed low-density lipoprotein receptor knockout mice. Arterioscler. Thromb. Vasc. Biol. 34: 1888-1899.
21. Zhu, X., J. Y. Lee, J. M. Timmins, J. M. Brown, E. Boudyguina, A. Mulya, A. K. Gebre, M. C. Willingham, E. M. Hiltbold, N. Mishra, et al. 2008. Increased cellular free cholesterol in macrophage-specific Abca1 knock-out mice enhances pro-inflammatory response of macrophages. J. Biol. Chem. 283: 22930-22941.
22. Millar, J. S., D. A. Cromley, M. G. McCoy, D. J. Rader, and J. T. Billheimer. 2005. Determining hepatic triglyceride production in mice: comparison of poloxamer 407 with Triton WR-1339. J. Lipid Res. 46: 2023-2028.
23. Carr, T. P., C. J. Andresen, and L. L. Rudel. 1993. Enzymatic determination of triglyceride, free cholesterol, and total cholesterol in tissue lipid extracts. Clin. Biochem. 26: 39-42.
24. Hattori, M., A. Tugores, L. Veloz, M. Karin, and D. A. Brenner. 1990. A simplified method for the preparation of transcriptionally active liver nuclear extracts. DNA Cell Biol. 9: 777-781.
25. Lee, J. H., P. Giannikopoulos, S. A. Duncan, J. Wang, C. T. Johansen, J. D. Brown, J. Plutzky, R. A. Hegele, L. H. Glimcher, and A. H. Lee. 2011. The transcription factor cyclic AMP-responsive element-binding protein H regulates triglyceride metabolism. Nat. Med. 17: 812-815.
26. Jeon, T. I., R. M. Esquejo, M. Roqueta-Rivera, P. E. Phelan, Y. A. Moon, S. S. Govindarajan, C. C. Esau, and T. F. Osborne. 2013. An SREBP-responsive microRNA operon contributes to a regulatory loop for intracellular lipid homeostasis. Cell Metab. 18: 51-61.
27. Rong, S., Q. Cao, M. Liu, J. Seo, L. Jia, E. Boudyguina, A. K. Gebre, P. L. Colvin, T. L. Smith, R. C. Murphy, et al. 2012. Macrophage 12/15 lipoxygenase expression increases plasma and hepatic lipid levels and exacerbates atherosclerosis. J. Lipid Res. 53: 686-695.
28. Hutchins, P. M., E. E. Moore, and R. C. Murphy. 2011. Electrospray MS/MS reveals extensive and nonspecific oxidation of cholesterol esters in human peripheral vascular lesions. J. Lipid Res. 52: 2070-2083.
29. Murphy, R. C., R. M. Barkley, K. Zemski Berry, J. Hankin, K. Harrison, C. Johnson, J. Krank, A. McAnoy, C. Uhlson, and S. Zarini. 2005. Electrospray ionization and tandem mass spectrometry of eicosanoids. Anal. Biochem. 346: 1-42.
30. Maurya, M. R., S. Gupta, X. Li, E. Fahy, A. R. Dinasarapu, M. Sud, H. A. Brown, C. K. Glass, R. C. Murphy, D. W. Russell, et al. 2013. Analysis of inflammatory and lipid metabolic networks across RAW264.7 and thioglycolate-elicited macrophages. J. Lipid Res. 54: 2525-2542.
31. Zhu, X., M. M. Westcott, X. Bi, M. Liu, K. M. Gowdy, J. Seo, Q. Cao, A. K. Gebre, M. B. Fessler, E. M. Hiltbold, et al. 2012. Myeloid cellspecific ABCA1 deletion protects mice from bacterial infection. Circ. Res. 111: 1398-1409.
32. Chung, S., J. M. Timmins, M. Duong, C. Degirolamo, S. Rong, J. K. Sawyer, R. R. Singaraja, M. R. Hayden, N. Maeda, L. L. Rudel, et al. 2010. Targeted deletion of hepatocyte ABCA1 leads to very low density lipoprotein triglyceride overproduction and low density lipoprotein hypercatabolism. J. Biol. Chem. 285: 12197-12209.
33. Brown, J. M., S. Chung, J. K. Sawyer, C. Degirolamo, H. M. Alger, T. M. Nguyen, X. Zhu, M. N. Duong, A. L. Brown, C. Lord, et al. 2010. Combined therapy of dietary fish oil and stearoyl-CoA desaturase 1 inhibition prevents the metabolic syndrome and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 30: 24-30.
34. Parks, J. S., F. L. Johnson, M. D. Wilson, and L. L. Rudel. 1990. Effect of fish oil diet on hepatic lipid metabolism in nonhuman primates: lowering of secretion of hepatic triglyceride but not apoB. J. Lipid Res. 31: 455-466.
35. Parks, J. S., M. D. Wilson, F. L. Johnson, and L. L. Rudel. 1989. Fish oil decreases hepatic cholesteryl ester secretion but not apoB secretion in African green monkeys. J. Lipid Res. 30: 1535-1544.
36. Nagy, L., P. Tontonoz, J. G. Alvarez, H. Chen, and R. M. Evans. 1998. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell. 93: 229-240.
37. Ricote, M., A. C. Li, T. M. Willson, C. J. Kelly, and C. K. Glass. 1998. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature. 391: 79-82.
38. Bell 3rd, T. A., K. Kelley, M. D. Wilson, J. K. Sawyer, and L. L. Rudel. 2007. Dietary fat-induced alterations in atherosclerosis are abolished by ACAT2-deficiency in ApoB100 only, LDLr-/- mice. Arterioscler. Thromb. Vasc. Biol. 27: 1396-1402.
39. Rudel, L. L., F. L. Johnson, J. K. Sawyer, M. S. Wilson, and J. S. Parks. 1995. Dietary polyunsaturated fat modifies low-density lipoproteins and reduces atherosclerosis of nonhuman primates with high and low diet responsiveness. Am. J. Clin. Nutr. 62: 463S-470S.
40. Rudel, L. L., J. S. Parks, and J. K. Sawyer. 1995. Compared with dietary monounsaturated and saturated fat, polyunsaturated fat protects African green monkeys from coronary artery atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 15: 2101-2110.
41. Forrest, L. M., E. Boudyguina, M. D. Wilson, and J. S. Parks. 2012. Echium oil reduces atherosclerosis in apoB100-only LDLrKO mice. Atherosclerosis. 220: 118-121.
42. Sala, A., G. Folco, and R. C. Murphy. 2010. Transcellular biosynthesis of eicosanoids. Pharmacol. Rep. 62: 503-510.
43. Thornburg, J. T., J. S. Parks, and L. L. Rudel. 1995. Dietary fatty acid modification of HDL phospholipid molecular species alters lecithin: cholesterol acyltransferase reactivity in cynomolgus monkeys. J. Lipid Res. 36: 277-289.
44. Rett, B. S., and J. Whelan. 2011. Increasing dietary linoleic acid does not increase tissue arachidonic acid content in adults consuming Western-type diets: a systematic review. Nutr. Metab. (Lond). 8: 36.
45. Demmelmair, H., B. Iser, A. Rauh-Pfeiffer, and B. Koletzko. 1999. Comparison of bolus versus fractionated oral applications of [13C]-linoleic acid in humans. Eur. J. Clin. Invest. 29: 603-609.
46. Hussein, N., E. Ah-Sing, P. Wilkinson, C. Leach, B. A. Griffin, and D. J. Millward. 2005. Long-chain conversion of [13C]linoleic acid and alpha-linolenic acid in response to marked changes in their dietary intake in men. J. Lipid Res. 46: 269-280.
47. Mathias, R. A., S. Sergeant, I. Ruczinski, D. G. Torgerson, C. E. Hugenschmidt, M. Kubala, D. Vaidya, B. Suktitipat, J. T. Ziegler, P. Ivester, et al. 2011. The impact of FADS genetic variants on omega6 polyunsaturated fatty acid metabolism in African Americans. BMC Genet. 12: 50.
48. Hester, A. G., R. C. Murphy, C. J. Uhlson, P. Ivester, T. C. Lee, S. Sergeant, L. R. Miller, T. D. Howard, R. A. Mathias, and F. H. Chilton. 2014. Relationship between a common variant in the fatty acid desaturase (FADS) cluster and eicosanoid generation in humans. J. Biol. Chem. 289: 22482-22489.
49. VanderLaan, P. A., C. A. Reardon, R. A. Thisted, and G. S. Getz. 2009. VLDL best predicts aortic root atherosclerosis in LDL receptor deficient mice. J. Lipid Res. 50: 376-385.
50. Skålén, K., M. Gustafsson, E. K. Rydberg, L. M. Hultén, O. Wiklund, T. L. Innerarity, and J. Borén. 2002. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature. 417: 750-754.
51. Melchior, J. T., J. K. Sawyer, K. L. Kelley, R. Shah, M. D. Wilson, R. R. Hantgan, and L. L. Rudel. 2013. LDL particle core enrichment in cholesteryl oleate increases proteoglycan binding and promotes atherosclerosis. J. Lipid Res. 54: 2495-2503.
52. Thomas, M. J., T. Thornburg, J. Manning, K. Hooper, and L. L. Rudel. 1994. Fatty acid composition of low-density lipoprotein influences its susceptibility to autoxidation. Biochemistry. 33: 1828-1834.
53. Whitman, S. C., J. R. Fish, M. L. Rand, and K. A. Rogers. 1994. n-3 fatty acid incorporation into LDL particles renders them more susceptible to oxidation in vitro but not necessarily more atherogenic in vivo. Arterioscler. Thromb. 14: 1170-1176.
54. Moore, K. J., and I. Tabas. 2011. Macrophages in the pathogenesis of atherosclerosis. Cell. 145: 341-355.
55. Yvan-Charvet, L., C. Welch, T. A. Pagler, M. Ranalletta, M. Lamkanfi, S. Han, M. Ishibashi, R. Li, N. Wang, and A. R. Tall. 2008. Increased inflammatory gene expression in ABC transporterdeficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation. 118: 1837-1847.
56. Bell 3rd, T. A., M. D. Wilson, K. Kelley, J. K. Sawyer, and L. L. Rudel. 2007. Monounsaturated fatty acyl-coenzyme A is predictive of atherosclerosis in human apoB-100 transgenic, LDLr-/- mice. J. Lipid Res. 48: 1122-1131.
57. Jump, D. B., and S. D. Clarke. 1999. Regulation of gene expression by dietary fat. Annu. Rev. Nutr. 19: 63-90.
58. Ou, J., H. Tu, B. Shan, A. Luk, R. A. DeBose-Boyd, Y. Bashmakov, J. L. Goldstein, and M. S. Brown. 2001. Unsaturated fatty acids inhibit transcription of the sterol regulatory element-binding protein-1c (SREBP-1c) gene by antagonizing ligand-dependent activation of the LXR. Proc. Natl. Acad. Sci. USA. 98: 6027-6032.
59. Hannah, V. C., J. Ou, A. Luong, J. L. Goldstein, and M. S. Brown. 2001. Unsaturated fatty acids down-regulate srebp isoforms 1a and 1c by two mechanisms in HEK-293 cells. J. Biol. Chem. 276: 4365-4372.
60. Chen, G., G. Liang, J. Ou, J. L. Goldstein, and M. S. Brown. 2004. Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proc. Natl. Acad. Sci. USA. 101: 11245-11250.
61. Xu, J., M. Teran-Garcia, J. H. Park, M. T. Nakamura, and S. D. Clarke. 2001. Polyunsaturated fatty acids suppress hepatic sterol regulatory element-binding protein-1 expression by accelerating transcript decay. J. Biol. Chem. 276: 9800-9807.
62. Botolin, D., Y. Wang, B. Christian, and D. B. Jump. 2006. Docosahexaneoic acid (22:6,n-3) regulates rat hepatocyte SREBP-1 nuclear abundance by Erk- and 26S proteasome-dependent pathways. J. Lipid Res. 47: 181-192.
63. Rioux, F. M., and S. M. Innis. 1992. Arachidonic acid concentrations in plasma and liver phospholipid and cholesterol esters of piglets raised on formulas with different linoleic and linolenic acid contents. Am. J. Clin. Nutr. 56: 106-112.
64. Moon, Y. A., R. E. Hammer, and J. D. Horton. 2009. Deletion of ELOVL5 leads to fatty liver through activation of SREBP-1c in mice. J. Lipid Res. 50: 412-423.
65. Lukivskaya, O. Y., E. Naruta, V. Sadovnichy, S. Kirko, and V. U. Buko. 2012. Reversal of experimental ethanol-induced liver steatosis by borage oil. Phytother. Res. 26: 1626-1631.
66. Brown, J. M., S. Chung, J. K. Sawyer, C. Degirolamo, H. M. Alger, T. Nguyen, X. Zhu, M. N. Duong, A. L. Wibley, R. Shah, et al. 2008. Inhibition of stearoyl-coenzyme A desaturase 1 dissociates insulin resistance and obesity from atherosclerosis. Circulation. 118: 1467-1475.
67. Reagan-Shaw, S., M. Nihal, and N. Ahmad. 2008. Dose translation from animal to human studies revisited. FASEB J. 22: 659-661.
68. Rizos, E. C., E. E. Ntzani, E. Bika, M. S. Kostapanos, and M. S. Elisaf. 2012. Association between omega-3 fatty acid supplementation and risk of major cardiovascular disease events: a systematic review and meta-analysis. JAMA. 308: 1024-1033.
69. Kris-Etherton, P. M., W. S. Harris, and L. J. Appel; American Heart Association Nutrition Committee. 2002. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation. 106: 2747-2757.