N-3 fatty acids decrease arterial low-density lipoprotein cholesterol delivery and lipoprotein lipase levels in insulin-resistant mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 30, Issue 12, 2010, Pages 2510-2517

  Chang, Chuchun L ^a   Seo, Toru ^a   Du, Christine B ^a   Accili, Domenico ^a   Deckelbaum, Richard J ^a  

^a Columbia University ^*  (United States)

Author keywords

atherosclerosis; diet; fish oils; insulin resistance; LDL; lipoprotein lipase; n 3 fatty acids

Indexed keywords

CHOLESTEROL ESTER; LIPOPROTEIN; LIPOPROTEIN LIPASE; LOW DENSITY LIPOPROTEIN CHOLESTEROL; OMEGA 3 FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA MEDIA; ARTICLE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DIET; INSULIN RESISTANCE; INTIMA; KNOCKOUT MOUSE; LIPID TRANSPORT; LIPOPROTEIN BLOOD LEVEL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANTIGENS, CD; AORTA; AORTIC DISEASES; APOLIPOPROTEINS B; ATHEROSCLEROSIS; BODY WEIGHT; CHOLESTEROL, LDL; CORN OIL; DIETARY FATS; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FISH OILS; HUMANS; INSULIN; INSULIN RESISTANCE; LIPOPROTEIN LIPASE; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; PLANT OILS; RECEPTOR, INSULIN; SAFFLOWER OIL; TIME FACTORS;

EID: 78650419086     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.110.215848     Document Type: Article

References (45)

1. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med. 1998;339:229-234.
2. Nigro J, Osman N, Dart AM, Little PJ. Insulin resistance and atherosclerosis. Endocr Rev. 2006;27:242-259.
3. De Vries R, Borggreve SE, Dullaart RP. Role of lipases, lecithin:choles-terol acyltransferase and cholesteryl ester transfer protein in abnormal high density lipoprotein metabolism in insulin resistance and type 2 diabetes mellitus. Clin Lab. 2003;49:601-613.
4. Sartippour MR, Renier G. Upregulation of macrophage lipoprotein lipase in patients with type 2 diabetes: role of peripheral factors. Diabetes. 2000;49:597-602.
5. Seo T, Qi K, Chang C, Liu Y, Worgall TS, Ramakrishnan R, Deckelbaum RJ. Saturated fat-rich diet enhances selective uptake of LDL cholesteryl esters in the arterial wall. J Clin Invest. 2005;115:2214-2222.
6. Chang CL, Seo T, Matsuzaki M, Worgall TS, Deckelbaum RJ. n-3 fatty acids reduce arterial LDL-cholesterol delivery and arterial lipoprotein lipase levels and lipase distribution. Arterioscler Thromb Vasc Biol. 2009;29:555-561.
7. Seo T, Al-Haideri M, Treskova E, Worgall TS, Kako Y, Goldberg IJ, Deckelbaum RJ. Lipoprotein lipase-mediated selective uptake from low density lipoprotein requires cell surface proteoglycans and is independent of scavenger receptor class B type 1. J Biol Chem. 2000;275: 30355-30362.
8. Rinninger F, Brundert M, Jackle S, Kaiser T, Greten H. Selective uptake of low-density lipoprotein-associated cholesteryl esters by human fibro-blasts, human HepG2 hepatoma cells and J774 macrophages in culture. Biochim Biophys Acta. 1995;1255:141-153.
9. Seo T, Velez-Carrasco W, Qi K, Hall M, Worgall TS, Johnson RA, Deckelbaum RJ. Selective uptake from LDL is stimulated by unsaturated fatty acids and modulated by cholesterol content in the plasma membrane: role of plasma membrane composition in regulating non-SR-BI-mediated selective lipid transfer. Biochemistry. 2002;41:7885-7894.
10. Okamoto H, Nakae J, Kitamura T, Park BC, Dragatsis I, Accili D. Transgenic rescue of insulin receptor-deficient mice. J Clin Invest. 2004; 114:214-223.
11. Yagyu H, Chen G, Yokoyama M, Hirata K, Augustus A, Kako Y, Seo T, Hu Y, Lutz EP, Merkel M, Bensadoun A, Homma S, Goldberg IJ. Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J Clin Invest. 2003;111:419-426.
12. Lachmanovich E, Shvartsman DE, Malka Y, Botvin C, Henis YI, Weiss AM. Co-localization analysis of complex formation among membrane proteins by computerized fluorescence microscopy: application to immu-nofluorescence co-patching studies. J Microsc. 2003;212:122-131.
13. Feng B, Zhang D, Kuriakose G, Devlin CM, Kockx M, Tabas I. Niemann-Pick C heterozygosity confers resistance to lesional necrosis and macrophage apoptosis in murine atherosclerosis. Proc Natl Acad Sci USA. 2003;100:10423-10428.
14. Abramoff MD, Magelhaes PJ, Ram SJ. Image processing with Image J. J Biophotonics Int. 2004;11:36-42.
15. Merat S, Casanada F, Sutphin M, Palinski W, Reaven PD. Western-type diets induce insulin resistance and hyperinsulinemia in LDL receptor-deficient mice but do not increase aortic atherosclerosis compared with normoinsulinemic mice in which similar plasma cholesterol levels are achieved by a fructoserich diet. Arterioscler Thromb Vasc Biol. 1999; 19:1223-1230.
16. Rumsey SC, Obunike JC, Arad Y, Deckelbaum RJ, Goldberg IJ. Lipoprotein lipase-mediated uptake and degradation of low density lipoproteins by fibro-blasts and macrophages. J Clin Invest. 1992;90:1504-1512.
17. Williams KJ, Fless GM, Petrie KA, Snyder ML, Brocia RW, Swenson TL. Mechanisms by which lipoprotein lipase alters cellular metabolism of lipoprotein (a), low density lipoprotein, and nascent lipoproteins: roles for low density lipoprotein receptors and heparan sulfate proteoglycans. J Biol Chem. 1992;267:13284-13292.
18. Li L, Beauchamp MC, Renier G. Peroxisome proliferator-activated receptor alpha and gamma agonists upregulate human macrophage lipoprotein lipase expression. Atherosclerosis. 2002;165:101-110.
19. Hayek T, Hussein K, Aviram M, Coleman R, Keidar S, Pavoltzky E, Kaplan M. Macrophage foam-cell formation in streptozotocin-induced diabetic mice: stimulatory effect of glucose. Atherosclerosis. 2005;183: 25-33.
20. Hu FB, Cho E, Rexrode KM, Albert CM, Manson JE. Fish and long-chain omega-3 fatty acid intake and risk of coronary heart disease and total mortality in diabetic women. Circulation. 2003;107:1852-1857.
21. Breslow JL. n-3 Fatty acids and cardiovascular disease. Am J Clin Nutr. 2006;83:1477S-1482S.
22. Deckelbaum RJ, Worgall TS, Seo T. n-3 Fatty acids and gene expression. Am J Clin Nutr. 2006;83:1520S-1525S.
23. Mozaffarian D, Rimm EB. Fish intake, contaminants, and human health: evaluating the risks and the benefits. JAMA. 2006;296:1885-1899.
24. Wang C, Harris WS, Chung M, Lichtenstein AH, Balk EM, Kupelnick B, Jordan HS, Lau J. n-3 Fatty acids from fish or fish-oil supplements, but not alpha-linolenic acid, benefit cardiovascular disease outcomes in primary- and secondary-prevention studies: a systematic review. Am J Clin Nutr. 2006;84:5-17.
25. Harris WS. n-3 Fatty acids and serum lipoproteins: animal studies. Am J Clin Nutr. 1997;65:1611S-1616S.
26. Han S, Liang CP, DeVries-Seimon T, Ranalletta M, Welch CL, Collins-Fletcher K, Accili D, Tabas I, Tall AR. Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions. Cell Metab. 2006;3:257-266.
27. Han S, Liang CP, Westerterp M, Senokuchi T, Welch CL, Wang Q, Matsumoto M, Accili D, Tall AR. Hepatic insulin signaling regulates VLDL secretion and atherogenesis in mice. J Clin Invest. 2009;119: 1029-1041.
28. Kim JK, Michael MD, Previs SF, Peroni OD, Mauvais-Jarvis F, Neschen S, Kahn BB, Kahn CR, Shulman GI. Redistribution of substrates to adipose tissue promotes obesity in mice with selective insulin resistance in muscle. J Clin Invest. 2000;105:1791-1797.
29. Haeusler RA, Accili D. The double life of Irs. Cell Metab. 2008;8:7-9.
30. Lee JY, Sohn KH, Rhee SH, Hwang D. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J Biol Chem. 2001;276: 16683-16689.
31. Lee JY, Ye J, Gao Z, Youn HS, Lee WH, Zhao L, Sizemore N, Hwang DH. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J Biol Chem. 2003;278:37041-37051.
32. Lee JY, Zhao L, Youn HS, Weatherill AR, Tapping R, Feng L, Lee WH, Fitzgerald KA, Hwang DH. Saturated fatty acid activates but polyunsat-urated fatty acid inhibits Toll-like receptor 2 dimerized with Toll-like receptor 6 or 1. J Biol Chem. 2004;279:16971-16979.
33. Kim F, Pham M, Luttrell I, Bannerman DD, Tupper J, Thaler J, Hawn TR, Raines EW, Schwartz MW. Toll-like receptor-4 mediates vascular inflammation and insulin resistance in diet-induced obesity. Circ Res. 2007;100:1589-1596.
34. Schwartz EA, Zhang WY, Karnik SK, Borwege S, Anand VR, Laine PS, Su Y, Reaven PD. Nutrient modification of the innate immune response: a novel mechanism by which saturated fatty acids greatly amplify monocyte inflammation. Arterioscler Thromb Vasc Biol. 2010;30: 802-808.
35. Maloney E, Sweet IR, Hockenbery DM, Pham M, Rizzo NO, Tateya S, Handa P, Schwartz MW, Kim F. Activation of NF-kappaB by palmitate in endothelial cells: a key role for NADPH oxidase-derived superoxide in response to TLR4 activation. Arterioscler Thromb Vasc Biol. 2009;29: 1370-1375.
36. Wang L, Sapuri-Butti AR, Aung HH, Parikh AN, Rutledge JC. Triglyc-eriderich lipoprotein lipolysis increases aggregation of endothelial cell membrane microdomains and produces reactive oxygen species. Am J Physiol Heart Circ Physiol. 2008;295:H237-H244.
37. Renier G, Lambert A. Lipoprotein lipase synergizes with interferon gamma to induce macrophage nitric oxide synthetase mRNA expression and nitric oxide production. Arterioscler Thromb Vasc Biol. 1995;15:392-399.
38. Kota RS, Ramana CV, Tenorio FA, Enelow RI, Rutledge JC. Differential effects of lipoprotein lipase on tumor necrosis factor-alpha and interferon-gamma-mediated gene expression in human endothelial cells. J Biol Chem. 2005;280:31076-31084.
39. Fisher RM, Benhizia F, Schreiber R, Makoveichuk E, Putt W, Al-Haideri M, Deckelbaum RJ, Olivecrona G, Humphries SE, Talmud PJ. Enhanced bridging function and augmented monocyte adhesion by lipoprotein lipase N9: insights into increased risk of coronary artery disease in N9 carriers. Atherosclerosis. 2003;166:243-251.
40. Li L, Renier G. Adipocyte-derived lipoprotein lipase induces macrophage activation and monocyte adhesion: role of fatty acids. Obesity (Silver Spring). 2007;15:2595-2604.
41. Beauchamp MC, Michaud SE, Li L, Sartippour MR, Renier G. Advanced glycation end products potentiate the stimulatory effect of glucose on mac-rophage lipoprotein lipase expression. J Lipid Res. 2004;45:1749-1757.
42. Rutledge JC, Woo MM, Rezai AA, Curtiss LK, Goldberg IJ. Lipoprotein lipase increases lipoprotein binding to the artery wall and increases endothelial layer permeability by formation of lipolysis products. Circ Res. 1997;80:819-828.
43. Renard CB, Kramer F, Johansson F, Lamharzi N, Tannock LR, von Herrath MG, Chait A, Bornfeldt KE. Diabetes and diabetes-associated lipid abnormalities have distinct effects on initiation and progression of atherosclerotic lesions. J Clin Invest. 2004;114:659-668.
44. Gerrity RG, Natarajan R, Nadler JL, Kimsey T. Diabetes-induced accelerated atherosclerosis in swine. Diabetes. 2001;50:1654-1665.
45. Mazzone T, Chait A, Plutzky J. Cardiovascular disease risk in type 2 diabetes mellitus: insights from mechanistic studies. Lancet. 2008;371: 1800-1809.