Dietary herring improves plasma lipid profiles and reduces atherosclerosis in obese low-density lipoprotein receptor-deficient mice

International Journal of Molecular Medicine

Volumn 29, Issue 3, 2012, Pages 331-337

  Gabrielsson, Britt G ^a   Wikström, Johannes ^b   Jakubowicz, Robert ^c   Marmon, Sofia K ^a   Carlsson, Nils Gunnar ^a   Jansson, Nina ^c   Gan, Li Ming ^b   Undeland, Ingrid ^a   Lönn, Malin ^d   Holmäng, Agneta ^c   Sandberg, Ann Sofie ^a  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b ASTRAZENECA R AND D   (Sweden)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

En face histology; Herring; Lipoprotein particle cholesterol profile; Low density lipoprotein receptor deficient

Indexed keywords

HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; OMEGA 3 FATTY ACID; PHOSPHOLIPID; SUCROSE; TAURINE; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA ARCH; ARTICLE; ATHEROSCLEROSIS; BEEF; BODY COMPOSITION; BODY WEIGHT; CARBOHYDRATE DIET; CELL SIZE; DIETARY INTAKE; EPIDIDYMIS FAT; FOOD INTAKE; HERRING; LIPID BLOOD LEVEL; LIPID COMPOSITION; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; ULTRASOUND;

ADIPOCYTES; ANIMALS; ATHEROSCLEROSIS; BODY WEIGHT; CELL SIZE; DIET, HIGH-FAT; FISHES; LIPID METABOLISM; LIPIDS; LIVER; MALE; MICE; MICE, KNOCKOUT; MICE, OBESE; RECEPTORS, LDL;

EID: 84856166834     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2011.856     Document Type: Article

References (49)

1. Joint WHO/FAO Expert Consultation: WHO Technical Report Series 916: Diet, Nutrition and the Prevention of Chronic Diseases. WHO, Geneva, 2003.
2. Brunner EJ, Mosdol A, Witte DR, et al: Dietary patterns and 15-y risks of major coronary events, diabetes, and mortality. Am J Clin Nutr 87: 1414-1421, 2008. (Pubitemid 351679785)
3. Heidemann C, Schulze MB, Franco OH, van Dam RM, Mantzoros CS and Hu FB: Dietary patterns and risk of mortality from cardiovascular disease, cancer, and all causes in a prospective cohort of women. Circulation 118: 230-237, 2008.
4. Menotti A, Kromhout D, Blackburn H, Fidanza F, Buzina R and Nissinen A: Food intake patterns and 25-year mortality from coronary heart disease: cross-cultural correlations in the Seven Countries Study. The Seven Countries Study Research Group. Eur J Epidemiol 15: 507-515, 1999. (Pubitemid 29400023)
5. Tourlouki E, Matalas AL and Panagiotakos DB: Dietary habits and cardiovascular disease risk in middle-aged and elderly populations: a review of evidence. Clin Interv Aging 4: 319-330, 2009.
6. He K, Song Y, Daviglus ML, et al: Accumulated evidence on fish consumption and coronary heart disease mortality: a meta-analysis of cohort studies. Circulation 109: 2705-2711, 2004. (Pubitemid 38737914)
7. Kromhout D, Bosschieter EB and de Lezenne Coulander C: The inverse relation between fish consumption and 20-year mortality from coronary heart disease. N Engl J Med 312: 1205-1209, 1985. (Pubitemid 15009153)
8. Engelfriet P, Hoekstra J, Hoogenveen R, Buchner F, van Rossum C and Verschuren M: Food and vessels: the importance of a healthy diet to prevent cardiovascular disease. Eur J Cardiovasc Prev Rehabil 17: 50-55, 2010.
9. Balk EM, Lichtenstein AH, Chung M, Kupelnick B, Chew P and Lau J: Effects of omega-3 fatty acids on serum markers of cardiovascular disease risk: a systematic review. Atherosclerosis 189: 19-30, 2006. (Pubitemid 44468073)
10. Kris-Etherton PM, Harris WS and Appel LJ; the American Heart Association, Nutrition Committee: Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106: 2747-2757, 2002.
11. Elvevoll EO, Eilertsen KE, Brox J, et al: Seafood diets: hypolipidemic and antiatherogenic effects of taurine and n-3 fatty acids. Atherosclerosis 200: 396-402, 2008.
12. Gunnarsdottir I, Tomasson H, Kiely M, et al: Inclusion of fish or fish oil in weight-loss diets for young adults: effects on blood lipids. Int J Obes (Lond) 32: 1105-1112, 2008. (Pubitemid 351986209)
13. Thorsdottir I, Tomasson H, Gunnarsdottir I, et al: Randomized trial of weight-loss-diets for young adults varying in fish and fish oil content. Int J Obes (Lond) 31: 1560-1566, 2007. (Pubitemid 47482660)
14. Undeland I, Lindqvist H, Chen-Yun Y, et al: Seafood and health: what is the full story? In: Marine functional food. Luten JB (ed). Wageningen Academic Publishers, Wageningen, The Netherlands, pp17-87, 2009.
15. Berr C, Akbaraly T, Arnaud J, Hininger I, Roussel AM and Barberger-Gateau P: Increased selenium intake in elderly high fish consumers may account for health benefits previously ascribed to omega-3 fatty acids. J Nutr Health Aging 13: 14-18, 2009.
16. Lindqvist HM, Langkilde AM, Undeland I and Sandberg AS: Herring (Clupea harengus) intake influences lipoproteins but not inflammatory and oxidation markers in overweight men. Br J Nutr 101: 383-390, 2009.
17. Lindqvist HM, Sandberg AS, Fagerberg B and Hulthe J: Plasma phospholipid EPA and DHA in relation to atherosclerosis in 61-year-old men. Atherosclerosis 205: 574-578, 2009.
18. Ishibashi S, Goldstein JL, Brown MS, Herz J and Burns DK: Massive xanthomatosis and atherosclerosis in cholesterol-fed low density lipoprotein receptor-negative mice. J Clin Invest 93: 1885-1893, 1994.
19. Teupser D, Persky AD and Breslow JL: Induction of atherosclerosis by low-fat, semisynthetic diets in LDL receptor-deficient C57BL/6J and FVB/NJ mice: comparison of lesions of the aortic root, brachiocephalic artery, and whole aorta (en face measurement). Arterioscler Thromb Vasc Biol 23: 1907-1913, 2003. (Pubitemid 37254883)
20. Schreyer SA, Lystig TC, Vick CM and LeBoeuf RC: Mice deficient in apolipoprotein E but not LDL receptors are resistant to accelerated atherosclerosis associated with obesity. Atherosclerosis 171: 49-55, 2003. (Pubitemid 37464628)
21. Varret M, Abifadel M, Rabès JP and Boileau C: Genetic heterogeneity of autosomal dominant hypercholesterolemia. Clin Genet 73: 1-13, 2008. (Pubitemid 350263516)
22. Summers RM, Andrasko-Bourgeois J, Feuerstein IM, et al: Evaluation of the aortic root by MRI: insights from patients with homozygous familial hypercholesterolemia. Circulation 98: 509-518, 1998. (Pubitemid 28371248)
23. Tahvanainen E, Molin M, Laakso J, et al: Interrelationships between low density lipoprotein receptor defect, serum fatty acid composition, and serum cholesterol concentration. J Nutr Biochem 10: 360-366, 1999. (Pubitemid 29255986)
24. Nookaew I, Gabrielsson BG, Holmäng A, Sandberg AS and Nielsen J: Identifying molecular effects of diet through systems biology: influence of herring diet on sterol metabolism and protein turnover in mice. PLoS One 5: e12361, 2010.
25. Lee CM, Trevino B and Chaiyawat M: A simple and rapid solvent extraction method for determining total lipids in fish tissue. J AOAC Int 79: 487-492, 1996. (Pubitemid 126428840)
26. Sjogren K, Hellberg N, Bohlooly-Y M, et al: Body fat content can be predicted in vivo in mice using a modified dual-energy X-ray absorptiometry technique. J Nutr 131: 2963-2966, 2001. (Pubitemid 33063131)
27. Björnheden T, Jakubowicz B, Levin M, et al: Computerized determination of adipocyte size. Obes Res 12: 95-105, 2004. (Pubitemid 41137492)
28. Gan LM, Grönros J, Hägg U, et al: Non-invasive real-time imaging of atherosclerosis in mice using ultrasound biomicroscopy. Atherosclerosis 190: 313-320, 2007. (Pubitemid 46091789)
29. Bourghardt J, Bergstrom G, Krettek A, Sjoberg S, Boren J and Tivesten A: The endogenous estradiol metabolite 2-methoxyestradiol reduces atherosclerotic lesion formation in female apolipoprotein E-deficient mice. Endocrinology 148: 4128-4132, 2007. (Pubitemid 47295675)
30. Folch J, Lees M and Sloane Stanley GH: A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497-509, 1957.
31. Kaluzny MA, Duncan LA, Merritt MV and Epps DE: Rapid separation of lipid classes in high yield and purity using bonded phase columns. J Lipid Res 26: 135-140, 1985. (Pubitemid 15133302)
32. Holm S: A simple sequentially rejective multiple test procedure. Scand J Statist 6: 65-70, 1979.
33. VanderLaan PA, Reardon CA, Thisted RA and Getz GS: VLDL best predicts aortic root atherosclerosis in LDL receptor deficient mice. J Lipid Res 50: 376-385, 2009.
34. Saraswathi V, Gao L, Morrow JD, Chait A, Niswender KD and Hasty AH: Fish oil increases cholesterol storage in white adipose tissue with concomitant decreases in inflammation, hepatic steatosis, and atherosclerosis in mice. J Nutr 137: 1776-1782, 2007. (Pubitemid 47037706)
35. Wang S, Wu D, Matthan NR, Lamon-Fava S, Lecker JL and Lichtenstein AH: Reduction in dietary omega-6 polyunsaturated fatty acids: eicosapentaenoic acid plus docosahexaenoic acid ratio minimizes atherosclerotic lesion formation and inflammatory response in the LDL receptor null mouse. Atherosclerosis 204: 147-155, 2009.
36. Zampolli A, Bysted A, Leth T, Mortensen A, De Caterina R and Falk E: Contrasting effect of fish oil supplementation on the development of atherosclerosis in murine models. Atherosclerosis 184: 78-85, 2006. (Pubitemid 41721072)
37. Anderson BM and Ma DW: Are all n-3 polyunsaturated fatty acids created equal? Lipids Health Dis 8: 33, 2009.
38. Chen W, Suruga K, Nishimura N, Gouda T, Lam VN and Yokogoshi H: Comparative regulation of major enzymes in the bile acid biosynthesis pathway by cholesterol, cholate and taurine in mice and rats. Life Sci 77: 746-757, 2005. (Pubitemid 40780000)
39. Murakami S, Kondo-Ohta Y and Tomisawa K: Improvement in cholesterol metabolism in mice given chronic treatment of taurine and fed a high-fat diet. Life Sci 64: 83-91, 1999. (Pubitemid 29012752)
40. Ratliff EP, Gutierrez A and Davis RA: Transgenic expression of CYP7A1 in LDL receptor-deficient mice blocks diet-induced hypercholesterolemia. J Lipid Res 47: 1513-1520, 2006. (Pubitemid 44079905)
41. Cheng KK, Benson GM, Grimsditch DC, Reid DG, Connor SC and Griffin JL: A metabolomic study of the LDL receptor null mouse fed a high-fat diet reveals profound perturbations in choline metabolism that are shared with ApoE null mice. Physiol Genomics: Mar 2, 2010 (Epub ahead of print).
42. Li Z and Vance DE: Thematic review series: glycerolipids. Phosphatidylcholine and choline homeostasis. J Lipid Res 49: 1187-1194, 2008.
43. LeBlanc MJ, Brunet S, Bouchard G, et al: Effects of dietary soybean lecithin on plasma lipid transport and hepatic cholesterol metabolism in rats. J Nutr Biochem 14: 40-48, 2003. (Pubitemid 36143750)
44. LeBlanc MJ, Gavino V, Pérea A, Yousef IM, Lévy E and Tuchweber B: The role of dietary choline in the beneficial effects of lecithin on the secretion of biliary lipids in rats. Biochim Biophys Acta 1393: 223-234, 1998. (Pubitemid 28467049)
45. Zeisel SH, Mar MH, Howe JC and Holden JM: Concentrations of choline-containing compounds and betaine in common foods. J Nutr 133: 1302-1307, 2003. (Pubitemid 36548698)
46. Weihrauch J and Son YS: Phospholipid content of foods. J Am Oil Chem Soc 60: 1971-1978, 1983.
47. Raclot T, Groscolas R, Langin D and Ferre P: Site-specific regulation of gene expression by n-3 polyunsaturated fatty acids in rat white adipose tissues. J Lipid Res 38: 1963-1972, 1997. (Pubitemid 27468005)
48. Jernas M, Palming J, Sjoholm K, et al: Separation of human adipocytes by size: hypertrophic fat cells display distinct gene expression. FASEB J 20: 1540-1542, 2006.
49. Hua S, Song C, Geczy CL, Freedman SB and Witting PK: A role for acute-phase serum amyloid A and high-density lipoprotein in oxidative stress, endothelial dysfunction and atherosclerosis. Redox Rep 14: 187-196, 2009.