The value of apolipoprotein E knockout mice for studying the effects of dietary fat and cholesterol on atherogenesis

Current Opinion in Lipidology

Volumn 11, Issue 1, 2000, Pages 25-29

  Osada, Jesús ^a   Joven, Jorge ^b   Maeda, Nobuyo ^c  

^a UNIVERSIDAD DE ZARAGOZA   (Spain)

^b HOSPITAL UNIVERSITARI SANT JOAN DE REUS   (Spain)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; CHOLESTEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ATHEROSCLEROSIS; CONTROLLED STUDY; DIET; DISEASE MODEL; FAT INTAKE; MOUSE; MOUSE STRAIN; NONHUMAN; NUTRIENT; PATHOLOGY; PRIORITY JOURNAL; REVIEW;

ANIMALS; APOLIPOPROTEINS E; ARTERIOSCLEROSIS; CHOLESTEROL, DIETARY; DIETARY FATS; HUMANS; LIPOPROTEINS; MICE; MICE, KNOCKOUT;

ANIMALIA;

EID: 0034099149     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041433-200002000-00004     Document Type: Review

References (58)

1. 1 Hofker MH, van Vlijmen BJ, Havekes LM. Transgenic mouse models to study the role of ApoE in hyperlipidemia and atherosclerosis. Atherosclerosis 1998; 137:1-11.
2. 2 Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 1992; 258:468-471.
3. 3 Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, et al. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 1992; 71:343-353.
4. 4 van Ree JH, van den Broek WJ, Dahlmans VE, Groot PH, Vidgeon-Hart M, Frants RR, et al. Diet-induced hypercholesterolemia and atherosclerosis in heterozygous apolipoprotein E-deficient mice. Atherosclerosis 1994; 111:25-37.
5. 5 Reddick RL, Zhang SH, Maeda N. Atherosclerosis in mice lacking apoE. Evaluation of lesional development and progression. Arterioscler Thromb 1994; 14:141-147.
6. 6 Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb 1994; 14:133-140.
7. 7 Tamminen M, Mottino G, Qiao JH, Breslow JL, Frank JS. Ultrastructure of early lipid accumulation in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 1999; 19:847-853. This study provides new data regarding the early stages of atherosclerosis using freeze-etch electron microscopy.
8. 8 Tse J, Martin-McNaulty B, Halks-Miller M, Kauser K, DelVecchio V, Vergona R, et al. Accelerated atherosclerosis and premature calcified cartilaginous metaplasia in the aorta of diabetic male Apo E knockout mice can be prevented by chronic treatment with 17 beta-estradiol. Atherosclerosis 1999; 144:303-313.
9. 9 Plump AS, Breslow JL. Apolipoprotein E and the apolipoprotein E-deficient mouse. Annu Rev Nutr 1995; 15:495-518.
10. 10 Smith JD, Breslow JL. The emergence of mouse models of atherosclerosis and their relevance to clinical research. J Intern Med 1997; 242:99-109.
11. 11 Smith JD. Mouse models of atherosclerosis. Lab Anim Sci 1998; 48:573-579.
12. 12 Tangirala RK, Casanada F, Miller E, Witztum JL, Steinberg D, Palinski W. Effect of the antioxidant N,N'-diphenyl 1,4-phenylendiamine (DPPD) on atherosclerosis in apoE-deficient mice. Arterioscler Thromb Vasc Biol 1995; 15:1625-1630.
13. 13 Moghadasian MH, McManus BM, Pritchard PH, Frohlich JJ. 'Tall oil'-derived phytosterols reduce atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 1997; 17:119-126.
14. 14 Paul A, Calleja L, Vilella E, Martinez R, Osada J, Joven J. Reduced progression of atherosclerosis in apolipoprotein E-deficient mice with phenylhydrazyne-induced anemia. Atherosclerosis 1999; 147:61-68.
15. 15 Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Diet-induced atherosclerosis in mice heterozygous and homozygous for apolipoprotein E gene disruption. J Clin Invest 1994; 94:937-945.
16. 16 Ni WH, Tsuda Y, Sakono M, Imaizumi K. Dietary soy protein isolate, compared with casein, reduces atherosclerotic lesion area in apolipoprotein E-deficient mice. J Nutr 1998; 128:1884-1889.
17. 17 Dansky HM, Charlton SA, Sikes JL, Heath SC, Simantov R, Levin LF, et al. Genetic background determines the extent of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 1999; 19:1960-1968. This paper shows that the genetic background of apolipoprotein E knockout progenies determines the atherosclerotic lesion area in a manner that is independent of lipoprotein and oxidative markers, suggesting the existence of new candidate genes.
18. 18 Calleja L, Paris MA, Paul A, Vilella E, Joven J, Jimenez A, et al. Low-cholesterol and high-fat diets reduce atherosclerotic lesion development in ApoE-knockout mice. Arterioscler Thromb Vasc Biol 1999; 19:2368-2375. This study describes the influence on atherosclerosis of several low-cholesterol, high-fat diets, and discusses potential mechanisms.
19. 19 Adan Y, Shibata K, Ni W, Tsuda Y, Sato M, Ikeda I, et al. Concentration of serum lipids and aortic lesion size in female and male apoE-deficient mice fed docosahexaenoic acid. Biosci Biotechnol Biochem 1999; 63:309-313.
20. 20 Truswell AS. Practical and realistic approaches to healthier diet modifications. Am J Clin Nutr 1996; 67(Suppl):583S-590S.
21. 21 Lee TS, Shiao MS, Pan CC, Chau LY. Iron-deficient diet reduces atherosclerotic lesions in apoE-deficient mice. Circulation 1999; 99:1222-1229. This study illustrates the mechanisms by which iron promotes the development of the atherosclerotic disease.
22. 22 Ormrod DJ, Holmes CC, Miller TE. Dietary chitosan inhibits hypercholesterolaemia and atherogenesis in the apolipoprotein E-deficient mouse model of atherosclerosis. Atherosclerosis 1998; 138:329-334.
23. 23 Moghadasian MH, McManus BM, Godin DV, Rodrigues B, Frohlich JJ. Proatherogenic and antiatherogenic effects of probucol and phytosterols in apolipoprotein E-deficient mice: possible mechanisms of action. Circulation 1999; 99:1733-1739.
24. 24 Masucci-Magoulas L, Plump A, Jiang XC, Walsh A, Breslow JL, Tall AR. Profound induction of hepatic cholesteryl ester transfer protein transgene expression in apolipoprotein E and low density lipoprotein receptor gene knockout mice. A novel mechanism signals changes in plasma cholesterol levels. J Clin Invest 1996; 97:154-161.
25. 25 Kuipers F, van Ree JM, Hofker MH, Wolters H, In't Veld G, Havinga R, et al. Altered lipid metabolism in apolipoprotein E-deficient mice does not affect cholesterol balance across the liver. Hepatology 1996; 24:241-247.
26. 26 Chang SY, Maeda N, Borensztajn J. The role of lipoprotein lipase and apoprotein E in the recognition of chylomicrons and chylomicron remnants by cultured isolated mouse hepatocytes. Biochem J 1996; 318:29-34.
27. 27 Crawford SE, Borensztajn J. Plasma clearance and liver uptake of chylomicron remnants generated by hepatic lipase lipolysis. Evidence for a lactoferrin-sensitive and apolipoprotein e-independent pathway. J Lipid Res 1999; 40:797-805.
28. 28 Amar MJA, Dugi KA, Haudenschild CC, Shamburek RD, Foger B, Chase M, et al. Hepatic lipase facilitates the selective uptake of cholesteryl esters from remnant lipoproteins in apoE-deficient mice. J Lipid Res 1998; 39:2436-2442.
29. 29 Bergeron N, Kotite L, Verges M, Blanche P, Hamilton RL, Krauss RM, et al. Lamellar lipoproteins uniquely contribute to hyperlipidemia in mice doubly deficient in apolipoprotein E and hepatic lipase. Proc Natl Acad Sci USA 1998; 95:15647-15652.
30. 30 Dansky HM, Charlton SA, Barlow CB, Tamminen M, Smith JD, Frank JS, et al. ApoA-I inhibits foam cell formation in apoE-deficient mice after monocyte adherence to endothelium. J Clin Invest 1999; 104:31-39. This interesting study suggested an in-vivo role of HDL in preventing the development of atherosclerosis.
31. 31 Sukovich DA, Kauser K, Shirley FD, DelVecchio V, HalksMiller M, Rubanyi GM. Expression of interleukin-6 in atherosclerotic lesions of male ApoE-knockout mice: inhibition by 17 beta-estradiol. Arterioscler Thromb Vasc Biol 1998; 18:1498-1505.
32. 32 Caligiuri G, Nicoletti A, Zhou X, Tornberg I, Hansson GK. Effects of sex and age on atherosclerosis and autoimmunity in apoE-deficient mice. Atherosclerosis 1999; 145:301-308.
33. 33 Huang Y, Zhu Y, Langer C, Raabe M, Wu S, Wiesenhutter B, et al. Effects of genotype and diet on cholesterol efflux into plasma and lipoproteins of normal, apolipoprotein A-I-, and apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 1997; 17:2010-2019.
34. 34 Linton MRF, Fazio S. Macrophages, lipoprotein metabolism, and atherosclerosis: insights from murine bone marrow transplantation studies. Curr Opin Lipidol 1999; 10:97-105. This review addresses the contribution of this technology to establish the role of macrophage proteins in the development of atherosclerosis.
35. 35 Zhu YH, Bellosta S, Langer C, Bernini F, Pitas RE, Mahley RW, et al. Low-dose expression of a human apolipoprotein E transgene in macrophages restores cholesterol efflux capacity of apolipoprotein E-deficient mouse plasma. Proc Natl Acad Sci USA 1998; 95:7585-7590.
36. 36 Hasty AH, Linton MF, Brandt SJ, Babaev VR, Gleaves LA, Fazio S. Retroviral gene therapy in ApoE-deficient mice: ApoE expression in the artery wall reduces early foam cell lesion formation. Circulation 1999; 99:2571-2576.
37. 37 Murayama T, Yokode M, Kataoka H, Imabayashi T, Yoshida H, Sano H, et al. Intraperitoneal administration of anti-c-fms monoclonal antibody prevents initial events of atherogenesis but does not reduce the size of advanced lesions in apolipoprotein E-deficient mice. Circulation 1999; 99:1740-1746.
38. 38 Reckless J, Rubin EM, Verstuyft JB, Metcalfe JC, Grainger DJ. Monocyte chemoattractant protein-1 but not tumor necrosis factor-alpha is correlated with monocyte infiltration in mouse lipid lesions. Circulation 1999; 99:2310-2316.
39. 39 Aiello RJ, Bourassa PA, Lindsey S, Weng W, Natoli E, Rollins BJ, et al. Monocyte chemoattractant protein-1 accelerates atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 1999; 19:1518-1525.
40. 40 Boring L, Gossling J, Cleary M, Charo IF. Decreased lesion formation in CCR2-/-mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 1998; 394:894-897.
41. 41 Dawson TC, Kuziel WA, Osahar TA, Maeda N. Absence of CC chemokine receptor-2 reduces atherosclerosis in apolipoprotein E-deficient mice. Atherosclerosis 1999; 143:205-211.
42. 42 Jeng AY, Chou M, Sawyer WK, Caplan SL, Linden-Reed J, Jeune M, et al. Enhanced expression of matrix metalloproteinase-3, -12, and -13 mRNAs in the aortas of apolipoprotein E-deficient mice with advanced atherosclerosis. Ann N Y Acad Sci 1999; 878:555-558.
43. 43 Ross R. Atherosclerosis. N Engl J Med 1999; 340:115-126. This is a comprehensive overview of risk factors and mechanisms of atherosclerosis.
44. 44 Nakashima Y, Rains EW, Plump AS, Breslow JL, Ross R. Upregulation of VCAM-1 and ICAM-1 at atherosclerosis-prone sites on the endothelium in the ApoE-deficient mouse. Arterioscler Thromb Vasc Biol 1998; 18:842-851. This paper establishes a link between cholesterol-containing diets and regulation of adhesion molecules.
45. 45 Patel SS, Thiagarajan R, Willerson JT, Yeh ET. Inhibition of alpha4 integrin and ICAM-1 markedly attenuate macrophage homing to atherosclerotic plaques in ApoE-deficient mice. Circulation 1998; 97:75-81. This paper reports an interesting experimental approach to identify the characteristics of endothelium on macrophage recruitment in vivo.
46. 46 Ramos CL, Huo Y, Jung U, Ghosh S, Manka DR, Sarembock IJ, et al. Direct demonstration of P-Selectin-and VCAM-1-dependent mononuclear cell rolling in early atherosclerotic lesions of apolipoprotein E-deficient mice. Circ Res 1999; 84:1237-1244.
47. 47 Roselaar SE, Kakkanathu PX, Daugherty A. Lymphocyte populations in atherosclerotic lesions of ApoE -/-and LDL receptor -/-mice: decreasing density with disease progression. Arterioscler Thromb Vasc Biol 1996; 16:1013-1018.
48. 48 Zhou XH, Paulsson G, Stemme S, Hansson GK. Hypercholesterolemia is associated with a T helper (Th) 1/Th2 switch of the autoimmune response in atherosclerotic apoE-knockout mice. J Clin Invest 1998; 101:1717-1725.
49. 49 Palinski W, Ord VA, Plump AS, Breslow JL, Steinberg D, Witztum JL ApoE-deficient mice are a model of lipoprotein oxidation in atherogenesis. Demonstration of oxidation-specific epitopes in lesions and high titers of autoantibodies to malondialdehyde-lysine in serum. Arterioscler Thromb 1994; 14:605-616.
50. 50 Letters JM, Witting PK, Christison JK, Eriksson AW, Pettersson K, Stocker R. Time-dependent changes to lipids and antioxidants in plasma and aortas of apolipoprotein E knockout mice. J Lipid Res 1999; 40:1104-1112.
51. 51 Pratico D, Tangirala RK, Rader DJ, Rokach J, FitzGerald GA. Vitamin E suppresses isoprostane generation in vivo and reduces atherosclerosis in ApoE-deficient mice. Nature Med 1998; 4:1189-1192.
52. 52 Hayek T, Fuhrman B, Vaya J, Rosenblat M, Belinky P, Coleman R, et al. Reduced progression of atherosclerosis in apolipoprotein E-deficient mice following consumption of red wine, or its polyphenois quercetin or catechin, is associated with reduced susceptibility of LDL to oxidation and aggregation. Arterioscler Thromb Vasc Biol 1997; 17:2744-2752.
53. 53 Fuhrman B, Buch S, Vaya J, Belinky PA, Coleman R, Hayek T, et al. Licorice extract and its major polyphenol glabridin protect low-density lipoprotein against lipid peroxidation: in vitro and ex vivo studies in humans and in atherosclerotic apolipoprotein E-deficient mice. Am J Clin Nutr 1997; 66:267-275.
54. 54 Rosenblat M, Belinky P, Vaya J, Levy R, Hayek T, Coleman R, et al. Macrophage enrichment with the isoflavan glabridin inhibits NADPH oxidase-induced cell-mediated oxidation of low density lipoprotein. A possible role for protein kinase C. J Biol Chem 1999; 274:13790-13799. This paper describes the accumulation of an antioxidant in macrophages and the change in oxidative stress of these cells that is reflected in lesion area in vivo. This warrants further research regarding attenuation of atherosclerosis and to investigate the molecular basis of this disease.
55. 55 Maor I, Hayek T, Coleman R, Aviram M. Plasma LDL oxidation leads to its aggregation in the atherosclerotic apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 1997; 17:2995-3005.
56. 56 Shaish A, George J, Gilburd B, Keren P, Levkovitz H, Harats D. Dietary beta-carotene and alpha-tocopherol combination does not inhibit atherogenesis in an ApoE-deficient mouse model. Arterioscler Thromb Vasc Biol 1999; 19:1470-1475.
57. 57 Leaf A. Dietary prevention of coronary heart disease. Circulation 1999; 99:733-735. This inspiring editorial emphasizes that diet may be of great value in controlling cardiovascular diseases.
58. 58 Noakes M, Nestel PJ, Clifton PM. Modifying the fatty acid profile of diary products through feedlot technology lowers plasma cholesterol of human consuming the products. Am J Clin Nutr 1996; 63:42-46.