Apolipoprotein E promotes the regression of atherosclerosis independently of lowering plasma cholesterol levels

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 25, Issue 2, 2005, Pages 436-441

  Raffai, Robert L ^a,b,c,d   Loeb, Samuel M ^c   Weisgraber, Karl H ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

ApoE; Atherosclerosis; Foam cell; Lipoprotein; Regression

Indexed keywords

APOLIPOPROTEIN A2; APOLIPOPROTEIN E; HIGH DENSITY LIPOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; CHOLESTEROL BLOOD LEVEL; COMPARATIVE STUDY; CONTROLLED STUDY; DIET; FEMALE; FOAM CELL; HYPERCHOLESTEROLEMIA; LIPID BLOOD LEVEL; LIPID OXIDATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; REMISSION;

ALLELES; ANIMALS; AORTIC DISEASES; APOLIPOPROTEINS E; ARTERIOSCLEROSIS; CHOLESTEROL; COLLAGEN; DIET, ATHEROGENIC; DIETARY FATS; FIBROSIS; FOAM CELLS; GENE EXPRESSION REGULATION; HYPERCHOLESTEROLEMIA; INTEGRASES; LIPOPROTEINS; MALE; MICE; MICE, MUTANT STRAINS; MODELS, ANIMAL; RECOMBINANT FUSION PROTEINS;

EID: 13244290159     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000152613.83243.12     Document Type: Article

References (51)

1. Stary HC. Atlas of Atherosclerosis: Progression and Regression. New York, NY: The Parthenon Publishing Group; 2003.
2. Armstrong ML, Megan MB. Lipid depletion in atheromatous coronary arteries in rhesus monkeys after regression diets. Circ Res. 1972;30:675-680.
3. Wissler RW, Vesselinovitch D. Brief overview of the mounting evidence that atherosclerosis is both preventable and reversible. J Clin Apheresis. 1988;4:52-58.
4. Aikawa M, Rabkin E, Okada Y, Voglic SJ, Clinton SK, Brinckerhoff CE, Sukhova GK, Libby P. Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma. A potential mechanism of lesion stabilization. Circulation. 1998;97:2433-2444.
5. Aikawa M, Rabkin E, Voglic SJ, Shing H, Nagai R, Schoen FJ, Libby P. Lipid lowering promotes accumulation of mature smooth muscle cells expressing smooth muscle myosin heavy chain isoforms in rabbit atheroma. Circ Res. 1998;83:1015-1026.
6. Tsukamoto K, Tangirala R, Chun SH, Puré E, Rader DJ. Rapid regression of atherosclerosis induced by liver-directed gene transfer of apoE in apoE-deficient mice. Arterioscler Thromb Vasc Biol. 1999;19:2162-2170.
7. Reis ED, Li J, Fayad ZA, Rong JX, Hansoty D, Aguinaldo J-G, Fallon JT, Fisher EA. Dramatic remodeling of advanced atherosclerotic plaques of the apolipoprotein E-deficient mouse in a novel transplantation model. J Vasc Surg. 2001;34:541-547.
8. Falk E, Shah PK, Fuster V. Coronary plaque disruption. Circulation. 1995;92:657-671.
9. Libby P. Molecular bases of the acute coronary syndromes. Circulation. 1995;91:2844-2850.
10. Kane JP, Malloy MJ, Ports TA, Phillips NR, Diehl JC, Havel RJ. Regression of coronary atherosclerosis during treatment of familial hypercholesterolemia with combined drug regimens. J Am Med Assoc. 1990;264:3007-3012.
11. Brown G, Albers JJ, Fisher LD, Schaefer SM, Lin JT, Kaplan C, Zhao X-Q, Bisson BD, Fitzpatrick VF, Dodge HT. Regression of coronary artery disease as a result of intensive lipid-lowering therapy in men with high levels of apolipoprotein B. N Engl J Med. 1990;323:1289-1298.
12. Helft G, Worthley SG, Fuster V, Fayad ZA, Zaman AG, Corti R, Fallon JT, Badimon JJ. Progression and regression of atherosclerotic lesions. Monitoring with serial noninvasive magnetic resonance imaging. Circulation. 2002;105:993-998.
13. Corti R, Fuster V, Fayad ZA, Worthley SG, Helft G, Smith D, Weinberger J, Wentzel J, Mizsei G, Mercuri M, Badimon JJ. Lipid lowering by simvastatin induces regression of human atherosclerotic lesions: Two years' follow-up by high-resolution noninvasive magnetic resonance imaging. Circulation. 2002;106:2884-2887.
14. Nissen SE, Tsunoda T, Tuzcu EM, Schoenhagen P, Cooper CJ, Yasin M, Eaton GM, Lauer MA, Sheldon WS, Grines CL, Halpern S, Crowe T, Blankenship JC, Kerensky R. Effect of recombinant apoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes. A randomized control trial. J Am Med Assoc. 2003;290:2292-2300.
15. Mahley RW, Huang Y. Apolipoprotein E: from atherosclerosis to Alzheimer's disease and beyond. Curr Opin Lipidol. 1999;10:207-217.
16. Curtiss LK, Boisvert WA. Apolipoprotein E and atherosclerosis. Curr Opin Lipidol. 2000;11:243-251.
17. Raffaï RL, Weisgraber KH. Hypomorphic apolipoprotein E mice. A new model of conditional gene repair to examine apolipoprotein E-mediated metabolism. J Biol Chem. 2002;277:11064-11068.
18. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 1996;380:435-439.
19. Nagy A, Moens C, Ivanyi E, Pawling J, Gertsenstein M, Hadjantonakis AK, Pirity M, Rossant J. Dissecting the role of N-myc in development using a single targeting vector to generate a series of alleles. Curr Biol. 1998;8:661-664.
20. Nagy A. Cre recombinase: The universal reagent for genome tailoring. Genesis. 2000;26:99-109.
21. Raffaï RL, Hasty AH, Wang Y, Mettler SE, Sanan DA, Linton MF, Fazio S, Weisgraber KH. Hepatocyte-derived apoE is more effective than non-hepatocyte-derived apoE in remnant lipoprotein clearance. J Biol Chem. 2003;278:11670-11675.
22. Basu SK, Brown MS, Ho YK, Havel RJ, Goldstein JL. Mouse macrophages synthesize and secrete a protein resembling apolipoprotein E. Proc Natl Acad Sci U S A. 1981;78:7545-7549.
23. Salomon RN, Underwood R, Doyle MV, Wang A, Libby P. Increased apolipoprotein E and c-fms gene expression without elevated interleukin 1 or 6 mRNA levels indicates selective activation of macrophage functions in advanced human atheroma. Proc Natl Acad Sci U S A. 1992;89:2814-2818.
24. Aikawa M, Libby P. Lipid lowering reduces proteolytic and prothrombotic potential in rabbit atheroma. Ann NY Acad Sci. 2000;902:140-152.
25. Desurmont C, Caillaud JM, Emmanuel F, Benoit P, Fruchart JC, Castro G, Branellec D, Heard JM, Duverger N. Complete atherosclerosis regression after human apoE gene transfer in apoE-deficient/nude mice. Arterioscler Thromb Vasc Biol. 2000;20:435-442.
26. -] adenovirus vector expressing human apoE. Hum Mol Genet. 2002;11:43-58.
27. Shi W, Wang X, Wang NJ, McBride WH, Lusis AJ. Effect of macrophage-derived apolipoprotein E on established atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2000;20:2261-2266.
28. Schiller NK, Kubo N, Boisvert WA, Curtiss LK. Effect of gamma-irradiation and bone marrow transplantation on atherosclerosis in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2001;21:1674-1680.
29. Oram JF, Lawn RM. ABCA1: The gatekeeper for eliminating excess tissue cholesterol. J Lipid Res. 2001;42:1173-1179.
30. Brewer HB Jr, Santamarina-Fojo S. Clinical significance of high-density lipoproteins and the development of atherosclerosis: focus on the role of the adenosine triphosphate- binding cassette protein A1 transporter. Am J Cardiol. 2003;92:10K-16K.
31. Llodra J, Angeli V, Liu J, Trogan E, Fisher EA, Randolph GJ. From the Cover: Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc Natl Acad Sci U S A. 2004;101:11779-11784.
32. Bruce C, Chouinard RA Jr, Tall AR. Plasma lipid transfer proteins, high-density lipoproteins, and reverse cholesterol transport. Annu Rev Nutr. 1998;18:297-330.
33. Assmann G, Huang Y, Wu S, von Eckardstein A. A lipoprotein containing only apoE present in normal and HDL-deficient plasmas releases cholesterol from cells. Atherosclerosis. 1994;103:334.
34. Huang Y, von Eckardstein A, Wu S, Maeda N, Assmann G. A plasma lipoprotein containing only apolipoprotein E and with γ mobility on electrophoresis releases cholesterol from cells. Proc Natl Acad Sci U S A. 1994;91:1834-1838.
35. Krimbou L, Marcil M, Chiba H, Genest J Jr. Structural and functional properties of human plasma high density-sized lipoprotein containing only apoE particles. J Lipid Res. 2003;44:884-892.
36. Sacre SM, Stannard AK, Owen JS. Apolipoprotein E (apoE) isoforms differentially induce nitric oxide production in endothelial cells. FEBS Lett. 2003;540:181-187.
37. Kühn R, Schwenk F, Aguet M, Rajewsky K. Inducible gene targeting in mice. Science. 1995;269:1427-1429.
38. Rohlmann A, Gotthardt M, Hammer RE, Herz J. Inducible inactivation of hepatic LRP gene by Cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J Clin Invest. 1998;101:689-695.
39. Davignon J, Cohn JS, Mabile L, Bernier L. Apolipoprotein E and atherosclerosis: Insight from animal and human studies. Clin Chim Acta. 1999;286:115-143.
40. Davignon J. Apolipoprotéine E, une molécule polymorphe et pléiotrope. Première partie. Rôle dans l'athé rosclérose et au-delà. Sang Thrombose et Vaisseaux. 2002;14:39-58.
41. Davignon J. Apolipoprotéine E, une molécule polymorphe et pléiotrope. Deuxième partie. Rôle dans l'athé rosclérose et au-delà. Sang Thrombose et Vaisseaux. 2002;14:107-120.
42. Tangirala RK, Praticó D, FitzGerald GA, Chun S, Tsukamoto K, Maugeais C, Usher DC, Puré E, Rader DJ. Reduction of isoprostanes and regression of advanced atherosclerosis by apolipoprotein E. J Biol Chem. 2001;276:261-266.
43. Linton MF, Atkinson JB, Fazio S. Prevention of atherosclerosis in apolipoprotein E-deficient mice by bone marrow transplantation. Science. 1995;267:1034-1037.
44. Bellosta S, Mahley RW, Sanan DA, Murata J, Newland DL, Taylor JM, Pitas RE. Macrophage-specific expression of human apolipoprotein E reduces atherosclerosis in hypercholesterolemic apolipoprotein E-null mice. J Clin Invest. 1995;96:2170-2179.
45. 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.
46. Fazio S, Babaev VR, Burleigh ME, Major AS, Hasty AH, Linton MF. Physiological expression of macrophage apoE in the artery wall reduces atherosclerosis in severely hyperlipidemic mice. J Lipid Res. 2002;43:1602-1609.
47. Oram JF. HDL apolipoproteins and ABCA1: partners in the removal of excess cellular cholesterol. Arterioscler Thromb Vasc Biol. 2003;23:720-727.
48. Kockx MM. Apoptosis in the atherosclerotic plaque. Quantitative and qualitative aspects. Arterioscler Thromb Vasc Biol. 1998;18:1519-1522.
49. Mabile L, Lefebvre C, Lavigne J, Boulet L, Davignon J, Lussier-Cacan S, Bernier L. Secreted apolipoprotein E reduces macrophage-mediated LDL oxidation in an isoform-dependent way. J Cell Biochem. 2003;90:766-776.
50. Glass CK, Witztum JL. Atherosclerosis: the road ahead. Cell. 2001;104: 503-516.
51. Raffaï RL, Dong LM, Farese RV Jr, Weisgraber KH. Introduction of human apolipoprotein E4 "domain interaction" into mouse apolipoprotein E. Proc Natl Acad Sci U S A. 2001;98:11587-11591.