Development of the lipid-rich core in human atherosclerosis.

In recent years the role of the atherosclerotic core in promoting plaque rupture has become well recognized. A new insight into core development is its origination early in atherogenesis, before formation of the fibrous plaque. The early core is associated with accumulation of vesicular lipid rich in free cholesterol. Later in core development, lipid deposits become more diverse. The weight of evidence points toward a direct extracellular process, probably lipoprotein aggregation and fusion, as the chief pathway of cholesteryl ester accumulation, although foam cell death may also contribute cholesteryl ester. The mechanism or mechanisms of formation of vesicular, cholesterol-rich deposits are unknown. Since the increase in free cholesterol is likely to have deleterious effects on cells bordering the core, the further elucidation of cellular and biochemical pathways leading to and responding to free cholesterol accumulation is of great importance. Complement activation and cellular stress responses are prominent in the vicinity of core lipids, but their pathogenetic roles remain to be established. Since the core appears so early in atherogenesis, these as well as other, yet to be determined cellular responses to core lipids, oxidized and unoxidized, could have a considerable effect on overall lesion development. Much remains to be learned about macrophage and smooth muscle responses, calcification, capillarization, and matrix protein alterations in the evolution of the core and surrounding arterial intima.

[1]  Y. Hannun,et al.  Programmed cell death induced by ceramide. , 1993, Science.

[2]  E. B. Smith,et al.  The release of an immobilized lipoprotein fraction from atherosclerotic lesions by incubation with plasmin. , 1976, Atherosclerosis.

[3]  G. Shipley,et al.  Physical chemistry of the lipids of human atherosclerotic lesions. Demonstration of a lesion intermediate between fatty streaks and advanced plaques. , 1976, The Journal of clinical investigation.

[4]  K. Watson,et al.  Bone morphogenetic protein expression in human atherosclerotic lesions. , 1993, The Journal of clinical investigation.

[5]  A. Chait,et al.  Phagocytosis of aggregated lipoprotein by macrophages: low density lipoprotein receptor-dependent foam-cell formation. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[6]  G. Schmitz,et al.  Ca++ Antagonists and ACAT Inhibitors Promote Cholesterol Efflux from Macrophages by Different Mechanisms: II. Characterization of Intracellular Morphologic Changes , 1988, Arteriosclerosis.

[7]  V. Tertov,et al.  Three types of naturally occurring modified lipoproteins induce intracellular lipid accumulation due to lipoprotein aggregation. , 1992, Circulation research.

[8]  S. Rankin,et al.  Role of oxidized low density lipoprotein in atherogenesis. , 1992, Progress in lipid research.

[9]  J. Guyton,et al.  The lipid-rich core region of human atherosclerotic fibrous plaques. Prevalence of small lipid droplets and vesicles by electron microscopy. , 1989, The American journal of pathology.

[10]  W. Wagner,et al.  Low density lipoprotein interaction with artery derived proteoglycan: the influence of LDL particle size and the relationship to atherosclerosis susceptibility. , 1989, Atherosclerosis.

[11]  D. Steinberg,et al.  Prevention of low density lipoprotein aggregation by high density lipoprotein or apolipoprotein A-I. , 1990, Journal of lipid research.

[12]  N. Simionescu,et al.  Intimal thickenings of human aorta contain modified reassembled lipoproteins. , 1995, Atherosclerosis.

[13]  M. Ferguson,et al.  Apolipoprotein E localization in human coronary atherosclerotic plaques by in situ hybridization and immunohistochemistry and comparison with lipoprotein lipase. , 1994, The American journal of pathology.

[14]  S. Srinivasan,et al.  Lipoprotein-proteoglycan complexes induce continued cholesteryl ester accumulation in foam cells from rabbit atherosclerotic lesions. , 1993, The Journal of clinical investigation.

[15]  S M Schwartz,et al.  Angiogenesis in human coronary atherosclerotic plaques. , 1994, The American journal of pathology.

[16]  J L Witztum,et al.  Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. , 1989, The New England journal of medicine.

[17]  M J Davies,et al.  Plaque fissuring--the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. , 1985, British heart journal.

[18]  J. Guyton,et al.  Cytotoxicity of oxidized LDL to porcine aortic smooth muscle cells is associated with the oxysterols 7-ketocholesterol and 7-hydroxycholesterol. , 1994, Arteriosclerosis and thrombosis : a journal of vascular biology.

[19]  L. J. Lewis,et al.  Lipoprotein Oxidation and Lipoprotein‐lnduced Cytotoxicity , 1983, Arteriosclerosis.

[20]  H. Kruth,et al.  Development of unesterified cholesterol-rich lipid particles in atherosclerotic lesions of WHHL and cholesterol-fed NZW rabbits. , 1994, Journal of lipid research.

[21]  R. Krauss,et al.  Lipolysis products promote the formation of complexes of very-low-density and low-density lipoproteins. , 1987, Biochimica et biophysica acta.

[22]  E. B. Smith,et al.  The lipids in raised fatty and fibrous lesions in human aorta. A comparison of the changes at different stages of development. , 1968, Journal of atherosclerosis research.

[23]  H. C. Stary Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. , 1989, Arteriosclerosis.

[24]  Y. Hannun,et al.  Functions of sphingolipids and sphingolipid breakdown products in cellular regulation. , 1989, Science.

[25]  A. Chenchik,et al.  Localization of apolipoprotein E in normal and atherosclerotic human aorta. , 1990, Atherosclerosis.

[26]  Kathleen M. Smith,et al.  Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[27]  M. Kazatchkine,et al.  The complement system in atherosclerosis. , 1988, Atherosclerosis.

[28]  G. Hansson,et al.  Complement receptors and regulatory proteins in human atherosclerotic lesions. , 1989, Arteriosclerosis.

[29]  C. Alpers,et al.  Osteopontin is elevated during neointima formation in rat arteries and is a novel component of human atherosclerotic plaques. , 1993, The Journal of clinical investigation.

[30]  D. Morel,et al.  7 beta-hydroperoxycholest-5-en-3 beta-ol, a component of human atherosclerotic lesions, is the primary cytotoxin of oxidized human low density lipoprotein. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[31]  P. Libby,et al.  Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. , 1994, The Journal of clinical investigation.

[32]  G. Camejo The interaction of lipids and lipoproteins with the intercellular matrix of arterial tissue: its possible role in atherogenesis. , 1982, Advances in lipid research.

[33]  D. Falcone,et al.  Fibronectin Stimulates Macrophage Uptake of Low Density Lipoprotein‐Heparin‐Collagen Complexes , 1988, Arteriosclerosis.

[34]  C. W. Adams,et al.  The action of human high density lipoprotein on cholesterol crystals. Part 1. Light-microscopic observations. , 1978, Atherosclerosis.

[35]  D. Steinberg,et al.  Enhanced Macrophage Uptake of Low Density Lipoprotein after Self‐Aggregation , 1988, Arteriosclerosis.

[36]  I. Tabas,et al.  Sphingomyelinase enhances low density lipoprotein uptake and ability to induce cholesteryl ester accumulation in macrophages. , 1991, The Journal of biological chemistry.

[37]  U. Steinbrecher,et al.  Scavenger receptor-independent stimulation of cholesterol esterification in macrophages by low density lipoprotein extracted from human aortic intima. , 1992, Arteriosclerosis and thrombosis : a journal of vascular biology.

[38]  D. Small The physical chemistry of lipids : from alkanes to phospholipids , 1986 .

[39]  S. Schwartz,et al.  Osteopontin is synthesized by macrophage, smooth muscle, and endothelial cells in primary and restenotic human coronary atherosclerotic plaques. , 1994, Arteriosclerosis and thrombosis : a journal of vascular biology.

[40]  J. Guyton,et al.  Human Aortic Fibrolipid Lesions: Immunochemical Localization of Apolipoprotein B and Apolipoprotein A , 1988, Arteriosclerosis.

[41]  A. Fogelman,et al.  Ultrastructure of the intima in WHHL and cholesterol-fed rabbit aortas prepared by ultra-rapid freezing and freeze-etching. , 1989, Journal of lipid research.

[42]  J. Guyton,et al.  Ultrastructure of the human aortic fibrolipid lesion. Formation of the atherosclerotic lipid-rich core. , 1986, The American journal of pathology.

[43]  W. J. Johnson,et al.  Cholesterol transport between cells and high-density lipoproteins. , 1991, Biochimica et biophysica acta.

[44]  D. Small Cellular Mechanisms for Lipid Deposition in Atherosclerosis , 1977 .

[45]  R. Mesa-Tejada,et al.  Identification and Distribution of Fibrinogen, Fibrin, and Fibrin(ogen) Products in Atherosclerosis: Use of Monoclonal Antibodies , 1989, Arteriosclerosis.

[46]  C. Chauzy,et al.  Localization and solubilization of hyaluronan and of the hyaluronan-binding protein hyaluronectin in human normal and arteriosclerotic arterial walls. , 1994, Atherosclerosis.

[47]  J. Guyton,et al.  Early extracellular and cellular lipid deposits in aorta of cholesterol-fed rabbits. , 1992, The American journal of pathology.

[48]  M. Mims,et al.  Altered ultrastructural morphology of self-aggregated low density lipoproteins: coalescence of lipid domains forming droplets and vesicles. , 1991, Journal of lipid research.

[49]  E. B. Smith,et al.  The microdissection of large atherosclerotic plaques to give morphologically and topographically defined fractions for analysis. 2. Studies on "nile blue" cells. , 1972, Atherosclerosis.

[50]  W. Harland,et al.  Squalene, 26-hydroxycholesterol and 7-ketocholesterol in human atheromatous plaques. , 1966, Biochimica et biophysica acta.

[51]  A. Fogelman,et al.  An ultrastructural study of lipoprotein accumulation in cardiac valves of the rabbit. , 1994, Arteriosclerosis and thrombosis : a journal of vascular biology.

[52]  U. Steinbrecher,et al.  Role of oxidatively modified LDL in atherosclerosis. , 1990, Free radical biology & medicine.

[53]  G. Schmitz,et al.  Ca++ Antagonists and ACAT Inhibitors Promote Cholesterol Efflux from Macrophages by Different Mechanisms: I. Characterization of Cellular Lipid Metabolism , 1988, Arteriosclerosis.

[54]  V. Tertov,et al.  Hydrolysis of cholesteryl ester in low density lipoprotein converts this lipoprotein to a liposome. , 1992, Journal of Biological Chemistry.

[55]  J. Guyton,et al.  Transitional features in human atherosclerosis. Intimal thickening, cholesterol clefts, and cell loss in human aortic fatty streaks. , 1993, The American journal of pathology.

[56]  W. J. Johnson,et al.  Formation of cholesterol monohydrate crystals in macrophage-derived foam cells. , 1994, Journal of lipid research.

[57]  E. B. Smith,et al.  The relationship between plasma and tissue lipids in human atherosclerosis. , 1974, Advances in lipid research.

[58]  J. Guyton,et al.  Quantitative Ultrastructural Analysis of Perifibrous Lipid and Its Association with Elastin in Nonatherosclerotic Human Aorta , 1985, Arteriosclerosis.

[59]  R. A. Cooper Abnormalities of cell-membrane fluidity in the pathogenesis of disease. , 1977, The New England journal of medicine.

[60]  N. Simionescu,et al.  Prelesional events in atherogenesis. Accumulation of extracellular cholesterol-rich liposomes in the arterial intima and cardiac valves of the hyperlipidemic rabbit. , 1986, The American journal of pathology.

[61]  G. Rothblat,et al.  Triglyceride and cholesteryl ester hydrolysis in a cell culture model of smooth muscle foam cells. , 1989, Journal of lipid research.

[62]  O. Portman,et al.  Hydrolysis of cholesteryl linoleate by a high-speed supernatant preparation of rat and monkey aorta. , 1966, Biochimica et biophysica acta.

[63]  B. Halliwell,et al.  Lipids and oxidised lipids in human atheroma and normal aorta. , 1993, Biochimica et biophysica acta.

[64]  T. Bocan,et al.  Comparison of CI-976, an ACAT inhibitor, and selected lipid-lowering agents for antiatherosclerotic activity in iliac-femoral and thoracic aortic lesions. A biochemical, morphological, and morphometric evaluation. , 1991, Arteriosclerosis and thrombosis : a journal of vascular biology.

[65]  J. Guyton,et al.  Human aortic fibrolipid lesions. Progenitor lesions for fibrous plaques, exhibiting early formation of the cholesterol-rich core. , 1985, The American journal of pathology.

[66]  J L Witztum,et al.  Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. , 1989, The Journal of clinical investigation.

[67]  G. Hansson,et al.  Prelesional complement activation in experimental atherosclerosis. Terminal C5b-9 complement deposition coincides with cholesterol accumulation in the aortic intima of hypercholesterolemic rabbits. , 1989, Laboratory investigation; a journal of technical methods and pathology.

[68]  W. Hollander,et al.  Soluble proteins in the human atheroschlerotic plaque , 1979 .

[69]  C. V. Smith,et al.  Lipid hydroperoxy and hydroxy derivatives in copper-catalyzed oxidation of low density lipoprotein. , 1990, Journal of lipid research.

[70]  R. Tangirala,et al.  Lysosomal accumulation of unesterified cholesterol in model macrophage foam cells. , 1993, The Journal of biological chemistry.

[71]  A. Daugherty,et al.  Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. , 1994, The Journal of clinical investigation.

[72]  H. Rus,et al.  Immunoelectron-microscopic localization of the terminal C5b-9 complement complex in human atherosclerotic fibrous plaque. , 1986, Atherosclerosis.

[73]  H. Kruth,et al.  Localization of unesterified cholesterol in human atherosclerotic lesions. Demonstration of filipin-positive, oil-red-O-negative particles. , 1984, The American journal of pathology.

[74]  Y. Zhang,et al.  Plasma protein insudation as an index of early coronary atherogenesis. , 1993, The American journal of pathology.

[75]  G. Hutchins,et al.  The relationship between coronary artery lesions and myocardial infarcts: ulceration of atherosclerotic plaques precipitating coronary thrombosis. , 1977, American heart journal.

[76]  R. Sato,et al.  Monoclonal antibody EMR1a/212D recognizing site of deposition of extracellular lipid in atherosclerosis: purification and characterization of the antigen. , 1989, The American journal of pathology.

[77]  M. Davies,et al.  Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content. , 1993, British heart journal.

[78]  W D Wagner,et al.  A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. , 1994, Circulation.

[79]  M. Bond,et al.  Immunohistochemical localization of heat shock protein-70 in normal-appearing and atherosclerotic specimens of human arteries. , 1990, The American journal of pathology.

[80]  R. Tracy,et al.  Variations in human aortic fatty streaks among geographic locations. , 1975, Atherosclerosis.

[81]  S. Srinivasan,et al.  Lipoprotein-hyaluronate associations in human aorta fibrous plaque lesions. , 1980, Atherosclerosis.

[82]  T. E. Whitaker,et al.  Oxidation of low density lipoprotein leads to particle aggregation and altered macrophage recognition. , 1992, The Journal of biological chemistry.

[83]  J. Resau,et al.  Unesterified cholesterol-rich lipid particles in atherosclerotic lesions of human and rabbit aortas. , 1988, The American journal of pathology.

[84]  H. Kruth Subendothelial accumulation of unesterified cholesterol. An early event in atherosclerotic lesion development. , 1985, Atherosclerosis.

[85]  P. Kovanen,et al.  Modification of low density lipoproteins by secretory granules of rat serosal mast cells. , 1991, The Journal of biological chemistry.

[86]  I. Tabas,et al.  Regulation of the threshold for lipoprotein-induced acyl-CoA:cholesterol O-acyltransferase stimulation in macrophages by cellular sphingomyelin content. , 1994, Journal of lipid research.

[87]  R. Wissler,et al.  A study of the immunohistochemical localization of serum lipoproteins and other plasma proteins in human atherosclerotic lesions. , 1965, Experimental and molecular pathology.

[88]  C. W. Adams,et al.  The action of human high density lipoprotein on cholesterol crystals. Part 2. Biochemical observations. , 1978, Atherosclerosis.

[89]  G. Anantharamaiah,et al.  Liposome-like particles isolated from human atherosclerotic plaques are structurally and compositionally similar to surface remnants of triglyceride-rich lipoproteins. , 1994, Arteriosclerosis and thrombosis : a journal of vascular biology.

[90]  J. Anderson,et al.  Immunoelectrophoretic and immunohistochemical characterizations of fibrinogen derivatives in atherosclerotic aortic intimas and vascular prosthesis pseudo-intimas. , 1992, The American journal of pathology.

[91]  M. J. Mitchinson,et al.  Insoluble lipids in human atherosclerotic plaques. , 1982, Atherosclerosis.

[92]  A. Fogelman,et al.  Lipid accumulation in rabbit aortic intima 2 hours after bolus infusion of low density lipoprotein. A deep-etch and immunolocalization study of ultrarapidly frozen tissue. , 1991, Arteriosclerosis and thrombosis : a journal of vascular biology.

[93]  J. Guyton,et al.  Development of the atherosclerotic core region. Chemical and ultrastructural analysis of microdissected atherosclerotic lesions from human aorta. , 1994, Arteriosclerosis and thrombosis : a journal of vascular biology.

[94]  W. J. Johnson,et al.  Cell Toxicity Induced by Inhibition of Acyl Coenzyme A:Cholesterol Acyltransferase and Accumulation of Unesterified Cholesterol * , 1995, The Journal of Biological Chemistry.

[95]  C. Böttcher,et al.  Changes in the composition of phospholipids and of phospholipid fatty acids associated with atherosclerosis in the human aortic wall , 1961 .

[96]  A. Gotto,et al.  Correlation of apolipoprotein B retention with the structure of atherosclerotic plaques from human aortas. , 1978, Laboratory investigation; a journal of technical methods and pathology.

[97]  M. Brown,et al.  Stimulation of Cholesteryl Ester Synthesis in Macrophages by Extracts of Atherosclerotic Human Aortas and Complexes of Albumin/Cholesteryl Esters , 1981, Arteriosclerosis.

[98]  M. Medow,et al.  Excess membrane cholesterol alters calcium movements, cytosolic calcium levels, and membrane fluidity in arterial smooth muscle cells. , 1991, Circulation research.

[99]  J. Resau,et al.  Characterization of two unique cholesterol-rich lipid particles isolated from human atherosclerotic lesions. , 1990, The American journal of pathology.

[100]  Qingbo Xu,et al.  Immunology of atherosclerosis. Demonstration of heat shock protein 60 expression and T lymphocytes bearing alpha/beta or gamma/delta receptor in human atherosclerotic lesions. , 1993, The American journal of pathology.

[101]  Reynolds Gd,et al.  C-reactive protein immunohistochemical localization in normal and atherosclerotic human aortas. , 1987 .

[102]  A. Chait,et al.  Phagocytosis of lipase-aggregated low density lipoprotein promotes macrophage foam cell formation. Sequential morphological and biochemical events. , 1991, Arteriosclerosis and thrombosis : a journal of vascular biology.