Macrophage-released proteoglycans enhance LDL aggregation: Studies in aorta from apolipoprotein E-deficient mice

Atherosclerosis

Volumn 150, Issue 1, 2000, Pages 91-101

  Maor, I ^a   Hayek, T ^a   Hirsh, M ^a   Iancu, T C ^a   Aviram, M ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Aggregated LDL; Aggregation; Apolipoprotein E; Arterial wall; Atherosclerosis; Macrophages; Proteoglycans

Indexed keywords

APOLIPOPROTEIN E; CHONDROITIN SULFATE; HEPARAN SULFATE; LOW DENSITY LIPOPROTEIN; PROTEOGLYCAN;

AGING; ANIMAL; AORTA; ARTERIOSCLEROSIS; ARTICLE; BIOSYNTHESIS; ELECTRON MICROSCOPY; MACROPHAGE; METABOLISM; MOUSE; PARTICLE SIZE; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

AGING; ANIMALS; AORTA; APOLIPOPROTEINS E; ARTERIOSCLEROSIS; CHONDROITIN SULFATES; HEPARITIN SULFATE; LIPOPROTEINS, LDL; MACROPHAGES; MICE; MICROSCOPY, ELECTRON; PARTICLE SIZE; PROTEOGLYCANS;

EID: 0034183036     PISSN: 00219150     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0021-9150(99)00390-1     Document Type: Article

References (58)

1. Wissler RW. Arterial foam cells with distinctive immunomorphologic and histochemical features of macrophages. Am J Pathol 1980;100:57-80.
2. Aviram M. Modified forms of low density lipoprotein and atherosclerosis. Atherosclerosis 1993;98:1-9.
3. Aviram M. Interaction of oxidized low density lipoprotein with macrophages in atherosclerosis and the antiatherogenicity of antioxidants. Eur J Clin Chem Clin Biochem 1996;34:599-608.
4. Aviram M. Beyond cholesterol: modifications of lipoproteins and increased atherogenicity. In: Neri Serneri GG, Gensini GF, Abbate R, Prisco D, editors. Atherosclerosis, Inflammation and Thrombosis. Florence: Scientific Press, 1993:15-36.
5. Hoff HF, O'Neil J. Lesion-derived low density lipoprotein and oxidized low density lipoprotein share a lability for aggregation, leading to enhanced macrophage degradation. Arterioscler Thromb 1991;11:1209-22.
6. Hoff HF, Gaubatz JW. Isolation, purification and characterization of a lipoprotein containing Apo-B from the human aorta. Atherosclerosis 1982;42:273-97.
7. Morton RE, West GA, Hoff HF. A low density lipoprotein-sized particle isolated from human atherosclerotic lesions is internalized by macrophages via a non-scavenger receptor mechanism. J Lipid Res 1986;27:1124-34.
8. Aviram M, Maor I, Keidar S, Hayek T, Oiknine J, Bar-El Y, Adler Z, Kertzman V, Milo S. Lesioned low density lipoprotein in atherosclerotic apolipoprotein E-deficient transgenic mice and in humans is oxidized and aggregated. Biochem Biophys Res Commun 1995;216:501-13.
9. Frank JS, Fogelman AM. Ultrastructure of the intima in WHHL and cholesterol-fed rabbit aortas prepared by ultra-rapid freezing and freezetetching. J Lipid Res 1989;30:967-78.
10. Nievelstein PF, Fogelman AM, Mottino G, Frank JS. Lipid accumulation in rabbit aortic intima 2 hours after bolus infusion of low density lipoprotein. Arterioscler Thromb 1991;11:1795-805.
11. Schissel SL, Tweedie-Hardman J, Rapp JH, Graham G, Williams KJ, Tabas I. Rabbit aorta and human atherosclerotic lesions hydrolyze the sphingomyelin of retained low-density lipoprotein. Proposed role for arterial wall sphingomyelinase in subendothelial retention and aggregation of atherogenic lipoproteins. J Clin Invest 1996;98:1455-64.
12. 2+ -stimulated sphingomyelinase is secreted by many cell types and is a product of the acid sphingomyelinase gene. J Biol Chem 1996;271:18431-6.
13. Khoo JC, Miller E, McLoughlin P, Steinberg D. Enhanced macrophage uptake of low density lipoprotein after self-aggregation. Arteriosclerosis 1988;8:348-58.
14. Suits AG, Chait A, Aviram M, Heinecke JW. Phagocytosis of aggregated lipoprotein by macrophages: low density lipoprotein receptor-dependent foam-cell formation. Proc Natl Acad Sci USA 1989;86:2713-7.
15. Heinecke JW, Suits AG, Aviram M, Chait A. Phagocytosis of lipasc-aggregated low density lipoprotein promotes macrophage foam cell formation. Sequential morphological and biochemical events. Arterioscler Thromb 1991;11:1643-51.
16. 2+-induced oxidation. Biochem J 1995;310:417-26.
17. Hoff HF, Whitaker TE, O'Neil J. Oxidation of low density lipoprotein leads to particle aggregation and altered macrophage recognition. J Biol Chem 1992;267:602-9.
18. Lougheed M, Steinbrecher UP. Mechanism of uptake of copper-oxidized low density lipoprotein in macrophages is dependent on its extent of oxidation. J Biol Chem 1996;20:11798-805.
19. Tertov W, Sobenin IA, Gabbasov ZA, Popov EG, Orekhov AN. Lipoprotein aggregation as an essential condition of intraccllular lipid accumulation caused by modified low density lipoproteins. Biochem Biophys Res Commun 1989;163:489-94.
20. Tertov W, Sobenin IA, Gabbasov ZA, Popov EG, Yaroslavov AA, Jauhiainen M, Ehnholm C, Smirnov VN, Orekhov AN. Three types of naturally occurring modified lipoproteins induce intracellular lipid accumulation in human aortic intimal cells - the role of lipoprotein aggregation. Eur J Clin Chem Clin Biochem 1992;30:171-8.
21. Maor I, Aviram M. Macrophage released proteoglycans are involved in cell-mediated aggregation of LDL. Atherosclerosis 1998;142:57-66.
22. Camejo G, Hurt E, Wiklund O, Rosengren B, Lopez F, Bondjers G. Modifications of low-density lipoprotein induced by arterial proteoglycans and chondroitin-6 sulfate. Biochim Biophys Acta 1991;1096:253-61.
23. Hurt-Camejo E, Camejo G, Rosengren B, Lopez F, Ahlstrom C, Fager G, Bondjers G. Effect of arterial proteoglycans and glycosaminoglycans on low density lipoprotein oxidation and its uptake by human macrophages and arterial smooth muscle cells. Arterioscler Thromb 1992;12:569-83.
24. Mitchinson MJ, Ball RY. Macrophages and atherogenesis. Lancet 1987;18:146-9.
25. Nathan CF. Secretory products of macrophages. J Clin Invest 1987;79:319-26.
26. Owens RT, Wagner WD. Proteoglycans produced by cholesterol-enriched macrophages bind plasma low density lipoprotein. Atherosclerosis 1991;91:229-40.
27. Edwards IJ, Xu H, Obunike JC, Goldberg IJ, Wagner WD. Differentiated macrophages synthesize a heparan sulfate proteoglycan and an oversulfated chondroitin sulfate proteoglycan that bind lipoprotein lipase. Arterioscler Thromb Vase Biol 1995;15:400-9.
28. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 1992;71:343-53.
29. Zhang SH, Reddick RC, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 1992;258:468-71.
30. Zhang SH, Reddick RL, Burkey B, Meada N. Diet-induced atherosclerosis in mice heterozygous and homozygous for apolipoprotein E gene disruption. J Clin Invest 1994;94:937-45.
31. Maor I, Hayek T, Coleman R, Aviram M. Plasma LDL oxidation leads to its aggregation in the atherosclerotic apolipoprotein E-deficient mice. Arterioscler Thromb Vase Biol 1997;17:2995-3005.
32. Jeong TS, Schissel SL, Tabas I, Pownall HJ, Tall AR, Jiang X. Increased sphingomyelin content of plasma lipoproteins in apolipoprotein E knockout mice reflects combined production and catabolic defects and enhances reactivity with mammalian sphingomyelinase. J Clin Invest 1998;101:905-12.
33. Aviram M. Plasma lipoprotein separation by discontinuous density gradient ultracentrifugation in hyperlipoproteinemic patients. Biochem Med 1983;30:111-8.
34. Bilheimer DW, Eisenberg S, Levy RI. The metabolism of very low density lipoprotein. Biochim Biophys Acta 1972;260:212-21.
35. Lowry OH, Rosebrough NJ, Farr AL, Randell R. Protein measurement with the folin reagent. J Biol Chem 1951;193:265-75.
36. Chaimori N, Henry RJ. Study of the ferric chloride method for determination of total cholesterol and cholesterol esters. Am J Clin Pathol 1959;31:305-9.
37. Wieland O. Fine enzymatische Method zur Bestimmung von Glycerin. Biochem Z 1957;324:313-7.
38. Barlett GR. Phosphorous assay in column chromatography. J Biol Chem 1959;234:466-8.
39. Piha M, Lindstedt L, Kovanen PT. Fusion of proteolyzed low-density lipoprotein in the fluid phase: a novel mechanism generating atherogenic lipoprotein particles. Biochemistry 1995;34:10120-9.
40. Vijayagopal P, Srinivasan SR, Xu JH, Dalferes ER Jr, Radhakrishnamurthy B, Berenson GS. Lipoprotein-proteoglycan complexes induce continued cholesteryl ester accumulation in foam cells from rabbit atherosclerotic lesion. J Clin Invest 1993;91:1011-8.
41. Van de Lest CH, Versteeg EM, Veerkamp JH, van Kuppevelt TH. A spectrophotometric method for the determination of heparan sulfate. Biochim Biophys Acta 1994;1201:305-11.
42. Rosenfeld ME, Khoo JC, Miller E, Parthasarathy S, Palinski W, Witztum JL. Macrophage-derived foam cells freshly isolated from rabbit atherosclerotic lesions degrade modified lipoproteins, promote oxidation of low-density lipoproteins, and contain oxidation-specific lipid protein adducats. J Clin Invest 1991;87:90-9.
43. Hagen TLM, Vianen WV, Bakker-Woudenberg AJM. Isolation and characterization of murine kupffer cells and splenic macrophages. J Immunol Methods 1996;193:81-91.
44. Ghosh SK, Chakraborti T, Michael JR, Chakraborti S. Oxidantmediated proteolytic activation of Ca(+)-ATPase in microsomes of pulmonary smooth muscle. FEBS Lett 1996;387:171-4.
45. Belinky PA, Aviram M, Fuhrman B, Rosenblat M, Vaya J. The antioxidative effects of the isoflavan constituents of LDL during its oxidation. Atherosclerosis 1988;137:49-61.
46. Fowler SD, Greenspan P. Application of nile red, a fluorescent hydrophobic probe for the detection of neutral lipid deposits in tissue sections: comparison with oil red O. J Histochem Cytochem 1985;33:833-6.
47. Marathe S, Schissel SL, Yellin MJ, Reatini N, Mintzer R, Williams KJ, Tabas I. Human vascular endothelial cells are rich and regulatable source of secretory sphingomyelinase. J Biol Chem 1998;273:4081-8.
48. Aviram M, Rosenblat M. Macrophage-mediated oxidation of extracellular low density lipoprotein requires an initial binding of the lipoprotein to its receptor. J Lipid Res 1994;35:385-98.
49. Aviram M, Rosenblat M, Etzioni A, Levy R. Activation of NADPH oxidase is required for macrophage-mediated oxidation of LDL. Metabolism 1996;45:1069-79.
50. Owens RT, Wagner WD. Chondroitin sulfate proteoglycan and heparan sulfate proteoglycan production by cultured pigeon peritoneal macrophages. J Leukocyte Biol 1992;51:626-33.
51. Christner JE. Biosynthesis of chondroitin sulfate proteoglycan by P388D1 macrophage-like cell line. Arteriosclerosis 1988;8:535-43.
52. Vijayagopal P, Srinivasan SR, Radhakrishnamurthy B, Berenson GS. Human monocyte-derived macrophages bind low-density lipoprotein-proteoglycan complexes by a receptor different from the low-density-lipoprotein receptor. Biochem J 1993;289:837-44.
53. Vijayagopal P, Srinivasan SR, Radhakrishnamurthy B, Berenson GS. Interaction of serum lipoproteins and a proteoglycan from bovine aorta. J Biol Chem 1981;256:8234-41.
54. Vijayagopal P, Srinivasan SR, Radhakrishnamurthy B, Berenson GS. Hemostatic properties and serum lipoprotein binding of a heparan sulfate proteoglycan from bovine aorta. Biochim Biophys Acta 1983;758:70-83.
55. Camejo G, Rosengren B, Olson U, Lopez F, Olofson SO, Westerlund C, Bondjers G. Molecular basis of the association of arterial proteoglycans with low density lipoproteins: its effect on the structure of the lipoprotein particle. Eur Heart J 1990;11:164-73.
56. Schissel SL, Jiang X, Tweedie-Hardman J, Jeong T, Camejo EH, Najib J, Rapp JH, Williams K, Tabas I. Secretory sphingomyelinase, a product of the acid sphingomyelinase gene, can hydrolyze atherogenic lipoproteins at neutral pH. J Biol Chem 1998;273:2738-48.
57. Kaplan M, Williams KJ, Mandel H, Aviram M. Role of macrophage glycosaminoglycans in the cellular catabolism of oxidized LDL and macrophages. Arterioscler Thromb Vase Biol 1998;18:542-53.
58. Havlorsen B, Aas UK, Kulseth MA, Drevon C, Christiansen EN, Kolset SO. Proteoglycans in macrophages: characterization and possible role in the cellular uptake of lipoproteins. Biochem J 1998;331:743-52.