Phagocytosis of mast cell granule remnant-bound LDL by smooth muscle cells of synthetic phenotype: A scavenger receptor-mediated process that effectively stimulates cytoplasmic cholesteryl ester synthesis

Journal of Lipid Research

Volumn 37, Issue 10, 1996, Pages 2155-2166

  Wang, Yenfeng ^a   Lindstedt, Ken A ^a   Kovanen, Petri T ^a  

^a WIHURI RESEARCH INSTITUTE   (Finland)

Author keywords

cholesteryl linoleate; cholesteryl oleate; heparin proteoglycans; lysosomes

Indexed keywords

ACETYL LOW DENSITY LIPOPROTEIN; CELL RECEPTOR; CHOLESTEROL ESTER; CHOLESTEROL OLEATE; FAT DROPLET; HEPARIN DERIVATIVE; LINOLEIC ACID; LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN; POLYINOSINIC ACID; PROTEOGLYCAN;

ADOLESCENT; ANIMAL CELL; ARTICLE; ATHEROSCLEROSIS; CELL GRANULE; FEMALE; FOAM CELL; LIPID METABOLISM; LIPID TRANSPORT; LYSOSOME; MAST CELL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; RABBIT; SMOOTH MUSCLE FIBER;

ANIMALS; AORTA; CHOLESTEROL ESTERS; CYTOPLASMIC GRANULES; FEMALE; HUMANS; LIPOPROTEINS, LDL; MAST CELLS; MEMBRANE PROTEINS; MUSCLE, SMOOTH, VASCULAR; PHAGOCYTOSIS; POLY I; RABBITS; RECEPTORS, IMMUNOLOGIC; RECEPTORS, LIPOPROTEIN; RECEPTORS, SCAVENGER; SCAVENGER RECEPTORS, CLASS B;

EID: 0029862487     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (56)

1. Thyberg, J., U. Hedin, M. Sjölund, L. Palmberg, and B. A. Bottger. 1990. Regulation of differentiated properties and proliferation of arterial smooth muscle cells. Arteriosclerosis. 10: 966-990.
2. Ross, R. 1986. The pathogenesis of atherosclerosis - an update. N. Engl. J. Med. 314: 488-500.
3. Simons, M., G. Leclerc, R. D. Safian, J. M. Isner, L. Weir, and D. S. Bairn. 1993. Relation between activated smooth-muscle cells in coronary-artery lesions and restenosis after atherectomy. N. Engl. J. Med. 328: 608-613.
4. Goldstein, J. L., R. G. W. Anderson, L. M. Buja, S. K. Basu, and M. S. Brown. 1977. Overloading human aortic smooth muscle cells with low density lipoprotein-cholesteryl esters reproduces features of atheroslerosis in vitro. J. Clin. Invest. 59: 1196-1202.
5. Wang, Y., K. A. Lindstedt, and P. T. Kovanen. 1995. Mast cell granule remnants carry LDL into smooth muscle cells of synthetic phenotype and induce their conversion into foam cells. Arterioscler. Thromb. Vasc. Biol. 15: 801-810.
6. Kovanen, P. T. 1991. Mast cell granule-mediated uptake of low density lipoproteins by macrophages: a novel carrier mechanism leading to the formation of foam cells. Ann. Med. 23: 551-559.
7. Kovanen, P. T. 1993. The mast cell - a potential link between inflammation and cellular cholesterol deposition in atherogenesis. Eur. Heart. J. 14 (Suppl K): 105-117.
8. Lindstedt, K. A., J. O. Kokkonen, and P. T. Kovanen. 1992. Soluble heparin proteoglycans released from stimulated mast cells induce uptake of low density lipoproteins by macrophages via scavenger receptor-mediated phagocytosis. J. Lipid Res. 33: 65-75.
9. Pitas, R. E., T. L. Innerarity, and R. W. Mahley. 1983. Foam cells in explants of atherosclerotic rabbit aortas have receptors for β-very low density lipoproteins and modified low density lipoproteins. Arteriosclerosis. 3: 2-12.
10. Bickel, P. E., and M. W. Freeman. 1992. Rabbit aortic smooth muscle cells express inducible macrophage scavenger receptor messenger RNA that is absent from endothelial cells. J. Clin. Invest. 90: 1450-1457.
11. Pitas, R. E., A. Friera, J. McGuire, and S. Dejager. 1992. Further characterization of the acetyl LDL (scavenger) receptor expressed by rabbit smooth muscle cells and fibroblasts. Arterioscler. Thromb. 12: 1235-1244.
12. Li, H., M. W. Freeman, and P. Libby. 1995. Regulation of smooth muscle cell scavenger receptor expression in vivo by atherogenic diets and in vitro by cytokines. J. Clin. Invest. 95: 122-133.
13. Falcone, D. J., N. Mated, H. Shio, C. R. Minick, and S. D. Fowler. 1984. Lipoprotein-heparin-fibronectin-denatured collagen complexes enhance cholesteryl ester accumulation in macrophages. J. Cell. Biol. 99: 1266-1274.
14. Kielian, M. C., R. M. Steinman, and Z. A. Cohn. 1982. Intralysosomal accumulation of polyanions. I. Fusion of pinocytic and phagocytic vacuoles with secondary lysosomes. J. Cell. Biol. 93: 866-874.
15. Avila, J. L., and J. Convit. 1975. Inhibition of leucocytic lysosomal enzymes by glycosaminoglycans in vitro. Biochem. J. 152: 57-64.
16. Avila, J. L., and J. Convit. 1976. Physicochemical characteristics of the glycosaminoglycan-lysosomal enzyme interaction in vitro. A model of control of leucocytic lysosomal activity. Biochem. J. 160: 129-136.
17. Lindstedt, K. A., J. O. Kokkonen, and P. T. Kovanen. 1993. Inhibition of copper-mediated oxidation of LDL by rat serosal mast cells: a novel cellular protective mechanism involving proteolysis of the substrate under oxidative stress. Arterioscler. Thromb. 13: 23-32.
18. Havel, R. J., H. A. Eder, and J. H. Bragdon. 1955. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J. Clin. Invest. 34: 1345-1353.
19. Paananen, K., and P. T. Kovanen. 1994. Proteolysis and fusion of low density lipoprotein particles independently strengthen their binding to exocytosed mast cell granules. J. Biol. Chem. 269: 2023-2031.
20. Mahley, R. W., K. H. Weisgraber, G. W. Melchior, T. L. Innerarity, and K. S. Holcombe. 1980. Inhibition of receptor-mediated clearance of lysine and arginine-modified lipoproteins from the plasma of rats and monkeys. Proc. Natl. Acad. Sci. USA. 77: 225-229.
21. Basu, S. K., J. L. Goldstein, R. G. W. Anderson, and M. S. Brown. 1976. Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc. Natl. Acad. Sci. USA. 73: 3178-3182.
22. Hessler, J. R., D. W. Morel, L. J. Lewis, and G. M. Chisolm. 1983. Lipoprotein oxidation and lipoprotein induced cytotoxicity. Arteriosclerosis. 3: 215-222.
23. Goldstein, J. L., and M. S. Brown. 1974. Binding and degradation of low density lipoproteins by cultured human fibroblasts. J. Biol. Chem. 249: 5135-5162.
24. Doi, T., T. Wada, T. Kodama, K. I. Higashi, Y. Kurihara, H. Itakura, Y. Yazaki, and A. Matsumoto. 1993. Charged collagen structure mediates the recognition of negatively charged macromolecules by macrophage scavenger receptors. J. Biol. Chem. 268: 2126-2133.
25. Brown, M. S., Y. K. Ho, and J. L. Goldstein. 1980. The cholesteryl ester cycle in macrophage foam cells. Continual hydrolysis and reesterification of cytoplasmic cholesteryl esters. J. Biol. Chem. 255: 9344-9352.
26. Kritharides, L., W. Jessup, J. Gifford, and R. T. Dean. 1993. A method for defining the stages of low-density lipoprotein oxidation by the separation of cholesterol-and cholesteryl ester-oxidation products using HPLC. Anal. Biochem. 213: 79-89.
27. Maor, I., and M. Aviram. 1994. Oxidized low density lipoprotein leads to macrophage accumulation of unesterified cholesterol as a result of lysosomal trapping of the lipoprotein hydrolyzed cholesteryl ester. J. Lipid Res. 35: 803-819.
28. Brown, M. S., S. E. Dana, and J. L. Goldstein. 1975. Receptor-dependent hydrolysis of cholesteryl esters contained in plasma low density lipoprotein. Proc. Natl. Acad. Sci. USA. 72: 2925-2929.
29. Goldstein, J. L., G. Y. Brunschede, and M. S. Brown. 1975. Inhibition of the proteolytic degradation of low density lipoprotein in human fibroblasts by chloroquine, concanavalin A, and triton WR 1339. J. Biol. Chem. 250: 7854-7862.
30. Slotte, J. P., and E. L. Bierman. 1988. Fatty acid specificity of the lysosomal acid cholesterol esterase in intact human arterial smooth muscle cells. Biochim. Biophys. Acta. 958: 308-312.
31. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with Folin phenol reagent. J. Biol. Chem. 193: 265-275.
32. Kokkonen, J. O., and P. T. Kovanen. 1989. Proteolytic enzymes of mast cell granules degrade low density lipoproteins and promote their granule-mediated uptake by macrophages in vitro. J. Biol. Chem. 264: 10749-10755.
33. Kokkonen, J. O., and P. T. Kovanen. 1987. Low density lipoprotein binding by mast cell granules: demonstration of binding of apolipoprotein B to heparin proteoglycan of exocytosed granules. Biochem. J. 241: 583-589.
34. Basu, S. K., M. S. Brown, Y. K. Ho, and J. L. Goldstein. 1979. Degradation of low density lipoprotein dextran sulfate complexes associated with deposition of cholesteryl esters in mouse macrophages. J. Biol. Chem. 254: 7141-7146.
35. Brown, M. S., and J. L. Goldstein. 1983. Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis. Annu. Rev. Biochem. 52: 223-261.
36. Goodman, D. S., D. Deykin, and T. Shiratori. 1964. The formation of cholesterol esters with rat liver enzymes. J. Biol. Chem. 239: 1335-1345.
37. Smith, E. B. 1974. The relationship between plasma and tissue lipids in human atherosclerosis. Adv. Lipid Res. 12: 1-49.
38. Srinivasan, S. R., P. Vijayagopal, K. Eberle, B. Radhakrishnamurthy, and G. S. Berenson. 1991. Interaction of high-affinity heparin subfraction with low-density-lipoprotein stimulates cholesteryl ester accumulation in mouse macrophages. Biochim. Biophys. Acta. 1081: 188-196.
39. Vijayagopal, P., S. R. Srinivasan, B. Radhakrishnamurthy, and G. S. Berenson. 1993. Human monocyte-derived macrophages bind low-density-lipoprotein-proteoglycan complexes by a receptor different from the low-density-lipoprotein receptor. Biochem. J. 289: 837-844.
40. Vijayagopal, P., S. R. Srinivasan, B. Radhakrishnamurthy, and G. S. Berenson. 1992. Lipoprotein-proteoglycan complexes from atherosclerotic lesions promote cholesteryl ester accumulation in human monocytes/macrophages. Arterioscler. Thromb. 12: 237-249.
41. Brown, M. S., and J. L. Goldstein. 1975. Regulation of the activity of the low density lipoprotein receptor in human fibroblasts. Cell. 6: 307-316.
42. Lindahl, U., H. Pertoft, and R. Seljelid. 1979. Uptake and degradation of mast-cell granules by mouse peritoneal macrophages. Biochem. J. 182: 189-193.
43. Atkins, F. M., and D. D. Metcalfe. 1983. Degradation of the heparin matrix of mast cell granules by cultured fibroblasts. J. Immunol. 131: 1420-1425.
44. Yurt, R. W., R. W. Leid, Jr., and K. F. Austen. 1977. Native heparin from rat peritoneal mast cells. J. Biol. Chem. 252: 518-521.
45. Kelley, J. L., C. A. Suenram, A. J. Valente, E. A. Sprague, M. M. Rozek, and C. J. Schwartz. 1985. Evolution of foam cells in subcutaneous rabbit carrageenan granulomas. II. Tissue and macrophage lipid composition. Am. J. Pathol. 120: 391-401.
46. Jaakkola, O., and T. Nikkari. 1990. Lipoprotein degradation and cholesterol esterification in primary cell cultures of rabbit atherosclerotic lesions. Am. J. Pathol. 137: 457-465.
47. Brockman, H. L. 1979. Enzymes of cholesteryl ester synthesis and hydrolysis in the arterial wall. In The Biochemistry of Atherosclerosis. A. M. Scanu, editor. Marcel Dekker, Inc. New York and Basel. 293-309.
48. Hajjar, D. P., K. B. Pomerantz, and J. W. Snow. 1990. Analysis of the physical state of cholesteryl esters in arterial-smooth-muscle-derived foam cells by differential scanning calorimetry. Biochem. J. 268: 693-697.
49. Pasquinelli, G., P. Preda, M. Vici, M. Gargiulo, A. Stella, M. D'Addato, and R. Laschi. 1989. Electron microscopy of lipid deposits in human atherosclerosis. Scanning Microsc. 3: 1151-1159.
50. Ylä-Herttuala, S., O. Jaakkola, C. Ehnholm, M. J. Tikkanen, T. Solakivi, T. Särkioja, and T. Nikkari. 1988. Characterization of two lipoproteins containing apolipoproteins B and E from lesion-free human aortic intima. J. Lipid Res. 29: 563-572.
51. Hoff, H. F., J. W. Gaubatz. 1982. Isolation, purification and characterization of a lipoprotein containing apoB from the human aorta. Atherosclerosis. 42: 273-297.
52. Camejo, G., E. Hurt, and M. Romano. 1985. Properties of lipoprotein complexes isolated by affinity chromatography from human aorta. Biochim. Biophys. Acta. 44: 389-401.
53. Belkner, J., R. Wiesner, H. Kühn, and V. Z. Lankin. 1991. The oxygenation of cholesterol esters by the reticulocyte lipoxygenase. FEBS Lett. 279: 110-114.
54. Hoff, H. F., N. Zyromski, D. Armstrong, and J. O'Neil. 1993. Aggregation as well as chemical modification of LDL during oxidation is responsible for poor processing in macrophages. J. Lipid Res. 34: 1919-1929.
55. Lee, M., L. K. Lindstedt, and P. T. Kovanen. 1992. Mast cell-mediated inhibition of reverse cholesterol transport. Arterioscler. Thromb. 12: 1329-1335.
56. Lindstedt, L., M. Lee, G. R. Castro, J-P. Fruchart, and P. T. Kovanen. 1996. Chymase in exocytosed rat mast cell granules effectively proteolyzes apolipoprotein A-I-containing lipoproteins, so reducing the cholesterol efflux-inducing ability of serum and aortic intimal fluid. J. Clin. Invest. 97: 2174-2182.