Uptake of oxidized LDL by macrophages differs from that of acetyl LDL and leads to expansion of an acidic endolysosomal compartment

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 19, Issue 8, 1999, Pages 1881-1890

  Lougheed, Marilee ^a   Moore, Edwin D W ^a   Scriven, David R L ^a   Steinbrecher, Urs ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Endocytosis; Lysosomes; Macrophages; Oxidized LDL; Scavenger receptors

Indexed keywords

ACETYL LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL PH; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FEMALE; FLUORESCENCE MICROSCOPY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

EID: 0032800011     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.19.8.1881     Document Type: Article

References (67)

1. Brown MS, Goldstein JL. Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis. Annu Rev Biochem. 1983;52:223-261.
2. Goldstein JL, Ho YK, Basu SK, Brown MS. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci U S A. 1979;76:333-337.
3. Steinbrecher UP, Parthasarathy S, Leake DS, Witztum JL, Steinberg D. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degradation of low density lipoprotein phospholipids. Proc Natl Acad Sci U S A. 1984;81:3883-3887.
4. Khoo JC, Miller E, McLoughlin P, Steinherg D. Enhanced macrophage uptake of low density lipoprotein after self-aggregation. Arteriosclerosis. 1988;8:348-358.
5. Lougheed M, Ming Lum C, Ling W, Suzuki H, Kodama T, Steinbrecher UP. High-affinity saturable uptake of oxidized low density lipoprotein by macrophages from mice lacking the scavenger receptor class A type I/II. J Biol Chem. 1997;272:12938-12944.
6. Sparrow CP, Parthasarathy S, Steinberg D. A macrophage receptor that recognizes oxidized low density lipoprotein but not acetylated low density lipoprotein. J Biol Chem. 1989;264:2599-2604.
7. Zhang H, Basra HJK, Steinbrecher UP. Effects of oxidatively modified LDL on cholesterol esterification in cultured macrophages. J Lipid Res. 1990;31:1361-1369.
8. Lougheed M, Steinbrecher U. Mechanism of uptake of copper-oxidized low density lipoprotein in macrophages is dependent on its extent of oxidation. J Biol Chem. 1996;271:11798-11805.
9. Lougheed M, Zhang H, Steinbrecher U. Oxidized low density lipoprotein is resistant to cathepsins and accumulates within macrophages. J Biol Chem. 1991;266:14519-14525.
10. Hoppe G, O'Neil J, Hoff H. Inactivation of lysosomal proteases by oxidized low density lipoprotein is partially responsible for its poor degradation by mouse peritoneal macrophages. J Clin Invest. 1994;94: 1506-1512.
11. O'Neil J, Hoppe G, Sayre LM, Hoff HF. Inactivation of cathepsin B by oxidized LDL involves complex formation induced by binding of putative reactive sites exposed at low pH to thiols on the enzyme. Free Radic Biol Med. 1997;23:215-225.
12. Jessup W, Mander EL, Dean RT. The intracellular storage and turnover of apolipoprotein B of oxidized LDL in macrophages. Biochim Biophys Acta. 1992;1126:167-177.
13. Roma P, Bernini F, Fogliatto R, Bertulli SM, Negri S, Fumagalli R, Catapano AL. Defective catabolism of oxidized LDL by J774 murine macrophages. J Lipid Res. 1992;33:819-829.
14. Swanson J, Bushnell A, Silverstein S. Tubular lysosome morphology and distribution within macrophages depend on the integrity of cytoplasmic microtubules. Proc Natl Acad Sci U S A. 1987;84:1921-1925.
15. Knapp P, Swanson J. Plasticity of the tubular lysosomal compartment in macrophages. J Cell Sci. 1990;95:433-439.
16. Tassin M-T, Lang T, Antoine J-T, Hellio R, Ryter A. Modified lysosomal compartment as carrier of slowly and non-degradable tracers in macrophages. Eur J Cell Biol. 1990;52:219-228.
17. Tabas I, Lim S, Xu X-X, Maxfield F. Endocytosed β-VLDL and LDL are delivered to different intracellular vesicles in mouse peritoneal macrophages. J Cell Biol. 1990;111:929-940.
18. Jerome W, Cash C, Webber R, Horton R, Yancey P. Lysosomal lipid accumulation from oxidized low density lipoprotein is correlated with hypertrophy of the Golgi apparatus and trans-Golgi network. J Lipid Res. 1998;39:1362-1371.
19. Suzuki H, Kurihara Y, Takeya M, Kamada N, Kataoka M, Jishage K, Ueda O, Sakaguchi T, Higashi T, Suzuki T, Takashima Y, Kawabe Y, Cynshi O, Wada Y, Honda M, Kurihara H, Toi T, Matsomoto A, Azuma A, Noda T, Toyoda Y, Itakura H, Yazaki Y, Horiuchi S, Takahashi K, Kruijt JK, van Berkel TJC, Steinbrecher UP, Ishibashi S, Maeda N, Gordon S, Kodama T. Resistance to atherosclerosis and susceptibility to infection in scavenger receptor knockout mice. Nature. 1997;386: 292-296.
20. Steinbrecher UP, Witztum JL, Parthasarathy S, Steinberg D. Decrease in reactive amino groups during oxidation or endothelial cell modification of LDL: correlation with changes in receptor-mediated catabolism. Arteriosclerosis. 1987;7:135-143.
21. 99mTechnetium-labeled low density lipoprotein: receptor recognition and intracellular sequestration of radiolabel. J Lipid Res. 1991;32:1-8.
22. Pitas RE, Innerarity TL, Weinstein JN, Mahley RW. Acetoacetylated lipoproteins used to distinguish fibroblasts from macrophages in vitro by fluorescence microscopy. Arteriosclerosis. 1981;1:177-185.
23. Carrington WA, Lynch RM, Moore ED, Isenberg G, Fogarty KE, Fay FS. Superresolution three-dimensional images of fluorescence in cells with minimal light exposure. Science. 1995;268:1483-1487.
24. Dean M, Martin J. Intracellular localization of β-glucuronidase in fibroblasts after direct transfer from macrophages. Biochem J. 1988;256: 335-341.
25. Peters TJ, Muller M, De Duve C. Lysosomes of the arterial wall, I: isolation and subcellular fractionation of cells from normal rabbit aorta. J Exp Med. 1972;136:1117-1139.
26. Seymour CA, Peters TJ. Enzyme activities in human liver biopsies: assay methods and activities of some lysosomal and membrane-bound enzymes in control tissue and serum. Clin Sci Mol Med. 1977;52:229-239.
27. Ling W, Lougheed M, Suzuki H, Buchan A, Kodama T, Steinbrecher U. Oxidized or acetylated low density lipoprotein are rapidly cleared by the liver in mice with disruption of the scavenger receptor class A type I/type II gene. J Clin Invest. 1997;100:244-252.
28. Hoff H, Zyromski N, Armstrong D, O'Neil J. Aggregation as well as chemical modification of LDL during oxidation is responsible for poor processing in macrophages. J Lipid Res. 1993;34:1919-1930.
29. Zhang W-Y, Gaynor P, Kruth H. Aggregated low density lipoprotein induces and enters surface-connected compartments of human monocyte-macrophages. J Biol Chem. 1997;272:31700-31706.
30. Blum J, Fiani M, Stahl P. Proteolytic cleavage of ricin A chain in endosomal vesicles. J Biol Chem. 1991;266:22091-22095.
31. Mander E, Jessup W, Dean R. Apolipoprotein B of oxidized LDL accumulates in the lysosomes of macrophages. Biochim Biophys Acta. 1994; 1212:80-92.
32. Henriksen T, Mahoney EM, Steinberg D. Enhanced macrophage degradation of biologically modified low density lipoprotein. Arteriosclerosis. 1983;3:149-159.
33. Esterbauer H, Jurgens G, Quehenberger O, Koller E. Autoxidation of human low density lipoprotein: loss of polyunsaturated fatty acids and vitamin E and generation of aldehydes. J Lipid Res. 1987;28:495-509.
34. Esterbauer H, Gebicki J, Puhl H, Jurgens G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med. 1992;13:341-390.
35. Brown M, Ho Y, Goldstein J. The cholesteryl ester cycle in macrophage foam cells. J Cell Biol. 1980;255:9344-9352.
36. McGookey D, Anderson R. Morphological characterization of the cholesteryl ester cycle in cultured mouse macrophage foam cells. J Cell Biol. 1983;97:1156-1168.
37. Shio H, Haley N, Fowler S. Characterization of lipid-laden aortic cells from cholesterol-fed rabbits. II: morphometric analysis of lipid-filled lysosomes and lipid droplets in aortic cell populations. Lab Invest. 1978; 1978:390-397.
38. Shio H, Haley N, Fowler S. Characterization of lipid-laden aortic cells from cholesterol-fed rabbits. III: intracellular localization of cholesterol and cholesteryl ester. Lab Invest. 1979;41:160-167.
39. Fowler S, Berberian P, Shio H, Goldfischer S, Wolinsky H. Characterization of cell populations isolated from aortas of rhesus monkeys with experimental atherosclerosis. Circ Res. 1980;46:520-530.
40. Jerome W, Lewis J. Early atherogenesis in White Carneau pigeons, II: ultrastructural and cytochemical observations. Am J Pathol. 1985;119: 210-222.
41. Lewis J, Taylor R, Ohta T. Lysosomal alterations during coronary atherosclerosis in the pigeon: correlative cytochemical and three-dimensional HVEM/IVEṀ observations. Exp Mol Pathol. 1988;48: 103-115.
42. Balls J, Haust M, More R. Electron-microscopic studies in human atherosclerosis: cellular elements in aortic fatty streaks. Exp Mol Pathol. 1964;3:511-525.
43. Marshall J, Adams J, O'Neal R, DeBakey M. The ultrastructure of uncomplicated human atheroma in surgically resected aortas. J Atheroscler Res. 1966;6:120-131.
44. Guyton JR, Klemp KF. The lipid-rich core region of human atherosclerotic fibrous plaques: prevalence of small droplets and vesicles by electron microscopy. Am J Pathol. 1989;134:705-717.
45. Mahlberg F, Glick J, Jerome W, Rothblat G. Metabolism of cholesterol ester lipid droplets in a J774 macrophage foam cell model. Biochim Biophys Acta. 1990;1045:291-298.
46. Tangirala R, Mahlberg F, Glick J, Jerome W, Rothblat G. Lysosomal accumulation of unesterified cholesterol in model macrophage foam cells. J Biol Chem. 1993;268:9653-9660.
47. Parhami F, Fang ZT, Fogelman AM, Andalibi A, Territo MC, Berliner JA. Minimally modified low density lipoprotein-induced inflammatory responses in endothelial cells are mediated by cyclic adenosine monophosphate. J Clin Invest. 1993;92:471-478.
48. Liao F, Berliner JA, Mehrabian M, Navab M, Demer LL, Lusis AJ, Fogelman AM. Minimally modified low density lipoprotein is biologically active in vivo in mice. J Clin Invest. 1991;87:2253-2257.
49. Berliner JA, Territo MC, Sevanian A, Ramin S, Kim JA, Bamshad B, Esterson M, Fogelman AM. Minimally modified low density hpoprotein stimulates monocyte endothelial interactions. J Clin Invest. 1990;85:1260-1266.
50. Cushing SD, Berliner JA, Valente AJ, Territo MC, Navab M, Parhami F, Gerrity R, Schwartz CJ, Fogelman AM. Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells. Proc Natl Acad Sci U S A. 1990;87:5134-5138.
51. Lang T, Tassin M, Ryter A. Bacterial immunolabeling of macrophages after phagocytosis and degradation of Bacillus subtilis. Infect Immun. 1988;56:468-478.
52. Bright NA, Reaves BJ, Mullock BM, Luzio JP. Dense core lysosomes can fuse with late endosomes and are re-formed from the resultant hybrid organelles. J Cell Sci. 1997;110:2027-2040.
53. Endemann G, Stanton LW, Madden KS, Bryant CM, White RT, Protter AA. CD36 is a receptor for oxidized low density lipoprotein. J Biol Chem. 1993;268:11811-11816.
54. Nicholson A, Frieda S, Pierce A, Silverstein R. Oxidized LDL binds to CD36 on human monocyte-derived macrophages and transfected cell lines. Arterioscler Thromb Vasc Biol. 1995;15:269-275.
55. Nozaki S, Kashiwagi H, Yamashita S, Nakagawa T, Kostner B, Tomiyami Y, Nakata A, Ishigami M, Miyagawa J-I, Kameda-Takemura K, Kurata Y, Matsuzawa Y. Reduced uptake of oxidized low density lipoproteins in monocyte-derived macrophages from CD36-deficient subjects. J Clin Invest. 1995;96:1859-1865.
56. da Silva RP, Platt N, de Villiers JS, Gordon S. Membrane molecules and macrophage endocytosis: scavenger receptor and macrosialin as markers of plasma-membrane and vacuolar functions. Biochem Soc Trans. 1996; 24:220-224.
57. Ramprasad M, Terpstra V, Kondratenko N, Quehenberger O, Steinberg D. Cell surface expression of mouse macrosialin and human CD68 and their roles as macrophage receptors for oxidized low density lipoprotein. Proc Natl Acad Sci U S A. 1996;93:14833-14838.
58. Stanton LW, White RT, Bryant CM, Protter AA, Endemann G. A macrophage Fc receptor for IgG is also a receptor for oxidized low density lipoprotein. J Biol Chem. 1992;267:22446-22451.
59. Elomaa O, Kangas M, Sahlberg C, Tuukkanen J, Sormunen R, Liakka A, Thesleff I, Kraal G, Tryggvason K. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell. 1995;80:603-609.
60. van der Laan LJW, Kangas M, Dopp EA, Brougholub E, Elomaa O, Tryggvason K, Kraal G. Macrophage scavenger receptor MARCO: in vitro and in vivo regulation and involvement in the anti-bacterial host defense. Immunol Lett. 1997;57:203-208.
61. Sawamura T, Kume N, Aoyama T, Moriwaki H, Hoshikawa H, Aiba Y, Tanaka T, Miwa S, Katsura Y, Kita T, Masaki T. An endothelial receptor for oxidized low-density lipoprotein. Nature. 1997;386:73-77.
62. Adachi H, Tsujimoto M, Arai H, Inoue K. Expression cloning of a novel scavenger receptor from human endothelial cells. J Biol Chem. 1997;272: 31217-31220.
63. Gruenberg J, Maxfield F. Membrane transport in the endocytic pathway. Curr Opin Cell Biol. 1995;5:552-563.
64. Novick P, Zerial M. The diversity of Rab proteins in vesicle transport. Curr Opin Cell Biol. 1997;9:496-504.
65. Murphy C, Saffrich R, Grummt M, Gournier H, Ryhin V, Rubino M, Auvinen P, Lutcke A, Parton RG, Zerial M. Endosome dynamics regulated by a Rho protein. Nature. 1996;384:427-432.
66. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol. 1996;135:913-924.
67. Folli F, Alvaro D, Gigliozzi A, Bassotti C, Kahn CR, Pontiroli AE, Capocaccia L, Jezequel AM, Benedetti A. Regulation of endocytic-transcytotic pathways and bile secretion by phosphatidylinositol 3-kinase in rats. Gastroenterology. 1997;113:954-965.