Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species

Journal of Clinical Investigation

Volumn 105, Issue 8, 2000, Pages 1095-1108

  Podrez, Eugene A ^a   Febbraio, Maria ^b   Sheibani, Nader ^c   Schmitt, David ^a   Silverstein, Roy L ^b   Hajjar, David P ^b   Cohen, Peter A ^a   Frazier, William A ^c   Hoff, Henry F ^a,d   Hazen, Stanley L ^a,d  

^a LERNER RESEARCH INSTITUTE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; LOW DENSITY LIPOPROTEIN; MYELOPEROXIDASE; REACTIVE OXYGEN METABOLITE; SCAVENGER RECEPTOR;

ANIMAL CELL; ARTICLE; ATHEROSCLEROSIS; CELL CULTURE; CELL LEVEL; FOAM CELL; HUMAN; HUMAN CELL; LIPID PEROXIDATION; LIPID TRANSPORT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL;

EID: 0034051080     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI8574     Document Type: Article

References (78)

1. Brown, M., and Goldstein, J. 1986. A receptor mediated pathway for cholesterol homeostasis. Science, 232:34-47.
2. Sreinbrecher, U.P., Zhang, H.F., and Lougheed, M. 1990. Role of the oxidatively modified LDL in atherosclerosis. Free Radic. Biol. Med. 9:155-168.
3. Witztum, J.L., and Steinberg, D. 1991. Rote of oxidized low density lipoprotein in atherogenesis. J. Clin. Invest. 88:1785-1792.
4. Berliner, J.A., et al. 1995. Atherosclerosis: basic mechanisms. Oxidation, inflammation, and genetics. Circulation, 91:2488-2496.
5. Steinberg, D. 1997. Lewis A. Conner Memorial Lecture. Oxidative modification of LDL and atherogenesis. Circulation. 95:1062-1071.
6. Chisolm, G.M., III, Hazen, S.L., Fox, P.L., and Cathcart, M.K. 1999. The oxidation of lipoproteins by monocytes-macrophages. Biochemical and biological mechanisms. J. Biol. Chem. 274:25959-25962.
7. Steinbrecher, U.P., Witztun, J.L., Parthasarathy, S., and Steinberg, D. 1987. Decrease in reactive amino groups during oxidation or endothelial cell modification of LDL. Correlation with changes in receptor-mediated catabolism. Arteriosclerosis. 7:135-143.
8. Steinbrecher, U.P. 1999. Receptors for oxidized low density lipoprotein. Biochim. Biophys. Acta. 1436:279-298.
9. Holvoet, P., and Collen, D. 1994. Oxidized lipoproteins in atherosclerosis and thrombosis. FASEB J. 8:1279-1284.
10. Krieger, M., and Herz, J. 1994. Structures and functions of multiligand lipoprotein receptors: Macrophage scavenger receptors and LDL receptor-related protein (LRP). Annu. Rev. Biochem. 63:601-637.
11. Dabbagh, A.J., and Frei, B. 1995. Human suction blister interstitial fluid prevents metal ion-dependent oxidation of low density lipoprotein by macrophages and in cell-free systems. J. Clin. Invest. 96:1958-1966.
12. Thomas, C.E. 1985. The influence of medium components in copper-dependent oxidation of low density lipoprotein making it cytotoxic. J. Leukoc. Biol. 38:341-350.
13. Leeuwenburgh, C., et al. 1997. Mass spectrometric quantification of markers for protein oxidation by tyrosyl radical, copper, and hydroxyl radical in low density lipoprotein isolated from human atherosclerotic plaques. J. Biol. Chem. 272:3520-3526.
14. Fu, S., Davies, M.J., Stocker, R., and Dean, R.T. 1998. Evidence for roles of radicals in protein oxidation in advanced human atherosclerotic plaque. Biochem. J. 333:519-525.
15. Podrez, E.A. Schmitt, D., Hoff, H.F., and Hazen, S.L. 1999. Myeloperoxidase-generated reactive nitrogen species convert LDL into an atherogenic form in vitro. J. Clin. Invest. 103:1547-1560.
16. Klebanoff, S.J., and Clark, R.A. 1978. The neutrophil: function and clinical disorders. In the neutrophil: function and clinical disorders. Elsevier/North Holland Biomedical Press. Amsterdam, The Netherlands. 447-451.
17. Agner, K. 1972. Structure and function of oxidation-reduction enzyme. In Structure and function of oxidation-reduction enzymes. A. Akeson and A. Ehrenberg, editors, Pergamon Press Inc. Tarrytown, NY. 329-335.
18. Krinsky, N.I. 1974. Singlet excited oxygen as a mediator of the antibacterial action of leukocytes. Science. 186:363-365.
19. Harrison, J.E., and Schultz, J. 1976. Studies on the chlorinating activity of myeloperoxidase. J. Biol. Chem. 251:1371-1374.
20. Hazen, S.L., Hsu, F.F., Mueller, D.M., Crowley, J.R., and Heinecke, J.W. 1996. Human neutrophils employ chlorine gas as an oxidant during phagocytosis. J. Clin. Invest. 98:1283-1289.
21. van der Vleit, A., Eiserich, J.P., Halliwell, B., and Cross, C.E. 1997. Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity. J. Biol. Chem. 272:7617-7625.
22. Eiserich, J.P., et al. 1998. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature. 391:393-397.
23. Daugherty, A., Dunn, J.L., Rateri, D.L., and Heinecke, J.W. 1994. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J. Clin. Invest. 94:437-444.
24. Hazell, L.J., et al. 1996. Presence of hypochlorite-modified proteins in human atherosclerotic lesions. J. Clin. Invest. 97:1535-1544.
25. Leeuwenburgh, C., et al. 1997. Reactive nitrogen intermediates promote low density lipoprotein oxidation in human atherosclerotic intima. J. Biol. Chem. 272:1433-1436.
26. Hazen, S.L., and J.W. Heinecke. 1997. 3-chlorotyrosine, a specific marker of myeloperoxidase-catalyzed oxidation, is markedly elevated in low density lipoprotein isolated from human atherosclerotic intima. J. Clin. Invest. 99:2075-2081.
27. Beckman, J.S., et al. 1994. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol. Chem. Hoppe Seyler. 375:81-88.
28. Hazen, S.L., et al. 1999. Formation of nitric oxide-derived oxidants by myeloperoxidase in monocytes: pathways for monocyte-mediated protein nitration and lipid peroxidation in vivo. Circ. Res. 85:950-958.
29. Ylä-Herttuala, S. 1991. Macrophages and oxidized low density lipoproteins in the pathogenesis of atherosclerosis. Ann Med. 23:561-567.
30. Suarna, C., Dean, R.T., May, J., and Stocker, R. 1995. Human atherosclerotic plaque contains both oxidized liptds and relatively large amounts of alpha-tocopherol and ascorbate. Artherioscler. Thromb. Vasc. Biol. 15:1616-1624.
31. Suzuki, H., et al. 1997. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature. 386:292-296.
32. Sakaguchi, H., et al. 1998. Role of macrophage scavenger receptors in diet-induced atherosclerosis in mice. Lab. Invest. 78:423-434.
33. Endemann, G., et al. 1993. CD36 is a receptor for oxidized low density lipoprotein. J. Biol. Chem. 268:11811-11816.
34. Nicholson, A.C., Frieda, S., Pearce, A., and Silverstein, R.L. 1995. Oxidized LDL binds to CD36 on human monocyte-derived macrophages and transfected cell lines: evidence implicating the lipid moiety of the lipoprotein as the binding site. Arterioscler. Thromb. 15:269-275.
35. Rigotti, A. Acton, S.L., and Krieger, M. 1995. The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J. Biol. Chem. 270:16221-16224.
36. Tait, J.F., and Smith, C. 1999. Phosphatidylserine receptors: role of CD36 in binding of anionic phospholipid vesicles to monocytic cells. J. Biol. Chem. 274:3048-3054.
37. Ryeom, S.W., Silverstein, R.L., Scotto, A., and Sparrow, J.R. 1996. Binding of anionic phospholipids to retinal pigment epithelium may be mediated by rhe scavenger receptor CD36. J. Biol. Chem. 271:20536-20539.
38. Ren, Y., Silverstein, R.L., Allen, J., and Savill, J. 1995. CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J. Exp. Med. 181:1857-1862.
39. Tandon, N.N., Kralisz, U., and Jamieson, G.A. 1989. Identification of glycoprotein IV (CD36) as a primary receptor for platelet-collagen adhesion. J. Biol. Chem. 264:7576-7583.
40. Silverstein, R.L., Asch, A.S., and Nachman, R.L. 1989. Glycoprotein IV mediates thrombospondin-dependent platelet-monocyte and platelet-U937 cell adhesion. J. Clin. Invest. 84:546-552.
41. Dawson, D.W., et al. 1997. CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell. Biol. 138:707-717.
42. Febbraio, M., et al. 1999. A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J. Biol. Chem. 274:19055-19062.
43. Savill, J., Hogg, N., Ren, Y., and Haslett, C. 1992. Thrombospondin cooperates with CD36 and rhe vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. invest. 90:1513-1522.
44. Nozaki, S., et al. 1995. Reduced uptake of oxidized low density lipoproteins in monocyte-derived macrophages from CD36-deficient subjects. J. Clin. Invest. 96:1859-1865.
45. Tontonoz, P., Nagy, L., Alvarez, J.G., Thomazy, V.A., and Evans, R.M. 1998. PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell. 93:241-252.
46. Nagy, L., Tontonoz, P., Alvarez, J.G., Chen, H., and Evans, R.M. 1998. Oxidized LDL regulates macrophage gene expression through ligand activation of PPARgamma. Cell. 93:229 240.
47. Han, J., Hajjar, D.P., Febbraio, M., and Nicholson, A.C. 1997. Native and modified low density lipoproteins increase the functional expression of the macrophage class B scavenger receptor, CD36. J. Biol. Chem. 272:21654-21659.
48. Han, J., Hajjar, D.P., Tauras, J.M., and Nicholson, A.C. 1999. Cellular cholesterol regulates expression of the macrophage type B scavenger receptor, CD36. J. Lipid. Res. 40:830-838.
49. Huh, H.Y., Pearce, S.F., Yesner, L.M., Schindler, J.L., and Silverstein, R.L. 1996. Regulated expression of CD36 during monocyte-to-macrophage differentiation: potential role of CD36 in foam cell formation. Blood. 87:2020-2028.
50. Nakata, A., et al. 1999. CD36, a novel receptor for oxidized low-density lipoproteins, is highly expressed on lipid-laden macrophages in human atherosclerotic aorta. Arterioscler. Thromb. Vasc. Biol. 19:1333-1339.
51. Hoppe, G., O'Neil, J., and Hoff, H.F. 1994. Inactivation of lysosomal proteases by oxidized low density lipoprotein is partially responsible for its poor degradation by mouse peritoneal macrophages. J. Clin. Invest. 94:1506-1512.
52. Czerniecki, B.J., et al. 1997. Calcium ionophore-treated peripheral blood monocytes and dendritic cells rapidly display characteristics of activated dendritic cells. J. Immunol. 159:3823-3837.
53. Crowley, J.R., Yarasheski, K., Leeuwenburgh, C., Turk, J., and Heinecke, J.W. 1998. Isotope dilution mass spectrometric quantification of 3-nitrotyrosine in proteins and tissues is facilitated by reduction to 3-aminotyrosine. Anal. Biochem. 259:127-135.
54. Morel, D.W., Hessler, J. R., and Chisolm, G.M. 1983. Low density lipoprotein cytotoxiciry induced by free radical peroxidation of lipid. J. Lipid Res. 24:1070-1076.
55. Ashkenas J., et al. 1993. Structures and high and low affinity ligand binding properties of murine type 1 and type II macrophage scavenger receptors. J. Lipid Res. 34:983-1000.
56. Sheibani, N., and Frazier, W.A. 1995. Thrombospondin 1 expression in transformed endothelial cells restores a normal phenotype and suppresses their tumorigenesis. Proc. Natl. Acad. Sci. USA. 92:6788-6792.
57. Terpstra, V., Bird, D.A., and Steinberg, D. 1998. Evidence that the lipid moiety of oxidized low density lipoprotem plays a role in its interaction with macrophage receptors. Proc. Natl. Acad. Sci. USA. 95:18006-18011.
58. Bligh, E.J., and Dyer, W.J. 1959, A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
59. Parthasarathy, S., Fong, L.G., Orero, D., and Steinberg, D. 1987. Recognition of solubilized apoproteins form delipidated, oxidixed low density lipoprorein (LDL) by the acetyl-LDL receptor. Proc. Natl. Acad. Sci. USA. 84:537-540.
60. Eiserich, J.P., Cross, C.E., Jones, A.D., Halliwell, B., and van der Vliet, A. 1996. Formation of nitrating and chlorinating species by reaction of nitrite with hypochlorous acid. A novel mechanism for nitric oxide-mediated protein modification. J. Biol. Chem. 271:19199-19208.
61. Hazell, L.J., van den Berg, J.J. and Stocker, R. 1994. Oxidation of low-density lipoprotein by hypochlorite causes aggregation that is mediated by modification of lysine residues rather than lipid oxidation. Biochem. J. 302:297-304.
62. Hazell, L.J., Davies, M.J., and Stocker, R. 1999. Secondary radicals derived from chloramines of apolipoprotein B-100 contribute to HOCl-induced lipid peroxidation of low-density lipoproteins. Biochem. J. 339:489-495.
63. Hazen, S.L., Hsu, F.F. Gaut, J.P., Crowley, J.R., and Heinecke, J.W. 1999. Modification of proteins and lipids by myeloperoxidase. Methods Enzymol. 300:88-105.
64. Puente Navazo, M.D., Daviet, L., Ninio, E., and McGregor, J.L. 1996. Identification on human CD36 of a domain (155-183) implicated in binding oxidized low-density lipoproteins (Ox-LDL). Arterioscler. Thromb. Vasc. Biol. 16:1033-1039.
65. Haberland, M.E., Olch, C.L., and Folgelman, A.M. 1984. Role of lysines in mediating interaction of modified low density lipoproteins with the scavenger receptor of human monocyte macrophages. J. Biol. Chem. 259:11305-11311.
66. Traber, M.G., Defendi, V., and Kayden, H.J. 1981. Receptor activities for low-density lipoprotein and acetylated low-density lipoprorein in a mouse macrophage cell line (IC21) and in human monocyte-derived macrophages. J. Exp. Med. 154:1852-1867.
67. Bird, D.A., et al. 1999. Receptors for oxidixed low-density lipoprorein on elicited mouse peritoneal macrophages can recognize both the modified lipid moieties and the modified protein moieties: Implications with respect to macrophage recognition of apoptotic cells. Proc. Natl. Acad. Sci. USA. 96:6347-6352.
68. Beckman, J.S., Chen, J., Ischiropoulos, H., and Crow, J.P. 1994. Oxidative chemistry of peroxinitrite. Methods Enzymol. 233:229-240.
69. Niu, X., Zammit, V., Upston, J.M., Dean, R.T., and Stocker, R. 1999. Coexistence of oxidixed lipids and alpha-tocopherol in all lipoprotein density fractions isolated from advanced human atherosclerotic plaques. Arterioscler. Thromb. Vasc. Biol. 19:1708-1718.
70. Aasa, R., Malmstrom, B.G., Saltman, P., and Vangard, T. 1963. The specific binding of Fe(III) and Cu(II) to transferrin and conalbumin. Biochem. Biophys. Acta. 75:203-222.
71. Schmitt, D., et al. 1999. Leukocytes utilize myeloperoxidase-generated nitrating intermediates as physiological catalysts for the generation of biologically active oxidixed lipids and sterols in serum. Biochemistry. 38:16904-16915.
72. Pathobiological Determinants of Atherosclerosis in Youth (PDAY) Research Group. 1993. Natural history of aortic and coronary atherosclerotic lesions in youth: findings from the PDAY study Arterioscler. Thromb. 13:1291-1298.
73. Napoli, C., et al. 1997. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia. Intimal accumulation of low density lipoprorein and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J. Clin. Invest. 100:2680-2690.
74. Ross, R. 1999. Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340:115-126.
75. Iwata, M., Colby, T.V., and Kitaichi, M. 1994. Diffuse panbronchiolitis: diagnosis and distinction from various pulmonary diseases with centrilobular interstitial foam cell accumulations. Hum. Pathol. 25:357-363.
76. Cozzutto, C., and Carbone, A. 1988. The xanthogranulomatous process. Xanthogranulomatous inflammation. Pathol. Res. Pract. 183:395-402.
77. Nakashiro, H., et al. 1995. Xanthogranulomatous cholecystis. Cell composition and a possible pathogenetic role of cell-mediated immunity. Pathol. Res. Pract. 191:1078-1086.
78. Furue, M., 1995. Colocalization of scavenger receptor in CD68 positive foam cells in verruciform xanthoma. J. Dermatol. Sci. 10:213-219.