Targeted disruption of the class B, scavenger receptor CD36 protects against atherosclerotic lesion development in mice

Journal of Clinical Investigation

Volumn 105, Issue 8, 2000, Pages 1049-1056

  Febbraio, Maria ^a,b   Podrez, Eugene A ^c   Smith, Jonathan D ^d   Hajjar, David P ^a,b   Hazen, Stanley L ^c,e   Hoff, Henry F ^c   Sharma, Kavita ^a   Silverstein, Roy L ^a,b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Weill Cornell Medical College of Cornell University   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d ROCKEFELLER UNIVERSITY   (United States)

^e CLEVELAND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD36 ANTIGEN; LOW DENSITY LIPOPROTEIN; SCAVENGER RECEPTOR;

ANIMAL CELL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CELL CULTURE; FOAM CELL; LIPID OXIDATION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL;

EID: 0034101821     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI9259     Document Type: Article

References (57)

1. Ross, R. 1993. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature: 362:801-809.
2. Marx, N., Sukhova, G., Murphy, C., Libby, P., and Plurzky, J. 1998. Macrophages in human arheroma contain PPAR-gamma: differentiationdependent peroxisomnl proliferator-activated receptor gamma (PPAR-gamma) expression and reduction of MMP-9 activity through PPAR-gamma activation in mononuclear phagocytes in vitro. Am. J. Pathol. 153:17-23.
3. Yla-Herttuala, S., et al. 1991. Expression of monocytes chemoattractant protein 1 in macrophage-rich areas of human and rabbit atherosclerotic lesions. Proc. Natl. Acad. Sci. USA. 88:5252-5256.
4. Boring, L., Gosling, J., Cleary, M., and Charo, I.F. 1998. Decreased lesion formation in CCR2 mice reveals a role for chemokines in the initiation of atherosclerosis. Nature. 394:894-897.
5. de Villiers, W.J., et al. 1998. Macrophage phenotype in mice deficient in both macrophage-colony-stimulating factor (op) and apolipoprotein E. Arterioscler.Thromb Vasc. Biol. 18:631-640.
6. Geng, Y.J., and Hansson, G.K. 1992. Interferon-gamma inhibits scavenger receptor expression and foam cell formation in human monocyte-derived macrophages. J. Clin. Invest. 89:1322-1330.
7. Berliner, J.A., et al. 1993. Induction of chemotactic cytokines by minimally oxidized LDL. Adv. Exp. Med. Biol. 351:13-18.
8. Frostegard, J., et al. 1990. Oxidized low density lipoprotein induces differentiation and adhesion of human monocytes and the monocytic cell line U937. Proc. Natl. Acad. Sci. USA. 87:904-908.
9. Ramprasad, M.P., Terpstra, V., Kondratenko, N., Quehenberger, O., and Steinberg, D. 1996. Cell surface expression of mouse macrosialin and human CD68 and their role as macrophage receptors for oxidized low density lipoprotem. Proc. Natl. Acad. Sci. USA. 93:14833-14838.
10. Parthasarathy, S., Printz, D.J., Boyd, D., Joy, L., and Sreinberg, D. 1986. Macrophage oxidation of low density lipoprotein generates a modified form recognized by the scavenger receptor. Arteriosclerosis. 6:505-510.
11. Krieger, M. 1992. Molecular flypaper and atherosclerosis: structure of the macrophage scavenger receptor. Trends Biochem. Sci. 17:141-146.
12. Endemann, G., et al. 1993. CD36 is a receptor for oxidized low density lipoprotein. J. Biol. Chem. 268:11811-11816.
13. Platt, N., da Silva, R.P., and Gordon, S. 1998. Recognizing death: the phagocytosis of apoptotic cells. Trends Cell Biol. 8:365-372.
14. Parthasarathy, S., Steinberg, D., and Witztum, J.L. 1992. The role of oxidized low-density lipoproteins in the pathogenesis of atherosclerosis. Annu. Rev. Med. 43:219-225.
15. Penn, M.S., and Chisolm, G.M. 1994. Oxidized lipoproteins, altered cell function and atherosclerosis. Atherosclerosis. 108(Suppl.):21-29.
16. Steinberg, D. 1997. Low density lipoprorein oxidation and its pathobiological significance. J. Biol. Chem. 272:20963-20966.
17. Yoshida, H., Quehenberger, O., Kondratenko, N., Green, S., and Steinberg, D. 1998. Minimally oxidized low-density lipoprotein increases expression of scavenger receptor A, CD36, and macrosialin in resident mouse peritoneal macrophages. Arterioscler. Thromb. Vasc. Biol. 18:794-802.
18. 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.
19. Han, J., and Nicholson, A.C. 1998. Lipoproteins modulate expression of the macrophage scavenger receptor Am. J. Pathol. 152:1647-1654.
20. Lougheed, M., et al. 1997. 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. 272:12938-12944.
21. Podrez, E.A., et al. 2000 Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species. J. Clin. Invest. 105:1095-1108.
22. Suzuki, H., et al. 1997. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature. 386:292-296.
23. Sakaguchi, H., et al. 1998. Role of macrophage scavenger receptors in diet-induced atherosclerosis in mice. Lab Invest. 78:423-434.
24. de Winther, M.P., et al. 1999. Scavenger receptor deficiency leads to more complex atherosclerotic lesions in APO-E3 Leiden transgenic mice. Atherosclerosis. 144:315-321.
25. Yesner, L.M., Hull, H.Y., Pearce, S.F., and Silverstein, R.L. 1996. Regulation of monocyte CD36 and thrombospondin-1 expression by soluble mediators. Arterioscler. Thromb. Vasc. Biol. 16:1019-1025.
26. Huh, H.V., 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.
27. Wal, A.C., Das, P.K., Tigges, A.J., and Becker, A.F. 1992. Macrophage differentiation in atherosclerosis: an in situ immunohistochemical analysis in humans. Am. J. Pathol. 141:161-168.
28. 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.
29. 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.
30. Nagy, L., Tontonoz, P., Alvarez, J.G., Chen, H., and Evans, R.M. 1998. Oxidized LDL regulates macrophage gene expression through ligand activation of PPAR-gamma. Cell. 93:229-240.
31. Tontonoz, P., Nagy, L., Alvarez, J.G., Thomazy, V.A., and Evans, R.M. 1998. PPAR-gamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell. 93:241-252.
32. Van Nieuwenhoven, F.A., et al. 1995. Putative membrane fatty acid translocate and cytoplasmic fatty acid-binding protein are co-expressed in rat heart and skeletal muscles. Biochem. Biophys. Res. Commun. 207:747-752.
33. Ryeom, S.W., Sparrow, J.R., and Silverstein, R.L. 1996. CD36 participates in the phagocytosis of rod outer segments by retinal pigment epithelium. J. Cell. Sci. 109:387-395.
34. Greenwalt, D.E., Watt, K.W., So, O.Y., and Jiwani, N. 1990. PAS IV, an integral membrane protein of mammary epithelial cells, is related to platelet and endothelial cell CD36 (GP IV). Biochemistry. 29:7054-7059.
35. Abumrad, N.A., el-Maghrabi, M.R., Amri, E.Z., Lopez, E., and Grimaldi, P.A. 1993. Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J. Biol. Chem. 268:17665-17668.
36. 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.
37. Ibrahimi, A., et al. 1999. Muscle-specific over-expression of FAT/CD36 enhances fatty acid oxidation by contracting muscle, reduces plasma triglycerides and fatty acids, and increases plasma glucose and insulin. J. Biol. Chem. 274:26761-26765.
38. Aitman, T.J., et al. 1999. Identification of Cd36 (Fat) as an insulin-resistance gene causing defective fatty acid and glucose metabolism in hypertensive rats. Nat. Genet. 21:76-83.
39. Plump, A.S., Scott, C.J., and Breslow, J.L. 1994. Human apolipoprorein A-1 gene expression increases high density lipoprotein and suppresses atherosclerosis in the apolipoprotein E-deficient mouse. Proc. Natl. Acad.Sci. USA. 91:9607-9611.
40. Markwell, M.A., Haas, S.M., Bieber, L.L., and Tolbert, N.E. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87:206-210.
41. 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.
42. Goldstein, J.L., Ho, Y.K., Basu, S.K., and Brown, M.S. 1979. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc. Natl. Acad. Sci. USA. 76:333-337.
43. Ohkawa, H., Ohishi, N., and Yagi, K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 95:351-358.
44. 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.
45. Rakita, R.M., Michel, B.R., and Rosen, H. 1990. Differential inactivation of Escherichia coli membrane dehydrogenases by a myeloperoxidase-mediated antimicrobial system. Biochemistry. 29:1075-1080.
46. Plump, A.S., et al. 1992. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 71:343-353.
47. Zhang, S.H., Reddick, R.L., Piedrahita, J.A., and Maeda, N. 1992. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 258:468-471.
48. Nakashima, Y., Plump, A.S., Raines, E.W., Breslow, J.L., and Ross, R. 1994. Apo E-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb. 14:133-140.
49. Ottnad, E., et al. 1995. A macrophage receptor for oxidized low density lipoprotein distinct from the receptor for acetyl low density lipoprotein: partial purification and role in recognition of oxidatively damaged cells. Proc. Natl. Acad Sci. USA. 92:1391-1395.
50. Ramprasad, M.P., et al. 1995. The 94-to 97-kDa mouse macrophage membrane protein that recognizes oxidized low density lipoprotein and phosphatidylserine-rich liposomes is identical to macrosialin, the mouse homologue of human CD68. Proc. Natl. Acad. Sci. USA. 92:9580-9584.
51. Palinski, W., et al. 1989. Low density lipoprotein undergoes oxidative modification in vivo. Proc Natl. Acad. Sci. USA. 86:1372-1376.
52. Palinski, W., et al. 1996. Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprorein E-deficient mice. Demonstration of epitopes of oxidized low density lipoprotein in human plasma. J. Clin. Invest. 98:800-814.
53. Yla-Herttuala, S., et al. 1989. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84:1086-1095.
54. 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. Vasc. Biol. 15:269-275.
55. 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.
56. Hazen, S.L., and Heinecke, J.W. 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.
57. Cyrus, T., et al. 1999. Disruption of the 12/15-lipoxygenase gene diminishes atherosclerosis in apo E-deficient mice. J. Clin. Invest. 103:1597-1604.