A CD36-dependent signaling cascade is necessary for macrophage foam cell formation

Cell Metabolism

Volumn 4, Issue 3, 2006, Pages 211-221

  Rahaman, S Ohidar ^a   Lennon, David J ^a,b   Febbraio, Maria ^a   Podrez, Evgeny A ^a   Hazen, Stanley L ^a   Silverstein, Roy L ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

SIGNALING

Indexed keywords

CD36 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE 9; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 2; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHOLIPID; PROTEIN KINASE LYN; PROTEIN TYROSINE KINASE; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR A; STRESS ACTIVATED PROTEIN KINASE 1; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FOAM CELL; HYPERLIPIDEMIA; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; INTIMA; MALE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIGENS, CD36; ANTILIPEMIC AGENTS; ATHEROSCLEROSIS; ENDOTHELIAL CELLS; ENZYME INHIBITORS; FEMALE; FOAM CELLS; HYPERLIPIDEMIAS; HYPOLIPIDEMIC AGENTS; LIPOPROTEINS, LDL; MACROPHAGES; MALE; MAP KINASE KINASE KINASE 2; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 9; OXIDATION-REDUCTION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TOLL-LIKE RECEPTOR 2;

EID: 33747859314     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2006.06.007     Document Type: Article

References (47)

1. Bamberger M.E., Harris M.E., McDonald D.R., Husemann J., and Landreth G.E. A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J. Neurosci. 23 (2003) 2665-2674
2. Bull H.A., Brickell P.M., and Dowd P.M. Src-related protein tyrosine kinases are physically associated with the surface antigen CD36 in human dermal microvascular endothelial cells. FEBS Lett. 351 (1994) 41-44
3. Chinetti G., Lestavel S., Bocher V., Remaley A.T., Neve B., Torra I.P., Teissier E., Minnich A., Jaye M., Duverger N., et al. PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat. Med. 7 (2001) 53-58
4. Cho S., Park E.M., Febbraio M., Anrather J., Park L., Racchumi G., Silverstein R.L., and Iadecola C. The class B scavenger receptor CD36 mediates free radical production and tissue injury in cerebral ischemia. J. Neurosci. 25 (2005) 2504-2512
5. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 103 (2000) 239-252
6. El Khoury J.B., Moore K.J., Means T.K., Leung J., Terada K., Toft M., Freeman M.W., and Luster A.D. CD36 mediates the innate host response to beta-amyloid. J. Exp. Med. 197 (2003) 1657-1666
7. Febbraio M., Podrez E.A., Smith J.D., Hajjar D.P., Hazen S.L., Hoff H.F., Sharma K., and Silverstein R.L. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J. Clin. Invest. 105 (2000) 1049-1056
8. Febbraio M., Hajjar D.P., and Silverstein R.L. CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J. Clin. Invest. 108 (2001) 785-791
9. Finnemann S.C., and Silverstein R.L. Differential roles of CD36 and alphavbeta5 integrin in photoreceptor phagocytosis by the retinal pigment epithelium. J. Exp. Med. 194 (2001) 1289-1298
10. Fadok V.A., Warner M.L., Bratton D.L., and Henson P.M. CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phosphatidylserine receptor or the vitronectin receptor (alpha v beta 3). J. Immunol. 161 (1998) 6250-6257
11. Febbraio M., Abumrad N.A., Hajjar D.P., Sharma K., Cheng W., Pearce S.F., and Silverstein R.L. A null mutation in murine CD36 reveals an important role in fatty acid and lipoprotein metabolism. J. Biol. Chem. 274 (1999) 19055-19062
12. Glass C.K., and Witztum J.L. Atherosclerosis. The road ahead. Cell 104 (2001) 503-516
13. Hoebe K., Georgel P., Rutschmann S., Du X., Mudd S., Crozat K., Sovath S., Shamel L., Hartung T., Zahringer U., and Beutler B. CD36 is a sensor of diacylglycerides. Nature 433 (2005) 523-527
14. Huang M.M., Bolen J.B., Barnwell J.W., Shattil S.J., and Brugge J.S. Membrane glycoprotein IV (CD36) is physically associated with the Fyn, Lyn, and Yes protein-tyrosine kinases in human platelets. Proc. Natl. Acad. Sci. USA 88 (1991) 7844-7848
15. Jimenez B., Volpert O.V., Crawford S.E., Febbraio M., Silverstein R.L., and Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat. Med. 6 (2000) 41-48
16. Janabi M., Yamashita S., Hirano K., Sakai N., Hiraoka H., Matsumoto K., Zhang Z., Nozaki S., and Matsuzawa Y. Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. Arterioscler. Thromb. Vasc. Biol. 20 (2000) 1953-1960
17. Kunjathoor V.V., Febbraio M., Podrez E.A., Moore K.J., Andersson L., Koehn S., Rhee J.S., Silverstein R., Hoff H.F., and Freeman M.W. Scavenger receptors Class A-I/II and CD36 are the principal receptors responsible for the uptake of modified low density lipoprotein leading to lipid loading in macrophages. J. Biol. Chem. 277 (2002) 49982-49988
18. Lusis A.J. Atherosclerosis. Nature 407 (2000) 233-241
19. Libby P. Inflamation in atherosclerosis. Nature 420 (2002) 868-874
20. Li A.C., Binder C.J., Gutierrez A., Brown K.K., Plotkin C.R., Pattison J.W., Valledor A.F., Davis R.A., Willson T.M., Witztum J.L., et al. Differential inhibition of macrophage foam-cell formation and atherosclerosis in mice by PPARalpha, beta/delta, and gamma. J. Clin. Invest. 114 (2004) 1564-1576
21. Moore K.J., El Khoury J., Medeiros L.A., Terada K., Geula C., Luster A.D., and Freeman M.W. A CD36-initiated signaling cascade mediates inflammatory effects of beta-amyloid. J. Biol. Chem. 277 (2002) 47373-47379
22. Medeiros L.A., Khan T., El Khoury J.B., Pham C.L., Hatters D.M., Howlett G.J., Lopez R., O'Brien K.D., and Moore K.J. Fibrillar amyloid protein present in atheroma activates CD36 signal transduction. J. Biol. Chem. 279 (2004) 10643-10648
23. Moore K.J., Rosen E.D., Fitzgerald M.L., Randow F., Andersson L.P., Altshule R.D., Milstone D.S., Mortensen R.M., Spiegelman B.M., and Freeman M.W. The role of PPAR-gamma in macrophage differentiation and cholesterol uptake. Nat. Med. 7 (2001) 41-47
24. Miao W.M., Vasile E., Lane W.S., and Lawler J. CD36 associates with CD9 and integrins on human blood platelets. Blood 97 (2001) 1689-1696
25. Miki S., Horikawa K., Nishizumi H., Suemura M., Sato B., Yamamoto M., Takatsu K., Yamamoto T., and Miki Y. Reduction of atherosclerosis despite hypercholesterolemia in lyn-deficient mice fed a high-fat diet. Genes Cells 6 (2001) 37-42
26. Metzler B., Hu Y., Dietrich H., and Xu Q. Increased expression and activation of stress-activated protein kinases/c-Jun NH(2)-terminal protein kinases in atherosclerotic lesions coincide with p53. Am. J. Pathol. 156 (2000) 1875-1886
27. Nagy L., Tontonoz P., Alvarez J.G., Chen H., and Evans R.M. OxLDL regulates macrophage gene expression through ligand activation of PPARγ. Cell 93 (1998) 229-240
28. Nicholls S.J., and Hazen S.L. Myeloperoxidase and Cardiovascular Disease. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1102-1111
29. Nakata A., Nakagawa Y., Nishida M., Nozaki S., Miyagawa J., Nakagawa T., Tamura R., Matsumoto K., Kameda-Takemura K., Yamashita S., and Matsuzawa Y. 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 (1999) 1333-1339
30. Pelkmans L., Fava E., Grabner H., Hannus M., Habermann B., Krausz E., and Zerial M. Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 436 (2005) 78-86
31. Platt N., and Gordon S. Is the class A macrophage scavenger receptor (SR-A) multifunctional?-The mouse's tale. J. Clin. Invest. 108 (2001) 649-654
32. Podrez E.A., Febbraio M., Sheibani N., Schmitt D., Silverstein R.L., Hajjar D.P., Cohen P.A., Frazier W.A., Hoff H.F., and Hazen S.L. Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species. J. Clin. Invest. 105 (2000) 1095-1108
33. Podrez E.A., Abu-Soud H.M., and Hazen S.L. Myeloperoxidase-generated oxidants and atherosclerosis. Free Radic. Biol. Med. 28 (2000) 1717-1725
34. Podrez E.A., Poliakov E., Shen Z., Zhang R., Deng Y., Sun M., Finton P.J., Shan L., Febbraio M., Hajjar D.P., et al. A novel family of atherogenic oxidized phospholipids promotes macrophage foam cell formation via the scavenger receptor CD36 and is enriched in atherosclerotic lesions. J. Biol. Chem. 277 (2002) 38517-38523
35. Palinski W., Rosenfeld M.E., Yla-Herttuala S., Gurtner G.C., Socher S.S., Butler S.W., Parthasarathy S., Carew T.E., Steinberg D., and Witztum J.L. LDL undergoes oxidative modification in vivo. Proc. Natl. Acad. Sci. USA 86 (1989) 1372-1376
36. Ricci R., Sumara G., Sumara I., Rozenberg I., Kurrer M., Akhmedov A., Hersberger M., Eriksson U., Eberli F.R., Becher B., et al. Requirement of JNK2 for scavenger receptor A-mediated foam cell. Science 306 (2004) 1558-1561
37. Silverstein R.L., and Febbraio M. CD36 and atherosclerosis. Curr. Opin. Lipidol. 11 (2000) 483-491
38. Suzuki H., Kurihara Y., Takeya M., Kamada N., Kataoka M., Jishage K., Ueda O., Sakaguchi H., Higashi T., Suzuki T., et al. A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 386 (1997) 292-296
39. Silverstein R.L., and Nachman R.L. Thrombospondin binds to monocytes-macrophages and mediates platelet-monocyte adhesion. J. Clin. Invest. 79 (1987) 867-874
40. Shattil S.J., and Brugge J.S. Protein tyrosine phosphorylation and the adhesive functions of platelets. Curr. Opin. Cell Biol. 3 (1991) 869-879
41. Shaw A.S., Chalupny J., Whitney J.A., Hammond C., Amrein K.E., Kavathas P., Sefton B.M., and Rose J.K. Short related sequences in the cytoplasmic domains of CD4 and CD8 mediate binding to the amino-terminal domain of the p56lck tyrosine protein kinase. Mol. Cell. Biol. 10 (1990) 1853-1862
42. Stuart L.M., Deng J., Silver J.M., Takahashi K., Tseng A.A., Hennessy E.J., Ezekowitz R.A., and Moore K.J. Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J. Cell Biol. 170 (2005) 477-485
43. Takeuchi O., Hoshino K., Kawai T., Sanjo H., Takada H., Ogawa T., Takeda K., and Akira S. Differential roles of TLR2 and TLR4 in recognition of Gramnegative and Gram-positive bacterial cell wall components. Immunity 11 (1999) 443-451
44. Turner J.M., Brodsky M.H., Irving B.A., Levin S.D., Perlmutter R.M., and Littman D.R. Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs. Cell 60 (1990) 755-765
45. Tontonoz P., Nagy L., Alvarez J.G., Thomazy V.A., and Evans R.M. PPARγ pro-motes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell 93 (1998) 241-252
46. Thorne R.F., Marshall J.F., Shafren D.R., Gibson P.G., Hart I.R., and Burns G.F. The integrins alpha3beta1 and alpha6beta1 physically and functionally associate with CD36 in human melanoma cells. Requirement for the extracellular domain of CD36. J. Biol. Chem. 275 (2000) 35264-35275
47. Yla-Herttuala S., Palinski W., Rosenfeld M.E., Parthasarathy S., Carew T.E., Butler S., Witztum J.L., and Steinberg D. Evidence for the presence of oxidatively modified low density lipoprotein in atherosclerotic lesions of rabbit and man. J. Clin. Invest. 84 (1989) 1086-1095