CD36 binds oxidized low density lipoprotein (LDL) in a mechanism dependent upon fatty acid binding

Journal of Biological Chemistry

Volumn 290, Issue 8, 2015, Pages 4590-4603

  Jay, Anthony G ^a   Chen, Alexander N ^a   Paz, Miguel A ^a   Hung, Justin P ^a   Hamilton, James A ^a  

^a BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BODY FLUIDS; CELL MEMBRANES; DISSOCIATION; LIPOPROTEINS; OXIDATION; PLASMONS; SURFACE PLASMON RESONANCE;

ASSOCIATION AND DISSOCIATION KINETICS; BIOPHYSICAL METHODS; CONFOCAL MICROSCOPY IMAGING; DOCOSAHEXAENOIC ACID; FUNCTIONAL PROPERTIES; OXIDIZED LOW-DENSITY LIPOPROTEINS; OXIDIZED LOW-DENSITY LIPOPROTEINS (OXLDL); PROTEIN CONFORMATION;

FATTY ACIDS;

ALBUMIN; CD36 ANTIGEN; DOCOSAHEXAENOIC ACID; ELAIDIC ACID; FATTY ACID; LINOLEIC ACID; OLEIC ACID; OXIDIZED LOW DENSITY LIPOPROTEIN; PALMITIC ACID; LOW DENSITY LIPOPROTEIN; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL ASSAY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISULFIDE BOND; EMBRYO; FATTY ACID ANALYSIS; FLUORESCENCE ANALYSIS; HUMAN; HUMAN CELL; LIGAND BINDING; LIPID DIET; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LIPID INTERACTION; SURFACE PLASMON RESONANCE; BLOOD; CELL MEMBRANE; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ANTIGENS, CD36; CELL MEMBRANE; DIABETES MELLITUS, TYPE 2; FATTY ACIDS; HEK293 CELLS; HELA CELLS; HUMANS; LIPOPROTEINS, LDL; OBESITY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SURFACE PLASMON RESONANCE;

EID: 84928888310     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.627026     Document Type: Article

References (70)

1. Moore, K. J., and Freeman, M. W. (2006) Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler. Thromb. Vasc. Biol. 26, 1702-1711
2. Plüddemann, A., Neyen, C., and Gordon, S. (2007) Macrophage scavenger receptors and host-derived ligands. Methods 43, 207-217
3. Murphy, J. E., Tedbury, P. R., Homer-Vanniasinkam, S., Walker, J. H., and Ponnambalam, S. (2005) Biochemistry and cell biology of mammalian scavenger receptors. Atherosclerosis 182, 1-15
4. Ramos-Arellano, L. E., Muñoz-Valle, J. F., De la Cruz-Mosso, U., Salgado-Bernabé, A. B., Castro-Alarcón, N., and Parra-Rojas, I. (2014) Circulating CD36 and oxLDL levels are associated with cardiovascular risk factors in young subjects. BMC Cardiovasc. Disord. 14, 54
5. Dushkin, M. I. (2012) Macrophage/foam cell is an attribute of inflammation: mechanisms of formation and functional role. Biochemistry 77, 327-338
6. Avraham-Davidi, I., Grunspan, M., and Yaniv, K. (2013) Lipid signaling in the endothelium. Exp. Cell Res. 319, 1298-1305
7. Silverstein, R. L., Li, W., Park, Y. M., and Rahaman, S. O. (2010) Mechanisms of cell signaling by the scavenger receptor CD36: implications in atherosclerosis and thrombosis. Trans. Am. Clin. Climatol Assoc. 121, 206-220
8. Maiolino, G., Rossitto, G., Caielli, P., Bisogni, V., Rossi, G. P., and Calò, L. A. (2013) The role of oxidized low-density lipoproteins in atherosclerosis: the myths and the facts. Mediators Inflamm. 2013, 714653
9. de Villiers, W. J., Cai, L., Webb, N. R., de Beer, M. C., van der Westhuyzen, D. R., and de Beer, F. C. (2001) CD36 does not play a direct role in HDL or LDL metabolism. J. Lipid Res. 42, 1231-1238
10. Greaves, D. R., and Gordon, S. (2009) The macrophage scavenger receptor at 30 years of age: current knowledge and future challenges. J. Lipid Res. 50, (suppl.) S282-S286
11. Kashiwagi, H., Tomiyama, Y., Honda, S., Kosugi, S., Shiraga, M., Nagao, N., Sekiguchi, S., Kanayama, Y., Kurata, Y., and Matsuzawa, Y. (1995) Molecular basis of CD36 deficiency. Evidence that a 478C→T substitution (proline903serine) in CD36 cDNA accounts for CD36 deficiency. J. Clin. Invest. 95, 1040-1046
12. Nozaki, S., Kashiwagi, H., Yamashita, S., Nakagawa, T., Kostner, B., Tomiyama, Y., Nakata, A., Ishigami, M., Miyagawa, J., and Kameda-Takemura, K. (1995) Reduced uptake of oxidized low density lipoproteins in monocyte-derived macrophages from CD36-deficient subjects. J. Clin. Invest. 96, 1859-1865
13. 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
14. Kar, N. S., Ashraf, M. Z., Valiyaveettil, M., and Podrez, E. A. (2008) Mapping and characterization of the binding site for specific oxidized phospholipids and oxidized low density lipoprotein of scavenger receptor CD36. J. Biol. Chem. 283, 8765-8771
15. Neculai, D., Schwake, M., Ravichandran, M., Zunke, F., Collins, R. F., Peters, J., Neculai, M., Plumb, J., Loppnau, P., Pizarro, J. C., Seitova, A., Trimble, W. S., Saftig, P., Grinstein, S., and Dhe-Paganon, S. (2013) Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36. Nature 504, 172-176
16. Martínez, V. G., Moestrup, S. K., Holmskov, U., Mollenhauer, J., and Lozano, F. (2011) The conserved scavenger receptor cysteine-rich superfamily in therapy and diagnosis. Pharmacol. Rev. 63, 967-1000
17. Rasmussen, J. T., Berglund, L., Rasmussen, M. S., and Petersen, T. E. (1998) Assignment of disulfide bridges in bovine CD36. Eur. J. Biochem. 257, 488-494
18. Gruarin, P., Primo, L., Ferrandi, C., Bussolino, F., Tandon, N. N., Arese, P., Ulliers, D., and Alessio, M. (2001) Cytoadherence of Plasmodium falciparum-infected erythrocytes is mediated by a redox-dependent conformational fraction of CD36. J. Immunol. 167, 6510-6517
19. Baillie, A. G., Coburn, C. T., and Abumrad, N. A. (1996) Reversible binding of long-chain fatty acids to purified FAT, the adipose CD36 homolog. J. Membr. Biol. 153, 75-81
20. Su, X., and Abumrad, N. A. (2009) Cellular fatty acid uptake: a pathway under construction. Trends Endocrinol. Metab. 20, 72-77
21. Xu, S., Jay, A., Brunaldi, K., Huang, N., and Hamilton, J. A. (2013) CD36 enhances fatty acid uptake by increasing the rate of intracellular esterification but not transport across the plasma membrane. Biochemistry 52, 7254-7261
22. Krammer, J., Digel, M., Ehehalt, F., Stremmel, W., Füllekrug, J., and Ehehalt, R. (2011) Overexpression of CD36 and acyl-CoA synthetases FATP2, FATP4 and ACSL1 increases fatty acid uptake in human hepatoma cells. Int. J. Med. Sci. 8, 599-614
23. Harmon, C. M., Luce, P., Beth, A. H., and Abumrad, N. A. (1991) Labeling of adipocyte membranes by sulfo-N-succinimidyl derivatives of longchain fatty acids: inhibition of fatty acid transport. J. Membr. Biol. 121, 261-268
24. Harmon, C. M., and Abumrad, N. A. (1993) Binding of sulfosuccinimidyl fatty acids to adipocyte membrane proteins: isolation and amino-terminal sequence of an 88-kD protein implicated in transport of long-chain fatty acids. J. Membr. Biol. 133, 43-49
25. Spector, A. A. (1975) Fatty acid binding to plasma albumin. J. Lipid Res. 16, 165-179
26. Kuda, O., Pietka, T. A., Demianova, Z., Kudova, E., Cvacka, J., Kopecky, J., and Abumrad, N. A. (2013) Sulfo-N-succinimidyl oleate (SSO) inhibits fatty acid uptake and signaling for intracellular calcium via binding CD36 lysine 164: SSO also inhibits oxidized low density lipoprotein uptake by macrophages. J. Biol. Chem. 288, 15547-15555
27. Takai, M., Kozai, Y., Tsuzuki, S., Matsuno, Y., Fujioka, M., Kamei, K., Inagaki, H., Eguchi, A., Matsumura, S., Inoue, K., and Fushiki, T. (2014) Unsaturated long-chain fatty acids inhibit the binding of oxidized lowdensity lipoproteins to a model CD36. Biosci. Biotechnol. Biochem. 78, 238-244
28. Kozai, Y., Tsuzuki, S., Takai, M., Eguchi, A., Matsumura, S., Inoue, K., and Fushiki, T. (2014) Further validation of unsaturated long-chain fatty acids as inhibitors for oxidized low-density lipoprotein binding to CD36 via assays with synthetic CD36 peptide-cross-linked plates. Biosci. Biotechnol. Biochem. 78, 839-842
29. Folcik, V. A., and Cathcart, M. K. (1994) Predominance of esterified hydroperoxy-linoleic acid in human monocyte-oxidized LDL. J. Lipid Res. 35, 1570-1582
30. Yaney, G. C., Civelek, V. N., Richard, A. M., Dillon, J. S., Deeney, J. T., Hamilton, J. A., Korchak, H. M., Tornheim, K., Corkey, B. E., and Boyd, A. E., 3rd. (2001) Glucagon-like peptide 1 stimulates lipolysis in clonal pancreatic beta-cells (HIT). Diabetes 50, 56-62
31. Byun, J., Verardo, M. R., Sumengen, B., Lewis, G. P., Manjunath, B. S., and Fisher, S. K. (2006) Automated tool for the detection of cell nuclei in digital microscopic images: application to retinal images. Mol. Vis. 12, 949-960
32. McDonnell, J. M. (2001) Surface plasmon resonance: towards an understanding of the mechanisms of biological molecular recognition. Curr. Opin. Chem. Biol. 5, 572-577
33. Zhang, F., Kamp, F., and Hamilton, J. A. (1996) Dissociation of long and very long chain fatty acids from phospholipid bilayers. Biochemistry 35, 16055-16060
34. Crouse, J. R., Parks, J. S., Schey, H. M., and Kahl, F. R. (1985) Studies of low density lipoprotein molecular weight in human beings with coronary artery disease. J. Lipid Res. 26, 566-574
35. Martin, C. A., Longman, E., Wooding, C., Hoosdally, S. J., Ali, S., Aitman, T. J., Gutmann, D. A., Freemont, P. S., Byrne, B., and Linton, K. J. (2007) Cd36, a class B scavenger receptor, functions as a monomer to bind acetylated and oxidized low-density lipoproteins. Protein Sci. 16, 2531-2541
36. Hoosdally, S. J., Andress, E. J., Wooding, C., Martin, C. A., and Linton, K. J. (2009) The Human Scavenger Receptor CD36: glycosylation status and its role in trafficking and function. J. Biol. Chem. 284, 16277-16288
37. Brunaldi, K., Huang, N., and Hamilton, J. A. (2010) Fatty acids are rapidly delivered to and extracted from membranes by methyl-β-cyclodextrin. J. Lipid Res. 51, 120-131
38. Pillai, B. K., Jasuja, R., Simard, J. R., and Hamilton, J. A. (2009) Fast diffusion of very long chain saturated fatty acids across a bilayer membrane and their rapid extraction by cyclodextrins: implications for adrenoleukodystrophy. J. Biol. Chem. 284, 33296-33304
39. Krenzel, E. S., Chen, Z., and Hamilton, J. A. (2013) Correspondence of fatty acid and drug binding sites on human serum albumin: a two-dimensional nuclear magnetic resonance study. Biochemistry 52, 1559-1567
40. Hamilton, J. A. (2013) NMR reveals molecular interactions and dynamics of fatty acid binding to albumin. Biochim. Biophys. Acta 1830, 5418-5426
41. Zhang, F., Lücke, C., Baier, L. J., Sacchettini, J. C., and Hamilton, J. A. (1997) Solution structure of human intestinal fatty acid binding protein: implications for ligand entry and exit. J. Biomol. NMR 9, 213-228
42. Cai, J., Lücke, C., Chen, Z., Qiao, Y., Klimtchuk, E., and Hamilton, J. A. (2012) Solution structure and backbone dynamics of human liver fatty acid binding protein: fatty acid binding revisited. Biophys. J. 102, 2585-2594
43. Abumrad, N., Coburn, C., and Ibrahimi, A. (1999) Membrane proteins implicated in long-chain fatty acid uptake by mammalian cells: CD36, FATP and FABPm. Biochim. Biophys. Acta 1441, 4-13
44. Gaubatz, J. W., Gillard, B. K., Massey, J. B., Hoogeveen, R. C., Huang, M., Lloyd, E. E., Raya, J. L., Yang, C. Y., and Pownall, H. J. (2007) Dynamics of dense electronegative low density lipoproteins and their preferential association with lipoprotein phospholipase A2. J. Lipid Res. 48, 348-357
45. Stoll, L. L., and Spector, A. A. (1984) Changes in serum influence the fatty acid composition of established cell lines. In Vitro. 20, 732-738
46. Madonna, R., Salerni, S., Schiavone, D., Glatz, J. F., Geng, Y. J., and De Caterina, R. (2011) Omega-3 fatty acids attenuate constitutive and insulininduced CD36 expression through a suppression of PPAR α/γ activity in microvascular endothelial cells. Thromb. Haemost. 106, 500-510
47. Tarhda, Z., Semlali, O., Kettani, A., Moussa, A., Abumrad, N. A., and Ibrahimi, A. (2013) Three dimensional structure prediction of fatty acid binding site on human transmembrane receptor CD36. Bioinform. Biol. Insights 7, 369-373
48. Pownall, H., and Moore, K. (2014) Commentary on fatty acid wars: the diffusionists versus the translocatists. Arterioscler. Thromb. Vasc. Biol. 34, e8-e9
49. Le Foll, C., Dunn-Meynell, A., Musatov, S., Magnan, C., and Levin, B. E. (2013) FAT/CD36: a major regulator of neuronal fatty acid sensing and energy homeostasis in rats and mice. Diabetes 62, 2709-2716
50. Degrace-Passilly, P., and Besnard, P. (2012) CD36 and taste of fat. Curr. Opin. Clin. Nutr. Metab. Care 15, 107-111
51. Silverstein, R. L. (2009) Inflammation, atherosclerosis, and arterial thrombosis: role of the scavenger receptor CD36. Cleve. Clin. J. Med. 76, S27-S30
52. Harmon, C. M., Luce, P., and Abumrad, N. A. (1992) Labelling of an 88 kDa adipocyte membrane protein by sulpho-N-succinimidyl long-chain fatty acids: inhibition of fatty acid transport. Biochem. Soc. Trans. 20, 811-813
53. Simard, J. R., Meshulam, T., Pillai, B. K., Kirber, M. T., Brunaldi, K., Xu, S., Pilch, P. F., and Hamilton, J. A. (2010) Caveolins sequester FA on the cytoplasmic leaflet of the plasma membrane, augment triglyceride formation, and protect cells from lipotoxicity. J. Lipid Res. 51, 914-922
54. Robbins, A. K., and Horlick, R. A. (1998) Macrophage scavenger receptor confers an adherent phenotype to cells in culture. BioTechniques 25, 240-244
55. Baranova, I. N., Vishnyakova, T. G., Bocharov, A. V., Leelahavanichkul, A., Kurlander, R., Chen, Z., Souza, A. C., Yuen, P. S., Star, R. A., Csako, G., Patterson, A. P., and Eggerman, T. L. (2012) Class B scavenger receptor types I and II and CD36 mediate bacterial recognition and proinflammatory signaling induced by Escherichia coli, lipopolysaccharide, and cytosolic chaperonin 60. J. Immunol. 188, 1371-1380
56. Hofnagel, O., Luechtenborg, B., Weissen-Plenz, G., and Robenek, H. (2007) Statins and foam cell formation: impact on LDL oxidation and uptake of oxidized lipoproteins via scavenger receptors. Biochim. Biophys. Acta 1771, 1117-1124
57. Amézaga, N., Sanjurjo, L., Julve, J., Aran, G., Pérez-Cabezas, B., Bastos-Amador, P., Armengol, C., Vilella, R., Escolá-Gil, J. C., Blanco-Vaca, F., Borrás, F. E., Valledor, A. F., and Sarrias, M. R. (2014) Human scavenger protein AIM increases foam cell formation and CD36-mediated oxLDL uptake. J. Leukocyte Biol. 95, 509-520
58. Gerich, J. E., Langlois, M., Schneider, V., Karam, J. H., and Noacco, C. (1974) Effects of alternations of plasma free fatty acid levels on pancreatic glucagon secretion in man. J. Clin. Invest. 53, 1284-1289
59. Sun, B., Boyanovsky, B. B., Connelly, M. A., Shridas, P., van der Westhuyzen, D. R., and Webb, N. R. (2007) Distinct mechanisms for OxLDL uptake and cellular trafficking by class B scavenger receptors CD36 and SR-BI. J. Lipid Res. 48, 2560-2570
60. Sun, B., Eckhardt, E. R., Shetty, S., van der Westhuyzen, D. R., and Webb, N. R. (2006) Quantitative analysis of SR-BI-dependent HDL retroendocytosis in hepatocytes and fibroblasts. J. Lipid Res. 47, 1700-1713
61. Kanicky, J. R., and Shah, D. O. (2002) Effect of degree, type, and position of unsaturation on the pKa of long-chain fatty acids. J. Colloid Interface Sci. 256, 201-207
62. Khan-Merchant, N., Penumetcha, M., Meilhac, O., and Parthasarathy, S. (2002) Oxidized fatty acids promote atherosclerosis only in the presence of dietary cholesterol in low-density lipoprotein receptor knockout mice. J. Nutr. 132, 3256-3262
63. Bassett, C. M., Edel, A. L., Patenaude, A. F., McCullough, R. S., Blackwood, D. P., Chouinard, P. Y., Paquin, P., Lamarche, B., and Pierce, G. N. (2010) Dietary vaccenic acid has antiatherogenic effects in LDLr-/- mice. J. Nutr. 140, 18-24
64. Stachowska, E., Dolegowska, B., Chlubek, D., Wesolowska, T., Ciechanowski, K., Gutowski, P., Szumilowicz, H., and Turowski, R. (2004) Dietary trans fatty acids and composition of human atheromatous plaques. Eur. J. Nutr. 43, 313-318
65. Saéz-Cirión, A., and Nieva, J. L. (2002) Conformational transitions of mem-brane- bound HIV-1 fusion peptide. Biochim. Biophys. Acta 1564, 57-65
66. Hebling, C. M., Morgan, C. R., Stafford, D. W., Jorgenson, J. W., Rand, K. D., and Engen, J. R. (2010) Conformational analysis of membrane proteins in phospholipid bilayer nanodiscs by hydrogen exchange mass spectrometry. Anal. Chem. 82, 5415-5419
67. Ebbert, J. O., and Jensen, M. D. (2013) Fat depots, free fatty acids, and dyslipidemia. Nutrients 5, 498-508
68. Mittendorfer, B., Magkos, F., Fabbrini, E., Mohammed, B. S., and Klein, S. (2009) Relationship between body fat mass and free fatty acid kinetics in men and women. Obesity 17, 1872-1877
69. Kashyap, S. R., Ioachimescu, A. G., Gornik, H. L., Gopan, T., Davidson, M. B., Makdissi, A., Major, J., Febbraio, M., and Silverstein, R. L. (2009) Lipid-induced insulin resistance is associated with increased monocyte expression of scavenger receptor CD36 and internalization of oxidized LDL. Obesity 17, 2142-2148
70. Ku, G., Thomas, C. E., Akeson, A. L., and Jackson, R. L. (1992) Induction of interleukin 1β expression from human peripheral blood monocyte-derived macrophages by 9-hydroxyoctadecadienoic acid. J. Biol. Chem. 267, 14183-14188