High binding affinity of electronegative LDL to human aortic proteoglycans depends on its aggregation level

Journal of Lipid Research

Volumn 50, Issue 3, 2009, Pages 446-455

  Bancells, Cristina ^a,b   Benítez, Sònia ^a   Jauhiainen, Matti ^c   Ordóñez Llanos, Jordi ^a,b   Kovanen, Petri T ^d   Villegas, Sandra ^b   Sánchez Quesada, José Luis ^a   Öörni, Katariina ^d  

^a HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^d WIHURI RESEARCH INSTITUTE   (Finland)

Author keywords

Glycosaminoglycans; Lipoprotein aggregation; Phospholipase C; Sphingomyelinase

Indexed keywords

LOW DENSITY LIPOPROTEIN; PHOSPHOLIPASE C; PROTEOGLYCAN; APOLIPOPROTEIN C3; APOLIPOPROTEIN E; GLYCOSAMINOGLYCAN; MULTIPROTEIN COMPLEX; SPHINGOMYELIN PHOSPHODIESTERASE;

AFFINITY CHROMATOGRAPHY; AORTA; ARTERY INTIMA; ARTICLE; ATHEROSCLEROSIS; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; HUMAN TISSUE; LIPID COMPOSITION; MICROTITER PLATE ASSAY; PRECIPITATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN LIPID INTERACTION; BLOOD; CHEMISTRY; ELECTROCHEMISTRY; IN VITRO STUDY; KINETICS; METABOLISM; PH; PROTEIN BINDING;

AORTA; APOLIPOPROTEIN C-III; APOLIPOPROTEINS E; CHROMATOGRAPHY, AFFINITY; ELECTROCHEMISTRY; GLYCOSAMINOGLYCANS; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; LIPOPROTEINS, LDL; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEOGLYCANS; SPHINGOMYELIN PHOSPHODIESTERASE; TYPE C PHOSPHOLIPASES;

EID: 64349100818     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800318-JLR200     Document Type: Article

References (54)

1. Srinivasan, S. R., P. Vijayagopal, E. R. Dalferes, Jr., B. Abbate, B. Radhakrishnamurthy, and G. S. Berenson. 1986. Low density lipoprotein retention by aortic tissue. Contribution of extracellular matrix. Atherosclerosis. 62: 201-208.
2. Hurt-Camejo, E., U. Olsson, O. Wiklund, G. Bondjers, and G. Camejo. 1997. Cellular consequences of the association of apoB lipoproteins with proteoglycans. Potential contribution to atherogenesis. Arterioscler. Thromb. Vasc. Biol. 17: 1011-1017.
3. Camejo, G., E. Hurt-Camejo, O. Wiklund, and G. Bondjers. 1998. Association of apo B lipoproteins with arterial proteoglycans: pathological significance and molecular basis. Atherosclerosis. 139: 205-222.
4. Williams, K. J., and I. Tabas. 1995. The response-to-retention hypothesis of early atherogenesis. Arterioscler. Thromb. Vasc. Biol. 15: 551-561.
5. Wight, T. N. 1995. The extracellular matrix and atherosclerosis. Curr. Opin. Lipidol. 6: 326-334.
6. Iverius, P. H. 1972. The interaction between human plasma lipoproteins and connective tissue glycosaminoglycans. J. Biol. Chem. 247: 2607-2613.
7. Weisgraber, K. H., and S. C. Rall, Jr. 1987. Human apolipoprotein B-100 heparin-binding sites. J. Biol. Chem. 262: 11097-11103.
8. Camejo, G., S. O. Olofsson, F. Lopez, P. Carlsson, and G. Bondjers. 1988. Identification of apo B-100 segments mediating the interaction of low density lipoproteins with arterial proteoglycans. Arteriosclerosis. 8: 368-377.
9. Cardin, A. D., and H. J. Weintraub. 1989. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis. 9: 21-32.
10. Flood, C., M. Gustafsson, R. E. Pitas, L. Arnaboldi, R. L. Walzem, and J. Boren. 2004. Molecular mechanism for changes in proteoglycan binding on compositional changes of the core and the surface of low-density lipoprotein-containing human apolipoprotein B100. Arterioscler. Thromb. Vasc. Biol. 24: 564-570.
11. Oorni, K., M. O. Pentikainen, M. Ala-Korpela, and P. T. Kovanen. 2000. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J. Lipid Res. 41: 1703-1714.
12. Asatryan, L., R. T. Hamilton, J. M. Isas, J. Hwang, R. Kayed, and A. Sevanian. 2005. LDL phospholipid hydrolysis produces modified electronegative particles with an unfolded apoB-100 protein. J. Lipid Res. 46: 115-122.
13. Mahley, R. W., K. H. Weisgraber, and T. L. Innerarity. 1979. Interaction of plasma lipoproteins containing apolipoproteins B and E with heparin and cell surface receptors. Biochim. Biophys. Acta. 575: 81-91.
14. Olin-Lewis, K., R. M. Krauss, M. La Belle, P. J. Blanche, P. H. Barrett, T. N. Wight, and A. Chait. 2002. ApoC-III content of apoB-containing lipoproteins is associated with binding to the vascular proteoglycan biglycan. J. Lipid Res. 43: 1969-1977.
15. Sanchez-Quesada, J. L., S. Benitez, and J. Ordonez-Llanos. 2004. Electronegative low-density lipoprotein. Curr. Opin. Lipidol. 15: 329-335.
16. Demuth, K., I. Myara, B. Chappey, B. Vedie, M. A. Pech-Amsellem, M. E. Haberland, and N. Moatti. 1996. A cytotoxic electronegative LDL subfraction is present in human plasma. Arterioscler. Thromb. Vasc. Biol. 16: 773-783.
17. Chen, C. H., T. Jiang, J. H. Yang, W. Jiang, J. Lu, G. K. Marathe, H. J. Pownall, C. M. Ballantyne, T. M. McIntyre, P. D. Henry, et al. 2003. Low-density lipoprotein in hypercholesterolemic human plasma induces vascular endothelial cell apoptosis by inhibiting fibroblast growth factor 2 transcription. Circulation. 107: 2102-2108.
18. Sanchez-Quesada, J. L., C. Otal-Entraigas, M. Franco, O. Jorba, F. Gonzalez-Sastre, F. Blanco-Vaca, and J. Ordonez-Llanos. 1999. Effect of simvastatin treatment on the electronegative low-density lipoprotein present in patients with heterozygous familial hypercholesterolemia. Am. J. Cardiol. 84: 655-659.
19. Sanchez-Quesada, J. L., A. Perez, A. Caixas, M. Rigla, A. Payes, S. Benitez, and J. Ordonez-Llanos. 2001. Effect of glycemic optimization on electronegative low-density lipoprotein in diabetes: relation to nonenzymatic glycosylation and oxidative modification. J. Clin. Endocrinol. Metab. 86: 3243-3249.
20. De Castellarnau, C., J. L. Sanchez-Quesada, S. Benitez, R. Rosa, L. Caveda, L. Vila, and J. Ordonez-Llanos. 2000. Electronegative LDL from normolipemic subjects induces IL-8 and monocyte chemotactic protein secretion by human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 20: 2281-2287.
21. Sanchez-Quesada, J. L., S. Benitez, C. Otal, M. Franco, F. Blanco-Vaca, and J. Ordonez-Llanos. 2002. Density distribution of electronegative LDL in normolipemic and hyperlipemic subjects. J. Lipid Res. 43: 699-705.
22. Sanchez-Quesada, J. L., M. Camacho, R. Anton, S. Benitez, L. Vila, and J. Ordonez-Llanos. 2003. Electronegative LDL of FH subjects: chemical characterization and induction of chemokine release from human endothelial cells. Atherosclerosis. 166: 261-270.
23. Hurt-Camejo, E., G. Camejo, B. Rosengren, F. Lopez, O. Wiklund, and G. Bondjers. 1990. Differential uptake of proteoglycan-selected subfractions of low density lipoprotein by human macrophages. J. Lipid Res. 31: 1387-1398.
24. Bartold, P. M., and R. C. Page. 1985. A microdetermination method for assaying glycosaminoglycans and proteoglycans. Anal. Biochem. 150: 320-324.
25. Davidsson, P., J. Hulthe, B. Fagerberg, B. M. Olsson, C. Hallberg, B. Dahllof, and G. Camejo. 2005. A proteomic study of the apolipoproteins in LDL subclasses in patients with the metabolic syndrome and type 2 diabetes. J. Lipid Res. 46: 1999-2006.
26. Sneck, M., P. T. Kovanen, and K. Oorni. 2005. Decrease in pH strongly enhances binding of native, proteolyzed, lipolyzed, and oxidized low density lipoprotein particles to human aortic proteoglycans. J. Biol. Chem. 280: 37449-37454.
27. Oorni, K., M. O. Pentikainen, A. Annila, and P. T. Kovanen. 1997. Oxidation of low density lipoprotein particles decreases their ability to bind to human aortic proteoglycans. Dependence on oxidative modification of the lysine residues. J. Biol. Chem. 272: 21303-21311.
28. Siggins, S., M. Jauhiainen, V. M. Olkkonen, J. Tenhunen, and C. Ehnholm. 2003. PLTP secreted by HepG2 cells resembles the highactivity PLTP form in human plasma. J. Lipid Res. 44: 1698-1704.
29. Benitez, S., J. L. Sanchez-Quesada, V. Ribas, O. Jorba, F. Blanco-Vaca, F. Gonzalez-Sastre, and J. Ordonez-Llanos. 2003. Platelet-activating factor acetylhydrolase is mainly associated with electronegative lowdensity lipoprotein subfraction. Circulation. 108: 92-96.
30. Bancells, C., S. Benitez, S. Villegas, O. Jorba, J. Ordonez-Llanos, and J. L. Sanchez-Quesada. 2008. Novel phospholipolytic activities associated with electronegative low-density lipoprotein are involved in increased self-aggregation. Biochemistry. 47: 8186-8194.
31. Holopainen, J. M., O. P. Medina, A. J. Metso, and P. K. Kinnunen. 2000. Sphingomyelinase activity associated with human plasma low density lipoprotein. J. Biol. Chem. 275: 16484-16489.
32. Forte, T., and A. V. Nichols. 1972. Application of electron microscopy to the study of plasma lipoprotein structure. Adv. Lipid Res. 10: 1-41.
33. Lobley, A., and B. A. Wallace. 2001. DICHROWEB: a website for the analysis of protein secondary structure from circular dichroism spectra. Biophys. J. 80: 373a.
34. Lobley, A., L. Whitmore, and B. A. Wallace. 2002. DICHROWEB: an interactive website for the analysis of protein secondary structure from circular dichroism spectra. Bioinformatics. 18: 211-212.
35. Xu, X. X., and I. Tabas. 1991. Sphingomyelinase enhances low density lipoprotein uptake and ability to induce cholesteryl ester accumulation in macrophages. J. Biol. Chem. 266: 24849-24858.
36. Pentikainen, M. O., E. M. Lehtonen, and P. T. Kovanen. 1996. Aggregation and fusion of modified low density lipoprotein. J. Lipid Res. 37: 2638-2649.
37. Oorni, K., J. K. Hakala, A. Annila, M. Ala-Korpela, and P. T. Kovanen. 1998. Sphingomyelinase induces aggregation and fusion, but phospholipase A2 only aggregation, of low density lipoprotein (LDL) particles. Two distinct mechanisms leading to increased binding strength of LDL to human aortic proteoglycans. J. Biol. Chem. 273: 29127-29134.
38. Suits, A. G., A. Chait, M. Aviram, and J. W. Heinecke. 1989. Phagocytosis of aggregated lipoprotein by macrophages: low density lipoprotein receptor-dependent foam-cell formation. Proc. Natl. Acad. Sci. USA. 86: 2713-2717.
39. Williams, K. J., and I. Tabas. 1998. The response-to-retention hypothesis of atherogenesis reinforced. Curr. Opin. Lipidol. 9: 471-474.
40. Volker, W., A. Schmidt, and E. Buddecke. 1989. Cytochemical changes in a human arterial proteoglycan related to atherosclerosis. Atherosclerosis. 77: 117-130.
41. Olsson, U., G. Ostergren-Lunden, and J. Moses. 2001. Glycosaminoglycan-lipoprotein interaction. Glycoconj. J. 18: 789-797.
42. Naghavi, M., R. John, S. Naguib, M. S. Siadaty, R. Grasu, K. C. Kurian, W. B. van Winkle, B. Soller, S. Litovsky, M. Madjid, et al. 2002. pH Heterogeneity of human and rabbit atherosclerotic plaques; a new insight into detection of vulnerable plaque. Atherosclerosis. 164: 27-35.
43. Leake, D. S. 1997. Does an acidic pH explain why low density lipoprotein is oxidised in atherosclerotic lesions? Atherosclerosis. 129: 149-157.
44. Bjornheden, T., M. Levin, M. Evaldsson, and O. Wiklund. 1999. Evidence of hypoxic areas within the arterial wall in vivo. Arterioscler. Thromb. Vasc. Biol. 19: 870-876.
45. Weisgraber, K. H., S. C. Rall, Jr., R. W. Mahley, R. W. Milne, Y. L. Marcel, and J. T. Sparrow. 1986. Human apolipoprotein E. Determination of the heparin binding sites of apolipoprotein E3. J. Biol. Chem. 261: 2068-2076.
46. Ji, Z. S., W. J. Brecht, R. D. Miranda, M. M. Hussain, T. L. Innerarity, and R. W. Mahley. 1993. Role of heparan sulfate proteoglycans in the binding and uptake of apolipoprotein E-enriched remnant lipoproteins by cultured cells. J. Biol. Chem. 268: 10160-10167.
47. Shuvaev, V. V., I. Laffont, and G. Siest. 1999. Kinetics of apolipoprotein E isoforms-binding to the major glycosaminoglycans of the extracellular matrix. FEBS Lett. 459: 353-357.
48. Paananen, K., J. Saarinen, A. Annila, and P. T. Kovanen. 1995. Proteolysis and fusion of low density lipoprotein particles strengthen their binding to human aortic proteoglycans. J. Biol. Chem. 270: 12257-12262.
49. Liu, H., D. G. Scraba, and R. O. Ryan. 1993. Prevention of phospholipase-C induced aggregation of low density lipoprotein by amphipathic apolipoproteins. FEBS Lett. 316: 27-33.
50. Schissel, S. L., J. Tweedie-Hardman, J. H. Rapp, G. Graham, K. J. Williams, and I. Tabas. 1996. Rabbit aorta and human atherosclerotic lesions hydrolyze the sphingomyelin of retained low-density lipoprotein. Proposed role for arterial-wall sphingomyelinase in subendothelial retention and aggregation of atherogenic lipoproteins. J. Clin. Invest. 98: 1455-1464.
51. Boren, J., I. Lee, W. Zhu, K. Arnold, S. Taylor, and T. L. Innerarity. 1998. Identification of the low density lipoprotein receptor-binding site in apolipoprotein B100 and the modulation of its binding activity by the carboxyl terminus in familial defective apo-B100. J. Clin. Invest. 101: 1084-1093.
52. Sartipy, P., G. Camejo, L. Svensson, and E. Hurt-Camejo. 1999. Phospholipase A(2) modification of low density lipoproteins forms small high density particles with increased affinity for proteoglycans and glycosaminoglycans. J. Biol. Chem. 274: 25913-25920.
53. Sartipy, P., G. Bondjers, and E. Hurt-Camejo. 1998. Phospholipase A2 type II binds to extracellular matrix biglycan: modulation of its activity on LDL by colocalization in glycosaminoglycan matrixes. Arterioscler. Thromb. Vasc. Biol. 18: 1934-1941.
54. Camejo, G., U. Olsson, E. Hurt-Camejo, N. Baharamian, and G. Bondjers. 2002. The extracellular matrix on atherogenesis and diabetes-associated vascular disease. Atheroscler. Suppl. 3: 3-9.