Misfolding of apoprotein B-100, LDL aggregation and 17-β -estradiol in atherogenesis

Current Medicinal Chemistry

Volumn 21, Issue 20, 2014, Pages 2276-2283

  Brunelli, R ^a   De Spirito, M ^b   Mei, G ^c   Papi, M ^b   Perrone, G ^a   Stefanutti, C ^d   Parasassi, T ^e  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b CATHOLIC UNIVERSITY   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d Unità di Tecniche Terapeutiche Extracorporee Ctro per Lo Stud Diagnosi Dipartimento di Medicina Molecolare   (Italy)

^e INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

Author keywords

17 estradiol; Amyloid; Electronegative low density lipoprotein; Oxidized low density lipoprotein; Phospholipase A2; Subendothelial droplets

Indexed keywords

AMYLOID PROTEIN; APOLIPOPROTEIN B100; APOLIPOPROTEIN E2; APOPROTEIN; CALCIUM DEPENDENT PHOSPHOLIPASE A2; CHOLESTEROL; ESTRADIOL; FAT DROPLET; FATTY ACID; LOW DENSITY LIPOPROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHOLIPASE A2; UNCLASSIFIED DRUG; APOLIPOPROTEIN B;

ATHEROGENESIS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CHOLESTEROL BLOOD LEVEL; CONFORMATIONAL TRANSITION; ENDOTHELIUM CELL; HUMAN; INFLAMMATION; LIPOLYSIS; OXIDATIVE STRESS; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTEIN MISFOLDING; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; REVIEW; CHEMISTRY; METABOLISM; OXIDATION REDUCTION REACTION; ULTRASTRUCTURE;

APOLIPOPROTEINS B; ATHEROSCLEROSIS; ESTRADIOL; HUMANS; LIPOPROTEINS, LDL; OXIDATION-REDUCTION; PROTEIN FOLDING;

EID: 84900323832     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867321666140120114944     Document Type: Review

References (57)

1. Tabas, I.; Williams, K.J.; Borén, J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation, 2007, 116(16), 1832-1844.
2. Skålén, K.; Gustafsson, M.; Rydberg, E. K.; Hultén, L. M.; Wiklund, O.; Innerarity, T. L.; Borén, J. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature, 2002, 417, 750-754.
3. Williams, K. J.; Tabas, I. Lipoprotein retention-and clues for atheroma regression. Arterioscler. Thromb. Vasc. Biol., 2005, 25, 1536-1540.
4. Lehti, S.; Käkelä, R.; Hörkkö, S.; Kummu, O.; Helske-Suihko, S.; Kupari, M.; Werkkala, K.; Kovanen, P.T.; Oörni, K. Modified lipoprotein-derived lipid particles accumulate in human stenotic aortic valves. PLoS One, 2013, 8(6), e65810. doi: 10.1371/journal. pone.0065810.
5. Sánchez-Quesada, J.L.; Villegas, S.; Ordóñez-Llanos, J. Electronegative low-density lipoprotein. A link between apolipoprotein B misfolding, lipoprotein aggregation and proteoglycan binding. Curr. Opin. Lipidol., 2012, 23(5), 479-486.
6. Bancells, C.; Villegas, S.; Blanco, F.J.; Benítez, S.; Gállego, I.; Beloki, L.; Pérez-Cuellar, M.; Ordóñez- Llanos, J.; Sánchez- Quesada, J.L. Aggregated electronegative low density lipoprotein in human plasma shows a high tendency toward phospholipolysis and particle fusion. J. Biol. Chem., 2010, 285(42), 32425-32435.
7. Ursini, F.; Davies, K.J.; Maiorino, M.; Parasassi, T.; Sevanian, A. Atherosclerosis: another protein misfolding disease? Trends. Mol. Med., 2002, 8(8), 370-374.
8. Parasassi, T.; De Spirito, M.; Mei, G.; Brunelli, R.; Greco, G.; Lenzi, L.; Maulucci, G.; Nicolai, E.; Papi, M.; Arcovito, G.; Tosatto, S.C.; Ursini, F. LowDensityLipoproteinMisfolding and Amyloidogenesis. FASEB J., 2008, 22(7), 2350-2356.
9. Bhakdi, S.; Lackner, K.J.; Han, S.R.; Torzewski, M.; Husmann, M. Beyond cholesterol: the enigma of atherosclerosis revisited. Thromb. Haemost., 2004, 91(4), 639-645.
10. Libby, P.; Ridker, P.M.; Hansson, G.K. Progress and challenges in translating the biology of atherosclerosis. Nature, 2011, 473(7347), 317-325.
11. Cannon, C.P.; Braunwald, E.; McCabe, C.H.; Rader, D.J.; Rouleau, J.L.; Belder, R.; Joyal, S.V.; Hill, K.A.; Pfeffer, M.A.; Skene, A.M. Pravastatin or Atorvastatin Evaluation and Infection Therapy-Thrombolysis in Myocardial Infarction 22 Investigators. Intensive versus moderate lipid lowering with statins after acute coronary syndromes. N. Engl. J. Med., 2004, 350(15), 1495-1504.
12. Pentikäinen, M.O.; Lehtonen, E.M.P.; Kovanen, P.T. Aggregation and fusion of modified low density lipoprotein. J. Lipid. Res., 1996, 37, 2638-2649.
13. Öörni, K.; Sneck, M.; Brömme, D.; Pentikäinen, M.O.; Lindstedt, K.A.; Mäyränpää, M.; Aitio, H.; Kovanen, P.T. Cysteine protease cathepsin F is expressed in human atherosclerotic lesions, is secreted by cultured macrophages, and modifies low density lipoprotein particles in vitro. J. Biol. Chem., 2004, 279, 34776-34784.
14. Sneck, M.; Nguyen, S.D.; Pihlajamaa, T.; Yohannes, G.; Riekkola, M.L.; Milne, R.; Kovanen, P.T.; Oörni, K. Conformational changes of apoB-100 in SMase-modified LDL mediate formation of large aggregates at acidic pH. J. Lipid Res., 2012, 53(9), 1832-1839.
15. Mello, A.P.; da Silva, I.T.; Abdalla, D.S.; Damasceno, N.R. Electronegative low density lipoprotein: origin and impact on health and disease. Atherosclerosis, 2011, 215, 257-265.
16. Niccoli, G.; Bacà, M.; De Spirito, M.; Parasassi, T.; Cosentino, N.; Greco, G.; Conte, M.; Montone, R.A.; Arcovito, G.; Crea, F. Impact of electronegative low-density lipoprotein on angiographic coronary atherosclerotic burden. Atherosclerosis, 2012, 223(1), 166-170.
17. Hoff, H.F.; Heideman, C.L.; Gaubatz, J.W.; Gotto, A.M. Jr.; Erickson, E.E.; Jackson, R.L. Quantification of apolipoprotein B in grossly normal human aorta. Circ. Res., 1977, 40, 56-64.
18. Ishigaki, Y.; Oka, Y.; Katagiri, H. Circulating oxidized LDL: a biomarker and a pathogenic factor. Curr. Opin. Lipidol., 2009, 20(5), 363-369.
19. Natella, F.; Ghiselli, A.; Guidi, A.; Ursini, F.; Scaccini, C. Red wine mitigates the postprandial increase of LDL susceptibility to oxidation. Free Radic. Biol. Med., 2001, 30(9), 1036-1044.
20. Hackenhaar, F.S.; Martinez, D.; Medeiros, T.M.; Klein, C.; Alabarse, P.V.; Wainstein, M.V.; Gonçalves, S.C.; Benfato, M.S. Oxidized- LDL and paraoxonase-1 as biomarkers of coronary artery disease in patients with sleep-disordered breathing. Curr. Med. Chem., 2012, 19(25), 4359-4366.
21. Tsimikas, S.; Willeit, P.; Willeit, J.; Santer, P.; Mayr, M.; Xu, Q.; Mayr, A.; Witztum, J.L.; Kiechl, S. Oxidation-specific biomarkers, prospective 15-year cardiovascular and stroke outcomes, and net reclassification of cardiovascular events. J. Am. Coll.Cardiol., 2012, 60(21), 2218-2229.
22. Bossola, M.; Tazza, L.; Luciani, G.; Tortorelli, A.; Tsimikas, S. OxPL/apoB, lipoprotein(a) and OxLDL biomarkers and cardiovascular disease in chronic hemodialysis patients. J. Nephrol., 2011, 24(5), 581-588.
23. Libby, P.; Okamoto, Y.; Rocha, V.Z.; Folco, E. Inflammation in atherosclerosis: transition from theory to practice. Circ. J., 2010, 74(2), 213-220.
24. Perrin-Cocon, L.; Coutant, F.; Agaugue, S.; Deforges, S.; Andre, P.; Lotteau, V. Oxidized low-density lipoprotein promotes mature dendritic cell transition from differentiating monocyte. J.Immunol., 2001, 167(7), 3785-3791.
25. Tedgui, A.; Mallat, Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol. Rev., 2006, 86, 515-581.
26. Stefanutti, C.; Vivenzio, A.; Di Giacomo, S.; Ferraro, P.M. Cytokines profile in serum of homozygous familial hypercholesterolemia is changed by LDL-apheresis. Cytokine, 55(2), 245-250.
27. Davignon, J.; Jacob, R.F.; Mason, R.P. The antioxidant effects of statins. Coron. Artery Dis., 2004, 15(5), 251-258.
28. Stefanutti, C.; Di Giacomo, S.;Vivenzio, A.; Isacchi, G.C.; Masella, R.; Caprari, P.; Vari, R.; Tarzia, A.; Mosiello, A.; Cantafora A. Acute and long-term effects of low-density lipoprotein (LDL)- apheresis on oxidative damage to LDL and reducing capacity of erythrocytes in patients with severe familial hypercholesterolaemia. Clin. Sci. (Lond), 2001, 100(2), 191-198.
29. Tsimikas, S.; Witztum, J.L.; Miller, E.R.; Sasiela, W.J.; Szarek, M.; Olsson, A.G.; Schwartz, G.G.; Myocardial Ischemia Reduction with Aggressive Cholesterol Lowering (MIRACL) Study Investigators. High-dose atorvastatin reduces total plasma levels of oxidized phospholipids and immune complexes present on apolipoprotein B- 100 in patients with acute coronary syndromes in the MIRACL trial. Circulation, 2004, 110(11), 1406-1412.
30. Stocker, R.; Keaney, J.F. Jr. Role of oxidative modifications in atherosclerosis. Physiol. Rev., 2004, 84(4), 1381-1478.
31. Gaubatz, J.W.; Gillard, B.K.; Massey, J.B.; Hoogeveen, R.C.; Huang, M.; Lloyd, E.E.; Raya, J.L.; Yang, C.Y.; Pownall, H.J. Dynamics of dense electronegative low density lipoproteins and their preferential association with lipoprotein phospholipase A(2). J. Lipid Res., 2007, 48(2), 348-357.
32. Benítez, S.; Ordóñez-Llanos, J.; Franco, M.; Marín, C.; Paz, E.; López-Miranda, J.; Otal, C.; Pérez-Jiménez, F.; Sánchez-Quesada, J.L. Effect of simvastatin in familial hypercholesterolemia on the affinity of electronegative low-density lipoprotein subfractions to the low-density lipoprotein receptor. Am. J.Cardiol., 2004, 93(4), 414-420.
33. Sánchez-Quesada, J.L.; Benitez, S.; Franco, M.; Blanco-Vaca, F.; Ordonez-Llanos, J. Density distribution of electronegative LDL [LDL(-)] in normolipemic and hyperlipemic subjects. J. Lipid Res., 2002, 43, 699-705.
34. Sánchez-Quesada, J.L.; Pérez, A.; Caixàs, A.; Rigla, M.; Payés, A.; Benítez, S.; Ordóñez-Llanos, J. Effect of glycemic optimization on electronegative low-density lipoprotein in diabetes: relation to nonenzymatic glycosylation and oxidative modification. J. Clin. Endocrinol. Metab., 2001, 86(7), 3243-3249.
35. Sánchez-Quesada, J.L.; Pérez, A. Modified lipoproteins as biomarkers of cardiovascular risk in diabetes mellitus. Endocrinol. Nutr., 2013, pii: S1575-0922(13)00045-4. doi: 10.1016/j.endonu. 2012.12.007.
36. Sánchez-Quesada, J.L.; Benítez, S.; Pérez, A.; Wagner, A.M.; Rigla, M.; Carreras, G.; Vila, L.; Camacho, M.; Arcelus, R.; Ordóñez-Llanos, J. The inflammatory properties of electronegative low-density lipoprotein from type 1 diabetic patients are related to increased platelet-activating factor acetylhydrolase activity. Diabetologia, 2005, 48(10), 2162-2169.
37. Benítez, S.; Pérez, A.; Sánchez-Quesada, J.L.; Wagner, A.M.; Rigla, M.; Arcelus, R.; Jorba, O.; Ordóñez-Llanos, J. Electronegative low-density lipoprotein subfraction from type 2 diabetic subjects is proatherogenic and unrelated to glycemic control. Diabetes Metab. Res. Rev., 2007, 23(1), 26-34.
38. de Queiroz Mello, A.P.; da Silva, I.T.; Oliveira, A.S.; Nunes, V.S.; Abdalla, D.S.; Gidlund, M.; Damasceno, N.R. Electronegative lowdensity lipoprotein is associated with dense low-density lipoprotein in subjects with different levels of cardiovascular risk. Lipids, 2010, 45(7), 619-625.
39. Sánchez-Quesada, J.L.; Benítez, S.; Ordóñez- Llanos J. Electronegative low-density lipoprotein. Curr. Opin. Lipidol., 2004, 15(3), 329-335.
40. Sánchez-Quesada, J.L.; Camacho, M.; Antón, R.; Benítez, S.; Vila, L.; Ordóñez-Llanos, J. Electronegative LDL of FH subjects: chemical characterization and induction of chemokine release from human endothelial cells. Atherosclerosis, 2003, 166(2), 261-270.
41. Benítez, S.; Camacho, M.; Bancells, C.; Vila, L.; Sánchez- Quesada, J.L.; Ordóñez-Llanos, J. Wide proinflammatory effect of electronegative low-density lipoprotein on human endothelial cells assayed by a protein array. Biochim. Biophys. Acta, 2006, 1761(9), 1014-1021.
42. de Castellarnau, C.; Bancells, C.; Benítez, S.; Reina, M.; Ordóñez- Llanos, J.; Sánchez-Quesada, J.L. Atherogenic and inflammatory profile of human arterial endothelial cells (HUAEC) in response to LDL subfractions. Clin. Chim. Acta, 2007, 376(1-2), 233-236.
43. De Castellarnau, C.; Sánchez-Quesada, J.L.; Benítez, S.; Rosa, R.; Caveda, L.; Vila, L.; Ordóñez-Llanos, J. Electronegative LDL from normolipemic subjects induces IL-8 and monocyte chemotactic protein secretion by human endothelial cells. Arterioscler. Thromb. Vasc. Biol., 2000, 20(10), 2281-2287.
44. Zhang, B.; Matsunaga, A.; Rainwater, D.L.; Miura, S.; Noda, K.; Nishikawa, H.; Uehara, Y.; Shirai, K.; Ogawa, M.; Saku, K. Effects of rosuvastatin on electronegative LDL as characterized by capillary isotachophoresis: the ROSARY Study. J. Lipid Res., 2009, 50(9), 1832-1841.
45. Benítez, S.; Villegas, V.; Bancells, C.; Jorba, O.; González-Sastre, F.; Ordóñez-Llanos, J.; Sánchez-Quesada, J.L. Impaired binding affinity of electronegative low-density lipoprotein (LDL) to the LDL receptor is related to nonesterified fatty acids and lysophosphatidylcholine content. Biochemistry, 2004, 43(50), 15863-15872.
46. Greco, G.; Balogh, G.; Brunelli, R.; Costa, G.; De Spirito, M.; Lenzi, L.; Mei, G.; Ursini, F.; Parasassi, T. Generation in human plasma of misfolded, aggregation-prone electronegative LDL. Biophys. J., 2009, 97(2), 628-635.
47. Rosenson, R.S.; Hurt-Camejo, E. Phospholipase A2 enzymes and the risk of atherosclerosis. Eur. Heart J., 2012, 33(23), 2899-2909.
48. Rosenson, R.S.; Hislop, C.; McConnell, D.; Elliott, M.; Stasiv, Y.; Wang, N.; Waters, D.D.; PLASMA Investigators. Effects of 1-Hindole- 3-glyoxamide (A-002) on concentration of secretory phospholipase A2 (PLASMA study): a phase II double-blind, randomised, placebo-controlled trial. Lancet, 2009, 373(9664), 649-658.
49. Hevonoja, T.; Pentikäinen, M.O.; Hyvönen, M.T.; Kovanen, P.T.; Ala-Korpela, M. Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim. Biophys. Acta, 2000, 1488(3), 189-210.
50. Brunelli, R.; Balogh, G.; Costa, G.; De Spirito, M.; Greco, G.; Mei, G.; Nicolai, E.; Vigh, L.; Ursini, F.; Parasassi, T. Estradiol binding prevents ApoB-100 misfolding in electronegative LDL(-). Biochemistry, 2010, 49(34), 7297-7302.
51. Parasassi, T.; Bittolo-Bon, G.; Brunelli, R.; Cazzolato, G.; Krasnowska, E.K.; Mei, G.; Sevanian, A.; Ursini, F. Loss of apoB-100 secondary structure and conformation in hydroperoxide rich, electronegative LDL(-). Free Radic. Biol. Med., 2001, 31(1), 82-89.
52. Stefani, M.; Dobson, C.M. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med., 2003, 81(11), 678-699.
53. De Spirito, M.; Brunelli, R.; Mei, G.; Bertani, F.R.; Ciasca, G.; Greco, G.; Papi, M.; Arcovito, G.; Ursini, F.; Parasassi, T. Low density lipoprotein aged in plasma forms clusters resembling subendothelial droplets: aggregation via surface sites. Biophys. J., 2006, 90(11), 4239-4247.
54. Oörni, K.; Pentikäinen, M.O.; Ala-Korpela, M.; Kovanen, P.T. Aggregation, fusion, and vesicle formation of modified low density lipoprotein particles: molecular mechanisms and effects on matrix interactions. J. Lipid Res., 2000, 41(11), 1703-1714.
55. Brunelli, R.; Greco, G.; Barteri, M.; Krasnowska, E.K.; Mei, G.; Natella, F.; Pala, A.; Rotella, S.; Ursini, F.; Zichella, L.; Parasassi, T. One site on the apoB-100 specifically binds 17-β-estradiol and regulates the overall structure of LDL. FASEB J., 2003, 17(14), 2127-2129.
56. Ruiz-Sanz, J.I.; Navarro, R.; Martínez, R.; Martín, C.; Lacort, M.; Matorras, R.; Ruiz-Larrea, M.B. 17β-estradiol affects in vivo the low density lipoprotein composition, particle size, and oxidizability. Free Radic. Biol. Med., 2001, 31(3), 391-397.
57. Brunelli, R.; Mei, G.; Krasnowska, E.K.; Pierucci, F.; Zichella, L.; Ursini, F.; Parasassi, T. Estradiol enhances the resistance of LDL to oxidation by stabilizing apoB-100 conformation. Biochemistry, 2000, 39(45), 13897-13903.