Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter July 10, 2014

Interrelatedness between C-reactive protein and oxidized low-density lipoprotein

  • Milan M. Obradovic EMAIL logo , Andreja Trpkovic , Vladan Bajic , Sanja Soskic , Aleksandra Jovanovic , Julijana Stanimirovic , Milos Panic and Esma R. Isenovic

Abstract

C-reactive protein (CRP) is a marker of inflammation. Atherosclerosis is now recognized as inflammatory disease, and it seems that CRP directly contributes to atherogenesis. Oxidation of low-density lipoprotein (LDL) molecule increases the uptake of lipid products by macrophages leading to cholesterol accumulation and subsequent foam cell formation. The elevated levels of high sensitivity CRP (hsCRP) and oxidized LDL (OxLDL) in the blood were found to be associated with cardiovascular diseases (CVD). In this review, we highlighted the evidence that CRP and OxLDL are involved in interrelated (patho) physiological pathways. The findings on association between hsCRP and OxLDL in the clinical setting will be also summarized.


Corresponding author: Dr. Milan M. Obradovic, Assistant Professor of Research Laboratory of Radiobiology and Molecular Genetics, Vinca Institute of Nuclear Sciences, University of Belgrade, PO Box 522, 11000 Belgrade, Serbia, Phone/Fax: +38 111 3408147, E-mail:

Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

Financial support: This work was supported by grant funded by the Ministry of Education and Science, Republic of Serbia, No. 173033 (to E. R. I.).

Employment or leadership: None declared.

Honorarium: None declared.

Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

References

1. Marcovina SM, Crea F, Davignon J, Kaski JC, Koenig W, Landmesser U, et al. Biochemical and bioimaging markers for risk assessment and diagnosis in major cardiovascular diseases: a road to integration of complementary diagnostic tools. J Intern Med 2007;261:214–34.10.1111/j.1365-2796.2006.01734.xSearch in Google Scholar

2. Verhoye E, Langlois MR. Circulating oxidized low-density lipoprotein: a biomarker of atherosclerosis and cardiovascular risk? Clin Chem Lab Med 2009;47:128–37.10.1515/CCLM.2009.037Search in Google Scholar

3. Steinberg D. The LDL modification hypothesis of atherogenesis: an update. J Lipid Res 2009;50(Suppl):S376–81.10.1194/jlr.R800087-JLR200Search in Google Scholar

4. Ansar W, Ghosh S. C-reactive protein and the biology of disease. Immunol Res 2013;56:131–42.10.1007/s12026-013-8384-0Search in Google Scholar

5. Moshage HJ, Roelofs HM, van Pelt JF, Hazenberg BP, van Leeuwen MA, Limburg PC, et al. The effect of interleukin-1, interleukin-6 and its interrelationship on the synthesis of serum amyloid A and C-reactive protein in primary cultures of adult human hepatocytes. Biochem Biophys Res Commun 1988;155:112–7.10.1016/S0006-291X(88)81056-8Search in Google Scholar

6. Calabro P, Willerson JT, Yeh ET. Inflammatory cytokines stimulated C-reactive protein production by human coronary artery smooth muscle cells. Circulation 2003;108:1930–2.10.1161/01.CIR.0000096055.62724.C5Search in Google Scholar

7. Thompson D, Pepys MB, Wood SP. The physiological structure of human C-reactive protein and its complex with phosphocholine. Structure 1999;7:169–77.10.1016/S0969-2126(99)80023-9Search in Google Scholar

8. Eisenhardt SU, Thiele JR, Bannasch H, Stark GB, Peter K. C-reactive protein: how conformational changes influence inflammatory properties. Cell Cycle 2009;8:3885–92.10.4161/cc.8.23.10068Search in Google Scholar PubMed

9. Calabro P, Golia E, Yeh ET. CRP and the risk of atherosclerotic events. Semin Immunopathol 2009;31:79–94.10.1007/s00281-009-0149-4Search in Google Scholar PubMed

10. Kuller LH, Tracy RP, Shaten J, Meilahn EN. Relation of C-reactive protein and coronary heart disease in the MRFIT nested case-control study. Multiple Risk Factor Intervention Trial. Am J Epidemiol 1996;144:537–47.Search in Google Scholar

11. Danesh J, Whincup P, Walker M, Lennon L, Thomson A, Appleby P, et al. Low grade inflammation and coronary heart disease: prospective study and updated meta-analyses. Br Med J 2000;321:199–204.10.1136/bmj.321.7255.199Search in Google Scholar PubMed PubMed Central

12. Koenig W, Sund M, Frohlich M, Fischer HG, Lowel H, Doring A, et al. C-Reactive protein, a sensitive marker of inflammation, predicts future risk of coronary heart disease in initially healthy middle-aged men: results from the MONICA (Monitoring Trends and Determinants in Cardiovascular Disease) Augsburg Cohort Study, 1984 to 1992. Circulation 1999;99:237–42.10.1161/01.CIR.99.2.237Search in Google Scholar

13. Ballantyne CM, Hoogeveen RC, Bang H, Coresh J, Folsom AR, Heiss G, et al. Lipoprotein-associated phospholipase A2, high-sensitivity C-reactive protein, and risk for incident coronary heart disease in middle-aged men and women in the Atherosclerosis Risk in Communities (ARIC) study. Circulation 2004;109:837–42.10.1161/01.CIR.0000116763.91992.F1Search in Google Scholar PubMed

14. Cushman M, Arnold AM, Psaty BM, Manolio TA, Kuller LH, Burke GL, et al. C-reactive protein and the 10-year incidence of coronary heart disease in older men and women: the cardiovascular health study. Circulation 2005;112:25–31.10.1161/CIRCULATIONAHA.104.504159Search in Google Scholar PubMed

15. Obradovic M, Sudar E, Zafirovic S, Stanimirovic J, Labudovic-Borovic M, Isenovic ER. Estradiol in vivo induces changes in cardiomyocytes size in obese rats. Angiology 2013. [Epub ahead of print 9 Dec 2013]. doi: 10.1177/0003319713514477.10.1177/0003319713514477Search in Google Scholar PubMed

16. Maravic-Stojkovic V, Lausevic-Vuk LJ, Obradovic M, Jovanovic P, Tanaskovic S, Stojkovic B, et al. Copeptin level after carotid endarterectomy and perioperative stroke. Angiology 2014;65:122–9.10.1177/0003319712473637Search in Google Scholar PubMed

17. Tanaskovic S, Isenovic ER, Radak D. Inflammation as a marker for the prediction of internal carotid artery restenosis following eversion endarterectomy – evidence from clinical studies. Angiology 2011;62:535–42.10.1177/0003319710398010Search in Google Scholar PubMed

18. Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest 2003;111:1805–12.10.1172/JCI200318921Search in Google Scholar

19. Pasceri V, Willerson JT, Yeh ET. Direct proinflammatory effect of C-reactive protein on human endothelial cells. Circulation 2000;102:2165–8.10.1161/01.CIR.102.18.2165Search in Google Scholar

20. Verma S, Li SH, Badiwala MV, Weisel RD, Fedak PW, Li RK, et al. Endothelin antagonism and interleukin-6 inhibition attenuate the proatherogenic effects of C-reactive protein. Circulation 2002;105:1890–6.10.1161/01.CIR.0000015126.83143.B4Search in Google Scholar

21. Pasceri V, Cheng JS, Willerson JT, Yeh ET. Modulation of C-reactive protein-mediated monocyte chemoattractant protein-1 induction in human endothelial cells by anti-atherosclerosis drugs. Circulation 2001;103:2531–4.10.1161/01.CIR.103.21.2531Search in Google Scholar PubMed

22. Jialal I, Devaraj S, Venugopal SK. C-reactive protein: risk marker or mediator in atherothrombosis? Hypertension 2004;44:6–11.10.1161/01.HYP.0000130484.20501.dfSearch in Google Scholar

23. Hein TW, Singh U, Vasquez-Vivar J, Devaraj S, Kuo L, Jialal I. Human C-reactive protein induces endothelial dysfunction and uncoupling of eNOS in vivo. Atherosclerosis 2009;206:61–8.10.1016/j.atherosclerosis.2009.02.002Search in Google Scholar

24. Valleggi S, Devaraj S, Dasu MR, Jialal I. C-reactive protein adversely alters the protein-protein interaction of the endothelial isoform of nitric oxide synthase. Clin Chem 2010;56: 1345–8.10.1373/clinchem.2009.142364Search in Google Scholar

25. Verma S, Wang CH, Li SH, Dumont AS, Fedak PW, Badiwala MV, et al. A self-fulfilling prophecy: C-reactive protein attenuates nitric oxide production and inhibits angiogenesis. Circulation 2002;106:913–9.10.1161/01.CIR.0000029802.88087.5ESearch in Google Scholar

26. Venugopal SK, Devaraj S, Jialal I. C-reactive protein decreases prostacyclin release from human aortic endothelial cells. Circulation 2003;108:1676–8.10.1161/01.CIR.0000094736.10595.A1Search in Google Scholar

27. Wang CH, Li SH, Weisel RD, Fedak PW, Dumont AS, Szmitko P, et al. C-reactive protein upregulates angiotensin type 1 receptors in vascular smooth muscle. Circulation 2003;107:1783–90.10.1161/01.CIR.0000061916.95736.E5Search in Google Scholar

28. Nickenig G, Harrison DG. The AT(1)-type angiotensin receptor in oxidative stress and atherogenesis: part II: AT(1) receptor regulation. Circulation 2002;105:530–6.10.1161/hc0402.102619Search in Google Scholar

29. Yasojima K, Schwab C, McGeer EG, McGeer PL. Generation of C-reactive protein and complement components in atherosclerotic plaques. Am J Pathol 2001;158:1039–51.10.1016/S0002-9440(10)64051-5Search in Google Scholar

30. Venugopal SK, Devaraj S, Jialal I. Macrophage conditioned medium induces the expression of C-reactive protein in human aortic endothelial cells: potential for paracrine/autocrine effects. Am J Pathol 2005;166:1265–71.10.1016/S0002-9440(10)62345-0Search in Google Scholar

31. Dehghan A, Dupuis J, Barbalic M, Bis JC, Eiriksdottir G, Lu C, et al. Meta-analysis of genome-wide association studies in >80 000 subjects identifies multiple loci for C-reactive protein levels. Circulation 2011;123:731–8.10.1161/CIRCULATIONAHA.110.948570Search in Google Scholar PubMed PubMed Central

32. Zacho J, Tybjaerg-Hansen A, Jensen JS, Grande P, Sillesen H, Nordestgaard BG. Genetically elevated C-reactive protein and ischemic vascular disease. N Engl J Med 2008;359:1897–908.10.1056/NEJMoa0707402Search in Google Scholar PubMed

33. Lowe GD, Pepys MB. C-reactive protein and cardiovascular disease: weighing the evidence. Curr Atheroscler Rep 2006;8: 421–8.10.1007/s11883-006-0040-xSearch in Google Scholar PubMed

34. Wensley F, Gao P, Burgess S, Kaptoge S, Di Angelantonio E, Shah T, et al. Association between C reactive protein and coronary heart disease: Mendelian randomisation analysis based on individual participant data. Br Med J 2011;342:d548.10.1136/bmj.d548Search in Google Scholar PubMed PubMed Central

35. Elliott P, Chambers JC, Zhang W, Clarke R, Hopewell JC, Peden JF, et al. Genetic Loci associated with C-reactive protein levels and risk of coronary heart disease. J Am Med Assoc 2009;302: 37–48.10.1001/jama.2009.954Search in Google Scholar PubMed PubMed Central

36. Hulthe J, Fagerberg B. Circulating oxidized LDL is associated with subclinical atherosclerosis development and inflammatory cytokines (AIR Study). Arterioscler Thromb Vasc Biol 2002;22:1162–7.10.1161/01.ATV.0000021150.63480.CDSearch in Google Scholar

37. Zhang YC, Wei JJ, Wang F, Chen MT, Zhang MZ. Elevated levels of oxidized low-density lipoprotein correlate positively with C-reactive protein in patients with acute coronary syndrome. Cell Biochem Biophys 2012;62:365–72.10.1007/s12013-011-9295-0Search in Google Scholar PubMed

38. Berneis KK, Krauss RM. Metabolic origins and clinical significance of LDL heterogeneity. J Lipid Res 2002;43:1363–79.10.1194/jlr.R200004-JLR200Search in Google Scholar PubMed

39. Nikolic D, Katsiki N, Montalto G, Isenovic ER, Mikhailidis DP, Rizzo M. Lipoprotein subfractions in metabolic syndrome and obesity: clinical significance and therapeutic approaches. Nutrients 2013;5:928–48.10.3390/nu5030928Search in Google Scholar PubMed PubMed Central

40. Knott TJ, Pease RJ, Powell LM, Wallis SC, Rall SC, Jr., Innerarity TL, et al. Complete protein sequence and identification of structural domains of human apolipoprotein B. Nature 1986;323:734–8.10.1038/323734a0Search in Google Scholar PubMed

41. Goldstein JL, Brown MS. The LDL receptor. Arterioscler Thromb Vasc Biol 2009;29:431–8.10.1161/ATVBAHA.108.179564Search in Google Scholar PubMed PubMed Central

42. Stocker R. Lipoprotein oxidation: mechanistic aspects, methodological approaches and clinical relevance. Curr Opin Lipidol 1994;5:422–33.10.1097/00041433-199412000-00005Search in Google Scholar

43. Banach M, Rizzo M, Obradovic M, Montalto G, Rysz J, Mikhailidis DP, et al. PCSK9 inhibition – a novel mechanism to treat lipid disorders? Curr Pharm Des 2013;19:3869–77.10.2174/13816128113199990303Search in Google Scholar

44. Third Report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III) final report. Circulation 2002;106:3143–421.10.1161/circ.106.25.3143Search in Google Scholar

45. Brunzell JD, Davidson M, Furberg CD, Goldberg RB, Howard BV, Stein JH, et al. Lipoprotein management in patients with cardiometabolic risk: consensus conference report from the American Diabetes Association and the American College of Cardiology Foundation. J Am Coll Cardiol 2008;51:1512–24.10.1016/j.jacc.2008.02.034Search in Google Scholar

46. Sudar E, Zafirovic S, Dobutovic BD, Obradovic M, Soskic SS, Jovanovic A, et al. Obesity as a risk factor for cardiovascular diseases: one of the biggest problem in health care today. Life Safety Security 2013;2:5–17.Search in Google Scholar

47. Yoshida H, Kisugi R. Mechanisms of LDL oxidation. Clin Chim Acta 2010;411:1875–82.10.1016/j.cca.2010.08.038Search in Google Scholar

48. Grundtman C, Wick G. The autoimmune concept of atherosclerosis. Curr Opin Lipidol 2011;22:327–34.10.1097/MOL.0b013e32834aa0c2Search in Google Scholar

49. Goyal T, Mitra S, Khaidakov M, Wang X, Singla S, Ding Z, et al. Current concepts of the role of oxidized LDL receptors in atherosclerosis. Curr Atheroscler Rep 2012:150–9.10.1007/s11883-012-0228-1Search in Google Scholar

50. Stanton LW, White RT, Bryant CM, Protter AA, Endemann G. A macrophage Fc receptor for IgG is also a receptor for oxidized low density lipoprotein. J Biol Chem 1992;267:22446–51.10.1016/S0021-9258(18)41692-4Search in Google Scholar

51. Goldstein JL, Ho YK, Basu SK, Brown MS. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci USA 1979;76:333–7.10.1073/pnas.76.1.333Search in Google Scholar PubMed PubMed Central

52. Witztum JL, Berliner JA. Oxidized phospholipids and isoprostanes in atherosclerosis. Curr Opin Lipidol 1998;9:441–8.10.1097/00041433-199810000-00008Search in Google Scholar PubMed

53. van Tits L, de Graaf J, Toenhake H, van Heerde W, Stalenhoef A. C-reactive protein and annexin A5 bind to distinct sites of negatively charged phospholipids present in oxidized low-density lipoprotein. Arterioscler Thromb Vasc Biol 2005;25:717–22.10.1161/01.ATV.0000157979.51673.2cSearch in Google Scholar PubMed

54. Shih HH, Zhang S, Cao W, Hahn A, Wang J, Paulsen JE, et al. CRP is a novel ligand for the oxidized LDL receptor LOX-1. Am J Physiol Heart Circ Physiol 2009;296:H1643–50.10.1152/ajpheart.00938.2008Search in Google Scholar PubMed

55. Chang MK, Binder CJ, Torzewski M, Witztum JL. C-reactive protein binds to both oxidized LDL and apoptotic cells through recognition of a common ligand: Phosphorylcholine of oxidized phospholipids. Proc Natl Acad Sci USA 2002;99:13043–8.10.1073/pnas.192399699Search in Google Scholar PubMed PubMed Central

56. Fujita Y, Kakino A, Nishimichi N, Yamaguchi S, Sato Y, Machida S, et al. Oxidized LDL receptor LOX-1 binds to C-reactive protein and mediates its vascular effects. Clin Chem 2009;55:285–94.10.1373/clinchem.2008.119750Search in Google Scholar PubMed

57. Hammond DJ, Jr., Singh SK, Thompson JA, Beeler BW, Rusinol AE, Pangburn MK, et al. Identification of acidic pH-dependent ligands of pentameric C-reactive protein. J Biol Chem 2010;285:36235–44.10.1074/jbc.M110.142026Search in Google Scholar PubMed PubMed Central

58. Chang MK, Hartvigsen K, Ryu J, Kim Y, Han KH. The pro-atherogenic effects of macrophages are reduced upon formation of a complex between C-reactive protein and lysophosphatidylcholine. J Inflamm (Lond) 2012;9:42.10.1186/1476-9255-9-42Search in Google Scholar PubMed PubMed Central

59. Chu CS, Wang YC, Lu LS, Walton B, Yilmaz HR, Huang RY, et al. Electronegative low-density lipoprotein increases C-reactive protein expression in vascular endothelial cells through the LOX-1 receptor. PLoS One 2013;8:e70533.10.1371/journal.pone.0070533Search in Google Scholar PubMed PubMed Central

60. Hein TW, Qamirani E, Ren Y, Xu X, Thengchaisri N, Kuo L. Selective activation of lectin-like oxidized low-density lipoprotein receptor-1 mediates C-reactive protein-evoked endothelial vasodilator dysfunction in coronary arterioles. Circ Res 2014;114: 92–100.10.1161/CIRCRESAHA.114.301763Search in Google Scholar PubMed

61. Fujita Y, Yamaguchi S, Kakino A, Iwamoto S, Yoshimoto R, Sawamura T. Lectin-like oxidized LDL receptor 1 is involved in CRP-mediated complement activation. Clin Chem 2011;57:1398–405.10.1373/clinchem.2011.168625Search in Google Scholar PubMed

62. Zhao XQ, Zhang MW, Wang F, Zhao YX, Li JJ, Wang XP, et al. CRP enhances soluble LOX-1 release from macrophages by activating TNF-alpha converting enzyme. J Lipid Res 2011;52:923–33.10.1194/jlr.M015156Search in Google Scholar PubMed PubMed Central

63. Li L, Roumeliotis N, Sawamura T, Renier G. C-reactive protein enhances LOX-1 expression in human aortic endothelial cells: relevance of LOX-1 to C-reactive protein-induced endothelial dysfunction. Circ Res 2004;95:877–83.10.1161/01.RES.0000147309.54227.42Search in Google Scholar

64. Singh U, Dasu MR, Yancey PG, Afify A, Devaraj S, Jialal I. Human C-reactive protein promotes oxidized low density lipoprotein uptake and matrix metalloproteinase-9 release in Wistar rats. J Lipid Res 2008;49:1015–23.10.1194/jlr.M700535-JLR200Search in Google Scholar

65. Eisenhardt SU, Starke J, Thiele JR, Murphy A, Bjorn Stark G, Bassler N, et al. Pentameric CRP attenuates inflammatory effects of mmLDL by inhibiting mmLDL – monocyte interactions. Atherosclerosis 2012;224:384–93.10.1016/j.atherosclerosis.2012.07.039Search in Google Scholar

66. Schwedler SB, Hansen-Hagge T, Reichert M, Schmiedeke D, Schneider R, Galle J, et al. Monomeric C-reactive protein decreases acetylated LDL uptake in human endothelial cells. Clin Chem 2009;55:1728–31.10.1373/clinchem.2009.125732Search in Google Scholar

67. Kobayashi K, Kishi M, Atsumi T, Bertolaccini ML, Makino H, Sakairi N, et al. Circulating oxidized LDL forms complexes with beta2-glycoprotein I: implication as an atherogenic autoantigen. J Lipid Res 2003;44:716–26.10.1194/jlr.M200329-JLR200Search in Google Scholar

68. Lin KY, Pan JP, Yang DL, Huang KT, Chang MS, Ding PY, et al. Evidence for inhibition of low density lipoprotein oxidation and cholesterol accumulation by apolipoprotein H (beta2-glycoprotein I). Life Sci 2001;69:707–19.10.1016/S0024-3205(01)01164-XSearch in Google Scholar

69. Zhang R, Zhou SJ, Li CJ, Wang XN, Tang YZ, Chen R, et al. C-reactive protein/oxidised low-density lipoprotein/beta2-glycoprotein I complex promotes atherosclerosis in diabetic BALB/c mice via p38mitogen-activated protein kinase signal pathway. Lipids Health Dis 2013;12:42.10.1186/1476-511X-12-42Search in Google Scholar PubMed PubMed Central

70. Tabuchi M, Inoue K, Usui-Kataoka H, Kobayashi K, Teramoto M, Takasugi K, et al. The association of C-reactive protein with an oxidative metabolite of LDL and its implication in atherosclerosis. J Lipid Res 2007;48:768–81.10.1194/jlr.M600414-JLR200Search in Google Scholar PubMed

71. Ueba T, Nomura S, Nishikawa T, Kajiwara M, Yamashita K. Circulating oxidized LDL, measured with FOH1a/DLH3 antibody, is associated with metabolic syndrome and the coronary heart disease risk score in healthy Japanese. Atherosclerosis 2009;203:243–8.10.1016/j.atherosclerosis.2008.05.048Search in Google Scholar PubMed

72. Zuliani G, Morieri ML, Volpato S, Vigna GB, Tch CB, Maggio M, et al. Determinants and clinical significance of plasma oxidized LDLs in older individuals. A 9 years follow-up study. Atherosclerosis 2013;226:201–7.10.1016/j.atherosclerosis.2012.10.028Search in Google Scholar PubMed PubMed Central

73. Tsimikas S, Kiechl S, Willeit J, Mayr M, Miller ER, Kronenberg F, et al. Oxidized phospholipids predict the presence and progression of carotid and femoral atherosclerosis and symptomatic cardiovascular disease: five-year prospective results from the Bruneck study. J Am Coll Cardiol 2006;47:2219–28.10.1016/j.jacc.2006.03.001Search in Google Scholar PubMed

74. Langlois MR, Rietzschel ER, De Buyzere ML, De Bacquer D, Bekaert S, Blaton V, et al. Femoral plaques confound the association of circulating oxidized low-density lipoprotein with carotid atherosclerosis in a general population aged 35–55 years: the Asklepios Study. Arterioscler Thromb Vasc Biol 2008;28:1563–8.10.1161/ATVBAHA.108.167346Search in Google Scholar PubMed

75. Park S, Kim M, Paik JK, Jang YJ, Lee SH, Lee JH. Oxidative stress is associated with C-reactive protein in nondiabetic postmenopausal women, independent of obesity and insulin resistance. Clin Endocrinol (Oxf) 2013;79:65–70.10.1111/j.1365-2265.2012.04512.xSearch in Google Scholar PubMed

76. van Tits LJ, van Himbergen TM, Lemmers HL, de Graaf J, Stalenhoef AF. Proportion of oxidized LDL relative to plasma apolipoprotein B does not change during statin therapy in patients with heterozygous familial hypercholesterolemia. Atherosclerosis 2006;185:307–12.10.1016/j.atherosclerosis.2005.06.006Search in Google Scholar PubMed

77. Rodenburg J, Vissers MN, Wiegman A, Miller ER, Ridker PM, Witztum JL, et al. Oxidized low-density lipoprotein in children with familial hypercholesterolemia and unaffected siblings: effect of pravastatin. J Am Coll Cardiol 2006;47:1803–10.10.1016/j.jacc.2005.12.047Search in Google Scholar PubMed

78. Holvoet P, Harris TB, Tracy RP, Verhamme P, Newman AB, Rubin SM, et al. Association of high coronary heart disease risk status with circulating oxidized LDL in the well-functioning elderly: findings from the Health, Aging, and Body Composition study. Arterioscler Thromb Vasc Biol 2003;23:1444–8.10.1161/01.ATV.0000080379.05071.22Search in Google Scholar PubMed

79. Fujii H, Shimizu M, Ino H, Yamaguchi M, Terai H, Mabuchi H, et al. Oxidative stress correlates with left ventricular volume after acute myocardial infarction. Jpn Heart J 2002;43:203–9.10.1536/jhj.43.203Search in Google Scholar PubMed

80. Fraley AE, Schwartz GG, Olsson AG, Kinlay S, Szarek M, Rifai N, et al. Relationship of oxidized phospholipids and biomarkers of oxidized low-density lipoprotein with cardiovascular risk factors, inflammatory biomarkers, and effect of statin therapy in patients with acute coronary syndromes: results from the MIRACL (Myocardial Ischemia Reduction With Aggressive Cholesterol Lowering) trial. J Am Coll Cardiol 2009;53:2186–96.10.1016/j.jacc.2009.02.041Search in Google Scholar PubMed

81. Holvoet P, Vanhaecke J, Janssens S, Van de Werf F, Collen D. Oxidized LDL and malondialdehyde-modified LDL in patients with acute coronary syndromes and stable coronary artery disease. Circulation 1998;98:1487–94.10.1161/01.CIR.98.15.1487Search in Google Scholar

82. Johnston N, Jernberg T, Lagerqvist B, Siegbahn A, Wallentin L. Oxidized low-density lipoprotein as a predictor of outcome in patients with unstable coronary artery disease. Int J Cardiol 2006;113:167–73.10.1016/j.ijcard.2005.11.006Search in Google Scholar PubMed

83. Tsimikas S, Brilakis ES, Miller ER, McConnell JP, Lennon RJ, Kornman KS, et al. Oxidized phospholipids, Lp(a) lipoprotein, and coronary artery disease. N Engl J Med 2005;353:46–57.10.1056/NEJMoa043175Search in Google Scholar PubMed

84. Tsimikas S, Witztum JL, Miller ER, Sasiela WJ, Szarek M, Olsson AG, et al. 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;110:1406–12.10.1161/01.CIR.0000141728.23033.B5Search in Google Scholar PubMed

85. Wu T, Willett WC, Rifai N, Shai I, Manson JE, Rimm EB. Is plasma oxidized low-density lipoprotein, measured with the widely used antibody 4E6, an independent predictor of coronary heart disease among U.S. men and women? J Am Coll Cardiol 2006;48:973–9.10.1016/j.jacc.2006.03.057Search in Google Scholar PubMed

86. Meisinger C, Baumert J, Khuseyinova N, Loewel H, Koenig W. Plasma oxidized low-density lipoprotein, a strong predictor for acute coronary heart disease events in apparently healthy, middle-aged men from the general population. Circulation 2005;112:651–7.10.1161/CIRCULATIONAHA.104.529297Search in Google Scholar PubMed

87. Huang Y, Wu Y, Hu Y. Correlation of oxidized low-density lipoprotein and C-reactive protein in patients with coronary artery disease. Cell Biochem Biophys 2013;65:285–6.10.1007/s12013-012-9409-3Search in Google Scholar PubMed

88. Tsimikas S, Willerson JT, Ridker PM. C-reactive protein and other emerging blood biomarkers to optimize risk stratification of vulnerable patients. J Am Coll Cardiol 2006;47:C19–31.10.1016/j.jacc.2005.10.066Search in Google Scholar PubMed

Received: 2014-6-3
Accepted: 2014-6-19
Published Online: 2014-7-10
Published in Print: 2015-1-1

©2015 by De Gruyter

Downloaded on 29.3.2024 from https://www.degruyter.com/document/doi/10.1515/cclm-2014-0590/html
Scroll to top button