Circulating autoantibodies against the apolipoprotein B-100 peptides p45 and p210 in relation to the occurrence of carotid plaques in 64-year-old women

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Fagerberg, Björn ^a   Gullberg, Ulrica Prahl ^a   Alm, Ragnar ^b   Nilsson, Jan ^b   Fredrikson, Gunilla Nordin ^b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A1; APOLIPOPROTEIN B; APOLIPOPROTEIN B100; APOLIPOPROTEIN B100 P210; APOLIPOPROTEIN B100 P45; AUTOANTIBODY; HEMOGLOBIN A1C; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; MALONALDEHYDE; OXIDIZED LOW DENSITY LIPOPROTEIN; UNCLASSIFIED DRUG; APOLIPOPROTEIN B-100 (661-680), HUMAN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; PEPTIDE FRAGMENT;

ADULT; ANTIBODY BLOOD LEVEL; ARTICLE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CAROTID ARTERY; CAROTID ATHEROSCLEROSIS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIABETES MELLITUS; DISEASE ASSOCIATION; ECHOGRAPHY; FEMALE; GLUCOSE TOLERANCE; HUMAN; IMMUNOASSAY; IMMUNOGLOBULIN BLOOD LEVEL; INCIDENCE; MAJOR CLINICAL STUDY; MIDDLE AGED; PROTEIN BLOOD LEVEL; RISK ASSESSMENT; SMOKING; SYSTOLIC BLOOD PRESSURE; BLOOD; CAROTID ARTERY OBSTRUCTION; COHORT ANALYSIS; DIAGNOSTIC IMAGING; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOLOGY; NONPARAMETRIC TEST; ODDS RATIO;

APOLIPOPROTEIN B-100; AUTOANTIBODIES; CAROTID STENOSIS; COHORT STUDIES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MIDDLE AGED; ODDS RATIO; PEPTIDE FRAGMENTS; STATISTICS, NONPARAMETRIC; ULTRASONOGRAPHY;

EID: 84929492961     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120744     Document Type: Article

References (44)

1. Nilsson J, Hansson GK. Autoimmunity in atherosclerosis: a protective response losing control? J Intern Med. 2008;263(5):464-78. doi: 10.1111/j.1365-2796.2008.01945.x PMID: 18410590
2. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol. 2011;12(3):204-12. doi: 10.1038/ni.2001 PMID: 21321594
3. Palinski W, Witztum JL. Immune responses to oxidative neoepitopes on LDL and phospholipids modulate the development of atherosclerosis. J Intern Med. 2000;247(3):371-80. PMID: 10762454
4. Frostegard J, Wu R, Giscombe R, Holm G, Lefvert AK, Nilsson J. Induction of T-cell activation by oxidized low density lipoprotein. Arterioscler Thromb. 1992;12(4):461-7. PMID: 1558837
5. Yla-Herttuala S, Palinski W, Butler SW, Picard S, Steinberg D, Witztum JL. Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LDL. Arterioscler Thromb. 1994;14(1):32-40. PMID: 7506053
6. Stemme S, Faber B, Holm J, Wiklund O, Witztum JL, Hansson GK. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc Natl Acad Sci U S A. 1995;92(9):3893-7. PMID: 7732003
7. Gupta S, Pablo AM, Jiang X, Wang N, Tall AR, Schindler C. IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest. 1997;99(11):2752-61. PMID: 9169506
8. Buono C, Binder CJ, Stavrakis G, Witztum JL, Glimcher LH, Lichtman AH. T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses. Proc Natl Acad Sci U S A. 2005;102(5):1596-601. PMID: 15665085
9. Palinski W, Miller E, Witztum JL. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc Natl Acad Sci U S A. 1995;92(3):821-5. PMID: 7846059
10. Ameli S, Hultgardh-Nilsson A, Regnstrom J, Calara F, Yano J, Cercek B, et al. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arterioscler Thromb Vasc Biol. 1996;16(8):1074-9. PMID: 8696949
11. Fredrikson GN, Andersson L, Soderberg I, Dimayuga P, Chyu K-Y, Shah PK, et al. Atheroprotective immunization with MDA-modified apo B-100 peptide sequence is associated with activation of Th2 specific antibody expression. Autoimmunity. 2005;38(2):171-9. PMID: 16040338
12. Fredrikson GN, Bjorkbacka H, Soderberg I, Ljungcrantz I, Nilsson J. Treatment with apo B peptide vaccines inhibits atherosclerosis in human apo B-100 transgenic mice without inducing an increase in peptidespecific antibodies. J Intern Med. 2008;264(6):563-70. doi: 10.1111/j.1365-2796.2008.01995.x PMID: 18783480
13. Fredrikson GN, Söderberg I, Lindholm M, Dimayuga P, Chyu K-Y, Shah PK, et al. Inhibition of atherosclerosis in apoE-null mice by immunization with apoB-100 peptide sequences. Arterioscler Thromb Vasc Biol. 2003;23:879-84. PMID: 12649092
14. Nilsson J, Hansson GK, Shah PK. Immunomodulation of atherosclerosis: implications for vaccine development. Arterioscler Thromb Vasc Biol. 2005;25(1):18-28. PMID: 15514204
15. Fredrikson GN, Hedblad B, Berglund G, Alm R, Ares M, Cercek B, et al. Identification of immune responses against aldehyde-modified peptide sequences in apoB associated with cardiovascular disease. Arterioscler Thromb Vasc Biol. 2003;23:872-8. PMID: 12649091
16. Fredrikson GN, Schiopu A, Berglund G, Alm R, Shah P, Nilsson J. Autoantibody against the amino acid sequence 661-680 in apoB-100 is associated with decreased carotid stenosis and cardiovascular events. Atherosclerosis. 2007;194:e188-e92. PMID: 17214995
17. Sjogren P, Fredrikson GN, Samnegard A, Ericsson CG, Ohrvik J, Fisher RM, et al. High plasma concentrations of autoantibodies against native peptide 210 of apoB-100 are related to less coronary atherosclerosis and lower risk of myocardial infarction. Eur Heart J. 2008;29(18):2218-26. doi: 10.1093/eurheartj/ehn336 PMID: 18664466
18. Niskanen L, Turpeinen A, Penttila I, Uusitupa MI. Hyperglycemia and compositional lipoprotein abnormalities as predictors of cardiovascular mortality in type 2 diabetes: a 15-year follow-up from the time of diagnosis. Diabetes Care. 1998;21(11):1861-9. PMID: 9802734
19. Brohall G, Oden A, Fagerberg B. Carotid artery intima-media thickness in patients with Type 2 diabetes mellitus and impaired glucose tolerance: a systematic review. Diabet Med. 2006;23(6):609-16. PMID: 16759301
20. Nilsson J, Bengtsson E, Fredrikson GN, Bjorkbacka H. Inflammation and immunity in diabetic vascular complications. Curr Opin Lipidol. 2008;19(5):519-24. doi: 10.1097/MOL.0b013e32830f47cd PMID: 18769234
21. Fredrikson GN, Anand DV, Hopkins D, Corder R, Alm R, Bengtsson E, et al. Associations between autoantibodies against apo B-100 peptides and vascular complications in patients with type 2 diabetes. Diabetologia. 2009;52:1426-33. doi: 10.1007/s00125-009-1377-9 PMID: 19448981
22. Engelbertsen D, Anand DV, Fredrikson GN, Hopkins D, Corder R, Shah PK, et al. High levels of IgM against methylglyoxal-modified apolipoprotein B100 are associated with less coronary artery calcification in patients with type 2 diabetes. J Intern Med. 2012;271(1):82-9. doi: 10.1111/j.1365-2796.2011. 02411.x PMID: 21668821
23. Brohall G, Behre CJ, Hulthe J, Wikstrand J, Fagerberg B. Prevalence of diabetes and impaired glucose tolerance in 64-year-old Swedish women: experiences of using repeated oral glucose tolerance tests. Diabetes Care. 2006;29(2):363-7. PMID: 16443888
24. Prahl U, Wikstrand J, Bergstrom GM, Behre CJ, Hulthe J, Fagerberg B. Slightly elevated highsensitivity C-reactive protein (hsCRP) concentrations are associated with carotid atherosclerosis in women with varying degrees of glucose tolerance. Angiology. 2010;61(8):793-801. doi: 10.1177/0003319710370959 PMID: 20547540
25. Behre CJ, Brohall G, Hulthe J, Wikstrand J, Fagerberg B. Are serum adiponectin concentrations in a population sample of 64-year-old Caucasian women with varying glucose tolerance associated with ultrasoundassessed atherosclerosis? J Intern Med. 2006;260(3):238-44. PMID: 16918821
26. Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med. 1998;15(7):539-53. PMID: 9686693
27. Prahl U, Holdfeldt P, Bergstrom G, Fagerberg B, Hulthe J, Gustavsson T. Percentage white: a new feature for ultrasound classification of plaque echogenicity in carotid artery atherosclerosis. Ultrasound Med Biol. 2010;36(2):218-26. doi: 10.1016/j.ultrasmedbio.2009.10.002 PMID: 20018430
28. Brohall G, Schmidt C, Behre CJ, Hulthe J, Wikstrand J, Fagerberg B. Association between impaired glucose tolerance and carotid atherosclerosis: a study in 64-year-old women and a meta-analysis. Nutr Metab Cardiovasc Dis. 2009;19(5):327-33. doi: 10.1016/j.numecd.2008.02.002 PMID: 19097767
29. Sampi M, Veneskoski M, Ukkola O, Kesaniemi YA, Horkko S. High plasma immunoglobulin (Ig) A and low IgG antibody titers to oxidized low-density lipoprotein are associated with markers of glucose metabolism. J Clin Endocrinol Metab. 2010;95(5):2467-75. doi: 10.1210/jc.2009-1858 PMID: 20332251
30. Garrido-Sanchez L, Garcia-Fuentes E, Cardona F, Rojo-Martinez G, Soriguer F, Tinahones FJ. Anti-oxidized LDL antibody levels are reduced in women with hypertension. Eur J Clin Invest. 2009;39(9):800-6. doi: 10.1111/j.1365-2362.2009.02156.x PMID: 19674079
31. Choi SH, Chae A, Miller E, Messig M, Ntanios F, De Maria AN, et al. Relationship between biomarkers of oxidized low-density lipoprotein, statin therapy, quantitative coronary angiography, and atheroma: volume observations from the REVERSAL (Reversal of Atherosclerosis with Aggressive Lipid Lowering) study. J Am Coll Cardiol. 2008;52(1):24-32. doi: 10.1016/j.jacc.2008.02.066 PMID: 18582631
32. Garrido-Sanchez L, Chinchurreta P, Garcia-Fuentes E, Mora M, Tinahones FJ. A higher level of IgM anti-oxidized LDL antibodies is associated with a lower severity of coronary atherosclerosis in patients on statins. Int J Cardiol. 2010;145(2):263-4. doi: 10.1016/j.ijcard.2009.09.472 PMID: 20004986
33. Boullier A, Hamon M, Walters-Laporte E, Martin-Nizart F, Mackereel R, Fruchart JC, et al. Detection of autoantibodies against oxidized low-density lipoproteins and of IgG-bound low density lipoproteins in patients with coronary artery disease. Clin Chim Acta. 1995;238(1):1-10. PMID: 7554289
34. Festa A, Kopp HP, Schernthaner G, Menzel EJ. Autoantibodies to oxidised low density lipoproteins in IDDM are inversely related to metabolic control and microvascular complications. Diabetologia. 1998;41(3):350-6. PMID: 9541177
35. Tornvall P, Waeg G, Nilsson J, Hamsten A, Regnstrom J. Autoantibodies against modified low-density lipoproteins in coronary artery disease. Atherosclerosis. 2003;167(2):347-53. PMID: 12818418
36. Karvonen J, Paivansalo M, Kesaniemi YA, Horkko S. Immunoglobulin M Type of Autoantibodies to Oxidized Low-Density Lipoprotein Has an Inverse Relation to Carotid Artery Atherosclerosis. Circulation. 2003;108:2107-12. PMID: 14530200
37. Goncalves I, Gronholdt M-LM, Soderberg I, Ares MPS, Nordestgaard BG, Bentzon JF, et al. Humoral immune response against defined oxidized LDL antigens reflects structure and disease activity of carotid plaques. Arterioscler Thromb Vasc Biol. 2005;25:1250-5. PMID: 15831809
38. McLeod O, Silveira A, Fredrikson GN, Gertow K, Baldassarre D, Veglia F, et al. Plasma autoantibodies against apolipoprotein B-100 peptide 210 in subclinical atherosclerosis. Atherosclerosis. 2014;232(1):242-8. doi: 10.1016/j.atherosclerosis.2013.11.041 PMID: 24401246
39. Tsimikas S, Brilakis ES, Lennon RJ, Miller ER, Witztum JL, McConnell JP, et al. Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events. J Lipid Res. 2007;48(2):425-33. PMID: 17093289
40. Hulthe J, Bokemark L, Fagerberg B. Antibodies to oxidized LDL in relation to intima-media thickness in carotid and femoral arteries in 58-year-Old subjectively clinically healthy Men. Arterioscler Thromb Vasc Biol. 2001;21(1):101-7. PMID: 11145940
41. Ravandi A, Boekholdt SM, Mallat Z, Talmud PJ, Kastelein JJ, Wareham NJ, et al. Relationship of IgG and IgM autoantibodies and immune complexes to oxidized LDL withmarkers of oxidation and inflammation and cardiovascular events: results from the EPIC-Norfolk Study. J Lipid Res. 2011;52(10):1829-36. doi: 10.1194/jlr. M015776 PMID: 21821825
42. Schiopu A, Bengtsson J, Soderberg I, Janciauskiene S, Lindgren S, Ares MP, et al. Recombinant human antibodies against aldehyde-modified apolipoprotein B-100 peptide sequences inhibit atherosclerosis. Circulation. 2004;110(14):2047-52. PMID: 15451805
43. Lewis MJ, Malik TH, Ehrenstein MR, Boyle JJ, Botto M, Haskard DO. Immunoglobulin M is required for protection against atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation. 2009;120(5):417-26. doi: 10.1161/CIRCULATIONAHA.109.868158 PMID: 19620499
44. Su J, Georgiades A, Wu R, Thulin T, De Faire U, Frostegard J. Antibodies of IgM subclass to phosphorylcholine and oxidized LDL are protective factors for atherosclerosis in patients with hypertension. Atherosclerosis. 2006;188:160-6. PMID: 16307748