Human monoclonal Fab and human plasma antibodies to carbamyl-epitopes cross-react with malondialdehyde-adducts

Immunology

Volumn 141, Issue 3, 2014, Pages 416-430

  Kummu, Outi ^a,b,c   Turunen, S Pauliina ^a,b,c   Prus, Piotr ^a   Lehtimäki, Jaakko ^a,b   Veneskoski, Marja ^a,b   Wang, Chunguang ^a,b   Hörkkö, Sohvi ^a,b,c  

^a UNIVERSITY OF OULU   (Finland)

^b MEDICAL RESEARCH CENTER OULU   (Finland)

^c OULU UNIVERSITY HOSPITAL   (Finland)

Author keywords

Antibody; Atherosclerosis; Carbamylation; Cross reaction; Low density lipoprotein

Indexed keywords

ACETALDEHYDE; CARBAMYL EPITOPES; CROSS REACTING ANTIBODY; EPITOPE; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M ANTIBODY; LOW DENSITY LIPOPROTEIN; MALONALDEHYDE; MALONDIALDEHYDE ACETALDEHYDE; UNCLASSIFIED DRUG;

ADULT; ANTIBODY AFFINITY; ANTIGEN BINDING; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BLOOD SAMPLING; CELL CLONE; CHEMOLUMINESCENCE; CONTROLLED STUDY; CROSS REACTION; FLOW CYTOMETRY; HUMAN; HUMAN EXPERIMENT; IMMUNOHISTOCHEMISTRY; LEUKEMIA CELL LINE; NORMAL HUMAN; OXIDATION; PERIPHERAL LYMPHOCYTE; PHAGE DISPLAY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ISOLATION; PROTEIN MODIFICATION; STEADY STATE; SURFACE PLASMON RESONANCE; T LYMPHOCYTE; UREMIA; YOUNG ADULT;

ANTIBODY; ATHEROSCLEROSIS; CARBAMYLATION; CROSS-REACTION; LOW-DENSITY LIPOPROTEIN;

ACETALDEHYDE; ANIMALS; ANTIBODIES, MONOCLONAL; APOPTOSIS; ATHEROSCLEROSIS; AUTOANTIBODIES; BINDING, COMPETITIVE; CELL SURFACE DISPLAY TECHNIQUES; CROSS REACTIONS; DISEASE MODELS, ANIMAL; EPITOPES; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULIN FAB FRAGMENTS; JURKAT CELLS; LIPOPROTEINS, LDL; MACROPHAGES; MALONDIALDEHYDE; MICE; OXIDATION-REDUCTION; T-LYMPHOCYTES;

EID: 84893584147     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12204     Document Type: Article

References (64)

1. Hörkkö S, Binder CJ, Shaw PX, Chang MK, Silverman G, Palinski W, Witztum JL. Immunological responses to oxidized LDL. Free Radic Biol Med 2000; 28:1771-9.
2. Karvonen J, Päivänsalo M, Kesäniemi YA, Hörkkö S. Immunoglobulin M type of autoantibodies to oxidized low-density lipoprotein has an inverse relation to carotid artery atherosclerosis. Circulation 2003; 108:2107-12.
3. 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.
4. Carrero JJ, Hua X, Stenvinkel P, Qureshi AR, Heimburger O, Barany P, Lindholm B, Frostegard J. Low levels of IgM antibodies against phosphorylcholine-A increase mortality risk in patients undergoing haemodialysis. Nephrol Dial Transplant 2009; 24:3454-60.
5. Tsimikas S, Willeit P, Willeit J et al. Oxidation-specific biomarkers, prospective 15-year cardiovascular and stroke outcomes, and net reclassification of cardiovascular events. J Am Coll Cardiol 2012; 60:2218-29.
6. Kyaw T, Tay C, Krishnamurthi S, Kanellakis P, Agrotis A, Tipping P, Bobik A, Toh BH. B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ Res 2011; 109:830-40.
7. Binder CJ, Hörkkö S, Dewan A et al. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat Med 2003; 9:736-43.
8. Chang MK, Bergmark C, Laurila A, Hörkkö S, Han KH, Friedman P, Dennis EA, Witztum JL. Monoclonal antibodies against oxidized low-density lipoprotein bind to apoptotic cells and inhibit their phagocytosis by elicited macrophages: evidence that oxidation-specific epitopes mediate macrophage recognition. Proc Natl Acad Sci USA 1999; 96:6353-8.
9. Hörkkö S, Bird DA, Miller E et al. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J Clin Invest 1999; 103:117-28.
10. Salonen JT, Ylä-Herttuala S, Yamamoto R et al. Autoantibody against oxidised LDL and progression of carotid atherosclerosis. Lancet 1992; 339:883-7.
11. Hörkkö S, Savolainen MJ, Kervinen K, Kesäniemi YA. Carbamylation-induced alterations in low-density lipoprotein metabolism. Kidney Int 1992; 41:1175-81.
12. Hörkkö S, Huttunen K, Kervinen K, Kesäniemi YA. Decreased clearance of uraemic and mildly carbamylated low-density lipoprotein. Eur J Clin Invest 1994; 24:105-13.
13. Apostolov EO, Shah SV, Ok E, Basnakian AG. Carbamylated low-density lipoprotein induces monocyte adhesion to endothelial cells through intercellular adhesion molecule-1 and vascular cell adhesion molecule-1. Arterioscler Thromb Vasc Biol 2007; 27:826-32.
14. Trepanier DJ, Thibert RJ. Carbamylation of erythrocyte membrane aminophospholipids: an in vitro and in vivo study. Clin Biochem 1996; 29:333-45.
15. Smith WG, Holden M, Benton M, Brown CB. Carbamylated haemoglobin in chronic renal failure. Clin Chim Acta 1988; 178:297-303.
16. Oimomi M, Hatanaka H, Yoshimura Y, Yokono K, Baba S, Taketomi Y. Carbamylation of insulin and its biological activity. Nephron 1987; 46:63-6.
17. Kraus LM, Kraus AP Jr. Carbamoylation of amino acids and proteins in uremia. Kidney Int Suppl 2001; 78:S102-7.
18. Berlyne GM. Carbamylated proteins and peptides in health and in uremia. Nephron 1998; 79:125-30.
19. Koeth RA, Kalantar-Zadeh K, Wang Z, Fu X, Tang WH, Hazen SL. Protein carbamylation predicts mortality in ESRD. J Am Soc Nephrol 2013; 24:853-61.
20. Berg AH, Drechsler C, Wenger J et al. Carbamylation of serum albumin as a risk factor for mortality in patients with kidney failure. Sci Transl Med 2013; 5:175ra29.
21. Wang Z, Nicholls SJ, Rodriguez ER et al. Protein carbamylation links inflammation, smoking, uremia and atherogenesis. Nat Med 2007; 13:1176-84.
22. -/- mice and bind plasma autoantibodies in humans under enhanced carbamylation. Antioxid Redox Signal 2013; 19:1047-62.
23. Apostolov EO, Shah SV, Ok E, Basnakian AG. Quantification of carbamylated LDL in human sera by a new sandwich ELISA. Clin Chem 2005; 51:719-28.
24. Bevan RJ, Durand MF, Hickenbotham PT et al. Validation of a novel ELISA for measurement of MDA-LDL in human plasma. Free Radic Biol Med 2003; 35:517-27.
25. Yamazaki K, Bujo H, Taira K, Itou N, Shibasaki M, Takahashi K, Saito Y. Increased circulating malondialdehyde-modified LDL in the patients with familial combined hyperlipidemia and its relation with the hepatic lipase activity. Atherosclerosis 2004; 172:181-7.
26. Miyazaki T, Shimada K, Sato O et al. Circulating malondialdehyde-modified LDL and atherogenic lipoprotein profiles measured by nuclear magnetic resonance spectroscopy in patients with coronary artery disease. Atherosclerosis 2005; 179:139-45.
27. Havel RJ, Eder HA, Bragdon JH. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest 1955; 34:1345-53.
28. Habeeb AF. Determination of free amino groups in proteins by trinitrobenzenesulfonic acid. Anal Biochem 1966; 14:328-36.
29. Turunen SP, Kummu O, Harila K, Veneskoski M, Soliymani R, Baumann M, Pussinen PJ, Hörkkö S. Recognition of Porphyromonas gingivalis gingipain epitopes by natural IgM binding to malondialdehyde modified low-density lipoprotein. PLoS ONE 2012; 7:e34910.
30. Andris-Widhopf J, Steinberger P, Fuller R, Rader C, Barbas CF 3rd. Generation of antibody libraries: PCR amplification and assembly of light- and heavy-chain coding sequences. In: Barbas CF3rd, Burton DR, Scott JK, Silverman GJ, eds. Phage Display: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press, 2001:9.1-9.113.
31. Brochet X, Lefranc MP, Giudicelli V. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res 2008; 36:W503-8.
32. Giudicelli V, Brochet X, Lefranc MP. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb Protoc 2011; 2011:695-715.
33. Wang C, Turunen SP, Kummu O, Veneskoski M, Lehtimäki J, Nissinen AE, Hörkkö S. Natural antibodies of newborns recognize oxidative stress-related malondialdehyde acetaldehyde adducts on apoptotic cells and atherosclerotic plaques. Int Immunol 2013; 25:575-87.
34. Veneskoski M, Turunen SP, Kummu O, Nissinen A, Rannikko S, Levonen AL, Hörkkö S. Specific recognition of malondialdehyde and malondialdehyde acetaldehyde adducts on oxidized LDL and apoptotic cells by complement anaphylatoxin C3a. Free Radic Biol Med 2011; 51:834-43.
35. Yamaguchi Y, Kunitomo M, Haginaka J. Assay methods of modified lipoproteins in plasma. J Chromatogr B Analyt Technol Biomed Life Sci 2002; 781:313-30.
36. Steinbrecher UP, Fisher M, Witztum JL, Curtiss LK. Immunogenicity of homologous low density lipoprotein after methylation, ethylation, acetylation, or carbamylation: generation of antibodies specific for derivatized lysine. J Lipid Res 1984; 25:1109-16.
37. Gonen B, Fallon JJ, Baker SA. Immunogenicity of malondialdehyde-modified low density lipoproteins. studies with monoclonal antibodies. Atherosclerosis 1987; 65:265-72.
38. Freigang S, Hörkkö S, Miller E, Witztum JL, Palinski W. Immunization of LDL receptor-deficient mice with homologous malondialdehyde-modified and native LDL reduces progression of atherosclerosis by mechanisms other than induction of high titers of antibodies to oxidative neoepitopes. Arterioscler Thromb Vasc Biol 1998; 18:1972-82.
39. Stark GR, Stein WH, Moore S. Reactions of the cyanate present in aqueous urea with amino acids and proteins. J Biol Chem 1960; 235:3177-81.
40. Stark GR. Reactions of cyanate with functional groups of proteins. 3. Reactions with amino and carboxyl groups. Biochemistry 1965; 4:1030-6.
41. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991; 11:81-128.
42. Tuma DJ, Thiele GM, Xu D, Klassen LW, Sorrell MF. Acetaldehyde and malondialdehyde react together to generate distinct protein adducts in the liver during long-term ethanol administration. Hepatology 1996; 23:872-80.
43. Tuma DJ, Kearley ML, Thiele GM, Worrall S, Haver A, Klassen LW, Sorrell MF. Elucidation of reaction scheme describing malondialdehyde-acetaldehyde-protein adduct formation. Chem Res Toxicol 2001; 14:822-32.
44. Palinski W, Hörkkö S, Miller E, Steinbrecher UP, Powell HC, Curtiss LK, Witztum JL. Cloning of monoclonal autoantibodies to epitopes of oxidized lipoproteins from apolipoprotein E-deficient mice. Demonstration of epitopes of oxidized low density lipoprotein in human plasma. J Clin Invest 1996; 98:800-14.
45. Shi J, Knevel R, Suwannalai P et al. Autoantibodies recognizing carbamylated proteins are present in sera of patients with rheumatoid arthritis and predict joint damage. Proc Natl Acad Sci USA 2011; 108:17372-7.
46. Shi J, van de Stadt LA, Levarht EW, Huizinga TW, Toes RE, Trouw LA, van Schaardenburg D. Anti-carbamylated protein antibodies are present in arthralgia patients and predict the development of rheumatoid arthritis. Arthritis Rheum 2013; 65:911-5.
47. Lindner A, Charra B, Sherrard DJ, Scribner BH. Accelerated atherosclerosis in prolonged maintenance hemodialysis. N Engl J Med 1974; 290:697-701.
48. Apostolov EO, Basnakian AG, Ok E, Shah SV. Carbamylated low-density lipoprotein: nontraditional risk factor for cardiovascular events in patients with chronic kidney disease. J Ren Nutr 2012; 22:134-8.
49. del Rincon ID, Williams K, Stern MP, Freeman GL, Escalante A. High incidence of cardiovascular events in a rheumatoid arthritis cohort not explained by traditional cardiac risk factors. Arthritis Rheum 2001; 44:2737-45.
50. Solomon DH, Goodson NJ, Katz JN, Weinblatt ME, Avorn J, Setoguchi S, Canning C, Schneeweiss S. Patterns of cardiovascular risk in rheumatoid arthritis. Ann Rheum Dis 2006; 65:1608-12.
51. Trouw LA, Huizinga TW, Toes RE. Autoimmunity in rheumatoid arthritis: different antigens - common principles. Ann Rheum Dis 2013; 72(Suppl. 2):ii132-6.
52. Sokolove J, Sharpe O, Brennan M et al. Citrullination within the atherosclerotic plaque: a potential target for the anti-citrullinated protein antibody response in rheumatoid arthritis. Arthritis Rheum 2013; 65:1719-24.
53. Bellazzi R, Maggi E, Bellomo G et al. Low-density lipoprotein oxidation and antioxidized LDL antibodies in peritoneal dialysis patients. Adv Perit Dial 1993; 9:312-7.
54. Maggi E, Bellazzi R, Falaschi F et al. Enhanced LDL oxidation in uremic patients: an additional mechanism for accelerated atherosclerosis? Kidney Int 1994; 45:876-83.
55. Maggi E, Bellazzi R, Gazo A, Seccia M, Bellomo G. Autoantibodies against oxidatively-modified LDL in uremic patients undergoing dialysis. Kidney Int 1994; 46:869-76.
56. Maggi E, Chiesa R, Melissano G, Castellano R, Astore D, Grossi A, Finardi G, Bellomo G. LDL oxidation in patients with severe carotid atherosclerosis. A study of in vitro and in vivo oxidation markers. Arterioscler Thromb 1994; 14:1892-9.
57. Lopes-Virella MF, Virella G, Orchard TJ, Koskinen S, Evans RW, Becker DJ, Forrest KY. Antibodies to oxidized LDL and LDL-containing immune complexes as risk factors for coronary artery disease in diabetes mellitus. Clin Immunol 1999; 90:165-72.
58. Tuominen A, Miller YI, Hansen LF, Kesäniemi YA, Witztum JL, Hörkkö S. A natural antibody to oxidized cardiolipin binds to oxidized low-density lipoprotein, apoptotic cells, and atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2006; 26:2096-102.
59. Manson JJ, Mauri C, Ehrenstein MR. Natural serum IgM maintains immunological homeostasis and prevents autoimmunity. Springer Semin Immunopathol 2005; 26:425-32.
60. Binder CJ. Natural IgM antibodies against oxidation-specific epitopes. J Clin Immunol 2010; 30(Suppl. 1):S56-60.
61. Kaveri SV, Silverman GJ, Bayry J. Natural IgM in immune equilibrium and harnessing their therapeutic potential. J Immunol 2012; 188:939-45.
62. Kim SJ, Gershov D, Ma X, Brot N, Elkon KB. I-PLA(2) activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J Exp Med 2002; 196:655-65.
63. Shaw PX, Hörkkö S, Tsimikas S, Chang MK, Palinski W, Silverman GJ, Chen PP, Witztum JL. Human-derived anti-oxidized LDL autoantibody blocks uptake of oxidized LDL by macrophages and localizes to atherosclerotic lesions in vivo. Arterioscler Thromb Vasc Biol 2001; 21:1333-9.
64. Jeon YE, Seo CW, Yu ES, Lee CJ, Park SG, Jang YJ. Characterization of human monoclonal autoantibody Fab fragments against oxidized LDL. Mol Immunol 2007; 44:827-36.