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Review

Advanced oxidation protein products (AOPP): novel uremic toxins, or components of the non-enzymatic antioxidant system of the plasma proteome?

Pages 1115-1123 | Received 05 May 2011, Accepted 23 Jun 2011, Published online: 15 Jul 2011

References

  • Witko-Sarsat V, Friedlander M, Capeillère-Blandin C, Nguyen-Khoa T, Nguyen AT, Zingraff J, . Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney Int 1996;49:1304–1313.
  • Witko V, Nguyen AT, Descamps-Latscha B. Microtiter plate assay for phagocyte-derived taurine-chloramines. J Clin Lab Anal 1992;6:47–53.
  • Capeillère-Blandin C, Gausson V, Descamps-Latscha B, Witko-Sarsat V. Biochemical and spectrophotometric significance of advanced oxidized protein products. Biochim Biophys Acta 2004;1689:91–102.
  • Matteucci E, Biasci E, Giampietro O. Advanced oxidation protein products in plasma: stability during storage and correlations with other clinical characteristics. Acta Diabetol 2001;38:187–189.
  • Buonocore G, Perrone S, Longini M, Terzuoli L, Bracci R. Total hydroperoxide and advanced oxidation protein products in preterm hypoxic babies. Pediatr Res 2000;47:221–224.
  • Kaneda H, Taguchi J, Ogasawara K, Aizawa T, Ohno M. Increased level of advanced oxidation protein products in patients with coronary artery disease. Atherosclerosis 2002; 162:221–225.
  • Kalousova M, Skrha J, Zima T. Advanced glycation end- products and advanced oxidation protein products in patients with diabetes mellitus. Physiol Res 2002;51:597–604.
  • Martin-Gallan P, Carrascosa A, Gussinye M, Dominguez C. Biomarkers of diabetes-associated oxidative stress and antioxidant status in young diabetic patients with or without subclinical complications. Free Radic Biol Med 2003;34: 1563–1574.
  • Piwowar A, Knapik-Kordecka M, Warwas M. Markers of oxidative protein damage in plasma and urine of type 2 diabetic patients. Br J Biomed Sci 2009;66:194–199.
  • Allanore Y, Borderie D, Lemarechal H, Ekindjian OG, Kahan A. Acute and sustained effects of dihydropyridine-type calcium channel antagonists on oxidative stress in systemic sclerosis. Am J Med 2004;116:595–600.
  • Yazici C, Köse K, Calis M, Kuzugüden S, Kirnap M. Protein oxidation status in patients with ankylosing spondylitis. Rheumatology (Oxford) 2004;43:1235–1239.
  • Yazici C, Köse K, Calis M, Demir M, Kirnap M, Ates F. Increased advanced oxidation protein products in Behçet's disease: a new activity marker? Br J Dermatol 2004;151: 105–111.
  • Selmeci L, Seres L, Antal M, Lukács J, Regöly-Mérei A, Acsády G. Advanced oxidation protein products (AOPP) for monitoring oxidative stress in critically ill patients: a simple, fast and inexpensive automated technique. Clin Chem Lab Med 2005;43:294–297.
  • Chiu-Braga YY, Hayashi SY, Schafranski M, Messias-Reason IJ. Further evidence of inflammation in chronic rheumatic valve disease (CRVD): high levels of advanced oxidation protein products (AOPP) and high sensitive C-reactive protein (hs-CRP). Int J Cardiol 2006;109: 275–276.
  • Fialova L, Malbohan I, Kalousova M, Soukupova J, Krofta L, Stipek S, Zima T. Oxidative stress and inflammation in pregnancy. Scand J Clin Lab Invest 2006;66:121–127.
  • Chang D, Wang F, Zhao YS, Pan HZ. Evaluation of oxidative stress in colorectal cancer patients. Biomed Environ Sci 2008; 21:286–289.
  • Zhou FL, Zhang WG, Wei YC, Meng S, Bai GG, Wang BY, . Involvement of oxidative stress in the relapse of acute myeloid leukemia. J Biol Chem 2010;285: 15010–15015.
  • Witko-Sarsat V, Nguyen-Khoa T, Jungers P, Drüeke TB, Descamps-Latscha B. Advanced oxidation protein products as a novel molecular basis of oxidative stress in uraemia. Nephrol Dial Transplant 1999;14(Suppl 1):76–78.
  • Valli A, Suliman ME, Meert N, Vanholder R, Lindholm B, Stenvinkel P, . Overestimation of advanced oxidation protein products in uremic plasma due to presence of triglycerides and other endogenous factors. Clin Chim Acta 2007; 379:87–94.
  • Anderstam B, Ann-Christin BH, Valli A, Stenvinkel P, Lindholm B, Suliman ME. Modification of the oxidative stress biomarker AOPP assay: application in uremic samples. Clin Chim Acta 2008;393:114–118.
  • Halliwell B, Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol 2004;142: 231–255.
  • Sies H. Oxidative stress: from basic research to clinical application. Am J Med 1991;91:31S–38S.
  • Dean RT, Fu S, Stocker R, Davies MJ. Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 1997;324:1–18.
  • Cloos PA, Christgau S. Non-enzymatic covalent modifications of proteins: mechanisms, physiological consequences and clinical applications. Matrix Biol 2002;21:39–52.
  • Davies MJ. The oxidative environment and protein damage. Biochim Biophys Acta 2005;1703:93–109.
  • Pattison DI, Hawkins CL, Davies MJ. What are the plasma targets of the oxidant hypochlorous acid? A kinetic modeling approach. Chem Res Toxicol 2009;22:807–817.
  • Gutteridge JM. Antioxidant properties of the proteins caeruloplasmin, albumin and transferrin. A study of their activity in serum and synovial fluid from patients with rheumatoid arthritis. Biochim Biophys Acta 1986;869:119–127.
  • Halliwell B. Albumin – an important extracellular antioxidant? Biochem Pharmacol 1988;37:569–571.
  • Halliwell B, Gutteridge JM. The antioxidants of human extracellular fluids. Arch Biochem Biophys 1990;280:1–8.
  • Roche M, Rondeau P, Singh NR, Tarnus E, Bourdon E. The antioxidant properties of serum albumin. FEBS Lett 2008;582:1783–1787.
  • Bourdon E, Blache D. The importance of proteins in defense against oxidation. Antioxid Redox Signal 2001;3:293–311.
  • Bourdon E, Loreau N, Lagrost L, Blache D. Differential effects of cysteine and methionine residues in the antioxidant activity of human seum albumin. Free Radic Res 2005;39: 15–20.
  • Witko-Sarsat V, Descamps-Latscha B. Advanced oxidation protein products: novel uremic toxins and pro-inflammatory mediators in chronic renal failure? Nephrol Dial Transplant 1997;12:1310–1312.
  • Himmelfarb J, McMonagle E, McMenamin E. Plasma protein thiol oxidation and carbonyl formation in chronic renal failure. Kidney Int 2000;58:2571–2578.
  • Himmelfarb J, McMonagle E. Albumin is the major plasma protein target of oxidant stress in uremia. Kidney Int 2001; 60:358–363.
  • Wratten ML, Sereni L, Tetta C. Oxidation of albumin is enhanced in the presence of uremic toxins. Ren Fail 2001;23: 563–571.
  • Anraku M, Kitamura K, Shinohara A, Adachi M, Suenga A, Maruyama T, . Intravenous iron administration induces oxidation of serum albumin in hemodialysis patients. Kidney Int 2004;66:841–848.
  • Mera K, Anraku M, Kitamura K, Nakajou K, Maruyama T, Otagiri M. The structure and function of oxidized albumin in hemodialysis patients: its role in elevated oxidative stress via neutrophil burst. Biochem Biophys Res Commun 2005;334: 1322–1328.
  • Terawaki H, Yoshimura K, Hasegawa T, Matsuyama Y, Negawa T, Yamada K, . Oxidative stress is enhanced in correlation with renal dysfunction: examination with the redox state of albumin. Kidney Int 2004;66:1988–1993.
  • Terawaki H, Nakayama K, Matsuyama Y, Nakayama M, Sato T, Hosoya T, . Dialyzable uremic solutes contribute to enhanced oxidation of serum albumin in regular hemodialysis patients. Blood Purif 2007;25:274–279.
  • Lim PS, Cheng YM, Yang SM. Impairments of the biological properties of serum albumin in patients on hemodialysis. Nephrology (Carlton) 2007;12:18–24.
  • Iwao Y, Anraku M, Hiraike M, Kawai K, Nakajou K, Kai T, . The structural and pharmacokinetic properties of oxidized human serum albumin, advanced oxidation protein products (AOPP). Drug Metab Pharmacokinet 2006;21: 140–146.
  • Pieniazek A, Brzeszczynska J, Kruszynska I, Gwozdzinski K. Investigation of albumin properties in patients with chronic renal failure. Free Radic Res 2009;43:1008–1018.
  • Mezzano D, Pais EO, Aranda E, Panes O, Downey P, Ortiz M, . Inflammation, not hyperhomocysteinemia, is related to oxidative stress and hemostatic and endothelial dysfunction in uremia. Kidney Int 2001;60:1844–1850.
  • Morena M, Cristol JP, Bosc JY, Tetta C, Forret G, Leger CL, . Convective and diffusive losses of vitamin C during haemodiafiltration session: a contributive factor to oxidative stress in haemodialysis patients. Nephrol Dial Transplant 2002;17:422–427.
  • Kalousova M, Zima T, Tesar V, Lachmanova J. Advanced glycation end products and advanced oxidation protein products in hemodialyzed patients. Blood Purif 2002;20: 531–536.
  • Kalousova M, Sulkova S, Fialova L, Soukupova J, Malbohan IM, Spacek P, . Glycoxidation and inflammation in chronic haemodialysis patients. Nephrol Dial Transplant 2003;18:2577–2581.
  • Descamps-Latscha B, Witko-Sarsat V. Oxidative stress in chronic renal failure and hemodialysis. Nephrologie 2003;24: 377–379.
  • Fialova L, Kalousova M, Soukupova J, Sulkova S, Merta M, Jelinkova E, . Relationship of pregnancy-associated plasma protein-a to renal function and dialysis modalities. Kidney Blood Press Res 2004;27:88–95.
  • Wu CC, Chen JS, Wu WM, Liao TN, Chu P, Lin SH, . Myeloperoxidase serves as a marker of oxidative stress during single haemodialysis session using two different biocompatible dialysis membranes. Nephrol Dial Transplant 2005;20: 1134–1139.
  • Rodriguez-Ayala E, Anderstam B, Suliman ME, Seeberger A, Heimbürger O, Lindholm B, Stenvinkel P. Enhanced RAGE-mediated NFkappaB stimulation in inflamed hemodialysis patients. Atherosclerosis 2005;180:333–340.
  • Coskun C, Kural A, Döventas Y, Koldas M, Ozturk H, Inal BB, Gümüs A. Hemodialysis and protein oxidation products. Ann N Y Acad Sci 2007;1100:404–408.
  • Witko-Sarsat V, Friedlander M, Nguyen Khoa T, Capeillère-Blandin C, Nguyen AT, Canteloup S, . Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure. J Immunol 1998;161:2524–2532.
  • Descamps-Latscha B, Witko-Sarsat V. Importance of oxidatively modified proteins in chronic renal failure. Kidney Int Suppl 2001;78:S108–S113.
  • Capeillère-Blandin C, Gausson V, Nguyen AT, Descamps-Latscha B, Drüeke T, Witko-Sarsat V. Respective role of uraemic toxins and myeloperoxidase in the uraemic state. Nephrol Dial Trasplant 2006;21:1555–1563.
  • wao Y, Nakajou K, Nagai R, Kitamura K, Anraku M, Maruyama T, Otagiri M. CD36 is one of important receptors promoting renal tubular injury by advanced oxidation protein products. Am J Physiol Renal Physiol 2008;295: F1871–F1880.
  • Marsche G, Frank S, Hrzenjak A, Holzer M, Dirnberger S, Wadsack C, . Plasma-advanced oxidation protein products are potent high-density lipoprotein receptor antagonists in vivo. Circ Res 2009;104:750–757.
  • Collen D, Tytgat GN, Claeys H, Piessens R. Metabolism and distribution of fibrinogen. I. Fibrinogen turnover in physiological conditions in humans. Br J Haematol 1972;22: 681–700.
  • Herrick S, Blanc-Brude O, Gray A, Laurent G. Fibrinogen. Int J Biochem Cell Biol 1999;31:741–746.
  • Lipinski B, Federman SM, Krolewsky AS. Plasma macromolecular protein complex: interaction with fibrin and fibrinolysis. Thromb Res 1995;78:461–465.
  • Kunitake ST, Carilli CT, Lau K, Protter AA, Naya-Vigne J, Kane JP. Identification of proteins associated with apolipoprotein A-I- containing lipoproteins purified by selected-affinity immunosorption. Biochemistry 1994;33:1988–1993.
  • Ernst A, Helmhold M, Brunner C, Pethö-Schramm A, Armstrong VW, Müller HJ. Identification of two functionally distinct lysine-binding sites in kringle 37 and in kringles 32-36 of human apolipoprotein(a). J Biol Chem 1995;270: 6227–6234.
  • Park CT, Wright SD. Fibrinogen is a component of a novel lipoprotein particle: factor H-related protein (FHRP)-associated lipoprotein particle (FALP). Blood 2000;95: 198–204.
  • Shacter E, Williams JA, Lim M, Levine RL. Differential susceptibility of plasma proteins to oxidative modification: examination by western blot immunoassay. Free Radic Biol Med 1994;17:429–437.
  • Shacter E. Quantification and significance of protein oxidation in biological samples. Drug Metab Rev 2000;32:307–326.
  • Ishida Y, Takiuchi H, Matsushima A, Inada Y. Functional consequences of tryptophan modification in human fibrinogen. Biochim Biophys Acta 1978;536:70–77.
  • Olinescu RM, Kummerow FA. Fibrinogen is an efficient antioxidant. J Nutr Biochem 2001;12:162–169.
  • Abudu N, Miller JJ, Levinson SS. Fibrinogen is a co- antioxidant that supplements the vitamin E analog trolox in a model system. Free Radic Res 2006;40:321–331.
  • Kaplan IV, Attaelmannan M, Levinson SS. Fibrinogen is an antioxidant that protects β-lipoproteins at physiological concentrations in a cell free system. Atherosclerosis 2001;158: 455–463.
  • Schwedler S, Schinzel R, Vaith P, Wanner C. Inflammation and advanced glycation end products in uremia: simple coexistence, potentiation, or causal relationship? Kidney Int Suppl 2001;78:S32–S36.
  • Giordano M, De Feo P, Lucidi P, dePascale E, Giordano G, Infantone L, . Increased albumin and fibrinogen synthesis in hemodialysis patients with normal nutritional status. J Am Soc Nephrol 2001;12:349–354.
  • Kirmizis D, Tsiandoulas A, Pangalou M, Koutoupa E, Rozi P, Protopappa M, Barboutis K. Validity of plasma fibrinogen, D-dimer, and the von Willebrand factor as markers of cardiovascular morbidity in patients on chronic hemodialysis. Med Sci Monit 2006;12:CR55–CR62.
  • Descamps-Latscha B, Witko-Sarsat V, Nguyen-Khoa T, Nguyen AT, Gausson V, Mothu N, . Advanced oxidation protein products as risk factors for atherosclerotic cardiovascular events in nondiabetic predialysis patients. Am J Kidney Dis 2005;45:39–47.
  • Lipinski B, Lipinska I, Kato Y. Is the macromolecular protein complex (MPC) a marker for oxidative stress in diabetes mellitus? Diabetologia 2001;44:1356 (Letter to the editor).
  • Lipinski B. Markers of oxidative stress in uremia. Kidney Int 2004;65:339–340 (Letter to the editor).
  • Selmeci L, Székely M, Soós P, Seres L, Klinga N, Geiger A, Acsády G. Human blood plasma advanced oxidation protein products (AOPP) correlates with fibrinogen levels. Free Radic Res 2006;40:952–958.
  • Lane DA, Ireland H, Knight I, Wolff S, Kyle P, Curtis JR. The significance of fibrinogen derivatives in plasma in human renal failure. Br J Haematol 1984;56:251–260.
  • Kozek-Langenecker SA, Masaki T, Mohammad H, Green W, Mohammad SF, Cheung AK. Fibrinogen fragments and platelet dysfunction in uremia. Kidney Int 1999;56:299–305.
  • Kaplan B, Cojocaru M, Unsworth E, Knecht A, Martin BM. Search for peptidic “middle molecules” in uremic sera: isolation and chemical identification of fibrinogen fragments. J Chromatogr B Analyt Technol Biomed Life Sci 2003;796: 141–153.
  • Thekkedath UR, Chirananthavat T, Leypoldt JK, Cheung AK, Mohammad SF. Elevated fibrinogen fragment levels in uremic plasma inhibit platelet function and expression of glycoprotein IIb-IIIa. Am J Hematol 2006;81:915–926.
  • Korte W, Riesen WF. Comparability of serum and plasma concentrations of haemostasis activation markers. Clin Chem Lab Med 2001;39:627–630.
  • Doolittle RF. The evolution of vertebrate fibrinogen. Fed Proc 1976;35:2145–2149.
  • Weisel JW. Fibrinogen and fibrin. Adv Protein Chem 2005; 70:247–299.
  • Doolittle RF. Coagulation in vertebrates with a focus on evolution and inflammation. J Innate Immun 2011;3: 9–16.
  • Kairies N, Beisel HG, Fuentes-Prior P, Tsuda R, Muta T, Iwanaga S, . The 2.0-A crystal structure of tachylectin 5A provides evidence for the common origin of the innate immunity and the blood coagulation system. Proc Natl Acad Sci USA 2001;98:13519–13524.
  • Henschen-Edman AH. Fibrinogen non-inherited heterogeneity and its relationship to function in health and disease. Ann N Y Acad Sci 2001;936:580–593.
  • Eaton DL, Fless GM, Kohr WJ, McLean JW, Xu QT, Miller CG, . Partial amino acid sequence of apolipoprotein(a) shows that it is homologous to plasminogen. Proc Natl Acad Sci USA 1987;84:3224–3228.
  • McLean JW, Tomlinson JE, Kuang WJ, Eaton DL, Chen EY, Fless GM, . cDNA sequence of human apolipoprotein(a) is homologous to plasminogen. Nature 1987;330:132–137.
  • Lawn RM, Schwartz K, Patthy L. Convergent evolution of apolipoprotein(a) in primates and hedgehog. Proc Natl Acad Sci USA 1997;94:11992–11997.
  • Harpel PC, Gordon BR, Parker TS. Plasmin catalyzes binding of lipoprotein(a) to immobilized fibrinogen and fibrin. Proc Natl Acad Sci USA 1989;86:3847–3851.
  • Selmeci L, Seres L, Soós P, Székely M, Acsády G. Kinetic assay for the determination of the oxidative stress biomarker, advanced oxidation protein products (AOPP) in the human blood plasma. Acta Physiol Hung 2008;95: 209–218.
  • Selmeci L, Seres L, Székely M, Soós P, Acsády G. Assay of oxidized fibrinogen reactivity (OFR) as a biomarker of oxidative stress in human plasma: the role of lysine analogs. Clin Chem Lab Med 2010;48:379–382.
  • Klose R, Fresser F, Kochl S, Parson W, Kapetanopoulos A, Fruchart-Najib J, . Mapping of a minimal apolipoprotein(a) interaction motif conserved in fibrin(ogen) beta- and gamma-chains. J Biol Chem 2000;275:38206–38212.
  • Tsurupa G, Yakovlev S, Pechik I, Lamanuzzi LB, Anglés-Cano E, Medved L. Interaction of fibrin(ogen) with apolipoprotein(a): further characterization and identification of a novel lysine-dependent apolipoprotein(a)-binding site within the gamma chain 287-411 region. Biochemistry 2006; 45:10624–10632.
  • Tsurupa G, Ho-Tin-Noé B, Anglés-Cano E, Medved L. Identification and characterization of novel lysine- independent apolipoprotein(a)-binding sites in fibrin(ogen) α-C-domains. J Biol Chem 2003;278:37154–37159.
  • Yakovlev S, Makogonenko E, Kurochkina N, Nieuwenhuizen W, Ingham K, Medved L. Conversion of fibrinogen to fibrin: mechanism of exposure of tPA- and plasminogen-binding sites. Biochemistry 2000;39:15730–15741.
  • Medved L, Nieuwenhuizen W. Molecular mechanisms of initiation of fibrinolysis by fibrin. Thromb Haemost 2003;89: 409–419.
  • Medved L, Tsurupa G, Yakovlev S. Conformational changes upon conversion of fibrinogen into fibrin. The mechanisms of exposure of cryptic sites. Ann N Y Acad Sci 2001;936: 185–204.
  • Tsurupa G, Medved L. Fibrinogen alpha C domains contain cryptic plasminogen and tPA binding sites. Ann N Y Acad Sci 2001;936:328–330.
  • Danesh J, Collins R, Peto R. Lipoprotein(a) and coronary heart disease. Meta-analysis of prospective studies. Circulation 2000;102:1082–1085.
  • Danesh J, Collins R, Appleby P, Peto R. Association of fibrinogen, C-reactive protein, albumin, or leukocyte count with coronary heart disease: meta-analyses of prospective studies. JAMA 1998;279:1477–1482.
  • Bini A, Kudryk BJ. Fibrinogen in human atherosclerosis. Ann N Y Acad Sci 1995;748:461–471.
  • Boonmark NW, Lou XJ, Yang ZJ, Schwartz K, Zhang JL, Rubin EM, Lawn RM. Modification of apolipoprotein(a) lysine binding site reduces atherosclerosis in transgenic mice. J Clin Invest 1997;100:558–564.
  • Lou XJ, Boonmark NW, Horrigan FT, Degen JL, Lawn RM. Fibrinogen deficiency reduces vascular accumulation of apolipoprotein(a) and development of atherosclerosis in apolipoprotein(a) transgenic mice. Proc Natl Acad Sci USA 1998;95:12591–12595.
  • Anglès-Cano E, de la Pena Diaz A, Loyau S. Inhibition of fibrinolysis by lipoprotein(a). Ann N Y Acad Sci 2001;936: 261–275.
  • Thornalley PJ, Rabbani N. Protein damage in diabetes and uremia – identifying hotspots of proteome damage where minimal modification is amplified to marked pathophysiological effect. Free Radic Res 2011;45:89–100.
  • Himmelfarb J, Stenvinkel P, Ikizler TA, Hakim RM. The elephant in uremia: oxidant stress as a unifying concept of cardiovascular disease in uremia. Kidney Int 2002;62: 1524–1538.
  • Himmelfarb J. Uremic toxicity, oxidative stress, and hemodialysis as renal replacement therapy. Semin Dial 2009;22: 636–643.

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