Dynamics of reactive oxygen species generation in the presence of copper(II)–histidine complex and cysteine

• Autorzy: Zabek-Adamska A. , Drozdz R. , Naskalski J. W.
• Języki publikacji: EN

Abstrakty

EN

Histidine-copper(II) complex (Cu-His2) is a form of bound copper necessary for cellular copper uptake. Due to the high affinity of histidine to copper(II) ions, the binding of copper(II) by histidine is considered a substantial part of plasma antioxidative defense. Also cysteine plays a role in the antioxidative system. However, we show here that in the presence of oxygen the histidine-copper(II) complex plus cysteine produces reactive oxygen species (ROS). Cysteine concentration was assayed using a thiol specific silver-mercury electrode. Hydrogen peroxide was assayed amperometrically using platinum electrode. ROS formation was followed by chemiluminescence of luminol-fluoresceine-enhanced system. Addition of cysteine to Cu-His2 solution at pH 7.4 in the presence of atmospheric oxygen initiates the synthesis of H2O2 and generation of ROS, which manifests as a burst of chemiluminescence. The reaction has two stages; in the first stage, cysteine is utilized for the synthesis of an unstable intermediary product which becomes a substrate for ROS formation. Anaerobic conditions inhibit ROS formation. Increased cysteine concentration enhances the lag phase of the oxidative burst without influencing the amount of ROS. The synthesis of ROS (measured by chemiluminescence) is proportional to the concentration of Cu-His2 employed. ROS production can be repetitively initiated by further additions of cysteine to the reaction medium. The study suggests that Cu-His2 catalyzes cysteine-dependent reduction of oxygen to superoxide employing an intermediary cysteine-copper(I) complex and enabling Fenton reaction with copper and hydrogen peroxide produced as a secondary product. In effect, Cu-His2 with cysteine may be a source of ROS in biological media.

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2013
• Tom: 60
• Numer: 4
• Opis fizyczny: p.565-571,fig.,ref.

Twórcy

autor

Zabek-Adamska A.

• Department of Clinical Biochemistry, Diagnostic Division, Jagiellonian University Medical College, Krakow, Poland

autor

Drozdz R.

• Department of Medical Diagnostics, Faculty of Pharmacy, Jagiellonian University Medical College, Krakow, Poland

autor

Naskalski J. W.

• Department of Clinical Biochemistry, Diagnostic Division, Jagiellonian University Medical College, Krakow, Poland

Bibliografia

• Biswas S, Chida AS, Rahman I (2006) Redox modifications of protein-thiols: emerging roles in cell signaling. Biochem Pharmacol 71: 551-564. 
• Brumas V, Alliey N, Berthon GA (1993) A new investigation of copper(II)-serine, copper(II)-histidine-serine, copper(II)-asparagine, and copper(II)-histidine-asparagine equilibria under physiological conditions, and implications for simulation models relative to blood plasma. J Inorg Biochem 52: 287-296. 
• Casella L, Gullotti M (1983) Coordination modes of histidine 4. Coordination structures in the copper(II)-L-histidine(1:2) system. J Inorg Biochem 18: 19-31. 
• De Silva DM, Aust SD (1993) Ferritin and ceruloplasmin in oxidative damage: review and recent findings. Can J Physiol Pharmacol 71: 715-720. 
• Deschamps P, Kulkarni PP, Gautam-Basak M, Sarkar B (2005) The saga of copper(II)-L-histidine. Coord Chem Rev 249: 895-909.
• Deschamps P, Kulkarni PP, Sarkar B (2003) The crystal structure of a novel copper(II) complex with asymmetric ligand derived from l-histidine. Inorg Chem 42: 7366-7368. 
• Drożdż R, Parmentier C, Hachad H, Leroy P, Siest G, Wellman M (1998) Gamma-glutamyltransferase dependent generation of reactive oxygen species from a glutathione/transferrin system. Free Radic Biol Med 25: 786-792. 
• Drożdż R, Naskalski J, Ząbek-Adamska A (2007) Potentiometric determination of cysteine with thiol sensitive silver-mercury electrode. Acta Biochim Polon 54: 205-211. 
• Gaubert S, Bouchaut M, Brumas V, Berthon G (2000) Copper-ligand interactions and the physiological free radical processes. Part 3. Influence of histidine, salicylic acid and anthranilic acid on copper-driven Fenton chemistry in vitro. Free Radic Res 32: 451-461. 
• Giustarini D, Dalle-Donne I, Milzani A, Rossi R (2011) Low molecular mass thiols, disulfides and protein mixed disulfides in rat tissues: influence of sample manipulation, oxidative stress and ageing. Mech Ageing Dev 132: 141-148. 
• Goode CA, Dinh CT, Linder MC (1989) Mechanism of copper transport and delivery in mammals: review and recent findings. Adv Exp Med Biol 258: 131-144. 
• Halliwell B (1994) Free radicals and antioxidants: a personal view. Review Nutr Rev 52: 253-265. 
• Hegde ML, Hegde PM, Holthauzen LM, Hazra TK, Rao KS, Mitra S (2010) Specific inhibition of NEIL-initiated repair of oxidized base damage in human genome by copper and iron. Potential etiological linkage to neurodegenerative diseases. J Biol Chem 285: 28812-28825. 
• Hodak M, Chisnell R, Lu W, Bernholc J (2009) Functional implications of multistage copper binding to the prion protein. Proc Natl Acad Sci USA 106: 11576-11581. 
• Hofstetter TE, Howder CR, Berden G, Oomens J, Armentrout PB (2011) Structural elucidation of biological and toxicological complexes: Investigation of monomeric and dimeric complexes of histidine with multiply charged transition metal (Zn and Cd) cations using IR action spectroscopy. J Phys Chem B 115: 12648-12661. 
• Kachur AV, Koch CJ, Biaglow JE (1999) Mechanism of copper-catalyzed autoxidation of cysteine. Free Radic Res 31: 23-34. 
• Khossravi M, Borchard RT (1998) Chemical pathways of peptide degradation. IX Metal catalyzed oxidation of histidine in model peptides. Pharm Res 15: 1096-1102. 
• Liu X, Zweier JL (2001) A real-time electrochemical technique for measurement of cellular hydrogen peroxide generation and consumption: evaluation in human polymorphonuclear leukocytes. Free Radic Biol Med 31: 894-901. 
• Lynch SM, Frei B (1997) Physiological thiol compounds exert pro- and anti-oxidant effects, respectively, on iron- and copper-dependent oxidation of human low-density lipoprotein. Biochim Biophys Acta 1345: 215-221. 
• Mesu JG, Visser T, Soulimani F, van Faassen EE, de Peinder P, Beale AM, Weckhuysen BM (2006) New Insights into the coordination chemistry and molecular structure of copper(II) histidine complexes in aqueous solutions. Inorg Chem 45: 1960-1971. 
• Moriya M, Ho YH, Grana A, Nguyen L, Alvarez A, Jamil R, Ackland ML, Michalczyk A (2008) Copper is taken up efficiently from albumin and alpha2-macroglobulin by cultured human cells by more than one mechanism. Am J Physiol Cell Physiol 295: C708-C721. 
• Munday R, Munday CM, Winterbourn CC (2004) Inhibition of copper-catalyzed cysteine oxidation by nanomolar concentrations of iron salts. Free Radic Biol Med 36: 757-766. 
• Pecci L, Montefoschi G, Cavallini D (1997) Some new details of the copper-hydrogen peroxide interaction. Biochem Biophys Res Commun 235: 264-267. 
• Sandstead HH R (1995) Requirements and toxicity of essential trace elements, illustrated by zinc and copper. Review. Am J Clin Nutr 61 (3 Suppl): 621S-624S. 
• Sarkar B, Kruck TP (1967) Separation of Cu(II)-amino acid complexes and evidence for the existence of histidine-Cu(II)-glutamine and histidine-Cu(II)-serine complexes at physiological pH. Can J Biochem 45: 2046-2049. 
• Shukla N, Maher J, Masters J, Angelini GD, Jeremy JY (2006) Does oxidative stress change ceruloplasmin from a protective to a vasculopathic factor? Atherosclerosis 187: 238-250. 
• Stadtman ER (1990) Metal ion-catalyzed oxidation of proteins: Biochemical mechanism and biologic consequences. Free Radic Biol Med 9: 315-325. 
• Theophanides T, Anastassopoulou J (2002) Copper and carcinogenesis. Crit Rev in Oncol and Hematol 42: 57-64. 
• Trigwell SM, Radford PM, Page SR, Loweth AC, James RF, Morgan NG, Todd I (2001) Islet glutamic acid decarboxylase modified by reactive oxygen species is recognized by antibodies from patients with type 1 diabetes mellitus. Clin Exp Immunol 126: 242-249. 
• Tubaro F, Ghiselli A, Rapuzzi P, Maiorino M, Ursini F (1998) Analysis of plasma antioxidant capacity by competition kinetics. Free Radic Biol Med 24: 1228-1234. 
• Ueda J, Sudo A, Mori A, Ozawa T (1994) Generation of hydroxyl radicals during dismutation of superoxide by SOD model compounds. Arch Biochem Biophys 315: 185-189. 
• Ueda JI, Hanaki A, Hatano K, Nakajima T (2000) Autoxidation of ascorbic acid catalyzed by the copper(II) bound to L-histidine oligopeptides, (His) i Gly and acetyl-(His) i Gly ( i=9, 19, 29). Relationship between catalytic activity and coordination mode. Chem Pharm Bull (Tokyo) 48: 908-913. 
• Ueland PM (1995) Homocysteine species as components of plasma redox thiol status. Clin Chem 41: 340-342. 
• Ullah MF, Ahmad A, Zubair H, Khan HY, Wang Z, Sarkar FH, Hadi S M (2011) Soy isoflavone genistein induces cell death in breast cancer cells through mobilization of endogenous copper ions and generation of reactive oxygen species. Mol Nutr Food Res 55: 553-559. 
• Wade AM, Tucker HN (1998) Antioxidant characteristics of L-histidine. J Nutr Biochem 9: 308-315.