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Mechanism of peroxynitrite interaction with cytochrome c.

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Kinetics of the reaction of peroxynitrite with ferric cytochrome c in the absence and presence of bicarbonate was studied. It was found that the heme iron in ferric cytochrome c does not react directly with peroxynitrite. The rates of the absorbance changes in the Soret region of cytochrome c spectrum caused by peroxynitrite or peroxynitrite/bicarbonate were the same as the rate of spontaneous isomerization of peroxynitrite or as the rate of the reaction of peroxynitrite with bicarbonate, respectively. This means that intermediate products of peroxynitrite decomposition, ·OH/·NO2 or, in the presence of bicarbonate, CO3-·/·NO2, are the species responsible for the absorbance changes in the Soret band of cytochrome c. Modifications of the heme center of cytochrome c by radiolytically produced radicals, ·OH, ·NO2 or CO3-·, were also studied. The absorbance changes in the Soret band caused by radiolytically produced ·OH or CO3-· were much more significant that those observed after peroxynitrite treatment, compared under similar concentrations of radicals. ·NO2 produced radiolytically did not interact with the heme center of cytochrome c. Cytochrome c exhibited an increased peroxidase-like activity after reaction with peroxynitrite as well as with radiolytically produced ·OH, ·NO2 or CO3-· radicals. This means that modification of protein structure: oxidation of amino acids and/or tyrosine nitration, facilitates reaction of H2O2 with the heme iron of cytochrome c, followed by reaction with the second substrate.
Physical description
  • Institute of Applied Radiation Chemistry, Technical University of Łódź, Wróblewskiego 15, 93-590 Łódź, Poland
  • Institute of Applied Radiation Chemistry, Technical University of Łódź, Wróblewskiego 15, 93-590 Łódź, Poland
  • Alayash AI, Ryan BA, Cashon RE. (1998) Peroxynitrite-mediated heme oxidation and protein modification of native and chemically modified hemoglobins. Arch Biochem Biophys.; 349: 65-73.
  • Augusto O, Bonini MG, Amanso AM, Linares E, Santos CCX, De Menezes SL. (2002) Nitrogen dioxide and carbonate radical anion: two emerging radicals in biology. Free Radic Biol Med.; 32: 841-59.
  • Bourassa JL, Ives EP, Marqueling AN, Shimanovich R, Groves JT. (2001) Myoglobin catalyzes its own nitration. J Am Chem Soc.; 123: 5142-3.
  • Buxton GV, Greenstock CL, Helman WP, Ross AB. (1988) Critical review of rate contants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (̇OH/O-̇) in aqueous solution. J Phys Chem Ref Data.; 17: 513-886.
  • Cassina AM, Hodara R, Souza JM, Thomson L, Castro L, Ischiropoulos H, Freeman BA, Radi R. (2000) Cytochrome c nitration by peroxynitrite. J Biol Chem.; 275: 21409-15.
  • Chen Y-R, Deterding LJ, Sturgeon BE, Tomer KB, Mason RP. (2002) Protein oxidation of cytochrome c by reactive halogen species enhances its peroxidase activity. J Biol Chem.; 277: 29781-91.
  • Childs RE, Bardsley WG. (1975) The steady-state kinetics of peroxidase with 2,2'-azino-di-(3-ethyl-benzthiazoline-6-sulphonic acid) as chromogen. Biochem J.; 145: 93-103.
  • Coddington JW, Hurst JK, Lymar SV. (1999) Hydroxyl radical formation during peroxynitrous acid decomposition. J Am Chem Soc.; 121: 2438-43.
  • Deiber A, Herold S, Schöneich C, Namgaladze D, Peterson JA, Ullrich V. (2000) Nitration and inactivation of cytochrome P450(BM-3) by peroxynitrite - Stopped-flow measurements prove ferryl intermediates. Eur J Biochem.; 267: 6729-39.
  • Diederix REM, Ubbink M, Canters GW. (2002) Peroxidase activity as a tool for studying the folding of c-type cytochromes. Biochemistry.; 41: 13067-77.
  • Exner M, Herold S. (2000) Kinetic and mechanistic studies of the peroxynitrite-mediated oxidation of oxymyoglobin and oxyhemoglobin. Chem Res Toxicol.; 13: 287-93.
  • Floris R, Piersma R, Yang G, Jones P, Wever R. (1993) Interaction of myeloperoxidase with peroxynitrite. Eur J Biochem.; 215: 767-75.
  • Gerasimov OV, Lymar SV. (1999) The yield of hydroxyl radical from the decomposition of peroxynitrous acid. Inorg Chem.; 38: 4317-21.
  • Gębicka L, Gębicki JL. (1992) Redox transformations in peroxidases studied by pulse radiolysis technique. Radiat Phys Chem.; 39: 113-6.
  • Gębicka L. (2001) Peroxidase-like activity of cytochrome c in the presence of anionic surfactants. Res Chem Intermed.; 27: 717-23.
  • Gębicka L, Gębicki JL. (2000) Reactions of heme peroxidases with peroxynitrite. IUBMB Life.; 49: 11-5.
  • Goldstein S, Czapski G. (1998) Formation of peroxynitrate from the reaction of peroxynitrite with CO2: Evidence for carbonate radical production. J Am Chem Soc.; 120: 3458-63.
  • Goldstein S, Meyerstein D, van Eldik R, Czapski G. (1999) Peroxynitrous acid decomposes via homolysis: evidence from high-pressure pulse radiolysis. J Phys Chem A.; 103: 6587-90.
  • Goto Y, Hagihara Y, Hamada D, Hoshino M, Nishi I. (1993) Acid-induced unfolding and refolding transitions of cytochrome c: A three-state mechanism in H2O and D2O. Biochemistry.; 32: 11878-85.
  • Gow A, Duran D, Thom SR, Ischiropoulos H. (1996) Carbon dioxide enhancement of peroxynitrite-mediated protein tyrosine nitration. Arch Biochem Biophys.; 333: 42-8.
  • Grisham MB, Johnson GG, Lancaster Jr JR. (1996) Quantitation of nitrate and nitrite in extracellular fluids. Methods Enzymol.; 268: 237-46.
  • Hamachi J, Fujita A, Kunitake T. (1994) Enhanced N-demethylase activity of cytochrome c bound to a phosphate-bearing synthetic bilayer membrane. J Am Chem Soc.; 116: 8811-2.
  • Hudges MN, Nicklin HG. (1968) The chemistry of pernitrites. Part I: Kinetics of decomposition of pernitrous acid. J Chem Soc.; 450-2.
  • Kissner R, Nauser T, Bugnon P, Lye PG, Koppenol WH. (1998) Formation and properties of peroxynitrite as studied by laser flash photolysis, high-pressure stopped-flow technique, and pulse radiolysis. Chem Res Toxicol.; 10: 1285-92.
  • Koppenol WH, Moreno JJ, Pryor WA, Ischiropoulos H, Beckman JS. (1992) Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide. Chem Res Toxicol.; 5: 834-42.
  • Lemercier JN, Padmaja S, Cueto R, Squadrito GL, Uppu RM, Pryor WA. (1997) Carbon dioxide modulation of hydroxylation and nitration of phenol by peroxynitrite. Arch Biochem Biophys.; 345: 160-70.
  • Lymar SV, . (1995) Rapid reaction between peroxynitrite ion and carbon dioxide: implications for biological activity. J Am Chem Soc.; 117: 8867-8.
  • Mehl M, Daibler A, Herold S, Shoun H, Ullrich V. (1999) Peroxynitrite reaction with heme protein. Nitric Oxide.; 3: 142-52.
  • Meli R, Nauser T, Latal P, Koppenol WH. (2002) Reaction of peroxynitrite with carbon dioxide: intermediates and determination of the yield of CO3-̇ and ̇NO2. J Biol Inorg Chem.; 7: 31-6.
  • Merenyi G, Lind J. (1997) Thermodynamics of peroxynitrite and its CO2 adduct. Chem Res Toxicol.; 10: 1216-20.
  • Merenyi G, Lind J. (1998) Free radical formation in the peroxynitrous acid (ONOOH)/peroxynitrite (ONOO-) system. Chem Res Toxicol.; 11: 243-6.
  • Minetti M, Scorza G, Pietraforte D. (1999) Peroxynitrite induces long-lived tyrosyl radical(s) in oxyhemoglobin of red blood cells through a reaction involving CO2 and ferryl species. Biochemistry.; 38: 2078-87.
  • Nakagawa H, Ohshima Y, Takusagawa M, Ikota N, Takahashi Y, Shimizu S, Ozawa T. (2001) Functional modification of cytochrome c by peroxynitrite in an electron transfer reaction. Chem Pharm Bull.; 49: 1547-54.
  • Neta P, Huie RE, Ross AB. (1988) Rate constants for reactions of inorganic radicals in aqueous solution. J Phys Ref Data.; 17: 1027-284.
  • Oellerich S, Wackerbarth H, Hildebrandt P. (2002) Spectroscopic characterization of nonnative conformational states of cytochrome c. J Phys Chem B.; 106: 6566-80.
  • Patel RP, McAndrew J, Sellak H, White CR, Jo H, Freeman BA, Darley-Usmar VM. (1999) Biological aspects of reactive nitrogen species. Biochim Biophys Acta.; 1411: 385-400.
  • Pietraforte D, Salzano AM, Scorza G, Marino G, Minetti M. (2001) Mechanism of peroxynitrite interaction with ferric hemoglobin and identification of nitrated tyrosine residues. CO2 inhibits heme-catalyzed scavenging and isomerization. Biochemistry.; 40: 15300-9.
  • Prütz A, Mönig H, Butler J, Land EJ. (1985) Reactions of nitrogen dioxide in aqueous model systems: oxidation of tyrosine units in peptides and proteins. Arch Biochem Biophys.; 243: 125-34.
  • Pryor WA, Cueto R, Jin X, Koppenol WH, Ngu-Schwemlein M, Squadrito GL, Uppu PL, Uppu MR. (1995) A practical method for preparing peroxynitrite solutions of low ionic strength and free of hydrogen peroxide. Free Radic Biol Med.; 18: 75-83.
  • Radi R, Peluffo G, Alvarez MN, Navillat M, Cayota A. (2001) Unraveling peroxynitrite formation in biological systems. Free Radic Biol Med.; 30: 463-88.
  • Radi R, Thomson L, Rubbo H, Prodanov E. (1991) Cytochrome c-catalyzed oxidation of organic molecules by hydrogen peroxide. Arch Biochem Biophys.; 288: 112-7.
  • Simic MG, Taub IA. (1977) Mechanisms of inter- and intra-molecular electron transfer in cytochromes. Faraday Discuss Chem Soc.; 63: 270-8.
  • Squadrito GL, Pryor WA. (1998) Oxidative chemistry of nitric oxide: the roles of superoxide, peroxynitrite and carbon dioxide. Free Radic Biol Med.; 25: 392-403.
  • Thomson L, Trujillo M, Telleri R, Radi R. (1995) Kinetics of cytochrome c2+ oxidation by peroxynitrite: implications for superoxide measurements in nitric oxide-producing biological systems. Arch Biochem Biophys.; 319: 491-7.
  • Uppu RM, Squadrito GL, Cueto R, Pryor WA. (1996) Synthesis of peroxynitrite by azide-ozone reaction. Methods Enzymol.; 269: 311-21.
  • Whitburn KD, Shieh JJ, Sellers RM, Hoffman MZ, Taub IA. (1982) Redox transformations in ferrimyoglobin induced by radiation-generated free radicals in aqueous solution. J Biol Chem.; 257: 1860-9.
  • Yeh SR, Han S, Rousseau DL. (1998) Cytochrome c folding and unfolding: A biphasic mechanism. Acc Chem Res.; 31: 727-36.
  • Yermilov V, Yoshie Y, Rubio J, Ohshima H. (1996) Effects of carbon dioxide/bicarbonate on induction of DNA single-strand breaks and formation of 8-nitroguanine, 8-oxoguanine and base-propenal mediated by peroxynitrite. FEBS Lett.; 399: 67-70.
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