View More View Less
  • 1 Institute of Biomolecular Chemistry, Chemical Research Center, Hungarian Academy of Sciences, Pusztaszeri út 59-67, Budapest 1025, Hungary
  • | 2 Institute of Structural Chemistry, Chemical Research Center, Hungarian Academy of Sciences, Pusztaszeri út 59-67, Budapest 1025, Hungary
  • | 3 Oxidative Stress and Disease Laboratory, Pennington Biomedical Research Center, Baton Rouge, LA, 70808, USA
Restricted access

Abstract

Pitfalls of peroxynitrite (ONOO) formation in diabetic rat aorta on luminol-induced chemiluminescence (LCL) are investigated based on a detailed reaction mechanism in a case where 1.0 × 10−7 M s−1 superoxide formation rate and nitric oxide (NO) formation were measured by electron paramagnetic resonance, while ONOO formation by LCL. Modeling ONOO formation at equimolar reactant ratio at pH 7.4 and 37 °C predicts 2.0 nM ONOO and 2.1 × 10−6 M steady-state NO concentrations, which are both biologically relevant. Comparison of steady-state concentrations to those obtained by modeling the LCL intensity at pH 10 shows that ONOO concentration increases with 10% while peroxynitrous acid (ONOOH) concentration decreases complying with the pH shift. Evaluation of steady-state reaction rates reveals that the contribution of CO3•− radicals to the formation of luminol radicals is 76%, that of NO2 is 24%, considerable, but that of OH radicals negligible. The contribution of additional superoxide formation by autoxidation of luminol is 13%, not negligible, but that of ONOOH homolysis is negligible. The NO2 is predominantly formed from the decomposition of the ONOO–carbon dioxide adduct and only 0.5% directly from NO oxidized by molecular oxygen. But the contribution of the latter pathway depends strongly on the NO and superoxide formation rate ratio, at a ratio of 2:1, it would increase to 14%. The measured time interval of the initial increase of LCL intensity complies with the time needed luminol aorta outside and inside concentrations in the sample to be equalized by diffusion, the 7 × 10−3 s−1 rate constant obtained by modeling enabled to estimate 5 × 10−7 cm2 s−1 as the diffusion coefficient of luminol in the diabetic rat aorta.

  • 1. Radi, R, Cosgrove, TP, Beckman, JS, Freeman, BA 1993 Peroxynitrite-induced luminol chemiluminescence. Biochem J 290:5157.

  • 2. Radi, R, Peluffo, RG, Alvarez, MN, Naviliat, M, Cayota, A 2001 Unraveling peroxynitrite formation in biological systems. Free Radic Biol Med 30:463488 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Dai, K, Vlessidis, GA, Evmiridis, NP 2003 Dialysis membrane sampler for on-line flow injection analysis/chemiluminescence-detection of peroxynitrite in biological samples. Talanta 59:5565 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Mumbengegwi, DR, Li, Q, Li, C, Bear, CE, Engelhardt, JF 2008 Evidence of a superoxide permeability pathway in endosomal membranes. Mol Cell Biol 28:37003712 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Lind, J, Merényi, G, Eriksen, TE 1983 Chemiluminescence mechanism of cyclic hydrazides such as luminol in aqueous solutions. J Am Chem Soc 105:7655 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Faulkner, K, Fridovich, I 1993 Luminol and lucigenin as detectors for O2 •−. Free Radic Biol Med 15:447451 .

  • 7. Wardman, P 2007 Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues, progress, pitfalls, and prospects. Free Radic Biol Med 43:9951022 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Stadler, K, Jenei, V G von Bölcsházy Somogyi, A, Jakus, J 2003 Increased nitric oxide levels as an early sign in premature aging in diabetes. Free Radic Biol Med 359:1240 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Wang, P, Zweier, JL 1996 Measurement on nitric oxide and peroxynitrite generation in the postischemic heart. J Biol Chem 271:2922329230 .

  • 10. Brovkovych, V, Patto, S, Brovkovych, S, Kiechle, F, Huk, I, Malinski, T 1997 In situ measurement of nitric oxide, superoxide and peroxynitrite during endotoxemia. J Physiol Pharmacol 48:633644.

    • Search Google Scholar
    • Export Citation
  • 11. Ferrer-Sueta, G, Radi, R 2009 Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem Biol 4:161177 .

  • 12. Radi, R, Cassina, A, Hodara, R, Quijano, C, Castro, L 2002 Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33:14511464 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Beckman, JS 2009 Understanding peroxynitrite biochemistry and its potential for treating human diseases. Arch Biochem Biophys 484:114116 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Quijano, C, Romero, N, Radi, R 2005 Tyrosine nitration by superoxide and nitric oxide fluxes in biological systems: modeling the impact of superoxide dismutase and nitric oxide diffusion. Free Radic Biol Med 39:728741 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Turányi, T 1990 KINAL—a program package for kinetic analysis of reaction mechanisms. Comput Chem 14:253254 .

  • 16. Németh, A, Stadler, K, Jakus, J, Vidóczy, T 2011 Kinetics of peroxynitrite formation and decay in diabetic rat aorta. Oxid Commun 34:128135.

    • Search Google Scholar
    • Export Citation
  • 17. Vitt, JE, Johnson, DC, Engstrom, RC 1991 The effect of electrode material on electrogenerated chemiluminescence of luminol. J Electrochem Soc 138:16371643 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Pastore, P, Favaro, G, Gallina, A, Antiochia, R 2002 Kinetic considerations on the electrogenerated luminescence of luminol at platinum electrode in the presence of hydrogen peroxide and oxygen. Ann Chim 92:271280.

    • Search Google Scholar
    • Export Citation
  • 19. Denicola, A, Batthyány, C, Lissi, E, Freeman, BA, Rubbo, H 2002 Diffusion of nitric oxide into low density lipoprotein. J Biol Chem 277:932936 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Huang, KT, Huang, Z, Kim-Shapiro, DB 2007 Nitric oxide red blood cell membrane permeability at high and low oxygen tension. Nitric Oxide 16:209216 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Redwood, WR, Rall, E, Pearl, W 1973 Red cell membrane permeability deduced from bulk diffusion coefficients. J Gen Physiol 64:706729 .

  • 22. Liu, X, Srinivasant, P, Collard, CE, Grajdenau, P, Zweier, JL, Friedman, A 2008 Nitric oxide diffusion rate is reduced in the aortic wall. Biophys J 94:18801889 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Et-Taouil, K, Safar, M, Plante, GE 2003 Mechanisms and consequences of large artery rigidity. Can J Physiol Pharmacol 81:205211 .

  • 24. Wolinsky H (1970) Response of the rat aortic media to hypertension. Circ Res 26: 507.

  • 25. Neuser, T, Koppenol, WH 2002 The rate constant of the reaction of superoxide with nitrogen monoxide: approaching the diffusion limit. J Phys Chem 106:40844086 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Lymar, SV, Hurst, JK 1995 Rapid reaction between peroxynitrite ion and carbon dioxide: implication for biological activity. J Am Chem Soc 117:88678868 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Squadrito, GL, Pryor, WA 2002 Mapping the reaction of peroxynitrite with CO2: energetics, reactive species, and biological implications. Chem Res Toxicol 15:885895 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Fridovich, I 1989 Superoxide dismutases. An adaption to a paramagnetic gas. J Biol Chem 26:77617764.

  • 29. Ross, AB, Mallard, WG, Helman, WP, Buxton, GV, Huie, RE, Neta, P 1998 NDRL/NIST solution kinetics database Notre Dame Radiation Laboratory Gaithersburg.

    • Search Google Scholar
    • Export Citation
  • 30. Goldstein, S, Czapski, G 1995 Kinetics of nitric oxide autooxidation in aqueous solution in the absence and presence of various reactants. The nature of oxidizing intermediates. J Am Chem Soc 117:1207812084 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Goldstein, S, Czapski, G, Lind, J, Merényi, G 2000 Tyrosine nitration by simultaneous generation of NO and O2 •− under physiological conditions. How radicals do the job. J Biol Chem 275:30313036 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Goldstein, S, Czapski, G, Lind, J, Merényi, G 1999 Effect of NO on the decomposition of peroxynitrite: reaction of N2O3 with ONOO. Chem Res Toxicol 12:132136 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Goldstein, S, Czapski, G, Lind, J, Merényi, G 1998 Mechanism of decomposition of peroxynitrites ion (O2NOO): evidence for the formation of O2 •− and NO radicals. Inorg Chem 37:39433947 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Merényi, G, Lind, J, Goldstein, S, Czapski, G 1999 Mechanism and thermochemistry of peroxynitrite decomposition in water. J Phys Chem 103:56855691 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Goldstein, S, Lind, J, Merényi, G 2005 Chemistry of peroxynitrites as compared to peroxynitrites. Chem Rev 105:24572470 .

  • 36. Mallard WG , Ross AB, Helman WP (1998) NIST standard reference database number 69. http://webbook.nist.gov/chemistry. Accessed 8 June 2011.

    • Search Google Scholar
    • Export Citation
  • 37. Chien, H, Sturtevant, JM 1963 The kinetics of the hydration of carbon dioxide at 25 °C. J Biol Chem 23:34993501.

  • 38. West RC (1977-1978) CRC Handbook of chemistry and physics. CRC Press, Cleveland.

  • 39. Merényi, G, Lind, JS, Eriksen, TE 1984 The equilibrium reaction of luminol radical with oxygen and the one-electron reduction potential of 5-aminophthalazine-1,4-dione. J Phys Chem 88:23202323 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40. Hsu, JL, Hsieh, Y, Tu, C, O'Connor, D, Nick, HS, Silverman, DN 1996 Catalytic properties of human manganese superoxide dismutase. J Biol Chem 271:1768717691 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41. Prutz, WA, Monig, H, Utler, JB, Land, EJ 1985 Reactions of nitrogen dioxide in aqueous model systems: oxidation of tyrosine units in peptides and proteins. Arch Biochem Biophys 243:125134 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42. Hodges, GR, Marwaha, J, Paul, T, Ingold, KU 2000 A novel procedure for generating both nitric oxide and superoxide in situ from chemical sources at any chosen mole ratio. First application: tyrosine oxidation and comparison with preformed peroxynitrite. Chem Res Toxicol 13:12871293 .

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43. Jin, F, Leicht, C J von Sonntag 1993 The superoxide radical reacts with tyrosine-derived phenoxyl radicals by addition rather than by electron transfer. J Chem Soc Perkin Trans 2:15831588.

    • Search Google Scholar
    • Export Citation
  • 44. Eiserich, JP, Butler, J A van Der Vliet Cross, CE, Halliwell, B 1995 Nitric oxide rapidly scavenges tyrosine and tryptophan radicals. Biochem J 310:745749.

    • Search Google Scholar
    • Export Citation
  • 45. Merényi, G, Lind, J 1998 Free radical formation in the peroxynitrous acid (ONOOH)/peroxynitrite (ONOO) system. Chem Res Toxicol 11:243246 .

  • 46. Merényi, G, Lind, JS 1980 Role of a peroxide intermediate in the chemiluminescence of luminal. J Am Chem 102:58305835 .

  • 47. Sturgeon, BE, Glover, RE, Chen, YR, Burka, LT, Mason, RP 2001 Tyrosine iminoxyl radical formation from tyrosyl radical/nitric oxide and nitrosotyrosine. J Biol Chem 276:4551645521 .

    • Crossref
    • Search Google Scholar
    • Export Citation