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Effect of fructose 1,6-bisphosphate on the iron redox state relating to the generation of reactive oxygen species

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Abstract

Role of fructose 1,6-bisphosphate-mediated iron oxidation in the generation of reactive oxygen species was analyzed. Aconitase the most sensitive enzyme to oxidative stress was inactivated potently by fructose 1,6-bisphosphate in the presence of ferrous ion, and further by ADP and PEP to a lesser extent. The inactivation requires cyanide, suggesting that the superoxide radical is responsible for the inactivation. Addition of ascorbic acid and dithiothreitol prevented aconitase from the inactivation. Fructose 1,6-bisphosphate, ADP and PEP stimulated the oxidation of ferrous ion causing one-electron reduction of oxygen molecule. Superoxide radical formed with iron oxidation participates in the oxidative inactivation of aconitase and the citric acid cycle, resulting in the induction of the Crabtree effect, that is, high glucose-mediated inhibition of oxidative metabolism in mitochondria.

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References

  • Bajić A, Zakrzewska J, Godjevac D, Andjus P, Jones DR, Spasić M, Spasojević I (2011) Relevance of the ability of fructose 1,6-bis(phosphate) to sequester ferrous but not ferric ions. Carbohydr Res 346:416–420

    Article  PubMed  Google Scholar 

  • Chapman C, Bartley W (1969) Adenosine phosphates and the control of glycolysis and gluconeogenesis in yeast. Biochem J 111:609–613

    CAS  PubMed Central  PubMed  Google Scholar 

  • Crabtree HG (1929) The carbohydrate metabolism of certain pathological overgrowths. Biochem J 22:1289–1298

    Google Scholar 

  • Diaz-Ruiz R, Avéret N, Araiza D, Pinson B, Uribe-Carvajal S, Devin A, Rigoulet M (2008) Mitochondrial oxidative phosphorylation is regulated by fructose 1,6-bisphosphate. A possible role in Crabtree effect induction? J Biol Chem 283:26948–26955

    Article  CAS  PubMed  Google Scholar 

  • Evtodienko Y-V, Teplova VV, Duszynski J, Bogucka K, Wojtczak L (1994) The role of cytoplasmic [Ca2+] in glucose-induced inhibition of respiration and oxidative phosphorylation in Ehrlich ascites tumour cells: a novel mechanism of the Crabtree effect. Cell Calcium 15:439–446

    Article  CAS  PubMed  Google Scholar 

  • Fridovich I (1995) Superoxide radical and superoxide dismutases. Ann Rev Biochem 64:97–112

    Article  CAS  PubMed  Google Scholar 

  • Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189:147–163

    Article  CAS  PubMed  Google Scholar 

  • Gardner PR (2002) Aconitase: sensitive target and measure of superoxide. Methods Enzymol 349:9–23

    Article  CAS  PubMed  Google Scholar 

  • Gardner PR, Fridovich I (1992) Inactivation-reactivation of aconitase in Escherichia coli. A sensitive measure of superoxide radical. J Biol Chem 267:8757–8763

    CAS  PubMed  Google Scholar 

  • Gatt S, Racker E (1959) Regulatory mechanisms in carbohydrate metabolism. I. Crabtree effect in reconstructed systems. J Biol Chem 234:1015–1023

    CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186:1–85

    Article  CAS  PubMed  Google Scholar 

  • Lee AC, Zizi M, Colombini M (1994) Beta-NADH decreases the permeability of the mitochondrial outer membrane to ADP by a factor of 6. J Biol Chem 269:30974–30980

    CAS  PubMed  Google Scholar 

  • Murakami K, Yoshino M (1997) Inactivation of aconitase in yeast exposed to oxidative stress. Biochem Mol Biol Int 41:481–486

    CAS  PubMed  Google Scholar 

  • Murakami K, Nagura H, Yoshino M (1980) Permeabilization of yeast cells: application to study on the regulation of AMP deaminase activity in situ. Anal Biochem 105:407–413

    Article  CAS  PubMed  Google Scholar 

  • Murakami K, Haneda M, Yoshino M (2006a) Prooxidant action of xanthurenic acid and quinoline compounds: role of transition metals in the generation of reactive oxygen species and enhanced formation of 8-hydroxy-2′-deoxyguanosine in DNA. Biometals 19:429–435

    Article  CAS  PubMed  Google Scholar 

  • Murakami K, Tsubouchi R, Fukayama M, Ogawa T, Yoshino M (2006b) Oxidative inactivation of reduced NADP-generating enzymes in E. coli: iron-dependent inactivation with affinity cleavage of NADP-isocitrate dehydrogenase. Arch Microbiol 186:385–392

    Article  CAS  PubMed  Google Scholar 

  • Pierre JL, Fontecave M (1999) Iron and activated oxygen species in biology: the basic chemistry. Biometals 12:195–199

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Enríquez S, Juárez O, Rodríguez-Zavala JS, Moreno-Sánchez R (2001) Multisite control of the Crabtree effect in ascites hepatoma cells. Eur J Biochem 268:2512–2519

    Article  PubMed  Google Scholar 

  • Salas ML, Vinuela E, Salas M, Sols A (1965) Citrate inhibition of phosphofructokinase and the Pasteur effect. Biochem Biophys Res Commun 19:371–376

    Article  CAS  PubMed  Google Scholar 

  • Tornheim K (1980) Co-ordinate control of phosphofructokinase and pyruvate kinase by fructose diphosphate: a mechanism for amplification and step changes in the regulation of glycolysis in liver. J Theor Biol 85:199–222

    Article  CAS  PubMed  Google Scholar 

  • Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12(10):1161–1208

    Article  CAS  PubMed  Google Scholar 

  • van Urk H, Voll WS, Scheffers WA, van Dijken JP (1990) Transient-state analysis of metabolic fluxes in crabtree-positive and Crabtree-negative yeasts. Appl Environ Microbiol 56:281–287

    PubMed Central  PubMed  Google Scholar 

  • Vásquez-Vivar J, Kalyanaraman J, Kennedy MC (2000) Mitochondrial aconitase is a source of hydroxyl radical. An electron spin resonance investigation. J Biol Chem 275:14064–14069

    Article  PubMed  Google Scholar 

  • Wojtczak L, Teplova VV, Bogucka K, Czyz A, Makowska A, Wieckowski MR, Duszyński J, Evtodienko YV (1999) Effect of glucose and deoxyglucose on the redistribution of calcium in Ehrlich ascites tumour and Zajdela hepatoma cells and its consequences for mitochondrial energetics. Further arguments for the role of Ca2+ in the mechanism of the Crabtree effect. Eur J Biochem 263:495–501

    Article  CAS  PubMed  Google Scholar 

  • Yoshino M, Murakami K (1985) AMP deaminase reaction as a control system of glycolysis in yeast. Role of ammonium ion in the interaction of phosphofructokinase and pyruvate kinase activity with the adenylate energy charge. J Biol Chem 260:4729–4732

    CAS  PubMed  Google Scholar 

  • Yoshino M, Murakami K (1998) Interaction of iron with polyphenolic compounds: application to antioxidant characterization. Anal Biochem 257:40–44

    Article  CAS  PubMed  Google Scholar 

  • Zizi M, Forte M, Blachly-Dyson E, Colombini M (1994) NADH regulates the gating of VDAC, the mitochondrial outer membrane channel. J Biol Chem 269:1614–1616

    CAS  PubMed  Google Scholar 

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  1. Department of Biochemistry, Aichi Medical University School of Medicine, Nagakute, Aichi, 480-1195, Japan

    Keiko Murakami & Masataka Yoshino

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  1. Keiko Murakami
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  2. Masataka Yoshino
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Correspondence to Masataka Yoshino.

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Murakami, K., Yoshino, M. Effect of fructose 1,6-bisphosphate on the iron redox state relating to the generation of reactive oxygen species. Biometals 28, 687–691 (2015). https://doi.org/10.1007/s10534-015-9856-6

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  • DOI: https://doi.org/10.1007/s10534-015-9856-6

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