Abstract
Different kinds of nucleotide binding enzymes are sensitive to fluoroberyllate complexes (BeF.) and fluoroaluminate complexes (AlFy). It has been hypothesized that the effects of these fluorometals are related to the generation at a nucleotide binding site of a pseudo nucleoside triphosphate, consisting of a fluorometal moiety bound to the β phosphate group of a molecule of nucleoside diphosphate (Bigay et al. 1985; Lunardi et al. 1985). In order to establish whether ternary complexes comprising ADP, beryllium and fluoride can exist in slightly alkaline solution in the absence of enzyme, we have carried out a multinuclear (31P, 9Be and t9F) NMR study. In preliminary experiments, pyrophosphate (PPi) was substituted for ADP and taken as a simpler analog of nucleoside diphosphate. In the absence of fluoride, three types of PPi-Be complexes were generated: two of these were bidentate chelates with either one or two pyrophosphate molecules bound per beryllium; the third one was a monodentate complex. It is probable that the same types of combination exist between the polyphosphate chain of ADP and Be. In the presence of fluoride, both ADP and PPi combined with beryllium to form ternary complexes. These complexes consisted of monofluoroberyllate(-BeF) or difluoroberyllate (-BeF,) bound to the two phosphates of one molecule of ADP or PPi as a bidentate chelate. We failed to observe the formation of complexes between ADP and trifluoroberyllate (-BeF3). The relevance of this study to the biological effects of fluoride and beryllium on various enzymic reactions is discussed.
Similar content being viewed by others
Abbreviations
- PPi:
-
pyrophosphate
- AMP:
-
adenosine -5′-monophos-phate
- ADP:
-
adenosine- 5′-diphosphate
- ADPβS:
-
adenosine-5′-O-(2-thiodiphosphate)
- Ap2A:
-
P1,p2-di(adenosine-5′)pyrophosphate
- F1-ATPase:
-
catalytic sector (soluble) of the beef heart mitochondrial ATPase complex
- Tris :
-
tris(hydroxymethyl)aminomethane
References
Bigay J, Deterre P, Pfister C, Chabre M (1985) Fluoroaluminates active transducin-GDP by mimicking the γ phosphate of GTP in its binding site. FEBS Lett 191:181–185
Bigay J, Deterre P, Pfister C, Chabre M (1987) Fluoride complexes of aluminium or beryllium act on G-proteins as reversibly bound analogues of the γ phosphate of GTP. EMBO J 6:2907–2913
Bock JL (1980) The binding of metal ions to ATP: a proton and phosphorus NMR investigation of diamagnetic metal-ATP complexes. J Inorg Biochem 12:119–130
Bock JL, Ash DE (1980) NMR and infrared spectroscopic investigations of the AI(III), Ga(III), and Be(II) complexes of ATP. J Inorg Biochem 13:105–110
Carlier M-F, Didry D, Melki R, Chabre M, Pantaloni D (1988) Stabilization of microtubules by inorganic phosphate and its structural analogues, the fluoride complexes of aluminum and beryllium. Biochemistry 27:3555–3559
Cohn M, Hughes Jr TR (1960) Phosphorus magnetic resonance spectra of adenosine di- and triphosphate. 1. Effect of pH. J Biol Chem 235:3250–3253
Cohn M, Hughes Jr TR (1962) Nuclear magnetic resonance spectra of adenosine di- and triphosphate. II. Effect of complexing with divalent metal ions. J Biol Chem 237:176–181
Combeau C, Carlier M-F (1988) Probing the mechanism of ATP hydrolysis on F-actin using vanadate and the structural analogs of phosphate BeF3 − and A1F4 −. J Biol Chem 263:17429–17436
Combeau C, Carlier M-F (1989) Characterization of the aluminum and beryllium fluoride species bound to F-actin and microtubules at the site of the γ-phosphate of the nucleotide. J Biol Chem 264:19017–19021
Cornelius RD, Hart PA, Clelan WW (1977) Phosphorus-31 NMR studies of complexes of adenosine triphosphate, adenosine diphosphate, tripolyphosphate, and pyrophosphate with cobalt (III) ammines. Inorg Chem 16:2799–2805
Cozzone PJ, Jardetzky O (1976) Phosphorus-31 Fourier transform nuclear magnetic resonance study of mononucleotides and dinucleotides. I. Chemical shifts. Biochemistry 15:4853–4859
Delpuech JJ, Peguy A, Rubini P, Steinmetz J (1977) Complexes du beryllium (II) avec des molecules organophosphorees: étude par RMN du béryllium-9, du phosphore-31, du carbone-13 et du proton. Nouv J Chim 1:133–139
Dupuis A, Isartel J-P, Vignais PV (1989) Direct identification of the fluoroaluminate and fluoroberyllate species responsible for inhibition of the mitochondrial F1-ATPase. FEBS Lett 255:47–52
Feeney J, Haque R, Reeves LW, Yue CP (1968) Nuclear spin-spin coupling constants; equilibrium and kinetic studies for fluoroberyllate complexes in solution. Can J Chem 46:1389–1398
Froede HC, Wilson IB (1985) The slow rate of inhibition of acetylcholinesterase by fluoride. Mol Pharmacol 27:630–633
Geraldes GFGC, Castro MMCA (1986) 1H and 31P NMR study of the interaction of molybdate with the nucleotides adenosine 5′-diphosphate and adenosine 5′-triphosphate. J Inorg Biochem 28:319–327
Goldstein G (1964) Equilibrium distribution of metal-fluoride complexes. Anal Chem 36:243–244
Gresser MJ, Tracey AS, Parkinson KM (1986) Vanadium (V) oxyanions: the interactions of vanadate with pyrophosphate, phosphate, and arsenate. J Am Chem Soc 108:6229–6234
Gutowsky HS, Hoffman CJ (1951) Nuclear magnetic shielding in fluorine and hydrogen compounds. J Chem Phys 19:1259–1267
Issartel J-P, Dupuis A, Lunardi J, Vignais PV (1991) Fluoroaluminum and fluoroberyllium nucleoside diphosphate complexes as probes of the enzymatic mechanism of the mitochondrial F1-ATPase. Biochemistry 30:4726–4733
Jackson GE (1988) The existence of A1F4 − in aqueous solution and its relevance to phosphorylase reactions. Inorg Chem Acta 151:273–276
Jaffe EK, Cohn M (1978) 31P nuclear magnetic resonance spectra of the triphosphate analogues of adenine nucleotides; effects of pH and Mg2+ binding. Biochemistry 17:652–7657
Kotz JC, Schaeffer R, Clouse A (1967) High-resolution nuclear magnetic resonance spectroscopy of some beryllium-containing compounds. Beryllium-9 and fluorine-19 spectra. Inorg Chem 6:620–622
Kovar RA, Morgan GL (1970) Beryllium-9 and hydrogen-1 magnetic resonance studies of beryllium compounds in solution. J Am Chem Soc 92:5067–5072
Lange AJ, Arion WJ, Burchell A, Burchell B (1986) Aluminum ions are required for stabilization and inhibition of hepatic microsomal glucose-6-phosphatase by sodium fluoride. J Biol Chem 261:101–107
Laurie O, Oakes J, Rockliffe JW, Smith EG (1986) Phosphorus and proton nuclear magnetic resonance studies of transition-metal complexes of triphosphate and pyrophosphate in aqueous solution. J Chem Soc Faraday Trans 182:3149–3161
Lincoln SF, Sandercock AC, Stranks DR (1977) A 19F nuclear magnetic resonance study of the exchange of the fluoro ligands of the tetrafluoroberyllium (II) ion. Aust J Chem 30:271–279
Lunardi J, Dupuis A, Garin J, Issartel J-P, Michel L, Chabre M, Vignais PV (1985) Inhibition of H+-transporting ATPase by formation of a tight nucleoside diphosphate-fluoroaluminate complex at the catalytic site. Proc Natl Acad Sci USA 85:8958–8962
Martin RB (1988) Ternary hydroxide complexes in neutral solutions of Al3+ and F−β. Biochem Biophys Res Commun 155:1194–1200
Mathieu L, Thivolle P, Delman M, Berger M (1982) 31P NMR spectroscopy of mixed aqueous Na pyrophosphate and stannous chloride solutions. Evidence for pyrophosphate-Sn complex formation. Magn Reson 46:332–337
Mesmer RE, Baes Jr CF (1969) Fluoride complexes of beryllium (II) in aqueous media. Inorg Chem 8:618–626
Missiaen L, Wuytack F, De Smedt H, Vrolix M, Casteels R (1988) AIF4 − reversibly inhibits “P”-type cation-transport ATPases, possibly by interacting with the phosphate-binding site of the ATPase. Biochem J 253:827–833
Ramirez F, Marecek JF (1980) Coordination of magnesium with adenosine 5'-diphosphate and triphosphate. Biochim Biophys Acta 589:21–29
Robinson JD, Davis RL, Steinberg M (1986) Fluoride and beryllium interact with the (Na + K)-dependent ATPase as analogs of phosphate. J Bioenerg Biomemb 18:521–531
Rosset R, Desbarres J, Jardy A, Bauer D (1985) Un exemple d'utilisation de l'informatique dans l'étude des équilibres en solution: le traitement d'effluents contenant du phosphate. J Chim Phys 82:647–651
Shyy YD, Tsai TC, Tsai MD (1985) Metal-nucleotide interactions. 3. 17O, 31P, and 1H NMR studies on the interactions of Sc(III), La(III) and Lu(III) with adenosine 5′-triphosphate. J Am Chem Soc 107:3478–3484
So H, Kolor M, Robinson PR, Haight Jr GP, Belford RL (1979) Reactions of molybdates with polyphosphates, 2. Magnetic resonance studies on molybdenum (V) polyphosphate and ATP complexes. J Coord Chem 9:43–51
Sternweis PC, Gilman AG (1982) Aluminum: a requirement for activation of regulatory component of adenylate cyclase by fluoride. Proc Natl Acad Sci USA 79:4888–4891
Tran-Dinh S, Neumann JM (1977) A 31P-NMR study of the interaction of Mg2+ ions with nucleoside diphosphates. Nucleic Acids Res 4:397–403
Wehrli FW (1978) Relaxation of quadrupolar nuclei. J Magn Reson 30:193–207
Author information
Authors and Affiliations
Additional information
Offprint requests to: J.-L. Girardet
Rights and permissions
About this article
Cite this article
Issartel, J.P., Dupuis, A., Moral, C. et al. Fluoride, beryllium and ADP combine as a ternary complex in aqueous solution as revealed by a multinuclear NMR study. Eur Biophys J 20, 115–126 (1991). https://doi.org/10.1007/BF00186260
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00186260