Artículo

Nicoletti, F.P.; Droghetti, E.; Boechi, L.; Bonamore, A.; Sciamanna, N.; Estrin, D.A.; Feis, A.; Boffi, A.; Smulevich, G. "Fluoride as a probe for h-bonding interactions in the active site of heme proteins: The case of thermobifida fusca hemoglobin" (2011) Journal of the American Chemical Society. 133(51):20970-20980
El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The structural and functional properties of the active site of the bacterial hemoglobin from Thermobifida fusca are largely determined by three polar amino acids: TrpG8, TyrCD1, and TyrB10. We have exploited the availability of a combinatorial set of mutants, in each of which these three amino acids have been singly, doubly, or triply replaced by a Phe residue, to perform a detailed study on H-bonding interactions between the protein and heme-bound fluoride. By appropriate choice of the excitation conditions, ν(Fe-F) stretching bands have been detected in the resonance Raman spectra. In the wild-type protein and one of the mutants, two ν(Fe-F) bands have been observed and assigned to the presence of two protein conformers where fluoride is singly or doubly H-bonded. Furthermore, by plotting the CT1 charge-transfer transition energy vs the ν(Fe-F) wavenumbers, an empirical correlation has been found. The data are well fitted by a straight line with a positive slope. The position along the correlation line can be considered as a novel, general spectroscopic indicator of the extent of H-bonding in the active site of heme proteins. In agreement with the spectroscopic results, we have observed that the rate of ligand dissociation in stopped-flow kinetic measurements progressively increases upon substitution of the H-bonding amino acids. Molecular dynamics simulations have been performed on the fluoride complexes of native and mutated forms, indicating the prevalent interactions at the active site. All the techniques yield evidence that TrpG8 and TyrCD1 can form strong H bonds with fluoride, whereas TyrB10 plays only a minor role in the stabilization of the ligand. © 2011 American Chemical Society.

Registro:

Documento: Artículo
Título:Fluoride as a probe for h-bonding interactions in the active site of heme proteins: The case of thermobifida fusca hemoglobin
Autor:Nicoletti, F.P.; Droghetti, E.; Boechi, L.; Bonamore, A.; Sciamanna, N.; Estrin, D.A.; Feis, A.; Boffi, A.; Smulevich, G.
Filiación:Dipartimento di Chimica Ugo Schiff, Università di Firenze, Via della Lastruccia 3-13, I-50019 Sesto Fiorentino (FI), Italy
Departamento de Química Inorgánica, Analítica y Química Física/INQUIMAE-CONICET, Ciudad Universitaria, Pabellón II, Buenos Aires (C1428EHA), Argentina
Institute Pasteur, Department of Biochemical Sciences and CNR, University of Rome La Sapienza, Piazzale Aldo Moro 5, I-00185 Rome, Italy
Palabras clave:Active site; Bacterial hemoglobin; Charge transfer transitions; Empirical correlations; Excitation conditions; Fluoride complexes; Functional properties; H-bonded; H-bonding; H-bonding interaction; H-bonds; Heme proteins; Ligand dissociation; Molecular dynamics simulations; Polar amino acids; Resonance Raman spectra; Stopped-flow kinetics; Stretching bands; Thermobifida fusca; Wave numbers; Wild-type proteins; Amino acids; Charge transfer; Hemoglobin; Hydrogen bonds; Ligands; Molecular dynamics; Porphyrins; Proteins; amino acid; fluoride; hemoglobin; hemoprotein; ligand; phenylalanine; article; dissociation; excitation; flow kinetics; hydrogen bond; molecular dynamics; mutant; Raman spectrometry; simulation; Thermobifida fusca; wild type; Actinomycetales; Bacterial Proteins; Catalytic Domain; Fluorides; Hydrogen Bonding; Molecular Dynamics Simulation; Mutation; Protein Binding; Spectrophotometry; Spectrum Analysis, Raman; Truncated Hemoglobins
Año:2011
Volumen:133
Número:51
Página de inicio:20970
Página de fin:20980
DOI: http://dx.doi.org/10.1021/ja209312k
Título revista:Journal of the American Chemical Society
Título revista abreviado:J. Am. Chem. Soc.
ISSN:00027863
CODEN:JACSA
CAS:amino acid, 65072-01-7; fluoride, 16984-48-8; hemoglobin, 9008-02-0; phenylalanine, 3617-44-5, 63-91-2; Bacterial Proteins; Fluorides; Truncated Hemoglobins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00027863_v133_n51_p20970_Nicoletti

Referencias:

  • Ma, L.H., Liu, Y., Zhang, X., Yoshida, T., La Mar, G.N., 1H NMR study of the magnetic properties and electronic structure of the hydroxide complex of substrate-bound heme oxygenase from Neisseria meningitidis: Influence of the axial water deprotonation on the distal H-bond network (2006) J. Am. Chem. Soc., 128, pp. 6657-6668
  • Streit, B.R., Blanc, B., Lukat-Rodgers, G.S., Rodgers, K.R., Dubois, J.L., How active-site protonation state influences the reactivity and ligation of the heme in chlorite dismutase (2010) J. Am. Chem. Soc., 132, pp. 5711-5724
  • Edwards, S.L., Poulos, T.L., Ligand binding and structural perturbations in cytochrome c peroxidase. A crystallographic study (1990) J. Biol. Chem., 265, pp. 2588-2595
  • Egawa, T., Yeh, S.-R., Structural and functional properties of hemoglobins from unicellular organisms as revealed by resonance Raman spectroscopy (2005) Journal of Inorganic Biochemistry, 99 (1), pp. 72-96. , DOI 10.1016/j.jinorgbio.2004.10.017, PII S0162013404003228, Heme-Diatomic Interactions, Part 1
  • Feis, A., Lapini, A., Catacchio, B., Brogioni, S., Foggi, P., Chiancone, E., Boffi, A., Smulevich, G., Unusually strong H-bonding to the heme ligand and fast geminate recombination dynamics of the carbon monoxide complex of Bacillus subtilis truncated hemoglobin (2008) Biochemistry, 47, pp. 902-910
  • Ouellet, H., Juszczak, L., Dantsker, D., Samuni, U., Ouellet, Y.H., Savard, P.-Y., Wittenberg, J.B., Guertin, M., Reactions of Mycobacterium tuberculosis truncated hemoglobin O with ligands reveal a novel ligand-inclusive hydrogen bond network (2003) Biochemistry, 42 (19), pp. 5764-5774. , DOI 10.1021/bi0270337
  • Rodriguez, J.C., Zeng, Y., Wilks, A., Rivera, M., The hydrogen-bonding network in heme oxygenase also functions as a modulator of enzyme dynamics: Chaotic motions upon disrupting the H-bond network in heme oxygenase from Pseudomonas aeruginosa (2007) Journal of the American Chemical Society, 129 (38), pp. 11730-11742. , DOI 10.1021/ja072405q
  • Ye, X., Demidov, A., Rosca, F., Wang, W., Kumar, A., Ionascu, D., Zhu, L., Champion, P.M., Investigations of Heme Protein Absorption Line Shapes, Vibrational Relaxation, and Resonance Raman Scattering on Ultrafast Time Scales (2003) J. Phys. Chem. A, 107, pp. 8156-8165
  • Springer, B.A., Sligar, S.G., Olson, J.S., Phillips Jr., G.N., Mechanisms of ligand recognition in myoglobin (1994) Chemical Reviews, 94 (3), pp. 699-714
  • Quillin, M.L., Li, T., Olson, J.S., Phillips Jr., G.N., Dou, Y., Ikeda-Saito, M., Regan, R., Li, H., Structural and functional effects of apolar mutations of the distal valine in myoglobin (1995) J. Mol. Biol., 245, pp. 416-436
  • Wittenberg, J.B., Bolognesi, M., Wittenberg, B.A., Guertin, M., Truncated hemoglobins: A new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants (2002) Journal of Biological Chemistry, 277 (2), pp. 871-874. , DOI 10.1074/jbc.R100058200
  • Bonamore, A., Ilari, A., Giangiacomo, L., Bellelli, A., Morea, V., Boffi, A., A novel thermostable hemoglobin from the actinobacterium Thermobifida fusca (2005) FEBS Journal, 272 (16), pp. 4189-4201. , DOI 10.1111/j.1742-4658.2005.04831.x
  • Nicoletti, F.P., Comandini, A., Bonamore, A., Boechi, L., Boubeta, F.M., Feis, A., Smulevich, G., Boffi, A., Sulfide Binding Properties of Truncated Hemoglobins (2010) Biochemistry, 49, pp. 2269-2278
  • Droghetti, E., Nicoletti, F.P., Bonamore, A., Boechi, L., Arroyo Manez, P., Estrin, D.A., Boffi, A., Feis, A., Heme pocket structural properties of a bacterial truncated hemoglobin from Thermobifida fusca (2010) Biochemistry, 49, pp. 10394-10402
  • Droghetti, E., Nicoletti, F.P., Bonamore, A., Sciamanna, N., Boffi, A., Feis, A., Smulevich, G., The optical spectra of fluoride complexes can effectively probe H-bonding interactions in the distal cavity of heme proteins (2011) J. Inorg. Biochem., 105, pp. 1338-1343
  • Jorgensen, W.L., Chandrasekar, J., Madura, J., Impey, R.W., Klein, M.L., Comparison of simple potential functions for simulating liquid water (1983) J. Chem. Phys., 79, pp. 926-935
  • Luty, B.A., Tironi, I.G., Van Gunsteren, W.F., Lattice-sum methods for calculating electrostatic interactions in molecular simulations (1995) J. Chem. Phys., 103, pp. 3014-3021
  • Pearlman, D.A., Case, D.A., Caldwell, J.W., Ross, W.S., Cheatham, T.E., Debolt, S., Ferguson, D., Kollman, P., AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules (1995) Comput. Phys. Commun., 91, pp. 1-41
  • Boechi, L., Manez, P.A., Luque, F.J., Marti, M.A., Estrin, D.A., Unraveling the molecular basis for ligand binding in truncated hemoglobins: The trHbO Bacillus subtilis case (2010) Proteins, 78, pp. 962-970
  • Boechi, L., Marti, M.A., Milani, M., Bolognesi, M., Luque, F.J., Estrin, D.A., Structural determinants of ligand migration in Mycobacterium tuberculosis truncated hemoglobin O (2008) Proteins, 73, pp. 372-379
  • Crespo, A., Marti, M.A., Kalko, S.G., Morreale, A., Orozco, M., Gelpi, J.L., Luque, F.J., Estrin, D.A., Theoretical study of the truncated hemoglobin HbN: Exploring the molecular basis of the NO detoxification mechanism (2005) Journal of the American Chemical Society, 127 (12), pp. 4433-4444. , DOI 10.1021/ja0450004
  • Marti, M.A., Capece, L., Bikiel, D.E., Falcone, B., Estrin, D.A., Oxygen affinity controlled by dynamical distal conformations: The soybean leghemoglobin and the Paramecium caudatum hemoglobin cases (2007) Proteins: Structure, Function and Genetics, 68 (2), pp. 480-487. , DOI 10.1002/prot.21454
  • Ye, L., Spiteller, D., Ullrich, R., Boland, W., Nuske, J., Diekert, G., Fluoride-dependent conversion of organic compounds mediated by manganese peroxidases in the absence of Mn (2+) ions (2010) Biochemistry, 49, pp. 7264-7271
  • Asher, S.A., Adams, M.L., Schuster, T.M., Resonance Raman and absorption spectroscopic detection of distal histidine-fluoride interactions in human methemoglobin fluoride and sperm whale metmyoglobin fluoride: Measurements of distal histidine ionization constants (1981) Biochemistry, 20 (12), pp. 3339-3346. , DOI 10.1021/bi00515a004
  • Beetlestone, J., George, P., A Magnetochemical Study of Equilibria between High and Low Spin States of Metmyoglobin Complexes (1964) Biochemistry, 3, pp. 707-714
  • Tamura, M., Optical and magnetic measurements of horseradish peroxidase. II. pH dependence of peroxidase (1971) Biochim. Biophys. Acta, 243, pp. 249-258
  • Yonetani, T., Wilson, D.F., Seamonds, B., Studies on cytochrome c peroxidase. 8. The effect of temperature on light absorptions of the enzyme and its derivatives (1966) J. Biol. Chem., 241, pp. 5347-5352
  • Makinen, M.W., Churg, A.K., (1983) Iron Porphyrins, (PART 1), pp. 143-225. , Lever, A.PB.P; Gray, H.B. Eds, Addison-Wesley Publishing Compay, Reading, USA
  • Asher, S.A., Vickery, L.E., Schuster, T.M., Sauer, K., Resonance Raman spectra of methemoglobin derivatives. Selective enhancement of axial ligand vibrations and lack of an effect of inositol hexaphosphate (1977) Biochemistry, 16 (26), pp. 5849-5856
  • Desbois, A., Lutz, M., Banerjee, R., Low-Frequency Vibrations in Resonance Raman Spectra of Horse Heart Myoglobin. Iron-Ligand and Iron-Nitrogen Vibrational Modes (1979) Biochemistry, 18, pp. 1510-1518
  • Yu, N.T., Resonance Raman studies of ligand binding (1986) Methods Enzymol., 150, pp. 350-409
  • Neri, F., Kok, D., Miller, M.A., Smulevich, G., Fluoride binding in hemoproteins: The importance of the distal cavity structure (1997) Biochemistry, 36 (29), pp. 8947-8953. , DOI 10.1021/bi970248+
  • Deatherage, J.F., Loe, R.S., Anderson, C.M., Moffat, K., Structure of cyanide methemoglobin (1976) J. Mol. Biol., 104, pp. 687-706
  • Aime, S., Fasano, M., Paoletti, S., Cutruzzola, F., Desideri, A., Bolognesi, M., Rizzi, M., Ascenzi, P., Structural determinants of fluoride and formate binding to hemoglobin and myoglobin: Crystallographic and 1H-NMR relaxometric study (1996) Biophysical Journal, 70 (1), pp. 482-488
  • Coletta, M., Ascoli, F., Brunori, M., Traylor, T.G., PH dependence of carbon monoxide binding to ferrous horseradish peroxidase (1986) Journal of Biological Chemistry, 261 (21), pp. 9811-9814
  • Feis, A., Santoni, E., Neri, F., Ciaccio, C., De Sanctis, G., Coletta, M., Welinder, K.G., Smulevich, G., Fine-tuning of the binding and dissociation of CO by the amino acids of the heme pocket of Coprinus cinereus peroxidase (2002) Biochemistry, 41 (44), pp. 13264-13273. , DOI 10.1021/bi026203c
  • Belyea, J., Belyea, C.M., Lappi, S., Franzen, S., Resonance raman study of ferric heme adducts of dehaloperoxidase from Amphitrite ornata (2006) Biochemistry, 45 (48), pp. 14275-14284. , DOI 10.1021/bi0609218
  • Feis, A., Rodriguez-Lopez, J.N., Thorneley, R.N.F., Smulevich, G., The distal cavity structure of carbonyl horseradish peroxidase as probed by the resonance Raman spectra of His 42 Leu and Arg 38 Leu mutants (1998) Biochemistry, 37 (39), pp. 13575-13581. , DOI 10.1021/bi981399v
  • Nicoletti, F.P., Thompson, M.K., Howes, B.D., Franzen, S., Smulevich, G., New Insights into the Role of Distal Histidine Flexibility in Ligand Stabilization of Dehaloperoxidase-Hemoglobin from Amphitrite ornata (2010) Biochemistry, 49, pp. 1903-1912
  • Smulevich, G., Mantini, A.R., Paoli, M., Coletta, M., Geraci, G., Resonance Raman studies of the heme active site of the homodimeric myoglobin from Nassa mutabilis: A peculiar case (1995) Biochemistry, 34, pp. 7507-7516
  • Spiro, T.G., Wasbotten, I.H., CO as a vibrational probe of heme protein active sites (2005) Journal of Inorganic Biochemistry, 99 (1), pp. 34-44. , DOI 10.1016/j.jinorgbio.2004.09.026, PII S0162013404002934, Heme-Diatomic Interactions, Part 1
  • Phillips Jr., G.N., Teodora, M.L., Li, T., Smith, B., Olson, J.S., Bound CO Is a Molecular Probe of Electrostatic Potential in the Distal Pocket of Myoglobin (1999) Journal of Physical Chemistry B, 103 (42), pp. 8817-8829
  • Spiro, T.G., Li, X.-Y., (1988) Biological Application of Raman Spectroscopy, 3, pp. 1-37. , Spiro, T. G. Wiley Interscience: New York
  • Kalsbeck, W.A., Ghosh, A., Pandey, R.K., Smith, K.M., Bocian, D.F., Determinants of the vinyl stretching frequency in protoporphyrins. Implications for cofactor-protein interactions in heme proteins (1995) Journal of the American Chemical Society, 117 (44), pp. 10959-10968. , DOI 10.1021/ja00149a019
  • Marzocchi, M.P., Smulevich, G., Relationship between heme vinyl conformation and the protein matrix in peroxidases (2003) J. Raman Spectrosc., 34, pp. 725-736
  • Neri, F., Indiani, C., Baldi, B., Vind, J., Welinder, K.G., Smulevich, G., Role of the distal phenylalanine 54 on the structure, stability, and ligand binding of Coprinus cinereus peroxidase (1999) Biochemistry, 38, pp. 7819-7827
  • Sage, J.T., Morikis, D., Champion, P.M., Spectroscopic studies of myoglobin at low pH: Heme structure and ligation (1991) Biochemistry, 30, pp. 1227-1237

Citas:

---------- APA ----------
Nicoletti, F.P., Droghetti, E., Boechi, L., Bonamore, A., Sciamanna, N., Estrin, D.A., Feis, A.,..., Smulevich, G. (2011) . Fluoride as a probe for h-bonding interactions in the active site of heme proteins: The case of thermobifida fusca hemoglobin. Journal of the American Chemical Society, 133(51), 20970-20980.
http://dx.doi.org/10.1021/ja209312k
---------- CHICAGO ----------
Nicoletti, F.P., Droghetti, E., Boechi, L., Bonamore, A., Sciamanna, N., Estrin, D.A., et al. "Fluoride as a probe for h-bonding interactions in the active site of heme proteins: The case of thermobifida fusca hemoglobin" . Journal of the American Chemical Society 133, no. 51 (2011) : 20970-20980.
http://dx.doi.org/10.1021/ja209312k
---------- MLA ----------
Nicoletti, F.P., Droghetti, E., Boechi, L., Bonamore, A., Sciamanna, N., Estrin, D.A., et al. "Fluoride as a probe for h-bonding interactions in the active site of heme proteins: The case of thermobifida fusca hemoglobin" . Journal of the American Chemical Society, vol. 133, no. 51, 2011, pp. 20970-20980.
http://dx.doi.org/10.1021/ja209312k
---------- VANCOUVER ----------
Nicoletti, F.P., Droghetti, E., Boechi, L., Bonamore, A., Sciamanna, N., Estrin, D.A., et al. Fluoride as a probe for h-bonding interactions in the active site of heme proteins: The case of thermobifida fusca hemoglobin. J. Am. Chem. Soc. 2011;133(51):20970-20980.
http://dx.doi.org/10.1021/ja209312k