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Abstract:

Hydrogen sulfide (H2S) was recently discovered as a gasotransmitter, capable of coordinating to the heme iron of hemeproteins. H2S is unique for its ability to render varying concentrations of the nucleophilic conjugate bases (HS- or S2-), either as free or bound species with expected outcomes on its further reactivity. There is no direct evidence about which species (H2S, HS-, or S2-) coordinates to the iron. We performed computer simulations to address the migration and binding processes of H2S species to the hemoglobin I of Lucina pectinata, which exhibits the highest affinity for the substrate measured to date. We found that H2S is the most favorable species in the migration from the bulk to the active site, through an internal pathway of the protein. After the coordination of H2S, an array of clustered water molecules modifies the active site environment, and assists in the subsequent deprotonation of the ligand, forming Fe(III)-SH-. The feasibility of the second deprotonation of the coordinated ligand is also discussed. © 2016 American Chemical Society.

Registro:

Documento: Artículo
Título:Access and Binding of H2S to Hemeproteins: The Case of HbI of Lucina pectinata
Autor:Boubeta, F.M.; Bari, S.E.; Estrin, D.A.; Boechi, L.
Filiación:Departamento de Química Inorgánica, Analítica y Química Física/INQUIMAE-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pab. II, Buenos Aires, C1428EHA, Argentina
Instituto de Cálculo/CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pab. II, Buenos Aires, C1428EHA, Argentina
Palabras clave:Ligands; Molecules; Active site; Binding process; Bound species; Clustered water; Coordinated ligands; Heme-proteins; Lucina pectinata; Nucleophilic conjugate basis; Bins; hemoglobin; hemoprotein; hydrogen sulfide; animal; binding site; bivalve; chemistry; conformation; molecular dynamics; Animals; Binding Sites; Bivalvia; Hemeproteins; Hemoglobins; Hydrogen Sulfide; Molecular Conformation; Molecular Dynamics Simulation
Año:2016
Volumen:120
Número:36
Página de inicio:9642
Página de fin:9653
DOI: http://dx.doi.org/10.1021/acs.jpcb.6b06686
Título revista:Journal of Physical Chemistry B
Título revista abreviado:J Phys Chem B
ISSN:15206106
CODEN:JPCBF
CAS:hemoglobin, 9008-02-0; hydrogen sulfide, 15035-72-0, 7783-06-4; Hemeproteins; Hemoglobins; Hydrogen Sulfide
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_15206106_v120_n36_p9642_Boubeta

Referencias:

  • Warenycia, M.W., Goodwin, L.R., Benishin, C.G., Reiffenstein, R.J., Francom, D.M., Taylor, J.D., Dieken, F.P., Acute Hydrogen Sulfide Poisoning. Demonstration of Selective Uptake of Sulfide by the Brainstem by Measurement of Brain Sulfide Levels (1989) Biochem. Pharmacol., 38 (6), pp. 973-981
  • Goodwin, L.R., Francom, D., Dieken, F.P., Taylor, J.D., Warenycia, M.W., Reiffenstein, R.J., Dowling, G., Determination of Sulfide in Brain Tissue by Gas Dialysis/Ion Chromatography: Postmortem Studies and Two Case Reports (1989) J. Anal. Toxicol., 13 (2), pp. 105-109
  • Furne, J., Saeed, A., Levitt, M.D., Whole Tissue Hydrogen Sulfide Concentrations Are Orders of Magnitude Lower than Presently Accepted Values (2008) AJP Regul. Integr. Comp. Physiol., 295 (5), pp. R1479-R1485
  • Ishigami, M., Hiraki, K., Umemura, K., Ogasawara, Y., Ishii, K., Kimura, H., A Source of Hydrogen Sulfide and a Mechanism of Its Release in the Brain (2009) Antioxid. Redox Signaling, 11 (2), pp. 205-214
  • Wintner, E.A., Deckwerth, T.L., Langston, W., Bengtsson, A., Leviten, D., Hill, P., Insko, M.A., Szabo, C., A Monobromobimane-Based Assay to Measure the Pharmacokinetic Profile of Reactive Sulphide Species in Blood: Monobromobimane Assay for Sulphide Detection (2010) Br. J. Pharmacol., 160 (4), pp. 941-957
  • Abe, K., Kimura, H., The Possible Role of Hydrogen Sulfide as an Endogenous Neuromodulator (1996) J. Neurosci. Off. J. Soc. Neurosci., 16 (3), pp. 1066-1071
  • Hosoki, R., Matsuki, N., Kimura, H., The Possible Role of Hydrogen Sulfide as an Endogenous Smooth Muscle Relaxant in Synergy with Nitric Oxide (1997) Biochem. Biophys. Res. Commun., 237 (3), pp. 527-531
  • Moore, P.K., Whiteman, M., Chemistry, Biochemistry and Pharmacology of Hydrogen Sulfide (2015) Handbook of Experimental Pharmacology 230, , Eds. In; Springer International Publishing: Switzerland
  • Zhang, H., Tang, J., Liu, X.-P., Wang, Y., Yu, W., Peng, W.-Y., Fang, F., Hu, L.-Y., Hydrogen Sulfide Promotes Root Organogenesis in Ipomoea Batatas, Salix Matsudana and Glycine Max (2009) J. Integr. Plant Biol., 51 (12), pp. 1086-1094
  • Zhang, H., Hu, L.-Y., Hu, K.-D., He, Y.-D., Wang, S.-H., Luo, J.-P., Hydrogen Sulfide Promotes Wheat Seed Germination and Alleviates Oxidative Damage against Copper Stress (2008) J. Integr. Plant Biol., 50 (12), pp. 1518-1529
  • Jin, Z., Pei, Y., Physiological Implications of Hydrogen Sulfide in Plants: Pleasant Exploration behind Its Unpleasant Odour (2015) Oxid. Med. Cell. Longevity, 2015, pp. 1-6
  • Papenbrock, J., Riemenschneider, A., Kamp, A., Schulz-Vogt, H.N., Schmidt, A., Characterization of Cysteine-Degrading and H 2 S-Releasing Enzymes of Higher Plants - From the Field to the Test Tube and Back (2007) Plant Biol., 9 (5), pp. 582-588
  • Ida, T., Sawa, T., Ihara, H., Tsuchiya, Y., Watanabe, Y., Kumagai, Y., Suematsu, M., Akaike, T., Reactive Cysteine Persulfides and S-Polythiolation Regulate Oxidative Stress and Redox Signaling (2014) Proc. Natl. Acad. Sci. U. S. A., 111 (21), pp. 7606-7611
  • Kimura, H., Physiological Role of Hydrogen Sulfide and Polysulfide in the Central Nervous System (2013) Neurochem. Int., 63 (5), pp. 492-497
  • Greiner, R., Pálinkás, Z., Bäsell, K., Becher, D., Antelmann, H., Nagy, P., Dick, T.P., Polysulfides Link H 2 S to Protein Thiol Oxidation (2013) Antioxid. Redox Signaling, 19 (15), pp. 1749-1765
  • Filipovic, M.R., Persulfidation (S-Sulfhydration) and H2S (2015) Chemistry, Biochemistry and Pharmacology of Hydrogen Sulfide, 230, pp. 29-59. , Moore, P. K. Whiteman, M. Springer International Publishing: Cham, Switzerland
  • Ono, K., Akaike, T., Sawa, T., Kumagai, Y., Wink, D.A., Tantillo, D.J., Hobbs, A.J., Fukuto, J.M., Redox Chemistry and Chemical Biology of H2S, Hydropersulfides, and Derived Species: Implications of Their Possible Biological Activity and Utility (2014) Free Radical Biol. Med., 77, pp. 82-94
  • Nishimori, I., Vullo, D., Minakuchi, T., Scozzafava, A., Osman, S.M., AlOthman, Z., Capasso, C., Supuran, C.T., Anion Inhibition Studies of Two New β-Carbonic Anhydrases from the Bacterial Pathogen Legionella Pneumophila (2014) Bioorg. Med. Chem. Lett., 24 (4), pp. 1127-1132
  • Kabil, O., Banerjee, R., Redox Biochemistry of Hydrogen Sulfide (2010) J. Biol. Chem., 285 (29), pp. 21903-21907
  • Kajimura, M., Fukuda, R., Bateman, R.M., Yamamoto, T., Suematsu, M., Interactions of Multiple Gas-Transducing Systems: Hallmarks and Uncertainties of CO, NO, and H 2 S Gas Biology (2010) Antioxid. Redox Signaling, 13 (2), pp. 157-192
  • Li, Q., Lancaster, J.R., Chemical Foundations of Hydrogen Sulfide Biology (2013) Nitric Oxide, 35, pp. 21-34
  • Cooper, C.E., Brown, G.C., The Inhibition of Mitochondrial Cytochrome Oxidase by the Gases Carbon Monoxide, Nitric Oxide, Hydrogen Cyanide and Hydrogen Sulfide: Chemical Mechanism and Physiological Significance (2008) J. Bioenerg. Biomembr., 40 (5), pp. 533-539
  • Hughes, M.N., Centelles, M.N., Moore, K.P., Making and Working with Hydrogen Sulfide (2009) Free Radical Biol. Med., 47 (10), pp. 1346-1353
  • Szabó, C., Hydrogen Sulphide and Its Therapeutic Potential (2007) Nat. Rev. Drug Discovery, 6 (11), pp. 917-935
  • Wagner, F., Asfar, P., Calzia, E., Radermacher, P., Szabó, C., Bench-to-Bedside Review: Hydrogen Sulfide - The Third Gaseous Transmitter: Applications for Critical Care (2009) Crit. Care, 13 (3), p. 213
  • Wever, R., Van Gelder, B.F., Dervartanian, D.V., Biochemical and Biophysical Studies on Cytochrome c Oxidase. XX. Reaction with Sulphide (1975) Biochim. Biophys. Acta, Bioenerg., 387 (2), pp. 189-193
  • Collman, J.P., Ghosh, S., Dey, A., Decreau, R.A., Using a Functional Enzyme Model to Understand the Chemistry behind Hydrogen Sulfide Induced Hibernation (2009) Proc. Natl. Acad. Sci. U. S. A., 106 (52), pp. 22090-22095
  • Blackstone, E., H2S Induces a Suspended Animation-Like State in Mice (2005) Science, 308 (5721), p. 518
  • Leslie, M., MEDICINE: Nothing Rotten about Hydrogen Sulfide's Medical Promise (2008) Science, 320 (5880), pp. 1155-1157
  • Chatfield, M.J., La Mar, G.N., Balch, A.L., Lecomte, J.T.J., Multiple Forms of Sulfmyoglobin as Detected by 1H Nuclear Magnetic Resonance Spectroscopy (1986) Biochem. Biophys. Res. Commun., 135 (1), pp. 309-315
  • Vitvitsky, V., Yadav, P.K., Kurthen, A., Banerjee, R., Sulfide Oxidation by a Noncanonical Pathway in Red Blood Cells Generates Thiosulfate and Polysulfides (2015) J. Biol. Chem., 290 (13), pp. 8310-8320
  • Kraus, D.W., Wittenberg, J.B., Hemoglobins of the Lucina Pectinata/bacteria Symbiosis. I. Molecular Properties, Kinetics and Equilibria of Reactions with Ligands (1990) J. Biol. Chem., 265 (27), pp. 16043-16053
  • Pietri, R., Lewis, A., León, R.G., Casabona, G., Kiger, L., Yeh, S.-R., Fernandez-Alberti, S., López-Garriga, J., Factors Controlling the Reactivity of Hydrogen Sulfide with Hemeproteins (2009) Biochemistry, 48 (22), pp. 4881-4894
  • Bieza, S.A., Boubeta, F., Feis, A., Smulevich, G., Estrin, D.A., Boechi, L., Bari, S.E., Reactivity of Inorganic Sulfide Species toward a Heme Protein Model (2015) Inorg. Chem., 54 (2), pp. 527-533
  • Watanabe, K., Suzuki, T., Kitagishi, H., Kano, K., Reaction between a Haemoglobin Model Compound and Hydrosulphide in Aqueous Solution (2015) Chem. Commun., 51 (19), pp. 4059-4061
  • 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 (10), pp. 2269-2278
  • Bakan, A., Kapralov, A.A., Bayir, H., Hu, F., Kagan, V.E., Bahar, I., Inhibition of Peroxidase Activity of Cytochrome c: De Novo Compound Discovery and Validation (2015) Mol. Pharmacol., 88 (3), pp. 421-427
  • Vidossich, P., Alfonso-Prieto, M., Carpena, X., Fita, I., Loewen, P.C., Rovira, C., The Dynamic Role of Distal Side Residues in Heme Hydroperoxidase Catalysis. Interplay between X-Ray Crystallography and Ab Initio MD Simulations (2010) Arch. Biochem. Biophys., 500 (1), pp. 37-44
  • Fernández-Fueyo, E., Acebes, S., Ruiz-Duenas, F.J., Martínez, M.J., Romero, A., Medrano, F.J., Guallar, V., Martínez, A.T., Structural Implications of the C-Terminal Tail in the Catalytic and Stability Properties of Manganese Peroxidases from Ligninolytic Fungi (2014) Acta Crystallogr., Sect. D: Biol. Crystallogr., 70 (12), pp. 3253-3265
  • Ramirez, E., Cruz, A., Rodriguez, D., Uchima, L., Pietri, R., Santana, A., López-Garriga, J., López, G.E., Effects of Active Site Mutations in Haemoglobin i from Lucina Pectinata: A Molecular Dynamic Study (2008) Mol. Simul., 34 (7), pp. 715-725
  • Campomanes, P., Rothlisberger, U., Alfonso-Prieto, M., Rovira, C., The Molecular Mechanism of the Catalase-like Activity in Horseradish Peroxidase (2015) J. Am. Chem. Soc., 137 (34), pp. 11170-11178
  • Fields, J.B., Hollingsworth, S.A., Chreifi, G., Heyden, M., Arce, A.P., Magana-Garcia, H.I., Poulos, T.L., Tobias, D.J., Bind and Crawl" Association Mechanism of Leishmania Major Peroxidase and Cytochrome c Revealed by Brownian and Molecular Dynamics Simulations (2015) Biochemistry, 54 (49), pp. 7272-7282
  • Navapour, L., Mogharrab, N., Amininasab, M., How Modification of Accessible Lysines to Phenylalanine Modulates the Structural and Functional Properties of Horseradish Peroxidase: A Simulation Study (2014) PLoS One, 9 (10), p. e109062
  • Case, D.A., Babin, V., Berryman, J.T., Betz, R.M., Cai, Q., Cerutti, D.S., Cheatham, T.E., III, Gohlke, H., (2014) AMBER 14, , University of California: San Francisco, CA
  • Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J.L., Dror, R.O., Shaw, D.E., Improved Side-Chain Torsion Potentials for the Amber ff99SB Protein Force Field (2010) Proteins: Struct., Funct., Genet., 78, pp. 1950-1958
  • (2004) Gaussian 03, , Gaussian, Inc. Wallingford, CT
  • Soldatova, A.V., Ibrahim, M., Olson, J.S., Czernuszewicz, R.S., Spiro, T.G., New Light on NO Bonding in Fe(III) Heme Proteins from Resonance Raman Spectroscopy and DFT Modeling (2010) J. Am. Chem. Soc., 132 (13), pp. 4614-4625
  • Marti, M.A., Crespo, A., Capece, L., Boechi, L., Bikiel, D.E., Scherlis, D.A., Estrin, D.A., Dioxygen Affinity in Heme Proteins Investigated by Computer Simulation (2006) J. Inorg. Biochem., 100 (4), pp. 761-770
  • Capece, L., Marti, M.A., Crespo, A., Doctorovich, F., Estrin, D.A., Heme Protein Oxygen Affinity Regulation Exerted by Proximal Effects (2006) J. Am. Chem. Soc., 128 (38), pp. 12455-12461
  • Marti, M.A., Capece, L., Bidon-Chanal, A., Crespo, A., Guallar, V., Luque, F.J., Estrin, D.A., Nitric Oxide Reactivity with Globins as Investigated Through Computer Simulation (2008) Methods in Enzymology, 437, pp. 477-498. , Elsevier: Amsterdam
  • Scherlis, D.A., Estrin, D.A., Structure and Spin-State Energetics of an Iron Porphyrin Model: An Assessment of Theoretical Methods (2002) Int. J. Quantum Chem., 87 (3), pp. 158-166
  • Martí, 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: Struct., Funct., Genet., 68 (2), pp. 480-487
  • Perdew, J.P., Burke, K., Ernzerhof, M., Generalized Gradient Approximation Made Simple (1996) Phys. Rev. Lett., 77 (18), pp. 3865-3868
  • Nadra, A.D., Martí, M.A., Pesce, A., Bolognesi, M., Estrin, D.A., Exploring the Molecular Basis of Heme Coordination in Human Neuroglobin (2008) Proteins: Struct., Funct., Genet., 71 (2), pp. 695-705
  • Breneman, C.M., Wiberg, K.B., Determining Atom-Centered Monopoles from Molecular Electrostatic Potentials. The Need for High Sampling Density in Formamide Conformational Analysis (1990) J. Comput. Chem., 11 (3), pp. 361-373
  • Howes, B.D., Giordano, D., Boechi, L., Russo, R., Mucciacciaro, S., Ciaccio, C., Sinibaldi, F., Smulevich, G., The Peculiar Heme Pocket of the 2/2 Hemoglobin of Cold-Adapted Pseudoalteromonas Haloplanktis TAC125 (2011) JBIC, J. Biol. Inorg. Chem., 16 (2), pp. 299-311
  • Capece, L., Lewis-Ballester, A., Yeh, S.-R., Estrin, D.A., Marti, M.A., Complete Reaction Mechanism of Indoleamine 2,3-Dioxygenase as Revealed by QM/MM Simulations (2012) J. Phys. Chem. B, 116 (4), pp. 1401-1413
  • Arroyo Manez, P., Lu, C., Boechi, L., Martí, M.A., Shepherd, M., Wilson, J.L., Poole, R.K., Estrin, D.A., Role of the Distal Hydrogen-Bonding Network in Regulating Oxygen Affinity in the Truncated Hemoglobin III from Campylobacter Jejuni (2011) Biochemistry, 50 (19), pp. 3946-3956
  • Cohen, J., Arkhipov, A., Braun, R., Schulten, K., Imaging the Migration Pathways for O2, CO, NO, and Xe Inside Myoglobin (2006) Biophys. J., 91 (5), pp. 1844-1857
  • Cohen, J., Olsen, K.W., Schulten, K., Finding Gas Migration Pathways in Proteins Using Implicit Ligand Sampling (2008) Methods in Enzymology, 437, pp. 439-457. , Elsevier: Amsterdam
  • Forti, F., Boechi, L., Bikiel, D., Martí, M.A., Nardini, M., Bolognesi, M., Viappiani, C., Luque, F.J., Ligand Migration in Methanosarcina Acetivorans Protoglobin: Effects of Ligand Binding and Dimeric Assembly (2011) J. Phys. Chem. B, 115 (46), pp. 13771-13780
  • Forti, F., Boechi, L., Estrin, D.A., Marti, M.A., Comparing and Combining Implicit Ligand Sampling with Multiple Steered Molecular Dynamics to Study Ligand Migration Processes in Heme Proteins (2011) J. Comput. Chem., 32 (10), pp. 2219-2231
  • Gabba, M., Abbruzzetti, S., Spyrakis, F., Forti, F., Bruno, S., Mozzarelli, A., Luque, F.J., Dewilde, S., CO Rebinding Kinetics and Molecular Dynamics Simulations Highlight Dynamic Regulation of Internal Cavities in Human Cytoglobin (2013) PLoS One, 8 (1), p. e49770
  • Oliveira, A., Singh, S., Bidon-Chanal, A., Forti, F., Martí, M.A., Boechi, L., Estrin, D.A., Luque, F.J., Role of PheE15 Gate in Ligand Entry and Nitric Oxide Detoxification Function of Mycobacterium Tuberculosis Truncated Hemoglobin N (2012) PLoS One, 7 (11), p. e49291
  • Humphrey, W., Dalke, A., Schulten, K., VMD: Visual Molecular Dynamics (1996) J. Mol. Graphics, 14 (1), pp. 33-38
  • Isralewitz, B., Gao, M., Schulten, K., Steered Molecular Dynamics and Mechanical Functions of Proteins (2001) Curr. Opin. Struct. Biol., 11 (2), pp. 224-230
  • Jensen, M.O., Park, S., Tajkhorshid, E., Schulten, K., Energetics of Glycerol Conduction through Aquaglyceroporin GlpF (2002) Proc. Natl. Acad. Sci. U. S. A., 99 (10), pp. 6731-6736
  • Jarzynski, C., Nonequilibrium Equality for Free Energy Differences (1997) Phys. Rev. Lett., 78 (14), pp. 2690-2693
  • Boechi, L., Martí, 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: Struct., Funct., Genet., 73 (2), pp. 372-379
  • Bidon-Chanal, A., Martí, M.A., Crespo, A., Milani, M., Orozco, M., Bolognesi, M., Luque, F.J., Estrin, D.A., Ligand-Induced Dynamical Regulation of NO Conversion in Mycobacterium Tuberculosis Truncated Hemoglobin-N (2006) Proteins: Struct., Funct., Genet., 64 (2), pp. 457-464
  • Di Lella, S., Martí, M.A., Álvarez, R.M.S., Estrin, D.A., Ricci, J.C.D., Characterization of the Galectin-1 Carbohydrate Recognition Domain in Terms of Solvent Occupancy (2007) J. Phys. Chem. B, 111 (25), pp. 7360-7366
  • Gauto, D.F., Di Lella, S., Guardia, C.M.A., Estrin, D.A., Martí, M.A., Carbohydrate-Binding Proteins: Dissecting Ligand Structures through Solvent Environment Occupancy (2009) J. Phys. Chem. B, 113 (25), pp. 8717-8724
  • Gauto, D.F., Di Lella, S., Estrin, D.A., Monaco, H.L., Martí, M.A., Structural Basis for Ligand Recognition in a Mushroom Lectin: Solvent Structure as Specificity Predictor (2011) Carbohydr. Res., 346 (7), pp. 939-948
  • López, E.D., Arcon, J.P., Gauto, D.F., Petruk, A.A., Modenutti, C.P., Dumas, V.G., Marti, M.A., Turjanski, A.G., WATCLUST: A Tool for Improving the Design of Drugs Based on Protein-Water Interactions (2015) Bioinformatics, 31 (22), pp. 3697-3699
  • Crespo, A., Scherlis, D.A., Martí, M.A., Ordejón, P., Roitberg, A.E., Estrin, D.A., A DFT-Based QM-MM Approach Designed for the Treatment of Large Molecular Systems: Application to Chorismate Mutase (2003) J. Phys. Chem. B, 107 (49), pp. 13728-13736
  • Arcon, J.P., Rosi, P., Petruk, A.A., Marti, M.A., Estrin, D.A., Molecular Mechanism of Myoglobin Autoxidation: Insights from Computer Simulations (2015) J. Phys. Chem. B, 119 (5), pp. 1802-1813
  • Choe, Y.-K., Tsuchida, E., Ikeshoji, T., First-Principles Molecular Dynamics Study on Aqueous Sulfuric Acid Solutions (2007) J. Chem. Phys., 126 (15), p. 154510
  • Hu, X.L., Klimeš, J., Michaelides, A., Proton Transfer in Adsorbed Water Dimers (2010) Phys. Chem. Chem. Phys., 12 (16), p. 3953
  • McDonnell, M.T., Xu, H., Keffer, D.J., Ab Initio Molecular Dynamics Simulations of an Excess Proton in a Triethylene Glycol-Water Solution: Solvation Structure, Mechanism, and Kinetics (2016) J. Phys. Chem. B, 120 (23), pp. 5223-5242
  • Zhang, H., Ye, Y.-K., Wang, S.-H., Luo, J.-P., Tang, J., Ma, D.-F., Hydrogen Sulfide Counteracts Chlorophyll Loss in Sweetpotato Seedling Leaves and Alleviates Oxidative Damage against Osmotic Stress (2009) Plant Growth Regul., 58 (3), pp. 243-250
  • Shaik, S., Kumar, D., De Visser, S.P., Altun, A., Thiel, W., Theoretical Perspective on the Structure and Mechanism of Cytochrome P450 Enzymes (2005) Chem. Rev., 105 (6), pp. 2279-2328
  • Senn, H.M., Thiel, W., QM/MM Studies of Enzymes (2007) Curr. Opin. Chem. Biol., 11 (2), pp. 182-187
  • Ranaghan, K.E., Mulholland, A.J., Investigations of Enzyme-Catalysed Reactions with Combined Quantum Mechanics/molecular Mechanics (QM/MM) Methods (2010) Int. Rev. Phys. Chem., 29 (1), pp. 65-133
  • Martí, M.A., Crespo, A., Bari, S.E., Doctorovich, F.A., Estrin, D.A., QM-MM Study of Nitrite Reduction by Nitrite Reductase of Pseudomonas Aeruginosa (2004) J. Phys. Chem. B, 108 (46), pp. 18073-18080
  • Martí, M.A., Capece, L., Crespo, A., Doctorovich, F., Estrin, D.A., Nitric Oxide Interaction with Cytochrome c and Its Relevance to Guanylate Cyclase. Why Does the Iron Histidine Bond Break? (2005) J. Am. Chem. Soc., 127 (21), pp. 7721-7728
  • Crespo, A., Martí, 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) J. Am. Chem. Soc., 127 (12), pp. 4433-4444
  • Nitsche, M.A., Ferreria, M., Mocskos, E.E., González Lebrero, M.C., GPU Accelerated Implementation of Density Functional Theory for Hybrid QM/MM Simulations (2014) J. Chem. Theory Comput., 10 (3), pp. 959-967
  • González Lebrero, M.C., Estrin, D.A., QM-MM Investigation of the Reaction of Peroxynitrite with Carbon Dioxide in Water (2007) J. Chem. Theory Comput., 3 (4), pp. 1405-1411
  • Zeida, A., Babbush, R., González Lebrero, M.C., Trujillo, M., Radi, R., Estrin, D.A., Molecular Basis of the Mechanism of Thiol Oxidation by Hydrogen Peroxide in Aqueous Solution: Challenging the S N 2 Paradigm (2012) Chem. Res. Toxicol., 25 (3), pp. 741-746
  • Bustamante, J.P., Abbruzzetti, S., Marcelli, A., Gauto, D., Boechi, L., Bonamore, A., Boffi, A., Viappiani, C., Ligand Uptake Modulation by Internal Water Molecules and Hydrophobic Cavities in Hemoglobins (2014) J. Phys. Chem. B, 118 (5), pp. 1234-1245
  • Goldbeck, R.A., Bhaskaran, S., Ortega, C., Mendoza, J.L., Olson, J.S., Soman, J., Kliger, D.S., Esquerra, R.M., Water and Ligand Entry in Myoglobin: Assessing the Speed and Extent of Heme Pocket Hydration after CO Photodissociation (2006) Proc. Natl. Acad. Sci. U. S. A., 103 (5), pp. 1254-1259
  • Ouellet, Y.H., Daigle, R., Lague, P., Dantsker, D., Milani, M., Bolognesi, M., Friedman, J.M., Guertin, M., Ligand Binding to Truncated Hemoglobin N from Mycobacterium Tuberculosis Is Strongly Modulated by the Interplay between the Distal Heme Pocket Residues and Internal Water (2008) J. Biol. Chem., 283 (40), pp. 27270-27278
  • Bustamante, J.P., Szretter, M.E., Sued, M., Martí, M.A., Estrin, D.A., Boechi, L., A Quantitative Model for Oxygen Uptake and Release in a Family of Hemeproteins (2016) Bioinformatics, 32, p. 1805
  • Boechi, L., Arrar, M., Marti, M.A., Olson, J.S., Roitberg, A.E., Estrin, D.A., Hydrophobic Effect Drives Oxygen Uptake in Myoglobin via Histidine E7 (2013) J. Biol. Chem., 288 (9), pp. 6754-6762
  • Scott, E.E., Gibson, Q.H., Olson, J.S., Mapping the Pathways for O2 Entry into and Exit from Myoglobin (2001) J. Biol. Chem., 276 (7), pp. 5177-5188
  • 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: Struct., Funct., Genet., 78 (4), pp. 962-970
  • Capece, L., Boechi, L., Perissinotti, L.L., Arroyo-Manez, P., Bikiel, D.E., Smulevich, G., Marti, M.A., Estrin, D.A., Small Ligand-globin Interactions: Reviewing Lessons Derived from Computer Simulation (2013) Biochim. Biophys. Acta, Proteins Proteomics, 1834 (9), pp. 1722-1738
  • Liphardt, J., Equilibrium Information from Nonequilibrium Measurements in an Experimental Test of Jarzynski's Equality (2002) Science, 296 (5574), pp. 1832-1835
  • Marques, H.M., Perry, C.B., Hemepeptide Models for Hemoproteins: The Behavior of N-Acetylmicroperoxidase-11 in Aqueous Solution (1999) J. Inorg. Biochem., 75 (4), pp. 281-291
  • Brunori, M., Amiconi, G., Antonini, E., Wyman, J., Zito, R., Rossi Fanelli, A., The Transition between "acid" and "alkaline" Ferric Heme Proteins (1968) Biochim. Biophys. Acta, Protein Struct., 154 (2), pp. 315-322
  • Sun, J., Wilks, A., Ortiz De Montellano, P.R., Loehr, T.M., Resonance Raman and EPR Spectroscopic Studies on Heme-Heme Oxygenase Complexes (1993) Biochemistry, 32 (51), pp. 14151-14157
  • Takahashi, S., Wang, J., Rousseau, D.L., Ishikawa, K., Yoshida, T., Host, J.R., Ikeda-Saito, M., Heme-Heme Oxygenase Complex. Structure of the Catalytic Site and Its Implication for Oxygen Activation (1994) J. Biol. Chem., 269 (2), pp. 1010-1014
  • Song, Y., Michonova-Alexova, E., Gunner, M.R., Calculated Proton Uptake on Anaerobic Reduction of Cytochrome C Oxidase: Is the Reaction Electroneutral? (2006) Biochemistry, 45 (26), pp. 7959-7975

Citas:

---------- APA ----------
Boubeta, F.M., Bari, S.E., Estrin, D.A. & Boechi, L. (2016) . Access and Binding of H2S to Hemeproteins: The Case of HbI of Lucina pectinata. Journal of Physical Chemistry B, 120(36), 9642-9653.
http://dx.doi.org/10.1021/acs.jpcb.6b06686
---------- CHICAGO ----------
Boubeta, F.M., Bari, S.E., Estrin, D.A., Boechi, L. "Access and Binding of H2S to Hemeproteins: The Case of HbI of Lucina pectinata" . Journal of Physical Chemistry B 120, no. 36 (2016) : 9642-9653.
http://dx.doi.org/10.1021/acs.jpcb.6b06686
---------- MLA ----------
Boubeta, F.M., Bari, S.E., Estrin, D.A., Boechi, L. "Access and Binding of H2S to Hemeproteins: The Case of HbI of Lucina pectinata" . Journal of Physical Chemistry B, vol. 120, no. 36, 2016, pp. 9642-9653.
http://dx.doi.org/10.1021/acs.jpcb.6b06686
---------- VANCOUVER ----------
Boubeta, F.M., Bari, S.E., Estrin, D.A., Boechi, L. Access and Binding of H2S to Hemeproteins: The Case of HbI of Lucina pectinata. J Phys Chem B. 2016;120(36):9642-9653.
http://dx.doi.org/10.1021/acs.jpcb.6b06686