Protonation of Histidine 55 Affects the Oxygen Access to Heme in the Alpha Chain of the Hemoglobin from the Antarctic Fish Trematomus bernacchii(370 views) Boechi L, Marti MA, Vergara A, Sica F, Mazzarella L, Estrin DA, Merlino A
Iubmb Life (ISSN: 1521-6543, 1521-6551), 2011 Mar; 63(3): 175-182.
Departamentos de Química Biologica y Química Inorgánica, Analítica y Química-Física (INQUIMAE-CONICET), Universidad de Buenos Aires, Ciudad de Buenos Aires, Argentina
Istituto di Biostrutture e Bioimmagini, (C.N.R.), via Mezzocannone 16, Napoli I-80134, Italy
Dipartimento di Chimica Paolo Corradini, Universiàdegli Studi di Napoli Federico II, via Cintia, I-80126 Napoli, Italy
References: Perutz, M.F., Fermi, G., Luisi, B., Shaanan, B., Liddington, R.C., Stereochemistry of cooperative mechanisms in hemoglobin (1987) Acc. Chem. Res., 9, pp. 309-32
Yokoyama, T., Chong, K.T., Miyazaki, G., Morimoto, H., Shih, D.T.-B., Unzai, S., Tame, J.R.H., Park, S.-Y., Novel mechanisms of pH sensitivity in tuna hemoglobin. A structural explanation of the root effect (2004) Journal of Biological Chemistry, 279 (27), pp. 28632-28640. , DOI 10.1074/jbc.M401740200
Brittain, T., The Root effect in hemoglobins (2005) J. Inorg. Biochem., 99, pp. 120-129
Tame, J.R., Wilson, J.C., Weber, R.E., The crystal structures of trout Hb i in the deoxy and carbonmonoxy forms J. Mol. Biol., 259, pp. 749-760
Mylvaganam, S.E., Bonaventura, C., Bonaventura, J., Getzoff, E.D., Structural basis for the root effect in haemoglobin (1996) Nature Structural Biology, 3 (3), pp. 275-283. , DOI 10.1038/nsb0396-275
Berenbrink, M., Koldkjaer, P., Kepp, O., Cossins, A.R., Evolution of oxygen secretion in fishes and the emergence of a complex physiological system (2005) Science, 307 (5716), pp. 1752-1757. , DOI 10.1126/science.1107793
Camardella, L., Caruso, C., D'Avino, R., Di Prisco, G., Rutigliano, B., Tamburini, M., Fermi, G., Perutz, M.F., Hemoglobin of the Antarctic fish Pagothenia bernacchii. Amino acid sequence, oxygen equilibria and crystal structure of its carbonmonoxy derivative (1992) J. Mol. Biol., 224, pp. 449-460
Ito, N., Komiyama, N.H., Fermi, G., Structure of deoxyhemoglobin of the Antarctic fish Pagothenia bernacchii with an analysis of the structural basis of the Root effect by comparison of the liganded and unliganded hemoglobin structures (1995) J. Mol. Biol., 250, pp. 648-658
Mazzarella, L., Vergara, A., Vitagliano, L., Merlino, A., Bonomi, G., Scala, S., Verde, C., Di Prisco, G., High resolution crystal structure of deoxy hemoglobin from Trematomus bernacchii at different pH values: The role of histidine residues in modulating the strength of the root effect (2006) Proteins: Structure, Function and Genetics, 65 (2), pp. 490-498. , DOI 10.1002/prot.21114
Mazzarella, L., Bonomi, G., Lubrano, M.C., Merlino, A., Riccio, A., Vergara, A., Vitagliano, L., Di Prisco, G., Minimal structural requirements for root effect: Crystal structure of the cathodic hemoglobin isolated from the Antarctic fish Trematomus newnesi (2006) Proteins: Structure, Function and Genetics, 62 (2), pp. 316-321. , DOI 10.1002/prot.20709
Mazzarella, L., D'Avino, R., Di Prisco, G., Savino, C., Vitagliano, L., Moody, P.C.E., Zagari, A., Crystal structure of trematomus newnesi haemoglobin re-opens the root effect question (1999) Journal of Molecular Biology, 287 (5), pp. 897-906. , DOI 10.1006/jmbi.1999.2632
Merlino, A., Verde, C., Di Prisco, G., Mazzarella, L., Vergara, A., Reduction of ferric hemoglobin from Trematomus bernacchii in a partial bis-histidyl state produces a deoxy coordination even when encapsulated into the crystal phase (2008) Spectroscopy, 22 (2-3), pp. 143-152. , DOI 10.3233/SPE-2008-0332, XII European Conference on the Spectroscopy of Biological Molecules, Bobigny, France, 1-6 September 2007, Part 1
Merlino, A., Vitagliano, L., Howes, B., Verde, C., Di Prisco, G., Smulevich, G., Sica, F., Vergara, A., Combined crystallographic and spectroscopic analysis of Trematomus bernacchii hemoglobin highlights analogies and differences in the peculiar oxidation pathway of Antarctic fish hemoglobins (2009) Biopolymers, 91, pp. 1117-1125
Vergara, A., Franzese, M., Merlino, A., Bonomi, G., Verde, C., Giordano, D., Di Prisco, G., Mazzarella, L., Correlation between hemichrome stability and the Root effect in tetrameric hemoglobins (2009) Biophys. J., 97, pp. 866-874
Vitagliano, L., Vergara, A., Bonomi, G., Merlino, A., Verde, C., Di Prisco, G., Howes, B.D., Mazzarella, L., Spectroscopic and crystallographic characterization of a tetrameric hemoglobin oxidation reveals structural features of the functional intermediate relaxed/tense state (2008) J. Am. Chem. Soc., 130, pp. 10527-10535
Baldwin, J., Chothia, C., Haemoglobin: The structural changes related to ligand binding and its allosteric mechanism (1979) Journal of Molecular Biology, 129 (2), pp. 175-220. , DOI 10.1016/0022-2836(79)90277-8
Ackers, G.K., Deciphering the molecular code of hemoglobin allostery (1998) Advances in Protein Chemistry, 51, pp. 185-253
Merlino, A., Vergara, A., Sica, F., Aschi, M., Amadei, A., Di Nola, A., Mazzarella, L., Free-energy profile for CO binding to separated chains of human and Trematomus newnesi hemoglobin: Insights from molecular dynamics simulations and perturbed matrix method (2010) J. Phys. Chem. B, 114, pp. 7002-7008
Scott, E.E., Gibson, Q.H., Olson, J.S., Distal histidine stabilizes bound O2 and acts as a gate for ligand entry in both subunits of adult human hemoglobin (2010) J. Biol. Chem., 285, pp. 8840-8854
Tilton, Jr.R.F., Kuntz, Jr.I.D., Petsko, G.A., Cavities in proteins: Structure of a metmyoglobin-xenon complex solved to 1.9 Å (1984) Biochemistry, 23, pp. 2849-2857
Tilton, Jr.R.F., Singh, U.C., Kuntz, Jr.I.D., Kollman, P.A., Protein-ligand dynamics. A 96 picosecond simulation of a myoglobin-xenon complex (1988) J. Mol. Biol., 199, pp. 195-211
Elber, R., Karplus, M., Enhanced sampling in molecular dynamics: Use of the time-dependent Hartree approximation for a simulation of carbon monoxide diffusion through myoglobin (1990) J. Am. Chem. Soc., 112, pp. 9161-9175
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. Bioinf., 73, pp. 372-379
Capece, L., Estrin, D.A., Marti, M.A., Dynamical characterization of the heme NO oxygen binding (HNOX) domain. Insight into soluble guanylate cyclase allosteric transition (2008) Biochemistry, 47, pp. 9416-9427
Perissinotti, L.L., Marti, M.A., Doctorovich, F., Luque, F.J., Estrin, D.A., A microscopic study of the deoxyhemoglobin-catalyzed generation of nitric oxide from nitrite anion (2008) Biochemistry, 47, pp. 9793-9802
Capece, L., Marti, M.A., Bidon-Chanal, A., Nadra, A., Luque, F.J., Estrin, D.A., High pressure reveals structural determinants for globin hexacoordination: Neuroglobin and myoglobin cases (2009) Proteins Struct. Funct. Bioinf., 75, pp. 885-894
Martí, M.A., Estrin, D.A., Roitberg, A.E., Molecular basis for the pH dependent structural transition of Nitrophorin 4 (2009) J. Phys. Chem. B, 113, pp. 2135-2142
Pearlman, D.A., Case, D.A., Caldwell, J.W., Ross, W.S., Cheatham Iii, 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) Comp. Phys. Comm., 91, pp. 1-3. , 1-41
Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A., Simmerling, C., Comparison of multiple amber force fields and development of improved protein backbone parameters (2006) Proteins: Structure, Function and Genetics, 65 (3), pp. 712-725. , DOI 10.1002/prot.21123
Mongan, J., Case, D.A., McCammon, J.A., Constant pH molecular dynamics in generalized born implicit solvent (2004) J. Comput. Chem., 25, pp. 2038-2048
Cohen, J., Olsen, K.W., Schulten, K., Finding gas migration pathways in proteins using implicit ligand sampling (2008) Methods Enzymol., 437, pp. 439-457
Humphrey, W., Dalke, A., Schulten, K., VMD-visual molecular dynamics (1996) J. Mol. Graph., 14, pp. 33-38
Lama, A., Pawaria, S., Bidon-Chanal, A., Anand, A., Gelpí, J.L., Arya, S., Martí, M., Dikshit, K.L., Role of Pre-A motif in nitric oxide scavenging by truncated hemoglobin, HbN, of Mycobacterium tuberculosis (2009) J. Biol. Chem., 284, pp. 14457-14468
Guallar, V., Jarzecki, A.A., Friesner, R.A., Spiro, T.G., Modeling of ligation-induced helix/loop displacements in myoglobin: Toward an understanding of hemoglobin allostery (2006) J. Am. Chem. Soc., 128, pp. 5427-5435
Alcantara, R.E., Xu, C., Spiro, T.G., Guallar, V., A quantum-chemical picture of hemoglobin affinity (2007) Proceedings of the National Academy of Sciences of the United States of America, 104 (47), pp. 18451-18455. , http://www.pnas.org/cgi/reprint/104/47/18451, DOI 10.1073/pnas.0706026104
Perutz, M.F., Mechanisms of cooperativity and allosteric regulation in proteins (1989) Q. Rev. Biophys., 22, pp. 139-237
Vallone, B., Nienhaus, K., Matthes, A., Brunori, M., Nienhaus, G.U., The structure of carbonmonoxy neuroglobin reveals a heme-sliding mechanism for control of ligand affinity (2004) Proceedings of the National Academy of Sciences of the United States of America, 101 (50), pp. 17351-17356. , DOI 10.1073/pnas.0407633101
Jenkins, J.D., Mausayev, F.N., Danso-Danquah, R., Abraham, D.J., Safo, M.K., Structure of relaxed-state of human haemoglobin:insight into ligand uptake, transport and release (2009) Acta Cryst. D, 65, pp. 41-48
Olson, J.S., Soman, J., Phillips Jr., G.N., Ligand pathways in myoglobin: A review of trp cavity mutations (2007) IUBMB Life, 59 (8-9), pp. 552-562. , DOI 10.1080/15216540701230495, PII 778491829, IUBMB Life Dedicated to Maurizio Brunori in the Occasion of his 70th Birthday
Yang, F., Phillips Jr., G.N., Crystal structures of CO-, Deoxy- and Met-myoglobins at various pH values (1996) Journal of Molecular Biology, 256 (4), pp. 762-774. , DOI 10.1006/jmbi.1996.0123
Perutz, M. F., Fermi, G., Luisi, B., Shaanan, B., Liddington, R. C., Stereochemistry of cooperative mechanisms in hemoglobin (1987) Acc. Chem. Res., 9, pp. 309-32
Tame, J. R., Wilson, J. C., Weber, R. E., The crystal structures of trout Hb i in the deoxy and carbonmonoxy forms J. Mol. Biol., 259, pp. 749-760
Mylvaganam, S. E., Bonaventura, C., Bonaventura, J., Getzoff, E. D., Structural basis for the root effect in haemoglobin (1996) Nature Structural Biology, 3 (3), pp. 275-283. , DOI 10. 1038/nsb0396-275
Ackers, G. K., Deciphering the molecular code of hemoglobin allostery (1998) Advances in Protein Chemistry, 51, pp. 185-253
Scott, E. E., Gibson, Q. H., Olson, J. S., Distal histidine stabilizes bound O2 and acts as a gate for ligand entry in both subunits of adult human hemoglobin (2010) J. Biol. Chem., 285, pp. 8840-8854
Tilton, Jr. R. F., Kuntz, Jr. I. D., Petsko, G. A., Cavities in proteins: Structure of a metmyoglobin-xenon complex solved to 1. 9 (1984) Biochemistry, 23, pp. 2849-2857
Boechi, L., Mart, 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. Bioinf., 73, pp. 372-379
Perissinotti, L. L., Marti, M. A., Doctorovich, F., Luque, F. J., Estrin, D. A., A microscopic study of the deoxyhemoglobin-catalyzed generation of nitric oxide from nitrite anion (2008) Biochemistry, 47, pp. 9793-9802
Mart, M. A., Estrin, D. A., Roitberg, A. E., Molecular basis for the pH dependent structural transition of Nitrophorin 4 (2009) J. Phys. Chem. B, 113, pp. 2135-2142
Pearlman, D. A., Case, D. A., Caldwell, J. W., Ross, W. S., Cheatham Iii, 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) Comp. Phys. Comm., 91, pp. 1-3. , 1-41
Alcantara, R. E., Xu, C., Spiro, T. G., Guallar, V., A quantum-chemical picture of hemoglobin affinity (2007) Proceedings of the National Academy of Sciences of the United States of America, 104 (47), pp. 18451-18455. , http: //www. pnas. org/cgi/reprint/104/47/18451, DOI 10. 1073/pnas. 0706026104
Perutz, M. F., Mechanisms of cooperativity and allosteric regulation in proteins (1989) Q. Rev. Biophys., 22, pp. 139-237
Jenkins, J. D., Mausayev, F. N., Danso-Danquah, R., Abraham, D. J., Safo, M. K., Structure of relaxed-state of human haemoglobin: insight into ligand uptake, transport and release (2009) Acta Cryst. D, 65, pp. 41-48
Olson, J. S., Soman, J., Phillips Jr., G. N., Ligand pathways in myoglobin: A review of trp cavity mutations (2007) IUBMB Life, 59 (8-9), pp. 552-562. , DOI 10. 1080/15216540701230495, PII 778491829, IUBMB Life Dedicated to Maurizio Brunori in the Occasion of his 70th Birthday
Protonation of Histidine 55 Affects the Oxygen Access to Heme in the Alpha Chain of the Hemoglobin from the Antarctic Fish Trematomus bernacchii
The Root effect describes the drastic drop of oxygen affinity and loss of cooperativity at acidic pH expressed in the hemoglobins (Hb) of certain fish. The comparison between the deoxy structures of the Root effect Hb from the Antarctic fish Trematomus bernacchii (HbTb) at different pHs (pH = 6.2 and pH = 8.4) shows that the most significant differences are localized at the CD alpha region, where a salt bridge between Asp48 and His55 breaks during the low-to-high pH transition. In order to shed light on the relationship between pH, CD alpha loop structure and dynamics, and oxygen access to the active site in the alpha chain of HbTb, different computer simulation techniques were performed. Our results highlight the importance of the protonation of His55 in regulating oxygen access, underscoring its pivotal role in the structural and functional properties of HbTb. These data provide further support to the hypothesis that this residue might contribute to the release of Root protons in HbTb and underline the fact that an efficient transport of molecular oxygen in Hbs relies on a subtle balance of tertiary structure and protein conformational flexibility. (C) 2011 IUBMB IUBMB Life, 63(3): 175-182, 2011
Protonation of Histidine 55 Affects the Oxygen Access to Heme in the Alpha Chain of the Hemoglobin from the Antarctic Fish Trematomus bernacchii