Structural characterization of ferric hemoglobins from three Antarctic fish species of the suborder notothenioidei(375 views) Vergara A, Franzese M, Merlino A, Vitagliano L, Verde C, Di Prisco G, Lee HC, Peisach J, Mazzarella L
Keywords: Hemoprotein, Methemoglobin, Antarctica, Article, Controlled Study, Crystal Structure, Fish, Geometry, Molecular Model, Nonhuman, Oxidation, Protein Structure, Wild Type, X Ray Crystallography, Animals, Antarctic Regions, Computer Simulation, Iron, Chemical, Protein Conformation, Species Specificity, Gymnodraco Acuticeps, Notothenioidei, Trematomus Bernacchii, Trematomus Newnesi,
Affiliations: *** IBB - CNR ***
Department of Chemistry, University of Naples Federico II, Complesso Universitario Monte S. Angelo, I-80126 Naples, Italy
Instituto di Biostrutture e Bioimmagini, Consiglio Nazionale Delle Ricerche, I-80134 Naples, Italy
Institute of Protein Biochemistry, Consiglio Nazionale Delle Ricerche, I-80131 Naples, Italy
Department of Physiology and Biophysics, Albert Einstein College of Medicine, Yeshiva University, New York, NY, United States
References: Shikama, K., The molecular mechanism of autoxidation for myoglobin and hemoglobin: A venerable puzzle (1998) Chem. Rev, 98, pp. 1357-137
Riess, J., Oxygen carriers ("blood substitutes") raison d'être, chemistry, and some physiology (2001) Chem. Rev, 101, pp. 2797-2919
Rifkind, J.M., Abugo, O., Levy, A., Heim, J.M., Detection, formation, and relevance of hemichrome and hemochrome (1994) Meth. Enzymol, 231, pp. 449-480
Riccio, A., Vitagliano, L., di Prisco, G., Zagari, A., Mazzarella, L., The crystal structure of a tetrameric hemoglobin in a partial hemichrome state (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 9801-9806
Vitagliano, L., Bonomi, G., Riccio, A., di Prisco, G., Smulevich, G., Mazzarella, L., The oxidation process of Antarctic fish hemoglobins (2004) Eur. J. Biochem, 271, pp. 1651-1659
Rachmilewitz, E.A., Peisach, J., Blumberg, W.E., Stability of oxyhemoglobin A and its constituent chains and their derivatives (1971) J. Biol. Chem, 246, pp. 3356-3366
Ramadas, N., Rifkind, J.M., Molecular dynamics of human methemoglobin: The transmission of conformational information between subunits in an αβ dimer (1999) Biophys. J, 76, pp. 1796-1811
Robinson, V.L., Smith, B.B., Arnone, A., A pH-dependent aquo-met-to-hemichrome transition in crystalline horse methemoglobin (2003) Biochemistry, 42, pp. 10113-10125
de Sanctis, D., Pesce, A., Nardini, M., Bolognesi, M., Bocedi, A., Ascenzi, P., Structure-function relationships in the growing hexacoordinate hemoglobin sub-family (2004) IUBMB Life, 56, pp. 643-651
Pesce, A., De Sanctis, D., Nardini, M., Dewilde, S., Moens, L., Hankeln, T., Burmester, T., Bolognesi, M., Reversible hexa- to penta-coordination of the heme Fe atom modulates ligand binding properties of neuroglobin and cytoglobin (2004) IUBMB Life, 56, pp. 657-664
Feng, L., Zhou, S., Gu, L., Gell, D., Mackay, J., Weiss, M., Gow, A., Shi, Y., Structure of oxidized α-haemoglobin bound to AHSP reveals a protective mechanism for haem (2005) Nature, 435, pp. 697-701
Camardella, L., Caruso, C., D'Avino, R., di Prisco, G., Rutigliano, B., Tamburrini, 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
D'Avino, R., Caruso, C., Tamburrini, M., Romano, M., Rutigliano, B., Polverino de Laureto, P., Camardella, L., di Prisco, G., Molecular characterization of the functionally distinct hemoglobins of the Antarctic fish Trematomus newnesi (1994) J. Biol. Chem, 269, pp. 9675-9681
Tamburini, M., A. Brancaccio, R. Ippoliti, and G. di Prisco. 1992. The amino acid sequence and oxygen-binding properties of the single hemoglobin of the cold-adapted Antarctic teleost Gymnodraco acuticeps. Arch. Biochem. Biophys. 292:295-302Otwinowski, Z., Minor, W., Processing of x-ray diffraction data collected in oscillation mode (1997) Meth. Enzymol, 276, pp. 307-326
Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Warren, G.L., Crystallography & NMR system: A new software suite for macromolecular structure determination (1998) Acta Crystallogr. D. Biol. Crystallogr, 54, pp. 905-921
Jones, T.A., Zou, J.Y., Cowan, S.W., Kjedgaard, M., Improved methods for binding protein models in electron density maps and the location of errors in these models (1991) Acta Crystallogr. D, 56, pp. 714-721
Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E., The Protein Data Bank (2000) Nucleic. Acids. Res, 28, pp. 235-242
Mitchell, D.T., Kitto, G.B., Hackert, M.L., Structural analysis of monomeric hemichrome and dimeric cyanomet hemoglobins from Caudina arenicola (1995) J. Mol. Biol, 251, pp. 421-431
Hargrove, M.S., Brucker, E.A., Stec, B., Sarath, G., Arredondo-Peter, R., Klucas, R.V., Olson, J.S., Phillips, G.N., Crystal structure of a nonsymbiotic plant hemoglobin (2000) Structure, 8, pp. 1005-1014
Pesce, A., Dewilde, S., Nardini, M., Moens, L., Ascenzi, P., Hankeln, T., Burmester, T., Bolognesi, M., Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity (2003) Structure, 11, pp. 1087-1093
Hoy, J.A., Kundu, S., Trent, J.T., Ramaswamy, S., Hargrove, M.S., The crystal structure of Synechocystis hemoglobin with a covalent heme linkage (2004) J. Biol. Chem, 279, pp. 16535-16542
Vallone, B., Nienhaus, K., Matthes, K., Brunori, M., Nienhaus, G., The structure of murine neuroglobin: Novel pathways for ligand migration and binding (2004) Proteins: Struct. Func. Bioinf, 56, pp. 85-92
de Sanctis, D., Dewilde, S., Pesce, A., Moens, L., Ascenzi, P., Hankeln, T., Burmester, T., Bolognesi, M., Crystal structure of cytoglobin: The fourth globin type discovered in man displays heme hexa-coordination (2004) J. Mol. Biol, 336, pp. 917-927
Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D. Biol. Crystallogr. 1:760-763Zaric, S., Popovic, D., Knapp, E., Factors determining the orientation of axially coordinated imidazoles in heme proteins (2001) Biochemistry, 40, pp. 7914-7928
Blumberg, W.E., Peisach, J., Low-spin ferric forms of hemoglobin and other heme proteins (1972) Wenner-Gren Center International Symposium Series, 18, pp. 219-225
Ikeda-Saito, M., Hori, H., Andersson, L.A., Prince, R.C., Pickering, I.J., George, G.N., Sanders, C.R., Mattera, R., Coordination structure of the ferric heme iron in engineered distal histidine myoglobin mutants (1992) J. Biol. Chem, 267, pp. 22843-22852
Quillin, M., Arduini, R., Olson, J., Phillips, G.J., High-resolution crystal structures of distal histidine mutants of sperm whale myoglobin (1993) J. Mol. Biol, 234, pp. 140-155
Smulevich, G., Feis, A., Howes, B.D., Fifteen years of Raman spectroscopy of engineered heme containing peroxidases: What have we learned? (2005) Acc. Chem. Res, 38, pp. 433-440
Ilari, A., Bonamore, A., Farina, A., Johnson, K., Boffi, A., The x-ray structure of ferric Escherichia coli flavohemoglobin reveals an unexpected geometry of the distal heme pocket (2002) J. Biol. Chem, 26, pp. 23725-23732
Marmo Moreira, L., Lima Poli, A., Costa-Filho, A.J., Imasato, H., Pentacoordinate and hexacoordinate ferric hemes in acid medium: EPR, UV-Vis and CD studies of the giant extracellular hemoglobin of Glossoscolex paulistus (2006) Biophys. Chem, 124, pp. 62-72
Boffi, A., Takahashi, S., Spagnuolo, C., Rousseau, D.L., Chiancone, E., Structural characterization of oxidized dimeric Scapharca inaequivalvis hemoglobin by resonance Raman spectroscopy (1994) J. Biol. Chem, 269, pp. 20437-20440
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, 65, pp. 490-498
Silva, M.M., Rogers, P.H., Arnone, A., A third quaternary structure of human hemoglobin A at 1.7-Å resolution (1992) J. Biol. Chem, 267, pp. 17248-17256
Walker, F.A., Reis, D., Balke, V.L., Models of the cytochromes b. 5. EPR studies of low-spin iron(III) tetraphenylporphyrins (1984) J. Am. Chem. Soc, 106, pp. 6888-6898
Bois-Poltoratsky, R., Ehrenberg, A., Magnetic and spectrophotometric investigations of cytochrome b5 (1967) Eur. J. Biochem, 2, pp. 361-365
Giangiacomo, L., D'Avino, R., di Prisco, G., Chiancone, E., Hemoglobin of the Antarctic fishes Trematomus bernacchii and Trematomus newnesi: Structural basis for the increased stability of the liganded tetramer relative to human hemoglobin (2001) Biochemistry, 40, pp. 3062-3068
Mazzarella, L., Bonomi, G., Lubrano, M.C., Merlino, A., Vergara, A., Vitagliano, L., Verde, C., di Prisco, G., Minimal structural requirement of root effect: Crystal structure of the cathodic hemoglobin isolated from Trematomus newnesi (2006) Proteins, 62, pp. 316-321
Vinck, E., Van Doorslaer, S., Dewilde, S., Moens, L., Structural change of the heme pocket due to disulfide bridge formation is significantly larger for neuroglobin than for cytoglobin (2004) J. Am. Chem. Soc, 126, pp. 4516-4517
Rifkind, J. M., Abugo, O., Levy, A., Heim, J. M., Detection, formation, and relevance of hemichrome and hemochrome (1994) Meth. Enzymol, 231, pp. 449-480
Rachmilewitz, E. A., Peisach, J., Blumberg, W. E., Stability of oxyhemoglobin A and its constituent chains and their derivatives (1971) J. Biol. Chem, 246, pp. 3356-3366
Robinson, V. L., Smith, B. B., Arnone, A., A pH-dependent aquo-met-to-hemichrome transition in crystalline horse methemoglobin (2003) Biochemistry, 42, pp. 10113-10125
Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Warren, G. L., Crystallography & NMR system: A new software suite for macromolecular structure determination (1998) Acta Crystallogr. D. Biol. Crystallogr, 54, pp. 905-921
Jones, T. A., Zou, J. Y., Cowan, S. W., Kjedgaard, M., Improved methods for binding protein models in electron density maps and the location of errors in these models (1991) Acta Crystallogr. D, 56, pp. 714-721
Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., Bourne, P. E., The Protein Data Bank (2000) Nucleic. Acids. Res, 28, pp. 235-242
Mitchell, D. T., Kitto, G. B., Hackert, M. L., Structural analysis of monomeric hemichrome and dimeric cyanomet hemoglobins from Caudina arenicola (1995) J. Mol. Biol, 251, pp. 421-431
Hargrove, M. S., Brucker, E. A., Stec, B., Sarath, G., Arredondo-Peter, R., Klucas, R. V., Olson, J. S., Phillips, G. N., Crystal structure of a nonsymbiotic plant hemoglobin (2000) Structure, 8, pp. 1005-1014
Hoy, J. A., Kundu, S., Trent, J. T., Ramaswamy, S., Hargrove, M. S., The crystal structure of Synechocystis hemoglobin with a covalent heme linkage (2004) J. Biol. Chem, 279, pp. 16535-16542
Blumberg, W. E., Peisach, J., Low-spin ferric forms of hemoglobin and other heme proteins (1972) Wenner-Gren Center International Symposium Series, 18, pp. 219-225
Silva, M. M., Rogers, P. H., Arnone, A., A third quaternary structure of human hemoglobin A at 1. 7- resolution (1992) J. Biol. Chem, 267, pp. 17248-17256
Walker, F. A., Reis, D., Balke, V. L., Models of the cytochromes b. 5. EPR studies of low-spin iron (III) tetraphenylporphyrins (1984) J. Am. Chem. Soc, 106, pp. 6888-6898
Structural characterization of ferric hemoglobins from three Antarctic fish species of the suborder notothenioidei
Spontaneous autoxidation of tetrameric Hbs leads to the formation of Fe (III) forms, whose physiological role is not fully understood. Here we report structural characterization by EPR of the oxidized states of tetrameric Hbs isolated from the Antarctic fish species Trematomus bernacchii, Trematomus newnesi, and Gymnodraco acuticeps, as well as the x-ray crystal structure of oxidized Trematomus bernacchii Hb, redetermined at high resolution. The oxidation of these Hbs leads to formation of states that were not usually detected in previous analyses of tetrameric Hbs. In addition to the commonly found aquo-met and hydroxy-met species, EPR analyses show that two distinct hemichromes coexist at physiological pH, referred to as hemichromes I and II, respectively. Together with the high-resolution crystal structure (1.5 angstrom) of T. bernacchii and a survey of data available for other heme proteins, hemichrome I was assigned by x-ray crystallography and by EPR as a bis-His complex with a distorted geometry, whereas hemichrome II is a less constrained (cytochrome b(5)-like) bis-His complex. In four of the five Antartic fish Hbs examined, hemichrome I is the major form. EPR shows that for HbCTn, the amount of hemichrome I is substantially reduced. In addition, the concomitant presence of a penta-coordinated high-spin Fe (III) species, to our knowledge never reported before for a wild-type tetrameric Hb, was detected. A molecular modeling investigation demonstrates that the presence of the bulkier Ile in position 67 beta in HbCTn in place of Val as in the other four Hbs impairs the formation of hemichrome I, thus favoring the formation of the ferric penta-coordinated species. Altogether the data show that ferric states commonly associated with monomeric and dimeric Hbs are also found in tetrameric Hbs.
Structural characterization of ferric hemoglobins from three Antarctic fish species of the suborder notothenioidei
Petraglia F, Singh AA, Carafa V, Nebbioso A, Conte M, Scisciola L, Valente S, Baldi A, Mandoli A, Petrizzi VB, Ingenito C, De Falco S, Cicatiello V, Apicella I, Janssen-megens EM, Kim B, Yi G, Logie C, Heath S, Ruvo M, Wierenga ATJ, Flicek P, Yaspo ML, Della Valle V, Bernard O, Tomassi S, Novellino E, Feoli A, Sbardella G, Gut I, Vellenga E, Stunnenberg HG, Mai A, Martens JHA, Altucci L * Combined HAT/EZH2 modulation leads to cancer-selective cell death(288 views) Oncotarget (ISSN: 1949-2553electronic, 1949-2553linking), 2018 May 22; 9(39): 25630-25646. Impact Factor:5.008 ViewExport to BibTeXExport to EndNote
Santulli G, Cipolletta E, Sorriento D, Del Giudice C, Anastasio A, Monaco S, Maione AS, Condorelli G, Puca A, Trimarco B, Illario M, Iaccarino G * CaMK4 gene deletion induces hypertension(349 views) J Am Heart Assoc Journal Of The American Heart Association (ISSN: 2047-9980), 2012; 1(4): N/D-N/D. Impact Factor:2.882 ViewExport to BibTeXExport to EndNote
Bruni AC, Bernardi L, Colao R, Rubino E, Smirne N, Frangipane F, Terni B, Curcio SA, Mirabelli M, Clodomiro A, Di Lorenzo R, Maletta R, Anfossi M, Gallo M, Geracitano S, Tomaino C, Muraca MG, Leotta A, Lio SG, Pinessi L, Rainero I, Sorbi S, Nee L, Milan G, Pappata S, Postiglione A, Abbamondi N, Forloni G, St George Hyslop P, Rogaeva E, Bugiani O, Giaccone G, Foncin JF, Spillantini MG, Puccio G * Worldwide distribution of PSEN1 Met146Leu mutation: A large variability for a founder mutation(1002 views) Neurology (ISSN: 0028-3878, 1526-632x, 1526-632xelectronic), 2010 Mar 9; 74(10): 798-806. Impact Factor:8.017 ViewExport to BibTeXExport to EndNote
Aloj L, Aurilio M, Rinaldi V, D'Ambrosio L, Tesauro D, Peitl PK, Maina T, Mansi R, Von Guggenberg E, Joosten L, Sosabowski JK, Breeman WA, De Blois E, Koelewijn S, Melis M, Waser B, Beetschen K, Reubi JC, De Jong M * The EEE project(449 views) Proc Int Cosm Ray Conf Icrc Universidad Nacional Autonoma De Mexico, 2007; 5(HEPART2): 977-980. Impact Factor:0 ViewExport to BibTeXExport to EndNote
Vitiello M, Finamore E, Falanga A, Raieta K, Cantisani M, Galdiero F, Pedone C, Galdiero M, Galdiero S * Fusion in Coq(481 views) Lecture Notes In Computer Science (ISSN: 0302-9743, 0302-974335404636319783540463634, 0302-974335402975459783540297543), 2001; 2178LNCS: 583-596. Impact Factor:0.415 ViewExport to BibTeXExport to EndNote