Artículo

Giordano, D.; Boron, I.; Abbruzzetti, S.; van Leuven, W.; Nicoletti, F.P.; Forti, F.; Bruno, S.; Cheng, C.-H.C.; Moens, L.; di Prisco, G.; Nadra, A.D.; Estrin, D.; Smulevich, G.; Dewilde, S.; Viappiani, C.; Verde, C. "Biophysical Characterisation of Neuroglobin of the Icefish, a Natural Knockout for Hemoglobin and Myoglobin. Comparison with Human Neuroglobin" (2012) PLoS ONE. 7(12)
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Abstract:

The Antarctic icefish Chaenocephalus aceratus lacks the globins common to most vertebrates, hemoglobin and myoglobin, but has retained neuroglobin in the brain. This conserved globin has been cloned, over-expressed and purified. To highlight similarities and differences, the structural features of the neuroglobin of this colourless-blooded fish were compared with those of the well characterised human neuroglobin as well as with the neuroglobin from the retina of the red blooded, hemoglobin and myoglobin-containing, closely related Antarctic notothenioid Dissostichus mawsoni. A detailed structural and functional analysis of the two Antarctic fish neuroglobins was carried out by UV-visible and Resonance Raman spectroscopies, molecular dynamics simulations and laser-flash photolysis. Similar to the human protein, Antarctic fish neuroglobins can reversibly bind oxygen and CO in the Fe 2+ form, and show six-coordination by distal His in the absence of exogenous ligands. A very large and structured internal cavity, with discrete docking sites, was identified in the modelled three-dimensional structures of the Antarctic neuroglobins. Estimate of the free-energy barriers from laser-flash photolysis and Implicit Ligand Sampling showed that the cavities are accessible from the solvent in both proteins. Comparison of structural and functional properties suggests that the two Antarctic fish neuroglobins most likely preserved and possibly improved the function recently proposed for human neuroglobin in ligand multichemistry. Despite subtle differences, the adaptation of Antarctic fish neuroglobins does not seem to parallel the dramatic adaptation of the oxygen carrying globins, hemoglobin and myoglobin, in the same organisms. © 2012 Giordano et al.

Registro:

Documento: Artículo
Título:Biophysical Characterisation of Neuroglobin of the Icefish, a Natural Knockout for Hemoglobin and Myoglobin. Comparison with Human Neuroglobin
Autor:Giordano, D.; Boron, I.; Abbruzzetti, S.; van Leuven, W.; Nicoletti, F.P.; Forti, F.; Bruno, S.; Cheng, C.-H.C.; Moens, L.; di Prisco, G.; Nadra, A.D.; Estrin, D.; Smulevich, G.; Dewilde, S.; Viappiani, C.; Verde, C.
Filiación:Institute of Protein Biochemistry, CNR, Naples, Italy
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad de Buenos Aires, Argentina
Departamento de Química Inorgánica, Analítica y Química Física/INQUIMAE-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, Buenos Aires, Argentina
Department of Physics, University of Parma, NEST Istituto Nanoscienze-CNR, Parma, Italy
Department of Biomedical Sciences, PPES, University of Antwerp, Universiteitsplein 1, Wilrijk, Belgium
Dipartimento di Chimica Ugo Schiff, Università di Firenze, Sesto Fiorentino (FI), Italy
Facultat de Farmacia, Departament de Fisicoquímica and Institut de Biomedicina, Universitat de Barcelona, Barcelona, Spain
Department of Biochemistry and Molecular Biology, University of Parma, Parma, Italy
Department of Animal Biology, University of Illinois, Urbana, IL, United States
Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad de Buenos Aires, Argentina
Consorzio Interuniversitario di Ricerca in Chimica dei Metalli nei Sistemi Biologici, Bari, Italy
Palabras clave:hemoglobin; myoglobin; neuroglobin; article; autooxidation; biophysics; Chaenocephalus aceratus; controlled study; Dissostichus mawsoni; fish; human; human versus animal comparison; laser flash photolysis; molecular cloning; molecular dynamics; nonhuman; oxygen affinity; oxygen transport; photolysis; protein analysis; protein expression; protein function; protein purification; protein structure; Raman spectrometry; site directed mutagenesis; ultraviolet spectroscopy; Animals; Biophysics; Carbon Monoxide; Fishes; Gene Knockout Techniques; Globins; Hemoglobins; Humans; Kinetics; Ligands; Molecular Dynamics Simulation; Mutagenesis, Site-Directed; Nerve Tissue Proteins; Spectrophotometry, Ultraviolet; Spectrum Analysis, Raman; Chaenocephalus aceratus; Dissostichus mawsoni; Vertebrata
Año:2012
Volumen:7
Número:12
DOI: http://dx.doi.org/10.1371/journal.pone.0044508
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CAS:hemoglobin, 9008-02-0; Carbon Monoxide, 630-08-0; Globins, 9004-22-2; Hemoglobins; Ligands; Nerve Tissue Proteins; neuroglobin
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_19326203_v7_n12_p_Giordano.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19326203_v7_n12_p_Giordano

Referencias:

  • Sun, Y., Jin, K., Mao, X.O., Zhu, Y., Greenberg, D.A., Neuroglobin is up-regulated by and protects neurons from hypoxic-ischemic injury (2001) Proc Natl Acad Sci U S A, 98, pp. 15306-15311
  • Sun, Y., Jin, K., Peel, A., Mao, X.O., Xie, L., Neuroglobin is up-regulated by and protects neurons from hypoxic-ischemic injury (2003) Proc Natl Acad Sci U S A, 100, pp. 3497-3500
  • Hundahl, C.A., Luuk, H., Ilmjärv, S., Falktoft, B., Raida, Z., Neuroglobin-deficiency exacerbates Hif1A and c-FOS response, but does not affect neuronal survival during severe hypoxia in vivo (2011) PLoS One, 6, pp. e28160
  • Wakasugi, K., Nakano, T., Morishima, I., Oxidized human neuroglobin acts as a heterotrimeric Galpha protein guanine nucleotide dissociation inhibitor (2003) J Biol Chem, 278, pp. 36505-36512
  • Khan, A.A., Mao, X.O., Banwait, S., Jin, K., Greenberg, D.A., Neuroglobin attenuates beta-amyloid neurotoxicity in vitro and transgenic Alzheimer phenotype in vivo (2007) Proc Natl Acad Sci U S A, 104, pp. 19114-19119
  • Brunori, M., Giuffrè, A., Nienhaus, K., Nienhaus, G.U., Scandurra, F.M., Neuroglobin, nitric oxide, and oxygen: functional pathways and conformational changes (2005) Proc Natl Acad Sci U S A, 102, pp. 8483-8488
  • Herold, S., Fago, A., Weber, R.E., Dewilde, S., Moens, L., Reactivity studies of the Fe(III) and Fe(II)NO forms of human neuroglobin reveal a potential role against oxidative stress (2004) J Biol Chem, 27, pp. 22841-22847
  • Tiso, M., Tejero, J., Basu, S., Azarov, I., Wang, X., Human neuroglobin functions as a redox-regulated nitrite reductase (2011) J Biol Chem, 286, pp. 18277-18289
  • Shiva, S., Huang, Z., Grubina, R., Sun, J., Ringwood, L.A., Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration (2007) Circ Res, 100, pp. 654-661
  • Hendgen-Cotta, U.B., Merx, M.W., Shiva, S., Schmitz, J., Becher, S., Nitrite reductase activity of myoglobin regulates respiration and cellular viability in myocardial ischemia-reperfusion injury (2008) Proc Natl Acad Sci U S A, 105, pp. 10256-10261
  • Jayaraman, T., Tejero, J., Chen, B.B., Blood, A.B., Frizzell, S., 14-3-3 binding and phosphorylation of neuroglobin during hypoxia modulate six-to-five heme pocket coordination and rate of nitrite reduction to nitric oxide (2011) J Biol Chem, 286, pp. 42679-42689
  • Ruud, J.T., Vertebrates without erythrocytes and blood pigment (1954) Nature, 173, pp. 848-850
  • Egginton, S., Skilbeck, C., Hoofd, L., Calvo, J., Johnston, I.A., Peripheral oxygen transport in skeletal muscle of Antarctic and sub-Antarctic notothenioid fish (2002) J Exp Biol, 205, pp. 769-779
  • Johnston, I.A., Fernandez, D.A., Calvo, J., Vieira, V.L., North, A.W., Reduction in muscle fibrenumber during adaptive radiation of notothenioid fishes: a phylogenetic perspective (2003) J Exp Biol, 206, pp. 2595-2609
  • Sidell, B.D., O'Brien, K.M., When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes (2006) J Exp Biol, 209, pp. 1791-1802
  • O'Brien, K.M., Xue, H., Sidell, B.D., Quantification of diffusion distance within the spongy myocardium of hearts from antarctic fishes (2000) Respir Physiol, 122, pp. 71-80
  • Sidell, B.D., Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature (1998) J Exp Biol, 201, pp. 1118-1127
  • Merx, M.W., Flögel, U., Stumpe, T., Gödecke, A., Decking, U.K., Myoglobin facilitates oxygen diffusion (2001) FASEB J, 15, pp. 1077-1079
  • Wittenberg, J.B., Wittenberg, B.A., Myoglobin function reassessed (2003) J Exp Biol, 206, pp. 2011-2020
  • Beers, J.M., Borley, K.A., Sidell, B.D., Relationship among circulating hemoglobin, nitric oxide synthase activities and angiogenic poise in red and white-blooded Antarctic notothenioid fishes (2010) Comp Biochem Physiol A Mol Integr Physiol, 156, pp. 422-429
  • Cheng, C.-H.C., di Prisco, G., Verde, C., Cold-adapted Antarctic fish: the discovery of neuroglobin in the dominant suborder Notothenioidei (2009) Gene, 433, pp. 100-101
  • Cheng, C.-H.C., di Prisco, G., Verde, C., The "icefish paradox." Which is the task of neuroglobin in Antarctic hemoglobin-less icefish? (2009) IUBMB Life, 61, pp. 184-188
  • Boron, I., Russo, R., Boechi, L., Cheng, C.-H.C., di Prisco, G., Structure and dynamics of Antarctic fish neuroglobin assessed by computer simulations (2011) IUBMB Life, 633, pp. 206-213
  • di Prisco, G., Eastman, J.T., Giordano, D., Parisi, E., Verde, C., Biogeography and adaptation of Notothenioid fish: hemoglobin function and globin-gene evolution (2007) Gene, 398, pp. 143-155
  • Vitagliano, L., Bonomi, G., Riccio, A., di Prisco, G., Smulevich, G., The oxidation process of Antarctic fish hemoglobins (2004) Eur J Biochem, 271, pp. 1651-1659
  • Vitagliano, L., Vergara, A., Bonomi, G., Merlino, A., Verde, C., 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
  • Watanabe, S., Wakasugi, K., Zebrafish neuroglobin is a cell-membrane-penetrating globin (2008) Biochemistry, 47, pp. 5266-5270
  • Dewilde, S., Mees, K., Kiger, L., Lechauve, C., Marden, M.C., Expression, purification, and crystallization of neuro- and cytoglobin (2008) Meth Enzymol, 436, pp. 341-357
  • Hayashi, A., Suzuki, T., Shin, M., An enzymic reduction system for metmyoglobin and methemoglobin, and its application to functional studies of oxygen carriers (1973) Biochim Biophys Acta - Protein Structure, 310, pp. 309-316
  • 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
  • Verde, C., Howes, B.D., De Rosa, M.C., Raiola, L., Smulevich, G., Structure and function of the Gondwanian hemoglobin of Pseudaphritis urvillii, a primitive notothenioid fish of temperate latitudes (2004) Protein Sci, 13, pp. 2766-2781
  • Ronda, L., Bruno, S., Faggiano, S., Bettati, S., Mozzarelli, A., Oxygen binding to heme proteins in solution, encapsulated in silica gels, and in the crystalline state (2008) Meth Enzymol, 437, pp. 311-328
  • Nadra, A.D., Martì, M.A., Pesce, A., Bolognesi, M., Estrin, D.A., Exploring the molecular basis of heme coordination in human neuroglobin (2008) Proteins, 71, pp. 695-705
  • Sali, A., Blundell, T.L., Comparative protein modelling by satisfaction of spatial restraints (1993) J Mol Biol, 234, pp. 779-815
  • Marti, M.A., Crespo, A., Capece, L., Boechi, L., Bikiel, D.E., Dioxygen affinity in heme proteins investigated by computer simulation (2006) J Inorg Biochem, 100, pp. 761-770
  • Bidon-Chanal, A., Marti, M.A., Crespo, A., Milani, M., Orozco, M., Ligand-induced dynamical regulation of NO conversion in Mycobacterium tuberculosis truncated hemoglobin-N (2006) Proteins, 64, pp. 457-464
  • Pearlman, D.A., Case, D.A., Caldwell, J.W., Ross, W.S., Cheatham III, T.E., 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
  • Cohen, J., Arkhipov, A., Braun, R., Schulten, K., Imaging the migration pathways for O2, CO, NO, and Xe inside myoglobin (2006) Biophys J, 91, pp. 1844-1857
  • Capece, L., Marti, M.A., Bidon-Chanal, A., Nadra, A., Luque, F.J., High pressure reveals structural determinants for globin hexacoordination: neuroglobin and myoglobin cases (2009) Proteins, 75, pp. 885-894
  • Abbruzzetti, S., Faggiano, S., Bruno, S., Spyrakis, F., Mozzarelli, A., Ligand migration through the internal hydrophobic cavities in human neuroglobin (2009) Proc Natl Acad Sci U S A, 106, pp. 18984-18989
  • Dewilde, S., Kiger, L., Burmester, T., Hankeln, T., Baudin-Creuza, V., Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family (2001) J Biol Chem, 276, pp. 38949-38955
  • Couture, M., Burmester, T., Hankeln, T., Rousseau, D.L., The heme environment of mouse neuroglobin. Evidence for the presence of two conformations of the heme pocket (2001) J Biol Chem, 276, pp. 36377-36382
  • Uno, T., Ryu, D., Tsutsumi, H., Tomisugi, Y., Ishikawa, Y., Residues in the distal heme pocket of neuroglobin. Implications for the multiple ligand binding steps (2004) J Biol Chem, 279, pp. 5886-5893
  • Shikama, K., The Molecular Mechanism of Autoxidation for Myoglobin and Hemoglobin: A Venerable Puzzle (1998) Chemical Reviews, 98, pp. 1357-1373
  • Vogel, K.M., Kozlowski, P.M., Zgierski, M.Z., Spiro, T.G., Determinants of the FeXO (X = C, N, O) vibrational frequencies in heme adducts from experiment and density functional theory (1999) J Am Chem Soc, 121, pp. 9915-9921
  • Spiro, T.G., Wasbotten, I.H., CO as a vibrational probe of heme protein active sites (2005) J Inorg Biochem, 99, pp. 34-44
  • Ishikawa, H., Kim, I.J.F.S., Kwak, K., Chung, J.K., Wakasugi, K., Neuroglobin dynamics observed with ultrafast 2D-IR vibrational echo spectroscopy (2007) Proc Natl Acad Sci U S A, 104, pp. 16116-16121
  • Sawai, H., Makino, M., Mizutani, Y., Ohta, T., Sugimoto, H., Structural characterization of the proximal and distal histidine environment of cytoglobin and neuroglobin (2005) Biochemistry, 44, pp. 13257-13265
  • Hori, H., Kitagawa, T., Iron-ligand stretching band in the resonance Raman spectra of ferrous iron porphyrin derivatives. Importance as a probe band for quaternary structure of hemoglobin (1980) J Am Chem Soc, 102, pp. 3608-3613
  • Kitagawa, T., The heme protein structure and the iron histidine stretching mode (1988) Biological Applications of Raman Spectroscopy, pp. 97-131. , In: Spiro TG editor, John Wiley & Sons, Inc, New York
  • Hu, S., Smith, K., Spiro, T.G., Assignment of protoheme resonance raman spectrum by heme labeling in myoglobin (1996) J Am Chem Soc, 118, pp. 12638-12646
  • Pesce, A., Dewilde, S., Nardini, M., Moens, L., Ascenzi, P., Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity (2003) Structure, 11, pp. 1087-1095
  • Moschetti, T., Mueller, U., Schulze, J., Brunori, M., Vallone, B., The structure of neuroglobin at high Xe and Kr pressure reveals partial conservation of globin internal cavities (2009) Biophys J, 97, pp. 1700-1708
  • Orlowski, S., Nowak, W., Topology and thermodynamics of gaseous ligands diffusion paths in human neuroglobin (2008) Biosystems, 94, pp. 263-266
  • Lutz, S., Nienhaus, K., Nienhaus, G.U., Meuwly, M., Ligand migration between internal docking sites in photodissociated carbonmonoxy neuroglobin (2009) J Phys Chem B, 113, pp. 15334-15343
  • Bocahut, A., Bernad, S., Sebban, P., Sacquin-Mora, S., Relating the diffusion of small ligands in human neuroglobin to its structural and mechanical properties (2009) J Phys Chem B, 113, pp. 16257-16267
  • Cohen, J., Olsen, K.W., Schulten, K., Finding gas migration pathways in Proteins using implicit ligand sampling (2008) Meth in Enzymology, 437, pp. 439-456
  • Anselmi, M., Nola, A.D., Amadei, A., Kinetics of carbon monoxide migration and binding in solvated neuroglobin as revealed by molecular dynamics simulations and quantum mechanical calculations (2011) J Phys Chem B, 115, pp. 2436-2446
  • Kriegl, J.M., Bhattacharyya, A.J., Nienhaus, K., Deng, P., Minkow, O., Ligand binding and protein dynamics in neuroglobin (2002) Proc Natl Acad Sci U S A, 99, pp. 7992-7997
  • Nienhaus, K., Kriegl, J.M., Nienhaus, G.U., Structural dynamics in the active site of murine neuroglobin and its effects on ligand binding (2004) J Biol Chem, 279, pp. 22944-22952
  • Smagghe, B.J., Kundu, S., Hoy, J.A., Halder, P., Weiland, T.R., Role of phenylalanine B10 in plant nonsymbiotic hemoglobins (2006) Biochemistry, 45, pp. 9735-9745
  • Fuchs, C., Heib, V., Kiger, L., Haberkamp, M., Roesner, A., Zebrafish reveals different and conserved features of vertebrate neuroglobin gene structure, expression pattern, and ligand binding (2004) J Biol Chem, 279, pp. 24116-24122
  • Lau, K.S., Grange, R.W., Isotani, E., Sarelius, I.H., Kamm, K.E., nNOS and eNOS modulate cGMP formation and vascular response in contracting fast-twitch skeletal muscle (2000) Physiol Genomics, 2, pp. 21-27
  • Morlà, M., Agustì, G.N.A., Rahman, I., Motterlini, R., Saus, C., Nitric oxide synthase type I (nNOS), vascular endothelial growth factor (VEGF) and myoglobin-like expression in skeletal muscle of Antarctic icefishes (Notothenioidei: Channichthyidae) (2003) Polar Biol, 26, pp. 458-462
  • Roesner, A., Hankeln, T., Burmester, T., Hypoxia induces a complex response of globin expression in zebrafish (Danio rerio) (2006) J Exp Biol, 209, pp. 2129-2137
  • Milton, S.L., Nayak, G., Lutz, P.L., Prentice, H.M., Gene transcription of neuroglobin is upregulated by hypoxia and anoxia in the brain of the anoxia-tolerant turtleTrachemys scripta (2006) J Biomed Sci, 13, pp. 509-514
  • Avivi, A., Gerlach, F., Joel, A., Reuss, S., Burmester, T., Neuroglobin, cytoglobin, and myoglobin contribute to hypoxia adaptation of the subterranean mole rat Spalax (2010) Proc Natl Acad Sci U S, A107, pp. 21570-21575
  • Williams, T.M., Zavanelli, M., Miller, M.A., Goldbeck, R.A., Morledge, M., Running, swimming and diving modifies neuroprotecting globins in the mammalian brain (2008) Proc Biol Sci, 275, pp. 751-758

Citas:

---------- APA ----------
Giordano, D., Boron, I., Abbruzzetti, S., van Leuven, W., Nicoletti, F.P., Forti, F., Bruno, S.,..., Verde, C. (2012) . Biophysical Characterisation of Neuroglobin of the Icefish, a Natural Knockout for Hemoglobin and Myoglobin. Comparison with Human Neuroglobin. PLoS ONE, 7(12).
http://dx.doi.org/10.1371/journal.pone.0044508
---------- CHICAGO ----------
Giordano, D., Boron, I., Abbruzzetti, S., van Leuven, W., Nicoletti, F.P., Forti, F., et al. "Biophysical Characterisation of Neuroglobin of the Icefish, a Natural Knockout for Hemoglobin and Myoglobin. Comparison with Human Neuroglobin" . PLoS ONE 7, no. 12 (2012).
http://dx.doi.org/10.1371/journal.pone.0044508
---------- MLA ----------
Giordano, D., Boron, I., Abbruzzetti, S., van Leuven, W., Nicoletti, F.P., Forti, F., et al. "Biophysical Characterisation of Neuroglobin of the Icefish, a Natural Knockout for Hemoglobin and Myoglobin. Comparison with Human Neuroglobin" . PLoS ONE, vol. 7, no. 12, 2012.
http://dx.doi.org/10.1371/journal.pone.0044508
---------- VANCOUVER ----------
Giordano, D., Boron, I., Abbruzzetti, S., van Leuven, W., Nicoletti, F.P., Forti, F., et al. Biophysical Characterisation of Neuroglobin of the Icefish, a Natural Knockout for Hemoglobin and Myoglobin. Comparison with Human Neuroglobin. PLoS ONE. 2012;7(12).
http://dx.doi.org/10.1371/journal.pone.0044508