Artículo

Boron, I.; Capece, L.; Pennacchietti, F.; Wetzler, D.E.; Bruno, S.; Abbruzzetti, S.; Chisari, L.; Luque, F.J.; Viappiani, C.; Marti, M.A.; Estrin, D.A.; Nadra, A.D. "Engineered chimeras reveal the structural basis of hexacoordination in globins: A case study of neuroglobin and myoglobin" (2015) Biochimica et Biophysica Acta - General Subjects. 1850(1):169-177
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:

Background Myoglobin (Mb) and neuroglobin (Ngb) are representative members of pentacoordinated and bis-histidyl, hexacoordinated globins. In spite of their low sequence identity, they show surprisingly similar three-dimensional folds. The ability of Ngb to form a hexacoordinated bis-histidyl complex with the distal HisE7 has a strong impact on ligand affinity. The factors governing such different behaviors have not been completely understood yet, even though they are extremely relevant to establish structure-function relationships within the globin superfamily. Methods In this work we generated chimeric proteins by swapping a previously identified regulatory segment - the CD region - and evaluated comparatively the structural and functional properties of the resulting proteins by molecular dynamics simulations, and spectroscopic and kinetic investigations. Results Our results show that chimeric proteins display heme coordination properties displaced towards those expected for the corresponding CD region. In particular, in the absence of exogenous ligands, chimeric Mb is found as a partially hexacoordinated bis-histidyl species, whereas chimeric Ngb shows a lower equilibrium constant for forming a hexacoordinated bis-histidyl species. Conclusions While these results confirm the regulatory role of the CD region for bis-histidyl hexacoordination, they also suggest that additional sources contribute to fine tune the equilibrium. General significance Globins constitute a ubiquitous group of heme proteins widely found in all kingdoms of life. These findings raise challenging questions regarding the structure-function relationships in these proteins, as bis-histidyl hexacoordination emerges as a novel regulatory mechanism of the physiological function of globins. ©2014 Elsevier B.V. All rights reserved.

Registro:

Documento: Artículo
Título:Engineered chimeras reveal the structural basis of hexacoordination in globins: A case study of neuroglobin and myoglobin
Autor:Boron, I.; Capece, L.; Pennacchietti, F.; Wetzler, D.E.; Bruno, S.; Abbruzzetti, S.; Chisari, L.; Luque, F.J.; Viappiani, C.; Marti, M.A.; Estrin, D.A.; Nadra, A.D.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Ciudad Universitaria, Pabellón 2, Buenos Aires, C1428EHA, Argentina
IQUIBICEN-CONICET, Argentina
Departamento de Química Inorgánica, Analítica y Química Física, Ciudad Universitaria, Pabellón 2, Buenos Aires, C1428EHA, Argentina
Dipartimento di Fisica e Scienze della Terra, Universitá Degli Studi di Parma, Italy
Dipartimento di Farmacia, Universitá Degli Studi di Parma, Italy
Departament de Fisicoquímica and Institut de Biomedicina (IBUB), Facultat de Farmàcia, Universitat de Barcelona, Avda. Prat de la Riba 171, Santa Coloma de Gramenet, 08921, Spain
INQUIMAE-CONICET, Argentina
Palabras clave:Bis-histidyl coordination; Flash photolysis; Molecular dynamics; Myoglobin; Neuroglobin; carbon monoxide; chimeric protein; myoglobin; neuroglobin; globin; heme; hybrid protein; ligand; myoglobin; nerve protein; neuroglobin; protein binding; Article; binding kinetics; CD region; dissociation; hexacoordination; molecular dynamics; photolysis; protein engineering; protein structure; spectroscopy; amino acid sequence; animal; chemistry; genetics; human; metabolism; molecular genetics; protein tertiary structure; regulatory sequence; sequence homology; spectrophotometry; Amino Acid Sequence; Animals; Globins; Heme; Humans; Ligands; Molecular Dynamics Simulation; Molecular Sequence Data; Myoglobin; Nerve Tissue Proteins; Protein Binding; Protein Engineering; Protein Structure, Tertiary; Recombinant Fusion Proteins; Regulatory Sequences, Nucleic Acid; Sequence Homology, Amino Acid; Spectrophotometry
Año:2015
Volumen:1850
Número:1
Página de inicio:169
Página de fin:177
DOI: http://dx.doi.org/10.1016/j.bbagen.2014.10.006
Título revista:Biochimica et Biophysica Acta - General Subjects
Título revista abreviado:Biochim. Biophys. Acta Gen. Subj.
ISSN:03044165
CODEN:BBGSB
CAS:carbon monoxide, 630-08-0; heme, 14875-96-8; Globins; Heme; Ligands; Myoglobin; Nerve Tissue Proteins; neuroglobin; Recombinant Fusion Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03044165_v1850_n1_p169_Boron

Referencias:

  • Vinogradov, S.N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Gough, J., Dewilde, S., Moens, L., Vanfleteren, J.R., A phylogenomic profile of globins (2006) BMC Evol. Biol., 6, p. 31
  • Vinogradov, S.N., Tinajero-Trejo, M., Poole, R.K., Hoogewijs, D., Bacterial and archaeal globins - A revised perspective (2013) Biochim. Biophys. Acta, 1834, pp. 1789-1800
  • Vinogradov, S.N., Hoogewijs, D., Bailly, X., Arredondo-Peter, R., Guertin, M., Gough, J., Dewilde, S., Vanfleteren, J.R., Three globin lineages belonging to two structural classes in genomes from the three kingdoms of life (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 11385-11389
  • 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, 1834, pp. 1722-1738
  • Trent, J.T., III, Watts, R.A., Hargrove, M.S., Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen (2001) J. Biol. Chem., 276, pp. 30106-30110
  • Burmester, T., Weich, B., Reinhardt, S., Hankeln, T., A vertebrate globin expressed in the brain (2000) Nature, 407, pp. 520-523
  • Brunori, M., Vallone, B., Neuroglobin, seven years after (2007) Cell. Mol. Life Sci., 64, pp. 1259-1268
  • Burmester, T., Ebner, B., Weich, B., Hankeln, T., Cytoglobin: A novel globin type ubiquitously expressed in vertebrate tissues (2002) Mol. Biol. Evol., 19, pp. 416-421
  • Kakar, S., Hoffman, F.G., Storz, J.F., Fabian, M., Hargrove, M.S., Structure and reactivity of hexacoordinate hemoglobins (2010) Biophys. Chem., 152, pp. 1-14
  • Smagghe, B.J., Hoy, J.A., Percifield, R., Kundu, S., Hargrove, M.S., Sarath, G., Hilbert, J.L., Appleby, C.A., Review: Correlations between oxygen affinity and sequence classifications of plant hemoglobins (2009) Biopolymers, 91, pp. 1083-1096
  • Hamdane, D., Kiger, L., Dewilde, S., Green, B.N., Pesce, A., Uzan, J., Burmester, T., Marden, M.C., The redox state of the cell regulates the ligand binding affinity of human neuroglobin and cytoglobin (2003) J. Biol. Chem., 278, pp. 51713-51721
  • Hamdane, D., Kiger, L., Dewilde, S., Green, B.N., Pesce, A., Uzan, J., Burmester, T., Marden, M.C., Coupling of the heme and an internal disulfide bond in human neuroglobin (2004) Micron, 35, pp. 59-62
  • Nadra, A.D., Marti, 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
  • Olson, J.S., Mathews, A.J., Rohlfs, R.J., Springer, B.A., Egeberg, K.D., Sligar, S.G., Tame, J., Nagai, K., The role of the distal histidine in myoglobin and haemoglobin (1988) Nature, 336, pp. 265-266
  • Springer, B.A., Sligar, S.G., Olson, J.S., Phillips, G.N., Jr., Mechanisms of ligand recognition in myoglobin (1994) Chem. Rev., 94, pp. 699-714
  • Antonini, E., Brunori, M., Hemoglobin and myoglobin in their reactions with ligands (1971) Frontiers of Biology, 178, p. 296. , North-Holland Publishing Co. Amsterdam
  • Dewilde, S., Kiger, L., Burmester, T., Hankeln, T., Baudin-Creuza, V., Aerts, T., Marden, M.C., Moens, L., Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family (2001) J. Biol. Chem., 276, pp. 38949-38955
  • 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. 1087-1095
  • Trent, J.T., III, Hvitved, A.N., Hargrove, M.S., A model for ligand binding to hexacoordinate hemoglobins (2001) Biochemistry, 40, pp. 6155-6163
  • Kriegl, J.M., Bhattacharyya, A.J., Nienhaus, K., Deng, P., Minkow, O., Nienhaus, G.U., Ligand binding and protein dynamics in neuroglobin (2002) Proc. Natl. Acad. Sci. U. S. A., 99, pp. 7992-7997
  • Kiger, L., Uzan, J., Dewilde, S., Burmester, T., Hankeln, T., Moens, L., Hamdane, D., Marden, M., Neuroglobin ligand binding kinetics (2004) IUBMB Life, 56, pp. 709-719
  • Giordano, D., Boron, I., Abbruzzetti, S., Van Leuven, W., Nicoletti, F.P., Forti, F., Bruno, S., Verde, C., Biophysical characterisation of neuroglobin of the icefish, a natural knockout for hemoglobin and myoglobin. Comparison with human neuroglobin (2012) PLoS One, 7, p. 44508
  • 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, pp. 5177-5188
  • Smith, L.J., Kahraman, A., Thornton, J.M., Heme proteins - Diversity in structural characteristics, function, and folding (2010) Proteins, 78, pp. 2349-2368
  • Lecomte, J.T., Vuletich, D.A., Lesk, A.M., Structural divergence and distant relationships in proteins: Evolution of the globins (2005) Curr. Opin. Struct. Biol., 15, pp. 290-301
  • 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, 75, pp. 885-894
  • Abbruzzetti, S., Bruno, S., Faggiano, S., Grandi, E., Mozzarelli, A., Viappiani, C., Time-resolved methods in biophysics. 2. Monitoring haem proteins at work with nanosecond laser flash photolysis (2006) Photochem. Photobiol. Sci., 5, pp. 1109-1120
  • Abbruzzetti, S., Faggiano, S., Bruno, S., Spyrakis, F., Mozzarelli, A., Dewilde, S., Moens, L., Viappiani, C., Ligand migration through the internal hydrophobic cavities in human neuroglobin (2009) Proc. Natl. Acad. Sci. U. S. A., 106, pp. 18984-18989
  • Sottini, S., Abbruzzetti, S., Viappiani, C., Ronda, L., Mozzarelli, A., Determination of microscopic rate constants for CO binding and migration in myoglobin encapsulated in silica gels (2005) J. Phys. Chem. B, 109, pp. 19523-19528
  • Uzan, J., Dewilde, S., Burmester, T., Hankeln, T., Moens, L., Hamdane, D., Marden, M.C., Kiger, L., Neuroglobin and other hexacoordinated hemoglobins show a weak temperature dependence of oxygen binding (2004) Biophys. J., 87, pp. 1196-1204
  • Hoy, J.A., Robinson, H., Trent, J.T., III, Kakar, S., Smagghe, B.J., Hargrove, M.S., Plant hemoglobins: A molecular fossil record for the evolution of oxygen transport (2007) J. Mol. Biol., 371, pp. 168-179
  • Spyrakis, F., Lucas, F., Bidon-Chanal, A., Viappiani, C., Guallar, V., Luque, F.J., Comparative analysis of inner cavities and ligand migration in non-symbiotic AHb1 and AHb2 (2013) Biochim. Biophys. Acta, 1834, pp. 1957-1967
  • Hargrove, M.S., Barry, J.K., Brucker, E.A., Berry, M.B., Phillips, G.N., Jr., Olson, J.S., Arredondo-Peter, R., Sarath, G., Characterization of recombinant soybean leghemoglobin a and apolar distal histidine mutants (1997) J. Mol. Biol., 266, pp. 1032-1042
  • Vallone, B., Nienhaus, K., Brunori, M., Nienhaus, G.U., The structure of murine neuroglobin: Novel pathways for ligand migration and binding (2004) Proteins, 56, pp. 85-92
  • 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, pp. 6754-6762
  • Du, W., Syvitski, R., Dewilde, S., Moens, L., La Mar, G.N., Solution 1h NMR characterization of equilibrium heme orientational disorder with functional consequences in mouse neuroglobin (2003) J. Am. Chem. Soc., 125, pp. 8080-8081
  • Bruno, S., Faggiano, S., Spyrakis, F., Mozzarelli, A., Abbruzzetti, S., Grandi, E., Viappiani, C., Dominici, P., The reactivity with CO of AHb1 and AHb2 from Arabidopsis thaliana is controlled by the distal HisE7 and internal hydrophobic cavities (2007) J. Am. Chem. Soc., 129, pp. 2880-2889
  • Yang, F., Phillips, G.N., Jr., Crystal structures of CO-, deoxy- and met-myoglobins at various pH values (1996) J. Mol. Biol., 256, pp. 762-774
  • 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 Struct. Funct. Genet., 65, pp. 712-725
  • Leach, A.R., (2001) Molecular Modelling: Principles and Applications, , Pearson Education EMA
  • Pearlman, D.A., Case, D.A., Caldwell, J.W., Ross, W.S., Cheatham, T.E., III, 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
  • Berendsen, H.J.C., Postma, J.P.M., Van Gunsteren, W.F., Dinola, A., Haak, J.R., Molecular dynamics with coupling to an external bath (1984) J. Chem. Phys., 81, pp. 3684-3690
  • Amadei, A., Linssen, A.B., Berendsen, H.J., Essential dynamics of proteins (1993) Proteins, 17, pp. 412-425
  • Bidon-Chanal, A., Marti, 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, 64, pp. 457-464

Citas:

---------- APA ----------
Boron, I., Capece, L., Pennacchietti, F., Wetzler, D.E., Bruno, S., Abbruzzetti, S., Chisari, L.,..., Nadra, A.D. (2015) . Engineered chimeras reveal the structural basis of hexacoordination in globins: A case study of neuroglobin and myoglobin. Biochimica et Biophysica Acta - General Subjects, 1850(1), 169-177.
http://dx.doi.org/10.1016/j.bbagen.2014.10.006
---------- CHICAGO ----------
Boron, I., Capece, L., Pennacchietti, F., Wetzler, D.E., Bruno, S., Abbruzzetti, S., et al. "Engineered chimeras reveal the structural basis of hexacoordination in globins: A case study of neuroglobin and myoglobin" . Biochimica et Biophysica Acta - General Subjects 1850, no. 1 (2015) : 169-177.
http://dx.doi.org/10.1016/j.bbagen.2014.10.006
---------- MLA ----------
Boron, I., Capece, L., Pennacchietti, F., Wetzler, D.E., Bruno, S., Abbruzzetti, S., et al. "Engineered chimeras reveal the structural basis of hexacoordination in globins: A case study of neuroglobin and myoglobin" . Biochimica et Biophysica Acta - General Subjects, vol. 1850, no. 1, 2015, pp. 169-177.
http://dx.doi.org/10.1016/j.bbagen.2014.10.006
---------- VANCOUVER ----------
Boron, I., Capece, L., Pennacchietti, F., Wetzler, D.E., Bruno, S., Abbruzzetti, S., et al. Engineered chimeras reveal the structural basis of hexacoordination in globins: A case study of neuroglobin and myoglobin. Biochim. Biophys. Acta Gen. Subj. 2015;1850(1):169-177.
http://dx.doi.org/10.1016/j.bbagen.2014.10.006