ATP regulation of the ligand-binding properties in temperate and cold-adapted haemoglobins. X-ray structure and ligand-binding kinetics in the sub-Antarctic fish Eleginops maclovinus

Daniela Coppola; Stefania Abbruzzetti; Francesco Nicoletti; Antonello Merlino; Alessandra Gambacurta; Daniela Giordano; Barry D. Howes; Giampiero De Sanctis; Luigi Vitagliano; Stefano Bruno; Guido di Prisco; Lelio Mazzarella; Giulietta Smulevich; Massimo Coletta; Cristiano Viappiani; Alessandro Vergara; Cinzia Verde

doi:10.1039/C2MB25210D

ATP regulation of the ligand-binding properties in temperate and cold-adapted haemoglobins. X-ray structure and ligand-binding kinetics in the sub-Antarctic fish Eleginops maclovinus†

Daniela Coppola,^a Stefania Abbruzzetti,^bc Francesco Nicoletti,^d Antonello Merlino,^ef Alessandra Gambacurta,^g Daniela Giordano,^a Barry D. Howes,^d Giampiero De Sanctis,^h Luigi Vitagliano,^f Stefano Bruno,ⁱ Guido di Prisco,^a Lelio Mazzarella,^ef Giulietta Smulevich,^d Massimo Coletta,^jk Cristiano Viappiani,^bc Alessandro Vergara*^ef and Cinzia Verde*^a

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* Corresponding authors

^a Institute of Protein Biochemistry, CNR, Via Pietro Castellino 111, I-80131 Naples, Italy
E-mail: c.verde@ibp.cnr.it
Fax: +39 0816132710
Tel: +39 0816132710

^b Dipartimento di Fisica, Università degli Studi di Parma, viale delle Scienze 7A, 43124 Parma, Italy

^c Istituto Nanoscienze, CNR, Piazza San Silvestro 12 - 56127 Pisa, Italy

^d Dipartimento di Chimica “Ugo Schiff”, Università di Firenze, Via della Lastruccia 3-13, 50019 Sesto Fiorentino (FI), Italy

^e Department of Chemical Sciences, University of Naples “Federico II”, Complesso Universitario Monte S. Angelo, Via Cinthia, 80126 Naples, Italy
E-mail: avergara@unina.it
Fax: +39 081674070
Tel: +39 081674259

^f Istituto di Biostrutture e Bioimmagini, CNR, Via Mezzocannone 6, I-80134 Naples, Italy

^g Dipartimento di Medicina Sperimentale e Chirurgia, Università di Roma Tor Vergata, Via Montpellier 1, 00133 Roma, Italy

^h Scuola di Bioscienze e Biotecnologie, Università di Camerino, 62032 Camerino (MC), Italy

ⁱ Dipartimento di Biochimica e Biologia Molecolare, Università di Parma, Viale G.P. Usberti 23/A, 43100 Parma, Italy

^j Department of Clinical Sciences and Translational Medicine, Università di Roma Tor Vergata, Via Montpellier 1, 00133 Rome, Italy

^k Interuniversity Consortium for the Research on the Chemistry of Metals in Biological Systems, Via C. Ulpiani 27, 70126 Bari, Italy

Abstract

The major haemoglobin of the sub-Antarctic fish Eleginops maclovinus was structurally and functionally characterised with the aim to compare molecular environmental adaptations in the O₂-transport system of sub-Antarctic fishes of the suborder Notothenioidei with those of their high-latitude relatives. Ligand-binding kinetics of the major haemoglobin of E. maclovinus indicated strong stabilisation of the liganded quaternary T state, enhanced in the presence of the physiological allosteric effector ATP, compared to that of high-Antarctic Trematomus bernacchii. The activation enthalpy for O₂ dissociation was dramatically lower than that in T. bernacchii haemoglobin, suggesting remarkable differences in temperature sensitivity and structural changes associated with O₂ release and exit from the protein. The haemoglobin functional properties, together with the X-ray structure of the CO form at 1.49 Å resolution, the first of a temperate notothenioid, strongly support the hypothesis that in E. maclovinus, whose life-style varies according to changes in habitat, the mechanisms that regulate O₂ affinity and the ATP-induced Root effect differ from those of high-Antarctic Notothenioids.

Molecular BioSystems

ATP regulation of the ligand-binding properties in temperate and cold-adapted haemoglobins. X-ray structure and ligand-binding kinetics in the sub-Antarctic fish Eleginops maclovinus†

Abstract

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ATP regulation of the ligand-binding properties in temperate and cold-adapted haemoglobins. X-ray structure and ligand-binding kinetics in the sub-Antarctic fish Eleginops maclovinus

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