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NO Binding and Dynamics in Reduced Heme−Copper Oxidases aa3 from Paracoccus denitrificans and ba3 from Thermus thermophilus†

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Laboratory for Optical Biosciences, INSERM U451, CNRS UMR 7645, Ecole Polytechnique-ENSTA, 91128 Palaiseau Cedex, France, Laboratoire de Bioénergétique et Ingéniérie des Protéines UPR 9036, Institut de Biologie Structurale et Microbiologie, CNRS, 31, Chemin Joseph Aiguier, 13402 Marseille, Cedex 20, France, Institut de Biologie Physico-Chimique, CNRS UPR 1261, 13 rue Pierre et Marie Curie, 75005 Paris, France, and Paul Scherrer Institute, Life Sciences, OSRA/008, CH-5232 Villigen PSI, Switzerland
Cite this: Biochemistry 2004, 43, 44, 14118–14127
Publication Date (Web):October 16, 2004
https://doi.org/10.1021/bi0488808
Copyright © 2004 American Chemical Society
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    Abstract

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    Cytochrome c oxidase (CcO) has a high affinity for nitric oxide (NO), a property involved in the regulation of respiration. It has been shown that the recombination kinetics of photolyzed NO with reduced CcO from Paracoccus denitrificans on the picosecond time scale depend strongly on the NO/enzyme stoichiometry and inferred that more than one NO can be accommodated by the active site, already at mildly suprastoichiometric NO concentrations. We have largely extended these studies by monitoring rebinding dynamics from the picosecond to the microsecond time scale, by performing parallel steady-state low-temperature electron paramagnetic resonance (EPR) characterizations on samples prepared similarly as for the optical experiments and comparing them with molecular-modeling results. A comparative study was performed on CcO ba3 from Thermus thermophilus, where two NO molecules cannot be copresent in the active site in the steady state because of its NO reductase activity. The kinetic results allow discrimination between different models of NO-dependent recombination and show that the overall NO escape probability out of the protein is high when only one NO is bound to CcO aa3, whereas strong rebinding on the 15-ns time scale was observed for CcO ba3. The EPR characterizations show similar results for aa3 at substoichiometric NO/enzyme ratios and for ba3, indicating formation of a 6-coordinate heme−NO complex. The presence of a second NO molecule in the aa3 active site strongly modifies the heme−NO EPR spectrum and can be rationalized by a rotation of the Fe−N−O plane with respect to the histidine that coordinates the heme iron. This proposal is supported by molecular-modeling studies that indicate a ∼63° rotation of heme-bound NO upon binding of a second NO to the close-lying copper center CuB. It is argued that the second NO binds to CuB.

    †

     This work was supported by the CNRS program “Physique et Chimie du Vivant”.

    ‡

     Ecole Polytechnique-ENSTA.

    §

     Institut de Biologie Structurale et Microbiologie.

    ‖

     Institut de Biologie Physico-Chimique.

    ⊥

     Paul Scherrer Institute.

    *

     To whom correspondence should be addressed. Phone:  +33-1-69334777. Fax:  +33-3-69333017. E-mail:  [email protected].

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    15. Takahiro Hayashi, I-Jin Lin, Ying Chen, James A. Fee, Pierre Moënne-Loccoz. Fourier Transform Infrared Characterization of a Cu B −Nitrosyl Complex in Cytochrome ba 3 from Thermus thermophilus :  Relevance to NO Reductase Activity in Heme−Copper Terminal Oxidases. Journal of the American Chemical Society 2007, 129 (48) , 14952-14958. https://doi.org/10.1021/ja074600a
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    17. Pierre Moënne-Loccoz. Spectroscopic characterization of heme iron–nitrosyl species and their role in NO reductase mechanisms in diiron proteins. Nat. Prod. Rep. 2007, 24 (3) , 610-620. https://doi.org/10.1039/B604194A
    18. Maria G. Mason, Peter Nicholls, Michael T. Wilson, Christopher E. Cooper. Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proceedings of the National Academy of Sciences 2006, 103 (3) , 708-713. https://doi.org/10.1073/pnas.0506562103
    19. Eftychia Pinakoulaki, Takehiro Ohta, Tewfik Soulimane, Teizo Kitagawa, Constantinos Varotsis. Detection of the His-Heme Fe 2+ −NO Species in the Reduction of NO to N 2 O by b a 3 -Oxidase from Thermus t hermophilus. Journal of the American Chemical Society 2005, 127 (43) , 15161-15167. https://doi.org/10.1021/ja0539490
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