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Kinetics and Interactions of Molybdenum and Iron−Sulfur Centers in Bacterial Enzymes of the Xanthine Oxidase Family:  Mechanistic Implications

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Fachrichtung Biophysik und Physikalische Grundlagen der Medizin, Universität des Saarlandes, Klinikum Geb. 76, D-66421 Homburg/Saar, Germany, John Innes Centre, Colney, Norwich NR4 7UH, U.K., School of Biological Science, University of Sussex, Brighton BN1 9QG, Sussex, U.K., School of Chemistry, Physics and Environmental Science, University of Sussex, Brighton BN1 9QJ, Sussex, U.K., and Fachbereich Biologie, Carl von Ossietzky Universität Oldenburg, Postfach 2503, D-26111 Oldenburg, Germany
Cite this: Biochemistry 1999, 38, 42, 14077–14087
Publication Date (Web):October 1, 1999
https://doi.org/10.1021/bi991089s
Copyright © 1999 American Chemical Society

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    Abstract

    For isoquinoline 1-oxidoreductase (IsoOr), the reaction mechanism under turnover conditions was studied by EPR spectroscopy using rapid-freeze methods. IsoOr displays several EPR-active Mo(V) species including the “very rapid” component found also in xanthine oxidase (XanOx). For IsoOr, unlike XanOx or quinoline 2-oxidoreductase (QuinOr), this species is stable for about 1 h in the absence of an oxidizing substrate [Canne, C., Stephan, I., Finsterbusch, J., Lingens, F., Kappl, R., Fetzner, S., and Hüttermann, J. (1997) Biochemistry36, 9780−9790]. Under rapid-freeze conditions in the presence of ferricyanide the very rapid species behaves as a kinetically competent intermediate present only during steady-state turnover. To explain the persistence of the very rapid species in IsoOr in the absence of an added oxidant, extremely slow product dissociation is required. This new finding that oxidative conditions facilitate decay of the very rapid signal for IsoOr supports the mechanism of substrate turnover proposed by Lowe, Richards, and Bray [Lowe, D. J., Richards, R. L., and Bray, R. C. (1997) Biochem. Soc. Trans. 25, 774−778]. Additional stopped-flow data reveal that alternative catalytic cycles occur in IsoOr and show that the product dissociates after transfer of a single oxidizing equivalent from ferricyanide. In rapid-freeze measurements magnetic interactions of the very rapid Mo(V) species and the iron−sulfur center FeSI of IsoOr and QuinOr were observed, proving that FeSI is located close to the molybdopterin cofactor in the two proteins. This finding is used to relate the two different iron−sulfur centers of the aldehyde oxidoreductase structure with the EPR-detectable FeS species of the enzymes.

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     Universität des Saarlandes.

    §

     John Innes Centre, Norwich.

     Universität Oldenburg.

     Biological Sciences, University of Sussex.

    #

     Chemistry, Physics and Environmental Science, University of Sussex.

    *

     To whom correspondence should be addressed.

     This work was supported by grants from the Deutsche Forschungsgemeinschaft (DFG), grants Hu 248/11-2 and Fe 383/4-2. Work at University of Sussex was supported in part by a grant from the Wellcome Trust.

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