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Selective Inactivation of Parvulin-Like Peptidyl-Prolyl cis/trans Isomerases by Juglone

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    Selective Inactivation of Parvulin-Like Peptidyl-Prolyl cis/trans Isomerases by Juglone†
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    Max-Planck Research Unit, Enzymology of Protein Folding, Kurt-Mothes-Str. 3, D-06120 Halle/Saale, Germany, Institute of Biology II, Albert-Ludwigs-University Freiburg, Schänzlestr. 1, D-79104 Freiburg i. Br., Germany, and Hans-Knöll-Institute of Natural Products Research e.V., Beutenbergstr. 11, D-07745 Jena, Germany
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    Biochemistry

    Cite this: Biochemistry 1998, 37, 17, 5953–5960
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    https://doi.org/10.1021/bi973162p
    Published April 4, 1998
    Copyright © 1998 American Chemical Society
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    Abstract

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    In contrast to FK506 binding proteins and cyclophilins, the parvulin family of peptidyl-prolyl cis/trans isomerases (PPIases; E.C. 5.2.1.8) cannot be inhibited by either FK506 or cyclosporin A. We have found that juglone, 5-hydroxy-1,4-naphthoquinone, irreversibly inhibits the enzymatic activity of several parvulins, like the E. coli parvulin, the yeast Ess1/Ptf1, and human Pin1, in a specific manner, thus allowing selective inactivation of these enzymes in the presence of other PPIases. The mode of action was studied by analyzing the inactivation kinetics and the nature of products of the reaction of E. coli parvulin and its Cys69Ala variant with juglone. For all parvulins investigated, complete inactivation was obtained by a slow process that is characterized by pseudo-first-order rate constants in the range of 5.3 × 10-4 to 4.5 × 10-3 s-1. The inactivated parvulin contains two juglone molecules that are covalently bound to the side chains of Cys41 and Cys69 because of a Michael addition of the thiol groups to juglone. Redox reactions did not contribute to the inactivation process. Because thiol group modification was shown to proceed 5-fold faster than the rate of enzyme inactivation, it was considered as a necessary but not sufficient condition for inactivation. When measured by far-UV circular dichroism (CD), the rate of structural alterations following thiol group modification parallels exactly the rate of inactivation. Thus, partial unfolding of the active site of the parvulins was thought to be the cause of the deterioration of PPIase activity.

    Copyright © 1998 American Chemical Society

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    †

     This work was supported by a grant of the Deutsche Forschungsgemeinschaft (Fi 455/1-3), the Fonds der Chemischen Industrie and the Boehringer Ingelheim Stiftung.

    ‡

     Institute of Biology II.

    §

     Max-Planck Research Unit Enzymology of Protein Folding.

    ∇

     Hans-Knöll Institute of Natural Products Research.

    *

     Corresponding author. Phone:  +49345 5522801. Fax:  +49345 5511972.

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    Biochemistry

    Cite this: Biochemistry 1998, 37, 17, 5953–5960
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    https://doi.org/10.1021/bi973162p
    Published April 4, 1998
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