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Factors that Affect Oxygen Activation and Coupling of the Two Redox Cycles in the Aromatization Reaction Catalyzed by NikD, an Unusual Amino Acid Oxidase
Journal article   Open access   Peer reviewed

Factors that Affect Oxygen Activation and Coupling of the Two Redox Cycles in the Aromatization Reaction Catalyzed by NikD, an Unusual Amino Acid Oxidase

Phaneeswara-Rao Kommoju, Robert C Bruckner, Patricia Ferreira, Christopher J Carrell, F. Scott Mathews and Marilyn Schuman Jorns
Biochemistry (Easton), v 48(40), pp 9542-9555
13 Oct 2009
PMID: 19702312
url
https://doi.org/10.1021/bi901056aView
Published, Version of Record (VoR) Open

Abstract

NikD is a flavoprotein oxidase that catalyzes the oxidation of piperideine-2-carboxylate (P2C) to picolinate in a remarkable aromatization reaction comprising two redox cycles and at least one isomerization step. Tyr258 forms part of an "aromatic cage" that surrounds the ring in picolinate and its precursors. Mutation of Tyr258 to Phe does not perturb the structure of nikD but does affect the coupling of the two redox cycles and causes a 10-fold decrease in turnover rate. Tyr258Phe catalyzes a quantitative 2-electron oxidation of P2C but only 60% of the resulting dihydropicolinate intermediate undergoes a second redox cycle to produce picolinate. The mutation does not affect product yield with an alternate substrate (3,4-dehydro-L-proline) that is aromatized in a single 2-electron oxidation step. Wild-type and mutant enzyme exhibit identical rate constants for P2C oxidation to dihydropicolinate and isomerization of a reduced enzyme•dihydropicolinate complex. The observed rates are 200- and 10-fold faster, respectively, than the mutant turnover rate. Picolinate release from Tyr258Phe is 100-fold faster than turnover. The presence of bound substrate or product is a key factor in oxygen activation by wild-type nikD, as judged by the 10- to 75-fold faster rates observed for complexes of the reduced enzyme with picolinate, benzoate or 1-cyclohexenoate, a 1-deaza P2C analog. The reduced Tyr258Phe•1-cyclohexenoate complex is 25-fold less reactive with oxygen than the wild-type complex. We postulate that mutation of Tyr258 causes subtle changes in active site dynamics that promote release of the reactive dihydropicolinate intermediate and disrupt the efficient synchronization of oxygen activation observed with wild-type nikD.

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Web of Science research areas
Biochemistry & Molecular Biology
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