Protection of the Queuosine Biosynthesis Enzyme QueF from Irreversible Oxidation by a Conserved Intramolecular Disulfide

Mohammad, Adeba; Bon Ramos, Adriana; Lee, Bobby W. K.; Cohen, Spencer W.; Kiani, Maryam K.; Iwata-Reuyl, Dirk; Stec, Boguslaw; Swairjo, Manal

doi:10.3390/biom7010030

Protection of the Queuosine Biosynthesis Enzyme QueF from Irreversible Oxidation by a Conserved Intramolecular Disulfide

Journal Article · Thu Mar 16 00:00:00 EDT 2017 · Biomolecules

DOI:https://doi.org/10.3390/biom7010030· OSTI ID:1628313

Mohammad, Adeba ^[1]; Bon Ramos, Adriana ^[2]; Lee, Bobby W. K. ^[2]; Cohen, Spencer W. ^[2]; Kiani, Maryam K. ^[3]; Iwata-Reuyl, Dirk ^[2]; Stec, Boguslaw ^[4]; Swairjo, Manal ^[3]

Western University of Health Sciences, Pomona, CA (United States); DOE/OSTI
Portland State Univ., OR (United States)
Western University of Health Sciences, Pomona, CA (United States)
San Diego State Univ., CA (United States)

QueF enzymes catalyze the nicotinamide adenine dinucleotide phosphate (NADPH)-dependent reduction of the nitrile group of 7-cyano-7-deazaguanine (preQ0) to 7-aminomethyl-7-deazaguanine (preQ1) in the biosynthetic pathway to the tRNA modified nucleoside queuosine. The QueF-catalyzed reaction includes formation of a covalent thioimide intermediate with a conserved active site cysteine that is prone to oxidation in vivo. Here, we report the crystal structure of a mutant of Bacillus subtilis QueF, which reveals an unanticipated intramolecular disulfide formed between the catalytic Cys55 and a conserved Cys99 located near the active site. This structure is more symmetric than the substrate-bound structure and exhibits major rearrangement of the loops responsible for substrate binding. Mutation of Cys99 to Ala/Ser does not compromise enzyme activity, indicating that the disulfide does not play a catalytic role. Peroxide-induced inactivation of the wild-type enzyme is reversible with thioredoxin, while such inactivation of the Cys99Ala/Ser mutants is irreversible, consistent with protection of Cys55 from irreversible oxidation by disulfide formation with Cys99. Conservation of the cysteine pair, and the reported in vivo interaction of QueF with the thioredoxin-like hydroperoxide reductase AhpC in Escherichia coli suggest that regulation by the thioredoxin disulfide-thiol exchange system may constitute a general mechanism for protection of QueF from oxidative stress in vivo.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory, Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1628313

Journal Information:: Biomolecules, Journal Name: Biomolecules Journal Issue: 4 Vol. 7; ISSN 2218-273X; ISSN BIOMHC

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

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Interplay of nucleophilic catalysis with proton transfer in the nitrile reductase QueF from Escherichia coli Jung, Jihye; Braun, Jan; Czabany, Tibor Catalysis Science & Technology, Vol. 9, Issue 3 https://doi.org/10.1039/c8cy02331j	journal	January 2019
Evidence of a sequestered imine intermediate during reduction of nitrile to amine by the nitrile reductase QueF from Escherichia coli Jung, Jihye; Nidetzky, Bernd Journal of Biological Chemistry, Vol. 293, Issue 10 https://doi.org/10.1074/jbc.m117.804583	journal	January 2018
Allosteric disulfides: Sophisticated molecular structures enabling flexible protein regulation Chiu, Joyce; Hogg, Philip J. Journal of Biological Chemistry, Vol. 294, Issue 8 https://doi.org/10.1074/jbc.rev118.005604	journal	January 2019

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Protection of the Queuosine Biosynthesis Enzyme QueF from Irreversible Oxidation by a Conserved Intramolecular Disulfide

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