Methionine sulfoxide reductase B from Corynebacterium diphtheriae catalyzes sulfoxide reduction via an intramolecular disulfide cascade

[EN] Corynebacterium diphtheriae is a human pathogen that causes diphtheria. In response to immune system-induced oxidative stress, C. diphtheriae expresses antioxidant enzymes, among which are methionine sulfoxide reductase (Msr) enzymes, which are critical for bacterial survival in the face of oxi...

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Detalhes bibliográficos
Autores: Tossounian, Maria-Armineh, Truong, Anh Co Khanh, Buts, Lieven, Wahni, Khadija, Mourenza Flórez, Álvaro, Leermakers, Martine, Vertommen, Didier, Mateos Delgado, Luis Mariano, Volkov, Alexander N., Messens, Joris
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Recursos:Ajuntament de Barcelona
Repositorio:BULERIA. Repositorio Institucional de la Universidad de León
OAI Identifier:oai:buleria.unileon.es:10612/23472
Acesso em linha:https://www.sciencedirect.com/science/article/pii/S0021925817486339
https://hdl.handle.net/10612/23472
Access Level:acceso abierto
Palavra-chave:Bioquímica
Enzyme mechanism
Enzyme structure
Nuclear magnetic resonance (NMR)
Kinetics
Redox regulation
Biochemistry
Hydrogen peroxide
Methionine sulfoxide
2302.09 Enzimología
2306.09 Radicales Libres
2414.03 Metabolismo Bacteriano
2415.01 Biología Molecular de Microorganismos
Descrição
Resumo:[EN] Corynebacterium diphtheriae is a human pathogen that causes diphtheria. In response to immune system-induced oxidative stress, C. diphtheriae expresses antioxidant enzymes, among which are methionine sulfoxide reductase (Msr) enzymes, which are critical for bacterial survival in the face of oxidative stress. Although some aspects of the catalytic mechanism of the Msr enzymes have been reported, several details still await full elucidation. Here, we solved the solution structure of C. diphtheriae MsrB (Cd-MsrB) and unraveled its catalytic and oxidation-protection mechanisms. Cd-MsrB catalyzes methionine sulfoxide reduction involving three redox-active cysteines. Using NMR heteronuclear single-quantum coherence spectra, kinetics, biochemical assays, and MS analyses, we show that the conserved nucleophilic residue Cys-122 is S-sulfenylated after substrate reduction, which is then resolved by a conserved cysteine, Cys-66, or by the nonconserved residue Cys-127. We noted that the overall structural changes during the disulfide cascade expose the Cys-122–Cys-66 disulfide to recycling through thioredoxin. In the presence of hydrogen peroxide, Cd-MsrB formed reversible intra- and intermolecular disulfides without losing its Cys-coordinated Zn2+, and only the nonconserved Cys-127 reacted with the low-molecular-weight (LMW) thiol mycothiol, protecting it from overoxidation. In summary, our structure-function analyses reveal critical details of the Cd-MsrB catalytic mechanism, including a major structural rearrangement that primes the Cys-122–Cys-66 disulfide for thioredoxin reduction and a reversible protection against excessive oxidation of the catalytic cysteines in Cd-MsrB through intra- and intermolecular disulfide formation and S-mycothiolation