Reduction of Protein Bound Methionine Sulfoxide by a Periplasmic Dimethyl Sulfoxide Reductase

Tarrago, Lionel; Grosse, Sandrine; Lemaire, David; Faure, Laëtitia; Tribout, Mathilde; Siponen, M.I.; Kojadinovic-Sirinelli, Mila; Pignol, David; Arnoux, Pascal; Sabaty, Monique

doi:10.3390/antiox9070616

Cited by 12 publications

(21 citation statements)

References 46 publications

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“…Nevertheless, DmsA was not demonstrated to reduce Met-O within proteins. Recently, the Rhodobacter sphaeroides periplasmic DMSO reductase DorA-type has been elegantly shown to reduce protein-bound S-Met-O ( Tarrago et al, 2020 ). In conclusion, MsrA, MsrB, MsrP, and DorA can reduce protein-bound Met-O residues and, per se , are involved in protein quality control processes.…”

Section: Introductionmentioning

confidence: 99%

Methionine Redox Homeostasis in Protein Quality Control

Aussel¹,

Ezraty²

2021

Front. Mol. Biosci.

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Bacteria live in different environments and are subject to a wide variety of fluctuating conditions. During evolution, they acquired sophisticated systems dedicated to maintaining protein structure and function, especially during oxidative stress. Under such conditions, methionine residues are converted into methionine sulfoxide (Met-O) which can alter protein function. In this review, we focus on the role in protein quality control of methionine sulfoxide reductases (Msr) which repair oxidatively protein-bound Met-O. We discuss our current understanding of the importance of Msr systems in rescuing protein function under oxidative stress and their ability to work in coordination with chaperone networks. Moreover, we highlight that bacterial chaperones, like GroEL or SurA, are also targeted by oxidative stress and under the surveillance of Msr. Therefore, integration of methionine redox homeostasis in protein quality control during oxidative stress gives a complete picture of this bacterial adaptive mechanism.

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Section: Introductionmentioning

confidence: 99%

Methionine Redox Homeostasis in Protein Quality Control

Aussel¹,

Ezraty²

2021

Front. Mol. Biosci.

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“…Another enzyme, fRMsr (free methionine-(R)-sulfoxide reductase) specifically reduces the free form of Met-R-O [7][8][9]. Some bacteria also possess several molybdoenzymes that reduce exclusively the free MetO [10,11] or both the free and protein-bound MetO [12][13][14][15]. Despite the lack of sequence and structure similarities, MsrA, MsrB and fRMsr generally catalyze the reduction of MetO using a similar 3-steps-mechanism [9,16] : i) a 'catalytic' Cys (or, less frequently, a selenocysteine, Sec) reduces the target MetO and is converted into a sulfenic (or selenic) acid [17], ii) an internal 'resolving' Cys reduces it through the formation of an intramolecular disulfide bond, and finally iii) the oxidized Msr is regenerated through disulfide exchange with a thioredoxin [18].…”

Section: Introductionmentioning

confidence: 99%

Distribution of methionine sulfoxide reductases in fungi and conservation of the free-methionine-R-sulfoxide reductase in multicellular eukaryotes

Hage

Rosso

Tarrago

2021

Free Radical Biology and Medicine

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Methionine, either as a free amino acid or included in proteins, can be oxidized into methionine sulfoxide (MetO), which exists as R and S diastereomers. Almost all characterized organisms possess thioloxidoreductases named methionine sulfoxide reductase (Msr) enzymes to reduce MetO back to Met.MsrA and MsrB reduce the S and R diastereomers of MetO, respectively, with strict stereospecificity and are found in almost all organisms. Another type of thiol-oxidoreductase, the free-methionine-Rsulfoxide reductase (fRMsr), identified so far in prokaryotes and a few unicellular eukaryotes, reduces the R MetO diastereomer of the free amino acid. Moreover, some bacteria possess molybdenumcontaining enzymes that reduce MetO, either in the free or protein-bound forms. All these Msrs play important roles in the protection of organisms against oxidative stress. Fungi are heterotrophic eukaryotes that colonize all niches on Earth and play fundamental functions, in organic matter recycling, as symbionts, or as pathogens of numerous organisms. However, our knowledge on fungal Msrs is still limited. Here, we performed a survey of msr genes in almost 700 genomes across the fungal kingdom.We show that most fungi possess one gene coding for each type of methionine sulfoxide reductase: MsrA, MsrB, and fRMsr. However, several fungi living in anaerobic environments or as obligate intracellular parasites were devoid of msr genes. Sequence inspection and phylogenetic analyses allowed us to identify non-canonical sequences with potentially novel enzymatic properties. Finaly, we identified several ocurences of msr horizontal gene transfer from bacteria to fungi. Material and methods Search for Msr homologs in fungi.The protein sequence of MsrA (Uniprot accession # C8Z745), MsrB (Uniprot accession # P25566) and fRMsr (Uniprot accession # P36088) from S. cerevisiae, MsrP (Uniprot accession # P76342) and BisC (Uniprot accession # P20099) from Escherichia coli, TorZ (Uniprot accession # P44798) from Haemophilus influenzae, and DorA (Uniprot accession # Q57366) from Rhodobacter sphaeroides were used as BLASTP and TBLASTN [49] queries to identify msr genes in 683 genomes available in the MycoCosm database [50] (https://mycocosm.jgi.doe.gov/mycocosm/home). 2.2.List of all explored fungal genomes.

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“…The reaction is reversible thanks to the action of methionine sulfoxide reductase (Msr) [12]. Four types of Msr have been identified that reduce Met(O) residues to their functional form [13]. The main types are the thiol-oxidoreductases MsrA and MsrB, which react specifically with diastereomers displaying the S-and R-configurations at the sulfur atom, respectively [14,15].…”

Section: Introductionmentioning

confidence: 99%

“…The fourth type of Msr belongs to the dimethyl sulfoxide (DMSO) reductase family. One example is the periplasmic Rhodobacter sphaeroides DorA DMSO reductase, which reduces DMSO and both free and protein-bound Met-S-O [13]. The primary role of the first three types of Msr is to regulate the Met(O) level in proteins; they reduce Met(O) residues more efficiently in unfolded proteins than in folded proteins [17].…”

Section: Introductionmentioning

confidence: 99%

Methionine Sulfoxide Reductases Contribute to Anaerobic Fermentative Metabolism in Bacillus cereus

et al. 2021

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Reversible oxidation of methionine to methionine sulfoxide (Met(O)) is a common posttranslational modification occurring on proteins in all organisms under oxic conditions. Protein-bound Met(O) is reduced by methionine sulfoxide reductases, which thus play a significant antioxidant role. The facultative anaerobe Bacillus cereus produces two methionine sulfoxide reductases: MsrA and MsrAB. MsrAB has been shown to play a crucial physiological role under oxic conditions, but little is known about the role of MsrA. Here, we examined the antioxidant role of both MsrAB and MrsA under fermentative anoxic conditions, which are generally reported to elicit little endogenous oxidant stress. We created single- and double-mutant Δmsr strains. Compared to the wild-type and ΔmsrAB mutant, single- (ΔmsrA) and double- (ΔmsrAΔmsrAB) mutants accumulated higher levels of Met(O) proteins, and their cellular and extracellular Met(O) proteomes were altered. The growth capacity and motility of mutant strains was limited, and their energy metabolism was altered. MsrA therefore appears to play a major physiological role compared to MsrAB, placing methionine sulfoxides at the center of the B. cereus antioxidant system under anoxic fermentative conditions.

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Reduction of Protein Bound Methionine Sulfoxide by a Periplasmic Dimethyl Sulfoxide Reductase

Cited by 12 publications

References 46 publications

Methionine Redox Homeostasis in Protein Quality Control

Methionine Redox Homeostasis in Protein Quality Control

Distribution of methionine sulfoxide reductases in fungi and conservation of the free-methionine-R-sulfoxide reductase in multicellular eukaryotes

Methionine Sulfoxide Reductases Contribute to Anaerobic Fermentative Metabolism in Bacillus cereus

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