Diversity of Plant Methionine Sulfoxide Reductases B and Evolution of a Form Specific for Free Methionine Sulfoxide

Dung Tien Le, Lionel Tarrago, Yasuko Watanabe, Alaattin Kaya, Byung Cheon Lee, Uyen Tran, Rie Nishiyama, Dmitri E. Fomenko, Vadim N. Gladyshev, Lam Son Phan Tran

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Methionine can be reversibly oxidized to methionine sulfoxide (MetO) under physiological conditions. Organisms evolved two distinct methionine sulfoxide reductase families (MSRA & MSRB) to repair oxidized methionine residues. We found that 5 MSRB genes exist in the soybean genome, including GmMSRB1 and two segmentally duplicated gene pairs (GmMSRB2 and GmMSRB5, GmMSRB3 and GmMSRB4). GmMSRB2 and GmMSRB4 proteins showed MSRB activity toward protein-based MetO with either DTT or thioredoxin (TRX) as reductants, whereas GmMSRB1 was active only with DTT. GmMSRB2 had a typical MSRB mechanism with Cys121 and Cys 68 as catalytic and resolving residues, respectively. Surprisingly, this enzyme also possessed the MSRB activity toward free Met-R-O with kinetic parameters similar to those reported for fRMSR from Escherichia coli, an enzyme specific for free Met-R-O. Overexpression of GmMSRB2 or GmMSRB4 in the yeast cytosol supported the growth of the triple MSRA/MSRB/fRMSR (Δ3MSRs) mutant on MetO and protected cells against H2O2-induced stress. Taken together, our data reveal an unexpected diversity of MSRBs in plants and indicate that, in contrast to mammals that cannot reduce free Met-R-O and microorganisms that use fRMSR for this purpose, plants evolved MSRBs for the reduction of both free and protein-based MetO.

Original languageEnglish
Article numbere65637
JournalPloS one
Volume8
Issue number6
DOIs
Publication statusPublished - 2013 Jun 12
Externally publishedYes

Fingerprint

Methionine Sulfoxide Reductases
methionine
Genes
Methionine
Thioredoxins
Proteins
Mammals
Reducing Agents
Enzymes
Soybeans
Kinetic parameters
Microorganisms
Cytosol
Yeast
Escherichia coli
reducing agents
proteins
Repair
enzymes
Yeasts

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Diversity of Plant Methionine Sulfoxide Reductases B and Evolution of a Form Specific for Free Methionine Sulfoxide. / Le, Dung Tien; Tarrago, Lionel; Watanabe, Yasuko; Kaya, Alaattin; Lee, Byung Cheon; Tran, Uyen; Nishiyama, Rie; Fomenko, Dmitri E.; Gladyshev, Vadim N.; Tran, Lam Son Phan.

In: PloS one, Vol. 8, No. 6, e65637, 12.06.2013.

Research output: Contribution to journalArticle

Le, DT, Tarrago, L, Watanabe, Y, Kaya, A, Lee, BC, Tran, U, Nishiyama, R, Fomenko, DE, Gladyshev, VN & Tran, LSP 2013, 'Diversity of Plant Methionine Sulfoxide Reductases B and Evolution of a Form Specific for Free Methionine Sulfoxide', PloS one, vol. 8, no. 6, e65637. https://doi.org/10.1371/journal.pone.0065637
Le, Dung Tien ; Tarrago, Lionel ; Watanabe, Yasuko ; Kaya, Alaattin ; Lee, Byung Cheon ; Tran, Uyen ; Nishiyama, Rie ; Fomenko, Dmitri E. ; Gladyshev, Vadim N. ; Tran, Lam Son Phan. / Diversity of Plant Methionine Sulfoxide Reductases B and Evolution of a Form Specific for Free Methionine Sulfoxide. In: PloS one. 2013 ; Vol. 8, No. 6.
@article{6c5f50d0f81b454db7abd8e1241f174f,
title = "Diversity of Plant Methionine Sulfoxide Reductases B and Evolution of a Form Specific for Free Methionine Sulfoxide",
abstract = "Methionine can be reversibly oxidized to methionine sulfoxide (MetO) under physiological conditions. Organisms evolved two distinct methionine sulfoxide reductase families (MSRA & MSRB) to repair oxidized methionine residues. We found that 5 MSRB genes exist in the soybean genome, including GmMSRB1 and two segmentally duplicated gene pairs (GmMSRB2 and GmMSRB5, GmMSRB3 and GmMSRB4). GmMSRB2 and GmMSRB4 proteins showed MSRB activity toward protein-based MetO with either DTT or thioredoxin (TRX) as reductants, whereas GmMSRB1 was active only with DTT. GmMSRB2 had a typical MSRB mechanism with Cys121 and Cys 68 as catalytic and resolving residues, respectively. Surprisingly, this enzyme also possessed the MSRB activity toward free Met-R-O with kinetic parameters similar to those reported for fRMSR from Escherichia coli, an enzyme specific for free Met-R-O. Overexpression of GmMSRB2 or GmMSRB4 in the yeast cytosol supported the growth of the triple MSRA/MSRB/fRMSR (Δ3MSRs) mutant on MetO and protected cells against H2O2-induced stress. Taken together, our data reveal an unexpected diversity of MSRBs in plants and indicate that, in contrast to mammals that cannot reduce free Met-R-O and microorganisms that use fRMSR for this purpose, plants evolved MSRBs for the reduction of both free and protein-based MetO.",
author = "Le, {Dung Tien} and Lionel Tarrago and Yasuko Watanabe and Alaattin Kaya and Lee, {Byung Cheon} and Uyen Tran and Rie Nishiyama and Fomenko, {Dmitri E.} and Gladyshev, {Vadim N.} and Tran, {Lam Son Phan}",
year = "2013",
month = "6",
day = "12",
doi = "10.1371/journal.pone.0065637",
language = "English",
volume = "8",
journal = "PLoS One",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "6",

}

TY - JOUR

T1 - Diversity of Plant Methionine Sulfoxide Reductases B and Evolution of a Form Specific for Free Methionine Sulfoxide

AU - Le, Dung Tien

AU - Tarrago, Lionel

AU - Watanabe, Yasuko

AU - Kaya, Alaattin

AU - Lee, Byung Cheon

AU - Tran, Uyen

AU - Nishiyama, Rie

AU - Fomenko, Dmitri E.

AU - Gladyshev, Vadim N.

AU - Tran, Lam Son Phan

PY - 2013/6/12

Y1 - 2013/6/12

N2 - Methionine can be reversibly oxidized to methionine sulfoxide (MetO) under physiological conditions. Organisms evolved two distinct methionine sulfoxide reductase families (MSRA & MSRB) to repair oxidized methionine residues. We found that 5 MSRB genes exist in the soybean genome, including GmMSRB1 and two segmentally duplicated gene pairs (GmMSRB2 and GmMSRB5, GmMSRB3 and GmMSRB4). GmMSRB2 and GmMSRB4 proteins showed MSRB activity toward protein-based MetO with either DTT or thioredoxin (TRX) as reductants, whereas GmMSRB1 was active only with DTT. GmMSRB2 had a typical MSRB mechanism with Cys121 and Cys 68 as catalytic and resolving residues, respectively. Surprisingly, this enzyme also possessed the MSRB activity toward free Met-R-O with kinetic parameters similar to those reported for fRMSR from Escherichia coli, an enzyme specific for free Met-R-O. Overexpression of GmMSRB2 or GmMSRB4 in the yeast cytosol supported the growth of the triple MSRA/MSRB/fRMSR (Δ3MSRs) mutant on MetO and protected cells against H2O2-induced stress. Taken together, our data reveal an unexpected diversity of MSRBs in plants and indicate that, in contrast to mammals that cannot reduce free Met-R-O and microorganisms that use fRMSR for this purpose, plants evolved MSRBs for the reduction of both free and protein-based MetO.

AB - Methionine can be reversibly oxidized to methionine sulfoxide (MetO) under physiological conditions. Organisms evolved two distinct methionine sulfoxide reductase families (MSRA & MSRB) to repair oxidized methionine residues. We found that 5 MSRB genes exist in the soybean genome, including GmMSRB1 and two segmentally duplicated gene pairs (GmMSRB2 and GmMSRB5, GmMSRB3 and GmMSRB4). GmMSRB2 and GmMSRB4 proteins showed MSRB activity toward protein-based MetO with either DTT or thioredoxin (TRX) as reductants, whereas GmMSRB1 was active only with DTT. GmMSRB2 had a typical MSRB mechanism with Cys121 and Cys 68 as catalytic and resolving residues, respectively. Surprisingly, this enzyme also possessed the MSRB activity toward free Met-R-O with kinetic parameters similar to those reported for fRMSR from Escherichia coli, an enzyme specific for free Met-R-O. Overexpression of GmMSRB2 or GmMSRB4 in the yeast cytosol supported the growth of the triple MSRA/MSRB/fRMSR (Δ3MSRs) mutant on MetO and protected cells against H2O2-induced stress. Taken together, our data reveal an unexpected diversity of MSRBs in plants and indicate that, in contrast to mammals that cannot reduce free Met-R-O and microorganisms that use fRMSR for this purpose, plants evolved MSRBs for the reduction of both free and protein-based MetO.

UR - http://www.scopus.com/inward/record.url?scp=84878954609&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84878954609&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0065637

DO - 10.1371/journal.pone.0065637

M3 - Article

VL - 8

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 6

M1 - e65637

ER -