Molecular Plant Advance Access published online on November 2, 2008
Molecular Plant, doi:10.1093/mp/ssn067
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Protein-Repairing Methionine Sulfoxide Reductases in Photosynthetic Organisms: Gene Organization, Reduction Mechanisms, and Physiological Roles
CEA, DSV, IBEB, Laboratoire d'Ecophysiologie Moléculaire des Plantes, Bâtiment 161, SBVME, CEA-Cadarache, 13108 Saint-Paul-lez-Durance, Cedex, France
1 To whom correspondence should be addressed. E-mail pascal.rey{at}cea.fr, fax 33 4 42 25 62 65, tel. 33 4 42 25 47 76.
 |
Abstract |
|---|
 TOP Abstract INTRODUCTIONRESULTSDISCUSSIONMETHODSSUPPLEMENTARY DATAFUNDING |
|---|
Methionine oxidation to methionine sulfoxide (MetSO) is reversed by two types of methionine sulfoxide reductases (MSRs), A and B, specific to the S- and R-diastereomers of MetSO, respectively. MSR genes are found in most organisms from bacteria to human. In the current review, we first compare the organization of the MSR gene families in photosynthetic organisms from cyanobacteria to higher plants. The analysis reveals that MSRs constitute complex families in higher plants, bryophytes, and algae compared to cyanobacteria and all non-photosynthetic organisms. We also perform a classification, based on gene number and structure, position of redox-active cysteines and predicted sub-cellular localization. The various catalytic mechanisms and potential physiological electron donors involved in the regeneration of MSR activity are then described. Data available from higher plants reveal that MSRs fulfill an essential physiological function during environmental constraints through a role in protein repair and in protection against oxidative damage. Taking into consideration the expression patterns of MSR genes in plants and the known roles of these genes in non-photosynthetic cells, other functions of MSRs are discussed during specific developmental stages and ageing in photosynthetic organisms.
Key Words: Genome • methionine • methionine sulfoxide reductase • oxidation • photosynthetic organisms • protein repair
Received for publication July 23, 2008. Accepted for publication September 12, 2008.
|
INTRODUCTION |
|---|
|
TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODSSUPPLEMENTARY DATAFUNDING |
|---|
Oxidative modification to amino acids in their lateral chain leads to changes in activity and conformation for many proteins (Davies, 2005). Sulfur-containing residues are the most susceptible to oxidative damage due to their high reactivity with reactive oxygen species (ROS). Cysteines can be engaged in disulfide bridges or oxidized to sulfenic or sulfinic forms, and methionine can be oxidized to methionine sulfoxide (MetSO). However, most of these modifications are reversible through the action of thiol reductases. While oxidized forms of cysteine are reduced by thioredoxins, glutaredoxins, and sulfiredoxin, methionine sulfoxide is reduced back to methionine by methionine sulfoxide reductases (MSRs) through redox-active cysteines (Davies, 2005).
Most organisms possess two types of MSRs, A and B, that display an absolute specificity towards the two S- and R-MetSO diastereoisomers, respectively, but do not share any sequence or structure similarity (Brot et al., 1981; Grimaud et al., 2001; Lowther et al., 2002). Both types are required for maintaining basal levels of MetSO, since oxidation of Met leads to a racemic mixture of isomers. Most MSRAs and MSRBs possess two redox-active cysteines and function generally using a similar three-step catalytic mechanism that involves the formation of a cysteine sulfenic acid intermediate, the subsequent formation of a disulfide bond and, lastly, the regeneration of reduced MSR by a reducing system, generally thioredoxin (Trx) (Boschi-Muller et al., 2000; Lowther et al., 2000; Kumar et al., 2002; Olry et al., 2002; Rouhier et al., 2007). Note some MSRB proteins, present in most organisms, lack the second resolving cysteine and are reduced through a different mechanism (Sagher et al., 2006a, 2006b; Vieira Dos Santos et al., 2007; Kim and Kim, 2008).
MSR proteins fulfill essential functions in stress tolerance and during ageing in bacterial, yeast, and mammal cells. In yeast, deletion and overexpression of MSRA gene result in reduced and increased viability, respectively (Koc et al., 2004). Deletion of MSRB does not noticeably affect yeast life span, but strains deficient for both MSRA and MSRB exhibit a greater reduction in viability compared to MSRA-deficient strains, demonstrating the essential role of the two MSR types. In mammal cells, the abundance of MSRs decreases upon ageing (Petropoulos et al., 2001; Picot et al., 2004) and diseases (Gabbita et al., 1999). Modifying the expression of MSRA genes revealed their participation in the responses to oxidative stress (Moskovitz et al., 1998; Ruan et al., 2002). Very recently, overexpression of human mitochondrial MSRB2 has been reported to protect lymphoblastic leukemia cells from protein damage and to increase cell survival under oxidative stress (Cabreiro et al., 2008). Altogether, these studies demonstrate that MSRs are key components in the control of oxidative damage associated with the development of disorders and the process of ageing.
With regard to photosynthetic organisms, the first report providing evidence for MSR activity was published in the eighties by Sanchez et al. (1983), who found that the activity was mostly localized in chloroplast extracts from various higher plants. The molecular identification and characterization of MSR enzymes have been performed much later, revealing the complexity of MSR gene families in higher plants compared to other organisms (Rouhier et al., 2006). In this review, we analyze the MSR gene families in photosynthetic organisms from cyanobacteria to higher plants by performing a comparison of the number of genes and of their sequence features. Then, we focus on the characteristics and specificities of MSRs in photosynthetic cells with regard to their regeneration mechanisms and physiological functions.
|
RESULTS |
|---|
|
TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODSSUPPLEMENTARY DATAFUNDING |
|---|
Organization of MSR Gene Families in Photosynthetic Organisms and Comparison with Non-Photosynthetic Organisms
We performed a systematic search of MSR genes in the sequenced genome data available, particularly those of photosynthetic organisms for which MSRs were not indexed: Vitis vinifera, Physcomitrella patens, algae, and cyanobacteria. Table 1 shows the number of MSR genes in various living organisms. Compared to mammals, yeast, and E. coli, which possess generally two to four MSR genes, eukaryotic photosynthetic organisms display more complex families. Thus, higher plants, such as Arabidopsis and rice, and the moss Physcomitrella patens possess 14, 6, and 8 MSR genes, respectively, and six to eight MSR genes are present in the genome of the three algae, for which data are available. With regard to the cyanobacterial kingdom, in which the genome of many species has been sequenced, MSR families are much more simple, with generally three genes present in the 20 species that we have analyzed (Table 1 and data not shown). One striking observation arising from Table 1 is the absence of MSR with a catalytic selenocysteine (Sec) instead of a Cys in all photosynthetic organisms, except for one MSRA type in algae. Note that Sec MSRBs are present only in mammals (Table 1).
|
Regarding MSRAs, non-photosynthetic organisms possess only one gene whereas all photosynthetic organisms have at least two genes. The bacterial MSRA gene is present as a whole transcription unit or in an operon fused to the MSRB coding sequence. As shown in Neisseria meningitidis, MSRA can be also included in a trimodular gene coding for Trx, MSRA, and MSRB domains (Ezraty et al., 2005; Wu et al., 2005). It is worth mentioning that, in several eukaryotic non-photosynthetic organisms, the unique MSRA gene is expressed as three distinct transcripts, allowing sub-cellular localization in mitochondrion, nucleus, and cytosol (Kim and Gladyshev, 2006).
In the case of MSRBs, we propose to distinguish two types, the 1-Cys type and the 2-Cys type, which display one or two redox-active cysteines, respectively (Table 1). Similarly to MSRA genes, non-photosynthetic organisms, but also cyanobacteria, possess a reduced number of MSRB genes compared to photosynthetic eukaryotes. Indeed, most prokaryote genomes contain only one MSRB gene (Delaye et al., 2007). Saccharomyces cerevisiae and Drosophila melanogaster possess also one MSRB gene, the fruit fly gene being alternatively spliced allowing addressing the protein to cytosol and mitochondrion (Kim and Gladyshev, 2006). Mammals possess three MSRB genes, one coding for a selenocysteine-containing enzyme (MSRB1) and two for cysteine-containing MSRBs (MSRB2 and MSRB3). N-terminal and C-terminal extensions in MSRB3, resulting from alternative splicing, allow protein repartition in most sub-cellular compartments (Kim and Gladyshev, 2006).
Compared to non-photosynthetic eukaryotes, fewer MSR genes could be processed through alternative splicing in photosynthetic eukaryotes. In these organisms, which display complex MSR gene families, the distribution of MSR isoforms in the various sub-cellular compartments likely originates from products encoded by distinct genes. In animal cells, alternative splicing would allow the production of distinct MSR isoforms and their distribution among cell compartments.
MSRA Gene Families in Photosynthetic Organisms
The model plant, Arabidopsis thaliana, possesses five MSRA genes, with a putative alternative splicing for AtMSRA5 (Table 2). AtMSRA1 to AtMSRA3 are predicted to be located in cytosol, AtMSRA4 is plastidial (Romero et al., 2004), and AtMSRA5.1 and 5.2 could be routed to endoplasmic reticulum or secretory pathway. In other higher plants, the organization of MSRA genes appears somewhat less complex, with only three types represented based on the similarity with Arabidopsis genes. Each type generally possesses a proper predicted sub-cellular localization: cytosol, plastid, or endoplasmic reticulum. Populus trichocarpa possesses five MSRA genes, two pairs of them being closely related: PtMSRA2.1 and PtMSRA2.2, PtMSRA4.1 and PtMSRA4.2, and PtMSRA5. Analysis of Oryza sativa genome reveals the presence of four genes, with one being possibly alternatively spliced (Table 2) and the search in the first release of the Sorghum bicolor genome allowed also four MSRA genes to be found (Supplemental Text File 3). Analyzing the Vitis vinifera genome, we identified three genes, named VvMSRA3, VvMSRA4, and VvMSRA5. The search in Physcomitrella patens genome indicates that the moss possesses five MSRA genes, PpMSRA4.1 and PpMSRA4.2 producing cytosolic proteins, PpMSRA3 and PpMSRA4.3 encoding plastidial enzymes, and PpMSRA5 encoding a predicted mitochondrial product. Since identification of MSRA genes in Chlamydomonas reinhardtii has been previously performed by V. Gladyshev's team (Novoselov et al., 2002; Table 3) and due to the very peculiar characteristics displayed for some of them, we conserved for green algae MSRA genes this nomenclature, which does not correspond to that used above. Note that the identified MSRA genes in Ostreococcus lucimarinus and Ostreococcus tauri genomes were named in step with Chlamydomonas genes. The three green algae possess one cytosolic selenocysteine-containing MSRA protein, named CrMSRA1 (Novoselov et al., 2002), OlMSRA1, and OtMSRA1. C. reinhardtii genome contains four other MSRA genes: CrMSRA2, CrMSRA3, and CrMSRA4 encoding proteins predicted to be mitochondrial, and CrMSRA5, a protein likely plastidial. O. lucimarinus and O. tauri genomes possess two and three other MSRA genes, respectively (Table 3). Note that the predicted sub-cellular localization of green algae's genes should be considered very carefully, the plastidial enzymes being often predicted to be addressed to mitochondrion (Dr S. Lemaire, personal communication).
|
|
All cyanobacteria possess two MSRA genes (Table 4 and data not shown), except Thermosynechococcus elongatus BP-1, which has only one gene, and Chlorobium tepidium TLS, for which the unique MSRA enzyme is encoded as a part of a bimodular protein including also one MSRB domain (data not shown).
|
On the basis of sequence alignment (Supplemental Figure 1), we constructed an unrooted phylogenetic tree that allowed separation of most MSRAs of photosynthetic organisms in six groups (Figure 1). MSRAs from higher plants are distributed in two distinct groups; the first contains cytosolic and plastidic MSRA1 to MSRA4, sharing 53–93% similarity, and the second includes MSRA5 isoforms, for which the overall similarity ranges from 43 to 67%. Proteins of the two groups share only 15–36% similarity. Intron/exon structure is also highly conserved in the genes forming the two groups. Indeed, MSRA1 to MSRA4 genes possess two exons, and MSRA5 genes display four exons, except PpMSRA5, which has no intron (Table 2). PpMSRA4.2, which possess three exons, can be included neither in this group, nor in the closest group to that including most higher plant MSRAs and containing also Chlamydomonas MSRA3 and MSRA4 proteins. The other MSRA proteins of green algae and cyanobacteria constitute three groups. In the first, Ostreococcus MSRA3 and MSRA4 proteins are clustered with one isoform from the cyanobacteria Anabaena sp. PCC 7120, Synechococcus sp. CC9311, and Synechocystis sp. PCC 6803. Proteins of this group share 23–75% overall similarity. Except the second MSRA of Anabaena sp. PCC 7120, other cyanobacteria MSRAs form one group with CrMSRA2, CrMSRA5, and O. tauri and O. lucimarinus MSRA2s, in which global similarity ranges from 21 to 41%. The last group of MSRAs is constituted by selenocysteine-containing proteins, which share 43–68% similarity, and are present only in green algae. Evolutionary analyses suggest an independent loss of selenoproteins in higher plants, cyanobacteria, yeast, and some mammals (Novoselov et al., 2002). The sequence alignment data and the tree presented in Figure 1 show that plastidic and cytosolic MSRAs from higher plants form a homogenous group rather distant from those of cyanobacteria, likely indicating that MSRA genes encoding plastidial isoforms do not have a cyanobacterial origin.
|
MSRB Gene Families in Photosynthetic Organisms
In a previous work, we described the nine genes forming the MSRB family in A. thaliana (Vieira Dos Santos et al., 2005; Table 5). AtMSRB1 displays only one conserved redox active cysteine and thus belongs to the 1-Cys type, whereas all others have two catalytic cysteines and are related to the 2-Cys type. AtMSRB1 and AtMSRB2 encode plastidial isoforms, AtMSRB3, a product routed to endoplasmic reticulum (Kwon et al., 2007), and AtMSRB4 to AtMSRB9, proteins predicted to be cytosolic. So far, Arabidopsis is the plant displaying the highest number of MSRB genes. Indeed, P. trichocarpa possesses four MSRB genes, named PtMSRB1, PtMSRB3.1, PtMSRB3.2, and PtMSRB5 based on the similarity with Arabidopsis genes. O. sativa genome contains three MSRB genes, OsMSRB1, OsMSRB3, and OsMSRB5, OsMSRB1 transcript being probably alternatively spliced. Similarly, three MSRB genes have been identified in the Sorghum bicolor genome, one related to the 1-Cys type and the two others to the 2-Cys type (Supplemental Text File 3). We identified three MSRB genes in Vitis vinifera genome, named VvMSRB1, VvMSRB3.1, and VvMSRB3.2. VvMSRB1 and VvMSRB3.2 are likely routed to plastids whereas VvMSRB3.1 would be cytosolic. The search of homologs in P. patens genome reveals the presence of three genes, PpMSRB1, PpMSRB2.1, and PpMSRB2.2, encoding products related to AtMSRB1 and AtMSRB2, respectively. PpMSRB1 and PpMSRB2.2 are predicted to be localized in plastid whereas PpMSRB2.1 could be cytosolic. In contrast to MSRA genes, the description of MSRB families in green algae has not been carried out previously. Consequently, we propose a nomenclature for C. reinhardtii, O. lucimarinus, and O. tauri, based on the similarity with Arabidopsis MSRB genes and on the presence of one or two redox cysteines. The three green algae's genomes contain two genes homologous to AtMSRB1. O. lucimarinus and O. tauri possess one gene homologous to AtMSRB2, whereas Chlamydomonas possesses two very similar genes, CrMSRB2.1 and CrMSRB2.2.
|
All cyanobacteria, for which the genome sequence is known, contain generally only one 1-Cys MSRB, and sometimes two, except Rhodopseudomonas palustris CGA009, which possesses also one 2-Cys MSRB. Based on protein alignment (Supplemental Figure 2), we constructed a phylogenetic tree (Figure 2) showing that MSRBs of photosynthetic organisms are divided into two main groups, with sequence similarity between the two groups ranging from 18 to 47%. The first contains eukaryotic 2-Cys MSRBs, sharing overall similarity from 36 to 95%, and could be subdivided in two subgroups, containing higher plants 2-Cys MSRBs in the first and green algae 2-Cys MSRBs in the second. Overall similarity ranges from 52 to 95% for higher plants 2-Cys MSRBs and from 45 to 72% for green algae proteins. In the second main group including all 1-Cys MSRBs, MSRB1s from higher plants, moss, and Synechococcus sp. CC9311 MSRB1.2 are clustered and share 47–98% similarity. Three other subgroups could be defined: CrMSRB1, Synechococcus sp. CC9311 MSRB1.2, and Ostreococcus MSRB1.2s in the first, the two cyanobacterial Synechocystis sp. PCC 6803 and Anabaena sp. PCC 7120 MSRB1s in the second, and the two atypical Ostreococcus MSRB1.1s sharing only 8–17% similarity with other MSRBs in the third. Their closest homologue CrMSRB1.2 cannot be clearly attached to a subgroup. To the exclusion of Ostreococcus MSRB1.1s, overall similarity between 1-Cys MSRB1s ranges from 23 to 83%. Genes coding for 2-Cys MSRBs and 1-Cys MSRBs in higher plants are composed of three to four and four to five exons, respectively (Table 5). One extra exon is also found in genes encoding 1-Cys MSRBs of O. lucimarinus and O. tauri. The intron/exon structure and the clear distribution into two groups suggest a distinct origin for the two types of MSRB genes. Since all 1-Cys MSRB genes from higher plants are clustered with those of cyanobacteria and code for plastidic proteins, we propose that this type of MSRBs in photosynthetic eukaryotes arose from a prokaryotic cyanobacterial ancestor, in consideration of the endosymbiotic theory.
|
Catalytic Mechanisms and Electron Donors to MSRs
Despite the absence of similarity between MSRAs and MSRBs, both generally share a common reaction mechanism including three steps (Figure 3A): (1) formation of a sulfenic acid intermediate on the ‘catalytic’ cysteine after reduction of one mole of Met per mole of enzyme; (2) formation of an intramolecular disulfide bond after nucleophilic attack of the ‘resolving’ cysteine; and (3) reduction of the disulfide bridge by a reductant (Lowther et al., 2000; Boschi-Muller et al., 2008). In vitro, dithiothreitol (DTT) is a ubiquitous reducing agent for most MSR enzymes (Brot et al., 1981; Sagher et al., 2006b). Thioredoxin (Trx) appears to be the major physiological reductant for all MSRA and many MSRB enzymes (Figure 4; Brot et al., 1981; Kumar et al., 2002). Accordingly, MSRA and MSRB proteins have been isolated as Trx targets in Chlamydomonas (Lemaire et al., 2004) and in higher plants (Marchand et al., 2004; Rey et al., 2005). Trxs are small and ubiquitous disulfide reductase proteins, present in all organisms, with an active site CGPC. They function as electron donors and play an essential role in many processes in plants, such as regulation of protein activity or control of redox homeostasis, by supplying the reducing power needed to reduce disulfide bonds (Meyer et al., 2005; Vieira Dos Santos and Rey, 2006). Compared to most other living organisms, plants display a great variety of Trx types. Meyer et al. (2005) reported the presence of no less than 40 Trxs or Trx-like genes in A. thaliana genome. This remarkable diversity could indicate a functional specialization or a high level of redundancy.
|
|
MSRAs
MSRA proteins possess one catalytic cysteine required for S-MetSO reduction and one or two recycling cysteines involved in the regeneration mechanism. As shown for E. coli and Bos taurus proteins, two resolving cysteines are involved in the formation of two subsequent disulfide bonds, the first being formed between the catalytic cysteine (CysA) and the first resolving (CysB), the second between the two resolving cysteines (CysB and CysC). Regarding photosynthetic kingdoms, the biochemical characteristics of only poplar cytosolic and plastidial MSRAs have been investigated by Rouhier et al. (2007). The recycling mechanism of PtMSRA2.1 is slightly different from that of the bacterial and mammal enzymes, with the first disulfide bond formed between the most C-terminal cysteine (CysC) and the catalytic one (CysA). All higher plant MSRAs possess the three cysteines equivalent to those of PtMSRA2.1 (Table 2 and Supplemental Figure 1), indicating that they likely follow a similar regeneration mechanism. Note that most enzymes from higher plants related to the MSRA5 type do not display any conserved cysteine, raising the question of their ability to reduce MetSO. With regard to green algae and cyanobacteria, all MSRAs possess a conserved catalytic cysteine, except MSRA1s, which display a selenocysteine at the corresponding position (Tables 3 and 4). Kim et al. (2006) showed that this isoform does not require a resolving cysteine for MetSO reduction and proposed that the selenenic acid intermediate could be directly reduced by thioredoxin (Figure 3B). Chlamydomonas MSRA3, which is the sole green algae isoform possessing the three cysteines conserved in higher plants, likely reduces MetSO via a mechanism similar to that of the poplar enzyme. Interestingly, several MSRAs from green algae and cyanobacteria, such as CrMSRA5 and sll1394, possess resolving cysteines equivalent to those of the Bos taurus enzyme, with the GYC signature for CysB, indicating that these enzymes could use a potential reduction mechanism similar to mammal MSRAs (Tables 3 and 4 and Supplemental Figure 1). At the present time, no investigation has been carried out to analyze the specificity of the various Trx types as electron suppliers to MSRAs in photosynthetic organisms.
MSRBs
The catalytic mechanisms and the regeneration by reductant of 1-Cys and 2-Cys MSRBs implicate one or two cysteines, respectively. Nearly 60% of MSRBs from various organisms possess the two redox-active cysteines and thus belong to the 2-Cys MSRB type (Neiers et al., 2004). The resolving cysteine, corresponding to Cys-63 in E. coli MSRB, is part of the conserved motif GCGWP and is involved in the regeneration of Cys-117, the catalytic cysteine included in the active site RXCXN, through the formation of an intramolecular disulfide bridge followed by Trx reduction (Figure 3A) (Olry et al., 2004; Kim and Gladyshev, 2005; Boschi-Muller et al., 2008). The remaining 40% MSRBs, including two mammalian MSRBs, lack the resolving cysteine, which is generally replaced by a threonine or a serine, and correspond to the 1-Cys MSRB type. Contrasting data have been published concerning the function of Trx in the reduction of this MSRB type. Kim and Gladyshev (2005) and Sagher et al. (2006b) reported that two mammal MSRBs, MSRB2 and MSRB3, are poorly reduced by Trx. However, very recently, Kim and Kim (2008) reported that a specific type of Trx, located in mitochondria like MSRB2 and MSRB3, could efficiently serve as a reductant for the latter. Besides demonstrating the ability of Trxs to reduce all MSRB types, this study points out that MSRs possess specific electron donors even in animal cells where the number of Trxs is much lower than in plant cells. Moreover, Kim and Kim (2008) provided biochemical evidence that Trx could physically interact via an intermolecular disulfide bond with the sulfenic acid form of MSRBs. In other respects, Sagher et al. (2006a, 2006b) reported that thionein, the reduced Cys-rich apoprotein of metallothionein, and selenocompounds such as selenocystamine and selenocystine could reduce mammal 1-Cys type MSRBs. Additional work is needed to determine whether these compounds function in vivo as physiological reductants.
The catalytic mechanisms of plant MSRBs have been recently investigated. Sequence analysis shows that all possess the catalytic Cys. 2-Cys MSRB isoforms have one resolving cysteine (Table 5 and Supplemental Figure 2). Except OtMSRB1.1, all 1-Cys MSRBs of photosynthetic organisms have a threonine in place of the resolving cysteine. In other respects, four non redox-active cysteines, disposed in two CXXC motifs, are conserved in MSRBs from higher plants, moss, green algae, and cyanobacteria, with the exception of CrMSRB1.2, OlMSRB1.1, and OtMSRB1.1. The two motifs are implicated in the fixation of one zinc atom and are critical for the folding and activity of MSRBs (Kumar et al., 2002). Note also that AtMSRB2, AtMSRB6, and two cyanobacterial 2-Cys MSRBs contain an extra-cysteine just before the first CXXC motif, whereas several 1-Cys MSRBs have an extra-cysteine included in this motif. No other cysteine, that could constitute an alternative potential resolving cysteine as shown for Xanthomonas campestris protein (Neiers et al., 2004), is present in 1-Cys MSRBs from photosynthetic organisms.
The plastidic 2-Cys MSRB from Arabidopsis, AtMSRB2, was first shown to be reduced by poplar Trx h1, whereas the activity of AtMSRB1, the other plastidic MSRB belonging to the 1-Cys type, could not be regenerated by this cytosolic Trx (Vieira Dos Santos et al., 2005). Much more relevant information about the identity of electron donors to these MSRBs from a physiological point of view has been gained in the work by Vieira Dos Santos et al. (2007). Simple-module plastidic Trxs f, m, and y are efficient reductants towards AtMSRB2, whereas another chloroplastic Trx, the type x, cannot reduce this MSRB. As AtMSRB2 possesses two redox-active cysteines, these data indicate that the enzyme activity is very likely regenerated through a three-step catalytic mechanism implicating a disulfide exchange with a Trx (Figure 3A), as reported for 2-Cys MSRBs from other organisms (Kumar et al., 2002; Olry et al., 2004). The data obtained on AtMSRB2, revealing a specificity among plastidic Trxs as electron suppliers towards MSRBs, lead us to propose that 2-Cys MSRBs located in other cell compartments also possess specific electron donors among Trxs, which display a tremendous variety in eukaryotic photosynthetic cells. For instance, cytosolic MSRBs might be reduced by specific Trxs h, such as h8 and h5, which are strongly induced by biotic and abiotic stress conditions, leading to an increase in ROS levels (Reichheld et al., 2002; Laloi et al., 2004).
In contrast to AtMSRB2, all simple module Trx types were found to be inefficient to provide electrons to AtMSRB1, the 1-Cys type plastidic enzyme. This enzyme could only be reduced by the peculiar Trx CDSP32 (Chloroplastic Drought-induced Stress Protein of 32 kDa) (Figure 4; Vieira Dos Santos et al., 2007). This strong electron donor specificity was further illustrated using NtMSRB1, the tobacco 1-Cys protein (Ding et al., 2007). Note that MSRB1 was first isolated in potato (Solanum tuberosum) as a target of CDSP32 on an affinity column (Rey et al., 2005), arguing for the physiological relevance of the in-vitro activity results. CDSP32 is composed of two typical thioredoxin modules, with only one active redox disulfide center in the C-terminal domain (Rey et al., 1998; Broin et al., 2002). This protein is induced under severe environmental stress conditions and is involved in the protection of the photosynthetic apparatus against oxidative damage (Broin et al., 2000, 2002; Broin and Rey, 2003). Interestingly, although there is no known mammalian homolog of CDSP32, this double-module Trx can serve as an electron donor to mammal MSRBs lacking the resolving cysteine (Ding et al., 2007). In other respects, glutaredoxins (Grx) have been identified as possible physiological electron donors to the 1-Cys type MSRB (Figure 4; Vieira Dos Santos et al., 2007), in agreement with the fact that many proteins targeted by Trxs also interact with Grxs (Rouhier et al., 2005). Grxs are small and ubiquitous oxidoreductases similar to Trxs, with a typical glutathione-reducible dithiol CXXC or monothiol CXXS active site. Similarly to Trxs, multigenic families encode plant Grxs with no fewer than 31 genes in A. thaliana, but the physiological role remains unknown for most of them. Interestingly, the di- and monothiol Grxs are able to regenerate 1-Cys MSRB activity with comparable catalytic efficiency through mechanisms that remain to be clearly delineated (Vieira Dos Santos et al., 2007).
The recycling mechanism of 1-Cys MSRBs likely implicates the direct reduction by Trxs and Grxs of the sulfenic acid generated upon catalysis and the formation of a transient intermolecular disulfide (Kim and Gladyshev, 2005; Kim and Kim, 2008) that might be reduced via the participation of one resolving cysteine in the electron donor or via glutathione (Figure 3B). However, in the case of Grxs displaying only one redox active cysteine (Vieira Dos Santos et al., 2007), a GSH adduct could be formed on the MSRB catalytic cysteine and subsequently reduced by Grx as proposed for some types of peroxiredoxins (Gama et al., 2008). Further work is needed to elucidate the pathway through which the activity of 1-Cys MSRBs is regenerated and to determine whether Trxs and Grxs share common catalytic mechanisms in this process.
Expression and Functional Analysis of MSR Genes in Photosynthetic Organisms
At the present time, the knowledge about the expression pattern and the function of MSR genes is very scarce in photosynthetic organisms other than higher plants, not to say completely non-existent in the case of cyanobacteria and mosses. In the model alga Chlamydomonas reinhardtii, no functional analysis of MSRs based on a genetic approach has been still reported. CrMSRA2 gene expression is triggered in Chlamydomonas when subjected to manganese deficiency (Allen et al., 2007). Note that this deficiency leads also to increased expression of genes encoding for glutathione and ascorbate peroxidases, and is associated with susceptibility to organic peroxides. The authors proposed that CrMSRA2 participates with other antioxidant genes in response to the oxidative stress resulting from manganese deficiency. As mentioned above, algae are the only photosynthetic organisms possessing selenocysteine-containing MSRA proteins (Novoselov et al., 2002). The presence of a catalytic selenocysteine instead of a cysteine in CrMSRA1 confers a much higher efficiency for reducing MetSO (Kim et al., 2006) and selenium has been found to be required for optimal growth of algae (Novoselov et al., 2002). Chlamydomonas possesses other antioxidant enzymes (glutathione peroxidase and thioredoxin-reductase) with the catalytic cysteine replaced by a selenocysteine. However, no difference in sensitivity to MetSO and H2O2 was observed in algae cultures grown either in the presence or in the absence of selenium. In Chlamydomonas, Lemaire et al. (2004) identified one MSRA (CrMSRA4) among proteins targeted by thioredoxin, which is known to fulfill a major role in the response to oxidative stress in most organisms (Arner and Holmgren, 2000; Vieira Dos Santos and Rey, 2006). This last finding and the few reports about the expression of MSR genes in algae give credence for the involvement of these genes in the tolerance of unicellular algae to oxidative stress conditions. But, thorough investigations particularly using genetic approaches have to be performed to firmly assess this function.
In higher plants, the expression patterns and roles of MSR proteins are comparatively more documented, although much remains to be done, particularly to analyze the physiological functions of each isoform. In a previous review, we reported the detailed expression patterns of MSRA and MSRB genes in the plant model Arabidopsis thaliana (Rouhier et al., 2006). We present here only a sum-up of the main expression features of these genes. Most Arabidopsis MSR genes display differential expression patterns, depending on organ type. Thus, on the basis of transcript levels, AtMSRA4, AtMSRB1, AtMSRB2, and AtMSRB6 genes are preferentially expressed in leaves and in other green organs, whereas AtMSRA2, AtMSRB5, AtMSRB7, AtMSRB8, and AtMSRB9 are more specifically expressed in roots. Many data also demonstrate that environmental and biotic stress conditions substantially modify the expression of MSR genes in higher plants. In Arabidopsis, AtMSRA4 expression is enhanced by oxidative treatments, high light and salt treatment (Romero et al., 2004; Oh et al., 2005; Vieira Dos Santos et al., 2005). In poplar, the abundance of plastidic PtMSRA is higher in the case of an incompatible reaction with the rust fungus Melanpsora larici-populina (Vieira Dos Santos et al., 2005), and, in rye, the abundance of a cytosolic MSRA protein increases during acclimation to low temperature (In et al., 2005). With regard to MSRB genes, AtMSRB3 is induced at the transcriptional level by low temperature in Arabidopsis (Kwon et al., 2007) and Arabidopsis plants subjected to photooxidative stress conditions generated by high light and low temperature exhibit noticeably higher levels of plastidic AtMSRB1 and AtMSRB2 proteins (Vieira Dos Santos et al., 2005).
Few studies investigated the level of MSR activity during environmental stress conditions. Ferguson and Burke (1994) noticed up- and down-variations, depending on species (cotton, pea, wheat, potato) in plants subjected to high temperature or water deficit. In Arabidopsis, a severe decrease in the total cellular MSR activity occurs during cold and high salt treatments (Oh et al., 2005). However, these authors noticed that AtMSRA4 is induced by high salt, but not by low temperature. In contrast, Romero et al. (2004) observed correlated increases in the abundance of plastidic AtMSRA4 and in the total MSR activity measured in leaf soluble fractions during environmental and oxidative stress conditions. Altogether, these data indicate that environmental stress exerts a strong control in the regulation of the activity of MSR proteins, and that this control is very likely achieved through distinct steps at the transcriptional and post-transcriptional levels. Further, each MSR gene very likely displays its own and highly specific pattern of expression and activity. This hypothesis is supported by the findings of Bechtold et al. (2004), who observed two peaks in total MSR activity in Arabidopsis plants grown under short-day conditions, one during the light period and the other in the dark. The second peak of activity was partially attributed to AtMSRA2, since it substantially diminished in a mutant lacking this protein.
Insights about the functional roles of plant MSRs have been gained in the past years using Arabidopsis mutants and transformants. Lower total MSR activities have been recorded in Arabidopsis plants lacking AtMSRB9 (Rodrigo et al., 2002) or AtMSRA2 (Bechtold et al., 2004), or underexpressing AtMSRA4 (Romero et al., 2004). Conversely, the MSR activity measured in chloroplast extracts strongly increased in plants overexpressing AtMSRA4 (Romero et al., 2004). In agreement with activity data, a higher MetSO content has been observed in plants with reduced expression levels of AtMSRB9, AtMSRB3, or AtMSRA4 genes, particularly under environmental constraints, and the MetSO content was lower in plants overexpressing AtMSRA4 (Rodrigo et al., 2002; Bechtold et al., 2004; Romero et al., 2004).
Physiological functions have been attributed to some MSR genes in higher plants on the basis of genetic approaches. Bechtold et al. (2004) reported that Arabidopsis mutants deficient for AtMSRA2 display reduced growth and slow development under short-day conditions, but not under long-day conditions. They proposed that cytosolic AtMSRA2 repairs oxidized proteins under long night periods to limit the loss of energy resulting from an increased rate of protein turnover. As abiotic constraints result in substantial changes in the expression of MSR genes, investigations have been performed to characterize the phenotype and the tolerance of plants under- or overexpressing MSR genes under such conditions. Compared to wild-type, plants overexpressing AtMSRA4 display a greater tolerance to severe photooxidative treatments generating damage within photosynthetic membranes such as high light and methyl viologen treatment (Romero et al., 2004). Conversely, Arabidopsis plants underexpressing AtMSRA4 are more sensitive to these treatments. From these data, plastidic MSRA has been proposed to play an essential function in the tolerance and protection of photosynthetic structures (Romero et al., 2004). The enzyme likely prevents oxidative damage to proteins due to the increased level of reactive oxygen species in chloroplast, a major site of production of these deleterious species in plant cells during environmental constraints (Foyer and Noctor, 2003). Very recently, Kwon et al. (2007) reported that the AtMSRB3 gene, encoding a protein localized in the endoplasmic reticulum, is cold responsive. They showed that plants lacking AtMSRB3 are more sensitive to a methyl viologen treatment and lose their ability to tolerate freezing temperatures following a pre-treatment to cold conditions. This report reveals a critical role of MSRs in the process of cold acclimation in plants. Taken together, the studies on Arabidopsis mutants demonstrate that plant MSRs constitute key actors in the responses of plants to various environmental constraints, very likely through a role in the repair of oxidatively damaged proteins.
|
DISCUSSION |
|---|
|
TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODSSUPPLEMENTARY DATAFUNDING |
|---|
Over the past few years, substantial information about the characteristics and roles of MSRs has been gained in higher plants, more particularly during environmental constraints. However, we are far from having a full understanding of the function of each isoform in these eukaryotic organisms upon abiotic and biotic stress conditions. Further, MSRs very likely play other key roles, such as in plant development. Indeed, some MSR genes are highly expressed during specific developmental stages, such as AtMSRA3 in stamen and pollen (Rouhier et al., 2006) or a MSRA1-related gene during maturation of strawberry fruit (Lopez et al., 2006). Regarding other photosynthetic organisms, the knowledge at the present time is very poor, no report being available, for instance, regarding the characterization of MSR genes in cyanobacteria. On the basis of the data reported in higher plants and non-photosynthetic organisms, MSRs very likely participate in the tolerance of unicellular photosynthetic organisms to environmental constraints generating oxidative damage. In other respects, the critical function of MSRs during ageing and in the control of life span has been extensively documented in yeast, insect, and mammal cells, as mentioned in the Introduction of this review. This is in agreement with the accumulation of oxidative damage in proteins, like carbonyl groups or methionine sulfoxide, observed over time in many organisms (Stadtman, 1992). In contrast, nothing is known about the role of MSRs during the ageing process in plants. In these organisms, leaf senescence is the ultimate stage of leaf development and precedes plant death. An increase in the abundance of carbonylated proteins first occurs during Arabidopsis leaf expansion, and then is followed by a strong decrease prior to bolting and during flower development (Johansson et al., 2004). Further, in Arabidopsis, high levels of carbonylated proteins are also observed during seed maturation and germination (Job et al., 2005). Clearly, these data show that the accumulation of carbonylated proteins in plants is not a marker of the ageing process, but is associated with specific stages of development. At the present time, no report describing the level of MetSO in the various plant organs and during the different developmental stages has been published. We previously reported a higher abundance of plastidial MSRs, particularly MSRBs, in young leaves compared to well expanded leaves during vegetative growth of Arabidopsis (Vieira Dos Santos et al., 2005), suggesting a decrease in MSR activity with age in leaves of higher plants. Thorough investigations have to be carried out to determine whether the amount of MetSO in proteins is positively correlated with the level of carbonyl groups during specific developmental stages in plants and the precise roles of MSRs during senescence in photosynthetic organisms.
The understanding of the physiological functions of MSRs in photosynthetic organisms will undoubtedly progress via the determination of the identity of their partners and substrates, which remain largely unknown. Most MSRAs and MSRBs are more efficient reducers for peptide-bound MetSO than for free MetSO (Olry et al., 2002, 2004; Vieira Dos Santos et al., 2005). Consequently, these reductases should be able to reduce all the proteins exhibiting methionine residues positioned on their surface, taking into consideration MetSO accessibility to the active sites of both MSR types (Boschi-Muller et al., 2008). Based on the consequences of Met oxidation in proteins, Oien and Moskowitz (2008) very recently classified MSR substrates into three groups:
- (1) One group in which Met oxidation is used as a switch to regulate signaling pathways. Thus, sulfoxidation of Met modulates in mammal cells the activities of calmodulin and of calmodulin-dependent protein kinase II, thus linking metabolic activity to cell redox state (Gao et al., 1998; Bigelow and Squier, 2005; Erickson et al., 2008).
- (2) The second group includes proteins termed scavenging substrates, which do not exhibit a substantial decrease in their activity when their methionines are oxidized. MSR proteins constitute good candidates to play a direct antioxidant role, since cyclic oxidation and reduction of Met could serve as an efficient pathway to scavenge ROS in cells (Stadtman et al., 2002; Weissbach et al., 2002).
- (3) The last group corresponds to substrates damaged in their function by Met oxidation, such as catalase that has been identified as a target of MSR in Helicobacter pylori (Alamuri and Maier, 2006).
- (2) The second group includes proteins termed scavenging substrates, which do not exhibit a substantial decrease in their activity when their methionines are oxidized. MSR proteins constitute good candidates to play a direct antioxidant role, since cyclic oxidation and reduction of Met could serve as an efficient pathway to scavenge ROS in cells (Stadtman et al., 2002; Weissbach et al., 2002).
|
METHODS |
|---|
|
TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODSSUPPLEMENTARY DATAFUNDING |
|---|
Gene sequences were obtained from TAIR (www.arabidopsis.org/) for Arabidopsis thaliana, JGI (http://genome.jgi-psf.org/Poptr1_1/Poptr1_1.home.html) for Populus trichocarpa, TIGR (www.tigr.org/tdb/e2k1/osa1/) for Oryza sativa, JGI (http://genome.jgi-psf.org/Sorbi1/Sorbi1.home.html) for Sorghum bicolor, JGI (http://genome.jgi-psf.org/Phypa1_1/Phypa1_1.home.html) for Physcomitrella patens ssp. patens, Genoscope (www.genoscope.cns.fr/externe/GenomeBrowser/Vitis/) for Vitis vinifera, JGI (http://genome.jgi-psf.org/Chlre3/Chlre3.home.html) for Chlamydomonas reinhardtii, JGI (http://genome.jgi-psf.org/Ost9901_3/Ost9901_3.home.html) for Ostreococcus lucimarinus, JGI (http://genome.jgi-psf.org/Ostta4/Ostta4.home.html) for Ostreococcus tauri, and CyanoBase (http://bacteria.kazusa.or.jp/cyanobase/) for cyanobacteria. The predicted sub-cellular localization of eukaryote proteins was the consensus obtained using TargetP (Emanuelsson et al., 2000; www.cbs.dtu.dk/services/TargetP/) and Predotar (Small et al., 2004; http://urgi.versailles.inra.fr/predotar/predotar.html). Phylogenetic trees, based on protein alignments made using ClustalW (Larkin et al., 2007), were built thanks to MEGA4 (Tamura et al., 2007), using the neighbor-joining method (Saitou and Nei, 1987) and the Poisson correction method (Zukerkandl and Pauling, 1965) to compute evolutionary distances. Supplemental Text File 3 contains all protein sequences indexed in this study including Sorghum bicolor gene accession numbers.
|
SUPPLEMENTARY DATA |
|---|
|
TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODSSUPPLEMENTARY DATAFUNDING |
|---|
Supplementary Data are available at Molecular Plant Online.
|
FUNDING |
|---|
|
TOPAbstractINTRODUCTIONRESULTSDISCUSSIONMETHODSSUPPLEMENTARY DATAFUNDING |
|---|
This work was supported by Région Provence-Alpes-Côtes-d'Azur to L.T. and by Agence Nationale de la Recherche (ANR-Génoplante, Grant GNP05010G) to E.L. No conflict of interest declared.
-
Alamuri P, Maier RJ. Methionine sulfoxide reductase in Helicobacter pylori: interaction with methionine-rich proteins and stress-induced expression. J. Bacteriol. (2006) 188:5839–5850.
Allen MD, Kropat J, Tottey S, Del Campo JA, Merchant SS. Manganese deficiency in Chlamydomonas results in loss of photosystem II and MnSOD function, sensitivity to peroxides, and secondary phosphorus and iron deficiency. Plant Physiol. (2007) 143:263–277.
Arner ES, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. (2000) 267:6102–6109.[Web of Science][Medline]
Bechtold U, Murphy DJ, Mullineaux PM. Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. Plant Cell. (2004) 16:908–919.
Bigelow DJ, Squier TC. Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim. Biophys. Acta. (2005) 1703:121–134.[Medline]
Boschi-Muller S, Azza S, Sanglier-Cianferani S, Talfournier F, Van Dorsselear A, Branlant G. A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coli. J. Biol. Chem. (2000) 275:35908–35913.
Boschi-Muller S, Gand A, Branlant G. The methionine sulfoxide reductases: catalysis and substrate specificities. Arch. Biochem. Biophys. (2008) 474:266–273.[CrossRef][Web of Science]
Brock JW, Cotham WC, Ames JM, Thorpe SR, Baynes JW. Proteomic method for the quantification of methionine sulfoxide. Ann. N Y Acad. Sci. (2005) 1043:284–289.[CrossRef][Web of Science][Medline]
Broin M, Rey P. Potato plants lacking the CDSP32 plastidic thioredoxin exhibit overoxidation of the BAS1 2-cysteine peroxiredoxin and increased lipid Peroxidation in thylakoids under photooxidative stress. Plant Physiol. (2003) 132:1335–1343.
Broin M, Cuine S, Eymery F, Rey P. The plastidic 2-cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. Plant Cell. (2002) 14:1417–1432.
Broin M, Cuine S, Peltier G, Rey P. Involvement of CDSP 32, a drought-induced thioredoxin, in the response to oxidative stress in potato plants. FEBS Lett. (2000) 467:245–248.[CrossRef][Web of Science][Medline]
Brot N, Weissbach L, Werth J, Weissbach H. Enzymatic reduction of protein-bound methionine sulfoxide. Proc. Natl Acad. Sci. U S A (1981) 78:2155–2158.
Cabreiro F, Picot CR, Perichon M, Castel J, Friguet B, Petropoulos I. Overexpression of mitochondrial methionine sulfoxide reductase B2 protects leukemia cells from oxidative stress-induced cell death and protein damage. J. Biol. Chem. (2008) 283:16673–16681.
Davies MJ. The oxidative environment and protein damage. Biochim. Biophys. Acta. (2005) 1703:93–109.
Delaye L, Becerra A, Orgel L, Lazcano A. Molecular evolution of peptide methionine sulfoxide reductases (MsrA and MsrB): on the early development of a mechanism that protects against oxidative damage. J. Mol. Evol. (2007) 64:15–32.[CrossRef][Web of Science][Medline]
Ding D, Sagher D, Laugier E, Rey P, Weissbach H, Zhang XH. Studies on the reducing systems for plant and animal thioredoxin-independent methionine sulfoxide reductases B. Biochem. Biophys. Res. Commun. (2007) 361:629–633.[CrossRef][Web of Science][Medline]
Emanuelsson O, Nielsen H, Brunak S, von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. (2000) 300:1005–1016.[CrossRef][Web of Science][Medline]
Erickson JR, et al. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell. (2008) 133:462–474.[CrossRef][Web of Science][Medline]
Ezraty B, Aussel L, Barras F. Methionine sulfoxide reductases in prokaryotes. Biochim. Biophys. Acta. (2005) 1703:221–229.
Ferguson DL, Burke JJ. Methionyl sulfoxide content and protein-methionine-S-oxide reductase activity in response to water deficits or high temperature. Physiol. Plant. (1994) 90:253–258.[CrossRef]
Foyer CH, Noctor G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant. (2003) 119:355–364.[CrossRef]
Gabbita SP, Aksenov MY, Lovell MA, Markesbery WR. Decrease in peptide methionine sulfoxide reductase in Alzheimer's disease brain. J. Neurochem. (1999) 73:1660–1666.[CrossRef][Web of Science][Medline]
Gama F, Brehelin C, Gelhaye E, Meyer Y, Jacquot JP, Rey P, Rouhier N. Functional analysis and expression characteristics of chloroplastic Prx IIE. Physiol. Plant. (2008) 131:599–610.
Gao J, Yin DH, Yao Y, Sun H, Qin Z, Schoneich C, Williams TD, Squier TC. Loss of conformational stability in calmodulin upon methionine oxidation. Biophys. J. (1998) 74:1115–1134.[Web of Science][Medline]
Grimaud R, Ezraty B, Mitchell JK, Lafitte D, Briand C, Derrick PJ, Barras F. Repair of oxidized proteins. Identification of a new methionine sulfoxide reductase. J. Biol. Chem. (2001) 276:48915–48920.
Gustavsson N, Kokke B, Härndahl U, Silow M, Bechtold U, Poghosyan Z, Murphy D, Boelens W, Sundby C. A peptide methionine sulfoxide reductase highly expressed in photosynthetic tissue in Arabidopsis thaliana can protect the chaperone-like activity of a chloroplast-localized small heat shock protein. Plant J. (2002) 29:545–553.[CrossRef][Web of Science][Medline]
In O, Berberich T, Romdhane S, Feierabend J. Changes in gene expression during dehardening of cold-hardened winter rye (Secale cereale L.) leaves and potential role of a peptide methionine sulfoxide reductase in cold-acclimation. Planta. (2005) 220:941–950.[CrossRef][Web of Science][Medline]
Job C, Rajjou L, Lovigny Y, Belghazi M, Job D. Patterns of protein oxidation in Arabidopsis seeds and during germination. Plant Physiol. (2005) 138:790–802.
Johansson E, Olsson O, Nystrom T. Progression and specificity of protein oxidation in the life cycle of Arabidopsis thaliana. J. Biol. Chem. (2004) 279:22204–22208.
Kim HY, Gladyshev VN. Different catalytic mechanisms in mammalian selenocysteine- and cysteine-containing methionine-R-sulfoxide reductases. PLoS Biol. (2005) 3:e375.[CrossRef][Medline]
Kim HY, Gladyshev VN. Alternative first exon splicing regulates subcellular distribution of methionine sulfoxide reductases. BMC Mol. Biol. (2006) 7:11.[CrossRef][Medline]
Kim HY, Kim JR. Thioredoxin as a reducing agent for mammalian methionine sulfoxide reductases B lacking resolving cysteine. Biochem. Biophys. Res. Commun. (2008) 371:490–494.[CrossRef][Web of Science][Medline]
Kim HY, Fomenko DE, Yoon YE, Gladyshev VN. Catalytic advantages provided by selenocysteine in methionine-S-sulfoxide reductases. Biochemistry (2006) 45:13697–13704.[CrossRef][Web of Science][Medline]
Koc A, Gasch AP, Rutherford JC, Kim HY, Gladyshev VN. Methionine sulfoxide reductase regulation of yeast lifespan reveals reactive oxygen species-dependent and -independent components of aging. Proc. Natl Acad. Sci. U S A (2004) 101:7999–8004.
Kumar RA, Koc A, Cerny RL, Gladyshev VN. Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-R-sulfoxide reductase. J. Biol. Chem. (2002) 277:37527–37535.
Kwon SJ, Kwon SI, Bae MS, Cho EJ, Park OK. Role of the methionine sulfoxide reductase MsrB3 in cold acclimation in Arabidopsis. Plant Cell Physiol. (2007) 48:1713–1723.
Laloi C, Mestres-Ortega D, Marco Y, Meyer Y, Reichheld JP. The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor. Plant Physiol. (2004) 134:1006–1016.
Larkin MA, et al. ClustalW and ClustalX version 2. Bioinformatics (2007) 23:2947–2948.
Lemaire SD, Guillon B, Le Marechal P, Keryer E, Miginiac-Maslow M, Decottignies P. New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. U S A (2004) 101:7475–7480.
Lopez A, Portales R, López-Ráez J, Medina-Escobar N, Blanco J, Franco A. Characterization of a strawberry late-expressed and fruit-specific peptide methionine sulphoxide reductase. Physiol. Plant. (2006) 126:129–139.[CrossRef]
Lowther WT, Brot N, Weissbach H, Honek JF, Matthews BW. Thiol-disulfide exchange is involved in the catalytic mechanism of peptide methionine sulfoxide reductase. Proc. Natl Acad. Sci. U S A (2000) 97:6463–6468.
Lowther WT, Weissbach H, Etienne F, Brot N, Matthews BW. The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat. Struct. Biol. (2002) 9:348–352.[Web of Science][Medline]
Marchand C, Le Marechal P, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P. New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics (2004) 4:2696–2706.[CrossRef][Web of Science][Medline]
Meyer Y, Reichheld JP, Vignols F. Thioredoxins in Arabidopsis and other plants. Photosynth. Res. (2005) 86:419–433.[CrossRef][Web of Science][Medline]
Moskovitz J, Flescher E, Berlett BS, Azare J, Poston JM, Stadtman ER. Overexpression of peptide-methionine sulfoxide reductase in Saccharomyces cerevisiae and human T cells provides them with high resistance to oxidative stress. Proc. Natl Acad. Sci. U S A (1998) 95:14071–14075.
Neiers F, Kriznik A, Boschi-Muller S, Branlant G. Evidence for a new sub-class of methionine sulfoxide reductases B with an alternative thioredoxin recognition signature. J. Biol. Chem. (2004) 279:42462–42468.
Novoselov SV, Rao M, Onoshko NV, Zhi H, Kryukov GV, Xiang Y, Weeks DP, Hatfield DL, Gladyshev VN. Selenoproteins and selenocysteine insertion system in the model plant cell system, Chlamydomonas reinhardtii. EMBO J. (2002) 21:3681–3693.[CrossRef][Web of Science][Medline]
Oh JE, et al. Modulation of gene expressions and enzyme activities of methionine sulfoxide reductases by cold, ABA or high salt treatments in Arabidopsis. Plant Sci. (2005) 169:1030–1036.[CrossRef][Web of Science]
Oien DB, Moskovitz J. Substrates of the methionine sulfoxide reductase system and their physiological relevance. Curr. Top. Develop. Biol. (2008) 80:93–133.
Olry A, Boschi-Muller S, Branlant G. Kinetic characterization of the catalytic mechanism of methionine sulfoxide reductase B from Neisseria meningitidis. Biochemistry (2004) 43:11616–11622.[CrossRef][Web of Science][Medline]
Olry A, Boschi-Muller S, Marraud M, Sanglier-Cianferani S, Van Dorsselear A, Branlant G. Characterization of the methionine sulfoxide reductase activities of PILB, a probable virulence factor from Neisseria meningitidis. J. Biol. Chem. (2002) 277:12016–12022.
Petropoulos I, Mary J, Perichon M, Friguet B. Rat peptide methionine sulphoxide reductase: cloning of the cDNA, and down-regulation of gene expression and enzyme activity during aging. Biochem. J. (2001) 355:819–825.[CrossRef][Web of Science][Medline]
Picot CR, Perichon M, Cintrat JC, Friguet B, Petropoulos I. The peptide methionine sulfoxide reductases, MsrA and MsrB (hCBS-1), are downregulated during replicative senescence of human WI-38 fibroblasts. FEBS Lett. (2004) 558:74–78.[CrossRef][Web of Science][Medline]
Reichheld JP, Mestres-Ortega D, Laloi C, Meyer Y. The multigenic family of thioredoxin h in Arabidopsis thaliana: specific expression and stress response. Plant Physiol. Biochem. (2002) 40:685–690.
Rey P, Cuine S, Eymery F, Garin J, Court M, Jacquot JP, Rouhier N, Broin M. Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J. (2005) 41:31–42.[CrossRef][Web of Science][Medline]
Rey P, Pruvot G, Becuwe N, Eymery F, Rumeau D, Peltier G. A novel thioredoxin-like protein located in the chloroplast is induced by water deficit in Solanum tuberosum L. plants. Plant J. (1998) 13:97–107.[CrossRef][Web of Science][Medline]
Rodrigo MJ, Moskovitz J, Salamini F, Bartels D. Reverse genetic approaches in plants and yeast suggest a role for novel, evolutionarily conserved, selenoprotein-related genes in oxidative stress defense. Mol. Genet. Genomics. (2002) 267:613–621.[CrossRef][Web of Science][Medline]
Romero HM, Berlett BS, Jensen PJ, Pell EJ, Tien M. Investigations into the role of the plastidial peptide methionine sulfoxide reductase in response to oxidative stress in Arabidopsis. Plant Physiol. (2004) 136:3784–3794.
Rouhier N, et al. Identification of plant glutaredoxin targets. Antioxid. Redox Signal (2005) 7:919–929.[CrossRef]
Rouhier N, Kauffmann B, Tete-Favier F, Palladino P, Gans P, Branlant G, Jacquot JP, Boschi-Muller S. Functional and structural aspects of poplar cytosolic and plastidial type a methionine sulfoxide reductases. J. Biol. Chem. (2007) 282:3367–3378.
Rouhier N, Vieira Dos Santos C, Tarrago L, Rey P. Plant methionine sulfoxide reductase A and B multigenic families. Photosynth. Res. (2006) 89:247–262.[CrossRef][Web of Science][Medline]
Ruan H, et al. High-quality life extension by the enzyme peptide methionine sulfoxide reductase. Proc. Natl Acad. Sci. U S A (2002) 99:2748–2753.
Sagher D, Brunell D, Brot N, Vallee BL, Weissbach H. Selenocompounds can serve as oxidoreductants with the methionine sulfoxide reductase enzymes. J. Biol. Chem. (2006a) 281:31184–31187.
Sagher D, Brunell D, Hejtmancik JF, Kantorow M, Brot N, Weissbach H. Thionein can serve as a reducing agent for the methionine sulfoxide reductases. Proc. Natl Acad. Sci. U S A (2006b) 103:8656–8661.
Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. (1987) 4:406–425.[Abstract]
Sanchez J, Nikolau BJ, Stumpf PK. Reduction of N-acetyl methionine sulfoxide in plants. Plant Physiol. (1983) 73:619–623.
Small I, Peeters N, Legeai F, Lurin C. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics (2004) 4:1581–1590.[CrossRef][Web of Science][Medline]
Stadtman ER. Protein oxidation and aging. Science (1992) 257:1220–1224.
Stadtman ER, Moskovitz J, Berlett BS, Levine RL. Cyclic oxidation and reduction of protein methionine residues is an important antioxidant mechanism. Mol. Cell Biochem. (2002) 234–235:3–9.
Sundby C, Harndahl U, Gustavsson N, Ahrman E, Murphy DJ. Conserved methionines in chloroplasts. Biochim. Biophys. Acta. (2005) 1703:191–202.
Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. (2007) 24:1596–1599.
Toda T, Morisama T, Kobayashi S, Nomura K, Hatozaki S, Hirota M. A proteomic approach to determination of the significance of protein oxidation in the ageing of mouse hippocampus. Appl. Genomics Proteomics (2003) 2:43–50.
Vieira Dos Santos C, Rey P. Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci. (2006) 11:329–334.[CrossRef][Web of Science][Medline]
Vieira Dos Santos C, Cuine S, Rouhier N, Rey P. The Arabidopsis plastidic methionine sulfoxide reductase B proteins. Sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A, and induction by photooxidative stress. Plant Physiol. (2005) 138:909–922.
Vieira Dos Santos C, Laugier E, Tarrago L, Massot V, Issakidis-Bourguet E, Rouhier N, Rey P. Specificity of thioredoxins and glutaredoxins as electron donors to two distinct classes of Arabidopsis plastidial methionine sulfoxide reductases B. FEBS Lett. (2007) 581:4371–4376.[CrossRef][Web of Science][Medline]
Weissbach H, Etienne F, Hoshi T, Heinemann SH, Lowther WT, Matthews B, St John G, Nathan C, Brot N. Peptide methionine sulfoxide reductase: structure, mechanism of action, and biological function. Arch. Biochem. Biophys. (2002) 397:172–178.[CrossRef][Web of Science][Medline]
Wu J, Neiers F, Boschi-Muller S, Branlant G. The N-terminal domain of PILB from Neisseria meningitidis is a disulfide reductase that can recycle methionine sulfoxide reductases. J. Biol. Chem. (2005) 280:12344–12350.
Zukerkandl E, Pauling L. Evolution divergence and convergence in proteins. In: Evolving Genes and Proteins—Bryson V, Vogel HJ, eds. (1965) New York: Academic Press. 97–166.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  L. Tarrago, E. Laugier, M. Zaffagnini, C. Marchand, P. Le Marechal, N. Rouhier, S. D. Lemaire, and P. Rey Regeneration Mechanisms of Arabidopsis thaliana Methionine Sulfoxide Reductases B by Glutaredoxins and Thioredoxins J. Biol. Chem., July 10, 2009; 284(28): 18963 - 18971. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||