Limits...
Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation.

Lázaro JJ, Jiménez A, Camejo D, Iglesias-Baena I, Martí Mdel C, Lázaro-Payo A, Barranco-Medina S, Sevilla F - Front Plant Sci (2013)

Bottom Line: In addition to ROS, there are compelling indications that nitric oxide can be generated in this organelle by both reductive and oxidative pathways.Cumulative results obtained from studies in salt stress models have demonstrated that these redox proteins play a significant role in the establishment of salt tolerance.This review summarizes our current knowledge in antioxidative systems in plant mitochondria, their interrelationships, mechanisms of compensation and some unresolved questions, with special focus on their response to abiotic stress.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Cellular and Molecular Biology of Plants, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas Granada, Spain.

ABSTRACT
Mitochondrial respiration provides the energy needed to drive metabolic and transport processes in cells. Mitochondria are a significant site of reactive oxygen species (ROS) production in plant cells, and redox-system components obey fine regulation mechanisms that are essential in protecting the mitochondrial integrity. In addition to ROS, there are compelling indications that nitric oxide can be generated in this organelle by both reductive and oxidative pathways. ROS and reactive nitrogen species play a key role in signaling but they can also be deleterious via oxidation of macromolecules. The high production of ROS obligates mitochondria to be provided with a set of ROS scavenging mechanisms. The first line of mitochondrial antioxidants is composed of superoxide dismutase and the enzymes of the ascorbate-glutathione cycle, which are not only able to scavenge ROS but also to repair cell damage and possibly serve as redox sensors. The dithiol-disulfide exchanges form independent signaling nodes and act as antioxidant defense mechanisms as well as sensor proteins modulating redox signaling during development and stress adaptation. The presence of thioredoxin (Trx), peroxiredoxin (Prx) and sulfiredoxin (Srx) in the mitochondria has been recently reported. Cumulative results obtained from studies in salt stress models have demonstrated that these redox proteins play a significant role in the establishment of salt tolerance. The Trx/Prx/Srx system may be subjected to a fine regulated mechanism involving post-translational modifications, among which S-glutathionylation and S-nitrosylation seem to exhibit a critical role that is just beginning to be understood. This review summarizes our current knowledge in antioxidative systems in plant mitochondria, their interrelationships, mechanisms of compensation and some unresolved questions, with special focus on their response to abiotic stress.

No MeSH data available.


Related in: MedlinePlus

Catalytic cycle of mitochondrial PrxIIF overoxidation and regeneration by Srx. In physiological conditions mitochondrial PrxIIF is oxidized to its sulfenic form in the reduction of peroxides (step 1). At high concentration of H2O2 PrxIIF may be overoxidized to the inactive sulfinic form (PrxIIF-SO2H; step 2) that is phosphorilated, through a reversible step, in the presence of Srx and ATP (step 3). The phosphoril ester (PrxIIF-SO2-) is converted into sulfinate (PrxIIF-SO-S-Srx) with Srx and Pi is released (step 4). A reducing agent (mitochondrial Trxo) reduces the heterocomplex to release PrxIIF-SOH and Srx-Trxo (step 5). The complex Srx-Trxo is subsequently reduced to Srx-SH by Trxo (step 6). The sulfenic form of PrxIIF is reduced by Trxo that forms the intermolecular complex PrxIIF-Trxo (step 7) and the active PrxIIF-SH is released by another Trxo (step 8) that forms the dimer Trxo-Trxo. The binary complexes between the three proteins in the cycle (sulfinic PrxIIF, Srx and Trxo) are in bold type. (cif. ref. Iglesias-Baena et al., 2011).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3842906&req=5

Figure 4: Catalytic cycle of mitochondrial PrxIIF overoxidation and regeneration by Srx. In physiological conditions mitochondrial PrxIIF is oxidized to its sulfenic form in the reduction of peroxides (step 1). At high concentration of H2O2 PrxIIF may be overoxidized to the inactive sulfinic form (PrxIIF-SO2H; step 2) that is phosphorilated, through a reversible step, in the presence of Srx and ATP (step 3). The phosphoril ester (PrxIIF-SO2-) is converted into sulfinate (PrxIIF-SO-S-Srx) with Srx and Pi is released (step 4). A reducing agent (mitochondrial Trxo) reduces the heterocomplex to release PrxIIF-SOH and Srx-Trxo (step 5). The complex Srx-Trxo is subsequently reduced to Srx-SH by Trxo (step 6). The sulfenic form of PrxIIF is reduced by Trxo that forms the intermolecular complex PrxIIF-Trxo (step 7) and the active PrxIIF-SH is released by another Trxo (step 8) that forms the dimer Trxo-Trxo. The binary complexes between the three proteins in the cycle (sulfinic PrxIIF, Srx and Trxo) are in bold type. (cif. ref. Iglesias-Baena et al., 2011).

Mentions: Under oxidative conditions, Prxs undergo a transient oxidation of their cysteine residues from thiol to sulfenic acid and further stable disulfide bridges, which are regenerated to the thiolic forms by Trxs interaction (Figure 4). Under severe oxidative stress, Prxs rapidly overoxidize to the sulfinic (Cys-SPO2H) and sulfonic (Cys-SpO3H) form, locking the enzyme in a permanent inactive state which was primarily hypothethized to serve as an internal indicator of the hyperoxidative conditions inside the cells. The oxidation of the sulfenic acid to sulfinic acid was thought to be an irreversible step (Yang et al., 2002) until Woo et al. (2003) reported that the sulfinic form, produced under high levels of H2O2, was reduced to the catalytically active thiol form. These seminal observations served to suggest the presence of an enzyme able to retroreduce the overoxidized form of Prxs. These results were further confirmed by studies of different mammalian 2-Cys Prxs (Chevallet et al., 2003), but the identification of the proposed enzyme was carried out by Biteau et al. (2003). They observed how yeast treated with H2O2 induced overexpression of a new protein that they called Srx. Concurrently, deletion of the Srx gene reduced the tolerance of yeast to H2O2. Since its discovery in yeast (Biteau et al., 2003; Vivancos et al., 2005), Srxs have been studied, in mammals (Chang et al., 2004; Woo et al., 2005; Jeong et al., 2006), plants (Liu et al., 2006; Rey et al., 2007; Iglesias-Baena et al., 2010) and cyanobacteria (Pascual et al., 2010; Boileau et al., 2011).


Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation.

Lázaro JJ, Jiménez A, Camejo D, Iglesias-Baena I, Martí Mdel C, Lázaro-Payo A, Barranco-Medina S, Sevilla F - Front Plant Sci (2013)

Catalytic cycle of mitochondrial PrxIIF overoxidation and regeneration by Srx. In physiological conditions mitochondrial PrxIIF is oxidized to its sulfenic form in the reduction of peroxides (step 1). At high concentration of H2O2 PrxIIF may be overoxidized to the inactive sulfinic form (PrxIIF-SO2H; step 2) that is phosphorilated, through a reversible step, in the presence of Srx and ATP (step 3). The phosphoril ester (PrxIIF-SO2-) is converted into sulfinate (PrxIIF-SO-S-Srx) with Srx and Pi is released (step 4). A reducing agent (mitochondrial Trxo) reduces the heterocomplex to release PrxIIF-SOH and Srx-Trxo (step 5). The complex Srx-Trxo is subsequently reduced to Srx-SH by Trxo (step 6). The sulfenic form of PrxIIF is reduced by Trxo that forms the intermolecular complex PrxIIF-Trxo (step 7) and the active PrxIIF-SH is released by another Trxo (step 8) that forms the dimer Trxo-Trxo. The binary complexes between the three proteins in the cycle (sulfinic PrxIIF, Srx and Trxo) are in bold type. (cif. ref. Iglesias-Baena et al., 2011).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3842906&req=5

Figure 4: Catalytic cycle of mitochondrial PrxIIF overoxidation and regeneration by Srx. In physiological conditions mitochondrial PrxIIF is oxidized to its sulfenic form in the reduction of peroxides (step 1). At high concentration of H2O2 PrxIIF may be overoxidized to the inactive sulfinic form (PrxIIF-SO2H; step 2) that is phosphorilated, through a reversible step, in the presence of Srx and ATP (step 3). The phosphoril ester (PrxIIF-SO2-) is converted into sulfinate (PrxIIF-SO-S-Srx) with Srx and Pi is released (step 4). A reducing agent (mitochondrial Trxo) reduces the heterocomplex to release PrxIIF-SOH and Srx-Trxo (step 5). The complex Srx-Trxo is subsequently reduced to Srx-SH by Trxo (step 6). The sulfenic form of PrxIIF is reduced by Trxo that forms the intermolecular complex PrxIIF-Trxo (step 7) and the active PrxIIF-SH is released by another Trxo (step 8) that forms the dimer Trxo-Trxo. The binary complexes between the three proteins in the cycle (sulfinic PrxIIF, Srx and Trxo) are in bold type. (cif. ref. Iglesias-Baena et al., 2011).
Mentions: Under oxidative conditions, Prxs undergo a transient oxidation of their cysteine residues from thiol to sulfenic acid and further stable disulfide bridges, which are regenerated to the thiolic forms by Trxs interaction (Figure 4). Under severe oxidative stress, Prxs rapidly overoxidize to the sulfinic (Cys-SPO2H) and sulfonic (Cys-SpO3H) form, locking the enzyme in a permanent inactive state which was primarily hypothethized to serve as an internal indicator of the hyperoxidative conditions inside the cells. The oxidation of the sulfenic acid to sulfinic acid was thought to be an irreversible step (Yang et al., 2002) until Woo et al. (2003) reported that the sulfinic form, produced under high levels of H2O2, was reduced to the catalytically active thiol form. These seminal observations served to suggest the presence of an enzyme able to retroreduce the overoxidized form of Prxs. These results were further confirmed by studies of different mammalian 2-Cys Prxs (Chevallet et al., 2003), but the identification of the proposed enzyme was carried out by Biteau et al. (2003). They observed how yeast treated with H2O2 induced overexpression of a new protein that they called Srx. Concurrently, deletion of the Srx gene reduced the tolerance of yeast to H2O2. Since its discovery in yeast (Biteau et al., 2003; Vivancos et al., 2005), Srxs have been studied, in mammals (Chang et al., 2004; Woo et al., 2005; Jeong et al., 2006), plants (Liu et al., 2006; Rey et al., 2007; Iglesias-Baena et al., 2010) and cyanobacteria (Pascual et al., 2010; Boileau et al., 2011).

Bottom Line: In addition to ROS, there are compelling indications that nitric oxide can be generated in this organelle by both reductive and oxidative pathways.Cumulative results obtained from studies in salt stress models have demonstrated that these redox proteins play a significant role in the establishment of salt tolerance.This review summarizes our current knowledge in antioxidative systems in plant mitochondria, their interrelationships, mechanisms of compensation and some unresolved questions, with special focus on their response to abiotic stress.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Cellular and Molecular Biology of Plants, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas Granada, Spain.

ABSTRACT
Mitochondrial respiration provides the energy needed to drive metabolic and transport processes in cells. Mitochondria are a significant site of reactive oxygen species (ROS) production in plant cells, and redox-system components obey fine regulation mechanisms that are essential in protecting the mitochondrial integrity. In addition to ROS, there are compelling indications that nitric oxide can be generated in this organelle by both reductive and oxidative pathways. ROS and reactive nitrogen species play a key role in signaling but they can also be deleterious via oxidation of macromolecules. The high production of ROS obligates mitochondria to be provided with a set of ROS scavenging mechanisms. The first line of mitochondrial antioxidants is composed of superoxide dismutase and the enzymes of the ascorbate-glutathione cycle, which are not only able to scavenge ROS but also to repair cell damage and possibly serve as redox sensors. The dithiol-disulfide exchanges form independent signaling nodes and act as antioxidant defense mechanisms as well as sensor proteins modulating redox signaling during development and stress adaptation. The presence of thioredoxin (Trx), peroxiredoxin (Prx) and sulfiredoxin (Srx) in the mitochondria has been recently reported. Cumulative results obtained from studies in salt stress models have demonstrated that these redox proteins play a significant role in the establishment of salt tolerance. The Trx/Prx/Srx system may be subjected to a fine regulated mechanism involving post-translational modifications, among which S-glutathionylation and S-nitrosylation seem to exhibit a critical role that is just beginning to be understood. This review summarizes our current knowledge in antioxidative systems in plant mitochondria, their interrelationships, mechanisms of compensation and some unresolved questions, with special focus on their response to abiotic stress.

No MeSH data available.


Related in: MedlinePlus