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Modulation of Potassium Channel Activity in the Balance of ROS and ATP Production by Durum Wheat Mitochondria-An Amazing Defense Tool Against Hyperosmotic Stress.

Trono D, Laus MN, Soccio M, Alfarano M, Pastore D - Front Plant Sci (2015)

Bottom Line: PmitoKATP is inhibited by ATP and activated by superoxide anion, as well as by free fatty acids (FFAs) and acyl-CoAs.Fully open channel is able to lower superoxide anion up to 35-fold compared to a condition of ATP-inhibited channel.In particular, under moderate hyperosmotic stress (mannitol or NaCl), PmitoKATP was found to be activated by ROS, so inhibiting further large-scale ROS production according to a feedback mechanism; moreover, a stress-activated phospholipase A2 may generate FFAs, further activating the channel.

View Article: PubMed Central - PubMed

Affiliation: Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per la Cerealicoltura , Foggia, Italy.

ABSTRACT
In plants, the existence of a mitochondrial potassium channel was firstly demonstrated about 15 years ago in durum wheat as an ATP-dependent potassium channel (PmitoKATP). Since then, both properties of the original PmitoKATP and occurrence of different mitochondrial potassium channels in a number of plant species (monocotyledonous and dicotyledonous) and tissues/organs (etiolated and green) have been shown. Here, an overview of the current knowledge is reported; in particular, the issue of PmitoKATP physiological modulation is addressed. Similarities and differences with other potassium channels, as well as possible cross-regulation with other mitochondrial proteins (Plant Uncoupling Protein, Alternative Oxidase, Plant Inner Membrane Anion Channel) are also described. PmitoKATP is inhibited by ATP and activated by superoxide anion, as well as by free fatty acids (FFAs) and acyl-CoAs. Interestingly, channel activation increases electrophoretic potassium uptake across the inner membrane toward the matrix, so collapsing membrane potential (ΔΨ), the main component of the protonmotive force (Δp) in plant mitochondria; moreover, cooperation between PmitoKATP and the K(+)/H(+) antiporter allows a potassium cycle able to dissipate also ΔpH. Interestingly, ΔΨ collapse matches with an active control of mitochondrial reactive oxygen species (ROS) production. Fully open channel is able to lower superoxide anion up to 35-fold compared to a condition of ATP-inhibited channel. On the other hand, ΔΨ collapse by PmitoKATP was unexpectedly found to not affect ATP synthesis via oxidative phosphorylation. This may probably occur by means of a controlled collapse due to ATP inhibition of PmitoKATP; this brake to the channel activity may allow a loss of the bulk phase Δp, but may preserve a non-classically detectable localized driving force for ATP synthesis. This ability may become crucial under environmental/oxidative stress. In particular, under moderate hyperosmotic stress (mannitol or NaCl), PmitoKATP was found to be activated by ROS, so inhibiting further large-scale ROS production according to a feedback mechanism; moreover, a stress-activated phospholipase A2 may generate FFAs, further activating the channel. In conclusion, a main property of PmitoKATP is the ability to keep in balance the control of harmful ROS with the mitochondrial/cellular bioenergetics, thus preserving ATP for energetic needs of cell defense under stress.

No MeSH data available.


Related in: MedlinePlus

PmitoKATP functioning and modulation in durum wheat mitochondria (DWM). PmitoKATP catalyzes the electrophoretic K+ uptake across the inner membrane toward the matrix, so lowering membrane potential; the cooperation between PmitoKATP and the K+/H+ antiporter allows a K+ cycle able to dissipate also ΔpH, the second component of the proton motive force generated by the respiratory chain. ATP inhibits the channel while free fatty acids (FFAs), acyl-CoAs and superoxide anion activate it. The reducing equivalent flux through the respiratory chain to molecular oxygen and the coupled proton ejection into the intermembrane space are also indicated. The topology of ATP, FFAs, acyl-CoAs and ROS interaction with PmitoKATP is not considered. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.
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Figure 1: PmitoKATP functioning and modulation in durum wheat mitochondria (DWM). PmitoKATP catalyzes the electrophoretic K+ uptake across the inner membrane toward the matrix, so lowering membrane potential; the cooperation between PmitoKATP and the K+/H+ antiporter allows a K+ cycle able to dissipate also ΔpH, the second component of the proton motive force generated by the respiratory chain. ATP inhibits the channel while free fatty acids (FFAs), acyl-CoAs and superoxide anion activate it. The reducing equivalent flux through the respiratory chain to molecular oxygen and the coupled proton ejection into the intermembrane space are also indicated. The topology of ATP, FFAs, acyl-CoAs and ROS interaction with PmitoKATP is not considered. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.

Mentions: In DWM, the PmitoKATP is highly active and may cooperate with the K+/H+ antiporter. The operation of a K+/H+ exchanger in mammalian mitochondria has long been known (for review, see Bernardi, 1999; Xu et al., 2015), with the molecular identity in yeast and humans proposed by Zotova et al. (2010). The existence of a very active K+/H+ antiporter has been reported also in plant mitochondria (Diolez and Moreau, 1985) and some potential candidate genes have been reported by Sze et al. (2004). In DWM, the occurrence of a negligible ΔpH and of a high ΔΨ is in line with the existence of a powerful K+/H+ antiporter (Trono et al., 2011). The cooperation between PmitoKATP and K+/H+ antiporter allows the operation of a K+ cycle that causes the re-entry of H+ into the matrix, thus collapsing the proton motive force (Δp) (Pastore et al., 1999; Trono et al., 2004, 2011) by dissipating, in particular, the ΔΨ, which represents the main part of Δp in plant mitochondria (Douce, 1985; Figure 1). Interestingly, it has been demonstrated that the rate-limiting step of the K+ cycle is represented by the electrophoretic K+ influx via PmitoKATP (Pastore et al., 1999). In this respect, PmitoKATP strongly differs from the mammalian counterpart. Indeed, in mammalian mitochondria the K+ cycle cannot uncouple completely, because the maximal rate of the cycle, that corresponds to the Vmax of the K+/H+ antiporter, is only about 20% of the maximal rate of proton ejection by the respiratory chain (Garlid and Paucek, 2003). Indeed, in heart mitochondria, the increased K+ influx associated to K+ channel opening is small and it was found to depolarize by only 1–2 mV (Kowaltowski et al., 2001). In rat liver mitochondria some ΔΨ decrease was observed which depended on KCl concentration (up to about 20 mV at 100 mM KCl), but it was compensated by an increase in ΔpH so that the Δp remained almost constant (Czyz et al., 1995).


Modulation of Potassium Channel Activity in the Balance of ROS and ATP Production by Durum Wheat Mitochondria-An Amazing Defense Tool Against Hyperosmotic Stress.

Trono D, Laus MN, Soccio M, Alfarano M, Pastore D - Front Plant Sci (2015)

PmitoKATP functioning and modulation in durum wheat mitochondria (DWM). PmitoKATP catalyzes the electrophoretic K+ uptake across the inner membrane toward the matrix, so lowering membrane potential; the cooperation between PmitoKATP and the K+/H+ antiporter allows a K+ cycle able to dissipate also ΔpH, the second component of the proton motive force generated by the respiratory chain. ATP inhibits the channel while free fatty acids (FFAs), acyl-CoAs and superoxide anion activate it. The reducing equivalent flux through the respiratory chain to molecular oxygen and the coupled proton ejection into the intermembrane space are also indicated. The topology of ATP, FFAs, acyl-CoAs and ROS interaction with PmitoKATP is not considered. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.
© Copyright Policy
Related In: Results  -  Collection

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Figure 1: PmitoKATP functioning and modulation in durum wheat mitochondria (DWM). PmitoKATP catalyzes the electrophoretic K+ uptake across the inner membrane toward the matrix, so lowering membrane potential; the cooperation between PmitoKATP and the K+/H+ antiporter allows a K+ cycle able to dissipate also ΔpH, the second component of the proton motive force generated by the respiratory chain. ATP inhibits the channel while free fatty acids (FFAs), acyl-CoAs and superoxide anion activate it. The reducing equivalent flux through the respiratory chain to molecular oxygen and the coupled proton ejection into the intermembrane space are also indicated. The topology of ATP, FFAs, acyl-CoAs and ROS interaction with PmitoKATP is not considered. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.
Mentions: In DWM, the PmitoKATP is highly active and may cooperate with the K+/H+ antiporter. The operation of a K+/H+ exchanger in mammalian mitochondria has long been known (for review, see Bernardi, 1999; Xu et al., 2015), with the molecular identity in yeast and humans proposed by Zotova et al. (2010). The existence of a very active K+/H+ antiporter has been reported also in plant mitochondria (Diolez and Moreau, 1985) and some potential candidate genes have been reported by Sze et al. (2004). In DWM, the occurrence of a negligible ΔpH and of a high ΔΨ is in line with the existence of a powerful K+/H+ antiporter (Trono et al., 2011). The cooperation between PmitoKATP and K+/H+ antiporter allows the operation of a K+ cycle that causes the re-entry of H+ into the matrix, thus collapsing the proton motive force (Δp) (Pastore et al., 1999; Trono et al., 2004, 2011) by dissipating, in particular, the ΔΨ, which represents the main part of Δp in plant mitochondria (Douce, 1985; Figure 1). Interestingly, it has been demonstrated that the rate-limiting step of the K+ cycle is represented by the electrophoretic K+ influx via PmitoKATP (Pastore et al., 1999). In this respect, PmitoKATP strongly differs from the mammalian counterpart. Indeed, in mammalian mitochondria the K+ cycle cannot uncouple completely, because the maximal rate of the cycle, that corresponds to the Vmax of the K+/H+ antiporter, is only about 20% of the maximal rate of proton ejection by the respiratory chain (Garlid and Paucek, 2003). Indeed, in heart mitochondria, the increased K+ influx associated to K+ channel opening is small and it was found to depolarize by only 1–2 mV (Kowaltowski et al., 2001). In rat liver mitochondria some ΔΨ decrease was observed which depended on KCl concentration (up to about 20 mV at 100 mM KCl), but it was compensated by an increase in ΔpH so that the Δp remained almost constant (Czyz et al., 1995).

Bottom Line: PmitoKATP is inhibited by ATP and activated by superoxide anion, as well as by free fatty acids (FFAs) and acyl-CoAs.Fully open channel is able to lower superoxide anion up to 35-fold compared to a condition of ATP-inhibited channel.In particular, under moderate hyperosmotic stress (mannitol or NaCl), PmitoKATP was found to be activated by ROS, so inhibiting further large-scale ROS production according to a feedback mechanism; moreover, a stress-activated phospholipase A2 may generate FFAs, further activating the channel.

View Article: PubMed Central - PubMed

Affiliation: Consiglio per la Ricerca in Agricoltura e l'Analisi dell'Economia Agraria, Centro di Ricerca per la Cerealicoltura , Foggia, Italy.

ABSTRACT
In plants, the existence of a mitochondrial potassium channel was firstly demonstrated about 15 years ago in durum wheat as an ATP-dependent potassium channel (PmitoKATP). Since then, both properties of the original PmitoKATP and occurrence of different mitochondrial potassium channels in a number of plant species (monocotyledonous and dicotyledonous) and tissues/organs (etiolated and green) have been shown. Here, an overview of the current knowledge is reported; in particular, the issue of PmitoKATP physiological modulation is addressed. Similarities and differences with other potassium channels, as well as possible cross-regulation with other mitochondrial proteins (Plant Uncoupling Protein, Alternative Oxidase, Plant Inner Membrane Anion Channel) are also described. PmitoKATP is inhibited by ATP and activated by superoxide anion, as well as by free fatty acids (FFAs) and acyl-CoAs. Interestingly, channel activation increases electrophoretic potassium uptake across the inner membrane toward the matrix, so collapsing membrane potential (ΔΨ), the main component of the protonmotive force (Δp) in plant mitochondria; moreover, cooperation between PmitoKATP and the K(+)/H(+) antiporter allows a potassium cycle able to dissipate also ΔpH. Interestingly, ΔΨ collapse matches with an active control of mitochondrial reactive oxygen species (ROS) production. Fully open channel is able to lower superoxide anion up to 35-fold compared to a condition of ATP-inhibited channel. On the other hand, ΔΨ collapse by PmitoKATP was unexpectedly found to not affect ATP synthesis via oxidative phosphorylation. This may probably occur by means of a controlled collapse due to ATP inhibition of PmitoKATP; this brake to the channel activity may allow a loss of the bulk phase Δp, but may preserve a non-classically detectable localized driving force for ATP synthesis. This ability may become crucial under environmental/oxidative stress. In particular, under moderate hyperosmotic stress (mannitol or NaCl), PmitoKATP was found to be activated by ROS, so inhibiting further large-scale ROS production according to a feedback mechanism; moreover, a stress-activated phospholipase A2 may generate FFAs, further activating the channel. In conclusion, a main property of PmitoKATP is the ability to keep in balance the control of harmful ROS with the mitochondrial/cellular bioenergetics, thus preserving ATP for energetic needs of cell defense under stress.

No MeSH data available.


Related in: MedlinePlus