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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

Effect of in vitro modulation of PmitoKATP on ΔΨ and reactive oxygen species (ROS) production. (A) When ATP inhibits PmitoKATP and, as a consequence, the K+ cycle due to the PmitoKATP-K+/H+ antiporter combined function, both high electrical membrane potential (ΔΨ) and high ROS production are observed. (B) On the contrary, in the presence of FFAs and their acyl-CoA derivatives, as well as of ROS, which activate PmitoKATP, K+ cycle is activated and both low ΔΨ and low ROS production are observed. In isolated DWM the degree of PmitoKATP functioning is dependent on the balance among modulators; a fully opened channel may completely collapse ΔΨ and ROS production. The reducing equivalent flux through the respiratory chain to molecular oxygen and the coupled proton ejection into the intermembrane space are also indicated; + and – signs refer to ΔΨ. The continuous or dotted arrows refer to a more or less active pathway, respectively. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.
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Figure 2: Effect of in vitro modulation of PmitoKATP on ΔΨ and reactive oxygen species (ROS) production. (A) When ATP inhibits PmitoKATP and, as a consequence, the K+ cycle due to the PmitoKATP-K+/H+ antiporter combined function, both high electrical membrane potential (ΔΨ) and high ROS production are observed. (B) On the contrary, in the presence of FFAs and their acyl-CoA derivatives, as well as of ROS, which activate PmitoKATP, K+ cycle is activated and both low ΔΨ and low ROS production are observed. In isolated DWM the degree of PmitoKATP functioning is dependent on the balance among modulators; a fully opened channel may completely collapse ΔΨ and ROS production. The reducing equivalent flux through the respiratory chain to molecular oxygen and the coupled proton ejection into the intermembrane space are also indicated; + and – signs refer to ΔΨ. The continuous or dotted arrows refer to a more or less active pathway, respectively. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.

Mentions: On the whole, in vitro modulation of PmitoKATP due to externally added ATP, FFAs/acyl-CoAs and ROS regulates the mitochondrial ΔΨ and ROS generation. Notably, as shown in Figure 2, ATP addition to DWM inhibits PmitoKATP and, consequently, the K+ cycle; this generates a high ΔΨ and a high ROS production (Figure 2A). On the contrary, the addition of FFAs and/or their acyl-CoA derivatives, as well as of ROS, which all activate PmitoKATP, determines an increase in the rate of the K+ cycle, thus leading to a decrease in ΔΨ and ROS production (Figure 2B).


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)

Effect of in vitro modulation of PmitoKATP on ΔΨ and reactive oxygen species (ROS) production. (A) When ATP inhibits PmitoKATP and, as a consequence, the K+ cycle due to the PmitoKATP-K+/H+ antiporter combined function, both high electrical membrane potential (ΔΨ) and high ROS production are observed. (B) On the contrary, in the presence of FFAs and their acyl-CoA derivatives, as well as of ROS, which activate PmitoKATP, K+ cycle is activated and both low ΔΨ and low ROS production are observed. In isolated DWM the degree of PmitoKATP functioning is dependent on the balance among modulators; a fully opened channel may completely collapse ΔΨ and ROS production. The reducing equivalent flux through the respiratory chain to molecular oxygen and the coupled proton ejection into the intermembrane space are also indicated; + and – signs refer to ΔΨ. The continuous or dotted arrows refer to a more or less active pathway, respectively. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.
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Related In: Results  -  Collection

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Figure 2: Effect of in vitro modulation of PmitoKATP on ΔΨ and reactive oxygen species (ROS) production. (A) When ATP inhibits PmitoKATP and, as a consequence, the K+ cycle due to the PmitoKATP-K+/H+ antiporter combined function, both high electrical membrane potential (ΔΨ) and high ROS production are observed. (B) On the contrary, in the presence of FFAs and their acyl-CoA derivatives, as well as of ROS, which activate PmitoKATP, K+ cycle is activated and both low ΔΨ and low ROS production are observed. In isolated DWM the degree of PmitoKATP functioning is dependent on the balance among modulators; a fully opened channel may completely collapse ΔΨ and ROS production. The reducing equivalent flux through the respiratory chain to molecular oxygen and the coupled proton ejection into the intermembrane space are also indicated; + and – signs refer to ΔΨ. The continuous or dotted arrows refer to a more or less active pathway, respectively. SH2, reduced substrates; S, oxidized substrates; i.m.m., inner mitochondrial membrane.
Mentions: On the whole, in vitro modulation of PmitoKATP due to externally added ATP, FFAs/acyl-CoAs and ROS regulates the mitochondrial ΔΨ and ROS generation. Notably, as shown in Figure 2, ATP addition to DWM inhibits PmitoKATP and, consequently, the K+ cycle; this generates a high ΔΨ and a high ROS production (Figure 2A). On the contrary, the addition of FFAs and/or their acyl-CoA derivatives, as well as of ROS, which all activate PmitoKATP, determines an increase in the rate of the K+ cycle, thus leading to a decrease in ΔΨ and ROS production (Figure 2B).

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