Changes of the Capacitance and Boundary Potential of a Bilayer Lipid Membrane Associated with a Fast Release of Protons on Its Surface

Tashkin, V. Yu.; Vishnyakova, V. E.; Shcherbakov, A. A.; Finogenova, O.A.; Ermakov, Yu. A.; Sokolov, V.S.

doi:10.1134/s1990747819020077

Cited by 4 publications

(10 citation statements)

References 12 publications

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“…The effect of electrical field on membrane deformation was observed, in part, by the method of inner field compensation on the bilayer membranes. Its application showed a change in the membrane thickness and capacitance when the membrane interacts with various compounds [ 85 , 86 , 87 ], including the membrane-bound proton fraction [ 3 , 4 ]. We proposed that a similar effect may also present in the MIM under proton pump functioning [ 2 ].…”

Section: Discussionmentioning

confidence: 99%

“…While Mitchell’s chemiosmotic theory provides a general understanding of the OXPHOS system functioning, it ignores a large number of experimental facts showing that after transmembrane transfer or after H + dissociation at the membrane–water interface, protons do not immediately equilibrate with a water bulk phase but are retained at the membrane–water interface in nonequilibrium state (review in [ 1 , 2 ]). The retention of the protons on the membrane was shown in the model bilayer membranes using different techniques for proton release [ 3 , 4 ]. On the liposomes [ 5 ] and even on the octane–water interface [ 6 ], it was shown that surface protons drive ATP synthesis.…”

Section: Introductionmentioning

confidence: 99%

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Contribution of the Collective Excitations to the Coupled Proton and Energy Transport along Mitochondrial Cristae Membrane in Oxidative Phosphorylation System

Nesterov

Yaguzhinsky²,

Василов³

et al. 2022

Entropy

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The results of many experimental and theoretical works indicate that after transport of protons across the mitochondrial inner membrane (MIM) in the oxidative phosphorylation (OXPHOS) system, they are retained on the membrane–water interface in nonequilibrium state with free energy excess due to low proton surface-to-bulk release. This well-established phenomenon suggests that proton trapping on the membrane interface ensures vectorial lateral transport of protons from proton pumps to ATP synthases (proton acceptors). Despite the key role of the proton transport in bioenergetics, the molecular mechanism of proton transfer in the OXPHOS system is not yet completely established. Here, we developed a dynamics model of long-range transport of energized protons along the MIM accompanied by collective excitation of localized waves propagating on the membrane surface. Our model is based on the new data on the macromolecular organization of the OXPHOS system showing the well-ordered structure of respirasomes and ATP synthases on the cristae membrane folds. We developed a two-component dynamics model of the proton transport considering two coupled subsystems: the ordered hydrogen bond (HB) chain of water molecules and lipid headgroups of MIM. We analytically obtained a two-component soliton solution in this model, which describes the motion of the proton kink, corresponding to successive proton hops in the HB chain, and coherent motion of a compression soliton in the chain of lipid headgroups. The local deformation in a soliton range facilitates proton jumps due to water molecules approaching each other in the HB chain. We suggested that the proton-conducting structures formed along the cristae membrane surface promote direct lateral proton transfer in the OXPHOS system. Collective excitations at the water–membrane interface in a form of two-component soliton ensure the coupled non-dissipative transport of charge carriers and elastic energy of MIM deformation to ATP synthases that may be utilized in ATP synthesis providing maximal efficiency in mitochondrial bioenergetics.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Contribution of the Collective Excitations to the Coupled Proton and Energy Transport along Mitochondrial Cristae Membrane in Oxidative Phosphorylation System

Nesterov

Yaguzhinsky²,

Василов³

et al. 2022

Entropy

View full text Add to dashboard Cite

show abstract

“…Its application showed a change of the membrane thickness and capacitance when the membrane interacts with various compounds (Abidor I.G. et al 1980; Cherny et al 1980; Jiménez-Munguía et al 2019), including the membrane-bound proton fraction (Antonenko et al 1993; Tashkin et al 2019). We proposed that a similar effect may also present in the MIM under proton pump functioning (Nesterov et al 2022).…”

Section: Discussionmentioning

confidence: 99%

“…While Mitchell’s chemiosmotic theory, of course, provides general understanding of OXPHOS functioning, it ignores a large number of experimental facts showing that after transmembrane transfer or after H + dissociation at the membrane-water interface, protons do not immediately equilibrate with a water bulk phase, but are retained at the membrane-water interface in non-equilibrium state (review in (Mulkidjanian et al 2006; Nesterov et al 2022)). The retention of the protons on the membrane was shown in the model bilayer membranes using different techniques for proton release (Antonenko et al 1993; Tashkin et al 2019). On the liposomes (Sjöholm et al 2017) and even on the octane-water interface (Yaguzhinsky et al 1976), it was shown that surface protons drives ATP synthesis.…”

Section: Introductionmentioning

confidence: 99%

Contribution of the collective excitations to the coupled proton and energy transport along mitochondrial crista membrane in oxidative phosphorylation system

Nesterov

Yaguzhinskiy

Василов

et al. 2022

Preprint

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The results of many experimental and theoretical works indicate that after transport of protons across the mitochondrial inner membrane (MIM) in oxidative phosphorylation system (OXPHOS), they are retained on the membrane-water interface in non-equilibrium state with free energy excess due to low proton surface-to-bulk release. This well-established phenomenon suggests that proton trapping on the membrane interface ensures vectorial lateral transport of protons from proton pumps to ATP synthases (proton acceptors). Despite the key role of the proton transport in bioenergetics, the molecular mechanism of proton transfer in OXPHOS is not yet completely established. Here, we developed a dynamic model of long-range transport of energized protons along the MIM accompanied by collective excitation of localized wave prorogating on the membrane surface. Our model is based on the new data on the macromolecular organization of OXPHOS showing the well-ordered structure of respirasomes and ATP synthases on the cristae membrane folds. We developed a two-component dynamic model of the proton transport considering two coupled subsystems: the ordered hydrogen bond chain of water molecules and lipid headgroups of MIM. We analytically obtained two-component soliton solution in this model, which describe the motion of the proton kink, corresponding to successive proton hops in the HB chain, and coherent motion of a compression soliton in the chain of lipid headpolar groups. The local deformation in a soliton range facilitates proton jumps due to water molecules approaching each other in the HB chain. We suggested that the proton-conducting structures formed along the cristae membrane surface promotes direct lateral proton transfer in OXPHOS. Collective excitations at the water-membrane interface in a form of two-component soliton ensure the coupled non-dissipative transport of charge carriers and elastic energy of MIM deformation to ATP synthases that may be utilized in ATP synthesis providing maximal efficiency in mitochondrial bioenergetics.

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“…More easy and rapid estimations of interfacial protons can be achieved by direct electric measurements of the membrane capacitance and electrostatic potentials. Recently, we have observed changes in these values caused by a fast light-driven release of protons from sodium 2-methoxy-5-nitrophenyl sulfate (MNPS) ( Figure 1 ) at the membrane surface that has relaxed in a timescale of about one minute [ 13 ]. Study of the kinetics of such slow relaxation can be informative for better understanding of processes coupled with light-driven release of protons from photosensitive compounds.…”

Section: Introductionmentioning

confidence: 99%

Electrostatic Potentials Caused by the Release of Protons from Photoactivated Compound Sodium 2-Methoxy-5-nitrophenyl Sulfate at the Surface of Bilayer Lipid Membrane

Sokolov,

Tashkin,

Zykova

et al. 2023

Membranes

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Lateral transport and release of protons at the water–membrane interface play crucial roles in cell bioenergetics. Therefore, versatile techniques need to be developed for investigating as well as clarifying the main features of these processes at the molecular level. Here, we experimentally measured the kinetics of binding of protons released from the photoactivated compound sodium 2-methoxy-5-nitrophenyl sulfate (MNPS) at the surface of a bilayer lipid membrane (BLM). We developed a theoretical model of this process describing the damage of MNPS coupled with the release of the protons at the membrane surface, as well as the exchange of MNPS molecules and protons between the membrane and solution. We found that the total change in the boundary potential difference across the membrane, ∆ϕb, is the sum of opposing effects of adsorption of MNPS anions and release of protons at the membrane–water interface. Steady-state change in the ∆ϕb due to protons decreased with the concentration of the buffer and increased with the pH of the solution. The change in the concentration of protons evaluated from measurements of ∆ϕb was close to that in the unstirred water layer near the BLM. This result, as well as rate constants of the proton exchange between the membrane and the bulk solution, indicated that the rate-limiting step of the proton surface to bulk release is the change in the concentration of protons in the unstirred layer. This means that the protons released from MNPS remain in equilibrium between the BLM surface and an adjacent water layer.

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Changes of the Capacitance and Boundary Potential of a Bilayer Lipid Membrane Associated with a Fast Release of Protons on Its Surface

Cited by 4 publications

References 12 publications

Contribution of the Collective Excitations to the Coupled Proton and Energy Transport along Mitochondrial Cristae Membrane in Oxidative Phosphorylation System

Contribution of the Collective Excitations to the Coupled Proton and Energy Transport along Mitochondrial Cristae Membrane in Oxidative Phosphorylation System

Contribution of the collective excitations to the coupled proton and energy transport along mitochondrial crista membrane in oxidative phosphorylation system

Electrostatic Potentials Caused by the Release of Protons from Photoactivated Compound Sodium 2-Methoxy-5-nitrophenyl Sulfate at the Surface of Bilayer Lipid Membrane

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