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Stabilization of Fo/Vo/Ao by a radial electric field

View Article: PubMed Central - PubMed

ABSTRACT

The membrane domain of rotary ATPases (Fo/Vo/Ao) contains a membrane-embedded rotor ring which rotates against an adjacent cation channel-forming subunit during catalysis. The mechanism that allows stabilization of the highly mobile and yet tightly connected domains during operation while not impeding rotation is unknown. Remarkably, all known ATPase rotor rings are filled by lipids. In the crystal structure of the rotor ring of a V-ATPase from Enterococcus hirae the ring filling lipids form a proper membrane that is lower with respect to the embedding membrane surrounding both subunits. I propose first, that a vertical shift between lumenal lipids and embedding outside membrane is a general feature of rotor rings and second that it leads to a radial potential fall-off between rotor ring and cation channel, creating attractive forces that impact rotor-stator interaction in Fo/Vo/Ao during rotation.

No MeSH data available.


Cartoon illustrating how horizontal proximity of the cation binding site and bulk solution on the inside of the rotor ring could result in a radial membrane potential fall-off, indicated by a purple triangle, at the interface of the rotor ring and the adjacent subunit. Regions of high dielectric constant are depicted in blue for bulk solution and red for lipid headgroups. Regions of low dielectric constant are shown in grey for protein and in yellow for the hydrophobic membrane core.
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f4-7_99: Cartoon illustrating how horizontal proximity of the cation binding site and bulk solution on the inside of the rotor ring could result in a radial membrane potential fall-off, indicated by a purple triangle, at the interface of the rotor ring and the adjacent subunit. Regions of high dielectric constant are depicted in blue for bulk solution and red for lipid headgroups. Regions of low dielectric constant are shown in grey for protein and in yellow for the hydrophobic membrane core.

Mentions: A water-filled half-channel in the stator of the Fo/Vo/Ao motor provides access to rotor ring cation binding sites from the P-side22,38,39. If the membrane shift observed in the K-ring is indeed a structural feature of rotor rings in general, then the P-side half-channel lies in proximity to the water-filled cytoplasmic inside of the rotor ring. Generally, location and direction of a potential fall-off across a membrane are determined by the geometry of the membrane and the membrane’s local dielectric constant. Thus, the membrane potential is expected to fall off where the distance across a region of low dielectric constant is the shortest, i.e. the insulation is thinnest. Along similar arguments of distance and geometry, a horizontal membrane potential fall-off between two half-channels has been incorporated as an important element for torque generation in a numerical model of the Fo motor40. The apparent proximity between P-side half-channel and cytoplasmic inside of the rotor ring makes it likely that at least a partial membrane potential fall-off is occurring radially between them (Fig. 4). I hypothesize that a potential fall-off between adjacent subunit and rotor ring inside will be accompanied by an electric field. Such an electric field will exert force on charges at the interface between adjacent subunit and rotor ring, possibly providing attraction between rotor and stator. This mutual attraction could compensate for frictional forces during rotation and thus stabilize the complex. Importantly, increased rotation due to a higher membrane potential would be accompanied by stronger attraction. Thus the stabilization of the stator-rotor interface is conceived to be achieved by two complementary forces: a “resting” interaction, e.g. by van der Waals forces, and a secondary one induced by a radial potential fall-off between P-side half-channel and rotor ring inside.


Stabilization of Fo/Vo/Ao by a radial electric field
Cartoon illustrating how horizontal proximity of the cation binding site and bulk solution on the inside of the rotor ring could result in a radial membrane potential fall-off, indicated by a purple triangle, at the interface of the rotor ring and the adjacent subunit. Regions of high dielectric constant are depicted in blue for bulk solution and red for lipid headgroups. Regions of low dielectric constant are shown in grey for protein and in yellow for the hydrophobic membrane core.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5036770&req=5

f4-7_99: Cartoon illustrating how horizontal proximity of the cation binding site and bulk solution on the inside of the rotor ring could result in a radial membrane potential fall-off, indicated by a purple triangle, at the interface of the rotor ring and the adjacent subunit. Regions of high dielectric constant are depicted in blue for bulk solution and red for lipid headgroups. Regions of low dielectric constant are shown in grey for protein and in yellow for the hydrophobic membrane core.
Mentions: A water-filled half-channel in the stator of the Fo/Vo/Ao motor provides access to rotor ring cation binding sites from the P-side22,38,39. If the membrane shift observed in the K-ring is indeed a structural feature of rotor rings in general, then the P-side half-channel lies in proximity to the water-filled cytoplasmic inside of the rotor ring. Generally, location and direction of a potential fall-off across a membrane are determined by the geometry of the membrane and the membrane’s local dielectric constant. Thus, the membrane potential is expected to fall off where the distance across a region of low dielectric constant is the shortest, i.e. the insulation is thinnest. Along similar arguments of distance and geometry, a horizontal membrane potential fall-off between two half-channels has been incorporated as an important element for torque generation in a numerical model of the Fo motor40. The apparent proximity between P-side half-channel and cytoplasmic inside of the rotor ring makes it likely that at least a partial membrane potential fall-off is occurring radially between them (Fig. 4). I hypothesize that a potential fall-off between adjacent subunit and rotor ring inside will be accompanied by an electric field. Such an electric field will exert force on charges at the interface between adjacent subunit and rotor ring, possibly providing attraction between rotor and stator. This mutual attraction could compensate for frictional forces during rotation and thus stabilize the complex. Importantly, increased rotation due to a higher membrane potential would be accompanied by stronger attraction. Thus the stabilization of the stator-rotor interface is conceived to be achieved by two complementary forces: a “resting” interaction, e.g. by van der Waals forces, and a secondary one induced by a radial potential fall-off between P-side half-channel and rotor ring inside.

View Article: PubMed Central - PubMed

ABSTRACT

The membrane domain of rotary ATPases (Fo/Vo/Ao) contains a membrane-embedded rotor ring which rotates against an adjacent cation channel-forming subunit during catalysis. The mechanism that allows stabilization of the highly mobile and yet tightly connected domains during operation while not impeding rotation is unknown. Remarkably, all known ATPase rotor rings are filled by lipids. In the crystal structure of the rotor ring of a V-ATPase from Enterococcus hirae the ring filling lipids form a proper membrane that is lower with respect to the embedding membrane surrounding both subunits. I propose first, that a vertical shift between lumenal lipids and embedding outside membrane is a general feature of rotor rings and second that it leads to a radial potential fall-off between rotor ring and cation channel, creating attractive forces that impact rotor-stator interaction in Fo/Vo/Ao during rotation.

No MeSH data available.