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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.


Central slice of the K-ring from Enterecoccus hirae (pdb 2BL2) perpendicular to the membrane plane. Protein is depicted in white ball&stick, protein surface in light grey, sodium as a red sphere, water as blue spheres and lipid as ball&stick and surface in gold-orange. Boundaries of the inside membrane and the expected position of the outside membrane are indicated by overlayed boxes. Notice the coincidence of height between outside bound sodium and inside lipid headgroups.
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f2-7_99: Central slice of the K-ring from Enterecoccus hirae (pdb 2BL2) perpendicular to the membrane plane. Protein is depicted in white ball&stick, protein surface in light grey, sodium as a red sphere, water as blue spheres and lipid as ball&stick and surface in gold-orange. Boundaries of the inside membrane and the expected position of the outside membrane are indicated by overlayed boxes. Notice the coincidence of height between outside bound sodium and inside lipid headgroups.

Mentions: In the high-resolution crystal structures of the same c11-ring from Ilyobacter tartaricus and the c15-ring from the cyanobacterium Spirullina platensis, lipids are absent from the inner lumen of the rotor ring. A molecular dynamic simulation of both rings that included outer and inner membrane, however, suggests a shift of the inner membrane with respect to the surrounding membrane towards the P-side35. So far, the only structural insight on the inner membrane of a rotor ring at atomic resolution was given by the serendipitous co-crystallization of the K-ring from the bacterial V-ATPase of Enterococcus hirae with native lipids bound to the rotor ring’s lumen31. This structure unequivocally shows the ring to be filled with lipids that form a proper lipid bilayer with upper and lower leaflet. Very much like the lipid plug of the c11 and c13 rings, the K-ring bilayer is located at the periplasmic end of the ring inside which results in a shift of the inner lipid membrane towards the P-side (Fig. 2). In this arrangement, the lipid head groups facing the N-side of the inner membrane align exactly to the height of the sodium cations bound at the outside of the ring. Thus, the cytoplasmic side of the rotor ring lumen is filled with water. Crystal structures of F1-c-ring complexes with the central shaft bound to the rotor ring show that the upper lumen of the rotor ring is not occupied by protein and is accessible from the cytoplasm25,26,36. Therefore, the upper inner lumen of these rotor rings is electrochemically connected to the cytoplasmic bulk solution.


Stabilization of Fo/Vo/Ao by a radial electric field
Central slice of the K-ring from Enterecoccus hirae (pdb 2BL2) perpendicular to the membrane plane. Protein is depicted in white ball&stick, protein surface in light grey, sodium as a red sphere, water as blue spheres and lipid as ball&stick and surface in gold-orange. Boundaries of the inside membrane and the expected position of the outside membrane are indicated by overlayed boxes. Notice the coincidence of height between outside bound sodium and inside lipid headgroups.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5036770&req=5

f2-7_99: Central slice of the K-ring from Enterecoccus hirae (pdb 2BL2) perpendicular to the membrane plane. Protein is depicted in white ball&stick, protein surface in light grey, sodium as a red sphere, water as blue spheres and lipid as ball&stick and surface in gold-orange. Boundaries of the inside membrane and the expected position of the outside membrane are indicated by overlayed boxes. Notice the coincidence of height between outside bound sodium and inside lipid headgroups.
Mentions: In the high-resolution crystal structures of the same c11-ring from Ilyobacter tartaricus and the c15-ring from the cyanobacterium Spirullina platensis, lipids are absent from the inner lumen of the rotor ring. A molecular dynamic simulation of both rings that included outer and inner membrane, however, suggests a shift of the inner membrane with respect to the surrounding membrane towards the P-side35. So far, the only structural insight on the inner membrane of a rotor ring at atomic resolution was given by the serendipitous co-crystallization of the K-ring from the bacterial V-ATPase of Enterococcus hirae with native lipids bound to the rotor ring’s lumen31. This structure unequivocally shows the ring to be filled with lipids that form a proper lipid bilayer with upper and lower leaflet. Very much like the lipid plug of the c11 and c13 rings, the K-ring bilayer is located at the periplasmic end of the ring inside which results in a shift of the inner lipid membrane towards the P-side (Fig. 2). In this arrangement, the lipid head groups facing the N-side of the inner membrane align exactly to the height of the sodium cations bound at the outside of the ring. Thus, the cytoplasmic side of the rotor ring lumen is filled with water. Crystal structures of F1-c-ring complexes with the central shaft bound to the rotor ring show that the upper lumen of the rotor ring is not occupied by protein and is accessible from the cytoplasm25,26,36. Therefore, the upper inner lumen of these rotor rings is electrochemically connected to the cytoplasmic bulk solution.

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.