Redox Regulation of the Rotation of F1-ATP Synthase

Bald, Dirk; Noji, Hiroyuki; Yoshida, Masasuke; Hirono-Hara, Yoko; Hisabori, Toru

doi:10.1074/jbc.c100436200

Cited by 63 publications

(42 citation statements)

References 28 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…By using the newly designed chimeric complex (␣ 3 ␤ 3 ␥ redox ) in single molecule studies we successfully confirmed that oxidation of the redox region caused frequent long pauses (Fig. 6, C and D), which was consistent with a previous study (18). In addition, we observed that duration of rotation under oxidized conditions was relatively shorter than that shown under reduced conditions (Fig.…”

Section: Discussionsupporting

confidence: 79%

“…In a previous study we prepared a chmieric ␣ 3 ␤ 3 ␥ TCT complex originating from the thermophilic bacteria Bacillus PS3 and spinach chloroplast, and reported that oxidized ␣ 3 ␤ 3 ␥ TCT caused frequent long pauses (Ͼ 1 min) (14,18). However, we could not assign the origin of these long pauses to one of the sub-steps, 80°and further 40°(28), because the significantly modified chimeric mutants had insufficient angular resolution to allow for identification of sub-steps.…”

Section: Discussionmentioning

confidence: 99%

“…In a previous study, we reported that the capacity for redox regulation could be conferred to non-redox regulated bacterial F 1 by substitution of the central region (residues 92-239) of the ␥ subunit with the counterpart of the ␥ subunit of chloroplast F 1 (14). By using this chimeric protein, we successfully showed redox-regulation of rotation of the ␥ subunit in the complex, and that an oxidized ␥ subunit results in an increase in the frequency of long pauses which in turn leads to a decrease in ATPase activity (18).…”

mentioning

confidence: 91%

See 2 more Smart Citations

Redox Regulation of Rotation of the Cyanobacterial F1-ATPase Containing Thiol Regulation Switch

Kim

Konno

Sugano

et al. 2011

Journal of Biological Chemistry

Self Cite

View full text Add to dashboard Cite

F 1 -ATP synthase (F 1 -ATPase) is equipped with a special mechanism that prevents the wasteful reverse reaction, ATP hydrolysis, when there is insufficient proton motive force to drive ATP synthesis. Chloroplast F 1 -ATPase is subject to redox regulation, whereby ATP hydrolysis activity is regulated by formation and reduction of the disulfide bond located on the ␥ subunit. To understand the molecular mechanism of this redox regulation, we constructed a chimeric F 1 complex (␣ 3 ␤ 3 ␥ redox ) using cyanobacterial F 1 , which mimics the regulatory properties of the chloroplast F 1 -ATPase, allowing the study of its regulation at the single molecule level. The redox state of the ␥ subunit did not affect the ATP binding rate to the catalytic site(s) and the torque for rotation. However, the long pauses caused by ADP inhibition were frequently observed in the oxidized state. In addition, the duration of continuous rotation was relatively shorter in the oxidized ␣ 3 ␤ 3 ␥ redox complex. These findings lead us to conclude that redox regulation of CF 1 -ATPase is achieved by controlling the probability of ADP inhibition via the ␥ subunit inserted region, a sequence feature observed in both cyanobacterial and chloroplast ATPase ␥ subunits, which is important for ADP inhibition (Sunamura, E., Konno, H., Imashimizu-Kobayashi, M., Sugano, Y., and Hisabori, T. (2010) Plant Cell Physiol. 51, 855-865).The ATP synthase complex is ubiquitously found in energytransducing membranes such as bacterial plasma membranes, mitochondrial inner membranes, and chloroplast thylakoid membranes, where its basic architecture is highly conserved. ATP synthase consists of two motor units: the F 1 portion which is powered by ATP, and the F o portion powered by the proton motive force formed across the energy transducing membranes (1). Fuelling of ATP synthase by ATP and proton motive force results in rotational motion of F 1 and F o , respectively, though they rotate in opposite directions. On the membranes, these two motors are directly connected by protein-protein interaction, and their functions are coupled to each other: the F 1 portion catalyzes ATP hydrolysis and ATP synthesis, and the F o portion catalyzes proton translocation. Upon formation of a proton motive force across the membranes as a result of respiratory or photosynthetic electron transport, the F o portion is forced to rotate by the proton motive force. Rotation of F o induces rotation of the central axis subunits, ␥ and ⑀, of F 1 , and finally ATP is formed at the catalytic sites on ␤ subunits, presumably due to forced conformational change at the catalytic sites. Vice versa, rotation of F 1 forced by ATP hydrolysis induces rotation of F o and consequently protons are transferred in the opposite direction, where a proton motive force is generated. This enzyme may therefore hydrolyze ATP and transport protons in the opposite direction when there is insufficient proton motive force to drive ATP synthesis.However this reverse reaction catalyzed by the enzyme is highly restricted ...

show abstract

Section: Discussionsupporting

confidence: 79%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 91%

See 1 more Smart Citation

Redox Regulation of Rotation of the Cyanobacterial F1-ATPase Containing Thiol Regulation Switch

Kim

Konno

Sugano

et al. 2011

Journal of Biological Chemistry

Self Cite

View full text Add to dashboard Cite

show abstract

“…Whereas in higher plants the re-oxidation of CF 1 , following a light-dark transition, takes over 1 h, in the alga Dunaliella salina CF 1 is several times faster re-oxidized by a specific endogenous oxidant (14). Only recently redox modulation of the ␥ rotation has also been reported (15).…”

mentioning

confidence: 99%

Inactivation of the Chloroplast ATP Synthase γ Subunit Results in High Non-photochemical Fluorescence Quenching and Altered Nuclear Gene Expression in Arabidopsis thaliana

Bosco

Lezhneva

Biehl³

et al. 2004

Journal of Biological Chemistry

102

View full text Add to dashboard Cite

The nuclear atpC1 gene encoding the ␥ subunit of the plastid ATP synthase has been inactivated by T-DNA insertion mutagenesis in Arabidopsis thaliana. In the seedling-lethal dpa1 (deficiency of plastid ATP synthase 1) mutant, the absence of detectable amounts of the ␥ subunit destabilizes the entire ATP synthase complex. The expression of a second gene copy, atpC2, is unaltered in dpa1 and is not sufficient to compensate for the lack of atpC1 expression. However, in vivo protein labeling analysis suggests that assembly of the ATP synthase ␣ and ␤ subunits into the thylakoid membrane still occurs in dpa1. As a consequence of the destabilized ATP synthase complex, photophosphorylation is abolished even under reducing conditions. Further effects of the mutation include an increased light sensitivity of the plant and an altered photosystem II activity. At low light intensity, chlorophyll fluorescence induction kinetics is close to those found in wild type, but non-photochemical quenching strongly increases with increasing actinic light intensity resulting in steady state fluorescence levels of about 60% of the minimal dark fluorescence. Most fluorescence quenching relaxed within 3 min after dark incubation. Spectroscopic and biochemical studies have shown that a high proton gradient is responsible for most quenching. Thylakoids of illuminated dpa1 plants were swollen due to an increased proton accumulation in the lumen. Expression profiling of 3292 nuclear genes encoding mainly chloroplast proteins demonstrates that most organelle functions are down-regulated. On the contrary, the mRNA expression of some photosynthesis genes is significantly up-regulated, probably to compensate for the defect in dpa1.

show abstract

“…A series of chimeras of F 1 with the FliJ-γ fusion rotor were prepared by substituting the C-terminal helix of FliJ with that of γ, to produce ChF 1 (xγ), where x indicates the length of substitution; x = 0, 9, 17, or 21. These chimeric complexes were expressed in E. coli and purified with Ni 2+ -affinity chromatography (Qiagen) followed by size-exclusion chromatography with Superdex 200 10/300GL (GE Healthcare) as previously reported (33). The purified enzymes were biotinylated at the two cysteines in the FliJ sequence and subjected to rotation analysis.…”

mentioning

confidence: 99%

Rotation of artificial rotor axles in rotary molecular motors

Baba

Iwamoto

Iino

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

F 1 -and V 1 -ATPase are rotary molecular motors that convert chemical energy released upon ATP hydrolysis into torque to rotate a central rotor axle against the surrounding catalytic stator cylinder with high efficiency. How conformational change occurring in the stator is coupled to the rotary motion of the axle is the key unknown in the mechanism of rotary motors. Here, we generated chimeric motor proteins by inserting an exogenous rod protein, FliJ, into the stator ring of F 1 or of V 1 and tested the rotation properties of these chimeric motors. Both motors showed unidirectional and continuous rotation, despite no obvious homology in amino acid sequence between FliJ and the intrinsic rotor subunit of F 1 or V 1 . These results showed that any residue-specific interactions between the stator and rotor are not a prerequisite for unidirectional rotation of both F 1 and V 1 . The torque of chimeric motors estimated from viscous friction of the rotation probe against medium revealed that whereas the F 1 -FliJ chimera generates only 10% of WT F 1 , the V 1 -FliJ chimera generates torque comparable to that of V 1 with the native axle protein that is structurally more similar to FliJ than the native rotor of F 1 . This suggests that the gross structural mismatch hinders smooth rotation of FliJ accompanied with the stator ring of F 1 .rotary molecular motor | protein design | ATPase | F 1 | V-ATPase

show abstract

Redox Regulation of the Rotation of F1-ATP Synthase

Cited by 63 publications

References 28 publications

Redox Regulation of Rotation of the Cyanobacterial F1-ATPase Containing Thiol Regulation Switch

Redox Regulation of Rotation of the Cyanobacterial F1-ATPase Containing Thiol Regulation Switch

Inactivation of the Chloroplast ATP Synthase γ Subunit Results in High Non-photochemical Fluorescence Quenching and Altered Nuclear Gene Expression in Arabidopsis thaliana

Rotation of artificial rotor axles in rotary molecular motors

Contact Info

Product

Resources

About