DOI: 10.1042/bj20100621. Essential arginine residue of the Fo-<i>a</i> subunit in FoF1-ATP synthase has a role to prevent the proton shortcut without <i>c</i>-ring rotation in the Fo proton channel

Essential arginine residue of the Fo-a subunit in FoF1-ATP synthase has a role to prevent the proton shortcut without c-ring rotation in the Fo proton channel

10.1042/bj20100621

Crossref journal-article

Portland Press Ltd.

Biochemical Journal (288)

Abstract

In FoF1 (FoF1-ATP synthase), proton translocation through Fo drives rotation of the oligomer ring of Fo-c subunits (c-ring) relative to Fo-a. Previous reports have indicated that a conserved arginine residue in Fo-a plays a critical role in the proton transfer at the Fo-a/c-ring interface. Indeed, we show in the present study that thermophilic FoF1s with substitution of this arginine (aR169) to other residues cannot catalyse proton-coupled reactions. However, mutants with substitution of this arginine residue by a small (glycine, alanine, valine) or acidic (glutamate) residue mediate the passive proton translocation. This translocation requires an essential carboxy group of Fo-c (cE56) since the second mutation (cE56Q) blocks the translocation. Rotation of the c-ring is not necessary because the same arginine mutants of the ‘rotation-impossible’ (c10-a)FoF1, in which the c-ring and Fo-a are fused to a single polypeptide, also exhibits the passive proton translocation. The mutant (aR169G/Q217R), in which the arginine residue is transferred to putatively the same topological position in the Fo-a structure, can block the passive proton translocation. Thus the conserved arginine residue in Fo-a ensures proton-coupled c-ring rotation by preventing a futile proton shortcut.

Bibliography

Mitome, N., Ono, S., Sato, H., Suzuki, T., Sone, N., & Yoshida, M. (2010). Essential arginine residue of the Fo-a subunit in FoF1-ATP synthase has a role to prevent the proton shortcut without c-ring rotation in the Fo proton channel. Biochemical Journal, 430(1), 171â177.

Authors 6

Noriyo Mitome (first)
Sakurako Ono (additional)
Hiroki Sato (additional)
Toshiharu Suzuki (additional)
Nobuhito Sone (additional)
Masasuke Yoshida (additional)

References 21 Referenced 64

10.1146/annurev.biochem.66.1.717 / Annu. Rev. Biochem. / The ATP synthase: a splendid molecular machine by Boyer (1997)
10.1038/35089509 / Nat. Rev. Mol. Cell Biol. / ATP synthase: a marvellous rotary engine of the cell by Yoshida (2001)
10.1073/pnas.0403545101 / Proc. Natl Acad. Sci. U.S.A. / Thermophilic ATP synthase has a decamer c-ring: indication of noninteger 10:3 H+/ATP ratio and permissive elastic coupling by Mitome (2004)
10.1073/pnas.95.12.6607 / Proc. Natl Acad. Sci. U.S.A. / Interacting helical faces of subunits a and c in the F1Fo ATP synthase of Escherichia coli defined by disulfide cross-linking by Jiang (1998)
10.1074/jbc.M111210200 / J. Biol. Chem. / Fo of ATP synthase is a rotary proton channel: obligatory coupling of proton translocation with rotation of c-subunit ring by Suzuki (2002)
10.1016/j.jmb.2006.01.011 / J. Mol. Biol / A new solution structure of ATP synthase subunit c from thermophilic Bacillus PS3, suggesting a local conformational change for H+-translocation by Nakano (2006)
10.1021/bi00005a020 / Biochemistry / Determination of local protein structure by spin label difference 2D NMR: the region neighboring Asp61 of subunit c of the F1Fo ATP synthase by Girvin (1995)
10.1126/science.1111199 / Science / Structure of the rotor ring of F-Type Na+-ATPase from Ilyobacter tartaricus by Meier (2005)
10.1074/jbc.273.26.16241 / J. Biol. Chem. / Transmembrane topography of subunit a in the Escherichia coli F1Fo ATP synthase by Valiyaveetil (1998)
10.1074/jbc.273.26.16235 / J. Biol. Chem. / Membrane topology of subunit a of the F1Fo ATP synthase as determined by labeling of unique cysteine residues by Long (1998)
10.1074/jbc.270.49.29407 / J Biol. Chem. / The essential arginine residue at position 210 in the α subunit of the Escherichia coli ATP synthase can be transferred to position 252 with partial retention of activity by Hatch (1995)
10.1074/jbc.272.51.32635 / J. Biol. Chem. / On the role of Arg-210 and Glu-219 of subunit a in proton translocation by the Escherichia coli F0F1-ATP synthase by Valiyaveetil (1997)
10.1074/jbc.273.26.16229 / J. Biol. Chem. / Insertion scanning mutagenesis of subunit a of the F1Fo ATP synthase near His245 and implications on gating of the proton channel by Vik (1998)
10.1016/S0014-5793(03)01101-3 / FEBS Lett. / Mechanics of coupling proton movements to c-ring rotation in ATP synthase by Fillingame (2003)
10.1016/S0968-0004(97)01129-8 / Trends Biochem. Sci. / An electrochemical transducer with rotatory mechanics by Junge (1997)
10.1128/jb.160.3.1055-1060.1984 / J. Bacteriol. / In vivo evidence for the role of the ϵ subunit as an inhibitor of the proton-translocating ATPase of Escherichia coli by Klionsky (1984)
10.1074/jbc.273.45.29701 / J. Biol. Chem. / Genetic fusions of subunit c in the F0 sector of H+-transporting ATP synthase. Functional dimers and trimers and determination of stoichiometry by cross-linking analysis by Jones (1998)
10.1016/j.bbabio.2007.11.004 / Biochim. Biophys. Acta / ATP synthesis without R210 of subunit a in the Escherichia coli ATP synthase by Ishmukhametov (2008)
10.1016/j.bbabio.2009.03.022 / Biochim. Biophys. Acta / A more robust version of the arginine 210-switched mutant in subunit a of the Escherichia coli ATP synthase by Bae (2009)
10.1038/35185 / Nature / Energy transduction in ATP synthase by Elston (1998)
10.1016/S0006-3495(04)74205-8 / Biophys. J. / Insights into the molecular mechanism of rotation in the Fo sector of ATP synthase by Aksimentiev (2004)

Dates

Type	When
Created	15 years, 3 months ago (June 3, 2010, 10:07 a.m.)
Deposited	3 years, 9 months ago (Nov. 22, 2021, 1:19 p.m.)
Indexed	1 month, 1 week ago (July 25, 2025, 6:42 a.m.)
Issued	15 years, 1 month ago (July 28, 2010)
Published	15 years, 1 month ago (July 28, 2010)
Published Online	15 years, 1 month ago (July 28, 2010)
Published Print	15 years ago (Aug. 15, 2010)

Funders 0

None

BibTeX

@article{Mitome_2010, title={Essential arginine residue of the Fo-a subunit in FoF1-ATP synthase has a role to prevent the proton shortcut without c-ring rotation in the Fo proton channel}, volume={430}, ISSN={1470-8728}, url={http://dx.doi.org/10.1042/bj20100621}, DOI={10.1042/bj20100621}, number={1}, journal={Biochemical Journal}, publisher={Portland Press Ltd.}, author={Mitome, Noriyo and Ono, Sakurako and Sato, Hiroki and Suzuki, Toshiharu and Sone, Nobuhito and Yoshida, Masasuke}, year={2010}, month=jul, pages={171–177} }

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