Twisting and Subunit Rotation in Single F(O)(F1)-ATP Synthase

Overview

Journal Philos Trans R Soc Lond B Biol Sci

Specialty Biology

Date 2012 Dec 26

PMID 23267178

Citations 16

Authors

Hendrik Sielaff

Michael Borsch

Affiliations

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Abstract

F(O)F(1)-ATP synthases are ubiquitous proton- or ion-powered membrane enzymes providing ATP for all kinds of cellular processes. The mechanochemistry of catalysis is driven by two rotary nanomotors coupled within the enzyme. Their different step sizes have been observed by single-molecule microscopy including videomicroscopy of fluctuating nanobeads attached to single enzymes and single-molecule Förster resonance energy transfer. Here we review recent developments of approaches to monitor the step size of subunit rotation and the transient elastic energy storage mechanism in single F(O)F(1)-ATP synthases.

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References

Hasler K, Engelbrecht S, Junge W . Three-stepped rotation of subunits gamma and epsilon in single molecules of F-ATPase as revealed by polarized, confocal fluorometry. FEBS Lett. 1998; 426(3):301-4. DOI: 10.1016/s0014-5793(98)00358-5. View

Jiang W, Hermolin J, Fillingame R . The preferred stoichiometry of c subunits in the rotary motor sector of Escherichia coli ATP synthase is 10. Proc Natl Acad Sci U S A. 2001; 98(9):4966-71. PMC: 33147. DOI: 10.1073/pnas.081424898. View

Fillingame R, Angevine C, Dmitriev O . Coupling proton movements to c-ring rotation in F(1)F(o) ATP synthase: aqueous access channels and helix rotations at the a-c interface. Biochim Biophys Acta. 2002; 1555(1-3):29-36. DOI: 10.1016/s0005-2728(02)00250-5. View

Bowler M, Montgomery M, Leslie A, Walker J . Ground state structure of F1-ATPase from bovine heart mitochondria at 1.9 A resolution. J Biol Chem. 2007; 282(19):14238-42. DOI: 10.1074/jbc.M700203200. View

Yasuda R, Noji H, Kinosita Jr K, Yoshida M . F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps. Cell. 1998; 93(7):1117-24. DOI: 10.1016/s0092-8674(00)81456-7. View

Verhalen B, Ernst S, Borsch M, Wilkens S . Dynamic ligand-induced conformational rearrangements in P-glycoprotein as probed by fluorescence resonance energy transfer spectroscopy. J Biol Chem. 2011; 287(2):1112-27. PMC: 3256922. DOI: 10.1074/jbc.M111.301192. View

Hayashi K, Ueno H, Iino R, Noji H . Fluctuation theorem applied to F1-ATPase. Phys Rev Lett. 2010; 104(21):218103. DOI: 10.1103/PhysRevLett.104.218103. View

Margittai M, Widengren J, Schweinberger E, Schroder G, Felekyan S, Haustein E . Single-molecule fluorescence resonance energy transfer reveals a dynamic equilibrium between closed and open conformations of syntaxin 1. Proc Natl Acad Sci U S A. 2003; 100(26):15516-21. PMC: 307599. DOI: 10.1073/pnas.2331232100. View

Hakulinen J, Klyszejko A, Hoffmann J, Eckhardt-Strelau L, Brutschy B, Vonck J . Structural study on the architecture of the bacterial ATP synthase Fo motor. Proc Natl Acad Sci U S A. 2012; 109(30):E2050-6. PMC: 3409797. DOI: 10.1073/pnas.1203971109. View

10.

Hirata T, Iwamoto-Kihara A, Sun-Wada G, Okajima T, Wada Y, Futai M . Subunit rotation of vacuolar-type proton pumping ATPase: relative rotation of the G and C subunits. J Biol Chem. 2003; 278(26):23714-9. DOI: 10.1074/jbc.M302756200. View

11.

Rosing J, SLATER E . The value of G degrees for the hydrolysis of ATP. Biochim Biophys Acta. 1972; 267(2):275-90. DOI: 10.1016/0005-2728(72)90116-8. View

12.

Borsch M, Diez M, Zimmermann B, Reuter R, Graber P . Stepwise rotation of the gamma-subunit of EF(0)F(1)-ATP synthase observed by intramolecular single-molecule fluorescence resonance energy transfer. FEBS Lett. 2002; 527(1-3):147-52. DOI: 10.1016/s0014-5793(02)03198-8. View

13.

BOYER P . The ATP synthase--a splendid molecular machine. Annu Rev Biochem. 1997; 66:717-49. DOI: 10.1146/annurev.biochem.66.1.717. View

14.

Fischer S, Graber P . Comparison of DeltapH- and Delta***φ***-driven ATP synthesis catalyzed by the H(+)-ATPases from Escherichia coli or chloroplasts reconstituted into liposomes. FEBS Lett. 1999; 457(3):327-32. DOI: 10.1016/s0014-5793(99)01060-1. View

15.

Forgac M . Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol. 2007; 8(11):917-29. DOI: 10.1038/nrm2272. View

16.

Panke O, Cherepanov D, Gumbiowski K, Engelbrecht S, Junge W . Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: angular torque profile of the enzyme. Biophys J. 2001; 81(3):1220-33. PMC: 1301604. DOI: 10.1016/S0006-3495(01)75780-3. View

17.

Sambongi Y, Iko Y, Tanabe M, Omote H, Ueda I, Yanagida T . Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. Science. 1999; 286(5445):1722-4. DOI: 10.1126/science.286.5445.1722. View

18.

Duser M, Bi Y, Zarrabi N, Dunn S, Borsch M . The proton-translocating a subunit of F0F1-ATP synthase is allocated asymmetrically to the peripheral stalk. J Biol Chem. 2008; 283(48):33602-10. PMC: 2662277. DOI: 10.1074/jbc.M805170200. View

19.

Moerner , Kador . Optical detection and spectroscopy of single molecules in a solid. Phys Rev Lett. 1989; 62(21):2535-2538. DOI: 10.1103/PhysRevLett.62.2535. View

20.

Humphrey W, Dalke A, Schulten K . VMD: visual molecular dynamics. J Mol Graph. 1996; 14(1):33-8, 27-8. DOI: 10.1016/0263-7855(96)00018-5. View