The Peripheral Stalk of Rotary ATPases

[en] Rotary ATPases are a family of enzymes that are thought of as molecular nanomotors and are classified in three types: F, A, and V-type ATPases. Two members (F and A-type) can synthesize and hydrolyze ATP, depending on the energetic needs of the cell, while the V-type enzyme exhibits only a hydrolytic activity. The overall architecture of all these enzymes is conserved and three main sectors are distinguished: a catalytic core, a rotor and a stator or peripheral stalk. The peripheral stalks of the A and V-types are highly conserved in both structure and function, however, the F-type peripheral stalks have divergent structures. Furthermore, the peripheral stalk has other roles beyond its stator function, as evidenced by several biochemical and recent structural studies. This review describes the information regarding the organization of the peripheral stalk components of F, A, and V-ATPases, highlighting the key differences between the studied enzymes, as well as the different processes in which the structure is involved.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Colina-Tenorio, Lilia; Universidad Nacional Autonoma de Mexico > Instituto de Fisiología Celular > Departamento de Genética Molecular

Dautant, Alain; Université Bordeaux > IBGC > Energy Transducing Systems and Mitochondrial Morphology

Miranda Astudillo, Héctor Vicente ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues

Giraud, Marife-France; Université Bordeaux > IBGC > Energy Transducing Systems and Mitochondrial Morphology

González-Halphen, Diego; Universidad Nacional Autonoma de Mexico > Instituto de Fisiología Celular > Departamento de Genética Molecular

Language :

English

Title :

The Peripheral Stalk of Rotary ATPases

Publication date :

04 September 2018

Journal title :

Frontiers in Physiology

eISSN :

1664-042X

Publisher :

Frontiers Media S.A., Switzerland

Special issue title :

Mitochondrial Research

Volume :

Pages :

1-19

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 04 September 2018

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Bibliography

Allegretti, M., Klusch, N., Mills, D. J., Vonck, J., Kühlbrandt, W., and Davies, K. M. (2015). Horizontal membrane-intrinsic a-helices in the stator a-subunit of an F-type ATP synthase. Nature 521, 237-240. doi: 10.1038/nature14185
Anselmi, C., Davies, K. M., and Faraldo-Gómez, J. D. (2018). Mitochondrial ATP synthase dimers spontaneously associate due to a long-range membrane-induced force. J. Gen. Physiol. 150, 763-770. doi: 10.1085/jgp.201812033
Arnold, I., Pfeiffer, K., Neupert, W., Stuart, R. A., and Scha, H. (1998). Yeast mitochondrial F 1 F 0-ATP synthase exists as a dimer: identi cation of three dimer-speci c subunits. EMBO J. 17, 7170-7178. doi: 10.1093/emboj/17.24.7170
Arnold, I., Pfeiffer, K., Neupert, W., Stuart, R. A., and Schägger, H. (1999). ATP synthase of yeast mitochondria. J. Biol. Chem. 274, 36-40. doi: 10.1074/jbc.274.1.36
Baker, L. A., Watt, I. N., Runswick, M. J., Walker, J. E., and Rubinstein, J. L. (2012). Arrangement of subunits in intact mammalian mitochondrial ATP synthase determined by cryo-EM. Proc. Natl. Acad. Sci. U.S.A. 109, 11675-11680. doi: 10.1073/pnas.1204935109
Balabaskaran Nina, P., Dudkina, N. V., Kane, L. A., van Eyk, J. E., Boekema, E. J., Mather, M. W., et al. (2010). Highly divergent mitochondrial ATP synthase complexes in Tetrahymena thermophila. PLoS Biol. 8:e1000418. doi: 10.1371/journal.pbio.1000418
Balakrishna, A. M., Hunke, C., and Grüber, G. (2012). The structure of subunit e of the Pyrococcus horikoshii OT3 A-ATP synthase gives insight into the elasticity of the peripheral stalk. J. Mol. Biol. 420, 155-163. doi: 10.1016/j.jmb.2012.04.012
Belogrudov, G. I., Tomich, J. M., and Hatefi, Y. (1996). Membrane topography and near-neighbor relationships of the mitochondrial ATP synthase subunits e, f, and g. J. Biol. Chem. 271, 20340-20345. doi: 10.1074/jbc.271.34.20340
Benlekbir, S., Bueler, S. A., and Rubinstein, J. L. (2012). Structure of the vacuolar-type ATPase from Saccharomyces cerevisiae at 11-Å resolution. Nat. Struct. Mol. Biol. 19, 1356-1362. doi: 10.1038/nsmb.2422
Bernal, R. A., and Stock, D. (2004). Three-dimensional structure of the intact Thermus thermophilus H +-ATPase/synthase by electron microscopy. Structure 12, 1789-1798. doi: 10.1016/j.str.2004.07.017
Bi, Y., Watts, J. C., Bamford, P. K., Briere, L. A. K., and Dunn, S. D. (2008). Probing the functional tolerance of the b subunit of Escherichia coli ATP synthase for sequence manipulation through a chimera approach. Biochim. Biophys. Acta 1777, 583-591. doi: 10.1016/j.bbabio.2008.03.004
Boekema, E. J., Ubbink-Kok, T., Lolkema, J. S., Brisson, A., and Konings, W. N. (1997). Visualization of a peripheral stalk in V-type ATPase: evidence for the stator structure essential to rotational catalysis. Proc. Natl. Acad. Sci. U.S.A. 94, 14291-14293. doi: 10.1073/pnas.94.26.14291
Böttcher, B., Schwarz, L., and Gräber, P. (1998). Direct indication for the existence of a double stalk in CF0F1. J. Mol. Biol. 281, 757-762. doi: 10.1006/jmbi.1998.1957
Brandt, K., Maiwald, S., Herkenhoff-Hesselmann, B., Gnirß, K., Greie, J. C., Dunn, S. D., et al. (2013). Individual interactions of the b subunits within the stator of the Escherichia coli ATP synthase. J. Biol. Chem. 288, 24465-24479. doi: 10.1074/jbc.M113.465633
Cano-Estrada, A., Vázquez-Acevedo, M., Villavicencio-Queijeiro, A., Figueroa-Martínez, F., Miranda-Astudillo, H., Cordeiro, Y., et al. (2010). Subunit-subunit interactions and overall topology of the dimeric mitochondrial ATP synthase of Polytomella sp. Biochim. Biophys. Acta 1797, 1439-1448. doi: 10.1016/j.bbabio.2010.02.024
Carbajo, R. J., Kellas, F. A., Yang, J. C., Runswick, M. J., Montgomery, M. G., Walker, J. E., et al. (2007). How the N-terminal domain of the OSCP subunit of bovine F1Fo-ATP synthase interacts with the N-terminal region of an alpha subunit. J. Mol. Biol. 368, 310-318. doi: 10.1016/j.jmb.2007.02.059
Cherepanov, D. A., Mulkidjanian, A. Y., and Junge, W. (1999). Transient accumulation of elastic energy in proton translocating ATP synthase. FEBS Lett. 449, 1-6. doi: 10.1016/S0014-5793(99)00386-5
Cipriano, D. J., Wood, K. S., Bi, Y., and Dunn, S. D. (2006). Mutations in the dimerization domain of the b subunit from the Escherichia coli ATP synthase: deletions disrupt function but not enzyme assembly. J. Biol. Chem. 281, 12408-12413. doi: 10.1074/jbc.M513368200
Claggett, S. B., Plancher, M. O. N., Dunn, S. D., and Cain, B. D. (2009). The b subunits in the peripheral stalk of F1F0 ATP synthase preferentially adopt an offset relationship. J. Biol. Chem. 284, 16531-16540. doi: 10.1074/jbc.M109.002980
Colina-Tenorio, L., Miranda-Astudillo, H., Cano-Estrada, A., Vázquez-Acevedo, M., Cardol, P., Remacle, C., et al. (2016). Subunit Asa1 spans all the peripheral stalk of the mitochondrial ATP synthase of the chlorophycean alga Polytomella sp. Biochim. Biophys. Acta 1857, 359-369. doi: 10.1016/j.bbabio.2015.11.012
Collinson, I. R., van Raajj, M. J., Runswick, M. J., Fearnley, I. M., Skehel, M. J., Orris, G. L., et al. (1994). ATP Synthase from bovine heart mitochondria in vitro assembly of a stalk complex in the presence of F1-ATPase and in its absence. J. Mol. Biol. 242, 408-421. doi: 10.1006/jmbi.1994.1591
Coskun,ü., Chaban, Y. L., Lingl, A., Müller, V., Keegstra, W., Boekema, E. J., et al. (2004). Structure and subunit arrangement of the A-type ATP synthase complex from the archaeon Methanococcus jannaschii visualized by electron microscopy. J. Biol. Chem. 279, 38644-38648. doi: 10.1074/jbc.M406196200
Cross, R. L., and Müller, V. (2004). The evolution of A-, F-, and V-type ATP synthases and ATPases: reversals in function and changes in the H+/ATP coupling ratio. FEBS Lett. 576, 1-4. doi: 10.1016/j.febslet.2004.08.065
Cross, R. L., and Taiz, L. (1990). Gene duplication as a means for altering H+/ATP ratios during the evolution of Fo F1 ATPases and synthases. FEBS Lett. 259, 227-229. doi: 10.1016/0014-5793(90)80014-A
D'Alessandro, M., and Melandri, B. A. (2010). ATP hydrolysis in ATP synthases can be differently coupled to proton transport and modulated by ADP and phosphate: a structure based model of the mechanism. Biochim. Biophys. Acta 1797, 755-762. doi: 10.1016/j.bbabio.2010.03.007
Davies, K. M., Anselmi, C., Wittig, I., Faraldo-Gomez, J. D., and Kuhlbrandt, W. (2012). Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. U.S.A. 109, 13602-13607. doi: 10.1073/pnas.1204593109
Davies, K. M., Strauss, M., Daum, B., Kief, J. H., Osiewacz, H. D., Rycovska, A., et al. (2011). Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc. Natl. Acad. Sci. U.S.A. 108, 14121-14126. doi: 10.1073/pnas.1103621108
Del Rizzo, P. A., Bi, Y., and Dunn, S. D. (2006). ATP synthase b subunit dimerization domain: a right-handed coiled coil with offset helices. J. Mol. Biol. 364, 735-746. doi: 10.1016/j.jmb.2006.09.028
Del Rizzo, P. A., Bi, Y., Dunn, S. D., and Shilton, B. H. (2002). The "second stalk" of Escherichia coli ATP synthase: structure of the isolated dimerization domain. Biochemistry 41, 6875-6884. doi: 10.1021/bi025736i
Deleon-Rangel, J., Ishmukhametov, R. R., Jiang, W., Fillingame, R. H., and Vik, S. B. (2013). Interactions between subunits a and b in the rotary ATP synthase as determined by cross-linking. FEBS Lett. 587, 892-897. doi: 10.1016/j.febslet.2013.02.012
Deppenmeier, U., and Müller, V. (2007). Life close to the thermodynamic limit: how methanogenic archaea conserve energy. Bioenergetics 45, 123-152. doi: 10.1007/400_2006_026
Dibrova, D. V., Galperin, M. Y., and Mulkidjanian, A. Y. (2010). Characterization of the N-ATPase, a distinct, laterally transferred Na+-translocating form of the bacterial F-type membrane ATPase. Bioinformatics 26, 1473-1476. doi: 10.1093/bioinformatics/btq234
Dickson, V. K., Silvester, J. A., Fearnley, I. M., Leslie, A. G. W., and Walker, J. E. (2006). On the structure of the stator of the mitochondrial ATP synthase. EMBO J. 25, 2911-2918. doi: 10.1038/sj.emboj.7601177
Diepholz, M., Venzke, D., Prinz, S., Batisse, C., Flörchinger, B., Rössle, M., et al. (2008). A different conformation for EGC stator subcomplex in solution and in the assembled yeast V-ATPase: possible implications for regulatory disassembly. Structure 16, 1789-1798. doi: 10.1016/j.str.2008.09.010
Dmitriev, O., Jones, P. C., Jiang, W., and Fillingame, R. H. (1999). Structure of the membrane domain of subunit b of the Escherichia coli F 0 F 1 ATP synthase. J. Biol. Chem. 274, 15598-15604. doi: 10.1074/jbc.274.22.15598
Drory, O., Frolow, F., and Nelson, N. (2004). Crystal structure of yeast V-ATPase subunit C reveals its stator function. EMBO Rep. 5, 1148-1152. doi: 10.1038/sj.embor.7400294
Dudkina, N. V., Heinemeyer, J., Keegstra, W., Boekema, E. J., and Braun, H. P. (2005). Structure of dimeric ATP synthase from mitochondria: an angular association of monomers induces the strong curvature of the inner membrane. FEBS Lett. 579, 5769-5772. doi: 10.1016/j.febslet.2005.09.065
Dudkina, N. V., Kouril, R., Peters, K., Braun, H. P., and Boekema, E. J. (2010). Structure and function of mitochondrial supercomplexes. Biochim. Biophys. Acta 1797, 664-670. doi: 10.1016/j.bbabio.2009.12.013
Dudkina, N. V., Sunderhaus, S., Braun, H. P., and Boekema, E. J. (2006). Characterization of dimeric ATP synthase and cristae membrane ultrastructure from Saccharomyces and Polytomella mitochondria. FEBS Lett. 580, 3427-3432. doi: 10.1016/j.febslet.2006.04.097
Dunn, S. D., Revington, M., Cipriano, D. J., and Shilton, B. H. (2000). The b subunit of Escherichia coli ATP synthase. J. Bioenerg. Biomembr. 32, 347-355. doi: 10.1023/A:1005571818730
Forgac, M. (2007). Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8, 917-929. doi: 10.1038/nrm2272
Fronzes, R., Weimann, T., Vaillier, J., Velours, J., and Brèthes, D. (2006). The peripheral stalk participates in the yeast ATP synthase dimerization independently of e and g subunits. Biochemistry 45, 6715-6723. doi: 10.1021/bi0601407
Fujikawa, M., Sugawara, K., Tanabe, T., and Yoshida, M. (2015). Assembly of human mitochondrial ATP synthase through two separate intermediates, F1-c-ring and b-e-g complex. FEBS Lett. 589, 2707-2712. doi: 10.1016/j.febslet.2015.08.006
Gavin, P. D., Prescott, M., and Devenish, R. J. (2005). Yeast F1F0-ATP synthase complex interactions in vivo can occur in the absence of the dimer specific subunit e. J. Bioenerg. Biomembr. 37, 55-66. doi: 10.1007/s10863-005-4128-8
Grüber, G., Manimekalai, M. S. S., Mayer, F., and Müller, V. (2014). ATP synthases from archaea: the beauty of a molecular motor. Biochim. Biophys. Acta 1837, 940-952. doi: 10.1016/j.bbabio.2014.03.004
Guo, H., Bueler, S. A., and Rubinstein, J. L. (2017). Atomic model for the dimeric FO region of mitochondrial ATP synthase. Science 358, 936-940. doi: 10.1126/science.aao4815
Habersetzer, J., Ziani, W., Larrieu, I., Stines-Chaumeil, C., Giraud, M. F., Brèthes, D., et al. (2013). ATP synthase oligomerization: from the enzyme models to the mitochondrial morphology. Int. J. Biochem. Cell Biol. 45, 99-105. doi: 10.1016/j.biocel.2012.05.017
Hahn, A., Parey, K., Bublitz, M., Mills, D. J., Zickermann, V., Vonck, J., et al. (2016). Structure of a complete ATP synthase dimer reveals the molecular basis of inner mitochondrial membrane morphology. Mol. Cell 63, 445-456. doi: 10.1016/j.molcel.2016.05.037
Hahn, A., Vonck, J., Mills, D. J., Meier, T., and Kuhlbrandt, W. (2018). Structure, mechanism, and regulation of the chloroplast ATP synthase. Science 360:eaat4318. doi: 10.1126/science.aat4318
He, J., Ford, H. C., Carroll, J., Douglas, C., Gonzales, E., Ding, S., et al. (2018). Assembly of the membrane domain of ATP synthase in human mitochondria. Proc. Natl. Acad. Sci. U.S.A. 115, 2988-2993. doi: 10.1073/pnas.1722086115
Hilbers, F., Eggers, R., Pradela, K., Friedrich, K., Herkenhoff-Hesselmann, B., Becker, E., et al. (2013). Subunit d is the key player for assembly of the H+-translocating unit of Escherichia coli FOF1 ATP synthase. J. Biol. Chem. 288, 25880-25894. doi: 10.1074/jbc.M113.484675
Hunt, I. E., and Bowman, B. J. (1997). The intriguing evolution of the "b" and "G" subunits in F-type and V-type ATPases: isolation of the vma-10 gene from Neurospora crassa. J. Bioenerg. Biomembr. 29, 533-540. doi: 10.1023/A:1022474816665
Junge, W., Sielaff, H., and Engelbrecht, S. (2009). Torque generation and elastic power transmission in the rotary F O F 1-ATPase. Nature 459, 364-370. doi: 10.1038/nature08145
Kane, P. M. (1995). Disassembly and reassembly of the yeast vacuolar H-ATPase in vivo. J. Biol. Chem. 270, 17025-17032
Kish-Trier, E., Briere, L. A. K., Dunn, S. D., and Wilkens, S. (2008). The stator complex of the A1A0-ATP synthase-structural characterization of the E and H subunits. J. Mol. Biol. 375, 673-685. doi: 10.1016/j.jmb.2007.10.063
Kish-Trier, E., and Wilkens, S. (2009). Domain architecture of the stator complex of the A1A0-ATP synthase from Thermoplasma acidophilum. J. Biol. Chem. 284, 12031-12040. doi: 10.1074/jbc.M808962200
Klusch, N., Murphy, B. J., Mills, D. J., Yildiz,ö., and Kühlbrandt, W. (2017). Structural basis of proton translocation and force generation in mitochondrial ATP synthase. eLife 6:e33274. doi: 10.7554/eLife.33274
Lapaille, M., Thiry, M., Perez, E., González-Halphen, D., Remacle, C., and Cardol, P. (2010). Loss of mitochondrial ATP synthase subunit beta (Atp2) alters mitochondrial and chloroplastic function and morphology in Chlamydomonas. Biochim. Biophys. Acta 1797, 1533-1539. doi: 10.1016/j.bbabio.2010.04.013
Lau, W. C. Y., and Rubinstein, J. L. (2012). Subnanometre-resolution structure of the intact Thermus thermophilus H +-driven ATP synthase. Nature 481, 214-219. doi: 10.1038/nature10699
Lee, J., Ding, S. J., Walpole, T. B., Holding, A. N., Montgomery, M. G., Fearnley, I. M., et al. (2015). Organization of subunits in the membrane domain of the bovine F-ATPase revealed by covalent cross-linking. J. Biol. Chem. 290, 13308-13320. doi: 10.1074/jbc.M115.645283
Lee, L. K., Stewart, A. G., Donohoe, M., Bernal, R. A., and Stock, D. (2010). The structure of the peripheral stalk of Thermus thermophilus H +-ATPase/synthase. Nat. Struct. Mol. Biol. 17, 373-378. doi: 10.1038/nsmb.1761
Lupas, A. (1996). Coiled coils: new structures and new functions. Trends Biochem. Sci. 21, 375-382. doi: 10.1016/S0968-0004(96)90126-7
Lytovchenko, O., Naumenko, N., Oeljeklaus, S., Schmidt, B., von der Malsburg, K., Deckers, M., et al. (2014). The INA complex facilitates assembly of the peripheral stalk of the mitochondrial F1Fo-ATP synthase. EMBO J. 33, 1624-1638. doi: 10.15252/embj.201488076
Mason, J. M., and Arndt, K. M. (2004). Coiled coil domains: stability, specificity, and biological implications. ChemBioChem 5, 170-176. doi: 10.1002/cbic.200300781
Mayer, F., and Müller, V. (2014). Adaptations of anaerobic archaea to life under extreme energy limitation. FEMS Microbiol. Rev. 38, 449-472. doi: 10.1111/1574-6976.12043
Mazhab-Jafari, M. T., and Rubinstein, J. L. (2016). Cryo-EM studies of the structure and dynamics of vacuolar-type ATPases. Sci. Adv. 2:e1600725. doi: 10.1126/sciadv.1600725
McLachlin, D. T., Bestard, J. A., and Dunn, S. D. (1998). The b and d subunits of the Escherichia coli ATP synthase interact via residues in their C-terminal regions. J. Biol. Chem. 273, 15162-15168. doi: 10.1074/jbc.273.24.15162
McLachlin, D. T., Coveny, A. M., Clark, S. M., and Dunn, S. D. (2000). Site-directed cross-linking of b to the alpha, beta, and a subunits of the Escherichia coli ATP synthase. J. Biol. Chem. 275, 17571-17577. doi: 10.1074/jbc.M000375200
Mellwig, C., and Böttcher, B. (2003). A unique resting position of the ATP-synthase from chloroplasts. J. Biol. Chem. 278, 18544-18549. doi: 10.1074/jbc.M212852200
Minauro-Sanmiguel, F., Wilkens, S., and Garcia, J. J. (2005). Structure of dimeric mitochondrial ATP synthase: novel F0 bridging features and the structural basis of mitochondrial cristae biogenesis. Proc. Natl. Acad. Sci. U.S.A. 102, 12356-12358. doi: 10.1073/pnas.0503893102
Miranda-Astudillo, H., Cano-Estrada, A., Vázquez-Acevedo, M., Colina-Tenorio, L., Downie-Velasco, A., Cardol, P., et al. (2014). Interactions of subunits Asa2, Asa4 and Asa7 in the peripheral stalk of the mitochondrial ATP synthase of the chlorophycean alga Polytomella sp. Biochim. Biophys. Acta 1837, 1-13. doi: 10.1016/j.bbabio.2013.08.001
Miranda-Astudillo, H., Colina-Tenorio, L., Jiménez-Suárez, A., Vázquez-Acevedo, M., Salin, B., Giraud, M.-F., et al. (2018). Oxidative phosphorylation supercomplexes and respirasome reconstitution of the colorless alga Polytomella sp. Biochim. Biophys. Acta 1859, 434-444. doi: 10.1016/j.bbabio.2018.03.004
Morales-Rios, E., Montgomery, M. G., Leslie, A. G. W., and Walker, J. E. (2015). Structure of ATP synthase from Paracoccus denitrificans determined by X-ray crystallography at 4.0 Å resolution. Proc. Natl. Acad. Sci. U.S.A. 112, 13231-13236. doi: 10.1073/pnas.1517542112
Muench, S. P., Huss, M., Song, C. F., Phillips, C., Wieczorek, H., Trinick, J., et al. (2009). Cryo-electron microscopy of the vacuolar ATPase motor reveals its mechanical and regulatory complexity. J. Mol. Biol. 386, 989-999. doi: 10.1016/j.jmb.2009.01.014
Muench, S. P., Trinick, J., and Harrison, M. A. (2011). Structural divergence of the rotary ATPases. Q. Rev. Biophys. 44, 311-356. doi: 10.1017/S0033583510000338
Mühleip, A. W., Dewar, C. E., Schnaufer, A., Kühlbrandt, W., and Davies, K. M. (2017). In situ structure of trypanosomal ATP synthase dimer reveals a unique arrangement of catalytic subunits. Proc. Natl. Acad. Sci. U.S.A. 114, 992-997. doi: 10.1073/pnas.1612386114
Mühleip, A. W., Joos, F., Wigge, C., Frangakis, A. S., Kühlbrandt, W., and Davies, K. M. (2016). Helical arrays of U-shaped ATP synthase dimers form tubular cristae in ciliate mitochondria. Proc. Natl. Acad. Sci. U.S.A. 113, 8442-8447. doi: 10.1073/pnas.1525430113
Mulkidjanian, A. Y., Makarova, K. S., Galperin, M. Y., and Koonin, E. V. (2007). Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nat. Rev. Microbiol. 11, 892-899. doi: 10.1038/nrmicro1767
Müller, V., and Grüber, G. (2003). ATP synthases: structure, function and evolution of unique energy converters. Cell. Mol. Life Sci. 60, 474-494. doi: 10.1007/s00018-003-
Nakanishi, A., Kishikawa, J. I., Tamakoshi, M., Mitsuoka, K., and Yokoyama, K. (2018). Cryo em structure of intact rotary H+-ATPase/synthase from Thermus thermophilus. Nat. Commun. 9:89. doi: 10.1038/s41467-017-02553-6
Naumenko, N., Morgenstern, M., Rucktäschel, R., Warscheid, B., and Rehling, P. (2017). INA complex liaises the F1Fo-ATP synthase membrane motor modules. Nat. Commun 8:1237. doi: 10.1038/s41467-017-01437-z
Neukirch, S., Goriely, A., and Hausrath, A. C. (2008). Elastic coiled-coils act as energy buffers in the ATP synthase. Int. J. Non Linear Mech. 43, 1064-1073. doi: 10.1016/j.ijnonlinmec.2008.06.008
Omote, H., Sambonmatsu, N., Saito, K., Sambongi, Y., Iwamoto-Kihara, A., Yanagida, T., et al. (1999). The gamma-subunit rotation and torque generation in F1-ATPase from wild-type or uncoupled mutant Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 96, 7780-7784. doi: 10.1073/pnas.96.14.7780
Oot, R. A., Couoh-Cardel, S., Sharma, S., Stam, N. J., and Wilkens, S. (2017). Breaking up and making up: the secret life of the vacuolar H+-ATPase. Protein Sci. 26, 896-909. doi: 10.1002/pro.3147
Oot, R. A., Huang, L. S., Berry, E. A., and Wilkens, S. (2012). Crystal structure of the yeast vacuolar ATPase heterotrimeric EGC head peripheral stalk complex. Structure 20, 1881-1892. doi: 10.1016/j.str.2012.08.020
Oot, R. A., and Wilkens, S. (2010). Domain characterization and interaction of the yeast vacuolar ATPase subunit C with the peripheral stator stalk subunits E and G. J. Biol. Chem. 285, 24654-24664. doi: 10.1074/jbc.M110.136960
Oot, R. A., and Wilkens, S. (2012). Subunit interactions at the V 1-V o interface in yeast vacuolar ATPase. J. Biol. Chem. 287, 13396-13406. doi: 10.1074/jbc.M112.343962
O'Shea, E., Klemm, J., Kim, P., and Alber, T. (1991). X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science 254, 539-544. doi: 10.1126/science.1948029
Paumard, P. (2002). The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21, 221-230. doi: 10.1093/emboj/21.3.221
Paumard, P., Arselin, G., Vaillier, J., Chaignepain, S., Bathany, K., Schmitter, J. M., et al. (2002). Two ATP synthases can be linked through subunits I in the inner mitochondrial membrane of Saccharomyces cerevisiae. Biochemistry 41, 10390-10396. doi: 10.1021/bi025923g
Poetsch, A., Berzborn, R. J., Heberle, J., Link, T. A., Dencher, N. A., and Seelert, H. (2007). Biophysics and bioinformatics reveal structural differences of the two peripheral stalk subunits in chloroplast ATP synthase. J. Biochem. 141, 411-420. doi: 10.1093/jb/mvm045
Pogoryelov, D., Klyszejko, A. L., Krasnoselska, G. O., Heller, E.-M., Leone, V., Langer, J. D., et al. (2012). Engineering rotor ring stoichiometries in the ATP synthase. Proc. Natl. Acad. Sci. U.S.A. 109, E1599-E1608. doi: 10.1073/pnas.1120027109
Qi, J., Wang, Y., and Forgac, M. (2007). The vacuolar (H+)-ATPase: subunit arrangement and in vivo regulation. J. Bioenerg. Biomembr. 39, 423-426. doi: 10.1007/s10863-007-9116-8
Radermacher, M., Ruiz, T., Wieczorek, H., and Grüber, G. (2001). The structure of the V1-ATPase determined by three-dimensional electron microscopy of single particles. J. Struct. Biol. 135, 26-37. doi: 10.1006/jsbi.2001.4395
Rak, M., Gokova, S., and Tzagoloff, A. (2011). Modular assembly of yeast mitochondrial ATP synthase. EMBO J. 30, 920-930. doi: 10.1038/emboj.2010.364
Rawson, S., Harrison, M. A., and Muench, S. P. (2016). Rotating with the brakes on and other unresolved features of the vacuolar ATPase. Biochem. Soc. Trans. 44, 851-855. doi: 10.1042/BST20160043
Razaka-Jolly, D., Rigoulet, M., Guérin, B., and Velours, J. (1994). Mutation in the hydrophobic domain of ATP synthase subunit 4 (Subunit b) of yeast mitochondria disturbs coupling between proton translocation and catalysis. Biochemistry 33, 9684-9691. doi: 10.1021/bi00198a038
Rees, D. M., Leslie, A. G. W., and Walker, J. E. (2009). The structure of the membrane extrinsic region of bovine ATP synthase. Proc. Natl. Acad. Sci. U.S.A. 106, 21597-21601. doi: 10.1073/pnas.0910365106
Rubinstein, J. L., and Walker, J. E. (2002). ATP synthase from Saccharomyces cerevisiae: location of the OSCP subunit in the peripheral stalk region. J. Mol. Biol. 321, 613-619. doi: 10.1016/S0022-2836(02)00671-X
Rühle, T., and Leister, D. (2015). Assembly of F1F0-ATP synthases. Biochim. Biophys. Acta 1847, 849-860. doi: 10.1016/j.bbabio.2015.02.005
Sánchez-Vásquez, L., Vázquez-Acevedo, M., de la Mora, J., Vega-deLuna, F., Cardol, P., Remacle, C., et al. (2017). Near-neighbor interactions of the membrane-embedded subunits of the mitochondrial ATP synthase of a chlorophycean alga. Biochim. Biophys. Acta 1858, 497-509. doi: 10.1016/j.bbabio.2017.04.004
Saroussi, S., Schushan, M., Ben-Tal, N., Junge, W., and Nelson, N. (2012). Structure and flexibility of the C-ring in the electromotor of rotary FoF1-ATPase of pea chloroplasts. PLoS One 7:e43045. doi: 10.1371/journal.pone.0043045
Schep, D. G., Zhao, J., and Rubinstein, J. L. (2016). Models for the a subunits of the Thermus thermophilus V/A-ATPase and Saccharomyces cerevisiae V-ATPase enzymes by cryo-EM and evolutionary covariance. Proc. Natl. Acad. Sci. U.S.A. 113, 3245-3250. doi: 10.1073/pnas.1521990113
Seelert, H., and Dencher, N. A. (2011). ATP synthase superassemblies in animals and plants: two or more are better. Biochim. Biophys. Acta 1807, 1185-1197. doi: 10.1016/j.bbabio.2011.05.023
Sielaff, H., Rennekamp, H., Wächter, A., Xie, H., Hilbers, F., Feldbauer, K., et al. (2008). Domain compliance and elastic power transmission in rotary F(O)F(1)-ATPase. Proc. Natl. Acad. Sci. U.S.A. 105, 17760-17765. doi: 10.1073/pnas.0807683105
Sobti, M., Smits, C., Wong, A. S. W., Ishmukhametov, R., Stock, D., Sandin, S., et al. (2016). Cryo-EM structures of the autoinhibited E. coli ATP synthase in three rotational states. eLife 5:e21598. doi: 10.7554/eLife.21598
Soga, N., Kimura, K., Kinosita, K., Yoshida, M., and Suzuki, T. (2017). Perfect chemomechanical coupling of F o F 1-ATP synthase. Proc. Natl. Acad. Sci. U.S.A. 114, 4960-4965. doi: 10.1073/pnas.1700801114
Song, J., Pfanner, N., and Becker, T. (2018). Assembling the mitochondrial ATP synthase. Proc. Natl. Acad. Sci. U.S.A. 2018:201801697. doi: 10.1073/pnas.1801697115
Sorgen, P. L., Bubb, M. R., and Cain, B. D. (1999). Lengthening the second stalk of F 1 F 0 ATP synthase in Escherichia coli. J. Biol. Chem. 274, 36261-36266. doi: 10.1074/jbc.274.51.36261
Sorgen, P. L., Caviston, T. L., Perry, R. C., and Cain, B. D. (1998). Deletions in the second stalk of F 1 F 0 ATP synthase in Escherichia coli. J. Biol. Chem. 273, 27873-27878. doi: 10.1074/jbc.273.43.27873
Soubannier, V., Vaillier, J., Paumard, P., Coulary, B., Schaeffer, J., and Velours, J. (2002). In the absence of the first membrane-spanning segment of subunit 4(b), the yeast ATP synthase is functional but does not dimerize or oligomerize. J. Biol. Chem. 277, 10739-10745. doi: 10.1074/jbc.M111882200
Spannagel, C., Vaillier, J., Arselin, G., Graves, P. V., Grandier-Vazeille, X., and Velours, J. (1998). Evidence of a subunit 4 (subunit b) dimer in favor of the proximity of ATP synthase complexes in yeast inner mitochondrial membrane. Biochim. Biophys. Acta 1414, 260-264. doi: 10.1016/S0005-2736(98)00174-6
Spannagel, C., Vaillier, J., Arselin, G., Graves, P. V., and Velours, J. (1997). The subunit f of mitochondrial yeast ATP synthase Characterization of the protein and disruption of the structural gene ATP17. Eur. J. Biochem. 247, 1111-1117. doi: 10.1111/j.1432-1033.1997.01111.x
Srivastava, A. P., Luo, M., Zhou, W., Symersky, J., Bai, D., Chambers, M. G., et al. (2018). High-resolution cryo-EM analysis of the yeast ATP synthase in a lipid membrane. Science 360:eaas9699. doi: 10.1126/science.aas9699
Stalz, W. D., Greie, J. C., Deckers-Hebestreit, G., and Altendorf, K. (2003). Direct interaction of subunits a and b of the F0 complex of Escherichia coli ATP synthase by forming an ab2 subcomplex. J. Biol. Chem. 278, 27068-27071. doi: 10.1074/jbc.M302027200
Stephens, A. N., Khan, M. A., Roucou, X., Nagley, P., and Devenish, R. J. (2003). The molecular neighborhood of subunit 8 of yeast mitochondrial F1F0-ATP synthase probed by cysteine scanning mutagenesis and chemical modification. J. Biol. Chem. 278, 17867-17875. doi: 10.1074/jbc.M300967200
Stewart, A. G., Laming, E. M., Sobti, M., and Stock, D. (2014). Rotary ATPases-dynamic molecular machines. Curr. Opin. Struct. Biol. 25, 40-48. doi: 10.1016/j.sbi.2013.11.013
Stewart, A. G., Lee, L. K., Donohoe, M., Chaston, J. J., and Stock, D. (2012). The dynamic stator stalk of rotary ATPases. Nat. Commun. 3:687. doi: 10.1038/ncomms1693
Stewart, A. G., Sobti, M., Harvey, R. P., and Stock, D. (2013). Rotary ATPases: models, machine elements and technical specifications. Bioarchitecture 3, 2-12. doi: 10.4161/bioa.23301
Stransky, L., Cotter, K., and Forgac, M. (2016). The function of V-ATPases in cancer. Physiol. Rev. 96, 1071-1091. doi: 10.1152/physrev.00035.2015
Strauss, M., Hofhaus, G., Schröder, R. R., and Kühlbrandt, W. (2008). Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J. 27, 1154-1160. doi: 10.1038/emboj.2008.35
Su, J. Y., Hodges, R. S., and Kay, C. M. (1994). Effect of chain length on the formation and stability of synthetic alpha-helical coiled coils. Biochemistry 33, 15501-15510. doi: 10.1021/bi00255a032
Sumner, J.-P., Dow, J. A., Early, F. G., Klein, U., Jäger, D., and Wieczorek, H. (1995). Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J. Biol. Chem. 270, 5649-5653. doi: 10.1074/jbc.270.10.5649
Tabke, K., Albertmelcher, A., Vitavska, O., Huss, M., Schmitz, H.-P., and Wieczorek, H. (2014). Reversible disassembly of the yeast V-ATPase revisited under in vivo conditions. Biochem. J. 462, 185-197. doi: 10.1042/BJ20131293
Thomas, D., Bron, P., Weimann, T., Dautant, A., Giraud, M.-F., Paumard, P., et al. (2008). Supramolecular organization of the yeast F1Fo-ATP synthase. Biol. Cell 100, 591-603. doi: 10.1042/BC20080022
Ubbink-kok, T., Boekema, E. J., van Breemen, J. F. L., Brisson, A., Konings, W. N., and Lolkema, J. S. (2000). Stator structure and subunit composition of the V(1)/V(0) Na(+)-ATPase of the thermophilic bacterium Caloramator fervidus. J. Mol. Biol. 296, 311-321. doi: 10.1006/jmbi.1999.3459
van Lis, R., Mendoza-Hernandez, G., Groth, G., and Atteia, A. (2007). New insights into the unique structure of the F0F1-ATP synthase from the chlamydomonad algae Polytomella sp. and Chlamydomonas reinhardtii. Plant Physiol. 144, 1190-1199. doi: 10.1104/pp.106.094060
Vázquez-Acevedo, M., Cardol, P., Cano-Estrada, A., Lapaille, M., Remacle, C., and González-Halphen, D. (2006). The mitochondrial ATP synthase of chlorophycean algae contains eight subunits of unknown origin involved in the formation of an atypical stator-stalk and in the dimerization of the complex. J. Bioenerg. Biomembr. 38, 271-282. doi: 10.1007/s10863-006-9046-x
Velours, J., Stines-Chaumeil, C., Habersetzer, J., Chaignepain, S., Dautant, A., and Brèthes, D. (2011). Evidence of the proximity of ATP synthase subunits 6 (a) in the inner mitochondrial membrane and in the supramolecular forms of Saccharomyces cerevisiae ATP synthase. J. Biol. Chem. 286, 35477-35484. doi: 10.1074/jbc.M111.275776
Velours, J., Vaillier, J., Paumard, P., Soubannier, V., Lai-Zhang, J., and Mueller, D. M. (2001). Bovine coupling factor 6, with just 14.5% shared identity, replaces subunit h in the yeast ATP synthase. J. Biol. Chem. 276, 8602-8607. doi: 10.1074/jbc.M008123200
Vik, S. B., and Antonio, B. J. (1994). A mechanism of proton translocation by F1F0 ATP synthases suggested by double mutants of the a subunit. J. Biol. Chem. 269, 30364-30369
Villavicencio-Queijeiro, A., Vázquez-Acevedo, M., Cano-Estrada, A., Zarco-Zavala, M., Tuena De Gómez, M., Mignaco, J. A., et al. (2009). The fully-active and structurally-stable form of the mitochondrial ATP synthase of Polytomella sp. is dimeric. J. Bioenerg. Biomembr. 41, 1-13. doi: 10.1007/s10863-009-9203-0
Vonck, J., Pisa, K. Y., Morgner, N., Brutschy, B., and Müller, V. (2009). Three-dimensional structure of A1A0 ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus by electron microscopy. J. Biol. Chem. 284, 10110-10119. doi: 10.1074/jbc.M808498200
Wächter, A., Bi, Y., Dunn, S. D., Cain, B. D., Sielaff, H., Wintermann, F., et al. (2011). Two rotary motors in F-ATP synthase are elastically coupled by a flexible rotor and a stiff stator stalk. Proc. Natl. Acad. Sci. U.S.A. 108, 3924-3929. doi: 10.1073/pnas.1011581108
Walker, J. E., and Dickson, V. K. (2006). The peripheral stalk of the mitochondrial ATP synthase. Biochim. Biophys. Acta 1757, 286-296. doi: 10.1016/j.bbabio.2006.01.001
Weber, J. (2006). ATP synthase: subunit-subunit interactions in the stator stalk. Biochim. Biophys. Acta 1757, 1162-1170. doi: 10.1016/j.bbabio.2006.04.007
Weber, J., Wilke-Mounts, S., Nadanaciva, S., and Senior, A. E. (2004). Quantitative determination of direct binding of b subunit to F1 in Escherichia coli F1F0-ATP synthase. J. Biol. Chem. 279, 11253-11258. doi: 10.1074/jbc.M312576200
Weimann, T., Vaillier, J., Salin, B., and Velours, J. (2008). The intermembrane space loop of subunit b (4) is a major determinant of the stability of yeast oligomeric ATP synthases. Biochemistry 47, 3556-3563. doi: 10.1021/bi702000g
Wilkens, S., Zhang, Z., and Zheng, Y. (2005). A structural model of the vacuolar ATPase from transmission electron microscopy. Micron 36, 109-126. doi: 10.1016/j.micron.2004.10.002
Wittig, I., Meyer, B., Heide, H., Steger, M., Bleier, L., Wumaier, Z., et al. (2010). Assembly and oligomerization of human ATP synthase lacking mitochondrial subunits a and A6L. Biochim. Biophys. Acta 1797, 1004-1011. doi: 10.1016/j.bbabio.2010.02.021
Wood, K. S., and Dunn, S. D. (2007). Role of the asymmetry of the homodimeric b2 stator stalk in the interaction with the F1 sector of Escherichia coli ATP synthase. J. Biol. Chem. 282, 31920-31927. doi: 10.1074/jbc.M706259200
Yadav, K. N. S., Miranda-Astudillo, H. V., Colina-Tenorio, L., Bouillenne, F., Degand, H., Morsomme, P., et al. (2017). Atypical composition and structure of the mitochondrial dimeric ATP synthase from Euglena gracilis. Biochim. Biophys. Acta 1858, 267-275. doi: 10.1016/j.bbabio.2017.01.007
Yasuda, R., Noji, H., Ishiwata, S., Yoshida, M., and Kinosita, K. Jr. (1998). F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 steps. Cell 93, 1117-1124. doi: 10.1016/S0092-8674(00)81456-7
Zhao, J., Benlekbir, S., and Rubinstein, J. L. (2015). Electron cryomicroscopy observation of rotational states in a eukaryotic V-ATPase. Nature 521, 241-245. doi: 10.1038/nature14365
Zhou, A., Rohou, A., Schep, D. G., Bason, J. V., Montgomery, M. G., Walker, J. E., et al. (2015). Structure and conformational states of the bovine mitochondrial ATP synthase by cryo-EM. eLife 4:e10180. doi: 10.7554/eLife.10180
Zíková, A., Schnaufer, A., Dalley, R. A., Panigrahi, A. K., and Stuart, K. D. (2009). The F0F1-ATP synthase complex contains novel subunits and is essential for procyclic Trypanosoma brucei. PLoS Pathog. 5:e1000436. doi: 10.1371/journal.ppat.1000436