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3.A.2 The H+- or Na+-translocating F-type, V-type and A-type ATPase (F-ATPase) Superfamily

F-type ATPases are found in eukaryotic mitochondria and chloroplasts as well as in bacteria. V-type ATPases are found in vacuoles of eukaryotes and in bacteria. A-type ATPases are found in archaea. All such systems are multisubunit complexes with at least 3 dissimilar subunits embedded as a complex in the membrane (F0, a:b:c = 1:2:~12) and (usually) at least 5 dissimilar subunits attached to F0 (F1, α:β:γ:δ:ε = 3:3:1:1:1 for F-type ATPases). The eukaryotic proteins are more complicated than the bacterial enzyme complexes. The a, b, δ and F1 hexamer (α3β3) comprise the stator. The rotor (which consists of the c, ε and γ subunits) is believed to rotate relative to the stator in response to either ATP hydrolysis by F1 or proton transport through F0. H+ transport and ATP synthesis may therefore be coupled mechanically. The F1 portion of the bovine mitochondrial F-type ATPase has been solved to 2.8 Å resolution. Cross-linking studies suggest that the H+ channel consists of a and c subunits where the external aqueous access channel is located to the inside of the a-subunit 4-helix bundle (Schwem and Fillingame, 2006). Minimal requirements for proton translocation by the ATP synthase include a positive charge in subunit a and a weak interface between subunit a and oligomeric subunit c (Ishmukhametov et al., 2007). These enzymes can pump H+ or Na+. A Na+ A-type ATPase from Pyrococcus furiosus has been described (Pisa et al., 2007b). ATP binding to the ε-subunit plays a regulatory role; ATP binding may stabilize the ATPase-active form by fixing the ε-subunit into the folded conformation (Kato et al., 2007).

All eukaryotic F-type ATPases pump 3-4 H+ out of mitochondria, or into thylakoids of chloroplasts, per ATP hydrolyzed. Bacterial F-type ATPases pump 3-4 H+ and/or Na+ (depending on the system) out of the cell per ATP hydrolyzed. These enzymes also operate in the opposite direction, synthesizing ATP when protons or Na+ flow through the 'ATP synthase' down the proton electrochemical gradient (the 'proton motive force' or pmf) (Ferguson et al., 2006). V-type ATPases may pump 2-3 H+ per ATP hydrolyzed, and these enzymes cannot catalyze pmf-driven ATP synthesis. It has been proposed that this difference between F-type and V-type ATPases is due to a 'proton slip' that results from an altered structure in the membrane sector of V-type ATPases (Perzov et al., 2001). This probably results from duplication (intragenic and/or intergenic) of the proteolipid (c) subunit.

The structure of the membrane integral rotor ring of the proton translocating F(1)F(0)-ATPase synthase from spinach chloroplasts was determined to 3.8 A resolution by X-ray crystallography (Vollmar et al., 2009). The rotor ring consists of 14 identical protomers which are symmetrically arranged around a central pore, but rings having anywhere from 8 protomers to 15 protomers have been reported (Watt et al., 2010). Comparisons to the c(11)-rotor ring of the sodium translocating ATPase from Ilyobacter tartaricus show that the conserved carboxylates involved in proton or sodium transport, respectively, are 10.6-10.8 A apart in both c-ring rotors. This finding suggests that both ATPases have the same gear distance despite their different stoichiometries. The putative proton binding site at the conserved carboxylate E61 in the chloroplast ATP synthase differs from the sodium binding site in Ilyobacter. Residues adjacent to the conserved carboxylate show increased hydrophobicity and reduced hydrogen bonding. The crystal structure reflects the protonated form of the chloroplast c-ring rotor. Vollmar et al., 2009 proposed that upon deprotonation, the conformation of E61 is changed to another rotamer and becomes fully exposed to the periphery of the ring. Reprotonation of E61 by a conserved arginine in the adjacent a subunit returns the carboxylate to its initial conformation.

Phylogenetic clustering of the integral membrane constituents of F-type ATPases generally corresponds to the phylogenies of the organisms of origin, and consequently the systems in different organisms are probably orthologues. The a subunit of F0 (one copy per complex) spans the membrane five or six times. The b subunits (2 copies per complex; heterodimeric in plant chloroplasts and blue green bacteria) span the membrane once; and the c subunits (called DCCD-binding lipoproteins; reportedly 10, 11, 12, or 14 copies per complex depending on the system) span the membrane two times. Some F-type ATPases such as the Na+-translocating ATPase of Acetobacterium woodii probably contains 3 dissimilar but homologous c-subunit proteolipids of 8 and 18 kDa. The V-type ATPase of S. cerevisiae also has 3 dissimilar c-subunits as mentioned in the next paragraph. While c-subunits in the E. coli F-ATPase have 2 TMSs (one acive site asp per subunit and 12 copies per complex), V-type ATPases have 4 TMSs (one active site glu per subunit and 6 copies per complex), and an archaeal A-ATPase has 6 TMSs (2 active site glus per subunit and 4 subunits per complex).

The α, β and c-subunits of F-type ATPases are homologues to the B, A and c- (or K-) subunits of V-type and A-type ATPases, respectively. Other subunits in these protein complexes are probably homologous to each other, but this fact cannot always be demonstrated by statistical analyses of the sequences. Thus, for the A-type ATPase of Methanosarcina mazei, the V-type ATPase of yeast, and the F-type ATPase of E. coli, respectively, the following subunit equivalences have been suggested: A = Vma1 (A) = β; B = Vma2 (B) = α; C = Vma6 (d) = no E. coli F-type ATPase equivalent; Vma8 (D) = γ; Vma4 (E) = δ; F = Vma7 (F) = ε; I = Vphl/stvl = a+b ?, and K = Vma3 (c) = c. Additionally, the yeast V-type ATPase has 3 dissimilar c-subunits: Vma3(c), Vmal1(c') and Vma6(c''), and three subunits, Vma13(H), Vma5(c) and Vma10(G) which are not found in either the A- or F-type ATPases. All of the yeast vacuolar ATPase subunits have an equivalent subunit in the V-type ATPases of clathrin-coated vesicles of higher eukaryotes.

Eukaryotic V-type ATPases acidify Golgi-derived vesicles, clathrin-coated vesicles, synaptic vesicles, liposomes, and plant vacuoles and function in protein trafficking, receptor-mediated endocytosis, neurotransmitter release, pH regulation, waste management, pro-hormone processing, protein degradation, etc (Kane, 2006). They also function in the entry of various pathogenic agents, including many envelope viruses, like influenza virus, and toxins, like anthrax toxin. Plasma membrane V-ATPases function in renal pH homeostasis, bone resorption and sperm maturation, and various disease processes, including renal tubular acidosis, osteopetrosis, and tumor metastasis (Toei et al., 2010). There are 13 subunits, 8 (A-H) in V1 and 5 (a, c, c', c'', d and e). The c-subunits are arranged in a ring with the a-subunit on the outside of the ring. The proton channel may be at the a/c interface, and c rotates relative to a when ATP is hydrolyzed and H+ is translocated. Rotation of V-type ATPases has been demonstrated (Imamura et al., 2003). Two important mechanisms of regulating V-ATPase activity in vivo are reversible dissociation of the V1 and V0 domains and changes in coupling efficiency of proton transport and ATP hydrolysis (Cipriano et al. 2008). V-type ATPase proteolipids can form symmetrical 6-membered rings as is true for gap junction sheets from Nephrops norvegicus which are formed by a protein identical to the 4 TMS V-ATPase c-subunit. A 14th subunit, Ac45, associated with V0, is found in some mammalian tissues. The crystal structure of the central axis DF complex of a prokaryotic V-ATPase has been solved (Saijo et al., 2011).

In mammalian cells, most of the V-ATPase subunits exist in multiple isoforms which are often expressed in a tissue specific manner. Isoforms of one of the V(0) subunits (subunit a) have been shown to possess information that targets the V-ATPase to distinct cellular destinations. Mutations in isoforms of subunit a lead to the human diseases osteopetrosis and renal tubular acidosis. The Vesicular proton pump (V-ATPase) in nerve terminals following exocytosis continues to pump, promoting neurotransmitter uptake via endocytosis (Tabares and Betz, 2010). A number of mechanisms are employed to regulate V-ATPase activity in vivo, including reversible dissociation of the V(1) and V(0) domains, control of the tightness of coupling of proton transport and ATP hydrolysis, and selective targeting of V-ATPases to distinct cellular membranes. Isoforms of subunit a are involved in regulation both via the control of coupling and via selective targeting (Toei et al., 2010).

The V-ATPase ring contains three different subunits, c, c' and c'' and is therefore probably asymmetric if two or all three are present. In the yeast vacuolar ATPase, C (VMA3p) and C' (VMA11p) are 4 TMS proteins with N- and C-termini in the vacuolar lumen, but C'' (VMA16p) is a 5 TMS protein with N-terminus in the cytosol and the C-terminus in the lumen (Flannery et al., 2004). Althought TMHMM predicts 7TMSs for the a subunit (P32563) of the yeast (S. cerevisiae) V-type ATPase, Wang et al (2008) provide evidence for an eight transmembrane helix model in which the C-terminus is located on the cytoplasmic side of the membrane. By angular reconstitution from electron microscopic images, a 21 Å resolution structure shows an asymmetric protein ring with two small openings on the lumenal side and one large opening on the cytoplasmic side. The central hole on the lumenal side is covered by a globular protein while the cytoplasmic opening is covered by two elongated proteins (Wilkens and Forgac, 2001). Evolution of the hexameric transmembrane ring of the eukaryotic V-ATPase proton pump has been investigated (Finnigan et al., 2012).

In the reversible coupled rotatory mechanism for ATP-hydrolysis driven H+ transport, the coupling scheme is now basically complete. During rotation of single molecules of F1, phosphate release drives the last 40° of the 120° step, and the 40° rotation accompanies reduction of the affinity for phosphate. Moreover, the affinity for ADP decreases with rotation, and thus, ADP release contributes part of energy for rotation (Adachi et al., 2007; Senior, 2007). Surprisingly, Uchihashi et al. (2011), using high speed atomic force microscopy, have shown that the F1 ATPase exhibits rotary catalysis in the absence of the rotor.

The rotary proton- and sodium-translocating ATPases are reversible molecular machines present in all cellular life forms that couple ion movement across membranes with ATP hydrolysis or synthesis. Sequence and structural comparisons of F- and V-type ATPases have revealed homology between their catalytic and membrane subunits, but not between the subunits of the central stalk that connects the catalytic and membrane components. It has been proposed that these ATPases originated from membrane protein translocases which evolved from RNA translocases (Mulkidjanian et al., 2007). The Na+-pumping ATP synthase of Acetobacterium woodii has an unusual feature: its membrane-embedded rotor is a hybrid made of F and V-like subunits in a stoichiometry of 9:1, apparently not variable with the growth conditions (Schmidt et al., 2009).

Bacterial operons for F(1)F(0)-ATP synthase typically include an uncI gene encodes a small hydrophobic protein. When Suzuki et al. (2007) expressed a hybrid F(1)F(0) (F(1) from thermophilic Bacillus PS3 and Na+-translocating F(0) from Propionigenium modestum) in E. coli cells, they found that uncI derived from P. modestum was indispensable to produce active enzyme; without uncI, c-subunits in F(1)F(0) existed as monomers but not as a functional c(11)-ring. A plasmid containing only uncI and the c-subunit gene produced c(11)-ring, but a plasmid containing only the c-subunit gene did not. Direct interaction of the UncI protein with c-subunits was demonstrated. Na+ induced dissociation of His-tagged UncI protein from the c(11)-ring but not from c-monomers. Thus, UncI is a chaperone-like protein that assists the c(11)-ring assembly from the c-monomers in the membrane (Suzuki et al., 2007). Ozaki et al., (2008) have confirmed these observations. The halotolerant cyanobacterium, Aphanothece halophytica, contains an Na+-dependent F1F0-ATP synthase with a potential role in salt-stress tolerance (Soontharapirakkul et al., 2011).

The prokaryotic V-ATPase of Enterococcus hirae, closely related to the eukaryotic enzymes, provides a unique opportunity to study ion translocation by V-ATPases because it transports Na+ ions, which are easier to detect by x-ray crystallography and radioisotope experiments (Murata et al., 2008). The purified rotor ring (K-ring) of the E. hirae V-ATPase binds one Na+ ion per K-monomer with high affinity, which is competitively inhibited by Li+ or H+. The K-ring structure was determined at 2.8 A in the presence of Li+. Association and dissociation rates of the Na+ to and from the purified K-ring were extremely slow compared with the Na+ translocation rate estimated from the enzymatic activity, suggesting that interaction with the stator subunit (I-subunit) is essential for Na+ binding to and release from the K-ring.

Subunit a of the vacuolar H+-ATPases is an integral membrane 100kDa subunit, thought to contribute to and leave buried carboxyl groups on the proteolipid subunits (c, c' and c'') during proton translocation. Subunit a contains a large N-terminal cytoplasmic domain followed by a C-terminal domain containing eight transmembrane (TM) helices. TM7 contains a buried arginine residue (Arg-735) that is essential for proton transport and is located on a helical face that interacts with the proteolipid ring (Toei et al., 2011). Residues important for proton transport are located on the cytoplasmic half of TM7 and TM8 and the luminal half of TM3, TM4 and TM7. The cytoplasmic hemi-channel is located at the interface of TM7 and TM8 of subunit a and the proteolipid ring, whereas the luminal hemi-channel is located within subunit a at the interface of TM3, TM4 and TM7.

Rotary ATPases/synthases from Thermus thermophilus and Enterococcus hirae are maintained intact with membrane and soluble subunit interactions preserved in vacuum. Mass spectra reveal subunit stoichiometries and the identity of tightly bound lipids within the membrane rotors. Moreover, subcomplexes formed in solution and gas phases reveal the regulatory effects of nucleotide binding on both ATP hydrolysis and proton translocation. Consequently, specific lipid and nucleotide binding can be linked with distinct regulatory roles (Zhou et al., 2011).

Rotations of F1-ATPase occurs reversibly in discrete 120° steps by precisely controlling both the external torque and the chemical potential of ATP hydrolysis. Toyabe et al. (2011) found that the maximal work performed by F1-ATPase per 120° step is nearly equal to the thermodynamic maximal work that can be extracted from a single ATP hydrolysis event under a broad range of conditions. Their results support a nearly 100% free-energy transduction efficiency and a tight mechanochemical coupling.

The ability of c-rings to rotate within the F(o) complex derives from the interplay between the ion-binding sites and their nonhomogenous microenvironment (Pogoryelov et al., 2010). Pogoryelov et al. (2010) demonstrated how the thermodynamic stability of the so-called proton-locked state is maximized by the lipid membrane. By contrast, a hydrophilic environment at the a-subunit-c-ring interface appears to unlock the binding-site conformation and promotes proton exchange with the surrounding solution. Rotation thus occurs as c-subunits stochastically alternate between these environments, directionally biased by the electrochemical transmembrane gradient.

 

The generalized transport reaction for F-type, V-type and A-type ATPases is:

nH+ (in) [or nNa+ (in)] + ATP nH+ (out) [or nNa+ (out)] + ADP + Pi.

 

References associated with 3.A.2 family:

Abrahams, J.P., A.G.W. Leslie, R. Lutter, and J.E. Walker. (1994). Structure at 2.8 Ċ resolution of F1-ATPase from bovine heart mitochondria. Nature 370: 621-628. 8065448
Adachi, K., K. Oiwa, T. Nishizaka, S. Furuike, H. Noji, H. Itoh, M. Yoshida, and K. Kinosita Jr. (2007). Coupling of rotation and catalysis in F(1)-ATPase revealed by single-molecule imaging and manipulation. Cell. 130: 309-321. 17662945
Anraku, Y. (1996). Structure and function of the yeast vacuolar membrane H+-ATPase. In: Handbook of Biological Physics, vol. 2, W.N. Konings, H.R. Daback and J.S. Lolkema (Eds.), Elsevier Science B.V., pp. 93-109.
Balabaskaran Nina, P., N.V. Dudkina, L.A. Kane, J.E. van Eyk, E.J. Boekema, M.W. Mather, and A.B. Vaidya. (2010). Highly divergent mitochondrial ATP synthase complexes in Tetrahymena thermophila. PLoS Biol 8: e1000418. 20644710
Blair, A., L. Ngo, J. Park, I.T. Paulsen, and M.H. Saier, Jr. (1996). Phylogenetic analyses of the homologous transmembrane channel-forming proteins of the F0F1-ATPases of bacteria, chloroplasts and mitochondria. Microbiology 142: 17-32. 8581162
Bowman, B.J., M.E. McCall, R. Baertsch, and E.J. Bowman. (2006). A model for the proteolipid ring and bafilomycin/concanamycin-binding site in the vacuolar ATPase of Neurospora crassa. J. Biol. Chem. 281: 31885-31893. 16912037
Brandt, K., D.B. Müller, J. Hoffmann, C. Hübert, B. Brutschy, G. Deckers-Hebestreit, and V. Müller. (2013). Functional production of the Na+ F1F(O) ATP synthase from Acetobacterium woodii in Escherichia coli requires the native AtpI. J. Bioenerg. Biomembr. 45: 15-23. 23054076
Cipriano, D.J., Y. Wang, S. Bond, A. Hinton, K.C. Jefferies, J. Qi, and M. Forgac. (2008). Structure and regulation of the vacuolar ATPases. Biochim. Biophys. Acta. 1777: 599-604. 18423392
Deckers-Hebestreit, G. and K. Altendorf. (1996). The F0F1-type ATP synthases of bacteria: structure and function of the F0 complex. Ann. Rev. Microbiol. 50: 791-824. 8905099
Dettmer, J., A. Hong-Hermesdorf, Y.D. Stierhof, and K. Schumacher. (2006). Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18: 715-730. 16461582
Dimroth, P., H. Wang, M. Grabe, and G. Oster. (1999). Energy transduction in the sodium F-ATPase of Propionigenium modestum. Proc. Natl. Acad. Sci. USA 96: 4924-4929. 10220395
Elston, T., H. Wang, and G. Oster. (1998). Energy transduction in ATP synthase. Nature 391: 510-513. 9461222
Ferguson, S.A., S. Keis, and G.M. Cook. (2006). Biochemical and Molecular Characterization of a Na+-Translocating F1F0-ATPase from the Thermoalkaliphilic Bacterium Clostridium paradoxum. J. Bacteriol. 188(14): 5045-5054.
Finnigan, G.C., V. Hanson-Smith, T.H. Stevens, and J.W. Thornton. (2012). Evolution of increased complexity in a molecular machine. Nature 481: 360-364. 22230956
Flannery, A.R., L.A. Graham, and T.H. Stevens. (2004). Topological characterization of the c, c', and c'' subunits of the vacuolar ATPase from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 279: 39856-39862. 15252052
Forgac, M. (1999). Structure and properties of the vacuolar (H+)-ATPases. J. Biol. Chem. 274: 12951-12954. 10224039
Gao, C., Y. Wang, B. Jiang, G. Liu, L. Yu, Z. Wei, and C. Yang. (2011). A novel vacuolar membrane H+-ATPase c subunit gene (ThVHAc1) from Tamarix hispida confers tolerance to several abiotic stresses in Saccharomyces cerevisiae. Mol Biol Rep 38: 957-963. 20526814
Goldsmith, E.J. (1996). Allosteric enzymes as models for chemomechanical energy transducing assemblies. FASEB J. 10: 702-708. 8635687
Harrison, M.A., J. Murray, B. Powell, Y.-I. Kim, M.E. Finbow, and J.B.C. Findlay. (1999). Helical interactions and membrane disposition of the 16-kDa proteolipid subunit of the vacuolar H+-ATPase analyzed by cysteine replacement mutagenesis. J. Biol. Chem. 274: 25461-25470. 10464277
Hilario, E. and J.P. Gogarten. (1998). The prokaryote-to-eukaryote transition reflected in the evolution of the V/F/A-ATPase catalytic and proteolipid subunits. J. Mol. Evol. 46: 703-715. 9608053
Hinton, A., S. Bond, and M. Forgac. (2009). V-ATPase functions in normal and disease processes. Pflugers Arch 457: 589-598. 18026982
Imamura, H., M. Nakano, H. Noji, E. Muneyuji, S. Ohkuma, M. Yoshida, and K. Yokoyama. (2003). Evidence for rotation of V1-ATPase. Proc. Natl. Acad. Sci. USA 100: 2312-2315. 12598655
Ishmukhametov, R.R., J.B. Pond, A. Al-Huqail, M.A. Galkin, and S.B. Vik. (2008). ATP synthesis without R210 of subunit a in the Escherichia coli ATP synthase. Biochim. Biophys. Acta. 1777(1): 32-38. 18068111
Jones, P.C., W. Jiang, and R.H. Fillingame. (1998). Arrangement of the multicopy H+-translocating subunit c in the membrane sector of the Escherichia coli F1F0 ATP synthase. J. Biol. Chem. 273: 17178-17185. 9642286
Kakinuma, Y., I. Yamato, and T. Murata. (1999). Structure and function of vacuolar Na+-translocating ATPase in Enterococcus hirae. J. Bioenerg. Biomemb. 31: 7-14. 10340844
Kane, P.M. (1999). Vacuolar ATPases: structure, function, assembly and biosynthesis. J. Bioenerg. Biomembr. 31: 1-83.
Kane, Patricia M. (2006).  The Where, When, and How of Organelle Acidification by the Yeast Vacuola H+ - ATPase.  Microbio. Molecular Bio. Rev. 70: 177-191.
Kartner, N., Y. Yao, A. Bhargava, and M.F. Manolson. (2013). Topology, glycosylation and conformational changes in the membrane domain of the vacuolar H+ -ATPase a Subunit. J. Cell. Biochem. [Epub: Ahead of Print] 23296946
Kato, S., M. Yoshida, and Y. Kato-Yamada. (2007). Role of the epsilon subunit of thermophilic F1-ATPase as a sensor for ATP. J. Biol. Chem. 282: 37618-37623. 17933866
Kinosita, K., Jr., R. Yasuda, H. Noji, S. Ishiwata, and M. Yoshida. (1998). F1-ATPase: a rotory motor made of a single molecule. Cell 93: 21-24. 9546388
Knight, A.J. and C.A. Behm. (2012). Minireview: the role of the vacuolar ATPase in nematodes. Exp Parasitol 132: 47-55. 21959022
Lau, W.C. and J.L. Rubinstein. (2012). Subnanometre-resolution structure of the intact Thermus thermophilus H+-driven ATP synthase. Nature 481: 214-218. 22178924
Long, J.C., S. Wang, and S.B. Vik. (1998). Membrane topology of subunit a of the F1F0 ATP synthase as determined by labeling of unique cysteine residues. J. Biol. Chem. 273: 16235-16240. 9632682
McMillan, D.G., S.A. Ferguson, D. Dey, K. Schröder, H.L. Aung, V. Carbone, G.T. Attwood, R.S. Ronimus, T. Meier, P.H. Janssen, and G.M. Cook. (2011). A1Ao-ATP synthase of Methanobrevibacter ruminantium couples sodium ions for ATP synthesis under physiological conditions. J. Biol. Chem. 286: 39882-39892. 21953465
Muhammed, Z., S. Arai, S. Saijo, I. Yamato, T. Murata, and A. Suenaga. (2012). Calculating the Na⁺ translocating V-ATPase catalytic site affinity for substrate binding by homology modeled NtpA monomer using molecular dynamics/free energy calculation. J Mol Graph Model 37: 59-66. 22622011
Mulkidjanian A.Y., K.S. Makarova, M.Y. Galperin, E.V. Koonin. (2007). Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nat Rev Microbiol. 5: 892-899. 17938630
Murata, T., I. Yamato, Y. Kakinuma, M. Shirouzu, J.E. Walker, S. Yokoyama, and S. Iwata. (2008). Ion binding and selectivity of the rotor ring of the Na+-transporting V-ATPase. Proc. Natl. Acad. Sci. USA 105: 8607-8612. 18559856
Müller, V., C. Ruppert, and T. Lemker. (1999). Structure and function of the A1A0-ATPases from methanogenic archaea. J. Bioenerg. 31: 15-27. 10340845
Nakamoto, R.K. (1996). Mechanisms of active transport in the F0F1 ATP synthase. J. Membr. Biol. 151: 101-111. 8661504
Nelson, N. and W.R. Harvey. (1999). Vacuolar and plasma membrane proton-adenosinetriphosphatases. Physiol. Rev. 79: 361-385. 10221984
Noji, H., R. Yasuda, M. Yoshida, and K. Kinosita, Jr. (1997). Direct observation of the rotation of F1-ATPase. Nature 386: 299-302. 9069291
Ouyang, Z., Z. Li, and X. Zhang. (2008). Cloning and sequencing of V-ATPase subunit d from mung bean and its function in passive proton transport. J. Bioenerg. Biomembr. 40: 569-576. 19194790
Owegi, M.A., D.L. Pappas, M.W. Finch, S.A. Bilbo, C.A. Resendiz, L.J. Jacquemin, A. Warrier, J.D. Trombley, K.M. McCulloch, K.L. Margalef, M.J. Mertz, J.M. Storms, C.A. Damin, and K.J. Parra. (2006). Identification of a domain in the V0 subunit d that is critical for coupling of the yeast vacuolar proton-translocating ATPase. J. Biol. Chem. 281: 30001-30014. 16891312
Ozaki, Y., T. Suzuki, Y. Kuruma, T. Ueda, and M. Yoshida. (2008). UncI protein can mediate ring-assembly of c-subunits of FoF1-ATP synthase in vitro. Biochem. Biophys. Res. Commun. 367: 663-666. 18182163
Perzov, N., V. Padler-Karavani, H. Nelson, and N. Nelson. (2001). Features of V-ATPases that distinguish them from F-ATPases. FEBS Lett. 504: 223-228. 11532458
Pisa, K.Y., C. Weidner, H. Maischak, H. Kavermann, and V. Müller. (2007). The coupling ion in the methanoarchaeal ATP synthases: H+ vs. Na+ in the A(1)A(o) ATP synthase from the archaeon Methanosarcina mazei Gö1. FEMS Microbiol. Lett. 277: 56-63. 17986085
Pisa, K.Y., H. Huber, M. Thomm, and V. Müller. (2007b). A sodium ion-dependent A1AO ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus. FEBS J. 274: 3928-3938. 17614964
Pogoryelov, D., A. Krah, J.D. Langer, &.#.2.1.4.;. Yildiz, J.D. Faraldo-Gómez, and T. Meier. (2010). Microscopic rotary mechanism of ion translocation in the F(o) complex of ATP synthases. Nat Chem Biol 6: 891-899. 20972431
Rahlfs, S. and V. Müller. (1997). Sequence of subunit c of the Na+-translocating F1F0 ATPase of Acetobacterium woodii: proposal for determinants of Na+ specificity as revealed by sequence comparisions. FEBS Lett. 404: 269-271. 9119076
Rahlfs, S., S. Aufurth, and V. Müller. (1999). The Na+-F1F0-ATPase operon from Acetobacterium woodii operon structure and presence of multiole copies of atpE which encode proteolipids of 8- and 18-kDa. J. Biol. Chem. 274: 33999-34004. 10567365
Rastogi, V.K. and M.E. Girvin. (1999). Structural changes linked to protein translocation by subunit C of the ATP synthase. Nature 402: 263-268. 10580496
Ruppert, C., H. Kavermann, S. Wimmers, R. Schmid, J. Kellermann, F. Lottspeich, H. Huber, K.O. Stetter, and V. Müller. (1999). The proteolipid of the A1A0 ATP synthase from Methanococcus jannaschii has six predicted transmembrane helices but only two proton-translocating carboxyl groups. J. Biol. Chem. 274: 25281-25284. 10464251
Saijo, S., S. Arai, K.M. Hossain, I. Yamato, K. Suzuki, Y. Kakinuma, Y. Ishizuka-Katsura, N. Ohsawa, T. Terada, M. Shirouzu, S. Yokoyama, S. Iwata, and T. Murata. (2011). Crystal structure of the central axis DF complex of the prokaryotic V-ATPase. Proc. Natl. Acad. Sci. USA 108: 19955-19960. 22114184
Sambongi, Y., Y. Iko, M. Tanabe, H. Omote, A. Iwamoto-Kihara, I. Ueda, T. Yanatcida, Y. Wada, and M. Futai. (1999). Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. Science 286: 1722-1723. 10576736
Schmidt, S., E. Biegel, and V. Müller. (2009). The ins and outs of Na+ bioenergetics in Acetobacterium woodii. Biochim. Biophys. Acta. 1787: 691-696. 19167341
Schulenberg, B., R. Aggeler, J. Murray, and R.A. Capaldi. (1999). The γε-c subunit interface in the ATP synthase of Escherichia coli. cross-linking of the epsilon subunit to the c subunit ring does not impair enzyme function, that of gamma to c subunits leads to uncoupling. J. Biol. Chem. 274: 34233-34237. 10567396
Schwem, B.E. and R.H. Fillingame. (2006). Cross-linking between helices within subunit a of Escherichia coli ATP synthase defines the transmembrane packing of a four-helix bundle. J. Biol. Chem. 281: 37861-37867. 17035244
Senior, A.E. (2007). ATP synthase: motoring to the finish line. Cell 130: 220-221. 17662937
Solioz, M. and K. Davies. (1994). Operon of vacuolar-type Na+-ATPase of Enterococcus hirae. J. Biol. Chem. 269: 9453-9459. 8144530
Soontharapirakkul, K., W. Promden, N. Yamada, H. Kageyama, A. Incharoensakdi, A. Iwamoto-Kihara, and T. Takabe. (2011). Halotolerant cyanobacterium Aphanothece halophytica contains an Na+-dependent F1F0-ATP synthase with a potential role in salt-stress tolerance. J. Biol. Chem. 286: 10169-10176. 21262962
Suzuki, T., Y. Ozaki, N. Sone, B.A. Feniouk, and M. Yoshida. (2007). The product of uncI gene in F1Fo-ATP synthase operon plays a chaperone-like role to assist c-ring assembly. Proc. Natl. Acad. Sci. U.S.A. 104(52):20776-20781. 18083842
Tabares, L. and B. Betz. (2010). Multiple functions of the vesicular proton pump in nerve terminals. Neuron. 68: 1020-1022. 21172605
Takase, K., S. Kakinuma, I. Yamato, K. Konishi, K. Igarashi, and Y. Kakinuma. (1994). Sequencing and characterization of the ntp gene cluster for vacuolar-type Na+-translocating ATPase of Enterococcus hirae. J. Biol. Chem. 269: 11037-11044. 8157629
Toei M., Saum R. and Forgac M. (2010). Regulation and isoform function of the V-ATPases. Biochemistry. 49(23):4715-23. 20450191
Toei, M., S. Toei, and M. Forgac. (2011). Definition of membrane topology and identification of residues important for transport in subunit a of the vacuolar ATPase. J. Biol. Chem. 286: 35176-35186. 21832060
Toyabe, S., T. Watanabe-Nakayama, T. Okamoto, S. Kudo, and E. Muneyuki. (2011). Thermodynamic efficiency and mechanochemical coupling of F1-ATPase. Proc. Natl. Acad. Sci. USA 108: 17951-17956. 21997211
Uchihashi, T., R. Iino, T. Ando, and H. Noji. (2011). High-speed atomic force microscopy reveals rotary catalysis of rotorless F₁-ATPase. Science 333: 755-758. 21817054
Velours, J., C. Stines-Chaumeil, J. Habersetzer, S. Chaignepain, A. Dautant, and D. Brèthes. (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. 21868388
Vollmar M., Schlieper D., Winn M., Buchner C. and Groth G. (2009). Structure of the c14 rotor ring of the proton translocating chloroplast ATP synthase. J Biol Chem. 284(27):18228-35. 19423706
Wang, Y., M. Toei, and M. Forgac. (2008). Analysis of the Membrane Topology of Transmembrane Segments in the C-terminal Hydrophobic Domain of the Yeast Vacuolar ATPase Subunit a (Vph1p) by Chemical Modification. J. Biol. Chem. 283: 20696-20702. 18508769
Weber, J. and A.E. Senior. (1997). Catalytic mechanism of F1-ATPase. Biochim. Biophys. Acta 1319: 19-58. 9107315
Wieczorek, H., D. Brown, S. Grinstein, J. Ehrenfeld, and W.R. Harvey. (1999). Animal plasma membrane energization by protein-motive V-ATPases. BioEssays 21: 637-648. 10440860
Wilkens, S. and M. Forgac (2001). Three-dimensional structure of the vacuolar ATPase proton channel by electron microscopy. J. Biol. Chem. 276: 44064-44068. 11533034
Xu, T. and M. Forgac. (2000). Subunit D (Vma8p) of the yeast vacuolar H+-ATPase plays a role in coupling of proton transport and ATP hydrolysis. J. Biol. Chem. 275: 22075-22081. 10801866
Yamada, H., Y. Moriyama, M. Maeda, and M. Futai. (1996). Transmembrane topology of Escherichia coli H+-ATPase (ATP synthase) subunit a. FEBS Lett. 390: 34-38. 8706824
Yokoyama, K., S. Ohkuma, H. Taguchi, T. Yasunaga, T. Wakabayashi, and M. Yoshida. (2000). V-Type H+-ATPase/synthase from a thermophilic eubacterium, Thermus thermophilus. J. Biol. Chem. 275: 13955-13961. 10788522
Zhou, M., N. Morgner, N.P. Barrera, A. Politis, S.C. Isaacson, D. Matak-Vinković, T. Murata, R.A. Bernal, D. Stock, and C.V. Robinson. (2011). Mass spectrometry of intact V-type ATPases reveals bound lipids and the effects of nucleotide binding. Science 334: 380-385. 22021858