Novel features of the rotary catalytic mechanism revealed in the structure of yeast F1 ATPase

  title={Novel features of the rotary catalytic mechanism revealed in the structure of yeast F1 ATPase},
  author={Venkataraman Kabaleeswaran and Neeti Puri and John E. Walker and Andrew G W Leslie and David M. Mueller},
  journal={The EMBO Journal},
The crystal structure of yeast mitochondrial F1 ATPase contains three independent copies of the complex, two of which have similar conformations while the third differs in the position of the central stalk relative to the α3β3 sub‐assembly. All three copies display very similar asymmetric features to those observed for the bovine enzyme, but the yeast F1 ATPase structures provide novel information. In particular, the active site that binds ADP in bovine F1 ATPase has an ATP analog bound and… 
The structure of F1-ATPase from Saccharomyces cerevisiae inhibited by its regulatory protein IF1
The structure of F1-ATPase from Saccharomyces cerevisiae inhibited by the yeast IF1 has been determined and provides further evidence of sequential product release, with the phosphate and the magnesium ion released before the ADP molecule.
Asymmetric Structure of the Yeast F1 ATPase in the Absence of Bound Nucleotides*
The crystal structure of nucleotide-free yeast F1 ATPase has been determined and the adenine-binding pocket of the βTP subunits is disrupted in the apoenzyme, suggesting that the βDP subunit is responsible for unisite catalytic activity.
Crystal Structures of Mutant Forms of the Yeast F1 ATPase Reveal Two Modes of Uncoupling*
The analysis identifies two mechanisms of structural uncoupling: one in which the empty catalytic site is altered and in doing so, apparently disrupts substrate (phosphate) binding, and a second where the steric hindrance predicted between γLeu83 and βDP residues, Leu-391 and Glu-395, is reduced allowing rotation of the γ-subunit with less impedance.
Correlation between the conformational states of F1-ATPase as determined from its crystal structure and single-molecule rotation
F1-ATPase chimera F1 showed a catalytic dwell pause in every turn because of the slowed ATP hydrolysis of β(E190D/E391C), indicating that the crystal structure represents the catalytic dwelling state and that βDP is the catalytically active form.
Structural evidence of a new catalytic intermediate in the pathway of ATP hydrolysis by F1–ATPase from bovine heart mitochondria
The molecular description of the mechanism of F1–ATPase is based mainly on high-resolution structures of the enzyme from mitochondria, coupled with direct observations of rotation in bacterial enzymes, and has captured another intermediate in the catalytic cycle, which helps to define the order of substrate release.
Structure of the ATP synthase catalytic complex (F1) from Escherichia coli in an auto-inhibited conformation
The crystal structure of the ATP synthase catalytic complex (F1) from Escherichia coli described here reveals the structural basis for autoinhibition by one of its rotary stalk subunits, and adopts a heretofore unknown, highly extended conformation that inserts deeply into the central cavity of the enzyme.
The six steps of the F1-ATPase rotary catalytic cycle
These findings provide a structural basis for the entire F1-ATPase rotary catalysis cycle and identify a putative phosphate-releasing tunnel that indicates how ADP and phosphate releasing steps are coordinated.
Structure of the c10 Ring of the Yeast Mitochondrial ATP Synthase in the Open Conformation
It is proposed that this new structure represents the functionally open form of the c subunit, which facilitates proton loading and release, and is a consequence of the amphiphilic nature of the crystallization buffer.
Crystal structure of A3B3 complex of V-ATPase from Thermus thermophilus
The A3B3 subcomplex structure provides the first molecular insight at the catalytic and non‐catalytic interfaces, which was not possible in the structures of the separate subunits alone and highlights the presence of a cluster composed of key hydrophobic residues, which are essential for ATP hydrolysis by V‐ATPases.
Crystal structures of the ATP-binding and ADP-release dwells of the V1 rotary motor
The crystal structures for two other dwell states obtained by soaking nucleotide-free V1 crystals in ADP are presented and a V1-ATPase rotational mechanism model is proposed, based on these and previous findings.


The structure of the central stalk in bovine F1-ATPase at 2.4 Å resolution
The central stalk in ATP synthase is made of γ, δ and ɛ subunits in the mitochondrial enzyme, and with crystals of F1-ATPase inhibited with dicyclohexylcarbodiimide, the complete structure was revealed.
The Structure of the Chloroplast F1-ATPase at 3.2 Å Resolution*
The structure probably represents an inactive latent state of the ATPase, which is unique to chloroplast and cyanobacterial enzymes, and probably represents the C-terminal domain of the γ-subunit.
The structure of bovine F1-ATPase complexed with the peptide antibiotic efrapeptin.
Efrapeptin appears to inhibit F1-ATPase by blocking the conversion of subunit beta E to a nucleotide binding conformation, as would be required by an enzyme mechanism involving cyclic interconversion of catalytic sites.
On the structure of the stator of the mitochondrial ATP synthase
The structure of most of the peripheral stalk, or stator, of the F‐ATPase from bovine mitochondria, determined at 2.8 Å resolution, contains residues 79–183, 3–123 and 5–70 of subunits b, d and F6,
A perspective of the binding change mechanism for ATP synthesis 1
  • P. Boyer
  • Chemistry
    FASEB journal : official publication of the Federation of American Societies for Experimental Biology
  • 1989
Research from various laboratories gives support to the binding change mechanism in which energy from proton translocation serves principally to promote release of tightly bound ATP, with sequential participation of three catalytic sites.
How azide inhibits ATP hydrolysis by the F-ATPases.
The structure of bovine F1-ATPase determined at 1.95-A resolution with crystals grown in the presence of ADP, 5'-adenylyl-imidodiphosphate, and azide explains the stimulatory effect of azide on ATP-sensitive potassium channels by enhancing the binding ofADP.
The Binding Mechanism of the Yeast F1-ATPase Inhibitory Peptide
A model is proposed that suggests that IF1 binds rapidly, but loosely to F1 with two or three catalytic sites filled, and is then locked in the enzyme during catalytic hydrolysis of ATP.
The 2.8-A structure of rat liver F1-ATPase: configuration of a critical intermediate in ATP synthesis/hydrolysis.
In the structure of the rat liver F1-ATPase, determined to 2.8-A resolution in the presence of physiological concentrations of nucleotides, all three beta subunits contain bound nucleotide and adopt similar conformations, which suggests a mechanism of ATP synthesis/hydrolysis in which configurations of the enzyme with three bound nucleotide play an essential role.
Rapid hydrolysis of ATP by mitochondrial F1-ATPase correlates with the filling of the second of three catalytic sites.
  • Y. Milgrom, R. L. Cross
  • Chemistry, Biology
    Proceedings of the National Academy of Sciences of the United States of America
  • 2005
It is concluded that ATP binding to a second catalytic site is sufficient to support rapid rates of catalysis.