ATP Synthesis by F0F1-ATP Synthase Independent of Noncatalytic Nucleotide Binding Sites and Insensitive to Azide Inhibition

Bald, Dirk; Amano, Toyoki; Muneyuki, Eiro; Pitard, Bruno; Rigaud, Jean‐Louis; Kruip, Jochen; Hisabori, Toru; Yoshida, Masasuke; Shibata, Masaki

doi:10.1074/jbc.273.2.865

Cited by 69 publications

(60 citation statements)

References 34 publications

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“…Azide also inhibits the ATP hydrolase activity of the mitochondrial F-ATPase but not its synthetic activity. It has a similar effect on F-ATPases in eubacteria and chloroplasts (4)(5)(6)(7). Like the other respiratory complexes, the F-ATPase is embedded in the inner membranes of mitochondria.…”

mentioning

confidence: 68%

“…In the structure of N 3 Ϫ -F 1 , azide stabilizes this ADP-inhibited state and helps to prevent the conversion of the ␤ DP tight binding site to the ␤ E conformation accompanied by ADP release. Because the rotation of the ␥-subunit in the synthetic direction expels ADP from that site (28), synthesis of ATP by the F 1 F o -ATPase is not inhibited by either ADP⅐Mg 2ϩ or azide (4). During hydrolysis, it appears that the energy provided by the binding of an ATP molecule does not always provide sufficient energy to expel ADP, and azide enhances the inhibitory effect of ADP.…”

Section: ͚H͚i͉i(h) ϫ I(h)i͉͚͞h͚ii(h)i Where I(h)mentioning

confidence: 99%

“…Another explanation that has been advanced to explain the inhibitory effect of azide is that it blocks cooperation between catalytic sites (26,27). Rotation of the ␥-subunit in the synthetic direction in an F 1 -ATPase complex inhibited with ADP and azide expels them from the enzyme (28), and ADP and azide do not inhibit ATP synthesis (4). As shown here, in the structure of F 1 -ATPase at 1.9-Å resolution, the bound azide is associated with ADP in the ␤ DP catalytic site.…”

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confidence: 99%

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How azide inhibits ATP hydrolysis by the F-ATPases

Bowler

Montgomery

Leslie

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

228

180

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In the structure of bovine F1-ATPase determined at 1.95-Å resolution with crystals grown in the presence of ADP, 5 -adenylylimidodiphosphate, and azide, the azide anion interacts with the ␤-phosphate of ADP and with residues in the ADP-binding catalytic subunit, ␤DP. It occupies a position between the catalytically essential amino acids, ␤-Lys-162 in the P loop and the ''arginine finger'' residue, ␣-Arg-373, similar to the site occupied by the ␥-phosphate in the ATP-binding subunit, ␤TP. Its presence in the ␤DP-subunit tightens the binding of the side chains to the nucleotide, enhancing its affinity and thereby stabilizing the state with bound ADP. This mechanism of inhibition appears to be common to many other ATPases, including ABC transporters, SecA, and DNA topoisomerase II␣. It also explains the stimulatory effect of azide on ATP-sensitive potassium channels by enhancing the binding of ADP.mitochondria ͉ oxidative phosphorylation ͉ inhibition ͉ mechanism

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mentioning

confidence: 68%

Section: ͚H͚i͉i(h) ϫ I(h)i͉͚͞h͚ii(h)i Where I(h)mentioning

confidence: 99%

mentioning

confidence: 99%

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How azide inhibits ATP hydrolysis by the F-ATPases

Bowler

Montgomery

Leslie

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

228

180

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“…During the preparation of this report, an interesting paper by Bald et al was published (45). They reconstituted the mutant F o F 1 -ATPase, which lacks nucleotide binding to the noncatalytic site, into liposomes with bR and examined lightdriven ATP synthesis.…”

Section: Inactivation Of V 1 -Atpase May Be Caused By Entrapment Of Imentioning

confidence: 99%

V-ATPase of Thermus thermophilus Is Inactivated during ATP Hydrolysis but Can Synthesize ATP

Yokoyama

Muneyuki

Amano

et al. 1998

Journal of Biological Chemistry

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The ATP hydrolysis of the V 1 -ATPase of Thermus thermophilus have been investigated with an ATP-regenerating system at 25°C. The ratio of ATPase activity to ATP concentration ranged from 40 to 4000 M; from this, an apparent K m of 240 ؎ 24 M and a V max of 5.2 ؎ 0.5 units/mg were deduced. An apparent negative cooperativity, which is frequently observed in case of F 1 -ATPases, was not observed for the V 1 -ATPase. Interestingly, the rate of hydrolysis decayed rapidly during ATP hydrolysis, and the ATP hydrolysis finally stopped. Furthermore, the inactivation of the V 1 -ATPase was attained by a prior incubation with ADP-Mg. The inactivated V 1 -ATPase contained 1.5 mol of ADP/mol of enzyme.Difference absorption spectra generated from addition of ATP-Mg to the isolated subunits revealed that the A subunit can bind ATP-Mg, whereas the B subunit can (3), clathrin-coated vesicles (4), chromaffine granules (5), and the central vacuoles of yeast (6). They are responsible for vacuolar acidification, which plays an important role in a number of cellular processes (1). V o V 1 -ATPases are also found in the plasma membranes of most archea (7-9) and some kinds of eubacteria (10 -12). Several studies indicate that the physiological role of V o V 1 -ATPases of some archea and the thermophilic eubacterium Thermus thermophilus is ATP synthesis coupled to proton flux across the plasma membranes (7,9,(13)(14)(15). Precise understanding of V o V 1 -ATPases would allow the comparison to F o F 1 -ATPases and the elucidation of the common essential mechanism for the coupling of proton translocation across a membrane with ATP formation. However, several problems, such as the difficulty of obtaining a large amount of pure enzyme from vacuolar membranes and an unstable V 1 moiety (17), have limited our investigation of enzymatic properties of V o V 1 -ATPases.T. thermophilus, originally isolated from a hot spring in Japan, is thermophilic, obligatory aerobic, Gram-negative, and chemoheterotrophic eubacterium (25). Its respiratory chain may include energy coupling Site I (26). This bacterium has a large amount of the V o V 1 -ATPase on the plasma membrane, instead of F o F 1 -ATPase (15).In contrast to eukaryotic equivalents, the V 1 moiety of T. thermophilus is easily detached from the membranes using chloroform treatment and ATPase-active stable complex can be obtained in large amounts (10). Throughout this manuscript, the V 1 moiety from T. thermophilus is refereed to V 1 -ATPase.

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“…Indeed, their result can be used to refine the potential curves. Mg⅐ADP inhibition is not a serious problem in ATP synthesis direction because the catalytic site is always occupied by ATP before entering this angular region (74,75).…”

Section: The Subunit Ensures Energy Coupling In the Synthesis Directionmentioning

confidence: 99%

Making ATP

Xing

Liao

Oster

2005

Proc. Natl. Acad. Sci. U.S.A.

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We present a mesoscopic model for ATP synthesis by F1Fo ATPase. The model combines the existing experimental knowledge of the F1 enzyme into a consistent mathematical model that illuminates how the stages in synthesis are related to the protein structure. For example, the model illuminates how specific interactions between the ␥, , and ␣3␤3 subunits couple the Fo motor to events at the catalytic sites. The model also elucidates the origin of ADP inhibition of F1 in its hydrolysis mode. The methodology we develop for constructing the structure-based model should prove useful in modeling other protein motors.ATP synthase ͉ ATP synthesis ͉ F1Fo ATPase M echanochemical proteins convert the energy of chemical bonds into mechanical forces and, in the case of one ancient protein, vice versa. ATP synthase (also called F 1 F o ATPase) uses the energy stored in a transmembrane electrochemical gradient to synthesize ATP. ATP synthase is unique in combining two rotary molecular motors in one protein so that the assembly can either synthesize ATP or pump ions across a membrane, depending on which motor dominates. The F 1 F o system has been studied extensively both experimentally and theoretically, so the basic operating principles of both the F o and F 1 motors are understood at near molecular detail (e.g. refs. 1-5).Modeling of mechanoenzymes takes three general approaches. Molecular dynamics (MD) attempts to account for the motion of every atom, and sometimes the surrounding water and other chemical species. Kinetic models represent the transitions between small numbers of chemical (Markov) states. Markov-FokkerPlanck (MFP) models lie somewhere between the atomic detail of MD and the phenomenology of kinetic models (6). These models describe the geometric motion along a few ''collective coordinates'' that describe the protein's major conformational movements. Motion is driven by forces derived from a set of potential functions assigned to each coordinate, with Markov jumps between the potentials corresponding to chemical transitions. MFP models generalize kinetic models by replacing the discrete kinetic states with potential functions representing collective spatial coordinates. The distinctions between, and relative advantages of, each of these models have been discussed in detail elsewhere (6). A prominent feature of MFP models is that structural and dynamical information can be included in the models without the computational load of MD models. In this work, we take this approach. We emphasize that MFP models complement MD and kinetic models; each has its proper place in understanding a mechanochemical system as complex as a protein motor.In constructing an MFP model, the central step is to identify the important degrees of freedom that must be treated explicitly, and construct a set of free energy potential surfaces with these degrees of freedom as geometrical coordinates. Identification of the collective coordinates can often be inferred from the protein structure and its biochemistry (7). Normal mode analysis also c...

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ATP Synthesis by F0F1-ATP Synthase Independent of Noncatalytic Nucleotide Binding Sites and Insensitive to Azide Inhibition

Cited by 69 publications

References 34 publications

How azide inhibits ATP hydrolysis by the F-ATPases

How azide inhibits ATP hydrolysis by the F-ATPases

V-ATPase of Thermus thermophilus Is Inactivated during ATP Hydrolysis but Can Synthesize ATP

Making ATP

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