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J. Biol. Chem., Vol. 278, Issue 38, 36013-36016, September 19, 2003

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Isolated Subunit of Thermophilic F₁-ATPase Binds ATP^*

Yasuyuki Kato-Yamada  and Masasuke Yoshida 

From the Chemical Resources Laboratory, Tokyo Institute of Technology, 4259 Nagatsuta, Yokohama 226-8503, Japan

Received for publication, June 11, 2003 , and in revised form, July 1, 2003.

	ABSTRACT

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 
F₁-ATPase, a soluble part of the F₀F₁-ATP synthase, has subunit structure ₃₃ in which nucleotide-binding sites are located in the and subunits and, as believed, in none of the other subunits. However, we report here that the isolated subunit of F₁-ATPase from thermophilic Bacillus strain PS3 can bind ATP. The binding was directly demonstrated by isolating the subunit-ATP complex with gel filtration chromatography. The binding was not dependent on Mg²⁺ but was highly specific for ATP; however, ADP, GTP, UTP, and CTP failed to bind. The subunit lacking the C-terminal helical hairpin was unable to bind ATP. Although ATP binding to the isolated subunits from other organisms has not been detected under the same conditions, a possibility emerges that the subunit acts as a built in cellular ATP level sensor of F₀F₁-ATP synthase.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 
F₀F₁-ATPase/synthase (F₀F₁)¹ catalyzes ATP synthesis coupled with the proton flow across the membrane through mechanical rotation of the central shaft subunits relative to the surrounding stator subunits (1, 2). F₁ is the water-soluble portion of F₀F₁ and has ATP hydrolysis activity by itself. It consists of five kinds of subunits with a stoichiometry of ₃₃₁₁₁ in which the catalytic nucleotide-binding sites are located on the subunits and the non-catalytic nucleotide-binding sites are on the subunits. The subunit inserts its long coiled-coil helices into the central cavity of the ₃₃ cylinder (3), and ATP hydrolysis occurring in the ₃₃ drives rotation of the subunit along with the subunit that is associated with the subunit (reviewed in Ref. 2).

Responding to the varying energy supply for ATP synthesis in living organisms, the activity of F₀F₁ must be regulated. Eukaryotic organellar F₀F₁ has developed unique regulatory systems; mitochondrial F₀F₁ has a specific ATPase inhibitor protein and its cofactor proteins (4, 5), and chloroplast F₀F₁ is regulated by the reversible formation of a disulfide bond in the subunit (reviewed in Ref. 6). More ubiquitous is the inhibition by the subunit, which was noticed since the early stage of studies of ATP synthase (7–9). The subunit is a small subunit of 130–140 residues consisting of two distinct domains, an N-terminal -sandwich domain and a C-terminal helical hairpin domain (10, 11). Accumulating biochemical and structural studies have revealed that the subunit can adopt at least two different conformational states in F₁ and F₀F₁, "down"-state and "up"-state (12–19). The structures of the isolated from Escherichia coli represent the down-state conformation that does not exhibit the inhibitory effect. The exact conformation of the upstate subunit in F₁ and F₀F₁ is not known, but it is certain that the C-terminal helical hairpin in the down state is opened in the up state (19) and comes in contact with the and subunits (20). The up-state exerts the inhibitory effect on ATP hydrolysis activity but, interestingly, not on ATP synthesis activity of F₀F₁ (21).

Several factors are known to induce the conformational transitions of the subunit. Illumination of thylakoid membranes resulted in the change of the arrangement of the subunit in chloroplast F₀F₁ as probed by the accessibility of the antibody against the subunit (22, 23). Also addition of ATP to F₁ stabilizes the down-state conformation of the subunit (17, 24). Since it has been thought that nucleotide-binding sites of F₀F₁ are exclusively located in and subunits and the mutant F₁ with incompetent nucleotide-binding sites on subunits still shows ATP-dependent conformational transition of the subunit (17), we have concluded that the ATP binding to the catalytic site(s) on the subunit(s) triggers the conformational transitions of the subunit. Here, however, we report that the isolated subunit of F₁ from thermophilic Bacillus strain PS3 (TF₁) has a binding site for ATP. This unexpected finding raises a new possibility that the subunit in F₀F₁ acts not only as a regulator of F₀F₁ but also as a sensor for cellular ATP level.

	EXPERIMENTAL PROCEDURES

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 
Construction of Expression Plasmids for Subunits—To obtain the wild-type subunit of TF₁, the expression plasmid pTE2 (14) and pET21c vector carrying TF₁ subunit gene (20) were used. The expression plasmid for the subunit of F₁ from E. coli (EF₁) was generated as follows. The gene for EF₁- subunit was amplified by PCR with two primers, one containing NdeI site and 5' region of EF₁- gene and the other containing complementary sequence to 3' region of EF₁- gene and HindIII site, using a plasmid containing E. coli F₀F₁ operon as a template. The resulting DNA fragment was digested with NdeI and HindIII and introduced into the respective sites of the pET21c expression vector (Novagen). The expression plasmid for the subunit of F₁ from Bacillus subtilis (BF₁) was generated by the same procedures by using genomic DNA of B. subtilis as a template for PCR. The expression plasmid for a mutant, Lys-109 to Ala (K109A), subunit of F₁ from Spinacia oleracea L. chloroplast (CF₁) was generated by the method of Kunkel et al. (25) from an expression plasmid for the wild-type CF₁- subunit, pMCE1 (26). DNA sequences were confirmed by DNA sequencing.

Purification of Recombinant Proteins—Wild-type and a truncated mutant (Val-90 to Stop) of TF₁- (^C) were purified as described (16). The subunits of EF₁ and BF₁ were expressed in E. coli BL21 (DE3) cells (26). EF₁- subunit was purified by the same method as used for the TF₁- subunit. BF₁- subunit was also purified by the same method except that flow-through fractions of the butyl-Toyopearl column chromatography were used because BF₁- subunit did not bind to the column. The isolation of the mutant (K109A) CF₁- subunit was carried out at 4 °C as follows. The cells were disrupted by sonication (S-250 Sonifier, Branson Ultrasonics, Japan), and the inclusion bodies were collected by a centrifugation at 8400 x g for 20 min. The precipitate was suspended in 50 mM Tris-HCl (pH 8), 1 mM EDTA, and 4% (v/v) Triton X-100. The mixture was mildly shaken for 30 min at room temperature and centrifuged at 8400 x g for 20 min. The washing was repeated 3 times. Then the precipitate was suspended in distilled water and centrifuged at 19,000 x g for 20 min. The precipitate was dissolved in 50 mM Tris-HCl (pH 8), 1 mM EDTA, and 6 M urea and was subjected to a DEAE-toyopearl column equilibrated with the same buffer. The flow-through was collected, and urea was removed by dialysis against 50 mM Tris-HCl (pH 8), and 1 mM EDTA. The solution was subjected to a butyl-Toyopearl column and eluted with the same conditions as used for TF₁- subunit purification. The mutant (K109A) CF₁- subunit, whose inhibitory effect on ATPase activity of CF₁ was unchanged, was used in the experiments. For simplicity, we call this mutant (K109A) CF₁- subunit as just CF₁- in this paper. Molecular masses of purified subunits examined by mass spectrography agreed with the values predicted from amino acid sequences (data not shown).

Preparation of Nucleotide-depleted TF₁-—The TF₁- subunits purified as above contained 0.3 to 1.1 mol/mol of bound ATP. To remove this bound ATP, TF₁- subunit was mixed with hexokinase (Roche Diagnostics) (15 units/ml) in 50 mM Tris-HCl buffer (pH 8), 100 mM KCl, 4 mM MgCl₂, and 200 mM glucose. The mixture was dialyzed against a 200-fold volume of the same buffer without hexokinase overnight at room temperature. Then the mixture was concentrated by a centrifugal ultrafiltration device (MWCO 5000K, Vivaspin, Vivascience) and subjected to a gel filtration HPLC column (Superdex 200HR 10/30, inner diameter 10 x 300 mm, Amersham Biosciences) equilibrated with 50 mM Tris-HCl (pH 8) and 100 mM KCl to remove hexokinase and glucose. The collected peak contained 0.06 mol of bound ATP/mol of (termed as (nd) for nucleotide-depleted subunit) and used in the experiments. As the subunits from other sources did not contain bound nucleotides, they were used for the gel filtration assay without such treatment.

Detection of ATP Binding to Subunit—TF₁-(nd) or subunits from other F₁-ATPase (25 µM) were preincubated with the indicated concentrations of nucleotides in 50 mM Tris-HCl buffer (pH 8), 100 mM KCl, and 4 mM MgCl₂ for 10 min at room temperature. Then the mixtures were subjected to a Sephadex G-25F (Amersham Biosciences) HPLC column (inner diameter 10 x 300 mm) at room temperature and eluted with 50 mM Tris-HCl buffer (pH 8), and 100 mM KCl at flow rate 1.5 ml/min. The elution of proteins was monitored by absorbance at 290 nm, and the elution of the nucleotides was monitored by absorbance at 260 nm. In the case when Mg²⁺ requirement was examined, MgCl₂ was omitted from the incubation buffer and 10 mM EDTA or 1,2-cyclohexanediaminetetraacetic acid (CyDTA) was included instead. For ADP, hexokinase (15 units/ml) and 200 mM glucose were included in the mixture during preincubation to remove the contaminated ATP in the commercial ADP.

Photoaffinity Labeling of Subunit by BzATP—TF₁-(nd) (5 µM) was incubated with 20 µM 3'(2')-O-(4-benzoyl)benzoyladenosine 5'-triphosphate (BzATP, Sigma) (27) for 10 min in 50 mM Tris-HCl (pH 8), 100 mM KCl, and 4 mM MgCl₂. UV irradiation was carried out with a UV transilluminator (CSF-10CF, Cosmo bio, Japan) with 5-cm spacing for 10 min. DTT (10 mM) was added after UV irradiation, and 30 µl of the reaction mixture was subjected to analysis with 15% SDS-PAGE. The proteins were stained with Coomassie Blue R-250.

Other Procedures—UV absorption spectra of TF₁- subunit were measured with a UV absorbance meter (V-550, Jasco, Japan) with a slit width at 5 nm. Protein concentrations were determined by the method of Bradford (28) using bovine serum albumin as a standard. For TF₁- subunit, the values of Bradford assays were corrected according to the quantitative amino acids analyses.

	RESULTS

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 
Unusual Absorption Spectrum of Purified TF₁-—We noticed that the UV absorption spectra of the TF₁- subunit isolated from expressing E. coli were unusual because the peak was 265 nm and magnitude was varied from preparation to preparation (Fig. 1). As the difference spectra among the preparations showed the peak around 262 nm, it was suspected that the TF₁- preparations might contain bound nucleotides. We denatured TF₁- by acid treatment, removed the denatured proteins, analyzed the supernatant fraction with HPLC as described (29), and found that the preparations indeed contained 0.3–1.1 mol of ATP per mol of subunit (data not shown). When the isolated TF₁- was incubated with hexokinase and glucose (see "Experimental Procedures"), the amount of the bound ATP decreased to 0.06 mol/mol of TF₁-, and the UV absorption spectrum of the thus treated TF₁-(nd) (Fig. 1) agreed roughly to the spectrum expected from the content of aromatic amino acid residues in TF₁- (two Tyrs and no Trp).

View larger version (20K): [in this window] [in a new window]   FIG. 1. UV absorption spectra of TF1- subunit. UV absorption spectra of different lots of TF1- preparations (25 µM) were measured. The difference spectra (lot 2 to lot 1) and that of 25 µM TF1-(nd) are also shown.

TF₁-(nd) Binds ATP—To know if TF₁-(nd) was able to bind ATP again, TF₁-(nd) was mixed with ATP, preincubated, and subjected to the gel filtration column chromatography. The TF₁- was eluted at 6.2 min, and the small peak of TF₁-(nd) without ATP preincubation seen in the elution profile monitored at 260 nm was attributed to the absorption of TF₁-(nd) itself (Fig. 2A). Elution of the TF₁-(nd):ATP (1:0.4) mixture showed the 6.2-min peak with increased height and no peak corresponding to the free ATP, indicating that all of the added ATP was associated to TF₁-(nd). The 6.2-min peak height was further increased for the elution of the TF₁-(nd):ATP (1:1) mixture but saturated for the 1:2 mixture elution in which the peak of free ATP appeared. These results suggest that TF₁-(nd) binds 1 mol of ATP and that the TF₁--ATP complex is stable as far as giving rise to an isolated peak in the gel filtration column chromatography. A notice should be added, however, that some fraction of the complex dissociated during chromatography because there was small tailing after the 6.2-min peak in the elution of the TF₁-(nd):ATP (1:1) mixture. Mg²⁺ was not required for ATP to bind to TF₁-(nd), because even when we omitted Mg²⁺ from the mixture and supplemented EDTA or CyDTA instead, ATP was still co-eluted with TF₁-(nd) at 6.2 min (Fig. 2B).

View larger version (16K): [in this window] [in a new window]   FIG. 2. Gel filtration analyses of the nucleotides binding to TF1- subunit. The mixtures of subunits (25 µM) and nucleotides at indicated molar ratios containing 4 mM Mg2+ (except for B) were incubated at room temperature, and binding of nucleotide to subunit was analyzed with a Sephadex G-25F HPLC column. Elutions monitored by absorbance at 260 nm are shown. subunit was eluted at 6.2 min (arrows). A, binding analysis of ATP to TF1-(nd). The mixtures with 1:0, 1:0.4, 1:1, and 1:2 TF1-(nd):ATP molar ratios were analyzed. B, binding analysis of Mg2+-free ATP to TF1-(nd). The TF1-(nd):ATP (1:1) mixtures in Mg2+-free buffer supplemented with 10 mM EDTA or CyDTA were analyzed. Elutions of TF1-(nd) only and the TF1-(nd): ATP (1:1) mixture with Mg2+ are also shown as thin lines for reference. C, binding analysis of the ADP, GTP, CTP, and UTP to TF1-(nd). The TF1-(nd):nucleotide (1:2) mixtures were analyzed. Elutions of TF1-(nd) only and the TF1-(nd):ATP (1:2) mixture are also shown as thin lines for reference. The vertical scale bar in A represents absorbance unit of 0.005 at 260 nm. Other experimental conditions are described under "Experimental Procedures."

Photoaffinity Label of TF₁- by BzATP—ATP binding to TF₁-(nd) was also confirmed by a different means. A photoaffinity ATP analog, BzATP, was added to the solution of TF₁-(nd) and irradiated by UV. As shown in Fig. 3, the irradiated TF₁-(nd) generated a new band in SDS-PAGE analysis (Fig. 3, arrowhead). This represents the TF₁-(nd) labeled by BzATP. The new band disappeared by addition of ATP, ensuring that BzATP competes for the same site with ATP.

View larger version (35K): [in this window] [in a new window]   FIG. 3. Photoaffinity labeling of TF1- subunit by BzATP. The TF1-(nd) was incubated with BzATP and irradiated with UV light. The reaction mixtures were subjected to SDS-PAGE analysis. Lane 1, TF1-(nd) without UV irradiation; lane 2, TF1-(nd) irradiated without nucleotides; lane 3, TF1-(nd) irradiated in the presence of 20 µM of BzATP; lane 4,TF1-(nd) irradiated in the presence of 20 µM BzATP and 200 µM ATP. A newly appeared band by irradiation in the presence of BzATP is marked with an arrowhead. Only the region around subunit bands is shown.

Specificity of Nucleotides That Bind to TF₁-—The bindings of ADP, GTP, UTP, and CTP were also tested by gel filtration chromatography. As shown in Fig. 2C, none of them changed the height of the 6.2-min peak of TF₁-(nd) but rather they were eluted as free nucleotides. Thus TF₁-(nd) only binds ATP but not other nucleotides under the examined conditions. This is in sharp contrast to the nucleotide binding specificity to the and subunits of F₁; ADP and GTP can bind to the and subunits (30, 31). The strict discrimination of ATP from ADP by TF₁- is indicative of a possible role of the subunit as a sensor for cellular ATP concentration.

TF₁-^C Did Not Bind ATP—It has been demonstrated that the C-terminally truncated TF₁-^C (Met¹–Val⁹⁰) is capable of mediating the binding of F₁ to F₀ to form F₀F₁ that catalyzes ATP-driven H⁺ pumping although it does not exert an inhibitory effect on ATPase activity (16). We examined the binding of ATP to the isolated TF₁-^C, but the binding was not detected (Fig. 4A). Therefore, the helical hairpin of the C-terminal domain is indispensable to generate the ATP-binding site on the subunit.

View larger version (17K): [in this window] [in a new window]   FIG. 4. Gel filtration analyses of the nucleotides binding to TF1-C and subunits from other sources. A, binding analysis of ATP to TF1-C. Elution of TF1-C only is shown as a reference. B–D, binding analysis of ATP to EF1-, BF1- and CF1-. The :ATP (1:2) mixtures were analyzed. Other conditions of analyses were the same as described in the legend of Fig. 2.

F₁- Subunits from Other Sources Did Not Bind ATP—Expecting that the ATP binding nature of F₁- would be common to wide range of organisms, we tested ATP binding to the isolated F₁- subunits from three sources as follows: a Gram-negative bacterium, E. coli; a Gram-positive bacterium, B. subtilis; and chloroplasts of the plant Spinacia oleracea L. However, none of them bound ATP under the conditions where TF₁- bound ATP (Fig. 4, B–D).

	DISCUSSION

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 
Since its isolation as the smallest subunit of F₁ 3 decade ago (32), the idea has never come to attention that the subunit has the ability to bind nucleotide. No typical nucleotide-binding motif has been found in the amino acid sequence of the subunit, and no typical nucleotide binding domain has been noticed in the three-dimensional structures of the subunit either as an isolated one or in the F₁ (11–19). However, now we know that the subunit, at least the one from thermophilic Bacillus, is an ATP-binding protein. It is surprising that such a small protein (14 kDa) can generate a very specific ATP-binding site in its structure, and probably TF₁- is one of the smallest proteins that bind nucleotide.

The finding raises an attractive possibility that the subunit of F₀F₁ senses the varying cellular ATP concentration, i.e. when ATP concentration is elevated, ATP binding to the subunit in the down state facilitates the conformational transition of the subunit in F₀F₁ from the up state, which is an ATP synthesis mode, to the down state, which is presumably the mode less favorable for ATP synthesis. In this hypothetical scenario, the subunit plays dual roles, sensing the ATP level in the cell and regulating the activity of F₀F₁ by conformational transition. However, apparently inconsistent with this hypothesis, the subunits from other sources do not bind ATP. Also, ATP binding to the subunit assembled in F₀F₁ (or F₁) has not been demonstrated yet. The affinity of ATP to the subunit in F₀F₁ is probably around the cellular ATP concentration, i.e. the order of mM, for effective sensing of cellular energy conditions. If so, detection of such weak binding might be difficult by usual binding measurements. The isolated TF₁- shows strong affinity to ATP probably only at temperatures much lower than the living temperature of the organism. Actually, ATP was dissociated from TF₁- rapidly at 50 °C.² We expect that the finding reported here will turn out to be the beginning of exploring a new regulation system of F₀F₁.

	FOOTNOTES

 
^* The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Supported by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists. Present address: Institute of Industrial Science, the University of Tokyo, 4-6-1 Komaba Meguro-ku, Tokyo 153-8505, Japan.

To whom correspondence should be addressed: Chemical Resources Laboratory, R-1, Tokyo Institute of Technology, 4259 Nagatsuta, Yokohama 226-8503, Japan. Tel.: 81-45-924-5233; Fax: 81-45-924-5277; E-mail: myoshida{at}res.titech.ac.jp.

¹ The abbreviations used are: F₀F₁, F₀F₁-ATPase/synthase; TF₁, F₁-ATPase from thermophilic Bacillus PS3, a soluble portion of F₀F₁; BF₁, F₁-ATPase from B. subtilis; CF₁, F₁-ATPase from S. oleracea L. chloroplast; EF₁, F₁-ATPase from E. coli; ^C, a mutant subunit of TF₁ truncated after Asp-89; TF₁-(nd), nucleotide-depleted wild-type TF₁- subunit; BzATP, 3'(2')-O-(4-benzoyl)benzoyladenosine 5'-triphosphate; CyDTA, 1, 2-cyclohexanediaminetetraacetic acid; HPLC, high performance liquid chromatography.

² Y. Kato-Yamada and M. Yoshida, unpublished results.

	ACKNOWLEDGMENTS

 
We thank K. Yamane at Tsukuba University for providing us the B. subtilis strain and M. Odaka at RIKEN Institute for quantitative amino acid analyses. We also thank Y.-H. Watanabe, S. P. Tsunoda, H. Taguchi, E. Azami, T. Amano, T. Hisabori, E. Muneyuki, and other members of our laboratory for their help and critical discussions.

	REFERENCES

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 

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