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J. Biol. Chem., Vol. 279, Issue 48, 50591-50600, November 26, 2004

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Crystal Structure of Bacterial Inorganic Polyphosphate/ATP-glucomannokinase

INSIGHTS INTO KINASE EVOLUTION^*

Takako Mukai, Shigeyuki Kawai, Shigetarou Mori, Bunzo Mikami¶, and Kousaku Murata¶||

From the Department of Basic and Applied Molecular Biotechnology, Division of Food and Biological Science, Graduate School of Agriculture, Kyoto University, Uji, Kyoto 611-0011, Japan and Laboratory of Food Quality Design and Development, Division of Agronomy and Horticultural Science, Graduate School of Agriculture, Kyoto University, Uji, Kyoto 611-0011, Japan

Received for publication, July 19, 2004 , and in revised form, September 7, 2004.

	ABSTRACT

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 
Inorganic polyphosphate (poly(P)) is a biological high energy compound presumed to be an ancient energy carrier preceding ATP. Several poly(P)-dependent kinases that use poly(P) as a phosphoryl donor are known to function in bacteria, but crystal structures of these kinases have not been solved. Here we present the crystal structure of bacterial poly(P)/ATP-glucomannokinase, belonging to Gram-positive bacterial glucokinase, complexed with 1 glucose molecule and 2 phosphate molecules at 1.8 Å resolution, being the first among poly(P)-dependent kinases and bacterial glucokinases. The poly(P)/ATP-glucomannokinase structure enabled us to understand the structural relationship of bacterial glucokinase to eucaryotic hexokinase and ADP-glucokinase, which has remained a matter of debate. These comparisons also enabled us to propose putative binding sites for phosphoryl groups for ATP and especially for poly(P) and to obtain insights into the evolution of kinase, particularly from primordial poly(P)-specific to ubiquitous ATP-specific proteins.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 
ATP participates universally in the transfer and storage of free energy in biological systems as the most common phosphoryl donor for kinases. Some Gram-positive bacteria such as Arthrobacter sp. strain KM and Mycobacterium tuberculosis possess inorganic polyphosphate (poly(P))¹-dependent kinases that use poly(P) instead of ATP as the phosphoryl donor (1–4). Poly(P) is a biopolymer of several (up to thousands) orthophosphate residues linked by a high energy phosphoanhydride bond approximately equivalent to that of ATP (5). Poly(P)-dependent kinases consist of poly(P)-glucokinase (GK) (1), poly(P)/ATP-GK (2), poly(P)/ATP-glucomannokinase (GMK) (3), and poly(P)/ATP-NAD kinase (4); the first three catalyze phosphorylation of glucose, the first step of glycolysis, and the last catalyzes that of NAD, the last step in NADP biosynthesis. Note that poly(P)-GK is poly(P)-specific, although poly(P)/ATP-type enzymes use poly(P) and ATP. Although the primary structures of these poly(P)-dependent kinases were determined (1–4), the lack of a crystal structure has prevented us from clarifying the poly(P)-utilizing mechanism of these unique kinases. Poly(P)-dependent kinases have ATP-specific partners, and a knowledge of the crystal structure of poly(P)-dependent kinase may aid in understanding the structural relationship of poly(P)-dependent kinase to the ubiquitous ATP-specific kinase, i.e. to understand structural determinants enabling poly(P)/ATP-type and poly(P)-specific type kinases to use poly(P), ATP-specific kinase to reject poly(P) and poly(P)-specific kinase to reject ATP. Such understanding would lend insights into the evolutionary relationship of poly(P)-dependent kinase to ubiquitous ATP-specific kinase, where relationships are also of interest, since poly(P) could be formed and participate in ATP synthesis under ancient prebiotic conditions and serve as a possible ancient energy carrier preceding ATP (5).

Among poly(P)-dependent kinases, GMK, isolated from the Gram-positive bacterium Arthrobacter sp. strain KM, is a monomer with 30 kDa that phosphorylates glucose and mannose with preference for glucose through the use of poly(P) and ATP (3). The primary structure of GMK shows high homology with those of poly(P)- and poly(P)/ATP-GKs and other Gram-positive bacterial GKs but little with those of Gram-negative bacterial GKs and eucaryotic hexokinases (HKs), except for a few conserved motifs (3, 6). HK shows a broad specificity for hexose, whereas GK has high specificity for glucose (7, 8). Although crystal structures of eucaryotic HKs from yeast (9–13), human (14–19), rat (20), and parasite Schistosoma mansoni (20) have been solved, no crystal structure has been reported for Gram-positive or negative bacterial GKs. Hence, the crystal structural and evolutionary relationships between bacterial GK and eucaryotic HK have remained matters of debate (7, 8). Crystal structures of archaeal ADP-GKs from Thermococcus litoralis (21), Pyrococcus horikoshii (22), and Pyrococcus furiosus (23) definitely show that ADP-GK is distinguished from eucaryotic HK. ADP-GKs use ADP, whereas eucaryotic HK and bacterial GK, except for poly(P)-dependent GK, are regarded as using ATP but not poly(P).

Here we show the crystal structure of GMK complexed with one glucose and two phosphate () molecules, the first among poly(P)-dependent kinases and bacterial GKs. Crystal structural analysis for GMK provides evidence for close crystal structural and evolutionary relationships between bacterial GK and eucaryotic HK and details of substrate-binding sites, especially for putative poly(P)-binding sites, enabling us to obtain insights into the evolution of kinases, particularly from primordial poly(P)-specific to ubiquitous ATP-specific proteins.

	EXPERIMENTAL PROCEDURES

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 
Purification, Crystallization, and X-ray Diffraction—GMK was expressed from the GMK gene at NdeI-XhoI sites of pET-21b (Novagen) as a recombinant-enzyme in Escherichia coli BL21(DE3) cells (Novagen) in LB medium by inducing isopropyl--D-thiogalactopyranoside (0.4 mM) as described elsewhere (4) but at 20 °C for 24 h with sufficient aeration. The expressed recombinant GMK was purified using the same procedure as for native-GMK (3), except that, after ammonium sulfate precipitation, the supernatant was directly applied to a butyl Toyopearl (Tosoh) column and eluted using the gradient in ammonium sulfate from 30 to 0%. After dialysis, eluted GMK was purified by a hydroxyl apatite (Nacalai Tesque) column using the gradient in potassium phosphate from 10 to 600 mM. Active fractions contained the purified GMK and were homogeneous on SDS-PAGE (24). GMK was crystallized by hanging-drop vapor diffusion method as described elsewhere (25). The solution of a crystallization drop was prepared on a siliconized coverslip by mixing 3 µl of protein solution (10 mg/ml GMK and 10 mM glucose in 10 mM potassium phosphate, pH 7.0) with 3 µl of mother liquor composed of 2.0 M ammonium sulfate, 2% (v/v) polyethylene glycol 400, 0.1 M Hepes, pH 8.0.

Crystals were soaked in several heavy atom derivative solutions composed of 1 mM UO₂Ac₂, 10 mM AgNO₃, 10 mM GdCl₃, 1 mM HgCl₂, 10 mM K₂Pt(CN)₄, 2 mM TmCl₂, and 1 mM EuCl₃ for 20–60 min at 20 °C. Derivative solutions were prepared in a mother liquor, but 0.1 M Tris-HCl, pH 7.0 (for UO₂Ac₂) and 0.1 M sodium acetate, pH 4.9 (for the remainder), were included instead of 0.1 M Hepes, pH 8.0. Diffraction data for the native crystal of GMK up to 2.8 Å and derivative crystals at about 3.0 Å were collected with a Bruker Hi-Star multiwire area detector at 20 °C using CuK radiation generated by a MAC Science M18XHF rotating anode generator and were processed with SADIE and SAINT software packages (Bruker). Diffraction data for further refinement up to 1.8 Å was collected using synchrotron radiation at a wave-length of 0.9 Å at the BL-41XU station of SPring-8 in Hyogo, Japan. Obtained data was processed, merged, and scaled using program package HKL 2000 (DENZO and SCALEPACK) (26) and truncated with the CCP4 program package.

Structure Determination and Refinement—The crystal structure of GMK was determined by multiple isomorphous replacement (MIR). Major sites of heavy atoms were determined by interpretation of difference Patterson maps calculated at 3.0 Å of resolution. Additional heavy atom sites were determined from difference Fourier maps. The phase refinement was performed with program PHASES (27). Results of heavy atom refinement and phasing by MIR at 3.0 Å of resolution are listed in Table I. An electron density map was made with the solvent-flattened (28) MIR phase using data from 15.0 to 3.0 Å, and the map was averaged using noncrystallographic symmetry. The initial model built using an averaged MIR map at 3.0 Å of resolution was refined by stimulated annealing with molecular dynamics using X-PLOR (29) and CNS (30). Then, several rounds of restrained least squares refinement followed by manual model building were conducted to improve the initial model to the R-factor of 19.2% (free R-factor = 26.2%) at 2.8 Å of resolution using the TURBO-FRODO (AFMB-CNRS) program on a Silicon Graphics Octan computer. The model was further refined by using diffraction data up to 1.8 Å with simulated annealing with molecular dynamics using a CNS program package. Several rounds of restrained least squares refinement to a resolution of 1.8 Å followed by manual model building were conducted. Water molecules were incorporated when the difference in density was more than 3.0 above the mean and the 2 F_o - F_c map showed a density of more than 1.0 . The final model was determined with an R-factor of 19.1% (free R-factor = 22.0%) at 50.0–1.8 Å resolution.

	RESULTS

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 
Structure Determination and Quality of Refined Model— Recombinant-GMK purified to homogeneity showed the same molecular structure (30 kDa, monomer) and N-terminal sequence and almost the same kinetic parameters as those of native-GMK (3). GMK was crystallized in the presence of glucose, phosphate, and sulfate, and prismatic colorless crystals of the GMK grew to a maximum 0.1 mm in 2 weeks at 20 °C. The GMK crystal belongs to space group P2₁2₁2₁ with unit cell dimensions of a = 65.21, b = 82.52, and c = 102.06 Å, and the solvent content was 49%, assuming 2 molecules in an asymmetric unit (25). The structure of GMK was determined by MIR. Refinement statistics for MIR phasing and the final model are given in Tables I and II.

Overall Structure of GMK Complexed with Glucose and Phosphates—The refined model consisted of 506 residues, 373 water, 2 glucose, and 4 phosphate molecules per 2 molecules of GMK (GMK-A/-B) in an asymmetric unit. Note that it was unclear if phosphate or sulfate was contained in GMK due to the similar molecular structures of the 2 anions and due to the presence of the 2 anions in the crystallization solution. To avoid confusion, we regard anions as phosphate A and B in this article.

A ribbon model of the overall crystal structure of GMK together with one bound glucose and two bound phosphates (phosphate A and B) in the interdomain cleft is shown in Fig. 1a, and the topology of secondary structure elements of GMK is shown in Fig. 1b. One molecule of GMK, which is active as a monomer (3), consisted of two globular domains. The two domains are called N and C domains and are connected by two segments between SA5 and H3 and between SB5 and H9 (Fig. 1, a and b). Each domain consisted of three layers (//). The N domain consisted of H1:H2/SA3:SA2:SA1:SA4:SA5/H9, and the C domain of H3/SB3:SB2:SB1:SB4:SB5/H4:H5:H6:H7:H8. The 5-stranded mixed -sheets in N and C domains showed order 32145 with strand 2 antiparallel to the rest of the sheet. The overall topology of the N domain was similar to that of the C domain (Fig. 1b). The primary structure of the N domain (residues 11–122) also showed homology with that of the C domain (residues 123–263), 18% identity, and 48% similarity over 116 residues, as calculated by ClustalW. The superimposition of the N domain on the C domain gave the root mean square deviation of 1.1 Å with 41 C within 2.0 Å (Fig. 1c). Taken together, we propose that the two domains stem from the duplication of one primordial domain.

View larger version (27K): [in this window] [in a new window]   FIG. 1. Structures of GMK. a, stereo view of ribbon model of GMK with glucose (red), phosphate A (orange), and phosphate B (yellow). b, topology of secondary elements of GMK. The -helix (H) and -strand (SA and SB for N and C domains) are designated by numbers from the N-terminal. c, stereo view of a C backbone trace of superimposed structures of N-domain (residues 11–122) (green) and C-domain (residues 139–246) (yellow-green) of GMK.

Glucose- and Phosphates-binding Sites of GMK—Ligands (glucose and phosphates) were refined with fractional occupancies of 1.0. The average B-factor for glucose was 13.4 Ų and lower than the average for all atoms (24.6 Ų), but B-factors for phosphate-A (46.3 Ų), especially for phosphate-B (64.3 Ų), were higher than the average for all atoms. The electron density of the glucose O1 atom was observed for the -anomer configuration (Fig. 2a). Selected contacts between GMK and ligands are listed in Table III. The O1 atom of phosphate B interacted with the Arg⁴² NH₂ atom in GMK-A but with water 466 in GMK-B due to different directions in the side chain of Arg⁴² between GMK-A and GMK-B (data not shown). The binding sites of GMK with bound glucose, phosphate A, and phosphate B and their interactions with GMK are shown in Fig. 2b.

View larger version (58K): [in this window] [in a new window]   FIG. 2. Substrate-binding sites. a, electron density map of glucose bound to GMK. Glucose oxygens are numbered. b, binding sites of GMK with glucose (red), phosphate A (orange), and phosphate B (yellow). Hydrogen bonds are indicated by dotted lines. c, binding sites of C-HKI with glucose (red) and ADP (orange) (PDB accession code 1DGK [PDB] ) (18). Interactions of residues with the -phosphoryl group are not indicated since this group was not located at the proper site (18).

	DISCUSSION

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

Overall Structures of GMK, Eucaryotic HK, and ADP-GK— The structural relationship of bacterial GK to eucaryotic HK and ADP-GK has not been understood. As mentioned above, however, the crystal structure of GMK appears to be related, at least to those of eucaryotic HK. We, therefore, attempted to compare GMK and eucaryotic HK in detail.

Eucaryotic HKs consist of isozymes (e.g. mammalian (human) HK I-VI) (7, 8). HK I (100 kDa) consists of N- and C-terminal halves (50 kDa), which have primary and tertiary structures, and substrate-binding sites, resembling each other and those of other 50 kDa eucaryotic HKs (human HK IV, also called GK, S. mansoni HK, and yeast HK PI and PII) (9–20). The C-terminal half of human HK I (C-HKI) has catalytic activity, but the N-terminal half is inactive (14–18). The tertiary structure of C-HKI (residues 525–913) complexed with glucose and ADP (18) was chosen as representative of eucaryotic HK for comparison with GMK. The tertiary structure of C-HKI consists of two domains, called large and small, between which glucose- and ADP-binding sites are formed, and shows "closed conformation" observed in eucaryotic HKs complexed with glucose (9–20) (Fig. 3a).

View larger version (28K): [in this window] [in a new window]   FIG. 3. Structures of C-HKI. a, ribbon model of C-HKI (residues 525–913) with glucose (red) and ADP (orange) (PDB accession code 1DGK [PDB] ) (18). b, topology of secondary elements of C-HKI (residues 525–913) as in Fig. 1b, but SA and SB correspond to small and large domains. The flexible subdomain (residues 766–811) is boxed.

View larger version (38K): [in this window] [in a new window]   FIG. 4. Stereo view of a C backbone trace of superimposed structures of GMK (light green) and C-HKI (light pink).

View larger version (44K): [in this window] [in a new window]   FIG. 5. Alignment of primary structures of GMK and C-HKI. Secondary elements are indicated based on Fig. 1b and Fig. 3b. Similarity was calculated by ClustalW using the primary structure of C-HKI, from which all additional elements in the structure of C-HKI were removed, and specified as dots and plus symbols (lower and higher similarities). Residues specified in the text are boxed in brown. Flexible subdomains (residues 766–811) in C-HKI are boxed in blue.

View larger version (56K): [in this window] [in a new window]   FIG. 6. Ribbon model of ADP-GK from P. furiosus with glucose (red) (PDB accession code 1UA4 [PDB] ) (23).

View larger version (55K): [in this window] [in a new window]   FIG. 7. Putative pentapolyphosphate-binding site in GMK. a, stereo view of binding sites of GMK with glucose (red), phosphate A (orange), phosphate B (yellow), and putatively bound pentapolyphosphate (yellow green). Interactions of residues with phosphate A and B are indicated by dotted lines. Two phosphoryl groups in pentapolyphosphate were superimposed on phosphate A and B with manual fitting. b, stereo view of a ribbon model of GMK with bound glucose and putative pentapolyphosphate as in a.

Residues in GMK, Thr²² and Lys²⁵, interacting with phosphate B (Fig. 2b) were conserved in the primary structures of C-HKI as Thr⁵³⁶ and Arg⁵³⁹ (Fig. 5) and in other eucaryotic HKs (13), Gram-negative and -positive bacterial GKs including poly(P)- and poly(P)/ATP-GKs (1, 3, 6), and even some proteins in the ASKHA superfamily (40, 44). The sequence around residues highly conserved in these proteins is called a "phosphate-1" motif (44). The phosphate-1 motif is regarded as conserved in ATP-utilizing proteins in the ASKHA superfamily such as acetate and sugar kinases, heat shock protein, and actin, and plays a significant role in interaction with ATP (40, 44). Thr⁵³⁶, Arg⁵³⁹, and Asp⁵³² in this motif of C-HKI are proposed to interact with phosphoryl groups of ATP via Mg²⁺ and water (18). Note that all crystal structure-solved proteins containing this motif except for GMK are ATP-specific, and we could find no crystal structures of these ATP-specific proteins showing the direct interaction of this motif with phosphate, suggesting that some structural elements in these ATP-specific proteins, not existing in GMK, possibly prevent this motif from binding to poly(P).

Where does adenine-ribose (adenosine) of ATP bind to GMK? Gly⁷⁴⁷ in C-HKI, interacting with ribose of ADP, appears to correspond slightly to Ala¹⁸⁵ in GMK in primary structural alignment (Fig. 5). Thr⁷⁸⁴, Lys⁷⁸⁵, Ser⁷⁸⁸, and Thr⁸⁶³ (interacting with adenine of ADP) in C-HKI were not conserved in GMK, however (Fig. 5). Note that Thr⁷⁸⁴, Lys⁷⁸⁵, and Ser⁷⁸⁸ in C-HKI are located in the flexible subdomain not found in GMK. Although the primary structure of poly(P)-GK (1) was highly conserved with those of GMK and poly(P)/ATP-GK (2), poly(P)-GK could not use ATP. Identifying the correct adenosine-binding site of GMK would aid in understanding why poly(P)-GK rejects ATP. To specify adenine- and poly(P)-binding sites in GMK, a crystallographic study of GMK complexed with poly(P) or ATP is currently in progress.

Insights into Kinase Evolution—The GMK crystal structure presented here led us to assume evolutionary relationships of bacterial GK with eucaryotic HK and archaeal ADP-GK. Tertiary structural and evolutionary relationships between bacterial GK and eucaryotic HK are currently matters of debate (7, 8), whereas relationships between eucaryotic HK and archaeal ADP-GK are distinctly diverse (7, 8, 21–23). Our study showed the close structural relationship between bacterial GK and eucaryotic HK from the points of overall tertiary structure (Fig. 4), binding sites for substrates (glucose and phosphoryl group) (Fig. 2, b and c), and primary structure (Fig. 5), and hence, we propose that eucaryotic HK and bacterial GK diverged from a common poly(P)-specific primordial protein as described below. The structural relationship between bacterial GK and ADP-GK is apparently diverse (Fig. 1a and Fig. 6), and hence, the evolutionary relationship would also be diverse, agreeing with the accepted idea that the structural and evolutionary relationship between eucaryotic HK and archaeal ADP-GK is distinctly diverse (7, 8, 21–23). It appeared that the common ancestor of bacterial GK and eucaryotic HK evolved into eucaryotic HK by acquiring several elements, including a flexible subdomain (Fig. 5), to satisfy physiological criteria required in eucaryotes (organisms containing mitochondria), whereas ancestors evolved into bacterial GK without such acquisitions. Eucaryotic HK appears to evolve to be suitable for organisms containing mitochondria, since (i) eucaryotic amitochondriate protist (without mitochondria), Trichomonas vaginalis, carries only Gram-negative bacterial GK (6), not eucaryotic HK, and (ii) human HK I interacts with mitochondria, permitting direct exchange of adenine nucleotides between the mitochondrial matrix and the HK active site (45, 46).

Crystal structural and evolutionary relationships of poly(P)-dependent kinase with ubiquitous ATP-specific kinase are also interesting and significant but remain to be clarified due to the lack of crystal structural information on poly(P)-dependent kinase. Here we present the crystal structure of this type of kinase and propose the putative poly(P)-binding site of GMK, which contains the phosphate-1 motif well conserved in ATP-specific proteins. Taking into account that (i) adenine-interacting residues in C-HKI are located in the flexible subdomain not found in GMK (Fig. 5), (ii) our proposition that eucaryotic HK acquired the flexible subdomain, interacting with adenine, during evolution, and finally (iii), GMK takes a fold similar to those of ATP-specific ASKHA proteins containing the phosphate-1 motif, we propose that ATP-specific proteins containing the phosphate-1 motif may have evolved from a primordial poly(P)-specific GMK-like protein and may acquire the ability to use ATP and lose that to use poly(P) during evolution, which agrees with the suggestion that poly(P) is an energy carrier preceding ATP (5).

	FOOTNOTES

 
The atomic coordinates and structure factors (code 1WOQ [PDB] ) have been deposited in the Protein Data Bank, Research Collaboratory for Structural Bioinformatics, Rutgers University, New Brunswick, NJ (http://www.rcsb.org/).

^* This work was supported in part by Grant-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology of Japan 15780212 and by the Program for Promotion of Basic Research Activities for Innovative Biosciences (PROBRAIN). 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.

^¶ These authors contributed equally to this work.

^|| To whom correspondence should be addressed. Tel.: 81-774-38-3766; Fax: 81-774-38-3767; E-mail: kmurata{at}kais.kyoto-u.ac.jp.

¹ The abbreviations used are: poly(P), polyphosphate; GK, glucokinase; GMK, poly(P)/ATP-glucomannokinase; HK, hexokinase; MIR, multiple isomorphous replacement.

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TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS DISCUSSION REFERENCES

 

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