Abstract
Phosphoglycerate kinase (PGK) is indispensable during glycolysis for anaerobic glucose degradation and energy generation. Here we present comprehensive structure analysis of two putative PGKs from Bacillus anthracis str. Sterne and Campylobacter jejuni in the context of their structural homologs. They are the first PGKs from pathogenic bacteria reported in the Protein Data Bank. The crystal structure of PGK from Bacillus anthracis str. Sterne (BaPGK) has been determined at 1.68 Å while the structure of PGK from Campylobacter jejuni (CjPGK) has been determined at 2.14 Å resolution. The proteins’ monomers are composed of two domains, each containing a Rossmann fold, hinged together by a helix which can be used to adjust the relative position between two domains. It is also shown that apo-forms of both BaPGK and CjPGK adopt open conformations as compared to the substrate and ATP bound forms of PGK from other species.
Abbreviations
- BaPGK:
-
Phosphoglycerate kinase from Bacillus anthracis
- CjPGK:
-
Phosphoglycerate kinase from Campylobacter jejuni
- PGK:
-
Phosphoglycerate kinase
- ATP:
-
Adenosine triphosphate
- ADP:
-
Adenosine diphosphate
- 3PG:
-
3-Phospho-d-glycerate
- SAXS:
-
Small-angle X-ray scattering
- ORF:
-
Open reading frame
- HEPES:
-
2-[4-(2-Hydroxyethyl)piperazin-1-yl]ethanesulfonic acid
- TCEP:
-
Tris(2-carboxyethyl)phosphine-HCl
- TEV:
-
Tobacco etch virus
- EDTA:
-
Ethylenediaminetetraacetic acid
- PEG:
-
Polyethylene glycol
- LS-CAT:
-
Life Science Collaborative Access Team
- EMBL:
-
European Molecular Biology Laboratory
- SAD:
-
Single-wavelength anomalous diffraction
- TLS:
-
Translation/libration/screw
- PDB:
-
Protein Databank
- RMSD:
-
Root mean square deviation
- GBS:
-
Guillain–Barré syndrome
- NIAID:
-
National Institute of Allergy and Infectious Diseases
- CSGID:
-
Center of Structural Genomics for Infectious Disease
References
Riedel S (2005) Anthrax: a continuing concern in the era of bioterrorism. Proc (Bayl Univ Med Cent) 18:234–243
Poropatich KO, Walker CL, Black RE (2010) Quantifying the association between Campylobacter infection and Guillain–Barre syndrome: a systematic review. J Health Popul Nutr 28:545–552
Anderson WF (2009) Structural genomics and drug discovery for infectious diseases. Infect Disord Drug Targets 9:507–517
Chen L, Oughtred R, Berman HM, Westbrook J (2004) TargetDB: a target registration database for structural genomics projects. Bioinformatics 20:2860–2862
Blake CC, Rice DW (1981) Phosphoglycerate kinase. Philos Trans R Soc Lond B Biol Sci 293:93–104
Rao DR, Oesper P (1961) Purification and properties of muscle phosphoglycerate kinase. Biochem J 81:405–411
Axelrod B, Bandurski RS (1953) Phosphoglyceryl kinase in higher plants. J Biol Chem 204:939–948
Garfinkel L, Garfinkel D (1985) Magnesium regulation of the glycolytic pathway and the enzymes involved. Magnesium 4:60–72
VandeBerg JL (1985) The phosphoglycerate kinase isozyme system in mammals: biochemical, genetic, developmental, and evolutionary aspects. Isozymes Curr Top Biol Med Res 12:133–187
Vas M, Varga A, Graczer E (2010) Insight into the mechanism of domain movements and their role in enzyme function: example of 3-phosphoglycerate kinase. Curr Protein Pept Sci 11:118–147
Yon JM, Desmadril M, Betton JM, Minard P, Ballery N, Missiakas D, Gaillard-Miran S, Perahia D, Mouawad L (1990) Flexibility and folding of phosphoglycerate kinase. Biochimie 72:417–429
Flachner B, Kovari Z, Varga A, Gugolya Z, Vonderviszt F, Naray-Szabo G, Vas M (2004) Role of phosphate chain mobility of MgATP in completing the 3-phosphoglycerate kinase catalytic site: binding, kinetic, and crystallographic studies with ATP and MgATP. Biochemistry 43:3436–3449
Banks RD, Blake CC, Evans PR, Haser R, Rice DW, Hardy GW, Merrett M, Phillips AW (1979) Sequence, structure and activity of phosphoglycerate kinase: a possible hinge-bending enzyme. Nature 279:773–777
Lallemand P, Chaloin L, Roy B, Barman T, Bowler MW, Lionne C (2011) Interaction of human 3-phosphoglycerate kinase with its two substrates: is substrate antagonism a kinetic advantage? J Mol Biol 409:742–757
Zerrad L, Merli A, Schroder GF, Varga A, Graczer E, Pernot P, Round A, Vas M, Bowler MW (2011) A spring-loaded release mechanism regulates domain movement and catalysis in phosphoglycerate kinase. J Biol Chem 286:14040–14048
Cliff MJ, Bowler MW, Varga A, Marston JP, Szabo J, Hounslow AM, Baxter NJ, Blackburn GM, Vas M, Waltho JP (2010) Transition state analogue structures of human phosphoglycerate kinase establish the importance of charge balance in catalysis. J Am Chem Soc 132:6507–6516
Gondeau C, Chaloin L, Lallemand P, Roy B, Perigaud C, Barman T, Varga A, Vas M, Lionne C, Arold ST (2008) Molecular basis for the lack of enantioselectivity of human 3-phosphoglycerate kinase. Nucleic Acids Res 36:3620–3629
Aslanidis C, Dejong PJ (1990) Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res 18:6069–6074
Haun RS, Serventi IM, Moss J (1992) Rapid, reliable ligation-independent cloning of pcr products using modified plasmid vectors. Biotechniques 13:515–518
Eschenfeldt WH, Lucy S, Millard CS, Joachimiak A, Mark ID (2009) A family of LIC vectors for high-throughput cloning and purification of proteins. Methods Mol Biol 498:105–115
Stols L, Gu MY, Dieckman L, Raffen R, Collart FR, Donnelly MI (2002) A new vector for high-throughput, ligation-independent cloning encoding a tobacco etch virus protease cleavage site. Protein Expr Purif 25:8–15
Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307–326
Minor W, Cymborowski M, Otwinowski Z, Chruszcz M (2006) HKL-3000: the integration of data reduction and structure solution—from diffraction images to an initial model in minutes. Acta Crystallogr D 62:859–866
Sheldrick GM (2008) A short history of SHELX. Acta Crystallogr A 64:112–122
Otwinowski Z (1991) Isomorphous replacement and anomalous scattering. In: Wolf W, Evans PR, Leslie AGW (eds) Proceedings of the CCP4 study weekend. SERC Daresbury Laboratory, Warrington, pp 80–86
Cowtan KD, Main P (1993) Improvement of macromolecular electron-density maps by the simultaneous application of real and reciprocal space constraints. Acta Crystallogr D 49:148–157
Perrakis A, Morris R, Lamzin VS (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol 6:458–463
Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67:235–242
Terwilliger TC, Berendzen J (1999) Automated MAD and MIR structure solution. Acta Crystallogr D 55:849–861
Terwilliger T (2004) SOLVE and RESOLVE: automated structure solution, density modification, and model building. J Synchrotron Radiat 11:49–52
Terwilliger TC (2002) Automated structure solution, density modification and model building. Acta Crystallogr D 58:1937–1940
Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53:240–255
Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213–221
Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D 60:2126–2132
Painter J, Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D Biol Crystallogr 62:439–450
Lovell SC, Davis IW, Adrendall WB, de Bakker PIW, Word JM, Prisant MG, Richardson JS, Richardson DC (2003) Structure validation by C alpha geometry: phi, psi and C beta deviation. Proteins 50:437–450
Yang HW, Guranovic V, Dutta S, Feng ZK, Berman HM, Westbrook JD (2004) Automated and accurate deposition of structures solved by X-ray diffraction to the Protein Data Bank. Acta Crystallogr D 60:1833–1839
Glaser F, Pupko T, Paz I, Bell RE, Bechor-Shental D, Martz E, Ben-Tal N (2003) ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 19:163–164
Ponstingl H, Kabir T, Thornton JM (2003) Automatic inference of protein quaternary structure from crystals. J Appl Crystallogr 36:1116–1122
Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774–797
Zheng H, Chruszcz M, Lasota P, Lebioda L, Minor W (2008) Data mining of metal ion environments present in protein structures. J Inorg Biochem 102:1765–1776
Schrődinger L (2010) The PyMOL molecular graphics system, Version-1.3r1
Bond C (2003) TopDraw: a sketchpad for protein structure topology cartoons RID B-4094-2011. Bioinformatics 19:311–312
Davies GJ, Gamblin SJ, Littlechild JA, Dauter Z, Wilson KS, Watson HC (1994) Structure of the ADP complex of the 3-phosphoglycerate kinase from Bacillus stearothermophilus at 1.65 A. Acta Crystallogr D Biol Crystallogr 50:202–209
Auerbach G, Huber R, Grattinger M, Zaiss K, Schurig H, Jaenicke R, Jacob U (1997) Closed structure of phosphoglycerate kinase from Thermotoga maritima reveals the catalytic mechanism and determinants of thermal stability. Structure 5:1475–1483
Holm L, Rosenstrom P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38:W545–W549
Ye Y, Godzik A (2003) Flexible structure alignment by chaining aligned fragment pairs allowing twists. Bioinformatics 19(Suppl 2):ii246–ii255
Acknowledgments
The authors would like to thank David R. Cooper, Ivan G. Shabalin, Jing Hou and the members of the Center of Structural Genomics for Infectious Diseases for valuable comments and discussions. This research was funded with Federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under Contract No. HHSN272200700058C. Use of the Advanced Photon Source was supported by the U. S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract No. DE-AC02-06CH11357. Use of the LS-CAT Sector 21 was supported by the Michigan Economic Development Corporation and the Michigan Technology Tri-Corridor for the support of this research program (Grant 085P1000817).
Conflict of interest
None declared.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zheng, H., Filippova, E.V., Tkaczuk, K.L. et al. Crystal structures of putative phosphoglycerate kinases from B. anthracis and C. jejuni . J Struct Funct Genomics 13, 15–26 (2012). https://doi.org/10.1007/s10969-012-9131-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10969-012-9131-9