Crystal structures of putative phosphoglycerate kinases from B. anthracis and C. jejuni

  • Heping Zheng
  • Ekaterina V. Filippova
  • Karolina L. Tkaczuk
  • Piotr Dworzynski
  • Maksymilian Chruszcz
  • Przemyslaw J. Porebski
  • Zdzislaw Wawrzak
  • Olena Onopriyenko
  • Marina Kudritska
  • Sarah Grimshaw
  • Alexei Savchenko
  • Wayne F. Anderson
  • Wladek Minor
Short Communication

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.

Keywords

Carbohydrate degradation Glycolysis PGK Phosphoglycerate kinase Pathogenic organism Anthrax Gastroenteritis Guillain–Barré syndrome Rossmann fold Bacillus anthracis Campylobacter jejuni 

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

  1. 1.
    Riedel S (2005) Anthrax: a continuing concern in the era of bioterrorism. Proc (Bayl Univ Med Cent) 18:234–243Google Scholar
  2. 2.
    Poropatich KO, Walker CL, Black RE (2010) Quantifying the association between Campylobacter infection and Guillain–Barre syndrome: a systematic review. J Health Popul Nutr 28:545–552PubMedCrossRefGoogle Scholar
  3. 3.
    Anderson WF (2009) Structural genomics and drug discovery for infectious diseases. Infect Disord Drug Targets 9:507–517PubMedCrossRefGoogle Scholar
  4. 4.
    Chen L, Oughtred R, Berman HM, Westbrook J (2004) TargetDB: a target registration database for structural genomics projects. Bioinformatics 20:2860–2862PubMedCrossRefGoogle Scholar
  5. 5.
    Blake CC, Rice DW (1981) Phosphoglycerate kinase. Philos Trans R Soc Lond B Biol Sci 293:93–104PubMedCrossRefGoogle Scholar
  6. 6.
    Rao DR, Oesper P (1961) Purification and properties of muscle phosphoglycerate kinase. Biochem J 81:405–411PubMedGoogle Scholar
  7. 7.
    Axelrod B, Bandurski RS (1953) Phosphoglyceryl kinase in higher plants. J Biol Chem 204:939–948PubMedGoogle Scholar
  8. 8.
    Garfinkel L, Garfinkel D (1985) Magnesium regulation of the glycolytic pathway and the enzymes involved. Magnesium 4:60–72PubMedGoogle Scholar
  9. 9.
    VandeBerg JL (1985) The phosphoglycerate kinase isozyme system in mammals: biochemical, genetic, developmental, and evolutionary aspects. Isozymes Curr Top Biol Med Res 12:133–187PubMedGoogle Scholar
  10. 10.
    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 11:118–147PubMedCrossRefGoogle Scholar
  11. 11.
    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 72:417–429PubMedCrossRefGoogle Scholar
  12. 12.
    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 43:3436–3449PubMedCrossRefGoogle Scholar
  13. 13.
    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 279:773–777PubMedCrossRefGoogle Scholar
  14. 14.
    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 409:742–757PubMedCrossRefGoogle Scholar
  15. 15.
    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 286:14040–14048PubMedCrossRefGoogle Scholar
  16. 16.
    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 132:6507–6516PubMedCrossRefGoogle Scholar
  17. 17.
    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 36:3620–3629PubMedCrossRefGoogle Scholar
  18. 18.
    Aslanidis C, Dejong PJ (1990) Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res 18:6069–6074PubMedCrossRefGoogle Scholar
  19. 19.
    Haun RS, Serventi IM, Moss J (1992) Rapid, reliable ligation-independent cloning of pcr products using modified plasmid vectors. Biotechniques 13:515–518PubMedGoogle Scholar
  20. 20.
    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 498:105–115PubMedCrossRefGoogle Scholar
  21. 21.
    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 25:8–15PubMedCrossRefGoogle Scholar
  22. 22.
    Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307–326CrossRefGoogle Scholar
  23. 23.
    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 62:859–866PubMedCrossRefGoogle Scholar
  24. 24.
    Sheldrick GM (2008) A short history of SHELX. Acta Crystallogr A 64:112–122PubMedCrossRefGoogle Scholar
  25. 25.
    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 80–86Google Scholar
  26. 26.
    Cowtan KD, Main P (1993) Improvement of macromolecular electron-density maps by the simultaneous application of real and reciprocal space constraints. Acta Crystallogr D 49:148–157PubMedCrossRefGoogle Scholar
  27. 27.
    Perrakis A, Morris R, Lamzin VS (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol 6:458–463PubMedCrossRefGoogle Scholar
  28. 28.
    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 67:235–242PubMedCrossRefGoogle Scholar
  29. 29.
    Terwilliger TC, Berendzen J (1999) Automated MAD and MIR structure solution. Acta Crystallogr D 55:849–861PubMedCrossRefGoogle Scholar
  30. 30.
    Terwilliger T (2004) SOLVE and RESOLVE: automated structure solution, density modification, and model building. J Synchrotron Radiat 11:49–52PubMedCrossRefGoogle Scholar
  31. 31.
    Terwilliger TC (2002) Automated structure solution, density modification and model building. Acta Crystallogr D 58:1937–1940PubMedCrossRefGoogle Scholar
  32. 32.
    Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53:240–255PubMedCrossRefGoogle Scholar
  33. 33.
    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 66:213–221PubMedCrossRefGoogle Scholar
  34. 34.
    Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D 60:2126–2132PubMedCrossRefGoogle Scholar
  35. 35.
    Painter J, Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D Biol Crystallogr 62:439–450PubMedCrossRefGoogle Scholar
  36. 36.
    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 50:437–450PubMedCrossRefGoogle Scholar
  37. 37.
    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 60:1833–1839PubMedCrossRefGoogle Scholar
  38. 38.
    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 19:163–164PubMedCrossRefGoogle Scholar
  39. 39.
    Ponstingl H, Kabir T, Thornton JM (2003) Automatic inference of protein quaternary structure from crystals. J Appl Crystallogr 36:1116–1122CrossRefGoogle Scholar
  40. 40.
    Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774–797PubMedCrossRefGoogle Scholar
  41. 41.
    Zheng H, Chruszcz M, Lasota P, Lebioda L, Minor W (2008) Data mining of metal ion environments present in protein structures. J Inorg Biochem 102:1765–1776PubMedCrossRefGoogle Scholar
  42. 42.
    Schrődinger L (2010) The PyMOL molecular graphics system, Version-1.3r1Google Scholar
  43. 43.
    Bond C (2003) TopDraw: a sketchpad for protein structure topology cartoons RID B-4094-2011. Bioinformatics 19:311–312PubMedCrossRefGoogle Scholar
  44. 44.
    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 50:202–209PubMedCrossRefGoogle Scholar
  45. 45.
    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 5:1475–1483PubMedCrossRefGoogle Scholar
  46. 46.
    Holm L, Rosenstrom P (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38:W545–W549PubMedCrossRefGoogle Scholar
  47. 47.
    Ye Y, Godzik A (2003) Flexible structure alignment by chaining aligned fragment pairs allowing twists. Bioinformatics 19(Suppl 2):ii246–ii255PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Heping Zheng
    • 1
    • 5
  • Ekaterina V. Filippova
    • 2
    • 5
  • Karolina L. Tkaczuk
    • 1
    • 5
  • Piotr Dworzynski
    • 1
    • 5
  • Maksymilian Chruszcz
    • 1
    • 5
  • Przemyslaw J. Porebski
    • 1
    • 5
  • Zdzislaw Wawrzak
    • 5
    • 6
  • Olena Onopriyenko
    • 3
    • 5
  • Marina Kudritska
    • 3
    • 5
  • Sarah Grimshaw
    • 4
    • 5
  • Alexei Savchenko
    • 3
    • 5
  • Wayne F. Anderson
    • 2
    • 5
  • Wladek Minor
    • 1
    • 5
  1. 1.Department of Molecular Physiology and Biological PhysicsUniversity of VirginiaCharlottesvilleUSA
  2. 2.Department of Molecular Pharmacology and Biological ChemistryNorthwestern University Feinberg School of MedicineChicagoUSA
  3. 3.Banting and Best Department of Medical ResearchUniversity of TorontoTorontoCanada
  4. 4.J. Craig Venter InstituteRockvilleUSA
  5. 5.Center for Structural Genomics of Infectious Diseases (CSGID)
  6. 6.Northwestern UniversitySynchrotron Research CenterArgonneUSA

Personalised recommendations