Advertisement

Crystal Structure of Apo and Ligand Bound Vibrio cholerae Ribokinase (Vc-RK): Role of Monovalent Cation Induced Activation and Structural Flexibility in Sugar Phosphorylation

  • Rakhi Paul
  • Madhumita Dandopath Patra
  • Udayaditya SenEmail author
Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 842)

Abstract

Ribokinase (RK; EC 2.7.1.15) catalyzes the transfer of γ-phosphate from adenosine tri-phosphate (ATP) to O5′ of d-ribose to form d-ribose-5-phosphate, a key step that enables d-ribose to enter into the metabolic pathways for further use. The phosphorylation reaction of ribose by RK is catalyzed by divalent cations whereas monovalent cations activate RK and allosterically regulate the reaction. In order to gain further insights into the catalytic functions of RK, crystal structures of Vibrio cholerae ribokinase (Vc-RK) have been solved in apo form (3.4 Å), sugar + ADP bound form (1.75 Å) and sugar + ADP + Cs+ (2.37 Å) bound form and compared with E. coli RK and Sa239 RK. Vc-RK, like E. coli RK and Sa239 RK, exists as a dimer and each monomer has two domains, a large catalytic α/β domain consisting of a central nine stranded twisted β-sheet which is flanked on both faces by five α-helices and a four stranded β-sheet region protruding from the α/β domain. The structure of Vc-RK in sugar + ADP bound form when compared with Cs+ bound E. coli RK structure is seen to be activated by a Na+ ion. The location of the Na+ ion is confirmed by the sugar + ADP + Cs+ bound Vc-RK structure where Cs+ occupies the same position as Na+. Comparisons between the apo and ligand bound Vc-RK structures have allowed us to identify the conformational changes associated with the activation in the presence of Na+, sugar induced structural changes and mechanism of phosphorylation reaction of Vc-RK.

Notes

Acknowledgements

The laboratory of US is supported by the MSACR project, DAE, Government of India and SINP. This work is supported by the Department of Biotechnology (DBT), Government of India (The BM14 beamline project for synchrotron data collection at the ESRF, Grenoble). M.D.P. thanks the DBT for a DBT-RA fellowship.

References

  1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung L, 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 66:213–221CrossRefGoogle Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410CrossRefGoogle Scholar
  3. Anderson A, Cooper RA (1969) The significance of ribokinase for ribose utilization by Escherichia coli. Biochim Biophys Acta 177:163–165CrossRefGoogle Scholar
  4. Anderson A, Cooper RA (1970) Biochemical and genetical studies on ribose catabolism in Escherichia coli K12. J Gen Microbiol 62:335–339CrossRefGoogle Scholar
  5. Andersson CE, Mowbray SL (2002) Activation of ribokinase by monovalent cations. J Mol Biol 315:409–419CrossRefGoogle Scholar
  6. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 67(4):271–281CrossRefGoogle Scholar
  7. Bork P, Sander C, Valencia A (1993) Convergent evolution of similar enzymatic function on different protein folds: the hexokinase, ribokinase, and galactokinase families of sugar kinases. Protein Sci 2:31–40CrossRefGoogle Scholar
  8. Cheng G, Bennett EM, Begley TP, Ealick SE (2002) Crystal structure of 4-amino-5-hydroxymethyl-2- methylpyrimidine phosphate kinase from Salmonella typhimurium at 2.3 Å resolution. Structure 10:225–235CrossRefGoogle Scholar
  9. Chua TK, Seetharaman J, Kasprzak JM, Ng C, Patel BK, Love C, Bujnicki JM, Sivaraman J (2010) Crystal structure of a fructokinase homolog from Halothermothrix orenii. J Struct Biol 171(3):397–401CrossRefGoogle Scholar
  10. Chuvikovsky DV, Esipov RS, Skoblov YS, Chupova LA, Muravyova TI, Miroshnikov AI, Lapinjoki S, Mikhailopulo IA (2006) Ribokinase from E. coli: expression, purification, and substrate specificity. Bioorg Med Chem 14:6327–6332CrossRefGoogle Scholar
  11. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126–2132CrossRefGoogle Scholar
  12. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62(1):72–82CrossRefGoogle Scholar
  13. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S, Paern J, Lopez R (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38:695–699CrossRefGoogle Scholar
  14. Iida A, Harayama S, Iino T, Hazelbauer GL (1984) Molecular cloning and characterization of genes required for ribose transport and utilization in Escherichia coli K-12. J Bacteriol 158(2):674–682CrossRefGoogle Scholar
  15. Karasevich I, Ivoĭlov VS (1975) Preliminary metabolism of d-ribose by Candida bombi. Mikrobiologiia 44(2):202–205 (Russian)PubMedGoogle Scholar
  16. Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372:774–797CrossRefGoogle Scholar
  17. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK—a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291CrossRefGoogle Scholar
  18. Li MH, Kwok F, Chang WR, Lau CK, Zhang JP, Lo SC, Jiang T, Liang DC (2002) Crystal structure of brain pyridoxal kinase, a novel member of the ribokinase superfamily. J Biol Chem 277(48):46385–46390CrossRefGoogle Scholar
  19. Li J, Wang C, Wu Y, Wu M, Wang L, Wang Y, Zang J (2012) Crystal structure of Sa239 reveals the structural basis for the activation of ribokinase by monovalent cations. J Struct Biol 177:578–582CrossRefGoogle Scholar
  20. Lopilato JE, Garwin JL, Emr SD, Silhavy TJ, Beckwith JR (1984) d-Ribose metabolism in Escherichia coli K-12: genetics, regulation, and transport. J Bacteriol 158:665–673CrossRefGoogle Scholar
  21. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40:658–674CrossRefGoogle Scholar
  22. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, Buso N, Cowley AP, Lopez R (2013) Analysis tool web services from the EMBL-EBI. Nucleic Acids Res 41:597–600CrossRefGoogle Scholar
  23. Painter J, Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D Biol Crystallogr 62:439–450CrossRefGoogle Scholar
  24. Park J, Gupta RS (2008) Adenosine kinase and ribokinase—the RK family of proteins. Cell Mol Life Sci 65:2875–2896CrossRefGoogle Scholar
  25. Paul R, Dandopath Patra M, Banerjee R, Sen U (2014) Crystallization and preliminary X-ray analysis of a ribokinase from Vibrio cholerae O395. Acta Crystallogr F Struct Biol Commun 70(8):1098–1102Google Scholar
  26. Potterton E, Briggs P, Turkenburg M, Dodson E (2003) A graphical user interface to the CCP4 program suite. Acta Crystallogr D Biol Crystallogr 59:1131–1137CrossRefGoogle Scholar
  27. Sack DA, Sack RB, Nair GB, Siddique AK (2004) Cholera. Lancet 363(9404):223–233CrossRefGoogle Scholar
  28. Schimmel SD, Hoffee P, Horecker BL (1974) Deoxyribokinase from Salmonella typhimurium: purification and properties. Arch Biochem Biophys 164:560–570CrossRefGoogle Scholar
  29. Sigrell JA, Cameron AD, Jones TA, Mowbray SL (1997) Purification, characterization, and crystallization of Escherichia coli ribokinase. Protein Sci 6:2474–2476CrossRefGoogle Scholar
  30. Sigrell JA, Cameron AD, Jones TA, Mowbray SL (1998) Structure of Escherichia coli ribokinase in complex with ribose and dinucleotide determined to 1.8 Å resolution: insights into a new family of kinase structures. Structure 6:183–193CrossRefGoogle Scholar
  31. Sigrell JA, Cameron AD, Jones TA, Mowbray SL (1999) Induced fit on sugar binding activates ribokinase. J Mol Biol 290:1009–1018CrossRefGoogle Scholar
  32. Suelter CH (1970) Enzymes activated by monovalent cations. Science 168:789–795CrossRefGoogle Scholar
  33. Zhang Y, Dougherty M, Downs DM, Ealick SE (2004) Crystal structure of an aminoimidazole riboside kinase from Salmonella enterica: implications for the evolution of the ribokinase superfamily. Structure 12(10):1809–1821CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Rakhi Paul
    • 1
  • Madhumita Dandopath Patra
    • 1
  • Udayaditya Sen
    • 1
    Email author
  1. 1.Crystallography and Molecular Biology DivisionSaha Institute of Nuclear PhysicsKolkataIndia

Personalised recommendations