Structure of inorganic pyrophosphatase from Staphylococcus aureus reveals conformational flexibility of the active site

Journal of Structural Biology

Volumn 189, Issue 2, 2015, Pages 81-86

  Gajadeera, Chathurada S ^a   Zhang, Xinyi ^b   Wei, Yinan ^b   Tsodikov, Oleg V ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Enzyme; Hydrolase; Novel drug target; Phosphatase; Phosphate metabolism; Pyrophosphorolysis

Indexed keywords

ALCOHOL DEHYDROGENASE; DIMER; INORGANIC PYROPHOSPHATASE; MANGANESE; MONOMER; BACTERIAL PROTEIN; PHOSPHATE; PROTEIN BINDING;

ARTICLE; BACILLUS MEGATERIUM; BACILLUS SUBTILIS; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME STRUCTURE; GEL PERMEATION CHROMATOGRAPHY; HYDROGEN BOND; METHANOCALDOCOCCUS JANNASCHII; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; STAPHYLOCOCCUS AUREUS; STOICHIOMETRY; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS GORDONII; STREPTOCOCCUS MUTANS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; KINETICS; PROTEIN QUATERNARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

EUKARYOTA; PROKARYOTA; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; INORGANIC PYROPHOSPHATASE; KINETICS; MANGANESE; MODELS, MOLECULAR; PHOSPHATES; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; STAPHYLOCOCCUS AUREUS;

EID: 84922721676     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2014.12.003     Document Type: Article

References (35)

1. Ahn S., Milner A.J., Futterer K., Konopka M., Ilias M., Young T.W., White S.A. The "open" and "closed" structures of the type-C inorganic pyrophosphatases from Bacillus subtilis and Streptococcus gordonii. J. Mol. Biol. 2001, 313:797-811.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 1997, 25:3389-3402.
3. Baykov A.A., Evtushenko O.A., Avaeva S.M. A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal. Biochem. 1988, 171:266-270.
4. Baykov A.A., Cooperman B.S., Goldman A., Lahti R. Cytoplasmic inorganic pyrophosphatase. Prog. Mol. Subcel. Biol. 1999, 23:127-150.
5. Bock C.W., Katz A.K., Markham G.D., Glusker J.P. Manganese as a replacement for magnesium and zinc: Functional comparison of the divalent ions. J. Am. Chem. Soc. 1999, 121:7360-7372.
6. Charney J., Fisher W.P., Hegarty C.P. Managanese as an essential element for sporulation in the genus Bacillus. J. Bacteriol. 1951, 62:145-148.
7. Chen J., Brevet A., Fromant M., Leveque F., Schmitter J.M., Blanquet S., Plateau P. Pyrophosphatase is essential for growth of Escherichia coli. J. Bacteriol. 1990, 172:5686-5689.
8. Colonna-Cesari F., Perahia D., Karplus M., Eklund H., Braden C.I., Tapia O. Interdomain motion in liver alcohol dehydrogenase. Structural and energetic analysis of the hinge bending mode. J. Biol. Chem. 1986, 261:15273-15280.
9. Eklund H., Nordstrom B., Zeppezauer E., Soderlund G., Ohlsson I., Boiwe T., Soderberg B.O., Tapia O., Branden C.I., Akeson A. Three-dimensional structure of horse liver alcohol dehydrogenase at 2-4A resolution. J. Mol. Biol. 1976, 102:27-59.
10. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Cryst. D 2004, 60:2126-2132.
11. Fabrichniy I.P., Lehtio L., Salminen A., Zyryanov A.B., Baykov A.A., Lahti R., Goldman A. Structural studies of metal ions in family II pyrophosphatases: the requirement for a Janus ion. Biochemistry 2004, 43:14403-14411.
12. Fabrichniy I.P., Lehtio L., Tammenkoski M., Zyryanov A.B., Oksanen E., Baykov A.A., Lahti R., Goldman A. A trimetal site and substrate distortion in a family II inorganic pyrophosphatase. J. Biol. Chem. 2007, 282:1422-1431.
13. Halonen P., Tammenkoski M., Niiranen L., Huopalahti S., Parfenyev A.N., Goldman A., Baykov A., Lahti R. Effects of active site mutations on the metal binding affinity, catalytic competence, and stability of the family II pyrophosphatase from Bacillus subtilis. Biochemistry 2005, 44:4004-4010.
14. Harding M.M. Geometry of metal-ligand interactions in proteins. Acta Cryst. D 2001, 57:401-411.
15. Koonin E.V., Tatusov R.L. Computer analysis of bacterial haloacid dehalogenases defines a large superfamily of hydrolases with diverse specificity. Application of an iterative approach to database search. J. Mol. Biol. 1994, 244:125-132.
16. Kornberg A. On the metabolic significance of phosphorolytic and pyrophosphorolytic reactions 1962, Academic Press, New York.
17. Kuhn N.J., Wadeson A., Ward S., Young T.W. Methanococcus jannaschii ORF mj0608 codes for a class C inorganic pyrophosphatase protected by Co(2+) or Mn(2+) ions against fluoride inhibition. Arch. Biochem. Biophys. 2000, 379:292-298.
18. Lahti R. Microbial inorganic pyrophosphatases. Microbiol. Rev. 1983, 47:169-178.
19. Laskowski R.A., MacArthur M.V., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 1993, 26:283-291.
20. Lovell S.C., Davis I.W., Arendall W.B., de Bakker P.I., Word J.M., Prisant M.G., Richardson J.S., Richardson D.C. Structure validation by C alpha geometry: phi, psi and C beta deviation. Proteins 2003, 50:437-450.
21. Luft J.R., Collins R.J., Fehrman N.A., Lauricella A.M., Veatch C.K., DeTitta G.T. A deliberate approach to screening for initial crystallization conditions of biological macromolecules. J. Struct. Biol. 2003, 142:170-179.
22. Lundin M., Baltscheffsky H., Ronne H. Yeast PPA2 gene encodes a mitochondrial inorganic pyrophosphatase that is essential for mitochondrial function. J. Biol. Chem. 1991, 266:12168-12172.
23. Martin M.E., Byers B.R., Olson M.O., Salin M.L., Arceneaux J.E., Tolbert C. A Streptococcus mutans superoxide dismutase that is active with either manganese or iron as a cofactor. J. Biol. Chem. 1986, 261:9361-9367.
24. McCoy A.J., Grosse-Kunstleve R.W., Adams P.D., Winn M.D., Storoni L.C., Read R.J. Phaser crystallographic software. J. Appl. Cryst. 2007, 40:658-674.
25. Merckel M.C., Fabrichniy I.P., Salminen A., Kalkkinen N., Baykov A.A., Lahti R., Goldman A. Crystal structure of Streptococcus mutans pyrophosphatase: a new fold for an old mechanism. Structure 2001, 9:289-297.
26. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Cryst. D 1997, 53:240-255.
27. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. A 1997, 276:307-326.
28. Parfenyev A.N., Salminen A., Halonen P., Hachimori A., Baykov A.A., Lahti R. Quaternary structure and metal ion requirement of family II pyrophosphatases from Bacillus subtilis, Streptococcus gordonii, and Streptococcus mutans. J. Biol. Chem. 2001, 276:24511-24518.
29. Peller L. On the free-energy changes in the synthesis and degradation of nucleic acids. Biochemistry 1976, 15:141-146.
30. Rantanen M.K., Lehtio L., Rajagopal L., Rubens C.E., Goldman A. Structure of the Streptococcus agalactiae family II inorganic pyrophosphatase at 2.80 A resolution. Acta Cryst. D 2007, 63:738-743.
31. Shintani T., Uchiumi T., Yonezawa T., Salminen A., Baykov A.A., Lahti R., Hachimori A. Cloning and expression of a unique inorganic pyrophosphatase from Bacillus subtilis: evidence for a new family of enzymes. FEBS Lett. 1998, 439:263-266.
32. Sonnewald U. Expression of E. coli inorganic pyrophosphatase in transgenic plants alters photoassimilate partitioning. Plant J. 1992, 2:571-581.
33. Tono H., Kornberg A. Biochemical studies of bacterial sporulation. 3. Inorganic pyrophosphatase of vegetative cells and spores of Bacillus subtilis. J. Biol. Chem. 1967, 242:2375-2382.
34. Yamagata A., Kakuta Y., Masui R., Fukuyama K. The crystal structure of exonuclease RecJ bound to Mn2+ ion suggests how its characteristic motifs are involved in exonuclease activity. Proc. Natl. Acad. Sci. USA 2002, 99:5908-5912.
35. Young T.W., Kuhn N.J., Wadeson A., Ward S., Burges D., Cooke G.D. Bacillus subtilis ORF yybQ encodes a manganese-dependent inorganic pyrophosphatase with distinctive properties: the first of a new class of soluble pyrophosphatase?. Microbiology 1998, 144:2563-2571.