Kinetic and structural properties of inorganic pyrophosphatase from the pathogenic bacterium Helicobacter pylori

Proteins: Structure, Function and Genetics

Volumn 65, Issue 3, 2006, Pages 670-680

  Chao, Ti Chun ^a   Huang, Haimei ^a   Tsai, Jia Yin ^a   Huang, Chung Yu ^a   Sun, Yuh Ju ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

Helicobacter pylori; Inorganic pyrophosphatase

Indexed keywords

ADENOSINE TRIPHOSPHATE; FLUORIDE SODIUM; INORGANIC PYROPHOSPHATASE; MAGNESIUM ION; METAL ION; N ETHYLMALEIMIDE; PHOSPHATE; PYROPHOSPHATE;

ALPHA HELIX; ARTICLE; BACTERIAL GENE; BETA SHEET; BIOSYNTHESIS; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENERGY CONSERVATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; GENE EXPRESSION; HELICOBACTER PYLORI; HYDROLYSIS; MOLECULAR CLONING; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HELICOBACTER PYLORI; HYDROLYSIS; INORGANIC PYROPHOSPHATASE; KINETICS; MAGNESIUM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHATES; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

EID: 33750085003     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21093     Document Type: Article

References (49)

1. Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984;1:1311-1315.
2. Bayerdorffer E, Miehlke S, Neubauer A, Stolte M. Gastric MALT-lymphoma and Helicobacter pylori infection. Aliment Pharmacol Ther 1997;11:89-94.
3. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD, Ketchum KA, Klenk HP, Gill S, Dougherty BA, Nelson K, Quackenbush J, Zhou L, Kirkness EF, Peterson S, Loftus B, Richardson D, Dodson R, Khalak HG, Glodek A, McKenney K, Fitzegerald LM, Lee N, Adams MD, Hickey EK, Berg DE, Gocayne JD, Utterback TR, Peterson JD, Kelley JM, Cotton MD, Weidman JM, Fujii C, Bowman C, Watthey L, Wallin E, Hayes WS, Borodovsky M, Karp PD, Smith HO, Fraser CM, Venter JC. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997;389:539-547.
4. Schilling CH, Covert MW, Famili I, Church GM, Edwards JS, Palsson BO. Genome-scale metabolic model of Helicobacter pylori 26695. J Bacteriol 2002;184:4582-4593.
5. Melchers K, Weitzenegger T, Buhmann A, Steinhilber W, Sachs G, Schafer KP. Cloning and membrane topology of a P type ATPase from Helicobacter pylori. J Biol Chem 1996;271:446-457.
6. Melchers K, Schuhmacher A, Buhmann A, Weitzenegger T, Belin D, Grau S, Ehrmann M. Membrane topology of CadA homologous P-type ATPase of Helicobacter pylori as determined by expression of phoA fusions in Escherichia coli and the positive inside rule. Res Microbiol 1999;150:507-520.
7. Lahti R, Pitkaranta R, Valve E, Ilta I, Kukko-Kalske E, Heinonen J. Cloning and characterization of the gene encoding inorganic pyrophosphatase of Escherichia coli K-12. J Bacteriol 1988;170: 5901-5907.
8. Oliva G, Romero I, Ayala G, Barrios-Jacobo I, Celis H. Characterization of the inorganic pyrophosphatase from the pathogenic bacterium Helicobacter pylori. Arch Microbiol 2000;174:104-110.
9. Chen J, Brevet A, Froment M, Leveque F, Schmitter J-M, Blanquet S, Plateau P. Pyrophosphatase is essential for growth of Escherichia coli. J Bacteriol 1990;172:5686-5689.
10. Harutyunyan EH, Oganessyan VY, Oganessyan NN, Avaeva SM, Nazarova TI, Vorobyeva NN, Kurilova SA, Huber R, Mather T. Crystal structure of holo inorganic pyrophosphatase from Escherichia coli at 1.9 A resolution. Mechanism of hydrolysis. Biochemistry 1997;36:7754-7760.
11. Shintani T, Uchiumi T, Yonezawa T, Salminen A, Baykov AA, 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.
12. Young T, Kuhn N, Wadeson A, Ward S, Burges D, Cooke GD. 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.
13. Avaeva SM. Active site interactions in oligomeric structures of inorganic pyrophosphatases. Biochemistry (Moscow) 2000;65:361-372.
14. 2+ dependence. Biochemistry 1996;35:4655-4661.
15. Baykov AA, Fabrichniy IP, Pohjanjoki P, Zyryanov AB, Lahti R. Fluoride effects along the reaction pathway of pyrophosphatase: evidence for a second enzyme pyrophosphate intermediate. Biochemistry 2000;39:11939-11947.
16. 2+ activation. J Biol Chem 1972;247:7308-7314.
17. 2+ inhibition. J Biol Chem 1972;247:7315-7319.
18. 2+ ions against fluoride inhibition. Arch Biochem Biophys 2000;379:292-298.
19. Ahn S, Milner AJ, Futterer K, Konopka M, Ilias M, Young TW, White SA. The "open" and "closed" structures of the type-C inorganic pyrophosphatases from Bacillus subtilis and Streptococcus gordonii. J Mol Biol 2001;313:797-811.
20. Harutyunyan EH, Kuranova IP, Vainshtein BK, Hohne WE, Lamzin VS, Dauter Z, Teplyakov AV, Wilson KS. X-ray structure of yeast inorganic pyrophosphatase complexed with manganese and phosphate. Eur J Biochem 1996;239:220-228.
21. Teplyakov A, Obmolova G, Wilson KS, Ishii K, Kaji H, Samejima T, Kuranova I. Crystal structure of inorganic pyrophosphatase from Thermus thermophilus. Protein Sci 1994;3: 1098-1107.
22. Leppanen VM, Nummelin H, Hansen T, Lahti R, Schafer G, Goldman A. Sulfolobus acidocaldarius inorganic pyrophosphatase: structure, thermostability, and effect of metal ion in an archael pyrophosphatase. Protein Sci 1999;8:1218-1231.
23. Liu B, Bartlam M, Gao R, Zhou W, Pang H, Liu Y, Feng Y, Rao Z. Crystal Structure of the hyperthermophilic inorganic pyrophosphatase from the archaeon Pyrococcus horikoshii. Biophys J 2004;86:420-427.
24. Kankare J, Salminen T, Lahti R, Cooperman BS, Baykov AA, Goldman A. Crystallographic identification of metal-binding sites in Escherichia coli inorganic pyrophosphatase. Biochemistry 1996;35:4670-4677.
25. Heikinheimo P, Lehtonen J, Baykov AA, Lahti R, Cooperman BS, Goldman A. The structural basis for pyrophosphatase catalysis. Structure 1996;4:1491-1508.
26. 2-: ligand-induced molecular asymmetry. FEBS Lett 1997; 410:502-508.
27. Heikinheimo P, Tuominen V, Ahonen A-K, Teplyakov A, Cooperman BS, Baykov AA, Lahti R, Goldman A. Toward a quantum-mechanical description of metal-assisted phosphoryl transfer in pyrophosphatase. Proc Natl Acad Sci USA 2001;98:3121-3126.
28. 2+ or CaPPi at atomic resolution and their mechanistic implications. J Mol Biol 2001;314:633-646.
29. +-pyrophosphatase. Biochim Biophys Acta 2004;1608:190-199.
30. McPherson A. Preparation and analysis of protein crystals. New York: Wiley; 1982.
31. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276A:307-326.
32. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallogr A 1994;50:157-163.
33. Mcree DE. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J Struct Biol 1999;25: 156-165.
34. Perrakis A, Morris R, Lamzin VS. Automated protein model building combined with iterative structure refinement. Nat Struct Mol Biol 1999;6:458-463.
35. Brunger AT, Adams PD, Clore GM, Delano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 1998;54:905-921.
36. Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 1997;53:240-255.
37. Laskowski RA, Macarthur MW, Moss DS, Thornton JM. Procheck-a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
38. Baykov A, Dudarenkov VY, Kapyla J, Alexander T, Hyytia T, Kasho VN, Husgafveli S, Cooperman BS, Goldman A, Lahti R. Dissociation of hexameric Escherichia coli inorganic pyrophosphatase into trimers on His-136→Gln or His-140→Gln substitution and its effect on enzyme catalytic properties. J Biol Chem 1995;270:30804-30812.
39. Velichko IS, Mikalahti K, Kasho VN, Dudarenkov VY, Hyytia T, Goldman A, Cooperman BS, Lahti R, Baykov AA. Trimeric inorganic pyrophosphatase of Escherichia coli obtained by directed mutagenesis. Biochemistry 1998;37:734-740.
40. Salminen A, Efimova IS, Parfenyev AN, Magretova NN, Mikalahti K, Goldman A, Baykovi AA, Lahti R. Reciprocal effects of substitutions at the subunit interfaces in hexameric pyrophosphatase of Escherichia coli. J Biol Chem 1999;274:33898-33904.
41. Rodina EV, Vainonen YP, Vorobyeva NN, Kurilova SA, Nazarova TI, Avaeva SM. The role of Asp42 in Escherichia coli inorganic pyrophosphatase functioning. Eur J Biochem 2001;268:3851-3857.
42. Islam MK, Miyoshi T, Kasuga-Aoki H, Isobe T, Arakawa T, Matsumoto Y, Tsuji N. Inorganic pyrophosphatase in the round-worm Ascaris and its role in the development and molting process of the larval stage parasites. Eur J Biochem 2003;270:2814-2826.
43. Thompson J, Higgins D, Gibson T. CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680.
44. Nicholls A, Sharp KA, Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 1991;11:281-296.
45. DeLano W The PyMOL user's manual. San Carlos, CA: DeLano Scientific; 2002.
46. Wallace A, Laskowski R, Thornton J. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 1995;8:127-134.
47. Liang J, Edelsbrunner H, Woodward C. Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design. Protein Sci 1998;7:1884-1897.
48. Jones S, Thornton JM. Principles of protein-protein interactions. Proc Natl Acad Sci USA 1996;93:13-20.
49. Avaeva S, Rodina E, Vorobyeva N, Kurilova S, Nazarova T, Sklyankina V, Oganessyan V, Harutyunyan E. Changes in Escherichia coli inorganic pyrophosphatase structure induced by binding of metal activators. Biochemistry (Moscow) 1998;63:699-707.