Biochemical and structural studies of N5-carboxyaminoimidazole ribonucleotide mutase from the acidophilic bacterium Acetobacter aceti

Biochemistry

Volumn 45, Issue 27, 2006, Pages 8193-8208

  Constantine, Charles Z ^a   Starks, Courtney M ^a   Mill, Christopher P ^a   Ransome, Aaron E ^a   Karpowicz, Steven J ^a   Francois, Julie A ^a   Goodman, Rena A ^a   Kappock, T Joseph ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CRYSTAL STRUCTURE; DECARBONIZATION; MATHEMATICAL MODELS; PROTONS; THERMAL EFFECTS;

ACID-LABILE COMPOUNDS; ACIDOPHILIC BACTERIUM ACETOBACTER ACETI (AAPURE); THERMAL UNFOLDING TEMPERATURE; WATER MOLECULE;

ENZYMES;

4 CARBOXY 5 AMINOIMIDAZOLE RIBONUCLEOTIDE; GENOMIC DNA; MUTASE; N5 CARBOXYAMINOIMIDAZOLE RIBONUCLEOTIDE MUTASE; RIBONUCLEOTIDE; UNCLASSIFIED DRUG;

ACETOBACTER; ACETOBACTER ACETI; ARTICLE; CRYSTAL STRUCTURE; DECARBOXYLATION; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME STABILITY; ENZYME STRUCTURE; ESCHERICHIA COLI; GENETIC COMPLEMENTATION; MOLECULAR CLONING; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTON TRANSPORT; PURINE SYNTHESIS; TEMPERATURE DEPENDENCE;

ACETOBACTER; AMINO ACID SEQUENCE; AMINOIMIDAZOLE CARBOXAMIDE; BACTERIAL PROTEINS; CATALYSIS; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HISTIDINE; HYDROGEN-ION CONCENTRATION; INTRAMOLECULAR TRANSFERASES; MODELS, MOLECULAR; MUTAGENESIS; MUTATION; PROTEIN FOLDING; RECOMBINANT PROTEINS; RIBONUCLEOTIDES;

ACETOBACTER ACETI; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33745852259     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060465n     Document Type: Article

References (62)

1. Kappock, T. J., Ealick, S. E., and Stubbe, J. (2000) Modular evolution of the purine biosynthetic pathway, Curr. Opin. Chem. Biol. 4, 567-572.
2. Mathews, I. I., Kappock, T. J., Stubbe, J., and Ealick, S. E. (1999) Crystal structure of Escherichia coli PurE, an unusual mutase in the purine biosynthetic pathway, Structure 7, 1395-1406.
3. 5-carboxyaminoimidazole ribonucleotide: Evidence for a new intermediate and two new enzymatic activities in the de novo purine biosynthetic pathway of Escherichia coli, Biochemistry 33, 2269-2278.
4. Meyer, E., Leonard, N. J., Bhat, B., Stubbe, J., and Smith, J. M. (1992) Purification and characterization of the purE, purK, and purC gene products: identification of a previously unrecognized energy requirement in the purine biosynthetic pathway, Biochemistry 31, 5022-5032.
5. 5-CAIR mutase, Biochemistry 38, 3012-3018.
6. Firestine, S. M., Poon, S.-W., Mueller, E. J., Stubbe, J., and Davisson, V. J. (1994) Reactions catalyzed by 5-aminoimidazole ribonucleotide carboxylases from Escherichia coli and Gallus gallus: a case for divergent catalytic mechanisms, Biochemistry 33, 11927-11934.
7. Waldrop, G. L., Rayment, I., and Holden, H. M. (1994) Three-dimensional structure of the biotin carboxylase subunit of acetyl-CoA carboxylase, Biochemistry 33, 10249-10256.
8. 5-carboxyaminoimidazole ribonucleotide synthetase: A member of the ATP grasp protein superfamily, Biochemistry 38, 15480-15492.
9. Kluger, R., and Adawadkar, P. D. (1976) A reaction proceeding through intramolecular phosphorylation of a urea. A chemical mechanism for enzymatic carboxylation of biotin involving cleavage of ATP, J. Am. Chem. Soc. 98, 3741-3742.
10. Ogita, T., and Knowles, J. R. (1988) On the intermediacy of carboxyphosphate in biotin-dependent carboxylations, Biochemistry 27, 8028-8033.
11. Asai, T. (1968) Acetic acid bacteria. Classification and biochemical activities, University of Tokyo Press, Tokyo.
12. Menzel, U., and Gottschalk, G. (1985) The internal pH of Acetobacterium wieringae and Acetobacter aceti during growth and production of acetic acid, Arch. Microbiol. 143, 47-51.
13. 5-carboxyaminoimidazole ribonucleotide mutase (PurE), Acta Crystallogr., Sect. D: Biol. Crystallogr. D60, 1753-1760.
14. Schendel, F. J. (1986) Ph.D. Thesis, University of Wisconsin, Madison, WI.
15. Firestine, S. M., and Davisson, V. J. (1994) Carboxylases in de novo purine biosynthesis. Characterization of the Gallus gallus bifunctional enzyme, Biochemistry 33, 11917-11926.
16. Srivastava, P. C., Mancuso, R. W., Rousseau, R. J., and Robins, R. K. (1974) Nucleoside peptides. 6. Synthesis of certain N-(5-amino-1-(β-D- ribofuranosyl)imidazole-4-carbonyl)amino acids related to naturally occurring intermediates in the purine biosynthetic pathway, J. Med. Chem. 17, 1207-1211.
17. Stouthamer, A. H., de Haan, P. G., and Nijkamp, H. J. (1965) Mapping of purine markers in Escherichia coli K 12, Genet. Res. 6, 442-453.
18. Staden, R., Beal, K. F., and Bonfield, J. K. (2000) The Staden package, 1998, Methods Mol. Biol. 132, 115-130.
19. Schrimsher, J. L., Schendel, F. J., and Stubbe, J. (1986) Isolation of a multifunctional protein with aminoimidazole ribonucleotide synthetase, glycinamide ribonucleotide synthetase, and glycinamide ribonucleotide transformylase activities: Characterization of aminoimidazole ribonucleotide synthetase, Biochemistry 25, 4356-4365.
20. Ellis, K. J., and Morrison, J. F. (1982) Buffers of constant ionic strength for studying pH-dependent processes, Methods Enzymol. 87, 405-426.
21. Bates, R. G., and Pinching, G. D. (1949) Resolution of the dissociation constants of citric acid at 0 to 50, and determination of certain related thermodynamic functions, J. Am. Chem. Soc. 71, 1274-1283.
22. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J.-S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr., Sect. D: Biol. Crystallogr. D54, 905-921.
23. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A 47, 110-119.
24. Kleywegt, G. J., and Jones, T. A. (1998) Databases in protein crystallography, Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 1119-1131.
25. Schüttelkopf, A. W., and van Aalten, D. M. F. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes, Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 1355-1363.
26. Vagin, A. A., Steiner, R. A., Lebedev, A. A., Potterton, L., McNicholas, S., Long, F., and Murshudov, G. N. (2004) REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use, Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2184-2195.
27. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs for protein crystallography, Acta Crystallogr. D 50, 760-770.
28. Kraulis, P. J. (1991) Molscript: A program to produce both detailed and schematic plots of protein structures, J. Appl. Crystallogr. 24, 946-950.
29. Merritt, E. A., and Bacon, D. J. (1997) Raster3D: Photorealistic molecular graphics, Methods Enzymol. 277, 505-524.
30. DeLano, W. L. (2002) The PyMOL Users Manual, San Carlos, CA.
31. Meyer, E. (1996), Ph.D. Thesis, Massachusetts Institute of Technology, Cambridge, MA.
32. Bernal, J. D., and Fowler, R. H. (1933) A theory of water and ionic solution, with particular reference to hydrogen and hydroxyl ions, J. Chem. Phys. 1, 515-548.
33. Litchfield, G. J., and Shaw, G. (1971) Purines, pyrimidines, and imidazoles. Part XXXVIII. A kinetic study of the decarboxylation of 5-amino-1-β-D-ribofuranosylimidazole-4-carboxylic acid 5′-phosphate and related compounds, J. Chem. Soc. B, 1474-1484.
34. 31P nuclear magnetic resonance study of phosphoribosyldiphosphate and its interaction with magnesium ions, J. Biol. Chem. 257, 6164-6170.
35. Boyle, M. P., Kalliomaa, A. K., Levdikov, V., Blagova, E., Fogg, M. J., Brannigan, J. A., Wilson, K. S., and Wilkinson, A. J. (2005) Crystal structure of PurE (BA0288) from Bacillus anthracis at 1.8 Å resolution, Proteins 61, 674-676.
36. Loladze, V. V., Ibarra-Molero, B., Sanchez-Ruiz, J. M., and Makhatadze, G. I. (1999) Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface, Biochemistry 38, 16419-16423.
37. Schwehm, J. M., Fitch, C. A., Dang, B. N., Garcia-Moreno, E. B., and Stites, W. E. (2003) Changes in stability upon charge reversal and neutralization substitution in staphylococcal nuclease are dominated by favorable electrostatic effects, Biochemistry 42, 1118-1128.
38. Spector, S., Wang, M., Carp, S. A., Robblee, J., Hendsch, Z. S., Fairman, R., Tidor, B., and Raleigh, D. P. (2000) Rational modification of protein stability by the mutation of charged surface residues, Biochemistry 39, 872-879.
39. Strickler, S. S., Gribenko, A. V., Keiffer, T. R., Tomlinson, J., Reihle, T., Loladze, V. V., and Makhatadze, G. I. (2006) Protein stability and surface electrostatics: a charged relationship, Biochemistry 45, 2761-2766.
40. Koide, A., Jordan, M. R., Horner, S. R., Batori, V., and Koide, S. (2001) Stabilization of a fibronectin type III domain by the removal of unfavorable electrostatic interactions on the protein surface, Biochemistry 40, 10326-10333.
41. Makhatadze, G. I., Loladze, V. V., Ermolenko, D. N., Chen, X., and Thomas, S. T. (2003) Contribution of surface salt bridges to protein stability: guidelines for protein engineering, J. Mol. Biol. 327, 1135-1148.
42. Hendsch, Z. S., and Tidor, B. (1994) Do salt bridges stabilize proteins? A continuum electrostatic analysis, Protein Sci. 3, 211-226.
43. Steiner, H., Jonsson, B. H., and Lindskog, S. (1975) The catalytic mechanism of carbonic anhydrase. Hydrogen-isotope effects on the kinetic parameters of the human C isoenzyme, Eur. J. Biochem. 59.
44. Silverman, D. N., and Lindskog, S. (1988) The catalytic mechanism of carbonic anhydrase: Implications of a rate-limiting protolysis of water, Acc. Chem. Res. 21, 30-36.
45. Frank, R. A. W., Titman, C. M., Pratap, J. V., Luisi, B. F., and Perham, R. N. (2004) A molecular switch and proton wire synchronize the active sites in thiamine enzymes, Science 306, 872-876.
46. Babbitt, P. C., Hasson, M. S., Wedekind, J. E., Palmer, D. R., Barrett, W. C., Reed, G. H., Rayment, I., Ringe, D., Kenyon, G. L., and Gerlt, J. A. (1996) The enolase superfamily: a general strategy for enzyme-catalyzed abstraction of the α-protons of carboxylic acids, Biochemistry 35, 16489-16501.
47. Gerlt, J. A., Babbitt, P. C., and Rayment, I. (2005) Divergent evolution in the enolase superfamily: the interplay of mechanism and specificity, Arch. Biochem. Biophys. 433, 59-70.
48. Fersht, A. (2000) Structure and mechanism in protein science, W. H. Freeman and Co., New York.
49. Litchfield, G. J., and Shaw, G. (1965) The mechanism of decarboxylation of some 5-aminoimidazole-4-carboxylic acids and the influence of transition metals, Chem. Commun., 563-565.
50. Litchfield, G. J., and Shaw, G. (1971) Purines, pyrimidines, and imidazoles. Part XXXV. Potentiometric and spectroscopic studies of some imidazoles related to intermediates in the biosynthesis de novo of purine nucleotides, J. Chem. Soc. C, 817-820.
51. Firestine, S. M., and Davisson, V. J. (1993) A tight binding inhibitor of 5-aminoimidazole ribonucleotide carboxylase, J. Med. Chem. 36, 3484-3486.
52. Schrimsher, J. L., Schendel, F. J., Stubbe, J., and Smith, J. M. (1986) Purification and characterization of aminoimidazole ribonucleotide synthetase from Escherichia coli, Biochemistry 25, 4366-4371.
53. Dunn, G. E., and Dayal, S. K. (1970) Mechanism of decarboxylation of substituted anthranilic acids at high acidity, Can. J. Chem. 48, 3349-3353.
54. Willi, A. V., Won, C. M., and Vilk, P. (1968) Kinetics and mechanism of the decarboxylation of anthranilic acid in aqueous solution, J. Phys. Chem. 72, 3142-3148.
55. 13Carbon kinetic isotope effects and the mechanism of decarboxylation of 2,4-dihydroxybenzoic acid, Chem. Ind., 782-783.
56. Appleby, T. C., Kinsland, C., Begley, T. P., and Ealick, S. E. (2000) The crystal structure and mechanism of orotidine 5′-monophosphate decarboxylase, Proc. Natl. Acad. Sci. U.S.A. 97, 2005-2010.
57. Begley, T. P., Appleby, T. C., and Ealick, S. E. (2000) The structural basis for the remarkable catalytic proficiency of orotidine 5′- monophosphate decarboxylase, Curr. Opin. Struct. Biol. 10, 711-718.
58. Hu, Q., and Kluger, R. (2005) Making thiamin work faster: acid-promoted separation of carbon dioxide, J. Am. Chem. Soc. 127, 12242-12243.
59. Blazevic, N., Kajfez, F., and Sunjic, V. (1970) σ values of some nitroimidazoles, J. Heterocycl. Chem. 7, 227-229.
60. Hodel, A., Kim, S. H., and Brünger, A. T. (1992) Model bias in macromolecular crystal structures, Acta Crystallogr. A 48, 851-858.
61. Francois, J. A., and Kappock, T. J. (2006) Alanine racemase from the acidophile Acetobacter aceti, Protein Expression Purif. (in press).
62. Chan, J. W., and Goodwin, P. H. (1995) Extraction of genomic DNA from extracellular polysaccharide-synthesizing Gram-negative bacteria, BioTechniques 18, 418-422.