Crystal structure of phosphoserine aminotransferase from Escherichia coli at 2.3 Å resolution: Comparison of the unligated enzyme and a complex with α-methyl-L-glutamate

Journal of Molecular Biology

Volumn 286, Issue 3, 1999, Pages 829-850

  Hester, Gerko ^a   Stark, Wilhelm ^a   Moser, Markus ^a   Kallen, Jörg ^a   Marković Housley, Zora ^a   Jansonius, Johan N ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Enzyme catalysis; nifS gene product; Pyridoxal 5' phosphate; Substrate analogue complex; Three dimensional structure

Indexed keywords

AMINOTRANSFERASE; BACTERIAL ENZYME; GLUTAMIC ACID DERIVATIVE; PHOSPHOSERINE; PYRIDOXAL 5 PHOSPHATE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; ENZYME SUBUNIT; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0033605317     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2506     Document Type: Article

References (90)

1. Abrahams J.-P., Leslie A. G. W. Methods used in the structure determination of bovine mitochondrial F-1 ATPase. Acta Crystallog. sect. D. 52:1996;30-42.
2. Alexander F. W., Sandmeier E., Mehta P. K., Christen P. Evolutionary relationships among pyridoxal-5′-phosphate-dependent enzymes. Eur. J. Biochem. 219:1994;953-960.
3. Antson A. A., Demidkina T. V., Gollnick R., Dauter Z., Von Tersch R. L., Long J., Berezhnoy S. N., Phillips R. S., Harutyunyan E. H., Wilson K. S. Three-dimensional structure of tyrosine phenol-lyase. Biochemistry. 32:1993;4195-4206.
4. Bacon D. J., Anderson W. F. A fast algorithm for rendering space-filling pictures (abstract of paper presented at the Seventh Annual Meeting of the Molecular Graphics Society). J. Mol. Graph. 6:1988;219-220.
5. Barton G. J. Protein multiple sequence alignment and flexible pattern matching. Methods Enzymol. 183:1990;403-428.
6. Barton G. J. ALSCRIPT, a tool to format multiple sequence alignments. Protein Eng. 6:1993;37-40.
7. Barton G. J., Sternberg M. J. A strategy for the rapid multiple alignment of protein sequences. Confidence levels from tertiary structure comparisons. J. Mol. Biol. 198:1987a;327-337.
8. Barton G. J., Sternberg M. J. Evaluation and improvements in the automatic alignment of protein sequences. Protein Eng. 1:1987b;89-94.
9. Basurko M.-J., Darriet M., Cassainge A. Catalytic properties and specificity of phosphoserine aminotransferase from beef liver. Biochem. Soc. Trans. 17:1989;787-788.
10. Battchikova N., Himanen J.-P., Ahjolahti M., Korpela T. Phosphoserine aminotransferase from Bacillus circulans subsp. alkalophilus: purification, gene cloning and sequencing. Biochim. Biophys. Acta. 1295:1996;187-194.
11. Belhumeur P., Fortin N., Clark M. W. A gene from Saccharomyces cerevisiae which codes for a protein with significant homology to the bacterial 3-phosphoserine aminotransferase. Yeast. 10:1994;385-389.
12. Bernstein F. C., Koetzle T. F., Williams G. J. B., Meyer E. J. Jr, Brice M. D., Rogers J. K., Kennard O., Shimanouchi T., Tasumi M. The Protein Data Bank: a computer-based archival file for macromolecular structure. J. Mol. Biol. 112:1977;535-542.
13. Brünger A. T. Free R value: A novel statistical quantity for assessing the accuracy of crystal structures. Nature. 355:1992;472-475.
14. Brünger A. T., Kuriyan J., Karplus M. Crystallographic R factor refinement by molecular dynamics. Science. 235:1987;458-460.
15. Cheung G. P., Rosenblum I. Y., Sallach H. J. Comparative studies of enzymes related to serine metabolism in higher plants. Plant Physiol. 43:1968;1813-1820.
16. Christen P., Mehta P. K., Sandmeier E. Molecular evolution of pyridoxal-5′-phosphate-dependent enzymes. Marino G., Sannia G., Bossa E. Biochemistry of Vitamin B6 and PQQ. 1994;9-13 Birkhäuser Verlag, Basel.
17. Clausen T., Huber R., Laber B., Pohlenz H.-D., Messerschmidt A. Crystal structure of the pyridoxal-5′-phosphate dependent cystathionine β-lyase from Escherichia coli at 1.83 Å J. Mol. Biol. 262:1996;202-224.
18. Cleland W. W. The kinetics of enzyme-catalyzed reactions with two or more substrates or products. I. Nomenclature and rate equations. Biochim. Biophys. Acta. 67:1963;104-137.
19. Acta Crystallog. sect. D. 50:1994;760-763.
20. Cowtan K. D., Main P. Phase combination and cross validation in iterated density modification calculations. Acta Crystallog. sect. D. 52:1996;43-48.
21. Dunathan H. C. Stereochemical aspects of pyridoxal phosphate catalysis. Advan. Enzymol. 35:1971;79-134.
22. Duncan K., Coggins J. R. The serC-aroA operon of Escherichia coli. Biochem. J. 234:1986;49-57.
23. Engh R. A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400.
24. Esnouf R. An extensively modified version of MOLSCRIPT that includes greatly enhanced colouring capabilities. J. Mol. Graph. Modeling. 15:1998;132-136.
25. Ford G. C., Eichele G., Jansonius J. N. Three-dimensional structure of a pyridoxal-phosphate-dependent enzyme, mitochondrial aspartate aminotransferase. Proc. Natl Acad. Sci. USA. 77:1980;2559-2563.
26. Goldberg J. M., Kirsch J. F. The reaction catalyzed by Escherichia coli aspartate aminotransferase has multiple partially rate-determining steps, while that catalyzed by the Y225F mutant is dominated by ketimine hydrolysis. Biochemistry. 35:1996;5280-5291.
27. m. Biochemistry. 30:1991;305-312.
28. Hayashi H., Kagamiyama H. Transient-state kinetics of the reaction of aspartate aminotransferase with aspartate at low pH reveals dual routes in the enzyme substrate association process. Biochemistry. 36:1997;13558-13569.
29. 6dependent enzyme with asymmetry in structure and active site reactivity. Proc. Natl Acad. Sci. USA. 94:1997;4866-4871.
30. Hirsch H., Greenberg D. M. Studies on phosphoserine aminotransferase of sheep brain. J. Biol. Chem. 242:1967;2283-2287.
31. Hodel A., Kim S.-H., Brünger A. T. Model bias in macromolecular crystal structures. Acta Crystallog. sect. A. 48:1992;851-859.
32. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:1993;123-138.
33. Ichihara A., Greenberg D. M. Further studies on the pathway of serine formation from carbohydrate. J. Biol. Chem. 224:1957;331-341.
34. Inoue K., Kuramitsu S., Okamoto A., Hirotsu K., Higuchi T., Morino Y., Kagamiyama H. Tyr225 in aspartate aminotransferase: contribution of the hydrogen bond between Tyr225 and coenzyme to the catalytic reaction. J. Biochem. 109:1991;570-576.
35. Jäger J., Moser M., Sauder U., Jansonius J. N. Crystal structures of Escherichia coli aspartate aminotransferase in two conformations. Comparison of an unliganded open and two liganded closed forms. J. Mol. Biol. 239:1994;285-305.
36. Jansonius J. N., Vincent M. G. Structural basis for catalysis by aspartate aminotransferase. Jurnak F. A., McPherson A. Biological Macromolecules & Assemblies. 1987;187-285 John Wiley & Sons, New York.
37. Jiang J.-S., Brünger A. T. Protein hydration observed by X-ray diffraction: solvation properties of penicillopepsin and neuraminidase crystal structures. J. Mol. Biol. 243:1994;100-115.
38. John R. A. Pyridoxal phosphate-dependent enzymes. Biochim. Biophys. Acta. 1248:1995;81-96.
39. Jones T. A., Zou J.-Y., Cowan S. W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
40. Kallen J., Kania M., Markovic-Housley Z., Vincent M. G., Jansonius J. N. Crystallographic and solution studies on phosphoserine aminotransferase from Escherichia coli. Christen P., Korpela T. Biochemistry of Vitamin B6. 1987;157-160 Birkhäuser Verlag, Basel.
41. Kamitori S., Okamoto A., Hirotsu K., Higushi T., Kuramitsu S., Kagamiyama H., Matsuura Y., Katsube Y. Three-dimensional structures of aspartate aminotransferase from Escherichia coli and its mutant enzyme at 2.5 Å resolution. J. Biochem. 108:1990;175-184.
42. Kirsch J. F., Eichele G., Ford G. C., Vincent M. G., Jansonius J. N., Gehring H., Christen P. Mechanism of action of aspartate aminotransferase proposed on the basis of its spatial structure. J. Mol. Biol. 174:1984;497-525.
43. Kleywegt G. J. Dictionaries for heteros. CCP4/ESF-EACBM Newsletter Protein Crystallog. 31:1995;45-50.
44. Kleywegt G. J., Brünger A. T. Checking your imagination: applications of the free R value. Structure. 4:1996;897-904.
45. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
46. Kuramitsu S., Hiromi K., Hayashi H., Morino Y., Kagamiyama H. Pre-steady state kinetics of Escherichia coli aspartate aminotransferase catalyzed reactions and thermodynamic aspects of its substrate specificity. Biochemistry. 29:1990;5469-5476.
47. Laskowski R. A., MacArthur M. W., Moss D. S., Thornton J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
48. Lewendon, A. 1984, Studies on the 5-enolpyruvylshikimate 3-phosphate synthase of Escherichia coli. PhD thesis, University of Glasgow, Scotland.
49. Lund K., Merril D. K., Guynn R. W. Purification and properties of phosphoserine aminotransferase from bovine liver. Arch. Biochem. Biophys. 254:1987;319-328.
50. Luzzati V. Traitement statistique des erreurs dans la détermination des structures cristallines. Acta Crystallog. 5:1952;802-810.
51. Markovic-Housley Z., Schirmer T., Hohenester E., Khomutov A. R., Khomutov R. M., Karpeisky M. Y., Sandmeier E., Christen P., Jansonius J. N. Crystal structures and solution studies of oxime adducts of mitochondrial aspartate aminotransferase. Eur. J. Biochem. 236:1996;1025-1032.
52. McKitrick J. C., Pizer L. I. Regulation of phosphoglycerate dehydrogenase levels and effect on serine synthesis in Escherichia coli K-12. J. Bacteriol. 141:1980;235-245.
53. McPhalen C. A., Vincent M. G., Jansonius J. N. X-ray structure refinement and comparison of three forms of mitochondrial aspartate aminotransferase. J. Mol. Biol. 225:1992a;495-517.
54. McPhalen C. A., Vincent M. G., Picot D., Jansonius J. N., Lesk A. M., Chothia C. Domain closure in mitochondrial aspartate aminotransferase. J. Mol. Biol. 227:1992b;197-213.
55. Mehta P. K., Christen P. Homology of pyridoxal-5′-phosphate-dependent aminotransferases with the cobC (cobalamin synthesis),nifS (nitrogen fixation) pabC (p -aminobenzoate synthesis) and malY (abolishing endogenous induction of the maltose system) gene products. Eur. J. Biochem. 211:1993;373-376.
56. Mehta P. K., Christen P. Homology of 1-aminocyclopropane-1-carboxylate synthase, 8-amino-7-oxononanoate synthase, 2-amino-6-caprolactam racemase, 2,2-dialkylglycine decarboxylase, glutamate-1-semialdehyde 2,1-aminomutase and isopenicillin-N-epimerase with aminotransferases. Biochem. Biophys. Res. Commun. 198:1994;138-143.
57. Mehta P. K., Hale T. I., Christen P. Aminotransferases: demonstration of homology and division into evolutionary subgroups. Eur. J. Biochem. 214:1993;549-561.
58. Merrit E. A., Murphy M. E. P. Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallog. sect. D. 50:1994;869-873.
59. Messerschmidt A., Pflugrath J. J. Crystal orientation and X-ray pattern prediction routines for area detector diffractometer systems in macromolecular crystallography. J. Appl. Crystallog. 20:1987;306-315.
60. Momany C., Ernst S., Ghosh R., Chang N.-L., Hackert M. L. Crystallographic structure of a PLP-dependent ornithine decarboxylase from Lactobacillus 30a to 3.0 Å resolution. J. Mol. Biol. 252:1995a;643-655.
61. Momany C., Ghosh R., Hackert M. L. Structural motifs for pyridoxal-5′phosphate binding in decarboxylases: an analysis based on the crystal structure of the Lactobacillus 30a ornithine decarboxylase. Protein Sci. 4:1995b;849-854.
62. 6-dependent enzymes. PhD thesis, University of Basel, Switzerland.
63. Moser M., Müller R., Battchikova N., Koivulehto M., Korpela T., Jansonius J. N. Crystallization and preliminary X-ray analysis of phosphoserine aminotransferase from Bacillus circulans subsp. alkalophilus. Protein Sci. 5:1996;1426-1428.
64. O'Gaora P., Maskel D., Coleman D., Cafferkey M., Dougan G. Cloning and characterization of the serC and aroA genes of Yersinia enterocolitica, and construction of an aroA mutant. Gene. 84:1989;23-30.
65. Otwinowski Z. Maximum likelihood refinement of heavy atom parameters. Wolf W., Evans P. R., Leslie A. G. W. Isomorphous Replacement and Anomalous Scattering. 1991;80-85 SERC Daresbury Laboratory, Warrington.
66. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
67. Ouzounis C., Sander C. Homology of the NifS family of proteins to a new class of pyridoxal phosphate-dependent enzymes. FEBS Letters. 322:1993;159-164.
68. Pizer L. I. The pathway and control of serine biosynthesis in Escherichia coli. J. Biol. Chem. 238:1963;3934-3944.
69. Read R. J. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallog. sect. A. 42:1986;140-149.
70. Reynolds P. H. S., Hine A., Rodber K. Serine metabolism in legume nodules: purification and properties of phosphoserine aminotransferase. Physiol. Plant. 74:1988;194-199.
71. Rice L. M., Brünger A. T. Torsion angle dynamics: reduced variable conformational sampling enhances crystallographic structure refinement. Proteins: Struct. Funct. Genet. 19:1994;277-290.
72. Saito K., Takagi Y., Ling H. C., Takahashi H., Noji M. Molecular cloning, characterization and expression of cDNA encoding phosphoserine aminotransferase involved in phosphorylated pathway of serine biosynthesis from spinach. Plant Mol. Biol. 33:1997;359-366.
73. Sandmeier E., Hale T. I., Christen P. Multiple evolutionary origin of pyridoxal-5′-phosphate-dependent amino acid decarboxylases. Eur. J. Biochem. 221:1994;997-1002.
74. Schmidt L. S., Sojka G. A. Enzymes of serine biosynthesis in Rhodopseudomonas capsulata. Arch. Biochem. Biophys. 159:1973;475-482.
75. Shen B. W., Hennig M., Hohenester E., Jansonius J. N., Schirmer T. Crystal structure of human recombinant ornithine aminotransferase. J. Mol. Biol. 277:1998;81-102.
76. Smith D. L., Almo S. C., Toney M. D., Ringe D. 2.8 Å resolution crystal structure of an active-site mutant of aspartate aminotransferase fromEscherichia coli. Biochemistry. 28:1989;8161-8167.
77. Stark W., Kallen J., Markovic-Housley Z., Fol B., Kania M., Jansonius J. N. The three-dimensional structure of phosphoserine aminotransferase from Escherichia coli. Fukui T., Kagamiyama H., Soda K., Wada H. Enzymes Dependent on Pyridoxal Phosphate and Other Carbonyl Compounds as Cofactors. 1991;111-115 Pergamon Press, Oxford.
78. Stolz M., Dornemann D. Purification, characterization and N-terminal sequence of phosphoserine aminotransferase from the green algaScenedesmus obliquus , mutant C-2 A. Z. Naturforschung. 49c:1994;63-69.
79. Stolz M., Dornemann D. Kinetic characteristics, substrate specificity and catalytic properties of phosphoserine aminotransferase from the green alga Scenedesmus obliquus, mutant C-2 A. Z. Naturforschung. 50c:1995;630-637.
80. Sugio S., Petsko G. A., Manning J. M., Soda K., Ringe D. Crystal structure of a D-amino acid aminotransferase: how the protein controls stereoselectivity. Biochemistry. 34:1995;9661-9669.
81. Toney M. D., Hohenester E., Cowan S. W., Jansonius J. N. Dialkylglycine decarboxylase structure: bifunctional active site and alkali metal sites. Science. 261:1993;756-759.
82. Toney M. D., Hohenester E., Keller J. W., Jansonius J. N. Structural and mechanistic analysis of two refined crystal structures of the pyridoxal-phosphate-dependent enzyme dialkylglycine decarboxylase. J. Mol. Biol. 245:1995;151-179.
83. Umbarger H. E., Umbarger M. E., Siu P. M. L. Biosynthesis of serine in Escherichia coli and Salmonella typhimurium. J. Bacteriol. 85:1963;1431-1439.
84. Walsh D. A., Sallach H. J. Comparative studies on the pathways for serine biosynthesis in animal tissues. J. Biol. Chem. 241:1966;4068-4076.
85. Walton N. J., Woolhouse H. W. Enzymes of serine and glycine metabolism in leaves and non-photosynthetic tissues of Pisum sativum L. Planta. 167:1986;119-128.
86. Watanabe N., Sakabe K., Sakabe N., Higashi T., Sasaki K., Aibara S., Morita Y., Yonaha K., Toyama S., Fukutani H. Crystal structure analysis of ω-amino acid:pyruvate aminotransferase with a newly developed Weissenberg camera and an imaging plate using synchrotron radiation. J. Biochem. 105:1989;1-3.
87. Yano T., Mizuno T., Kagamiyama H. A hydrogen-bonding network modulating enzyme function: asparagine-194 and tyrosine-225 of Escherichia coli aspartate aminotransferase. Biochemistry. 32:1993;1810-1815.
88. Zheng L., White R. H., Cash V. L., Jack R. F., Dean D. R. Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc. Natl Acad. Sci. USA. 90:1993;2754-2758.
89. Zheng L., White R. H., Cash V. L., Dean D. R. Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry. 33:1994;4714-4720.
90. Zvelebil M. J., Barton G. J., Taylor W. R., Sternberg M. J. E. Prediction of protein secondary structure and active sites using the alignment of homologous sequences. J. Mol Biol. 195:1987;957-961.