Mechanism for multiple-substrates recognition of a-aminoadipate aminotransferase from Thermus thermophilus

Proteins: Structure, Function and Bioinformatics

Volumn 75, Issue 2, 2009, Pages 348-359

  Tomita, Takeo ^a   Miyagawa, Tomoharu ^a   Miyazaki, Takashi ^a   Fushinobu, Shinya ^a   Kuzuyama, Tomohisa ^a   Nishiyama, Makoto ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b RIKEN Harima Institute Research   (Japan)

Author keywords

Aminotransferase; Crystal structure; Induced fit; Lysine biosynthesis; Thermostability

Indexed keywords

2 AMINOADIPATE AMINOTRANSFERASE; AMINOADIPIC ACID; ARGININE; LEUCINE; N PHOSPHOPYRIDOXYL ALPHA AMINOADIPIC ACID; N PHOSPHOPYRIDOXYL LEUCINE; PYRIDOXAL 5 PHOSPHATE; UNCLASSIFIED DRUG; 2 AMINOADIPIC ACID; AMINOTRANSFERASE; DRUG DERIVATIVE; KYNURENINE OXOGLUTARATE TRANSAMINASE; KYNURENINE-OXOGLUTARATE TRANSAMINASE; N PHOSPHOPYRIDOXYL ALPHA AMINOADIPATE; N PHOSPHOPYRIDOXYLLEUCINE; N-PHOSPHOPYRIDOXYL-ALPHA-AMINOADIPATE; N-PHOSPHOPYRIDOXYLLEUCINE;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME STABILITY; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; THERMOSTABILITY; THERMUS THERMOPHILUS; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; HEAT; HUMAN; METABOLISM; POINT MUTATION; PROTEIN CONFORMATION; STRUCTURAL HOMOLOGY;

GLUTA; MAMMALIA; THERMUS THERMOPHILUS;

2-AMINOADIPATE TRANSAMINASE; 2-AMINOADIPIC ACID; ENZYME STABILITY; HOT TEMPERATURE; HUMANS; LEUCINE; POINT MUTATION; PROTEIN CONFORMATION; PYRIDOXAL PHOSPHATE; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; THERMUS THERMOPHILUS; TRANSAMINASES;

EID: 66149104738     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22245     Document Type: Article

References (47)

1. Broquist HP. Lysine biosynthesis (yeast). Methods Enzymol 1971; 17:112-129.
2. Rico B, Alberati-Giani D, Malherbe P, Kohler C, Broger C, Cesura AM. Cloning and functional expression of a soluble form of kynu-renine/a- aminoadipate aminotransferase from rat kidney. J Biol Chem 1995;270:29330-29335.
3. Vogel HJ. Distribution of lysine pathway among fungi: evolutionary implications. Am Natl 1964;98:446-55.
4. Kobashi N, Nishiyama M, Tanokura M. Aspartate kinase-independ-ent lysine synthesis in an extremely thermophilic bacterium. Ther-mus thermophilics: lysine is synthesized via a-aminoadipic acid, not via diaminopimeric acid. J Bacteriol 1999;181:1713-1718.
5. Miyazaki J, Kobashi N, Nishiyama M, Yamane H. Functional and evolutionary relationship between arginine biosynthesis and prokary-otic lysine biosynthesis through a-aminoadipate. J Bacteriol 2001; 183:5067-5073.
6. Miyazaki J, Kobashi N, Nishiyama M, Yamane H. Characterization of homoisocitrate dehydrogenase involved in lysine biosynthesis of an extremely thermophilic bacterium. Thermus thermophilus HB27, and evolutionary implication of (b-decarboxylating dehydrogenase J Biol Chem 2003;278:1864-1871.
7. Miyazaki J, Kobashi N, Fujii T, Nishiyama M, Yamane H. Characterization of a lysK gene as an argE homolog in Thermus thermophi-lus HB27. FEBS Lett 2002;512:269-274.
8. Nishida H, Nishiyama M, Kobashi N, Kosuge T, Hoshino T, Yamane H. A prokaryotic gene cluster involved in synthesis of ly-sine through the amino adipate pathway: a key to the evolution of amino acid biosynthesis. Genome Res 1999;9:1175-1183.
9. Irvin SD, Bhattacharjee JK. A unique fungal lysine biosynthesis enzyme shares a common ancestor with tricarboxylic acid cycle and leucine biosynthetic enzymes found in diverse organisms. J Mol Evol 1998;46:401-08.
10. Cunin R, Glandsorff N, Oierard A, Stalon V. Biosynthesis and metabolism of arginine in bacteria. Microbiol Rev 1986;50:314-352.
11. Miyazaki T, Miyazaki J, Yamane H, Nishiyama M. a-Aminoadipate aminotransferase from an extremely thermophilic bacterium. Ther-mus thermophilus Microbiology 2004;150:2327-2334.
12. Wulandari AP, Miyazaki J, Kobashi N, Nishiyama M, Hoshino T, Yamane H. Characterization of bacterial homocitrate synthase involved in lysine biosynthesis. FEBS Lett 2002;522:35-40.
13. Iraqui I, Vissers S, Cartiaux M, Urrestarazu A. Characterisation of Saccharomyces cerevisiae ARO8 and ARO9 genes encoding aromatic aminotransferases I and II reveals a new aminotransferase subfamily. Mol Gen Genet 1998;257:238-248.
14. Parsons CG, Danysz W, Quack G, Hartmann S, Lorenz B, Wollenburg C, Baran L, Przegalinski E, Kostowski W, Krzascik P, Chizh B, Headley PM. Novel systemically active antagonists of the glycine site of the N- methyl-D-aspartate receptor: electrophysiological, biochemical and behavioral characterization. J Pharmacol Exp Ther 1997;283:1264-1275.
15. 7 nicotinic receptor expression: physiopathological implications. J Neurosci 2001;21: 7463-7473.
16. Erhardt S, Schwieler L, Engberg G. Kynurenic acid and schizophrenia. Adv Exp Med Biol 2003;527:155-165.
17. Sapko MT, Guidetti P, Yu P, Tagle DA, Pellicciari R, Schwarcz R. Endogenous kynurenate controls the vulnerability of striatal neurons to quinolinate: implications for Huntington's disease. Exp Neurol 2006;197:31-40.
18. Rossi F, Garavaglia S, Montalbano V, Walsh MA, Rizzi M. Crystal structure of human kynurenine aminotransferase II, a drug target for the treatment of schizophrenia. J Biol Chem 2008;283:3559-3566.
19. Han Q, Robinson H, Li J. Crystal structure of human kynurenine aminotransferase II. J Biol Chem 2008;283:3567-3573.
20. Chon H, Matsumura H, Koga Y, Takano K, Kanaya S. Crystal structure of a human kynurenine aminotransferase II homologue from Pyrococcus horikoshii OT3 at 2.20 A resolution. Proteins 2005;61: 685-688.
21. Islam MM, Goto M, Miyahara I, Hirotsu K, Hayashi H. Binding of C5-dicarboxylic substrate to aspartate aminotransferase: implications for the conformational change at the transaldimination step. Biochemistry 2005;44:8218-8229.
22. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-326.
23. Vagin A, Teplyakov A. MOLREP: an automated program for molecular replacement. J Appl Crystallogr 1997;30:1022-1025.
24. Collaborative Computational Project N. The CCP4 suite: programs for protein crystallography. Acta Crystallogr 1994;D50:760-763.
25. McRee DE. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J Struct Biol 1999;125: 156-165.
26. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr 2004;D60:2126-2132.
27. 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 & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr 1998;D54:905-921.
28. Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolec-ular structures by the maximum-likelihood method. Acta Crystal-logr 1997;D53:240-255.
29. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PRO-CHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
30. Merritt EA, Bacon DJ. Raster3D: photorealistic molecular graphics. Methods Enzymol 1998;277:505-524.
31. Nakai T, Okada K, Akutsu S, Miyahara I, Kawaguchi S, Kato R, Kuramitsu S, Hirotsu K. Structure of Thermus thermophilus HB8 aspartate aminotransferase and its complex with maleate. Biochemistry 1999;38:2413-2424.
32. Okamoto A, Nakai Y, Hayashi H, Hirotsu K, Kagamiyama H. Crystal structures of Paracoccus denitrificans aromatic amino acid ami-notransferase: a substrate recognition site constructed by rearrangement of hydrogen bond network. J Mol Biol 1998;280:443-461.
33. Jensen RA, Gu W. Evolutionary recruitment of biochemically specialized subdivisions of Family I within the protein superfamily of aminotransferases. J Bacteriol 1996;178:2161-2171.
34. Urrestarazu A, Vissers S, Iraqui I, Grenson M. Phenylalanine-and tyrosine-auxotrophic mutants of Saccharomyces cerevisiae impaired in transamination. Mol Gen Genet 1998;257:230-237.
35. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: 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.
36. Kumar S, Tamura K, Jakobsen IB, Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 2001;17:1244-1245.
37. Gouet P, Courcelle E, Stuart DI, Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999;15:305-308.
38. '-phosphate Schiff base of aspartate amino-transferase lowers its pKa in the unliganded enzyme and is crucial for the successive increase in the pKa during catalysis. Biochemistry 1998;37:15076-15085.
39. Hayashi H, Mizuguchi H, Miyahara I, Nakajima Y, Hirotsu K, Kagamiyama H. Conformational change in aspartate aminotransfer-ase on substrate binding induces strain in the catalytic group and enhances catalysis. J Biol Chem 2003;278:9481-9488.
40. Jager J, Moser M, Sauder U, Jansonius JN. Crystal structures of Escherichia coli aspartate aminotransferase in two conformations. Comparison of an unliganded open and two liganded closed forms. J Mol Biol 1994;239:285-305.
41. McPhalen CA, Vincent MG, Picot D, Jansonius JN, Lesk AM, Cho-thia C. Domain closure in mitochondrial aspartate aminotransfer-ase. J Mol Biol 1992;227:197-213.
42. Nobe Y, Kawaguchi S, Ura H, Nakai T, Hirotsu K, Kato R, Kura-mitsu S. The novel substrate recognition mechanism utilized by aspartate aminotransferase of the extreme thermophile Thermus thermophilus HB8. J Biol Chem 1998;273:29554-29564.
43. Inoue K, Kuramitsu S, Aki K, Watanabe Y, Takagi T, Nishigai M, Ikai A, Kagamiyama H. Branched-chain amino acid aminotransfer-ase of Escherichia coli: overproduction and properties. J Biochem (Tokyo) 1988;104:777-784.
44. Okada K, Hirotsu K, Hayashi H, Kagamiyama H. Structures of Escherichia coli branched-chain amino acid aminotransferase and its complexes with 4-methylvalerate and 2-methylleucine: induced fit and substrate recognition of the enzyme. Biochemistry 2001;40: 7453-7463.
45. Goto M, Miyahara I, Hayashi H, Kagamiyama H, Hirotsu K. Crystal structures of branched-chain amino acid aminotransferase complexed with glutamate and glutarate: true reaction intermediate and double substrate recognition ofthe enzyme. Biochemistry 2003;42: 3725-3733.
46. Flocco MM, Mowbray SL. Planar stacking interactions of arginine and aromatic side-chains in proteins. J Mol Biol 1994;235:709-717.
47. Robinson-Rechavi M, Alibes A, Godzik A. Contribution of electrostatic interactions, compactness and quaternary structure to protein thermostability: lessons from structural genomics of Thermotoga maritima. J Mol Biol 2006;356:547-557.