Biochemical properties and crystal structure of a β-phenylalanine aminotransferase from Variovorax paradoxus

Applied and Environmental Microbiology

Volumn 79, Issue 1, 2013, Pages 185-195

  Crismaru, Ciprian G ^a   Wybenga, Gjalt G ^a   Szymanski, Wiktor ^b   Wijma, Hein J ^a   Wu, Bian ^a   Bartsch, Sebastian ^a   de Wildeman, Stefaan ^c   Poelarends, Gerrit J ^d   Feringa, Ben L ^b   Dijkstra, Bauke W ^a   Janssen, Dick B ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c DSM Pharmaceutical Products   (Netherlands)

^d UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

16S RRNA GENE; 2-OXOGLUTARATE; AMINO DONORS; AMINOTRANSFERASE; AMINOTRANSFERASE ACTIVITIES; BIOCHEMICAL PROPERTIES; DNA LIBRARY; ENANTIOMERIC EXCESS; ENANTIOSELECTIVE; ENZYME ASSAYS; KINETIC RESOLUTION; MESORHIZOBIUM SP; NITROGEN SOURCES; OPTIMUM TEMPERATURE; PARTIAL GENOMES; PHENYL RINGS; PYRUVATES; RECOMBINANT ENZYMES; SELECTIVE ENRICHMENT; SEQUENCE MOTIFS; SPECIFIC ACTIVITY; STRUCTURAL SIMILARITY; SUBSTRATE RANGE; VARIOVORAX PARADOXUS;

CLONING; ENANTIOSELECTIVITY; ENZYMES; ESCHERICHIA COLI; GENES; RNA;

AMINO ACIDS;

AMINOTRANSFERASE; BACTERIAL DNA; PHENYLALANINE; PHENYLALANINE AMINOTRANSFERASE; RECOMBINANT PROTEIN; RIBOSOME DNA; RNA 16S;

AMINO ACID; BACTERIUM; BIOASSAY; BIOCHEMICAL COMPOSITION; CLONE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; GENE EXPRESSION; REACTION KINETICS; RECOMBINATION;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; COMAMONADACEAE; DNA SEQUENCE; ENZYME SPECIFICITY; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; MOLECULAR WEIGHT; PROTEIN CONFORMATION; TEMPERATURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; COMAMONADACEAE; CRYSTALLOGRAPHY, X-RAY; DNA, BACTERIAL; DNA, RIBOSOMAL; ESCHERICHIA COLI; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PHENYLALANINE; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SUBSTRATE SPECIFICITY; TEMPERATURE; TRANSAMINASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MESORHIZOBIUM; VARIOVORAX PARADOXUS;

EID: 84871915345     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02525-12     Document Type: Article

References (81)

1. Seebach D, Beck A, Bierbaum D. 2004. The world of beta- and gammapeptides comprised of homologated proteinogenic amino acids and other components. Chem. Biodivers. 1:1111-1239.
2. Burley SK, David PR, Lipscomb WN. 1991. Leucine aminopeptidase: bestatin inhibition and a model for enzyme-catalyzed peptide hydrolysis. Proc. Natl. Acad. Sci. U. S. A. 88:6916-6920.
3. Geueke B, Kohler H. 2007. Bacterial beta-peptidyl aminopeptidases: on the hydrolytic degradation of beta-peptides. Appl. Microbiol. Biotechnol. 74:1197-1204.
4. Juaristi E, Soloshonok V. 2005. Enantioselective synthesis of β-amino acids. Wiley-VHC, New York, NY.
5. Shih C, Gossett LS, Gruber JM, Grossman CS, Andis SL, Schultz RM, Worzalla JF, Corbett TH, Metz JT. 1999. Synthesis and biological evaluation of novel cryptophycin analogs with modification in the betaalanine region. Bioorg. Med. Chem. Lett. 9:69-74.
6. Mekhail TM, Markman M. 2002. Paclitaxel in cancer therapy. Expert Opin. Pharmacother. 3:755-766.
7. Ojima I, Lin S, Wang T. 1999. Recent advances in the medicinal chemistry of taxoids with novel beta-amino acid side chains. Curr. Med. Chem. 6:927-954.
8. Crews P, Manes LV, Boehler M. 1986. Jasplakinolide, a cyclodepsipeptide from the marine sponge, Jaspis sp. Tetrahedron Lett. 27:2797-2800.
9. Weiner B, Szymanski W, Janssen DB, Minnaard AJ, Feringa BL. 2010. Recent advances in the catalytic asymmetric synthesis of beta-amino acids. Chem. Soc. Rev. 39:1656-1691.
10. Liljeblad A, Kanerva LT. 2006. Biocatalysis as a profound tool in the preparation of highly enantiopure beta-amino acids. Tetrahedron 62: 5831-5854.
11. Rehdorf J, Mihovilovic MD, Bornscheuer UT. 2010. Exploiting the regioselectivity of Baeyer-Villiger monooxygenases for the formation of beta-amino acids and beta-amino alcohols. Angew. Chem. Int. Ed. Engl. 49:4506-4508.
12. Chirpich TP, Zappia V, Costilow RN, Barker HA. 1970. Lysine 2,3-aminomutase. Purification and properties of a pyridoxal phosphate and S-adenosylmethionine-activated enzyme. J. Biol. Chem. 245:1778-1789.
13. Ruzicka FJ, Frey PA. 2007. Glutamate 2,3-aminomutase: a new member of the radical SAM superfamily of enzymes. Biochim. Biophys. Acta 1774: 286-296.
14. Wu B, Szymanski W, Heberling MM, Feringa BL, Janssen DB. 2011. Aminomutases: mechanistic diversity, biotechnological applications and future perspectives. Trends Biotechnol. 29:352-362.
15. Cronan JE .Jr. 1980. Beta-alanine synthesis in Escherichia coli. J. Bacteriol. 141:1291-1297.
16. Christianson CV, Montavon TJ, Festin GM, Cooke HA, Shen B, Bruner SD. 2007. The mechanism of MIO-based aminomutases in beta-amino acid biosynthesis. J. Am. Chem. Soc. 129:15744-15745.
17. Christen P, Metzler DE. 1985. Transaminases. Wiley, New York, NY.
18. Stirling DI. 1992. The use of aminotransferases for the production of chiral amino acids and amines. In Collins AN, Sheldrake GN, Crosby J (ed), Chirality in industry. Wiley, New York, NY.
19. Kim J, Kyung D, Yun H, Cho BK, Kim BG. 2006. Screening and purification of a novel transaminase catalyzing the transamination of aryl beta-amino acid from Mesorhizobium sp LUK. J. Microbiol. Biotechnol.
20. Shin JS, Kim BG. 2001. Comparison of the omega-transaminases from different microorganisms and application to production of chiral amines. Biosci. Biotechnol. Biochem. 65:1782-1788.
21. Yun H, Lim S, Cho BK, Kim BG. 2004. Omega-amino acid:pyruvate transaminase from Alcaligenes denitrificans Y2k-2: a new catalyst for kinetic resolution of beta-amino acids and amines. Appl. Environ. Microbiol. 70:2529-2534.
22. Percudani R, Peracchi A. 2009. The B6 database: a tool for the description and classification of vitamin B6-dependent enzymatic activities and of the corresponding protein families. BMC Bioinformatics 10:273.
23. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, Bateman A. 2010. The Pfam protein families database. Nucleic Acids Res. 38:D211-D222.
24. Yonaha K, Suzuki K, Minei H, Toyama S. 1983. Distribution of omegaamino acid-pyruvate transaminase and aminobutyrate-alphaketoglutarate transaminase in microorganisms. Agric. Biol. Chem. Tokyo 47:2257-2265.
25. Christen P, Mehta P. 2001. From cofactor to enzymes. The molecular evolution of pyridoxal-5'-phosphate-dependent enzymes. Chem. Rec. 1:436-447.
26. Mehta PK, Hale TI, Christen P. 1993. Aminotransferases-demonstration of homology and division into evolutionary subgroups. Eur. J. Biochem. 214: 549-561.
27. Kim J, Kyung D, Yun H, Cho BK, Seo JH, Cha M, Kim BG. 2007. Cloning and characterization of a novel beta-transaminase from Mesorhizobium sp. strain LUK: a new biocatalyst for the synthesis of enantiomerically pure beta-amino acids. Appl. Environ. Microbiol. 73:1772-1782.
28. Hwang BY, Cho BK, Yun H, Koteshwar K, Kim BG. 2005. Revisit of aminotransferase in the genomic era and its application to biocatalysis. J. Mol. Catal. B Enzym. 37:47-55.
29. Koszelewski D, Lavandera I, Clay D, Guebitz GM, Rozzell D, Kroutil W. 2008. Formal asymmetric biocatalytic reductive amination. Angew. Chem. Int. Ed. Engl. 47:9337-9340.
30. Koszelewski D, Tauber K, Faber K, Kroutil W. 2010. Omegatransaminases for the synthesis of non-racemic alpha-chiral primary amines. Trends Biotechnol. 28:324-332.
31. Rozzell JD. May 1985. Production of amino acids by transamination. US patent 4518692.
32. Stewart JD. 2001. Dehydrogenases and transaminases in asymmetric synthesis. Curr. Opin. Chem. Biol. 5:120-129.
33. Taylor PP, Pantaleone DP, Senkpeil RF, Fotheringham IG. 1998. Novel biosynthetic approaches to the production of unnatural amino acids using transaminases. Trends Biotechnol. 16:412-418.
34. Wu B, Szymanski W, Crismaru CG, Feringa BL, Janssen DB. 2012. C-N lyases catalyzing addition of ammonia, amines and amides to C=C and C=O bonds, p 749-778. In Drauz K, Groger H, May O (ed), Enzyme catalysis in organic synthesis. Wiley-VCH, New York, NY.
35. Nowicki C, Hunter GR, Montemartini-Kalisz M, Blankenfeldt W, Hecht H, Kalisz HM. 2001. Recombinant tyrosine aminotransferase from Trypanosoma cruzi: structural characterization and site directed mutagenesis of a broad substrate specificity enzyme. Biochim. Biophys. Acta 1546: 268-281.
36. Rudat J, Brucher BR, Syldatk C. 2012. Transaminases for the synthesis of enantiopure beta-amino acids. AMB Express. 2:11.
37. Szymanski W, Wu B, Weiner B, de Wildeman S, Feringa BL, Janssen DB. 2009. Phenylalanine aminomutase-catalyzed addition of ammonia to substituted cinnamic acids: a route to enantiopure alpha- and beta-amino acids. J. Org. Chem. 74:9152-9157.
38. Janssen DB, Scheper A, Witholt B. 1984. Biodegradation of 2-chloroethanol and 1,2-dichloroethane by pure bacterial cultures. Prog. Ind. Microbiol. 20:169-178.
39. Gabor E, de Vries E, Janssen D. 2004. Construction, characterization, and use of small-insert gene banks of DNA isolated from soil and enrichment cultures for the recovery of novel amidases. Environ. Microbiol. 6:948-958.
40. Hill DW, Walters FH, Wilson TD, Stuart JD. 1979. High performance liquid chromatographic determination of amino acids in the picomole range. Anal. Chem. 51:1338-1341.
41. Woese CR. 1987. Bacterial evolution. Microbiol. Rev. 51:221-271.
42. Poelarends G, Wilkens M, Larkin M, van Elsas J, Janssen D. 1998. Degradation of 1,3-dichloropropene by Pseudomonas cichorii 170. Appl. Environ. Microbiol. 64:2931-2936.
43. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Staskawicz B, Dahlbeck D, Keen N, Napoli C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
45. Brady OL, Elsmie GV. 1926. The use of 2:4-dinitrophenylhydrazine as a reagent for aldehydes and ketones. Analyst 51:77-78.
46. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li WZ, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7:539.
47. Drummond AJ AB, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A. 2010. Geneious v5.5, 5.5.3 ed. Biomatters, Auckland, New Zealand.
48. Wybenga GG, Crismaru CG, Janssen DB, Dijkstra BW. 2012. Structural determinants of the beta-selectivity of a bacterial aminotransferase. J. Biol. Chem. 287:28495-28502.
49. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62:72-82.
50. Kabsch W. 2010. Integration, scaling, space-group assignment and postrefinement. Acta Crystallogr. D Biol. Crystallogr. 66:133-144.
51. Bailey S. 1994. The CCP4 Suite-programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50:760-763.
52. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J. Appl. Crystallogr. 40: 658-674.
53. Langer G, Cohen SX, Lamzin VS, Perrakis A. 2008. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3:1171-1179.
54. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132.
55. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240-255.
56. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66:12-21.
57. Kleywegt GJ, Jones TA. 1998. Databases in protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 54:1119-1131.
58. Schuttelkopf AW, van Aalten DM. 2004. PRODRG: a tool for highthroughput crystallography of protein-ligand complexes. Acta Crystallogr. D Biol. Crystallogr. 60:1355-1363.
59. Holm L, Rosenstrom P. 2010. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38:W545-W549.
60. Krissinel E, Henrick K. 2007. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372:774-797.
61. Davis IW, Baker D. 2009. RosettaLigand docking with full ligand and receptor flexibility. J. Mol. Biol. 385:381-392.
62. Davis IW, Raha K, Head MS, Baker D. 2009. Blind docking of pharmaceutically relevant compounds using RosettaLigand. Protein Sci. 18: 1998-2002.
63. Richter F, Leaver-Fay A, Khare SD, Bjelic S, Baker D. 2011. De novo enzyme design using Rosetta3. PLoS One 6:e19230. 10.1371/ journal.pone.0019230.
64. Krieger E, Koraimann G, Vriend G. 2002. Increasing the precision of comparative models with YASARA NOVA-a self-parameterizing force field. Proteins 47:393-402.
65. OpenEye Scientific Software, Inc. 2010. OEChem TK programming library for chemistry and cheminformatics. OpenEye Scientific Software, Inc., Santa Fe, NM.
66. Zhang Z, Schwartz S, Wagner L, Miller W. 2000. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 7:203-214.
67. Han JI, Choi HK, Lee SW, Orwin PM, Kim J, Laroe SL, Kim TG, O'Neil J, Leadbetter JR, Lee SY, Hur CG, Spain JC, Ovchinnikova G, Goodwin L, Han C. 2011. Complete genome sequence of the metabolically versatile plant growth-promoting endophyte Variovorax paradoxus S110. J. Bacteriol. 193:1183-1190.
68. Bea HS, Park HJ, Lee SH, Yun H. 2011. Kinetic resolution of aromatic beta-amino acids by omega-transaminase. Chem. Commun. (Camb) 47: 5894-5896.
69. Tipton KF. 1996. Patterns of enzyme inhibition, p 115-174. In Engel PC (ed), Enzymology. Academic Press, San Diego, CA.
70. Grishin NV, Phillips MA, Goldsmith EJ. 1995. Modeling of the spatial structure of eukaryotic ornithine decarboxylases. Protein Sci. 4:1291-1304.
71. Schneider G, Kack H, Lindqvist Y. 2000. The manifold of vitamin B6 dependent enzymes. Structure 8:R1-R6.
72. John RA, Charteris A. 1978. The reaction of amino-oxyacetate with pyridoxal phosphate-dependent enzymes. Biochem. J. 171:771-779.
73. Markovic-Housley Z, Schirmer T, Hohenester E, Khomutov AR, Khomutov RM, Karpeisky MY, Sandmeier E, Christen P, Jansonius JN. 1996. Crystal structures and solution studies of oxime adducts of mitochondrial aspartate aminotransferase. Eur. J. Biochem. 236:1025-1032.
74. Stetefeld J, Jenny M, Burkhard P. 2006. Intersubunit signaling in glutamate-1-semialdehyde-aminomutase. Proc. Natl. Acad. Sci. U. S. A. 103: 13688-13693.
75. Lowe PN, Rowe AF. 1985. Aspartate-2-oxoglutarate aminotransferase from Trichomonas vaginalis: identity of aspartate-aminotransferase and aromatic amino-acid aminotransferase. Biochem. J. 232:689-695.
76. Shin JS, Yun H, Jang JW, Park I, Kim BG. 2003. Purification, characterization, and molecular cloning of a novel amine:pyruvate transaminase from Vibrio fluvialis JS17. Appl. Microbiol. Biotechnol. 61:463-471.
77. Sung MH, Tanizawa K, Tanaka H, Kuramitsu S, Kagamiyama H, Soda K. 1990. Purification and characterization of thermostable aspartateaminotransferase from a thermophilic Bacillus species. J. Bacteriol. 172: 1345-1351.
78. Shin JS, Kim BG. 2002. Exploring the active site of amine:pyruvate aminotransferase on the basis of the substrate structure-reactivity relationship: how the enzyme controls substrate specificity and stereo selectivity. J. Org. Chem. 67:2848-2853.
79. Okamoto A, Nakai Y, Hayashi H, Hirotsu K, Kagamiyama H. 1998. Crystal structures of Paracoccus denitrificans aromatic amino acid aminotransferase: a substrate recognition site constructed by rearrangement of hydrogen bond network. J Mol. Biol. 280:443-461.
80. Eliot AC, Kirsch JF. 2004. Pyridoxal phosphate enzymes: mechanistic, structural, and evolutionary considerations. Annu. Rev. Biochem. 73: 383-415.
81. Hohne M, Schatzle S, Jochens H, Robins K, Bornscheuer UT. 2010. Rational assignment of key motifs for function guides in silico enzyme identification. Nat. Chem. Biol. 6:807-813.