Free energy analysis of ω-transaminase reactions to dissect how the enzyme controls the substrate selectivity

Enzyme and Microbial Technology

Volumn 49, Issue 4, 2011, Pages 380-387

  Park, Eul Soo ^a   Shin, Jong Shik ^a  

^a Yonsei University   (South Korea)

Author keywords

Binding energy; Protein flexibility; Substrate selectivity; Transaminase; Transition state

Indexed keywords

ACTIVE SITE; ACTIVE SITE RESIDUES; BULKY SUBSTITUENTS; CHIRAL AMINES; ENZYME-SUBSTRATE BINDING; FREE ENERGY ANALYSIS; MICHAELIS COMPLEX; NATURALLY OCCURRING; PARACOCCUS DENITRIFICANS; PH DEPENDENCE; PROTEIN FLEXIBILITY; STERIC CONSTRAINT; STRUCTURAL DIFFERENCES; SUBSTRATE BINDING; SUBSTRATE SELECTIVITY; THERMODYNAMIC INVESTIGATION; TRANSAMINASE; TRANSITION STATE;

ACTIVATION ANALYSIS; ACTIVATION ENERGY; AMINES; BINDING ENERGY; ENERGY MANAGEMENT; ENZYMES; FREE ENERGY; KETONES; POTENTIAL ENERGY; REACTION INTERMEDIATES;

SUBSTRATES;

AMINOTRANSFERASE; OMEGA TRANSAMINASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CATALYSIS; ENERGY YIELD; ENZYME KINETICS; ENZYME MECHANISM; NONHUMAN; PARACOCCUS DENITRIFICANS; THERMODYNAMICS;

BINDING SITES; CATALYSIS; CATALYTIC DOMAIN; ESCHERICHIA COLI; GENETIC ENGINEERING; HYDROGEN-ION CONCENTRATION; KINETICS; MUTAGENESIS, SITE-DIRECTED; PARACOCCUS; PROTEIN BINDING; RECOMBINATION, GENETIC; SUBSTRATE SPECIFICITY; THERMODYNAMICS; TRANSAMINASES;

PARACOCCUS DENITRIFICANS;

EID: 80051792179     PISSN: 01410229     EISSN: 18790909     Source Type: Journal    
DOI: 10.1016/j.enzmictec.2011.06.019     Document Type: Article

References (57)

1. Breuer M., Ditrich K., Habicher T., Hauer B., Keßeler M., Stürmer R., et al. Industrial methods for the production of optically active intermediates. Angew Chem Int Ed 2004, 43:788-824.
2. Farlow M.R., Cummings J.L. Effective pharmacologic management of Alzheimer's disease. Am J Med 2007, 120:388-397.
3. Fuchs M., Koszelewski D., Tauber K., Kroutil W., Faber K. Chemoenzymatic asymmetric total synthesis of (S)-Rivastigmine using ω-transaminases. Chem Commun 2010, 46:5500-5502.
4. Logigian E.L., Martens W.B., Moxley R.T., McDermott M.P., Dilek N., Wiegner A.W., et al. Mexiletine is an effective antimyotonia treatment in myotonic dystrophy type 1. Neurology 2010, 74:1441-1448.
5. Sasaki K., Makita N., Sunami A., Sakurada H., Shirai N., Yokoi H., et al. Unexpected mexiletine responses of a mutant cardiac Na+ channel implicate the selectivity filter as a structural determinant of antiarrhythmic drug access. Mol Pharmacol 2004, 66:330-336.
6. Koszelewski D., Pressnitz D., Clay D., Kroutil W. Deracemization of mexiletine biocatalyzed by ω-transaminases. Org Lett 2009, 11:4810-4812.
7. Omvik P., Lund-Johansen P. Long-term hemodynamic effects at rest and during exercise of newer antihypertensive agents and salt restriction in essential hypertension: review of epanolol, doxazosin, amlodipine, felodipine, diltiazem, lisinopril, dilevalol, carvedilol, and ketanserin. Cardiovasc Drugs Ther 1993, 7:193-206.
8. Turner N.J. Directed evolution drives the next generation of biocatalysts. Nat Chem Biol 2009, 5:567-573.
9. Gotor V. Non-conventional hydrolase chemistry: amide and carbamate bond formation catalyzed by lipases. Bioorg Med Chem 1999, 7:2189-2197.
10. Gotor-Fernández V., Gotor V. Biocatalytic routes to chiral amines and amino acids. Curr Opin Drug Disc Dev 2009, 12:784-797.
11. Ismail H., Lau R.M., Van Rantwijk F., Sheldon R.A. Fully enzymatic resolution of chiral amines: acylation and deacylation in the presence of Candida antarctica lipase B. Adv Synth Catal 2008, 350:1511-1516.
12. Carr R., Alexeeva M., Dawson M.J., Gotor-Fernández V., Humphrey C.E., Turner N.J. Directed evolution of an amine oxidase for the preparative deracemisation of cyclic secondary amines. ChemBioChem 2005, 6:637-639.
13. Carr R., Alexeeva M., Enright A., Eve T.S.C., Dawson M.J., Turner N.J. Directed evolution of an amine oxidase possessing both broad substrate specificity and high enantioselectivity. Angew Chem Int Ed 2003, 42:4807-4810.
14. Shin J.S., Kim B.G. Kinetic modeling of ω-transamination for enzymatic kinetic resolution of α-methylbenzylamine. Biotechnol Bioeng 1998, 60:534-540.
15. Shin J.S., Kim B.G., Liese A., Wandrey C. Kinetic resolution of chiral amines with ω-transaminase using an enzyme-membrane reactor. Biotechnol Bioeng 2001, 73:179-187.
16. Hanson R.L., Davis B.L., Chen Y., Goldberg S.L., Parker W.L., Tully T.P., et al. Preparation of (R)-amines from racemic amines with an (S)-amine transaminase from Bacillus megaterium. Adv Synth Catal 2008, 350:1367-1375.
17. Truppo M.D., Turner N.J., Rozzell J.D. Efficient kinetic resolution of racemic amines using a transaminase in combination with an amino acid oxidase. Chem Commun 2009, 2127-2129.
18. Höhne M., Robins K., Bornscheuer U.T. A protection strategy substantially enhances rate and enantioselectivity in ω-transaminase-catalyzed kinetic resolutions. Adv Synth Catal 2008, 350:807-812.
19. Shin J.S., Kim B.G. Asymmetric synthesis of chiral amines with ω-transaminase. Biotechnol Bioeng 1999, 65:206-211.
20. Cassimjee K.E., Branneby C., Abedi V., Wells A., Berglund P. Transaminations with isopropyl amine: equilibrium displacement with yeast alcohol dehydrogenase coupled to in situ cofactor regeneration. Chem Commun 2010, 46:5569-5571.
21. Koszelewski D., Lavandera I., Clay D., Guebitz G.M., Rozzell D., Kroutil W. Formal asymmetric biocatalytic reductive amination. Angew Chem Int Ed 2008, 47:9337-9340.
22. Koszelewski D., Lavandera I., Clay D., Rozzell D., Kroutil W. Asymmetric synthesis of optically pure pharmacologically relevant amines employing ω-transaminases. Adv Synth Catal 2008, 350:2761-2766.
23. Truppo M.D., David Rozzell J., Turner N.J. Efficient production of enantiomerically pure chiral amines at concentrations of 50g/L using transaminases. Org Process Res Dev 2010, 14:234-237.
24. Truppo M.D., Rozzell J.D., Moore J.C., Turner N.J. Rapid screening and scale-up of transaminase catalysed reactions. Org Biomol Chem 2009, 7:395-398.
25. Höhne M., Kühl S., Robins K., Bornscheuer U.T. Efficient asymmetric synthesis of Chiral amines by combining transaminase and pyruvate decarboxylase. ChemBioChem 2008, 9:363-365.
26. Shin J.S., Kim B.G. Exploring the active site of amine:pyruvate aminotransferase on the basis of the substrate structure-reactivity relationship: How the enzyme controls substrate specificity and stereoselectivity. J Org Chem 2002, 67:2848-2853.
27. Hirotsu K., Goto M., Okamoto A., Miyahara I. Dual substrate recognition of aminotransferases. Chem Rec 2005, 5:160-172.
28. Koszelewski D., Tauber K., Faber K., Kroutil W. ω-Transaminases for the synthesis of non-racemic α-chiral primary amines. Trends Biotechnol 2010, 28:324-332.
29. Baumann W.K., Bizzozero S.A., Dutler H. Kinetic investigation of the α-chymotrypsin-catalyzed hydrolysis of peptide substrates. Eur J Biochem 1973, 39:381-391.
30. Zerner B., Bond R.P.M., Bender M.L. Kinetic evidence for the formation of acyl-enzyme intermediates in the α-chymotrypsin-catalyzed hydrolyses of specific substrates. J Am Chem Soc 1964, 86:3674-3679.
31. Gaj T., Mercer A.C., Gersbach C.A., Gordley R.M., Barbas C.F. Structure-guided reprogramming of serine recombinase DNA sequence specificity. Proc Natl Acad Sci USA 2011, 108:498-503.
32. Reetz M.T., Prasad S., Carballeira J.D., Gumulya Y., Bocola M. Iterative saturation mutagenesis accelerates laboratory evolution of enzyme stereoselectivity: rigorous comparison with traditional methods. J Am Chem Soc 2010, 132:9144-9152.
33. Reetz M.T., Kahakeaw D., Lohmer R. Addressing the numbers problem in directed evolution. ChemBioChem 2008, 9:1797-1804.
34. Caglio R., Valetti F., Caposio P., Gribaudo G., Pessione E., Giunta C. Fine-tuning of catalytic properties of catechol 1,2-dioxygenase by active site tailoring. ChemBioChem 2009, 10:1015-1024.
35. Craik C., Largman C., Fletcher T., Roczniak S., Barr P., Fletterick R., et al. Redesigning trypsin: alteration of substrate specificity. Science 1985, 228:291-297.
36. Oue S., Okamoto A., Yano T., Kagamiyama H. Redesigning the substrate specificity of an enzyme by cumulative effects of the mutations of non-active site residues. J Biol Chem 1999, 274:2344-2349.
37. Yano T., Oue S., Kagamiyama H. Directed evolution of an aspartate aminotransferase with new substrate specificities. Proc Natl Acad Sci USA 1998, 95:5511-5515.
38. Park E., Kim M., Shin J.S. One-pot conversion of L-threonine into L-homoalanine: biocatalytic production of an unnatural amino acid from a natural one. Adv Synth Catal 2010, 352:3391-3398.
39. Fersht A. Structure and mechanism in protein science: a guide to enzyme catalysis and protein folding 1998, Freeman, New York.
40. Fersht A.R., Daggett V. Protein folding and unfolding at atomic resolution. Cell 2002, 108:573-582.
41. Fersht A.R., Sato S. Φ-value analysis and the nature of protein-folding transition states. Proc Natl Acad Sci USA 2004, 101:7976-7981.
42. Dobson C.M. Protein folding and misfolding. Nature 2003, 426:884-890.
43. Matouschek A., Kellis J.T., Serrano L., Fersht A.R. Mapping the transition state and pathway of protein folding by protein engineering. Nature 1989, 340:122-126.
44. Iwasaki M., Hayashi H., Kagamiyama H. Protonation state of the active-site Schiff base of aromatic amino acid aminotransferase: modulation by binding of ligands and implications for its role in catalysis. J Biochem 1994, 115:156-161.
45. Goldberg J.M., Swanson R.V., Goodman H.S., Kirsch J.F. The tyrosine-225 to phenylalanine mutation of Escherichia coli aspartate aminotransferase results in an alkaline transition in the spectrophotometric and kinetic pKa values and reduced values of both kcat and Km. Biochemistry 1991, 30:305-312.
46. Guillén Schlippe Y.V., Hedstrom L. A twisted base? The role of arginine in enzyme-catalyzed proton abstractions. Arch Biochem Biophys 2005, 433:266-278.
47. Malashkevich V.N., Onuffer J.J., Kirsch J.F., Jansonius J.N. Alternating arginine-modulated substrate specificity in an engineered tyrosine aminotransferase. Nat Struct Biol 1995, 2:548-553.
48. Mainul Islam M., Hayashi H., Mizuguchi H., Kagamiyama H. The substrate activation process in the catalytic reaction of Escherichia coli aromatic amino acid aminotransferase. Biochemistry 2000, 39:15418-15428.
49. Hayashi H., Mizuguchi H., Kagamiyama H. The imine-pyridine torsion of the pyridoxal 5'-phosphate schiff base of aspartate aminotransferase lowers its pKa in the unliganded enzyme and is crucial for the successive increase in the pKa during catalysis. Biochemistry 1998, 37:15076-15085.
50. Koshland D.E. Correlation of structure and function in enzyme action. Science 1963, 142:1533-1541.
51. Kawaguchi S.I., Nobe Y., Yasuoka J.I., Wakamiya T., Kusumoto S., Kuramitsu S. Enzyme flexibility: a new concept in recognition of hydrophobic substrates. J Biochem 1997, 122:55-63.
52. Mizuguchi H., Hayashi H., Okada K., Miyahara I., Hirotsu K., Kagamiyama H. Strain is more important than electrostatic interaction in controlling the pKa of the catalytic group in aspartate aminotransferase. Biochemistry 2001, 40:353-360.
53. Okamoto A., Ishii S., Hirotsu K., Kagamiyama H. The active site of Paracoccus denitrificans aromatic amino acid aminotransferase has contrary properties: flexibility and rigidity. Biochemistry 1999, 38:1176-1184.
54. Hayashi H., Mizuguchi H., Miyahara I., Nakajima Y., Hirotsu K., Kagamiyama H. Conformational change in aspartate aminotransferase on substrate binding induces strain in the catalytic group and enhances catalysis. J Biol Chem 2003, 278:9481-9488.
55. Kagamiyama H., Hayashi H. Release of enzyme strain during catalysis reduces the activation energy barrier. Chem Rec 2001, 1:385-394.
56. Hayashi H., Mizuguchi H., Miyahara I., Islam M.M., Ikushiro H., Nakajima Y., et al. Strain and catalysis in aspartate aminotransferase. BBA-Proteins Proteomics 2003, 1647:103-109.
57. Savile C.K., Janey J.M., Mundorff E.C., Moore J.C., Tam S., Jarvis W.R., et al. Biocatalytic asymmetric synthesis of chiral amines from ketones applied to sitagliptin manufacture. Science 2010, 329:305-309.