Mandelamide hydrolase from Pseudomonas putida: Characterization of a new member of the amidase signature family

Biochemistry

Volumn 43, Issue 24, 2004, Pages 7725-7735

  Gopalakrishna, Kota N ^a,b   Stewart, Betty H ^a,c   Kneen, Malea M ^a   Andricopulo, Adriano D ^a,d   Kenyon, George L ^a   McLeish, Michael J ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c AUSTIN COLLEGE   (United States)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BENZENE; ENZYMES; FATTY ACIDS; HYDROLYSIS; ISOMERS;

SEQUENCE FAMILY;

BIOCHEMISTRY;

ACETANILIDE; AMIDASE; AMIDE; AMMONIA; BACTERIAL ENZYME; ESTER; FATTY ACID AMIDASE; MANDELAMIDE; MANDELAMIDE HYDROLASE; MANDELIC ACID; PHENYL GROUP; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; ENANTIOMER; ENZYME ACTIVE SITE; ENZYME ISOLATION; ENZYME KINETICS; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME SUBSTRATE; ESCHERICHIA COLI; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN HYDROLYSIS; PSEUDOMONAS PUTIDA; STEREOCHEMISTRY;

AMIDOHYDROLASES; AMINO ACID SEQUENCE; BASE SEQUENCE; CIRCULAR DICHROISM; DNA PRIMERS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PSEUDOMONAS PUTIDA; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS; PSEUDOMONAS PUTIDA;

EID: 2942724459     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049907q     Document Type: Article

References (71)

1. Fewson, C. A. (1988) Microbial metabolism of mandelate: a microcosm of diversity, FEMS Microbiol. Rev. 4, 85-110.
2. Wheelis, M. L., and Stanier, R. Y. (1970) The genetic control of dissimilatory pathways in Pseudomonas putida, Genetics 66, 245-266.
3. Tsou, A. Y., Ransom, S. C., Gerlt, J. A., Powers, V. M., and Kenyon, G. L. (1989) Selection and characterization of a mutant of the cloned gene for mandelate racemase that confers resistance to an affinity label by greatly enhanced production of enzyme, Biochemistry 28, 969-975.
4. Tsou, A. Y., Ransom, S. C., Gerlt, J. A., Buechter, D. D., Babbitt, P. C., and Kenyon, G. L. (1990) Mandelate pathway of Pseudomonas putida: sequence relationship involving mandelate racemase, (S)-mandelate dehydrogenase, and benzoylformate decarboxylase and expression of benzoylformate decarboxylase in Escherichia coli, Biochemistry 29, 9856-9862.
5. +-dependent benzaldehyde dehydrogenase from Pseudomonas putida ATCC 12633, J. Bacteriol. 185, 2451-2456.
6. Mayaux, J. F., Cerbelaud, E., Soubrier, F., Yeh, P., Blanche, F., and Petre, D. (1991) Purification, cloning, and primary structure of a new enantiomer-selective amidase from a Rhodococcus strain: structural evidence for a conserved genetic coupling with nitrile hydratase, J. Bacteriol. 173, 6694-6704.
7. Chebrou, H., Bigey, F., Arnaud, A., and Galzy, P. (1996) Study of the amidase signature group, Biochim. Biophys. Acta 1298, 285-293.
8. Shin, S., Yun, Y. S., Koo, H. M., Kim, Y. S., Choi, K. Y., and Oh, B. H. (2003) Characterization of a novel Ser-cisSer-Lys catalytic triad in comparison with the classical Ser-His-Asp triad, J. Biol. Chem. 278, 24937-24943.
9. Patricelli, M. P., and Cravatt, B. F. (2000) Clarifying the catalytic roles of conserved residues in the amidase signature family, J. Biol. Chem. 275, 19177-19184.
10. Mazumder, A., Gerlt, J. A., Absalon, M. J., Stubbe, J., Cunningham, R. P., Withka, J., and Bolton, P. H. (1991) Stereochemical studies of the β-elimination reactions at aldehydic abasic sites in DNA: endonuclease III from Escherichia coli, sodium hydroxide, and Lys-Trp-Lys, Biochemistry 30, 1119-1126.
11. Gomi, K., Kitamoto, K., and Kumagai, C. (1991) Cloning and molecular characterization of the acetamidase-encoding gene (amdS) from Aspergillus oryzae, Gene 108, 91-98.
12. Gaffney, T. D., da Costa e Silva, O., Yamada, T., and Kosuge, T. (1990) Indoleacetic acid operon of Pseudomonas syringae subsp. savastanoi: transcription analysis and promoter identification, J. Bacteriol. 172, 5593-5601.
13. Deutsch, D. G., and Chin, S. A. (1993) Enzymatic synthesis and degradation of anandamide, a cannabinoid receptor agonist, Biochem. Pharmacol. 46, 791-796.
14. Cravatt, B. F., Giang, D. K., Mayfield, S. P., Boger, D. L., Lerner, R. A., and Gilula, N. B. (1996) Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides, Nature 384, 83-87.
15. Curnow, A. W., Hong, K., Yuan, R., Kim, S., Martins, O., Winkler, W., Henkin, T. M., and Soll, D. (1997) Glu-tRNAGln amidotransferase: a novel heterotrimeric enzyme required for correct decoding of glutamine codons during translation, Proc. Natl. Acad. Sci. U.S.A. 94, 11819-11826.
16. Schon, A., Kannangara, C. G., Gough, S., and Soll, D. (1988) Protein biosynthesis in organelles requires misaminoacylation of tRNA, Nature 331, 187-190.
17. Fowler, C. J., Jonsson, K. O., and Tiger, G. (2001) Fatty acid amide hydrolase: biochemistry, pharmacology, and therapeutic possibilities for an enzyme hydrolyzing anandamide, 2-arachidonoylglycerol, palmitoylethanolamide, and oleamide, Biochem. Pharmacol. 62, 517-526.
18. Boger, D. L., Sato, H., Lerner, A. E., Hedrick, M. P., Fecik, R. A., Miyauchi, H., Wilkie, G. D., Austin, B. J., Patricelli, M. P., and Cravatt, B. F. (2000) Exceptionally potent inhibitors of fatty acid amide hydrolase: the enzyme responsible for degradation of endogenous oleamide and anandamide, Proc. Natl. Acad. Sci. U.S.A. 97, 5044-5049.
19. Patricelli, M. P., Lovato, M. A., and Cravatt, B. F. (1999) Chemical and mutagenic investigations of fatty acid amide hydrolase: evidence for a family of serine hydrolases with distinct catalytic properties, Biochemistry 38, 9804-9812.
20. Patricelli, M. P., and Cravatt, B. F. (1999) Fatty acid amide hydrolase competitively degrades bioactive amides and esters through a nonconventional catalytic mechanism, Biochemistry 38, 14125-14130.
21. McKinney, M. K., and Cravatt, B. F. (2003) Evidence for distinct roles in catalysis for residues of the serine-serine-lysine catalytic triad of fatty acid amide hydrolase, J. Biol. Chem. 278, 37393-37399.
22. Shin, S., Lee, T. H., Ha, N. C., Koo, H. M., Kim, S. Y., Lee, H. S., Kim, Y. S., and Oh, B. H. (2002) Structure of malonamidase E2 reveals a novel Ser-cisSer-Lys catalytic triad in a new serine hydrolase fold that is prevalent in nature, EMBO J. 21, 2509-2516.
23. Bracey, M. H., Hanson, M. A., Masuda, K. R., Stevens, R. C., and Cravatt, B. F. (2002) Structural adaptations in a membrane enzyme that terminates endocannabinoid signaling, Science 298, 1793-1796.
24. Labahn, J., Neumann, S., Buldt, G., Kula, M. R., and Granzin, J. (2002) An alternative mechanism for amidase signature enzymes, J. Mol. Biol. 322, 1053-1064.
25. Murzin, A. G., Brenner, S. E., Hubbard, T., and Chothia, C. (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures, J. Mol. Biol. 247, 536-540.
26. Koo, H. M., Choi, S. O., Kim, H. M., and Kim, Y. S. (2000) Identification of active-site residues in Bradyrhizobiumjaponicum malonamidase E2, Biochem. J. 349, 501-507.
27. Kobayashi, M., Fujiwara, Y., Goda, M., Komeda, H., and Shimizu, S. (1997) Identification of active sites in amidase: evolutionary relationship between amide bond- and peptide bond-cleaving enzymes, Proc. Natl. Acad. Sci. U.S.A. 94, 11986-11991.
28. Omeir, R. L., Arreaza, G., and Deutsch, D. G. (1999) Identification of two serine residues involved in catalysis by fatty acid amide hydrolase, Biochem. Biophys. Res. Commun. 264, 316-320.
29. Audrieth, L. F., and Sveda, M. (1955) Mandelamide, in Organic Syntheses (Homing, E. C., Ed.) Collect. Vol. III, pp 536-538, Wiley & Sons, New York.
30. Dictionary of Organic Compounds, 6th ed. (1996) Vol. 4, p 3790, Chapman & Hall, London.
31. Bailén, M. A., Chinchilla, R., Dodsworth, D. J., and Nájera, C. (2000) Efficient synthesis of primary amides using 2-mercaptopyridone-1-oxide-based uronium salts, Tetrahedron Lett. 41, 9809-9813.
32. Bovin, J., El Kaim, L., and Zard, S. Z. (1995) A New and Efficient Synthesis of Trifluoromethyl Ketones from Carboxylic Acids. Part I, Tetrahedron 51, 2573-2584.
33. McPhee, W. D., and Klingsberg, E. (1955) Benzyl chloromethyl ketone, In Organic Syntheses (Homing, E. C., Ed.) Collect. Vol. 3, pp 119-200, Wiley & Sons, New York.
34. Krallmann-Wenzel, U. (1985) An improved method of ammonia determination, applicable to amidases and other ammonia-producing enzyme systems of mycobacteria, Am. Rev. Respir. Dis. 131, 432-434.
35. Boshoff, H. I., and Mizrahi, V. (1998) Purification, gene cloning, targeted knockout, overexpression, and biochemical characterization of the major pyrazinamidase from Mycobacterium smegmatis, J. Bacteriol. 180, 5809-5814.
36. Ellis, K. J., and Morrison, J. F. (1982) Buffers of constant ionic strength for studying pH-dependent processes, Methods Enzymol. 87, 405-426.
37. Zhu, Z., Sun, D., and Davidson, V. L. (2000) Conversion of methylamine dehydrogenase to a long-chain amine dehydrogenase by mutagenesis of a single residue, Biochemistry 39, 11184-11186.
38. Dixon, M. (1953) The determination of enzyme inhibitor constants, Biochem. J. 55, 170-171.
39. Wei, Y., Kurihara, T., Suzuki, T., and Esaki, N. (2003) A novel esterase from a psychrotrophic bacterium, Acinetobacter sp. strain no. 6, that belongs to the amidase signature family, J. Mol. Catal. B: Enzym. 23, 357-365.
40. Neumann, S., and Kula, M. R. (2002) Gene cloning, overexpression and biochemical characterization of the peptide amidase from Stenotrophomonas maltophilia, Appl. Microbiol. Biotechnol. 58, 772-780.
41. Patricelli, M. P., Lashuel, H. A., Giang, D. K., Kelly, J. W., and Cravatt, B. F. (1998) Comparative characterization of a wild type and transmembrane domain-deleted fatty acid amide hydrolase: identification of the transmembrane domain as a site for oligomerization, Biochemistry 37, 15177-15187.
42. Kim, Y. S., and Kang, S. W. (1994) Novel malonamidases in Bradyrhizobium japonicum. Purification, characterization, and immunological comparison, J. Biol. Chem. 269, 8014-8021.
43. Kaplan, A. (1969) The determination of urea, ammonia, and urease, Methods Biochem. Anal. 17, 311-324.
44. Hegazi, M. F., Quinn, D. M., and Schowen, R. L. (1978) Transition-state properties in acyl and methyl transfer, in Transition States of Biochemical Processes (Gandour, R. D., and Schowen, R. L., Eds.) pp 355-428, Plenum Press, New York.
45. Stein, R. L. (2002) Enzymatic hydrolysis of p-nitroacetanilide: mechanistic studies of the aryl acylamidase from Pseudomonas fluorescens, Biochemistry 41, 991-1000.
46. Walsh, C. T. (1979) Enzymatic Reaction Mechanisms, W. H. Freeman and Co., San Francisco.
47. Schoellmann, G., and Shaw, E. (1963) Direct evidence for the presence of histidine in the active center of chymotrypsin, Biochemistry 2, 252-255.
48. Koo, C. W. (1997) Mandelamide hydrolase from Pseudomonas putida, Ph.D. Thesis, Department of Pharmaceutical Chemistry, University of California, San Francisco.
49. Ueda, N., Kurahashi, Y., Yamamoto, S., and Tokunaga, T. (1995) Partial purification and characterization of the porcine brain enzyme hydrolyzing and synthesizing anandamide, J. Biol. Chem. 270, 23823-23827.
50. Koutek, B., Prestwich, G. D., Howlett, A. C., Chin, S. A., Salehani, D., Akhavan, N., and Deutsch, D. G. (1994) Inhibitors of arachidonoyl ethanolamide hydrolysis, J. Biol. Chem. 269, 22937-22940.
51. Stein, R. L., Strimpler, A. M., Edwards, P. D., Lewis, J. J., Mauger, R. C., Schwartz, J. A., Stein, M. M., Trainor, D. A., Wildonger, R. A., and Zottola, M. A. (1987) Mechanism of slow-binding inhibition of human leukocyte elastase by trifluoromethyl ketones, Biochemistry 26, 2682-2689.
52. Allen, K. N., and Abeles, R. H. (1989) Inhibition of pig liver esterase by trifluoromethyl ketones: modulators of the catalytic reaction alter inhibition kinetics, Biochemistry 28, 135-140.
53. Boger, D. L., Fecik, R. A., Patterson, J. E., Miyauchi, H., Patricelli, M. P., and Cravatt, B. F. (2000) Fatty acid amide hydrolase substrate specificity, Bioorg. Med. Chem. Lett. 10, 2613-2616.
54. Lang, W., Qin, C., Lin, S., Khanolkar, A. D., Goutopoulos, A., Fan, P., Abouzid, K., Meng, Z., Biegel, D., and Makriyannis, A. (1999) Substrate specificity and stereoselectivity of rat brain microsomal anandamide amidohydrolase, J. Med. Chem. 42, 896-902.
55. Mayaux, J. F., Cerebelaud, E., Soubrier, F., Faucher, D., and Petre, D. (1990) Purification, cloning, and primary structure of an enantiomer-selective amidase from Brevibacterium sp. strain R312: structural evidence for genetic coupling with nitrile hydratase, J. Bacteriol. 172, 6764-6773.
56. Hirrlinger, B., Stolz, A., and Knackmuss, H. J. (1996) Purification and properties of an amidase from Rhodococcus erythropolis MP50 which enantioselectively hydrolyzes 2-arylpropionamides, J. Bacteriol. 178, 3501-3507.
57. Trott, S., Burger, S., Calaminus, C., and Stolz, A. (2002) Cloning and heterologous expression of an enantioselective amidase from Rhodococcus erythropolis strain MP50, Appl. Environ. Microbiol. 68, 3279-3286.
58. Trott, S., Bauer, R., Knackmuss, H. J., and Stolz, A. (2001) Genetic and biochemical characterization of an enantioselective amidase from Agrobacterium tumefaciens strain d3, Microbiology 147, 1815-1824.
59. Yamana, T., Mizukami, Y., Tsuji, A., Yasuda, Y., and Masuda, K. (1972) Stability of amides. I. Hydrolysis mechanism of N-substituted aliphatic amides, Chem. Pharm. Bull. 20, 881-891.
60. Gregoriou, M., and Brown, P. R. (1980) Adaptation to phenylacetamide as a growth substrate by an acetanilide-utilizing mutant of Pseudomonas aeruginosa, Arch. Microbiol. 125, 277-283.
61. Carter, P., and Wells, J. A. (1988) Dissecting the catalytic triad of a serine protease, Nature 332, 564-568.
62. Zwizinski, C., Date, T., and Wickner, W. (1981) Leader peptidase is found in both the inner and outer membranes of Escherichia coli, J. Biol. Chem. 256, 3593-3597.
63. Deutsch, D. G., Omeir, R., Arreaza, G., Salehani, D., Prestwich, G. D., Huang, Z., and Howlett, A. (1997) Methyl arachidonyl fluorophosphonate: a potent irreversible inhibitor of anandamide amidase, Biochem. Pharmacol. 53, 255-260.
64. Patricelli, M. P., Patterson, J. E., Boger, D. L., and Cravatt, B. F. (1998) An endogenous sleep-inducing compound is a novel competitive inhibitor of fatty acid amide hydrolase, Bioorg. Med. Chem. Lett. 8, 613-618.
65. Stein, R. L., and Strimpler, A. M. (1987) Slow-binding inhibition of chymotrypsin and cathepsin G by the peptide aldehyde chymostatin, Biochemistry 26, 2611-2615.
66. Kettner, C. A., and Shenvi, A. B. (1984) Inhibition of the serine proteases leukocyte elastase, pancreatic elastase, cathepsin G, and chymotrypsin by peptide boronic acids, J. Biol. Chem. 259, 15106-15114.
67. Imperiali, B., and Abeles, R. H. (1986) Inhibition of serine proteases by peptidyl fluoromethyl ketones, Biochemistry 25, 3760-3767.
68. Brady, K., Wei, A. Z., Ringe, D., and Abeles, R. H. (1990) Structure of chymotrypsin-trifluoromethyl ketone inhibitor complexes: comparison of slowly and rapidly equilibrating inhibitors, Biochemistry 29, 7600-7607.
69. Morrison, J. F., and Walsh, C. T. (1988) The behavior and significance of slow-binding enzyme inhibitors, Adv. Enzymol. Relat. Areas Mol. Biol. 61, 201-301.
70. Boger, D. L., Sato, H., Lerner, A. E., Austin, B. J., Patterson, J. E., Patricelli, M. P., and Cravatt, B. F. (1999) Trifluoromethyl ketone inhibitors of fatty acid amide hydrolase: a probe of structural and conformational features contributing to inhibition, Bioorg. Med. Chem. Lett. 9, 265-270.
71. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Res. 25, 3389-3402.