Kinetic and structural studies on the catalytic role of the aspartic acid residue conserved in copper amine oxidase

Biochemistry

Volumn 45, Issue 13, 2006, Pages 4105-4120

  Chiu, Yen Chen ^a,h   Okajima, Toshihide ^a,f   Murakawa, Takeshi ^a   Uchida, Mayumi ^b   Taki, Masayasu ^b   Hirota, Shun ^c,d   Kim, Misa ^e,f   Yamaguchi, Hiroshi ^e   Kawano, Yoshiaki ^f   Kamiya, Nobuo ^f,i   Kuroda, Shun'ichi ^a   Hayashi, Hideyuki ^g   Yamamoto, Yukio ^b   Tanizawa, Katsuyuki ^a  

^a OSAKA UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e KWANSEI GAKUIN UNIVERSITY   (Japan)

^f INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^g OSAKA MEDICAL COLLEGE   (Japan)

^h NATIONAL TAIWAN UNIVERSITY OF SPORT   (Taiwan)

ⁱ Osaka Prefecture University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CATALYST ACTIVITY; COPPER; PROTONS; REDOX REACTIONS; SUBSTRATES;

ASPARTIC ACID RESIDUE; COPPER AMINE OXIDASE; SCHIFF BASES; SINGLE-CRYSTAL MICROSPECTROPHOTOMETRY; TOPA QUINONE (TPQ);

ENZYMES;

ASPARTIC ACID; COPPER AMINE OXIDASE; COPPER DERIVATIVE; QUINONE DERIVATIVE; SCHIFF BASE; TOPAQUINONE; UNCLASSIFIED DRUG;

ARTHROBACTER GLOBIFORMIS; ARTICLE; CATALYSIS; CONJUGATION; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYME KINETICS; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; STEREOSPECIFICITY; STRUCTURE ACTIVITY RELATION; ULTRAVIOLET SPECTROSCOPY; X RAY DIFFRACTION;

AMINE OXIDASE (COPPER-CONTAINING); AMINO ACID SEQUENCE; ARTHROBACTER; ASPARTIC ACID; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DIHYDROXYPHENYLALANINE; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, MOLECULAR; OXIDATION-REDUCTION; SCHIFF BASES; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTRUM ANALYSIS, RAMAN;

ARTHROBACTER GLOBIFORMIS; KOBUS;

EID: 33344459198     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052464l     Document Type: Article

References (59)

1. McIntire, W. S., and Hartmann, C. (1993) Copper-containing amine oxidases, in Principles and Applications of Quinoproteins (Davidson, V. L., Ed.) pp 97-171, Marcel Dekker, New York.
2. Klinman, J. P., and Mu, D. (1994) Quinoenzymes in biology, Annu. Rev. Biochem. 63, 299-344.
3. Knowles, P. F., and Dooley, D. M. (1994) Amine oxidases, in Metal Ions in Biological Systems (Sigel, H., and Sigel, A., Eds.) Vol. 30, pp 361-403, Marcel Dekker, New York.
4. Matsuzaki, R., Fukui, T., Sato, H., Ozaki, Y., and Tanizawa, K. (1994) Generation of the topa quinone cofactor in bacterial monoamine oxidase by cupric ion-dependent autooxidation of a specific tyrosyl residue, FEBS Lett. 351, 360-364.
5. Cai, D., and Klinman, J. P. (1994) Copper amine oxidase: Heterologous expression, purification, and characterization of an active enzyme in Saccharomyces cerevisiae, Biochemistry 33, 7647-7653.
6. Choi, Y. H., Matsuzaki, R., Fukui, T., Shimizu, E., Yorifuji, T., Sato, H., Ozaki, Y., and Tanizawa, K. (1995) Copper/topa quinone-containing histamine oxidase from Arthrobacter globiformis. Molecular cloning and sequencing, overproduction of precursor enzyme, and generation of topa quinone cofactor, J. Biol. Chem. 270, 4712-4720.
7. Wilce, M. C. J., Dooley, D. M., Freeman, H. C., Guss, J. M., Matsunami, H., McIntire, W. S., Tanizawa, K., and Yamaguchi, H. (1997) Crystal structures of the copper-containing amine oxidase from Arthrobacter globiformis in the holo and apo forms: Implications for the biogenesis of topaquinone, Biochemistry 36, 16116-16133.
8. Kishishita, S., Okajima, T., Kim, M., Yamaguchi, H., Hirota, S., Suzuki, S., Kuroda, S., Tanizawa, K., and Mure, M. (2003) Role of copper ion in bacterial copper amine oxidase: Spectroscopic and crystallographic studies of metal-substituted enzymes, J. Am. Chem. Soc. 125, 1041-1055.
9. Kumar, V., Dooley, D. M., Freeman, H. C., Guss, J. M., Harvey, I., McGuirl, M. A., Wilce, M. C., and Zubak, V. M. (1996) Crystal structure of a eukaryotic (pea seedling) copper-containing amine oxidase at 2.2 Å resolution, Structure 4, 943-955.
10. Parsons, M. R., Convery, M. A., Wilmot, C. M., Yadav, K. D., Blakeley, V., Corner, A. S., Phillips, S. E., McPherson, M. J., and Knowles, P. F. (1995) Crystal structure of a quinoenzyme: Copper amine oxidase of Escherichia coli at 2 Å resolution, Structure 3, 1171-1184.
11. Li, R., Klinman, J. P., and Mathews, F. S. (1998) Copper amine oxidase from Hansenula polymorpha: The crystal structure determined at 2.4 Å resolution reveals the active conformation, Structure 6, 293-307.
12. Duff, A. P., Cohen, A. E., Ellis, P. J., Kuchar, J. A., Langley, D. B., Shepard, E. M., Dooley, D. M., Freeman, H. C., and Guss, J. M. (2003) The crystal structure of Pichia pastoris lysyl oxidase, Biochemistry 42, 15148-15157.
13. Lunelli, M., Di Paolo, M. L., Biadene, M., Calderone, V., Battistutta, R., Scarpa, M., Rigo, A., and Zanotti, G. (2005) Crystal structure of amine oxidase from bovine serum, J. Mol. Biol. 346, 991-1004.
14. Airenne, T. T., Nymalm, Y., Kidron, H., Smith, D. J., Pihlavisto, M., Salmi, M., Jalkanen, S., Johnson, M. S., and Salminen, T. A. (2005) Crystal structure of the human vascular adhesion protein-1: Unique structural features with functional implications, Protein Sci. 14, 1964-1974.
15. Mure, M., Mills, S. A., and Klinman, J. P. (2002) Catalytic mechanism of the topa quinone containing copper amine oxidases, Biochemistry 41, 9269-9278.
16. Mure, M., and Klinman, J. P. (1995) Model studies of topaquinone- dependent amine oxidases. 2. Characterization of reaction intermediates and mechanism, J. Am. Chem. Soc. 117, 8707-8718.
17. Wilmot, C. M., Murray, J. M., Alton, G., Parsons, M. R., Convery, M. A., Blakeley, V., Corner, A. S., Palcic, M. M., Knowles, P. F., McPherson, M. J., and Phillips, S. E. (1997) Catalytic mechanism of the quinoenzyme amine oxidase from Escherichia coli: Exploring the reductive half-reaction, Biochemistry 36, 1608-1620.
18. Plastino, J., Green, E. L., Sanders-Loehr, J., and Klinman, J. P. (1999) An unexpected role for the active site base in cofactor orientation and flexibility in the copper amine oxidase from Hansenula polymorpha, Biochemistry 38, 8204-8216.
19. Murray, J. M., Saysell, C. G., Wilmot, C. M., Tambyrajah, W. S., Jaeger, J., Knowles, P. F., Phillips, S. E., and McPherson, M. J. (1999) The active site base controls cofactor reactivity in Escherichia coli amine oxidase: X-ray crystallographic studies with mutational variants, Biochemistry 38, 8217-8227.
20. Dooley, D. M., McGuirl, M. A., Brown, D. E., Turowski, P. N., McIntire, W. S., and Knowles, P. F. (1991) A Cu(I)-semiquinone state in substrate-reduced amine oxidases, Nature 349, 262-264.
21. Turowski, P. N., McGuirl, M. A., and Dooley, D. M. (1993) Intramolecular electron-transfer rate between active-site copper and topa quinone in pea seedling amine oxidase, J. Biol. Chem. 268, 17680-17682.
22. Su, Q., and Klinman, J. P. (1998) Probing the mechanism of proton coupled electron transfer to dioxygen: The oxidative half-reaction of bovine serum amine oxidase, Biochemistry 37, 12513-12525.
23. Farnum, M., Palcic, M., and Klinman, J. P. (1986) pH dependence of deuterium isotope effects and tritium exchange in the bovine plasma amine oxidase reaction: A role for single-base catalysis in amine oxidation and imine exchange, Biochemistry 25, 1898-1904.
24. Saysell, C. G., Tambyrajah, W. S., Murray, J. M., Wilmot, C. M., Phillips, S. E., McPherson, M. J., and Knowles, P. F. (2002) Probing the catalytidmechanism of Escherichia coli amine oxidase using mutational variants and a reversible inhibitor as a substrate analogue, Biochem. J. 365, 809-816.
25. Uchida, M., Ohtani, A., Kohyama, N., Okajima, T., Tanizawa, K., and Yamamoto, Y. (2003) Stereochemistry of 2-phenylethylamine oxidation catalyzed by bacterial copper amine oxidase, Biosci., Biotechnol., Biochem. 67, 2664-2667.
26. Ruggiero, C. E., and Dooley, D. M. (1999) Stoichiometry of the topa quinone biogenesis reaction in copper amine oxidases, Biochemistry 38, 2892-2898.
27. Ellis, K. J., and Morrison, J. F. (1982) Buffers of constant ionic strength for studying pH-dependent processes, Methods Enzymol. 87, 405-426.
28. Cleland, W. W. (1979) Statistical analysis of enzyme kinetic data, Methods Enzymol. 63, 103-138.
29. Leslie, A. G. W. (1992) Joint CCP4 and EESF-EACMB Newsletter on Protein Crystallography, SERC Daresbury Laboratory, Warrington, U.K.
30. Collaborative Computational Project Number 4 (1994) The CCP 4 suite: Programs for protein crystallography, Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 760-763.
31. Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921.
32. McRee, D. E. (1999) XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density, J. Struct. Biol. 125, 156-165.
33. Kleywegt, G. J., and Jones, T. A. (1997) Model building and refinement practice, Methods Enzymol. 277, 208-230.
34. Janes, S. M., and Klinman, J. P. (1991) An investigation of bovine serum amine oxidase active site stoichiometry: Evidence for an aminotransferase mechanism involving two carbonyl cofactors per enzyme dimmer, Biochemistry 30, 4599-4605.
35. Okajima, T., Kishishita, S., Chiu, Y.-C., Murakawa, T., Kim, M., Yamaguchi, H., Hirota, S., Kuroda, S., and Tanizawa, K. (2005) Reinvestigation of metal ion specificity for quinone cofactor biogenesis in bacterial copper amine oxidase, Biochemistry 44, 12041-12048.
36. Paz, M. A., Flückiger, R., Boak, A., Kagan, H. M., and Gallop, P. M. (1991) Specific detection of quinoproteins by redox-cycling staining, J. Biol. Chem. 266, 689-692.
37. Nakamura, N., Moenne-Loccoz, P., Tanizawa, K., Mure, M., Suzuki, S., Klinman, J. P., and Sanders-Loehr, J. (1997) Topaquinone-dependent amine oxidases: Identification of reaction intermediates by Raman spectroscopy, Biochemistry 36, 11479-11486.
38. Mure, M., and Klinman, J. P. (1993) Synthesis and spectroscopic characterization of model compounds for the active site cofactor in copper amine oxidases, J. Am. Chem. Soc. 115, 7117-7127.
39. Hevel, J. M., Mills, S. A., and Klinman, J. P. (1999) Mutation of a strictly conserved, active-site residue alters substrate specificity and cofactor biogenesis in a copper amine oxidase, Biochemistry 38, 3683-3693.
40. a values of some substituted phenylethylamines, J. Am. Chem. Soc. 81, 92-94.
41. Steinebach, V., de Vries, S., and Duine, J. A. (1996) Intermediates in the catalytic cycle of copper-quinoprotein amine oxidase from Escherichia coli, J. Biol. Chem. 271, 5580-5588.
42. Hartmann, C., Brzovic, P., and Klinman, J. P. (1993) Spectroscopic detection of chemical intermediates in the reaction of parasubstituted benzylamines with bovine serum amine oxidase, Biochemistry 32, 2234-2241.
43. Hirota, S., Iwamoto, T., Kishishita, S., Okajima, T., Yamaguchi, O., and Tanizawa, K. (2001) Spectroscopic observation of intermediates formed during the oxidative half-reaction of copper/topa quinone-containing phenylethylamine oxidase, Biochemistry 40, 15789-15796.
44. O'Connell, K. M., Langley, D. B., Shepard, E. M., Duff, A. P., Jeon, H.-B., Sun, G., Freeman, H. C., Guss, J. M., Sayre, L. M., and Dooley, D. M. (2004) Differential inhibition of six copper amine oxidases by a family of 4-(aryloxy)-2-butynamines: Evidence for a new mode of inactivation, Biochemistry 43, 10965-10978.
45. Mure, M., Brown, D. E., Saysell, C., Rogers, M. S., Wilmot, C. M., Kurtis, C. R., McPherson, M. J., Phillips, S. E., Knowles, P. F., and Dooley, D. M. (2005) Role of the interactions between the active site base and the substrate Schiff base in amine oxidase catalysis. Evidence from structural and spectroscopic studies of the 2-hydrazinopyridine adduct of Escherichia coli amine oxidase, Biochemistry 44, 1568-1582.
46. Matsuzaki, R., and Tanizawa, K. (1998) Exploring a channel to the active site of copper/topaquinone-containing phenylethylamine oxidase by chemical modification and site-specific mutagenesis, Biochemistry 37, 13947-13957.
47. Fersht, A. (1998) Structure and Mechanism in Protein Science, W. H. Freeman and Company, New York.
48. Medda, R., Padiglia, A., Pedersen, J. Z., Rotilio, G., Finazzi Agrò, A., and Floris, G. (1995) The reaction mechanism of copper amine oxidase: Detection of intermediates by the use of substrates and inhibitors, Biochemistry 34, 16375-16381.
49. do Amaral, L., Sandstron, W. A., and Cordes, E. H. (1966) Some aspects of mechanism and catalysis for carbonyl addition reactions, J. Am. Chem. Soc. 88, 2225-2233.
50. Zhang, X. M., and Bordwell, F. G. (1994) Equilibrium acidities and homolytic bond-dissociation energies of the acidic C-H bonds in P-substituted triphenylphosphonium cations, J. Am. Chem. Soc. 116, 968-972.
51. Agro, A. F., Guerrieri, P., Costa, M. T., and Mondovi, B. (1977) On the nature of chromophore in pig kidney diamine oxidase, Eur. J. Biochem. 74, 435-440.
52. Rios, A., Amyes, T. L., and Richard, J. P. (2000) Formation and stability of organic zwitterions in aqueous solution: Enolates of the amino acid glycine and its derivatives, J. Am. Chem. Soc. 122, 9373-9385.
53. Hayashi, H., and Kagamiyama, H. (1995) Reaction of aspartate aminotransferase with L-erythro-3-hydroxyaspartate: Involvement of Tyr70 in stabilization of the catalytic intermediates, Biochemistry 34, 9413-9423.
54. Kyte, J. (1995) Mechanism in Protein Chemistry, Garland Publishing, Inc., New York.
55. Kishishita, S. (1997) M.S. Thesis, Osaka University, Osaka, Japan.
56. Battersby, A. R., Staunton, J., Klinman, J., and Summers, M. C. (1979) Stereochemistry of oxidation of benzylamine by the amine oxidase from beef plasma, FEBS Lett. 99, 297-298.
57. Coleman, A. A., Hindsgaul, O., and Palcic, M. M. (1989) Stereochemistry of copper amine oxidase reactions, J. Biol. Chem. 264, 19500-19505.
58. Dunathan, H. C. (1966) Conformation and reaction specificity in pyridoxal phosphate enzymes, Proc. Natl. Acad. Sci. U.S.A. 55, 712-716.
59. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Jr., Stratmann, R. E., Burant, J. C., Dapprich, S., Millam, J. M., Daniels, A. D., Kudin, K. N., Strain, M. C., Farkas, O., Tomasi, J., Barone, V., Cossi, M., Cammi, R., Mennucci, B., Pomelli, C., Adamo, C., Clifford, S., Ochterski, J., Petersson, G. A., Ayala, P. Y., Cui, Q., Morokuma, K., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Cioslowski, J., Ortiz, J. V., Baboul, A. G., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Gomperts, R., Martini, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Andres, J. L., Gonzalez, C., Head-Gordon, M., Replogle, E. S., and Pople, J. A. (1998) Gaussian 98, Revision A.9, Gaussian, Inc., Pittsburgh, PA.