The role of cofactor binding in tryptophan accessibility and conformational stability of His-tagged d-amino acid oxidase from Trigonopsis variabilis

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1774, Issue 5, 2007, Pages 556-565

  Arroyo, Miguel ^a   Menéndez, Margarita ^b   García, José Luis ^c   Campillo, Nuria ^d   Hormigo, Daniel ^a   de la Mata, Isabel ^a   Castillón, María Pilar ^a   Acebal, Carmen ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^c CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^d INSTITUTO DE QUÍMICA MÉDICA   (Spain)

Author keywords

Circular dichroism; Cofactor binding; d amino acid oxidase; Dissociation constant; Flavoprotein; Fluorescence; Secondary structure; Thermal stability

Indexed keywords

ACRYLAMIDE; AMINO ACID; AMINO ACID OXIDASE; APOENZYME; FLAVINE ADENINE NUCLEOTIDE; FLAVOPROTEIN; HISTIDINE; HOLOENZYME; TRYPTOPHAN;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CIRCULAR DICHROISM; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DISSOCIATION CONSTANT; ENZYME ACTIVITY; ENZYME STABILITY; FLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; SPECTROSCOPY; TEMPERATURE; THERMOSTABILITY; TITRIMETRY; TRIGONOPSIS VARIABILIS; YEAST;

ACRYLAMIDE; AMINO ACID SEQUENCE; D-AMINO-ACID OXIDASE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; SPECTROPHOTOMETRY, ULTRAVIOLET; TRYPTOPHAN; YEASTS;

RHODOSPORIDIUM TORULOIDES; SUIDAE; TRIGONOPSIS VARIABILIS;

EID: 34247645601     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2007.03.009     Document Type: Article

References (60)

1. Pilone M.S. d-amino acid oxidase: new findings. Cell. Mol. Life Sci. 57 (2000) 1732-1747
2. Tishkov V.I., and Khoronenkova S.V. d-amino acid oxidase: structure, catalytic mechanism and practical application. Biochemistry (Moscow) 70 (2005) 40-54
3. Fischer L. d-amino acid oxidases in biotechnology. Recent Res. Devel. Microbiol. 2 (1998) 295-317
4. Krebs H.A. CXCVII. Metabolism of amino acids, III. Deamination of amino acids. Biochem. J. 29 (1935) 1620-1644
5. Pilone M.S., and Pollegioni L. d-amino acid oxidase as an industrial biocatalyst. Biocatal. Biotransform. 20 (2002) 145-159
6. Reithorst W., and Reichert A. An industrial view of enzymes for the cleavage of cephalosporin C. Chimia 53 (1999) 600-607
7. Alonso J., Barredo J.L., Armisén P., Díez B., Salto F., Guisán J.M., García J.L., and Cortés E. Engineering the d-aminoacid oxidase from Trigonopsis variabilis to facilitate its overproduction in Escherichia coli and its downstream processing by tailor-made metal chelate supports. Enzyme Microb. Technol. 25 (1999) 88-95
8. Lin L.-L., Chien H.R., Wang W.-C., Hwang T.-S., Fu H.-M., and Hsu W.-H. Expression of Trigonopsis variabilis d-amino acid oxidase gene in Escherichia coli and characterization of its inactive mutants. Enzyme Microb. Technol. 27 (2000) 482-491
9. Hwang T.-S., Fu H.-M., Lin L.-L., and Hsu W.-H. High-level expression of Trigonopsis variabilis d-amino acid oxidase in Escherichia coli using lactose as inducer. Biotechnol. Lett. 22 (2000) 655-658
10. Luo H., Yu H., Li Q., and Shen Z. Cloning and co-expression of d-amino acid oxidase and glutaryl-7-aminocephalosporanic acid acylase genes in Escherichia coli. Enzyme Microb. Technol. 35 (2004) 514-518
11. González F.J., Montes J., Martin F., López M.C., Ferminan E., Catalán J., Galán M.A., and Domínguez A. Molecular cloning of TvDAO1, a gene encoding a d-aminoacid oxidase from Trigonopsis variabilis and its expression in Saccharomyces cerevisiae and Kluyveromyces lactis. Yeast 13 (1997) 1399-1408
12. Isoai A., Kimura H., Reichert A., Schörgendorfer K., Nikaido K., Tohda H., Giga-Hama Y., Mutoh N., and Kumagai H. Production of d-amino acid oxidase from Trigonopsis variabilis in Schizosaccharomyces pombe and the characterization of biocatalysts prepared with recombinant cells. Biotechnol. Bioeng. 80 (2002) 22-32
13. Yu J., Li D.-Y., Zhang Y.-J., Yang S., Li R.-B., and Yuan Z.-Y. High expression of Trigonopsis variabilis d-amino acid oxidase in Pichia pastoris. J. Mol. Catal., B Enzym. 18 (2002) 291-297
14. Zheng H., Wang X., Chen J., Zhu K., Zhao Y., Yang Y., Yang S., and Jiang W. Expression, purification, and immobilization of His-tagged d-amino acid oxidase of Trigonopsis variabilis in Pichia pastoris. Appl. Microbiol. Biotechnol. 70 (2006) 683-689
15. Horner R., Wagner F., and Fischer L. Induction of d-amino acid oxidase from Trigonopsis variabilis. Appl. Environ. Microbiol. 62 (1996) 2106-2110
16. Pollegioni L., Butò S., Tischer W., Ghisla S., and Pilone M.S. Characterization of d-amino acid oxidase from Trigonopsis variabilis. Biochem. Mol. Biol. Int. 31 (1993) 709-717
17. Pollegioni L., Caldinelli L., Molla G., Sacchi S., and Pilone M.S. Catalytic properties of d-amino acid oxidase in cephalosporin C bioconversion: a comparison between proteins from different sources. Biotechnol. Prog. 20 (2004) 467-473
18. Schräder T., and Andreesen J.R. Properties and chemical modification of d-amino acid oxidase from Trigonopsis variabilis. Arch. Microbiol. 165 (1996) 41-47
19. Szwajcer E., and Mosbach K. Isolation and partial characterization of d-amino acid oxidase active against cephalosporin C from the yeast Trigonopsis variabilis. Biotechnol. Lett. 7 (1985) 1-7
20. Kubicek-Pranz M., and Rohr M. d-amino acid oxidase from the yeast Trigonopsis variabilis. J. Appl. Biochem. 7 (1985) 104-113
21. Mattevi A., Vanoni M.A., Todone F., Rizzi M., Teplyakov A., Coda A., Bolognesi M., and Curti B. Crystal structure of d-amino acid oxidase: a case of active site mirror-image convergent evolution with flavocytochrome b2. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 7496-7501
22. Umhau S., Pollegioni L., Molla G., Diederichs K., Welte W., Pilone M.S., and Ghisla S. The X-ray structure of d-amino acid oxidase at very high resolution identifies the chemical mechanism of flavin-dependent substrate dehydrogenation. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 12463-12468
23. Dupont D.R., Keim P.S., Chui A.H., Bello R., Bozzini M., and Wilson K.J. In: Hugli T. (Ed). Techniques in Protein Chemistry (1989), Academic Press, San Diego 284-294
24. Böhm G., Muhr R., and Jaenicke R. Quantitative analysis of protein far-UV circular dichroism spectra by neural networks. Protein Eng. 5 (1992) 191-195
25. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
26. Cuff J.A., Clamp M.E., Siddiqui A.S., Finlay M., and Barton G.J. Jpred: a consensus secondary structure prediction server. Bioinformatics 14 (1998) 892-893
27. Rost B. PHD: predicting one-dimensional protein structure by profile based neural networks. Methods Enzymol. 266 (1996) 525-539
28. McGuffin L.J., Bryson K., and Jones D.T. The PSIPRED protein structure prediction server. Bioinformatics 16 (2000) 404-405
29. Ouali M., and King R.D. Cascaded multiple classifiers for secondary structure prediction. Protein Sci. 9 (2000) 1162-1176
30. Pollastri G., Przybylski D., Rost B., and Baldi P. Improving the prediction of protein secondary structure in three and eight classes using recurrent neural networks and profiles. Proteins 47 (2002) 228-235
31. Sali A., and Blundell T.L. Comparative model by satisfaction of spatial restraints. J. Mol. Biol. 234 (1993) 779-815
32. Sali A., and Blundell T.L. Definition of general topological equivalence in protein structures. A procedure involving comparison of properties and relationships through simulated annealing and dynamic programming. J. Mol. Biol. 212 (1990) 403-428
33. Thompson J.D., Higgins D.G., and Gibson T.J. Clustal W: improving the sensitivity of progressive multiple sequence alignment thorough sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 (1994) 4673-4680
34. Luthy R., Bowie J.V., and Eisnberg D. Assessment of protein models with three-dimensional profiles. Nature 356 (1992) 83-85
35. Laskowski R.A., McArthur W., Moss D., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
36. Mizuguchi K., Deane C.M., Blundell T.L., Johnson M.S., and Overington J.P. JOY: protein sequence structure representation and analysis. Bioinformatics 14 (1998) 617-623
37. Ronchi S., Minchiotti L., Galliano M., Curti B., Swenson R.P., Williams C.H., and Massey V. The primary structure of d-amino acid oxidase from pig kidney. II. Isolation and sequence of overlap peptides and the complete sequence. J. Biol. Chem. 257 (1982) 8824-8834
38. Faotto L., Pollegioni L., Ceciliani F., Ronchi S., and Pilone M.S. The primary structure of d-amino acid oxidase from Rhodotorula gracilis. Biotechnol. Lett. 17 (1995) 193-198
39. Curti B., Ronchi S., Branzoli U., Ferri G., and Williams C.H. Improved purification, amino acid analysis and molecular weight of homogeneous d-amino acid oxidase from pig kidney. Biochim. Biophys. Acta 327 (1973) 266-273
40. Casalin P., Pollegioni L., Curti B., and Pilone M. A study on apoenzyme from Rhodotorula gracilis d-amino acid oxidase. Eur. J. Biochem. 197 (1991) 513-517
41. Lakowicz J.R. Protein Fluorescence. In: Lakowicz J.R. (Ed). Principles of Fluorescence Spectroscopy. 2nd ed. (1999), Kluwer Academic/Plenum Publishers, New York 446-485
42. Tu S.-C., and McCormick D.B. Conformation of porcine d-amino acid oxidase as studied by protein fluorescence and optical rotatory dispersion. Biochemistry 13 (1974) 893-899
43. Massey V., and Ganther H. On the interpretation of the absorption spectra of flavoproteins with special reference to d-amino acid oxidase. Biochemistry 4 (1965) 1161-1173
44. Arroyo M., de la Mata I., Castillón P., Acebal C., García J.L., and Menéndez M. Inactivation mechanisms of His-tagged d-amino acid oxidase from Trigonopsis variabilis. In: Méndez-Vilas A. (Ed). Modern Multidisciplinary Applied Microbiology (2006), Wiley-VCH, Weinheim 227-231
45. Dixon M., and Kleppe K. d-amino acid oxidase: dissociation and recombination of the holoenzyme. Biochim. Biophys. Acta 96 (1965) 357-367
46. Eftink M.R., and Ghiron C.A. Exposure of tryptophanyl residues in proteins. Quantitative determination by fluorescence quenching studies. Biochemistry 15 (1976) 672-680
47. Eftink M.R., and Ghiron C.A. Exposure of tryptophanyl residues and protein dynamics. Biochemistry 16 (1977) 5546-5551
48. Pollegioni L., Iametti S., Fessas D., Caldinelli L., Piubelli L., Barbirolli A., Pilone M.S., and Bonomi F. Contribution of the dimeric state to the thermal stability of the flavoprotein d-amino acid oxidase. Protein Sci. 12 (2003) 1018-1029
49. Caldinelli L., Molla G., Pilone M.S., and Pollegioni L. Tryptophan 243 affects interprotein contacts, cofactor binding and stability in d-amino acid oxidase from Rhodotorula gracilis. FEBS J. 273 (2006) 504-512
50. Piubelli L., Molla G., Caldinelli L., Pilone M.S., and Pollegioni L. Dissection of the structural determinants involved in formation of the dimeric form of d-amino acid oxidase from Rhodotorula gracilis: role of the size of the βF5-βF6 loop. Protein Eng. 16 (2003) 1063-1069
51. Mizutani H., Miyahara I., Hirotsu K., Nishina Y., Shiga K., Setoyama C., and Miura R. Three-dimensional structure of porcine kidney d-amino acid oxidase at 3.0 Å resolution. J. Biochem. 120 (1996) 14-17
52. Pollegioni L., Diederichs K., Molla G., Umahu S., Welte W., Ghisla S., and Pilone M.S. Yeast d-amino acid oxidase: structural basis of its catalytic properties. J. Mol. Biol. 324 (2002) 535-546
53. Slavica A., Dib I., and Nidetzky B. Single-site oxidation, cysteine 108 to cysteine sulfinic acid, in d-amino acid oxidase from Trigonopsis variabilis and its structural and functional consequences. Appl. Environ. Microbiol. 71 (2005) 8061-8068
54. Facchiano A.M., Struso P., Chuisano M.L., Caraglia M., Giuberti G., Marra M., Abbruzzese A., and Colonna G. Homology modelling of the human eucaryotic initiation factor 5A (eIF-5A). Protein Eng. 14 (2001) 881-890
55. Monterroso B., López-Zumel C., García J.L., Saiz J.L., García P., Campillo N., and Menéndez M. Unravelling the structure of the pneumococcal autolytic lysozyme. Biochem. J. 391 (2005) 41-49
56. Ju S.-S., Lin L.-L., Wang W.-C., and Hsu W.-H. A conserved aspartate is essential for FAD binding and catalysis in d-amino acid oxidase from Trigonopsis variabilis. FEBS Lett. 436 (1998) 119-122
57. Lin L.-L., Wang W.-C., Ju S.-S., Chien H.R., and Hsu W.-H. The role of conserved histidine residue His324 in Trigonopsis variabilis d-amino acid oxidase. FEMS Microbiol. Lett. 176 (1999) 443-448
58. Dib I., Slavica A., Riethorst W., and Nidetzky B. Thermal inactivation of d-amino acid oxidase from Trigonopsis variabilis occurs via three parallel paths of irreversible denaturation. Biotechnol. Bioeng. 94 (2006) 645-654
59. Slavica A., Acai P., Riethorst W., and Nidetzky B. Study of the thermal stability of d-amino acid oxidase from Trigonopsis variabilis reveals enzyme inactivation via multiple steps. Biocatal. Biotransform. 24 (2006) 426-436
60. Piubelli L., Caldinelli L., Molla G., Pilone M.S., and Pollegioni L. Conversion of the dimeric d-amino acid oxidase from Rhodotorula gracilis to a monomeric form. A rational mutagenesis approach. FEBS Lett. 526 (2002) 43-48