The 1.7 Å crystal structure of the apo form of the soluble quinoprotein glucose dehydrogenase from acinetobacter calcoaceticus reveals a novel internal conserved sequence repeat

Journal of Molecular Biology

Volumn 289, Issue 2, 1999, Pages 319-333

  Oubrie, Arthur ^a   Rozeboom, Henriëtte J ^a   Kalk, Kor H ^a   Duine, Johannis A ^b   Dijkstra, Bauke W ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Electron transfer; Glucose dehydrogenase; PQQ; Quinoprotein; X ray structure

Indexed keywords

ASPARTIC ACID; CALCIUM ION; GLUCOSE DEHYDROGENASE; MONOMER; PROTEIN; PYRROLOQUINOLINEQUINONE; QUINONE DERIVATIVE; APOENZYME; GLUCOSE DEHYDROGENASE (PYRROLOQUINOLINE QUINONE); GLUCOSE DEHYDROGENASE (PYRROLOQUINOLINE-QUINONE); RECOMBINANT PROTEIN;

ACINETOBACTER CALCOACETICUS; AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; CELL DENSITY; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENZYME BINDING; GENETIC PROCEDURES; HYDROGEN BOND; NONHUMAN; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; SEQUENCE HOMOLOGY; SOLUBILITY; SURFACE PROPERTY; X RAY CRYSTALLOGRAPHY; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; COMPUTER GRAPHICS; COMPUTER PROGRAM; ENZYMOLOGY; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT;

ACINETOBACTER CALCOACETICUS; NEGIBACTERIA;

ACINETOBACTER CALCOACETICUS; AMINO ACID SEQUENCE; APOENZYMES; BINDING SITES; COMPUTER GRAPHICS; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; GLUCOSE DEHYDROGENASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SOFTWARE;

EID: 0033522648     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2766     Document Type: Article

References (61)

1. Altschul S. F., Madden T. L., Schiffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein data base search programs. Nucl. Acids Res. 25:1997;3389-3402.
2. Baker S. C., Saunders N. F. W., Willis A. C., Ferguson S. J., Hajdu J., Fülöp V. Cytochrome cd1 structure: unusual haem environments in a nitrite reductase and analysis of factors contributing to β-propeller folds. J. Mol. Biol. 269:1997;440-455.
3. Barton G. J. ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng. 6:1993;37-40.
4. Blattner F. R., Plunkett G. III, Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K., Mayhew G. F., Gregor J., Davis N. W., Kirkpatrick H. A., Goeden M. A., Rose D. J., Mau B., Shao Y. The complete genome sequence of Escherichia coli K-12. Science. 277:1997;1453-1474.
5. Blow D. M., Matthews B. M. Parameter refinement in the multiple isomorphous-replacement method. Acta Crystallog. sect. A. 29:1973;56-62.
6. Bork P., Doolittle R. F. Drosophila kelch motif is derived from a common enzyme fold. J. Mol. Biol. 236:1994;1277-1282.
7. Brünger A. T. Free R value: a novel statistical quantity for assessing the accuracy of structures. Nature. 355:1992;472-475.
8. Brünger A. T., Kuriyan J., Karplus M. Crystallographic R-factor refinement by molecular dynamics. Science. 235:1987;458-460.
9. Chen L., Mathews F. S., Davidson V. L., Huizinga E. G., Vellieux F. M., Hol W. G. Three-dimensional structure of the quinoprotein methylamine dehydrogenase from Paracoccus denitrificans determined by molecular replacement at 2.8 Å resolution. Proteins: Struct. Funct. Genet. 14:1992;288-299.
10. Cleton-Jansen A.-M., Goosen N., Wenzel T. J., van de Putte P. Cloning of the gene encoding quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus: evidence for the presence of a second enzyme. J. Bacteriol. 170:1988;2121-2125.
11. Cleton-Jansen A.-M., Goosen N., Fayet O., van de Putte P. Cloning, mapping, and sequencing of the gene encoding Escherichia coli quinoprotein glucose dehydrogenase. J. Bacteriol. 172:1990;6308-6315.
12. Cowtan K. D., Main P. Improvement of macromolecular electron-density maps by the simultaneous application of real and reciprocal space constraints. Acta Crystallog. sect. D. 49:1993;148-157.
13. Crennell S., Garman E., Laver G., Vimr E., Taylor G. Crystal structure of Vibrio cholerae neuraminidase reveals dual lectin-like domains in addition to the catalytic domain. Structure. 2:1994;535-544.
14. Dodson E. J., Winn M., Ralph A. Collaborative computational project, number 4: providing programs for protein crystallography. Methods Enzymol. 277:1997;620-633.
15. Dokter P., Frank Jzn J., Duine J. A. Purification and characterization of quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus L.M.D. 79.41. Biochem. J. 239:1986;163-167.
16. Dokter P., van Wielink J. E., van Kleef M. A., Duine J. A. Cytochrome b-562 from Acinetobacter calcoaceticus L.M.D. 79.41. Its characteristics and role as electron acceptor for quinoprotein glucose dehydrogenase. Biochem. J. 254:1988;131-138.
17. Duine J. A. Quinoproteins: enzymes containing the quinonoid cofactor pyrroloquinoline quinone, topaquinone or tryptophan-tryptophan quinone. Eur. J. Biochem. 200:1991;271-284.
18. Engh R. A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 47:1991;392-400.
19. Faber H. R., Groom C. R., Baker H. M., Morgan W. T., Smith A., Baker E. N. 1.8 Å crystal structure of the C-terminal domain of rabbit serum haemopexin. Structure. 3:1995;551-559.
20. Fülöp V., Moir J. W., Ferguson S. J., Hajdu J. The anatomy of a bifunctional enzyme: structural basis for reduction of oxygen to water and synthesis of nitric oxide by cytochrome cd1. Cell. 81:1995;369-377.
21. Furey W., Swaminathan S. PHASES-95: a program package for processing and analyzing diffraction data from macromolecules. Methods Enzymol. 277:1997;590-620.
22. Gaskell A., Crennell S., Taylor G. The three domains of a bacterial sialidase: a β-propeller, an immunoglobulin module and a galactose-binding jelly-roll. Structure. 3:1995;1197-1205.
23. Geiger O., Görisch H. Crystalline quinoprotein glucose dehydrogenase from Acinetobacter calcoaceticus. Biochemistry. 25:1986;6043-6048.
24. 2+ ions are necessary for re-activation. Biochem. J. 261:1989;415-421.
25. Ghosh M., Anthony C., Harlos K., Goodwin M. G., Blake C. The refined structure of the quinoprotein methanol dehydrogenase from Methylobacterium extorquens at 1.94 Å Structure. 3:1995;177-187.
26. Gohlke U., Gomis-Rüth F.-X., Crabbe T., Murphy G., Docherty A. J., Bode W. The C-terminal (haemopexin-like) domain structure of human gelatinase A (MMP2): structural implications for its function. FEBS Letters. 378:1996;126-130.
27. Hoenes J. Colorimetric assay by enzymatic oxidation in the presence of an aromatic nitroso or oxime compound. US Patent 5206147. 1993;Boehringer Mannheim GmbH.
28. Hoenes J. Process and agent for the colorimetric determination of an analyte by means of enzymatic oxidation. US Patent 5334508. 1994;Boehringer Mannheim GmbH.
29. Hoenes J., Unkrig V. Method for the calorimetric determination of an analyte with a PQQ-dependent dehydrogenase. US Patent 5484708. 1996;Boehringer Mannheim GmbH.
30. Hommes R. J. W., Postma P. W., Neijssel O. M., Tempest D. W., Dokter P., Duine J. A. Evidence of a quinoprotein glucose dehydrogenase apoenzyme in several strains of Escherichia coli. FEMS Microb. Letters. 24:1984;329-333.
31. Ito N., Phillips S. E. V., Stevens C., Ogel Z. B., McPherson M. J., Keen J. N., Yadav K. D. S., Knowles P. F. Novel thioether bond revealed by a 1.7 Å crystal structure of galactose oxidase. Nature. 350:1991;87-90.
32. Ito N., Phillips S. E. V., Yadav K. D. S., Knowles P. F. Crystal structure of a free radical enzyme, galactose oxidase. J. Mol. Biol. 238:1994;794-814.
33. Jabs A., Weiss M. S., Hilgenfeld R. Non-proline cis peptide bonds in proteins. J. Mol. Biol. 286:1999;291-304.
34. Jones T. A., Zou J.-Y., Cowan S. W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
35. Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M., Sasamoto S., Kimura T., Hosouchi T., Matsuno A., Muraki A., Nakazaki N. et al. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3:1996;109-136.
36. Kraulis P. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
37. Li J., Brick P., O'Hare M. C., Skarzynski T., Lloyd L. F., Curry V. A., Clark I. M., Bigg H. F., Hazleman B. L., Cawston T. E., Blow D. M. Structure of full-length porcine synovial collagenase reveals a C-terminal domain containing a calcium-linked, four-bladed β-propeller. Structure. 3:1995;541-549.
38. Libson A. M., Gittis A. G., Collier I. E., Marmer B. L., Goldberg G. I., Lattman E. E. Crystal structure of the haemopexin-like C-terminal domain of gelatinase A. Nature Struct. Biol. 2:1995;938-942.
39. Matsushita K., Shinagawa E., Adachi O., Ameyama M. Quinoprotein D-glucose dehydrogenase of the Acinetobacter calcoaceticus respiratory chain: membrane-bound and soluble forms are different molecular species. Biochemistry. 28:1989;6276-6280.
40. Murzin A. G. Structural principles for the propeller assembly of beta-sheets: the preference for seven-fold symmetry. Proteins: Struct. Funct. Genet. 14:1992;191-201.
41. Nakai K., Kanehisa M. Expert system for predicting localization sites in Gram-negative bacteria. Proteins: Struct. Funct. Genet. 11:1991;95-110.
42. Neer E. J., Smith T. F. G protein heterodimers: new structures propel new questions. Cell. 84:1996;175-178.
43. Nicholls A., Honig B. GRASP1.1. 1993;Columbia University, New York.
44. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1997;1-6.
45. Olsthoorn A. J. J., Duine J. A. Production, characterization, and reconstitution of recombinant quinoprotein glucose dehydrogenase (soluble type; EC 1.1.99.17) apoenzyme of Acinetobacter calcoaceticus. Arch. Biochem. Biophys. 336:1996;42-48.
46. 2+ and its substitutes have two different binding sites and roles in soluble, quinoprotein (pyrroloquinoline-quinone-containing) glucose dehydrogenase. Eur. J. Biochem. 247:1997;659-665.
47. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
48. Ramakrishnan C., Ramachandran G. N. Stereochemical criteria for polypeptide and protein chain conformation. Biophys. J. 5:1965;909-933.
49. Read R. J. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallog. sect. A. 42:1986;140-149.
50. Renault L., Nassar N., Vetter I., Becker J., Klebe C., Roth M., Wittinghofer A. The 1.7 angstrom crystal structure of the regulator of chromosome condensation (RCC1) reveals a seven-bladed propeller. Nature. 392:1998;97-101.
51. Rudenko G., Bonten E., Dazzo A., Hol W. G. J. Structure determination of the human protective protein: twofold averaging reveals the three-dimensional structure of a domain which was entirely absent in the initial model. Acta Crystallog. sect. D. 52:1996;923-936.
52. Schlunegger M. P., Grütter M. G., Streiff M. B., Olsthoorn A. J., Duine J. A. Crystallization and preliminary crystallographic investigations of the soluble glucose dehydrogenase from Acinetobacter calcoaceticus. J. Mol. Biol. 233:1993;784-786.
53. A protein βγ dimer at 2.1 Å resolution. Nature. 379:1996;369-374.
54. van Kleef M. A., Duine J. A. Factors relevant in bacterial pyrroloquinoline quinone production. Appl. Environ. Microbiol. 55:1989;1209-1213.
55. Varghese J. N., Colman P. M. Three-dimensional structure of the neuraminidase of influenza virus A/Tokyo/3/67 at 2.2 Å resolution. J. Mol. Biol. 221:1991;473-486.
56. Varghese J. N., Laver W. G., Colman P. M. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution. Nature. 303:1983;35-40.
57. Vellieux F. M., Huitema F., Groendijk H., Kalk K. H., Frank Jzn J., Jongejan J. A., Duine J. A., Petratos K., Drenth J., Hol W. G. Structure of quinoprotein methylamine dehydrogenase at 2.25 Å resolution. EMBO J. 8:1989;2171-2178.
58. iα1β1γ2. Cell. 83:1995;1047-1058.
59. Xia Z.-X., Dai W.-W., Xiong J.-P., Hao Z. P., Davidson V. L., White S., Mathews F. S. The three-dimensional structures of methanol dehydrogenase from two methylotrophic bacteria at 2.6-Å resolution. J. Biol. Chem. 267:1992;22289-22297.
60. Xia Z.-X., Dai W.-W., Zhang Y.-E., White S. A., Boyd G. D., Mathews F. S. Determination of the gene sequence and the three-dimensional structure at 2.4 angstroms resolution of methanol dehydrogenase from Methylophilus W3A1. J. Mol. Biol. 259:1996;480-501.
61. Ye L., Hämmerle M., Olsthoorn A. J. J., Schuhmann W., Schmidt H.-L., Duine J. A., Heller A. High current density "wired" quinoprotein glucose dehydrogenase electrode. Anal. Chem. 65:1993;238-241.