Crystal structure of an electron transfer complex between aromatic amine dehydrogenase and azurin from Alcaligenes faecalis

Biochemistry

Volumn 45, Issue 45, 2006, Pages 13500-13510

  Sukumar, Narayanasami ^a,f   Chen, Zhi Wei ^a   Ferrari, Davide ^b   Merli, Angelo ^b   Rossi, Gian Luigi ^b   Bellamy, Henry D ^c,g   Chistoserdov, Andrei ^d   Davidson, Victor L ^e   Mathews, F Scott ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PARMA   (Italy)

^c SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^d UNIVERSITY OF LOUISIANA AT LAFAYETTE   (United States)

^e UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^f ARGONNE NATIONAL LABORATORY   (United States)

^g LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CHARGE TRANSFER; CRYSTAL ORIENTATION; CRYSTAL STRUCTURE; ENZYMES; HYDROGEN BONDS; HYDROPHOBICITY; INTERFACES (MATERIALS);

AMICYANIN COMPLEX; BINDING CONSTANTS; BOND LINKING; QUINOPROTEINS;

AROMATIC COMPOUNDS;

AMICYANIN; AMINE DEHYDROGENASE; ARALKYLAMINE DEHYDROGENASE; AZURIN; BINDING PROTEIN; COPPER; CUPREDOXIN; OXIDOREDUCTASE; PROTEIN DERIVATIVE; QUINONE DERIVATIVE; QUINOPROTEIN; TRYPTOPHYLQUINONE; UNCLASSIFIED DRUG;

ALCALIGENES FAECALIS; AMINO ACID SEQUENCE; ARTICLE; ATOM; BINDING AFFINITY; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENZYME BINDING; HYDROGEN BOND; HYDROPHOBICITY; IONIC STRENGTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; ROTATION; STRUCTURE ANALYSIS;

ALCALIGENES FAECALIS; AZURIN; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ELECTRON TRANSPORT; INDOLEQUINONES; MODELS, MOLECULAR; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; TRYPTOPHAN;

ALCALIGENES FAECALIS;

EID: 33751010484     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0612972     Document Type: Article

References (43)

1. Pelletier, H., and Kraut, J. (1992) Crystal structure of a complex between electron transfer partners, cytochrome c peroxidase and cytochrome c, Science 258, 1748-1755.
2. Lange, C., and Hunte, C. (2002) Crystal structure of the yeast cytochrome bel complex with its bound substrate cytochrome c, Proc. Natl. Acad. Sci. U.S.A. 99, 2800-2805.
3. Toogood, H. S., van Thiel, A., Basran, J., Sutcliffe, M. J., Scrutton, N. S., and Leys, D. (2004) Extensive domain motion and electron transfer in the human electron transferring flavoprotein. Medium chain acyl-CoA dehydrogenase complex, J. Biol. Chem. 279, 32904-32912.
4. Leys, D., Basran, J., Talfournier, F., Sutcliffe, M. J., and Scrutton, N. S. (2003) Extensive conformational sampling in a ternary electron transfer complex, Nat. Struct. Biol. 10, 219-225.
5. + reductase, Nat. Struct. Biol. 8, 117-121.
6. Chen, L., Durley, R., Poliks, B. J., Hamada, K., Chen, Z., Mathews, F. S., Davidson, V. L., Satow, Y., Huizinga, E., and Vellieux, F. M. (1992) Crystal structure of an electron-transfer complex between methylamine dehydrogenase and amicyanin, Biochemistry 31, 4959-4964.
7. 551i, Science 264, 86-90.
8. Govindaraj, S., Eisenstein, E., Jones, L. H., Sanders-Loehr, J., Chistoserdov, A. Y., Davidson, V. L., and Edwards, S. L. (1994) Aromatic amine dehydrogenase, a second tryptophan tryptophylquinone enzyme, J. Bacteriol. 176, 2922-2929.
9. Hyun, Y. L., and Davidson, V. L. (1995) Mechanistic studies of aromatic amine dehydrogenase, a tryptophan tryptophylquinone enzyme, Biochemistry 34, 816-823.
10. McIntire, W. S., Wemmer, D. E., Chistoserdov, A., and Lidstrom, M. E. (1991) A new cofactor in a prokaryotic enzyme: Tryptophan tryptophylquinone as the redox prosthetic group in methylamine dehydrogenase, Science 252, 817-824.
11. Hyun, Y. L., and Davidson, V. L. (1995) Unusually large isotope effect for the reaction of aromatic amine dehydrogenase. A common feature of quinoproteins? Biochim. Biophys. Acta 1251, 198-200.
12. Masgrau, L., Roujeinikova, A., Johannissen, L. O., Hothi, P., Basran, J., Ranaghan, K. E., Mulholland, A. J., Sutcliffe, M. J., Scrutton, N. S., and Leys, D. (2006) Atomic description of an enzyme reaction dominated by proton tunneling, Science 312, 237-241.
13. Edwards, S. L., Davidson, V. L., Hyun, Y. L., and Wingfield, P. T. (1995) Spectroscopic evidence for a common electron transfer pathway for two tryptophan tryptophylquinone enzymes, J. Biol. Chem. 270, 4293-4298.
14. Hyun, Y. L., and Davidson, V. L. (1995) Electron transfer reactions between aromatic amine dehydrogenase and azurin, Biochemistry 34, 12249-12254.
15. Hyun, Y. L., Zhu, Z., and Davidson, V. L. (1999) Gated and ungated electron transfer reactions from aromatic amine dehydrogenase to azurin, J. Biol. Chem. 274, 29081-29086.
16. Davidson, V. L. (2002) Chemically gated electron transfer. A means of accelerating and regulating rates of biological electron transfer, Biochemistry 41, 14633-14636.
17. Chistoserdov, A. Y. (2001) Cloning, sequencing and mutagenesis of the genes for aromatic amine dehydrogenase from Alcaligenes faecalis and evolution of amine dehydrogenases, Microbiology 147, 2195-2202.
18. Brooks, H. B., Jones, L. H., and Davidson, V. L. (1993) Deuterium kinetic isotope effect and stopped-flow kinetic studies of the quinoprotein methylamine dehydrogenase, Biochemistry 32, 2725-2729.
19. Davidson, V. L., Graichen, M. E., and Jones, L. H. (1993) Binding constants for a physiologic electron-transfer protein complex between methylamine dehydrogenase and amicyanin. Effects of ionic strength and bound copper on binding, Biochim. Biophys. Acta 1144, 39-45.
20. Davidson, V. L., Jones, L. H., Graichen, M. E., Mathews, F. S., and Hosler, J. P. (1997) Factors which stabilize the methylamine dehydrogenase-amicyanin electron transfer protein complex revealed by site-directed mutagenesis, Biochemistry 36, 12733-12738.
21. Baker, E. N. (1988) Structure of azurin from Alcaligenes denitrificans refinement at 1.8 Å resolution and comparison of the two crystallographically independent molecules, J. Mol. Biol. 203, 1071-1095.
22. Durley, R., Chen, L., Lim, L. W., Mathews, F. S., and Davidson, V. L. (1993) Crystal structure analysis of amicyanin and apoamicyanin from Paracoccus denitrificans at 2.0 Å and 1.8 Å resolution, Protein Sci. 2, 739-752.
23. Merli, A., Brodersen, D. E., Morini, B., Chen, Z., Durley, R. C., Mathews, F. S., Davidson, V. L., and Rossi, G. L. (1996) Enzymatic and electron transfer activities in crystalline protein complexes, J. Biol. Chem. 271, 9177-9180.
24. Ferrari, D., Merli, A., Peracchi, A., Di Valentin, M., Carbonera, D., and Rossi, G. L. (2003) Catalysis and electron transfer in protein crystals: The binary and ternary complexes of methylamine dehydrogenase with electron acceptors, Biochim. Biophys. Acta 1647, 337-342.
25. McPherson, A. (1999) Crystallization of biological macromolecules, Cold Spring Harbor Laboratory Press, Plainview, NY.
26. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected by oscillation methods, Methods Enzymol. 276, 307-326.
27. Chen, L., Mathews, F. S., Davidson, V. L., Tegoni, M., Rivetti, C., and Rossi, G. L. (1993) Preliminary crystal structure studies of a ternary electron transfer complex between a quinoprotein, a blue copper protein, and a c-type cytochrome, Protein Sci. 2, 147-154.
28. Rivetti, C., Mozzarelli, A., Rossi, G. L., Henry, E. R., and Eaton, W. A. (1993) Oxygen binding by single crystals of hemoglobin, Biochemistry 32, 2888-2906.
29. Pearson, A. R., Mozzarelli, A., and Rossi, G. L. (2004) Microspectrophotometry for structural enzymology, Curr. Opin. Struct. Biol. 14, 656-662.
30. Collaborative Computational Project Number 4 (1994) Collaborative computational project number 4, Acta Crystallogr. D50, 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 & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
32. Roussel, A., and Cambillau, C. (1991) in Silicon graphics geometry partners directory 86, Silicon Graphics, Mountain View, CA.
33. Schomaker, V., and Trueblood, K. (1968) On the rigid-body motion of molecules in crystals, Acta Crystallogr. B24, 63-76.
34. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of t1s parameters to model anisotropic displacements in macro molecular refinement, Acta Crystallogr. D57, 122-133.
35. Kurnikov, I. V. (2000) HARLEM, University of Pittsburgh, Pittsburgh, PA.
36. Onuchic, J. N., Beratan, D. N., Winkler, J. R., and Gray, H. B. (1992) Pathway analysis of protein electron-transfer reactions, Annu. Rev. Biophys. Biomol. Struct. 21, 349-377.
37. Regan, J. J., Risser, S. M., Beratan, D. N., and Onuchic, J. N. (1993) Protein electron transport: Single versus multiple pathways, J. Phys. Chem. 97, 13083-13088.
38. 15N-NMR of the tryptophan tryptophylquinone aminoquinol reaction intermediate of methylamine dehydrogenase, J. Am. Chem. Soc. 118, 12868-12869.
39. 13C NMR, Biochem. J. 330 (Part 3), 1159-1163.
40. Bishop, G. R., and Davidson, V. L. (1995) Intermolecular electron transfer from substrate-reduced methylamine dehydrogenase to amicyanin is linked to proton transfer, Biochemistry 34, 12082-12086.
41. Marcus, R. A., and Sutin, N. (1985) Electron transfers in chemistry and biology, Biochim. Biophys. Acta 811, 265-322.
42. Brooks, H. B., and Davidson, V. L. (1994) Kinetic and thermodynamic analysis of a physiologic intermolecular electron-transfer reaction between methylamine dehydrogenase and amicyanin, Biochemistry 33, 5696-5701.
43. Gray, H. B., and Winkler, J. R. (2005) Long-range electron transfer, Proc. Natl. Acad. Sci. U.S.A. 102, 3534-3539.