Characterization of electron tunneling and hole hopping reactions between different forms of maug and methylamine dehydrogenase within a natural protein complex

Biochemistry

Volumn 51, Issue 35, 2012, Pages 6942-6949

  Choi, Moonsung ^a   Shin, Sooim ^a   Davidson, Victor L ^a  

^a UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR DAMAGE; COMPUTATIONAL ANALYSIS; DRIVING FORCES; ELECTRON DONORS; ELECTRON TRANSFER; ELECTRONIC COUPLING; HOPPING MECHANISM; METHYLAMINE DEHYDROGENASE; MULTI-STEP; MULTISTEP HOPPING; NATURAL PROTEINS; PROTEIN COMPLEXES; PROTEIN MATRIX; REDOX POTENTIALS; RELATIVE VALUE; SINGLE-STEP; THERMO DYNAMIC ANALYSIS; TUNNELING REACTION;

AMINO ACIDS; BIOACTIVITY; ELECTRON TUNNELING; REDOX REACTIONS; THERMOANALYSIS;

PROTEINS;

AMINE DEHYDROGENASE; ENZYME; MAUG PROTEIN; QUINONE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME MECHANISM; ENZYME STRUCTURE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; SCANNING TUNNELING MICROSCOPY; SYNTHESIS; THERMODYNAMICS;

BACTERIAL PROTEINS; ELECTRON TRANSPORT; KINETICS; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; PARACOCCUS DENITRIFICANS; QUINONES; THERMODYNAMICS;

EID: 84865713421     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300817d     Document Type: Article

References (44)

1. Beratan, D. N., Onuchic, J. N., and Hopfield, J. J. (1987) Electron tunneling through covalent and noncovalent pathways in proteins J. Chem. Phys. 86, 4488-4498
2. Gray, H. B. and Winkler, J. R. (2003) Electron tunneling through proteins Q. Rev. Biophys. 36, 341-372
3. Marcus, R. A. and Sutin, N. (1985) Electron transfers in chemistry and biology Biochim. Biophys. Acta 811, 265-322
4. Page, C. C., Moser, C. C., Chen, X., and Dutton, P. L. (1999) Natural engineering principles of electron tunnelling in biological oxidation-reduction Nature 402, 47-52
5. Davidson, V. L. (2008) Protein control of true, gated and coupled electron transfer reactions Acc. Chem. Res. 41, 730-738
6. Giese, B., Graber, M., and Cordes, M. (2008) Electron transfer in peptides and proteins Curr. Opin. Chem. Biol. 12, 755-759
7. Wang, Y., Graichen, M. E., Liu, A., Pearson, A. R., Wilmot, C. M., and Davidson, V. L. (2003) MauG, a novel diheme protein required for tryptophan tryptophylquinone biogenesis Biochemistry 42, 7318-7325
8. Davidson, V. L. (2001) Pyrroloquinoline quinone (PQQ) from methanol dehydrogenase and tryptophan tryptophylquinone (TTQ) from methylamine dehydrogenase Adv. Protein Chem. 58, 95-140
9. Pearson, A. R., De La Mora-Rey, T., Graichen, M. E., Wang, Y., Jones, L. H., Marimanikkupam, S., Agger, S. A., Grimsrud, P. A., Davidson, V. L., and Wilmot, C. M. (2004) Further insights into quinone cofactor biogenesis: Probing the role of mauG in methylamine dehydrogenase tryptophan tryptophylquinone formation Biochemistry 43, 5494-5502
10. Li, X., Fu, R., Lee, S., Krebs, C., Davidson, V. L., and Liu, A. (2008) A catalytic di-heme bis-Fe(IV) intermediate, alternative to an Fe(IV) - O porphyrin radical Proc. Natl. Acad. Sci. U.S.A. 105, 8597-8600
11. Afzali, A., Dimitrakopoulos, C. D., and Breen, T. L. (2002) High-performance, solution-processed organic thin film transistors from a novel pentacene precursor J. Am. Chem. Soc. 124, 8812-8813
12. Berlin, Y. A., Hutchison, G. R., Rempala, P., Ratner, M. A., and Michl, J. (2003) Charge Hopping in Molecular Wires as a Sequence of Electron-Transfer Reactions J. Phys. Chem. A 107, 3970-3980
13. Genereux, J. C. and Barton, J. K. (2010) Mechanisms for DNA charge transport Chem. Rev. 110, 1642-1662
14. Giese, B. (2002) Electron transfer in DNA Curr. Opin. Chem. Biol. 6, 612-618
15. Lewis, F. D., Letsinger, R. L., and Wasielewski, M. R. (2001) Dynamics of photoinduced charge transfer and hole transport in synthetic DNA hairpins Acc. Chem. Res. 34, 159-170
16. Bixon, M., Giese, B., Wessely, S., Langenbacher, T., Michel-Beyerle, M. E., and Jortner, J. (1999) Long-range charge hopping in DNA Proc. Natl. Acad. Sci. U.S.A. 96, 11713-11716
17. Giese, B., Amaudrut, J., Kohler, A. K., Spormann, M., and Wessely, S. (2001) Direct observation of hole transfer through DNA by hopping between adenine bases and by tunnelling Nature 412, 318-320
18. Stubbe, J., Nocera, D. G., Yee, C. S., and Chang, M. C. (2003) Radical initiation in the class I ribonucleotide reductase: Long-range proton-coupled electron transfer? Chem. Rev. 103, 2167-2201
19. Baldwin, J., Krebs, C., Ley, B. A., Edmondson, D. E., Huynh, B. H., and Bollinger, J. H. (2000) Mechanism of rapid electron transfer during oxygen activation in the R2 subunit of Escherichia coli ribonucleotide reductase. 1. Evidence for a transient tryptophan radical J. Am. Chem. Soc. 122, 12195-12206
20. Lukacs, A., Eker, A. P., Byrdin, M., Brettel, K., and Vos, M. H. (2008) Electron hopping through the 15 Å triple tryptophan molecular wire in DNA photolyase occurs within 30 ps J. Am. Chem. Soc. 130, 14394-14395
21. Shih, C., Museth, A. K., Abrahamsson, M., Blanco-Rodriguez, A. M., Di Bilio, A. J., Sudhamsu, J., Crane, B. R., Ronayne, K. L., Towrie, M., Vlcek, A., Jr., Richards, J. H., Winkler, J. R., and Gray, H. B. (2008) Tryptophan-accelerated electron flow through proteins Science 320, 1760-1762
22. Seifert, J. L., Pfister, T. D., Nocek, J. M., Lu, Y., and Hoffman, B. M. (2005) Hopping in the electron-transfer photocycle of the 1:1 complex of Zn-cytochrome c peroxidase with cytochrome c J. Am. Chem. Soc. 127, 5750-5751
23. Abu Tarboush, N., Jensen, L. M. R., Yukl, E. T., Geng, J., Liu, A., Wilmot, C. M., and Davidson, V. L. (2011) Mutagenesis of tryptophan199 suggets that hopping is required for MauG-dependent tryptophan tryptophylquinone biosynthesis Proc. Natl. Acad. Sci. U.S.A. 108, 16956-16961
24. Jensen, L. M., Sanishvili, R., Davidson, V. L., and Wilmot, C. M. (2010) In crystallo posttranslational modification within a MauG/pre-methylamine dehydrogenase complex Science 327, 1392-1394
25. Li, X., Jones, L. H., Pearson, A. R., Wilmot, C. M., and Davidson, V. L. (2006) Mechanistic possibilities in MauG-dependent tryptophan tryptophylquinone biosynthesis Biochemistry 45, 13276-13283
26. Wang, Y., Li, X., Jones, L. H., Pearson, A. R., Wilmot, C. M., and Davidson, V. L. (2005) MauG-dependent in vitro biosynthesis of tryptophan tryptophylquinone in methylamine dehydrogenase J. Am. Chem. Soc. 127, 8258-8259
27. Shin, S., Abu Tarboush, N., and Davidson, V. L. (2010) Long-range electron transfer reactions between hemes of MauG and different forms of tryptophan tryptophylquinone of methylamine dehydrogenase Biochemistry 49, 5810-5816
28. Lee, S., Shin, S., Li, X., and Davidson, V. (2009) Kinetic mechanism for the initial steps in MauG-dependent tryptophan tryptophylquinone biosynthesis Biochemistry 48, 2442-2447
29. Davidson, V. L. (1990) Methylamine dehydrogenases from methylotrophic bacteria Methods Enzymol. 188, 241-246
30. Kurnikov, I. V. (2000) HARLEM Computer Program, University of Pittsburgh, Pittsburgh, PA (http://harlem.chem.cmu.edu/).
31. Abu Tarboush, N., Jensen, L. M., Feng, M., Tachikawa, H., Wilmot, C. M., and Davidson, V. L. (2010) Functional importance of tyrosine 294 and the catalytic selectivity for the bis-Fe(IV) state of MauG revealed by replacement of this axial heme ligand with histidine Biochemistry 49, 9783-9791
32. Li, X., Feng, M., Wang, Y., Tachikawa, H., and Davidson, V. L. (2006) Evidence for redox cooperativity between c-type hemes of MauG which is likely coupled to oxygen activation during tryptophan tryptophylquinone biosynthesis Biochemistry 45, 821-828
33. Brooks, H. B. and Davidson, V. L. (1994) Free energy dependence of the electron transfer reaction between methylamine dehydrogenase and amicyanin J. Am. Chem. Soc. 116, 11201-11202
34. 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
35. Sun, D., Chen, Z. W., Mathews, F. S., and Davidson, V. L. (2002) Mutation of αPhe55 of methylamine dehydrogenase alters the reorganization energy and electronic coupling for its electron transfer reaction with amicyanin Biochemistry 41, 13926-13933
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. Davidson, V. L. (2000) What controls the rates of interprotein electron-transfer reactions Acc. Chem. Res. 33, 87-93
38. Li, X., Fu, R., Liu, A., and Davidson, V. L. (2008) Kinetic and physical evidence that the diheme enzyme MauG tightly binds to a biosynthetic precursor of methylamine dehydrogenase with incompletely formed tryptophan tryptophylquinone Biochemistry 47, 2908-2912
39. Feng, M., Jensen, L. M., Yukl, E. T., Wei, X., Liu, A., Wilmot, C. M., and Davidson, V. L. (2012) Proline 107 is a major determinant in maintaining the structure of the distal pocket and reactivity of the high-spin heme of MauG Biochemistry 51, 1598-1606
40. Battistuzzi, G., Bellei, M., Bortolotti, C. A., and Sola, M. (2010) Redox properties of heme peroxidases Arch. Biochem. Biophys. 500, 21-36
41. DeFelippis, M. R., Murthy, C. P., Faraggi, M., and Klapper, M. H. (1989) Pulse radiolytic measurement of redox potentials: The tyrosine and tryptophan radicals Biochemistry 28, 4847-4853
42. Tommos, C., Skalicky, J. J., Pilloud, D. L., Wand, A. J., and Dutton, P. L. (1999) De novo proteins as models of radical enzymes Biochemistry 38, 9495-9507
43. Davidson, V. L. (2000) Effects of kinetic coupling on experimentally determined electron transfer parameters Biochemistry 39, 4924-4928
44. Winkler, J. R. and Gray, H. B. (1992) Electron transfer in ruthenium-modified proteins Chem. Rev. 92, 369-379