Mediation by indole analogues of electron transfer during oxygen activation in variants of Escherichia coli ribonucleotide reductase R2 lacking the electron-shuttling tryptophan 48

Biochemistry

Volumn 43, Issue 20, 2004, Pages 5943-5952

  Saleh, Lana ^a   Kelch, Brian A ^a,b   Pathickal, Betsy A ^a,c   Baldwin, Jeffrey ^a,d   Ley, Brenda A ^a   Bollinger Jr , J Martin ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON TRANSITIONS; ENZYMES; ESCHERICHIA COLI; OXIDATION; QUENCHING;

CHEMICAL MEDIATION; ELECTRON TRANSFER;

BIOCHEMISTRY;

1 METHYLINDOLE; 2 METHYLINDOLE; 3 (2 HYDROXYLETHYL)INDOLE; 3 (HYDROXYMETHYL)INDOLE; ARGININE; CARBOXYLATE BRIDGED DIIRON; CARBOXYLIC ACID DERIVATIVE; HYBRID PROTEIN; INDOLE; INDOLE DERIVATIVE; OXYGEN; PHENYLALANINE; RIBONUCLEOTIDE REDUCTASE; RIBONUCLEOTIDE REDUCTASE R2; SKATOLE; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CATION TRANSPORT; CHEMICAL REACTION; CHEMICAL REACTION KINETICS; ELECTRON TRANSPORT; ENZYME ANALYSIS; ESCHERICHIA COLI; IRON TRANSPORT; MEDIATOR RELEASE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN STABILITY; PROTEIN VARIANT; REDUCTION KINETICS; STRUCTURE ANALYSIS;

ELECTRON TRANSPORT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; INDOLES; IRON; MOLECULAR STRUCTURE; OXYGEN; RIBONUCLEOTIDE REDUCTASES; SPECTROSCOPY, MOSSBAUER; TRYPTOPHAN;

CHEN; ESCHERICHIA COLI; NEGIBACTERIA;

EID: 2442642829     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi036098m     Document Type: Article

References (57)

1. Atkin, C. L., Thelander, L., and Reichard, P. (1973) Iron and free radical in ribonucleotide reductase. Exchange of iron and Mössbauer spectroscopy of the protein B2 subunit of the Escherichia coli enzyme, J. Biol. Chem. 248, 7464-7472.
2. Sjöberg, B.-M., Reichard, P., Gräslund, A., and Ehrenberg, A. (1977) Nature of the free radical in ribonucleotide reductase from Escherichia coli, J. Biol. Chem. 252, 536-541.
3. Larsson, A., and Sjöbere, B.-M. (1986) Identification of the stable free radical tyrosine residue in ribonucleotide reductase, EMBO J. 5, 2037-2040.
4. Fontecave, M., Nordlund, P., Eklund, H., and Reichard, P. (1992) The redox centers of ribonucleotide reductase of Escherichia coli, Adv. Enzymol. Relat. Areas Mol. Biol. 65, 147-183.
5. Sjöberg, B.-M. (1997) Ribonucleotide reductases - A group of enzymes with different metallosites and a similar reaction mechanism, Struct. Bond. 88, 139-173.
6. Stubbe, J., and Riggs-Gelasco, P. (1998) Harnessing free radicals: formation and function of the tyrosyl radical in ribonucleotide reductase, Trends Biochem. Sci. 23, 438-443.
7. Stubbe, J. (1990) Ribonucleotide Reductases: amazing and confusing, J. Biol. Chem. 265, 5329-5332.
8. Mao, S. S., Yu, G. X., Chalfoun, D., and Stubbe, J. (1992) Characterization of C439SR1, a mutant of Escherichia coli ribonucleoside diphosphate reductase: evidence that C439 is a residue essential for nucleotide reduction and C439SR1 is a protein possessing novel thioredoxin-like activity, Biochemistry 31, 9752-9759.
9. Mao, S. S., Holler, T. P., Yu, G. X., Bollinger, J. M., Jr., Booker, S., Johnston, M. I., and Stubbe, J. (1992) A model for the role of multiple cysteine residues involved in ribonucleotide reduction: amazing and still confusing, Biochemistry 31, 9733-9743.
10. Uhlin, U., and Eklund, H. (1994) Structure of ribonucleotide reductase protein R1, Nature 370, 533-539.
11. Stubbe, J., and Ackles, D. (1980) On the mechanism of ribonucleoside diphosphate reductase from Escherichia coli, J. Biol. Chem. 255, 8027-8030.
12. Stubbe, J., Nocera, D. G., Yee, C. S., and Chang, M. C. Y. (2003) Radical initiation in the class I ribonucleotide reductase: longrange proton-coupled electron transfer? Chem. Rev. 103, 2167-2202.
13. Ekberg, M., Potsch, S., Sandin, E., Thunnissen, M., Nordlund, P., Sahlin, M., and Sjöberg, B.-M. (1998) Preserved catalytic activity in an engineered ribonucleotide reductase R2 protein with a nonphysiological radical transfer pathway. The importance of hydrogen bond connections between the participating residues, J. Biol. Chem. 273, 21003-21008.
14. Ekberg, M., Sahlin, M., Eriksson, M., and Sjöberg, B.-M. (1996) Two conserved tyrosine residues in protein R1 participate in an intermolecular electron transfer in ribonucleotide reductase, J. Biol. Chem. 271, 20655-20659.
15. Rova, U., Adrait, A., Potsch, S., Gräslund, A., and Thelander, L. (1999) Evidence by mutagenesis that Tyr(370) of the mouse ribonucleotide reductase R2 protein is the connecting link in the intersubunit radical transfer pathway, J. Biol. Chem. 274, 23746-23751.
16. Rova, U., Goodtzova, K., Ingemarson, R., Behravan, G., Gräslund, A., and Thelander, L. (1995) Evidence by site-directed mutagenesis supports long-range electron transfer in mouse ribonucleotide reductase, Biochemistry, 34, 4267-4275.
17. Siegbahn, P. E. M., Eriksson, L., Himo, F., and Pavlov, M. (1998) Hydrogen atom transfer in ribonucleotide reductase (RNR), J. Phys. Chem. 102, 10622-10629.
18. Bollinger, J. M., Jr., Edmondson, D. E., Huynh, B. H., Filley, J., Norton, J. R., and Stubbe, J. (1991) Mechanism of assembly of the tyrosyl radical-dinuclear iron cluster cofactor of ribonucleotide reductase, Science 253, 292-298.
19. 2+ reaction by optical, EPR, and Mössbauer spectroscopies, J. Am. Chem. Soc. 116, 8015-8023.
20. 2+ reaction by optical, EPR, and Mössbauer spectroscopies, J. Am. Chem. Soc. 116, 8024-8032.
21. Bollinger, J. M., Jr., Tong, W. H., Ravi, N., Huynh, B. H., Edmondson, D. E., and Stubbe, J. (1995) Use of rapid kinetics methods to study the assembly of the diferric-tyrosyl radical cofactor of Escherichia coli ribonucleotide reductase, Methods Enzymol. 258, 278-303.
22. Tong, W. H., Chen, S., Lloyd, S. G., Edmondson, D. E., Huynh, B. H., and Stubbe, J. (1996) Mechanism of assembly of the diferric cluster-tyrosyl radical cofactor of Escherichia coli ribonucleotide reductase from the diferrous form of the R2 subunit, J. Am. Chem. Soc. 118, 2107-2108.
23. Ochiai, E., Mann, G. J., Gräslund, A., and Thelander, L. (1990) Tyrosyl free radical formation in the small subunit of mouse ribonucleotide reductase, J. Biol. Chem, 265, 15758-15761.
24. Elgren, T. E., Lynch, J. B., Juarez-Garcia, C., Münck, E., Sjöberg, B.-M., and Que, L., Jr. (1991) Electron- transfer associated with oxygen activation in the B2 protein of ribonucleotide reductase from Escherichia coli, J. Biol. Chem. 266, 19265-19268.
25. Bollinger, J. M., Jr., Stubbe, J., Huynh, B. H., and Edmondson, D. E. (1991) Novel diferric radical intermediate responsible for tyrosyl radical formation in assembly of the cofactor of ribonucleotide reductase, J. Am. Chem. Soc. 113, 6289-6291.
26. Ravi, N., Bollinger, J. M., Jr., Huynh, B. H., Edmondson, D. E., and Stubbe, J. (1994) Mechanism of assembly of the tyrosyl radical-diiron(III) cofactor of Escherichia coli ribonucleotide reductase: 1. Mössbauer characterization of the diferric radical precursor, J. Am. Chem. Soc. 116, 8007-8014.
27. Sturgeon, B. E., Burdi, D., Chen, S., Huynh, B. H., Edmondson, D. E., Stubbe, J., and Hoffman, B. M. (1996) Reconsideration of X, the diiron intermediate formed during cofactor assembly in Escherichia coli ribonucleotide reductase, J. Am. Chem. Soc. 118, 7551-7557.
28. 170, J. Am. Chem. Soc. 118, 281-282.
29. 1,2HCW and pulsed ENDOR, J. Am. Chem. Soc. 119, 9816-9824.
30. 17 ENDOR, J. Am. Chem. Soc. 120, 12910-12919.
31. Riggs-Gelasco, P. J., Shu, L., Chen, S., Burdi, D., Huynh, B. H., Que, L., Jr., and Stubbe, J. (1998) EXAFS characterization of the intermediate X generated during the assembly of the Eschetichia coli ribonucleotide reductase R2 diferric tyrosyl radical cofactor, J. Am. Chem. Soc. 120, 849-860.
32. Baldwin, J., Krebs, C., Ley, B. A., Edmondson, D. E., Huynh, B. H., and Bollinger, J. M., Jr. (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.
33. Schmidt, P. P., Rova, U., Katterle, B., Thelander, L., and Gräslund, A. (1998) Kinetic evidence that a radical transfer pathway in protein R2 of mouse ribonucleotide reductase is involved in generation of the tyrosyl free radical, J. Biol. Chem. 273, 21463-21472.
34. Krebs, C., Chen, S., Baldwin, J., Ley, B. A., Patel, U., Edmondson, D. E., Huynh, B. H., and Bollinger, J. M., Jr. (2000) Mechanism of rapid electron transfer during oxygen activation in the R2 subunit of Escherichia coli ribonucleotide reductase. 2. Evidence for and consequences of blocked electron transfer in the W48F variant, J. Am. Chem. Soc. 122, 12207-12219.
35. Ormö, M., deMarë, F., Regnström, K., Åberg, A., Sahlin, M., Ling, J., Loehr, T. M., Sanders-Loehr, J., and Sjöberg, B.-M. (1992) Engineering of the iron site in ribonucleotide reductase to a self-hydroxylating monoxygenase, J. Biol. Chem. 267, 8711-8714.
36. Åberg, A., Ormö, M., Nordlund, P., and Sjöberg, B.-M. (1993) Autocatalytic generation of dopa in the engineered protein R2 F208Y from Escherichia coli ribonucleotide reductase and crystal structure of the dopa 208 protein, Biochemistry 32, 9845-9850.
37. Parkin, S. E., Chen, S., Ley, B. A., Mangravite, L., Edmondson, D. E., Huynh, B. H., and Bollinger, J. M., Jr. (1998) Electron injection through a specific pathway determines the outcome of oxygen activation at the diiron cluster in the F208Y mutant of Escherichia coli ribonucleotide reductase protein R2, Biochemistry 37, 1124-1130.
38. Toney, M. D., and Kirsch, J. F. (1989) Direct Brönsted analysis of the restoration of activity to a mutant enzyme by exogenous amines, Science 243, 1485-1488.
39. Sivaraja, M., Goodin, D. B., Smith, M., and Hoffman, B. M. (1989) Identification by ENDOR of Trpl91 as the free-radical site in cytochrome c peroxidase compound ES, Science 245, 738-740.
40. Erman, J. E., Vitello, L. B., Mauro, J. M., and Kraut, J. (1989) Detection of an oxyferryl porphyrin π-cation-radical intermediate in the reaction between hydrogen peroxide and a mutant yeast cytochrome c peroxidase. Evidence for tryptophan- 191 involvement in the radical site of compound I, Biochemistry 28, 7992-7995.
41. Houseman, A. L. P., Doan, P. E., Goodin, D. B., and Hoffman, D. M. (1993) Comprehensive explanation of the anomalous EPR spectra of wild-type and mutant cytochrome c peroxidase compound ES, Biochemistry 32, 4430-4443.
42. Huyett, J. E., Doan, P. E., Gurbiel, R., Houseman, A. L., Sivaraja, M., Goodin, D. B., and Hoffman, B. M. (1995) Compound ES of cytochrome c peroxidase contains a Trp π-Cation radical: characterization by continuous wave and pulsed Q-Band electron nuclear double resonance spectroscopy, J. Am. Chem. Soc. 117, 9033-9041.
43. Fitzgerald, M. M., Churchill, M. J., McRee, D. E., and Goodin, D. B. (1994) Small molecule binding to an artificially created cavity at the active site of cytochrome c peroxidase, Biochemistry 33, 3807-3818.
44. Fitzgerald, M. M., Musah, R. A., McRee, D. E., and Goodin, D. B. (1996) A ligand-gated, hinged loop rearrangement opens a channel to a buried artificial protein cavity, Nat. Struct. Biol. 3, 626-631.
45. Fitzgerald, M. M., Trester, M. L., Jensen, G. M., McRee, D. E., and Goodin, D. B. (1995) The role of aspartate-235 in the binding of cations to an artifical cavity at the radical site of cytochrome c peroxidase, Protein Sci. 4, 1844-1850.
46. Musah, R. A., Jensen, G. M., Rosenfeld, R. J., McRee, D. E., and Goodin, D. B. (1997) Variation in strength of an unconventional C-H to O hydrogen bond in an engineered protein cavity, J. Am. Chem. Soc. 119, 9083-9084.
47. peroxo, the putative peroxodiiron(III) complex from the methane monooxygenase catalytic cycle, J. Am. Chem. Soc. 120, 1094-1095.
48. Baldwin, J., Voegtli, W. C., Khidelkel, N., Moënne-Loccoz, P., Krebs, C., Pereira, A. S., Ley, B. A., Huynh, B. H., Loehr, T. M., Riggs-Gelasco, P. J., Rosenzweig, A. C.,and Bollinger, J. M., Jr. (2001) Rational reprogramming of the R2 subunit of Escherichia coli ribonucleotide reductase into a self-hydroxylating monooxygenase, J. Am. Chem. Soc. 123, 7017-7030.
49. Saleh, L., Krebs, C., Ley, B. A., Naik, S., Huynh, B. H., and Bollinger, J. M., Jr. (2004) Use of a chemical trigger for electron transfer to characterize a precursor to cluster X in assembly of the iron-radical cofactor of Escherichia coli ribonucleotide reductase, Biochemistry 43, 5953-5964.
50. 2 activation by non-heme diiron proteins: Identification of a symmetric μ-1,2-peroxide in a mutant of ribonucleotide reductase, Biochemistry 37, 14659-14663.
51. Salowe, S. P., and Stubbe, J. (1986) Cloning, overproduction, and purification of the B2 subunit of ribonucleoside diphosphate reductase, J. Bacteriol. 165, 363-366.
52. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data, Anal. Biochem. 182, 319-326.
53. Raibekas, A. A., and Massey, V. (1996) Glycerol-induced development of catalytically active conformation of Crotalus adamanteus L-amino acid oxidase in uitro, Proc. Natl. Acad. Sci. U.S.A. 93, 7546-7551.
54. Raibekas, A. A., and Massey, V. (1997) Glycerol-assisted restorative adjustment of flavoenzyme conformation perturbed by site-directed mutagenesis, J. Biol. Chem. 272, 22248-22252.
55. Jensen, G. M., Goodin, D. B., and Bunte, S. W. (1996) Density functional and MP2 calculations of spin densities of oxidized 3-methylindole: models for tryptophan radicals, J. Phys. Chem. 100, 954-959.
56. Liu, K. E., Wang, D., Huynh, B. H., Edmondson, D. E., Salifoglou, A., and Lippard, S. J. (1994) Spectroscopic detection of intermediates in the reaction of dioxygen with the reduced methane monooxygenase/hydroxylase from Methylococcus capsulatus (Bath), J. Am. Chem. Soc. 116, 7465-7466.
57. Baldwin, J., Krebs, C., Saleh, L., Stelling, M., Huynh, B. H., Bollinger, J. M., Jr., and Riggs-Gelasco, P. (2003) Structural characterization of the peroxodiiron(III) intermediate generated during oxygen activation by the W48A/D84E variant of ribonucleotide reductase protein R2 from Escherichia coli, Biochemistry 42, 13269-13279.