Branched activation- and catalysis-specific pathways for electron relay to the manganese/iron cofactor in ribonucleotide reductase from Chlamydia trachomatis

Biochemistry

Volumn 47, Issue 33, 2008, Pages 8477-8484

  Jiang, Wei ^a   Saleh, Lana ^a,c   Barr, Eric W ^a   Xie, Jiajia ^a   Gardner, Monique Maslak ^a   Krebs, Carsten ^a,b   Bollinger Jr , J Martin ^a,b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Department of Chemistry Pennsylvania State University ^*  (United States)

^c NEW ENGLAND BIOLABS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLAMYDIA TRACHOMATIS; CLASS I; COFACTOR; ELECTRON RELAY; RIBONUCLEOTIDE REDUCTASE; TYROSYL RADICALS;

ASCORBIC ACID; IRON; MANGANESE; RIBONUCLEOTIDE REDUCTASE;

ARTICLE; CATALYSIS; CHLAMYDIA TRACHOMATIS; CONTROLLED STUDY; ELECTRON; ELECTRON TRANSPORT; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REDUCTION;

CHLAMYDIA TRACHOMATIS; ESCHERICHIA COLI;

EID: 49749105567     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800881m     Document Type: Article

References (55)

1. Nordlund, P., and Reichard, P. (2006) Ribonucleotide reductases. Annu. Rev. Biochem. 75, 681-706.
2. Stubbe, J. (2003) Di-iron-tyrosyl radical ribonucleotide reductases. Curr. Opin. Chem. Biol. 7, 183-188.
3. Mao, S. S., Yu, G. X., Chalfoun, D., and Stubbe, J. (1992) Characterization of C439SR1, a mutant of Escherichia coli ribonucleotide 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.
4. Uhlin, U., and Eklund, H. (1994) Structure of ribonucleotide reductase protein R1. Nature 370, 533-539.
5. Stubbe, J., Nocera, D. G., Yee, C. S., and Chang, M. C. Y. (2003) Radical initiation in the class I ribonucleotide reductase: Long-range proton-coupled electron transfer? Chem. Rev. 103, 2167-2202.
6. Stubbe, J., and Ackles, D. (1980) On the mechanism of ribonucleo-side diphosphate reductase from Escherchia coli. Evidence for 3′-C-H bond cleavage. J. Biol. Chem. 255, 8027-8030.
7. Stubbe, J., Ator, M., and Krenitsky, T. (1983) Mechanism of ribonucleoside diphosphate reductase from Escherichia coli. Evidence for 3′-C-H bond cleavage. J. Biol. Chem. 258, 1625-1631.
8. Licht, S., Gerfen, G. J., and Stubbe, J. (1996) Thiyl radicals in ribonucleotide reductases. Science 271, 477-481.
9. 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.
10. Ekberg, M., Pötsch, 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.
11. Ekberg, M., Sahlin, M., Eriksson, M., and Sjöberg, B.-M. (1996) Two conserved tyrosine residues in protein Rl participate in an intermolecular electron transfer in ribonucleotide reductase. J. Biol. Chem. 271, 20655-20659.
12. Nordlund, P., Sjöberg, B.-M., and Eklund, H. (1990) Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345, 593-598.
13. Rova, U., Adrait, A., Pötsch, 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.
14. 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.
15. Seyedsayamdost, M. R., and Stubbe, J. (2006) Site-specific replacement of Y356 with 3,4-dihydroxyphenylalanine in the β2 subunit of E. coli ribonucleotide reductase. J. Am. Chem. Soc. 128, 2522-2523.
16. 356DOPA-β2 heterodimer of E. coli ribonucleotide reductase. J. Am. Chem. Soc. 129, 2226-2227.
17. 731 in radical propagation. J. Am. Chem. Soc. 129, 15060-15071.
18. Atkin, C. L., Thelander, L., Reichard, P., and Lang, G. (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.
19. 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.
20. 2+ reaction by optical, EPR, and Mössbauer spectroscopies. J. Am. Chem. Soc. 116, 8015-8023.
21. Elgren, T. E., Lynch, J. B., Juarez-Garcia, C., Münck, E., Sjöberg, B.-M., and Que, L. (1991) Electron transfer associated with oxygen activation in the B2 protein of ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 266, 19265-19268.
22. 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.
23. 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.
24. 2+ reaction by optical, EPR, and Mössbauer spectroscopies. J. Am. Chem. Soc. 116, 8024-8032.
25. 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.
26. 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.
27. 2O. J. Am. Chem. Soc. 118, 281-282.
28. 17O ENDOR. J. Am. Chem. Soc. 120, 12910-12919.
29. 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 E. coli ribonucleotide reductase. 1. Mössbauer characterization of the diferric radical precursor. J. Am. Chem. Soc. 116, 8007-8014.
30. 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 E. coli ribonucleotide reductase. J. Am. Chem. Soc. 118, 7551-7557.
31. 1,2H CW and pulsed ENDOR. J. Am. Chem. Soc. 119, 9816-9824.
32. 2 activation by protein R2 of Escherichia coli ribonucleotide reductase: Relevance to R1-R2 radical transfer in nucleotide reduction? Biochemistry 45, 8823-8830.
33. Climent, I., Sjöberg, B.-M., and Huang, C. Y. (1992) Site-directed mutagenesis and deletion of the carboxyl terminus of Escherichia coli ribonucleotide reductase protein R2. Effects on catalytic activity and subunit interaction. Biochemistry 31, 4801-4807.
34. Jiang, W., Yun, D., Saleh, L., Barr, E. W., Xing, G., Hoffart, L. M., Maslak, M.-A., Krebs, C., and Bollinger, J. M., Jr. (2007) A manganese(IV)/iron(III) cofactor in Chlamydia trachomatis ribonucleotide reductase. Science 316, 1188-1191.
35. Jiang, W., Bollinger, J. M., Jr., and Krebs, C. (2007) The active form of Chlamydia trachomatis ribonucleotide reductase R2 protein contains a heterodinuclear Mn(IV)/Fe(III) cluster with S = 1 ground state. J. Am. Chem. Soc. 129, 7504-7505.
36. Voevodskaya, N., Lendzian, F., Ehrenberg, A., and Gräslund, A. (2007) High catalytic activity achieved with a mixed manganeseiron site in protein R2 of Chlamydia ribonucleotide reductase. FEBS Lett. 581, 3351-3355.
37. Roshick, C., Iliffe-Lee, E. R., and McClarty, G. (2000) Cloning and characterization of ribonucleotide reductase from Chlamydia trachomatis. J. Biol. Chem. 275, 38111-38119.
38. Jiang, W., Hoffart, L. M., Krebs, C., and Bollinger, J. M., Jr. (2007) A manganese(IV)/iron(IV) intermediate in assembly of the manganese(IV)/iron(III) cofactor of Chlamydia trachomatis ribonucleotide reductase. Biochemistry 46, 8709-8716.
39. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326.
40. Jiang, W., Xie, J., Nørgaard, H., Bollinger, J. M., Jr., and Krebs, C. (2008) Rapid and quantitative activation of Chlamydia trachomatis ribonucleotide reductase by hydrogen peroxide. Biochemistry 47, 4477-4483.
41. Price, J. C., Barr, E. W., Tirupati, B., Bollinger, J. M., Jr., and Krebs, C. (2003) The first direct characterization of a high-valent iron intermediate in the reaction of an α-ketoglutarate-dependent dioxygenase: A high-spin Fe(IV) complex in taurine/a-ketoglutarate dioxygenase (TauD) from Escherichia coli. Biochemistry 42, 7497-7508.
42. Högbom, M., Stenmark, P., Voevodskaya, N., McClarty, G., Gräslund, A., and Nordlund, P. (2004) The radical site in Chlamydial ribonucleotide reductase defines a new R2 subclass. Science 305, 245-248.
43. Bollinger, J. M., Jr., Krebs, C., Vicol, A., Chen, S., Ley, B. A., Edmondson, D. E., and Huynh, B. H. (1998) Engineering the diiron site of Escherichia coli ribonucleotide reductase protein R2 to accumulate an intermediate similar to Hperoxo, the putative peroxodiiron(III) complex from the methane monooxygenase catalytic cycle. J. Am. Chem. Soc. 120, 1094-1095.
44. 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.
45. 2 activation by binuclear non-heme iron enzymes. J. Am. Chem. Soc. 126, 8842-8855.
46. Baldwin, J., Voegtli, W. C., Khidekel, N., Moenne-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.
47. Valentine, A. M., Stahl, S. S., and Lippard, S. J. (1999) Mechanistic studies of the reaction of reduced methane monooxygenase hydroxylase with dioxygen and substrates. J. Am. Chem. Soc. 121, 3876-3887.
48. Yun, D., Krebs, C., Gupta, G. P., Iwig, D. F., Huynh, B. H., and Bollinger, J. M., Jr. (2002) Facile electron transfer during formation of cluster X and kinetic competence of X for tyrosyl radical production in protein R2 of ribonucleotide reductase from mouse. Biochemistry 41, 981-990.
49. Yun, D., Garcia-Serres, R., Chicalese, B. M., An, Y. H., Huynh, B. H., and Bollinger, J. M., Jr. (2007) (μ-1,2-Peroxo)diiron(III/III) complex as a precursor to the diiron(III/IV) intermediate X in the assembly of the iron-radical cofactor of ribonucleotide reductase from mouse. Biochemistry 46, 1925-1932.
50. 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.
51. 1H-ENDOR and X-ray studies. Biochim. Biophys. Acta 1774, 1254-1263.
52. IV replacement of tyrosyl radical in a class I ribonucleotide reductase. Biochem. Biophys. Res. Commun. 330, 1213-1216.
53. IV cluster. Proc. Natl. Acad. Sci. U.S.A. 103, 9850-9854.
54. Hristova, D., Wu, C.-H., Jiang, W., Krebs, C., and Stubbe, J. (2008) Importance of the maintenance pathway in the regulation of the activity of Escherichia coli ribonucleotide reductase. Biochemistry 47, 3989-3999.
55. Wu, C. H., Jiang, W., Krebs, C., and Stubbe, J. (2007) YfaE, a ferredoxin involved in diferric-tyrosyl radical maintenance in Escherichia coli ribonucleotide reductase. Biochemistry 46, 11577-11588.