Use of 3-aminotyrosine to examine the pathway dependence of radical propagation in Escherichia coli ribonucleotide reductase

Biochemistry

Volumn 48, Issue 51, 2009, Pages 12125-12132

  Minnihan, Ellen C ^a   Seyedsayamdost, Mohammad R ^a,b   Stubbe, Joanne ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ALLOSTERIC EFFECTORS; COFACTORS; DIPHOSPHATES; DOUBLE MUTANTS; EPR SPECTROSCOPY; RIBONUCLEOTIDE REDUCTASE; STOPPED FLOW; THIYL RADICALS; TYROSYL RADICALS;

BINDING ENERGY; BINDING SITES; BIOCHEMISTRY; ELECTRON RESONANCE; ESCHERICHIA COLI; NUCLEOTIDES; OXIDATION; PARAMAGNETIC RESONANCE; QUANTUM THEORY; RATE CONSTANTS;

ELECTRON SPIN RESONANCE SPECTROSCOPY;

3 AMINOTYROSINE; RIBONUCLEOTIDE REDUCTASE; TYROSINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME BINDING; ESCHERICHIA COLI; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; ULTRAVIOLET SPECTROSCOPY;

ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FREE RADICALS; OXIDATION-REDUCTION; RIBONUCLEOSIDE DIPHOSPHATE REDUCTASE; TYROSINE;

ESCHERICHIA COLI;

EID: 73149099389     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901439w     Document Type: Article

References (44)

1. Gray, H. B., and Winkler, J. R. (2005) Long-range electron transfer. Proc. Natl. Acad. Sci. U.S.A. 102, 3534-3539.
2. Verkhovskaya, M. L., Belevich, N., Euro, L., Wikstrom, M., and Verkhovsky, M. I. (2008) Real-time electron transfer in respiratory complex I. Proc. Natl. Acad. Sci. U.S.A. 105, 3763-3767.
3. Igarashi, R. Y., and Seefeldt, L. C. (2003) Nitrogen fixation: The mechanism of the Mo-dependent nitrogenase. Crit. Rev. Biochem. Mol. Biol. 38, 351-384.
4. Loll, B., Kern, J., Saenger, W., Zouni, A., and Biesiadka, J. (2005) Towards complete cofactor arrangement in the 3.0 A ° resolution structure of photosystem II. Nature 438, 1040-1044.
5. Page, C. C., Moser, C. C., Chen, X., and Dutton, P. L. (1999) Natural engineering principles of electron tunnelling in biological oxidationreduction. Nature 402, 47-52.
6. Marcus, R. A., and Sutin, N. (1985) Nature of biological electron transfer. Biochim. Biophys. Acta 811, 265-322.
7. Langen, R., Chang, I. J., Germanas, J. P., Richards, J. H., Winkler, J. R., and Gray, H. B. (1995) Electron tunneling in proteins: Coupling through a β strand. Science 268, 1733-1735.
8. Osyczka, A., Moser, C. C., Daldal, F., and Dutton, P. L. (2004) Reversible redox energy coupling in electron transfer chains. Nature 427, 607-612.
9. Xiong, P., Nocek, J. M., Griffin, A. K., Wang, J., and Hoffman, B. M. (2009) Electrostatic redesign of the [myoglobin, cytochrome b5] interface to create a well-defined docked complex with rapid interprotein electron transfer. J. Am. Chem. Soc. 131, 6938-6939.
10. Sjöberg, B. M., and Reichard, P. (1977) Nature of the free radical in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 252, 536-541.
11. Barry, B. A., and Babcock,G. T. (1987) Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc. Natl. Acad. Sci. U.S.A. 84, 7099-7103.
12. 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, 2167-2201.
13. Stubbe, J., and van der Donk,W.A. (1998) Protein radicals in enzyme catalysis. Chem. Rev. 98, 705-762.
14. Uhlin, U., and Eklund, H. (1994) Structure of ribonucleotide reductase protein R1. Nature 370, 533-539.
15. Seyedsayamdost, M. R., Xie, J., Chan, C. T., Schultz, P. G., and Stubbe, J. (2007) Site-specific insertion of 3-aminotyrosine into subunit R2 of E. coli ribonucleotide reductase: Direct evidence for involvement of Y730 and Y731 in radical propagation. J. Am. Chem. Soc. 129, 15060-15071.
16. 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.
17. Cordes, M., Kottgen, A., Jasper, C., Jacques, O., Boudebous, H., and Giese, B. (2008) Influence of amino acid side chains on long-distance electron transfer in peptides: Electron hopping via "stepping stones". Angew. Chem., Int. Ed. 47, 3461-3463.
18. Bhattacharjee, S., Deterding, L. J., Jiang, J., Bonini, M. G., Tomer, K. B., Ramirez, D. C., and Mason, R. P. (2007) Electron transfer between a tyrosyl radical and a cysteine residue in hemoproteins: Spin trapping analysis. J. Am. Chem. Soc. 129, 13493-13501.
19. Lendzian, F. (2005) Structure and interactions of amino acid radicals in class I ribonucleotide reductase studied by ENDOR and high-field EPR spectroscopy. Biochim. Biophys. Acta 1707, 67-90.
20. Sahlin, M., Lassmann, G., Pötsch, S., Slaby, A., Sjöberg, B. M., and Gräslund, A. (1994) Tryptophan radicals formed by iron/oxygen reaction with Escherichia coli ribonucleotide reductase protein R2 mutant Y122F. J. Biol. Chem. 269, 11699-11702.
21. Sahlin, M., Lassmann, G., Pötsch, S., Sjöberg, B. M., and Gräslund, A. (1995) Transient free radicals in iron/oxygen reconstitution of mutant protein R2 Y122F. Possible participants in electron transfer chains in ribonucleotide reductase. J. Biol. Chem. 270, 12361-12372.
22. Choudhury, K., Sundaramoorthy, M., Hickman, A., Yonetani, T., Woehl, E., Dunn,M. F., and Poulos, T. L. (1994) Role of the proximal ligand in peroxidase catalysis. Crystallographic, kinetic, and spectral studies of cytochrome c peroxidase proximal ligand mutants. J. Biol. Chem. 269, 20239-20249.
23. Karthein, R., Dietz, R., Nastainczyk, W., and Ruf, H. H. (1988) Higher oxidation states of prostaglandin H synthase. EPR study of a transient tyrosyl radical in the enzyme during the peroxidase reaction. Eur. J. Biochem. 171, 313-320.
24. Sancar, A. (2003) Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. Chem. Rev. 103, 2203-2237.
25. Aubert, C., Vos, M. H., Mathis, P., Eker, A. P., and Brettel, K. (2000) Intraprotein radical transfer during photoactivation of DNA photolyase. Nature 405, 586-590.
26. Byrdin, M., Eker, A. P., Vos, M. H., and Brettel, K. (2003) Dissection of the triple tryptophan electron transfer chain in Escherichia coli DNA photolyase: Trp382 is the primary donor in photoactivation. Proc. Natl. Acad. Sci. U.S.A. 100, 8676-8681.
27. Lukacs, A., Eker, A. P., Byrdin,M., Villette, S., Pan, J., Brettel,K., and Vos, M. H. (2006) Role of the middle residue in the triple tryptophan electron transfer chain of DNAphotolyase: ultrafast spectroscopy of a Trp f Phe mutant. J. Phys. Chem. B 110, 15654-15658.
28. Lukacs, A., Eker, A. P., Byrdin, M., Brettel, K., and Vos, M. H. (2008) Electron hopping through the 15 A° triple tryptophan molecular wire in DNA photolyase occurs within 30 ps. J. Am. Chem. Soc. 130, 14394-14395.
29. 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.
30. 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.
31. 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.
32. 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.
33. 356-R2s (n = 2, 3, 4)in Escherichia coli ribonucleotide reductase: Evidence that Y356 is a redox-active amino acid along the radical propagation pathway. J. Am. Chem. Soc. 128, 1562-1568.
34. 356 with 3,4-dihydroxyphenylalanine in the β2 subunit of E. coli ribonucleotide reductase. J. Am. Chem. Soc. 128, 2522-2523.
35. 2Y-α2s: Distance measurements between residues involved in the radical propagation pathway of E. coli ribonucleotide reductase. J. Am. Chem. Soc. 129, 15748-15749.
36. Seyedsayamdost, M. R., and Stubbe, J. (2007) Forward and reverse electron transfer with the Y356DOPA-β2 heterodimer of E. coli ribonucleotide reductase. J. Am. Chem. Soc. 129, 2226-2227.
37. Seyedsayamdost, M. R. (2007) Investigation of the mechanism of radical propagation in E. coli ribonucleotide reductase by site-specific incorporation of unnatural amino acids. Ph.D. Thesis, Massachusetts Institute of Technology, Cambridge, MA.
38. Ge, J., Yu, G., Ator, M. A., and Stubbe, J. (2003) Pre-steady-state and steady-state kinetic analysis of E. coli class I ribonucleotide reductase. Biochemistry 42, 10071-10083.
39. Reece, S. Y., Seyedsayamdost, M. R., Stubbe, J., and Nocera, D. G. (2007) Photoactive peptides for light-initiated tyrosyl radical generation and transport into ribonucleotide reductase. J. Am. Chem. Soc. 129, 8500-8509.
40. Reece, S. Y., Seyedsayamdost, M. R., Stubbe, J., and Nocera, D. G. (2007) Direct observation of a transient tyrosine radical competent for initiating turnover in a photochemical ribonucleotide reductase. J. Am. Chem. Soc. 129, 13828-13830.
41. Yee, C. S., Seyedsayamdost, M. R., Chang, M. C. Y., Nocera, D. G., and Stubbe, J. (2003) Generation of the R2 subunit of ribonucleotide reductase by intein chemistry: Insertion of 3-nitrotyrosine at residue 356 as a probe of the radical initiation process. Biochemistry 42, 14541-14552.
42. Climent, I., Sjöberg, B. M., and Huang, C. Y. (1991) Carboxylterminal peptides as probes for Escherichia coli ribonucleotide reductase subunit interaction: Kinetic analysis of inhibition studies. Biochemistry 30, 5164-5171.
43. Palmer, G. (1967) Electron paramagnetic resonance. Methods Enzymol. 10, 595-610.
44. Nordlund, P., Sjöberg, B. M., and Eklund, H. (1990) Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345, 593-598.