Generation of a stable, aminotyrosyl radical-induced α2β2 complex of Escherichia coli class Ia ribonucleotide reductase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 10, 2013, Pages 3835-3840

  Minnihan, Ellen C ^a   Ando, Nozomi ^a,b   Brignole, Edward J ^a,b   Olshansky, Lisa ^a   Chittuluru, Johnathan ^c   Asturias, Francisco J ^c   Drennan, Catherine L ^a,b   Nocera, Daniel G ^a   Stubbe, JoAnne ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Conformational equilibria; Radical transfer; Unnatural amino acid

Indexed keywords

AMINO ACID; CYSTEINE; RIBONUCLEOTIDE REDUCTASE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; FLUORESCENCE; KINETICS; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RADIATION SCATTERING; SIGNAL TRANSDUCTION;

CATALYTIC DOMAIN; ELECTRON TRANSPORT; ENZYME STABILITY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, QUATERNARY; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; RIBONUCLEOTIDE REDUCTASES; SCATTERING, SMALL ANGLE; SPECTROMETRY, FLUORESCENCE; X-RAY DIFFRACTION;

EID: 84874632835     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220691110     Document Type: Article

References (37)

1. Stubbe J, van Der Donk WA (1998) Protein radicals in enzyme catalysis. Chem Rev 98(2):705-762.
2. Nordlund P, Reichard P (2006) Ribonucleotide reductases. Annu Rev Biochem 75: 681-706.
3. Brown NC, Reichard P (1969) Ribonucleoside diphosphate reductase. Formation of active and inactive complexes of proteins B1 and B2. J Mol Biol 46(1):25-38.
4. Thelander L (1973) Physicochemical characterization of ribonucleoside diphosphate reductase from Escherichia coli. J Biol Chem 248(13):4591-4601.
5. Brown NC, Reichard P (1969) Role of effector binding in allosteric control of ribonucleoside diphosphate reductase. J Mol Biol 46(1):39-55.
6. Nordlund P, Sjöberg BM, Eklund H (1990) Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345(6276):593-598.
7. Uhlin U, Eklund H (1994) Structure of ribonucleotide reductase protein R1. Nature 370(6490):533-539.
8. Climent I, Sjöberg BM, Huang CY (1991) Carboxyl-terminal peptides as probes for Escherichia coli ribonucleotide reductase subunit interaction: Kinetic analysis of inhibition studies. Biochemistry 30(21):5164-5171.
9. Seyedsayamdost MR, Xie J, Chan CT, Schultz PG, Stubbe J (2007) Site-specific insertion of 3-aminotyrosine into subunit α2 of E. coli ribonucleotide reductase: Direct evidence for involvement of Y730 and Y731 in radical propagation. J Am Chem Soc 129(48): 15060-15071.
10. Minnihan EC, Seyedsayamdost MR, Uhlin U, Stubbe J (2011) Kinetics of radical intermediate formation and deoxynucleotide production in 3-aminotyrosinesubstituted Escherichia coli ribonucleotide reductases. J Am Chem Soc 133(24): 9430-9440.
11. Ando N, et al. (2011) Structural interconversions modulate activity of Escherichia coli ribonucleotide reductase. Proc Natl Acad Sci USA 108(52):21046-21051.
12. Stubbe J, Nocera DG, Yee CS, Chang MCY (2003) Radical initiation in the class I ribonucleotide reductase: Long-range proton-coupled electron transfer? Chem Rev 103(6):2167-2201.
13. Reece SY, Hodgkiss JM, Stubbe J, Nocera DG (2006) Proton-coupled electron transfer: The mechanistic underpinning for radical transport and catalysis in biology. Philos Trans R Soc Lond B Biol Sci 361(1472):1351-1364.
14. Climent I, Sjöberg BM, Huang CY (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(20):4801-4807.
15. Ekberg M, Sahlin M, Eriksson M, Sjöberg BM (1996) Two conserved tyrosine residues in protein R1 participate in an intermolecular electron transfer in ribonucleotide reductase. J Biol Chem 271(34):20655-20659.
16. Seyedsayamdost MR, Chan CT, Mugnaini V, Stubbe J, Bennati M (2007) PELDOR spectroscopy with DOPA-β2 and NH2Y-α2s: Distance measurements between residues involved in the radical propagation pathway of E. coli ribonucleotide reductase. J Am Chem Soc 129(51):15748-15749.
17. Rofougaran R, Crona M, Vodnala M, Sjöberg BM, Hofer A (2008) Oligomerization status directs overall activity regulation of the Escherichia coli class Ia ribonucleotide reductase. J Biol Chem 283(51):35310-35318.
18. Zimanyi CM, et al. (2012) Tangled up in knots: Structures of inactivated forms of E. coli class Ia ribonucleotide reductase. Structure 20(8):1374-1383.
19. Holder PG, Pizano AA, Anderson BL, Stubbe J, Nocera DG (2012) Deciphering radical transport in the large subunit of class I ribonucleotide reductase. J Am Chem Soc 134(2):1172-1180.
20. Seyedsayamdost MR (2007) Investigation of the mechanism of radical propagation in E. coli ribonucleotide reductase by site-specific incorporation of unnatural amino acids. PhD thesis (Massachusetts Institute of Technology, Cambridge, MA).
21. Minnihan EC, Seyedsayamdost MR, Stubbe J (2009) Use of 3-aminotyrosine to examine the pathway dependence of radical propagation in Escherichia coli ribonucleotide reductase. Biochemistry 48(51):12125-12132.
22. Hassan AQ, Wang Y, Plate L, Stubbe J (2008) Methodology to probe subunit interactions in ribonucleotide reductases. Biochemistry 47(49):13046-13055.
23. Eriksson M, et al. (1997) Binding of allosteric effectors to ribonucleotide reductase protein R1: Reduction of active-site cysteines promotes substrate binding. Structure 5(8):1077-1092.
24. Radermacher M, Wagenknecht T, Verschoor A, Frank J (1987) Three-dimensional reconstruction from a single-exposure, random conical tilt series applied to the 50S ribosomal subunit of Escherichia coli. J Microsc 146(Pt 2):113-136.
25. Konarev PV, Petoukhov MV, Volkov VV, Svergun DI (2006) ATSAS 2.1, a program package for small-angle scattering data analysis. J Appl Cryst 39(Pt 2):277-286.
26. Mertens HD, Svergun DI (2010) Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J Struct Biol 172(1):128-141.
27. Ge J, Yu G, Ator MA, Stubbe J (2003) Pre-steady-state and steady-state kinetic analysis of E. coli class I ribonucleotide reductase. Biochemistry 42(34):10071-10083.
28. Yokoyama K, Uhlin U, Stubbe J (2010) A hot oxidant, 3-NO2Y122 radical, unmasks conformational gating in ribonucleotide reductase. J Am Chem Soc 132(43): 15368-15379.
29. Minnihan EC, Young DD, Schultz PG, Stubbe J (2011) Incorporation of fluorotyrosines into ribonucleotide reductase using an evolved, polyspecific aminoacyl-tRNA synthetase. J Am Chem Soc 133(40):15942-15945.
30. Fritscher J, et al. (2005) Structure of the nitrogen-centered radical formed during inactivation of E. coli ribonucleotide reductase by 2′-azido-2′-deoxyuridine-5′-diphosphate: Trapping of the 3′-ketonucleotide. J Am ChemSoc 127(21):7729-7738.
31. Seyedsayamdost MR, Stubbe J (2007) Forward and reverse electron transfer with the Y356DOPA-β2 heterodimer of E. coli ribonucleotide reductase. J Am Chem Soc 129(8): 2226-2227.
32. Reece SY, Lutterman DA, SeyedsayamdostMR, Stubbe J, Nocera DG (2009) Re(bpy)(CO)3CN as a probe of conformational flexibility in a photochemical ribonucleotide reductase. Biochemistry 48(25):5832-5838.
33. Suloway C, et al. (2005) Automated molecular microscopy: The new Leginon system. J Struct Biol 151(1):41-60.
34. Frank J, et al. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116(1):190-199.
35. Yang Z, Fang J, Chittuluru J, Asturias FJ, Penczek PA (2012) Iterative stable alignment and clustering of 2D transmission electron microscope images. Structure 20(2): 237-247.
36. Nielsen SS, Møller M, Gillilan RE (2012) High-throughput biological small-angle X-ray scattering with a robotically loaded capillary cell. J Appl Cryst 45(Pt 2): 213-223.
37. Ando N, Chenevier P, Novak M, Tate MW, Gruner SM (2008) High hydrostatic pressure small-angle X-ray scattering cell for protein solution studies featuring diamond windows and disposable sample cells. J Appl Cryst 41(Pt 1):167-175.