Chapter 3 Replacement of Y730 and Y731 in the α2 Subunit of Escherichia coli Ribonucleotide Reductase with 3-Aminotyrosine using an Evolved Suppressor tRNA/tRNA-Synthetase Pair

Methods in Enzymology

Volumn 462, Issue , 2009, Pages 45-76

  Seyedsayamdost, Mohammad R ^a   Stubbe, JoAnne ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOTYROSINE; ADENOSINE DIPHOSPHATE; AMINO ACID; AMINO ACID TRANSFER RNA LIGASE; RIBONUCLEOTIDE REDUCTASE; TRANSFER RNA; TYROSINE DERIVATIVE; UNCLASSIFIED DRUG; 3-AMINOTYROSINE; DRUG DERIVATIVE; ESCHERICHIA COLI PROTEIN; MUTANT PROTEIN; TYROSINE; TYROSINE TRANSFER RNA; TYROSINE TRANSFER RNA LIGASE;

AMINO ACID SUBSTITUTION; AMINO ACID TRANSPORT; CATALYSIS; ELECTRON SPIN RESONANCE; ENZYME MECHANISM; ENZYME SUBUNIT; ESCHERICHIA COLI; FREEZING; KINETICS; MOLECULAR EVOLUTION; MOLECULAR MODEL; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVIEW; TOXICITY; ULTRAVIOLET SPECTROSCOPY; AMINO ACID SEQUENCE; ARTICLE; BIOCATALYSIS; BIOSYNTHESIS; CHEMISTRY; DIRECTED MOLECULAR EVOLUTION; DRUG ANTAGONISM; ENZYME ACTIVE SITE; METABOLISM; OXIDATION REDUCTION REACTION;

ESCHERICHIA COLI;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BIOCATALYSIS; CATALYTIC DOMAIN; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTANT PROTEINS; OXIDATION-REDUCTION; RIBONUCLEOTIDE REDUCTASES; RNA, TRANSFER, TYR; TYROSINE; TYROSINE-TRNA LIGASE;

EID: 67650756179     PISSN: 00766879     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0076-6879(09)62003-6     Document Type: Review

References (91)

1. Alfonta L., Zhang Z., Uryu S., Loo J.A., and Schultz P.G. Site-specific incorporation of a redox-active amino acid into proteins. J. Am. Chem. Soc. 125 (2003) 14662-14663
2. Amann E., Ochs B., and Abel K.J. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69 (1988) 301-315
3. Atkin C.L., Thelander L., Reichard P., and Lang G. Iron and free radical in ribonucleotide reductase. Exchange of iron and Mossbauer spectroscopy of the protein B2 subunit of the Escherichia coli enzyme. J. Biol. Chem. 248 (1973) 7464-7472
4. Ballou D.P., and Palmer G. Practical rapid quenching instrument for the study of reaction mechanisms by electron paramagnetic resonance spectroscopy. Anal. Chem. 46 (1974) 1248-1253
5. Bennati M., Weber A., Antonic J., Perlstein D.L., Robblee J., and Stubbe J. Pulsed ELDOR spectroscopy measures the distance between the two tyrosyl radicals in the R2 subunit of the E. coli ribonucleotide reductase. J. Am. Chem. Soc. 125 (2003) 14988-14989
6. Berglund O., and Eckstein F. Synthesis of ATP- and dATP-substituted sepharoses and their application in the purification of phage-T4-induced ribonucleotide reductase. Eur. J. Biochem. 28 (1972) 492-496
7. Berglund O., and Eckstein F. ATP-and dATP-substituted agaroses and the purification of ribonucleotide reductases. Methods Enzymol. 34 (1974) 253-261
8. Bollinger Jr. J.M., Tong W.H., Ravi N., Huynh B.H., Edmondson D.E., and Stubbe J. Use of rapid kinetics methods to study the assembly of the diferric-tyrosyl radical cofactor of E. coli ribonucleotide reductase. Methods Enzymol. 258 (1995) 278-303
9. Chin J.W., Martin A.B., King D.S., Wang L., and Schultz P.G. Addition of a photocrosslinking amino acid to the genetic code of Escherichia coli. Proc. Natl. Acad. Sci. USA 99 (2002) 11020-11024
10. Chivers P.T., Prehoda K.E., Volkman B.F., Kim B.M., Markley J.L., and Raines R.T. Microscopic pKa values of Escherichia coli thioredoxin. Biochemistry 36 (1997) 14985-14991
11. Climent I., Sjöberg B.-M., and Huang C.Y. 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 (1992) 4801-4807
12. Cotton G.J., Ayers B., Xu R., and Muir T.W. Insertion of a Synthetic Peptide into a Recombinant Protein Framework: A Protein Biosensor. J. Am. Chem. Soc. 121 (1999) 1100-1101
13. Craw M., Chedekel M.R., Truscott T.G., and Land E.J. The photochemical interaction between the triplet state of 8-methoxypsoralen and the melanin precursor L-3,4 dihydroxyphenylalanine. Photochem. Photobiol. 39 (1984) 155-159
14. Cukier R.I., and Nocera D.G. Proton-coupled electron transfer. Annu. Rev. Phys. Chem. 49 (1998) 337-369
15. Dawson P.E., and Kent S.B. Synthesis of native proteins by chemical ligation. Annu. Rev. Biochem. 69 (2000) 923-960
16. DeFelippis M.R., Murthy C.P., Broitman F., Weinraub D., Faraggi M., and Klapper M.H. Electrochemical properties of tyrosine phenoxy and tryptophan indolyl radicals in peptides and amino acid analogs. J. Phys. Chem. 95 (1991) 3416-3419
17. Ehrenberg A., and Reichard P. Electron spin resonance of the iron-containing protein B2 from ribonucleotide reductase. J. Biol. Chem. 247 (1972) 3485-3488
18. Ekberg M., Pötsch S., Sandin E., Thunnissen M., Nordlund P., Sahlin M., and Sjöberg B.-M. 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 (1998) 21003-21008
19. Ekberg M., Sahlin M., Eriksson M., and Sjöberg B.-M. Two conserved tyrosine residues in protein R1 participate in an intermolecular electron transfer in ribonucleotide reductase. J. Biol. Chem. 271 (1996) 20655-20659
20. Eklund H., Uhlin U., Färnegårdh M., Logan D.T., and Nordlund P. Structure and function of the radical enzyme ribonucleotide reductase. Prog. Biophys. Mol. Biol. 77 (2001) 177-268
21. Farrell I.S., Toroney R., Hazen J.L., Mehl R.A., and Chin J.W. Photo-cross-linking interacting proteins with a genetically encoded benzophenone. Nat. Methods 2 (2005) 377-384
22. Fritscher J., Artin E., Wnuk S., Bar G., Robblee J.H., Kacprzak S., Kaupp M., Griffin R.G., Bennati M., and Stubbe J. 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. Chem. Soc. 127 (2005) 7729-7738
23. Ge J., Yu G., Ator M.A., and Stubbe J. Pre-steady-state and steady-state kinetic analysis of E. coli class I ribonucleotide reductase. Biochemistry 42 (2003) 10071-10083
24. Giriat I., and Muir T.W. Protein semi-synthesis in living cells. J. Am. Chem. Soc. 125 (2003) 7180-7181
25. Gräslund A., Sahlin M., and Sjöberg B.-M. The tyrosine free radical in ribonucleotide reductase. Environ. Health Perspect. 64 (1985) 139-149
26. Gray H.B., and Winkler J.R. Electron transfer in proteins. Annu. Rev. Biochem. 65 (1996) 537-561
27. Hobbs J.B., and Eckstein F. A general method for the synthesis of 2′-azido-2′-deoxy- and 2′-amino-2′-deoxyribofuranosyl purines. J. Org. Chem. 42 (1977) 714-719
28. Hooker J.M., Kovacs E.W., and Francis M.B. Interior surface modification of bacteriophage MS2. J. Am. Chem. Soc. 126 (2004) 3718-3719
29. Jackson J.C., Duffy S.P., Hess K.R., and Mehl R.A. Improving nature's enzyme active site with genetically encoded unnatural amino acids. J. Am. Chem. Soc. 128 (2006) 11124-11127
30. Jordan A., and Reichard P. Ribonucleotide reductases. Annu. Rev. Biochem. 67 (1998) 71-98
31. Jovanovic S.J.S., Tosic M., Marjanovic B., and Simic M.G. Flavonoids as antioxidants. J. Am. Chem. Soc. 116 (1994) 4846-4851
32. Kiga D., Sakamoto K., Kodama K., Kigawa T., Matsuda T., Yabuki T., Shirouzu M., Harada Y., Nakayama H., Takio K., Hasegawa Y., Endo Y., et al. An engineered Escherichia coli tyrosyl-tRNA synthetase for site-specific incorporation of an unnatural amino acid into proteins in eukaryotic translation and its application in a wheat germ cell-free system. Proc. Natl. Acad. Sci. USA 99 (2002) 9715-9720
33. Kobayashi T., Nureki O., Ishitani R., Yaremchuk A., Tukalo M., Cusack S., Sakamoto K., and Yokoyama S. Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion. Nat. Struct. Biol. 10 (2003) 425-432
34. Kobayashi T., Takimura T., Sekine R., Kelly V.P., Kamata K., Sakamoto K., Nishimura S., and Yokoyama S. Structural snapshots of the KMSKS loop rearrangement for amino acid activation by bacterial tyrosyl-tRNA synthetase. J. Mol. Biol. 346 (2005) 105-117
35. Kovacs E.W., Hooker J.M., Romanini D.W., Holder P.G., Berry K.E., and Francis M.B. Dual-surface-modified bacteriophage MS2 as an ideal scaffold for a viral capsid-based drug delivery system. Bioconjug. Chem. 18 (2007) 1140-1147
36. Licht S., and Stubbe J. Mechanistic investigations of ribonucleotide reductases. In: Barton S.D., Nakanishi K., Meth-Cohn O., and Poulter C.D. (Eds). Comprehensive Natural Products Chemistry. (1999), Elsevier Science, New York 163-203
37. Mao S.S., Johnston M.I., Bollinger Jr. J.M., and Stubbe J. Mechanism-based inhibition of a mutant Escherichia coli ribonucleotide reductase (cysteine-225→serine) by its substrate CDP. Proc. Natl. Acad. Sci. USA 86 (1989) 1485-1489
38. Marcus R.A., and Sutin N. Electron transfer in chemistry and biology. Biochim. Biophys. Acta 811 (1985) 265-322
39. Mootz H.D., Blum E.S., Tyszkiewicz A.B., and Muir T.W. Conditional protein splicing: A new tool to control protein structure and function in vitro and in vivo. J. Am. Chem. Soc. 125 (2003) 10561-10569
40. Moser C.C., Keske J.M., Warncke K., Farid R.S., and Dutton P.L. Nature of biological electron transfer. Nature 355 (1992) 796-802
41. Muir T.W. Semisynthesis of proteins by expressed protein ligation. Annu. Rev. Biochem. 72 (2003) 249-289
42. Muralidharan V., and Muir T.W. Protein ligation: An enabling technology for the biophysical analysis of proteins. Nat. Methods 3 (2006) 429-438
43. Neumann H., Hazen J.L., Weinstein J., Mehl R.A., and Chin J.W. Genetically encoding protein oxidative damage. J. Am. Chem. Soc. 130 (2008) 4028-4033
44. Nilsson B., Moks T., Jansson B., Abrahmsen L., Elmblad A., Holmgren E., Henrichson C., Jones T.A., and Uhlen M. A synthetic IgG-binding domain based on staphylococcal protein A. Protein Eng. 1 (1987) 107-113
45. Nordlund P., Sjöberg B.-M., and Eklund H. Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345 (1990) 593-598
46. Nyholm S., Thelander L., and Gräslund A. Reduction and loss of the iron center in the reaction of the small subunit of mouse ribonucleotide reductase with hydroxyurea. Biochemistry 32 (1993) 11569-11574
47. Page C.C., Moser C.C., Chen X., and Dutton P.L. Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402 (1999) 47-52
48. Page C.C., Moser C.C., and Dutton P.L. Mechanism for electron transfer within and between proteins. Curr. Opin. Chem. Biol. 7 (2003) 551-556
49. Palmer G. Electron paramagnetic resonance. Methods Enzymol. 10 (1967) 595-610
50. Pellois J.P., and Muir T.W. Semisynthetic proteins in mechanistic studies: Using chemistry to go where nature can't. Curr. Opin. Chem. Biol. 10 (2006) 487-491
51. Perler F.B. Protein splicing mechanisms and applications. IUBMB Life 57 (2005) 469-476
52. Reece S.Y., Hodgkiss J.M., Stubbe J., and Nocera D.G. Proton-coupled electron transfer: The mechanistic underpinning for radical transport and catalysis in biology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361 (2006) 1351-1364
53. Reichard P., and Ehrenberg A. Ribonucleotide reductase: A radical enzyme. Science 221 (1983) 514-519
54. Robins M.J., Hawrelak S.D., Hernandez A.E., and Wnuk S.F. Nucleic acid related compounds. LXXXI. Efficient general synthesis of purine (amino, azido, and triflate)-sugar nucleosides. Nucleosides Nucleotides 11 (1992) 821-834
55. Russel M., and Model P. Direct cloning of the trxB gene that encodes thioredoxin reductase. J. Bacteriol. 163 (1985) 238-242
56. Ryu Y., and Schultz P.G. Efficient incorporation of unnatural amino acids into proteins in Escherichia coli. Nat. Methods 3 (2006) 263-265
57. Salowe S., Bollinger Jr. J.M., Ator M., and Stubbe J. Alternative model for mechanism-based inhibition of Escherichia coli ribonucleotide reductase by 2′-azido-2′-deoxyuridine 5′-diphosphate. Biochemistry 32 (1993) 12749-12760
58. Salowe S.P., Ator M.A., and Stubbe J. Products of the inactivation of ribonucleoside diphosphate reductase from Escherichia coli with 2′-azido-2′-deoxyuridine 5′-diphosphate. Biochemistry 26 (1987) 3408-3416
59. Salowe S.P., and Stubbe J. Cloning, overproduction, and purification of the B2 subunit of ribonucleoside-diphosphate reductase. J. Bacteriol. 165 (1986) 363-366
60. Santoro S.W., Wang L., Herberich B., King D.S., and Schultz P.G. An efficient system for the evolution of aminoacyl-tRNA synthetase specificity. Nat. Biotechnol. 20 (2002) 1044-1048
61. Seagle R.L., and Cowgill R.W. Fluorescence and the structure of proteins. XXI. Fluorescence of aminotyrosyl residues in peptides and helical proteins. Biochim. Biophys. Acta 439 (1976) 461-469
62. 2Y-α2s: Distance measurements between residues involved in the radical propagation pathway of E. coli ribonucleotide reductase. J. Am. Chem. Soc. 129 (2007) 15748-15749
63. Seyedsayamdost M.R., Reece S.Y., Nocera D.G., and Stubbe J. Mono-, di-, tri-, and tetra-substituted fluorotyrosines: New probes for enzymes that use tyrosyl radicals in catalysis. J. Am. Chem. Soc. 128 (2006) 1569-1579
64. 356 with 3,4-dihydroxyphenylalanine in the β2 subunit of E. coli ribonucleotide reductase. J. Am. Chem. Soc. 128 (2006) 2522-2523
65. 731 in radical propagation. J. Am. Chem. Soc. 129 (2007) 15060-15071
66. 356 is a redox-active amino acid along the radical propagation pathway. J. Am. Chem. Soc. 128 (2006) 1562-1568
67. Seyedsayamdost M.R., Yee C.S., and Stubbe J. Site-specific incorporation of fluorotyrosines into the R2 subunit of E. coli ribonucleotide reductase by expressed protein ligation. Nat. Protoc. 2 (2007) 1225-1235
68. Sjöberg B.-M., Gräslund A., and Eckstein F. A substrate radical intermediate in the reaction between ribonucleotide reductase from Escherichia coli and 2′-azido-2′-deoxynucleoside diphosphates. J. Biol. Chem. 258 (1983) 8060-8067
69. Sjöberg B.-M., Reichard P., Gräslund A., and Ehrenberg A. The tyrosine free radical in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 253 (1978) 6863-6865
70. Steeper J.R., and Steuart C.D. A rapid assay for CDP reductase activity in mammalian cell extracts. Anal. Biochem. 34 (1970) 123-130
71. Stubbe J. Ribonucleotide reductases: Amazing and confusing. J. Biol. Chem. 265 (1990) 5329-5332
72. Stubbe J. Ribonucleotide reductases in the twenty-first century. Proc. Natl. Acad. Sci. USA 95 (1998) 2723-2724
73. Stubbe J., Nocera D.G., Yee C.S., and Chang M.C.Y. Radical initiation in the class I ribonucleotide reductase: long-range proton-coupled electron transfer?. Chem. Rev. 103 (2003) 2167-2201
74. Stubbe J., and Riggs-Gelasco P. Harnessing free radicals: Formation and function of the tyrosyl radical in ribonucleotide reductase. Trends Biochem. Sci. 23 (1998) 438-443
75. Stubbe J., and van der Donk W.A. Protein radicals in enzyme catalysis. Chem. Rev. 98 (1998) 705-762
76. Thelander L., Larsson B., Hobbs J., and Eckstein F. Active site of ribonucleoside diphosphate reductase from Escherichia coli: Inactivation of the enzyme by 2′-substituted ribonucleoside diphosphates. J. Biol. Chem. 251 (1976) 1398-1405
77. Turner J.M., Graziano J., Spraggon G., and Schultz P.G. Structural plasticity of an aminoacyl-tRNA synthetase active site. Proc. Natl. Acad. Sci. USA 103 (2006) 6483-6488
78. Uhlin U., and Eklund H. Structure of ribonucleotide reductase protein R1. Nature 370 (1994) 533-539
79. van der Donk W.A., Stubbe J., Gerfen G.G., Bellew B.F., and Griffin R.G. EPR investigations of the inactivation of E. coli ribonucleotide reductase with 2′-azido-2′-deoxyuridine 5′-diphosphate: Evidence for the involvement of the thiyl radical of C225-R1. J. Am. Chem. Soc. 117 (1995) 8909-8916
80. Wang L., Brock A., Herberich B., and Schultz P.G. Expanding the genetic code of Escherichia coli. Science 292 (2001) 498-500
81. Wang L., and Schultz P.G. A general approach for the generation of orthogonal tRNAs. Chem. Biol. 8 (2001) 883-890
82. Wang L., and Schultz P.G. Expanding the genetic code. Angew. Chem. Int. Ed. Engl. 44 (2004) 34-66
83. Wang L., Xie J., and Schultz P.G. Expanding the genetic code. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 225-249
84. Wang L., Zhang Z., Brock A., and Schultz P.G. Addition of the keto functional group to the genetic code of Escherichia coli. Proc. Natl. Acad. Sci. USA 100 (2003) 56-61
85. Xie J., and Schultz P.G. An expanding genetic code. Methods 36 (2005) 227-238
86. Xie J., and Schultz P.G. A chemical toolkit for proteins: An expanded genetic code. Nat. Rev. Mol. Cell Biol. 7 (2006) 775-782
87. Yee C.S., Chang M.C.Y., Ge J., Nocera D.G., and Stubbe J. 2,3-Difluorotyrosine at position 356 of ribonucleotide reductase R2: A probe of long-range proton-coupled electron transfer. J. Am. Chem. Soc. 125 (2003) 10506-10507
88. Yee C.S., Seyedsayamdost M.R., Chang M.C.Y., Nocera D.G., and Stubbe J. 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 (2003) 14541-14552
89. Zhang Y., Wang L., Schultz P.G., and Wilson I.A. Crystal structures of apo wild-type M. jannaschii tyrosyl-tRNA synthetase (TyrRS) and an engineered TyrRS specific for O-methyl-L-tyrosine. Protein Sci. 14 (2005) 1340-1349
90. Zhang Z., Smith B.A., Wang L., Brock A., Cho C., and Schultz P.G. A new strategy for the site-specific modification of proteins in vivo. Biochemistry 42 (2003) 6735-6746
91. Zhang Z., Wang L., Brock A., and Schultz P.G. The selective incorporation of alkenes into proteins in Escherichia coli. Angew. Chem. Int. Ed. Engl. 41 (2002) 2840-2842