Electron paramagnetic resonance and nuclear magnetic resonance studies of class I ribonucleotide reductase

Annual Review of Biophysics and Biomolecular Structure

Volumn 25, Issue , 1996, Pages 259-286

  Graslund A ^a   Sahlin, M ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

diiron oxygen protein; ribonucleotide reductase; tyrosyl radical

Indexed keywords

BACTERIAL PROTEIN; CYSTEINE; FREE RADICAL; IRON; RIBONUCLEOTIDE REDUCTASE; TRYPTOPHAN; TYROSINE;

CARBOXY TERMINAL SEQUENCE; COMPETITIVE INHIBITION; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ESCHERICHIA COLI; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REVIEW;

EID: 0030000063     PISSN: 10568700     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.bb.25.060196.001355     Document Type: Review

References (71)

1. Åberg A. 1993. Ribonucleotide reductase from Escherichia coli: Structural aspects of protein function. PhD thesis. Stockholm Univ. 59 pp.
2. Åberg A, Ormö M, Nordlund P, 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 32:9845-50
3. Allard P, Kuprin S, Ehrenberg A. 1994. Conformation of dCDP bound to protein R1 of Escherichia coli ribonucleotide reductase. J. Magn. Reson. B103:242-46
4. 1H NMR. Eur. J. Biochem. 208:635-42
5. Allard P, Barra AL, Andersson KK, Schmidt PP, Atta M, Gräslund A. 1996. Characterization of a new tyrosyl free radical in Salmonella typhimurium ribonucleotide reductase with EPR at 9.45 and 245 GHz. J. Am. Chem. Soc. In press
6. Andersson KK, Gräslund A. 1995. Diiron-oxygen proteins. Adv. Inorg. Chem. 43:359-408
7. Atta M, Andersson KK, Ingemarsson R, Thelander L, Gräslund A. 1994. EPR studies of mixed-valent [FeII-FeIII] clusters formed in the R2 subunit of ribonucleotide reductase from mouse or herpes simplex virus: mild chemical reduction of the diferric centers. J. Am. Chem. Soc. 116:6429-30
8. Atta M, Nordlund P, Åberg A, Eklund H, Fontecave M. 1992. Substitution of manganese for iron in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 267:20682-88
9. Atta M, Debaecker N, Andersson KK, Latour JM, Thelander L, Gräslund A. 1995. EPR and multi-field magnetization of reduced forms of the binuclear iron center in ribonucleotide reductase from mouse. J. Biol. Inorg. Chem. In press
10. Behravan G, Sen S, Rova U, Thelander L, Eckstein F, Gräslund A. 1995. Formation of a free radical of the sulfenylimine type in the mouse ribonucleotide reductase reaction with 2′-azido-2′deoxycytidine 5′diphosphate. Biochim. Biophys. Acta. 1264: 323-29
11. Bender CJ, Sahlin M, Babcock GT, Barry BA, Chandrashekar TK, et al. 1989. An ENDOR study of the tyrosyl free radical in ribonucleotide reductase from Escherichia coli. J. Am. Chem. Soc. 111:8076-83
12. Bollinger JM Jr, Edmondson DE, Huyhn BH, Filley J, Norton JR, Stubbe J. 1991. Mechanism of assembly of the tyrosyl radical-dinuclear iron cluster cofactor of ribonucleotide reductase. Science 253:292-98
13. 2+ reaction by optical, EPR, and Mössbauer spectroscopies. J. Am. Chem. Soc. 116:8015-23
14. 2+ reaction by optical, EPR, and Mössbauer spectroscopies. J. Am. Chem. Soc. 116:8024-52
15. Bushweller JH, Bartlett PA. 1991. Investigation of an octapeptide inhibitor of Escherichia coli ribonucleotide reductase by transferred nuclear overhauser effect spectroscopy. Biochemistry 30:8144-51
16. Cohen EA, Gaudreau P, Brazeau P, Langelier Y. 1986. Specific inhibition of herpesvirus ribonucleotide reductase by a nonapeptide derived from the carboxy terminus of subunit 2. Nature 321:441-43
17. Davydov R, Kuprin S, Gräslund A, Ehrenberg A. 1994. Electron paramagnetic resonance study of the mixed-valent diiron center in Escherichia coli ribonucleotide reductase produced by reduction of radical-free protein R2 at 77 K. J. Am. Chem. Soc. 116:11120-28
18. 3. J. Am. Chem. Soc. 117: 2778-92
19. van der Donk WA, Stubbe J, Gerfen GJ, Bellew BF, Griffin RG. 1995. 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. 117:8908-16
20. Dutia BM, Frame MC, Subak-Sharpe JH, Clark WN, Marsden HS. 1986. Specific inhibition of herpesvirus ribonucleotide reductase by synthetic peptides. Nature 321:439-41
21. Ehrenberg A, Reichard P. 1972. Electron spin resonance of the iron-containing protein B2 from ribonucleotide reductase. J. Biol. Chem. 247: 3485-88
22. Elgren TE, Hendrich MP, Que L Jr. 1993. Azide binding to the diferrous clusters of the R2 protein of ribonucleotide reductase from Escherichia coli. J. Am. Chem. Soc. 115:9291-92
23. Elgren TE, Ming L-J, Que L Jr. 1994. Spectroscopic studies of Co(II)-reconstituted ribonucleotide reductase R2 from Escherichia coli. Inorg. Chem. 33:891-94
24. Fisher A, Laub PB, Cooperman BS. 1995. NMR structure of an inhibitory R2 C-terminal peptide bound to mouse ribonucleotide reductase R1 subunit. Nature Struct. Biol. 2:951-55
25. Fontecave M, Nordlund P, Eklund H, Reichard P. 1992. The redox centers of ribonucleotide reductase of Excherichia coli. Adv. Enzymol. 65:147-83
26. Galli C, Atta M, Andersson KK, Gräslund A, Brudvig GW. 1995. Variations of the diferric exchange coupling in the R2 subunit of ribonucleotide reductase from four species as determined by saturation-recovery EPR spectroscopy. J. Am. Chem. Soc. 117: 740-46
27. Gerez C, Fontecave M. 1992. Reduction of small subunits of Escherichia coli ribonucleotide reductase by hydrazines and hydroxylamine. Biochemistry 31:780-86
28. Gerfen GJ, Bellew BF, Un S, Bollinger JM Jr, Stubbe J, et al. 1993. High frequency (139.5 GHz) EPR spectroscopy of the tyrosyl radical in Escherichia coli ribonucleotide reductase. J. Am. Chem. Soc. 115: 6420-21
29. Goldberg DP, Koulougliotis D, Brudvig GW, Lippard SJ. 1995. A (μ-Oxo ) bis ( μ -carboxylato)diiron (III) complex with a tethered phenoxyl radical as a model for the active site of the protein R2 of ribonucleotide reductase. J. Am. Chem. Soc. 117: 3134-44
30. Gräslund A, Sahlin M, Sjöberg B-M. 1985. The tyrosyl free radical in ribonucleotide reductase. Environ. Health Perspect. 64:139-49
31. Hendrich MP, Elgren TE, Que L Jr. 1991. A mixed valence form of the iron cluster in the B2 protein of ribonucleotide reductase from Escherichia coli. Biochem. Biophys. Res. Commun. 176:705-10
32. Henriksen M, Cooperman BS, Salem JS, Li L-S, Rubin H. 1994. The stable tyrosyl radical in mouse ribonucleotide reductase is not essential for enzymatic activity. J. Am. Chem. Soc. 116: 9773-74
33. Hoganson K, Babcock GT. 1992. Protein-tyrosyl radical interactions in photosystem II studied by electron spin resonance and electron nuclear resonance spectroscopy: comparison with ribonucleotide reductase and in vitro tyrosine. Biochemistry 31: 11874-80
34. Houseman ALP, Doan PE, Goodin DB, Hoffman BM. 1993. Comprehensive explanation of the anomalous EPR spectra of wild-type and mutant cytochrome c peroxidase compound ES. Biochemistry 32:4430-43
35. Gunther MR, Kelman DJ, Corbett JT, Mason RP. 1995. Self-peroxidation of metmyoglobin results in formation of an oxygen-reactive tryptophancentered radical. J. Biol. Chem. 270: 16075-81
36. Jordan A, Pontis E, Atta M, Krook M, Gibert I, et al. 1994. A second class I ribonucleotide reductase in Enterobacteriaceae: characterization of the Salmonella typhimurium enzyme. Proc. Natl. Acad. Sci. USA 91:12892-96
37. Kjöller Larsen I, Sjöberg BM, Thelander L. 1982. Characterization of the active site of ribonucleotide reductase of Escherichia coli, bacteriophage T4 and mammalian cells by inhibition studies with hydroxyurea analogues. Eur. J. Biochem. 125:75-81
38. Kurtz DM Jr. 1990. Oxo- and hydroxybridged diiron complexes: a chemical perspective on a biological unit. Chem. Rev. 90:585-606
39. Laplante SR, Aubry N, Liuzzi M, Thelander L, Ingemarson R, Moss N. 1994. The critical C-terminus of the small subunit of the herpes simplex virus ribonucleotide reductase is mobile and conformationally similar to C-terminal peptides. Int. J. Peptide Protein Res. 44:549-55
40. Larsson Å, Sjöberg B-M. 1986. Identification of the stable free radical tyrosine radical in ribonucleotide reductase. EMBO J. 5:2037-40
41. Ling J, Sahlin M, Sjöberg B-M, Loehr TM, Sanders-Loehr J. 1994. Dioxygen is the source of the μ-oxo bridge in iron ribonucleotide reductase. J. Biol. Chem. 269:5595-601
42. Liuzzi M, Déziel R, Moss N, Beaulieu P, Bonneau A-M, et al. 1994. A potent peptido-mimetic inhibitor of HSV ribonucleotide reductase with antiviral activity in vivo. Nature 372:695-98
43. 1H NMR studies of mouse ribonucleotide reductase: The R2 protein carboxyl-terminal tail, essential for subunit interaction, is highly flexible but becomes rigid in the presence of protein R1. Biochemistry 33:2838-42
44. Lycksell P, Sahlin M. 1995. Demonstration of segmental mobility in the functionally essential carboxy terminal part of ribonucleotide reductase from Escherichia coli. FEBS Lett. 368: 441-44
45. Mann GJ, Gräslund A, Ochai E-I, Ingmarson R, Thelander L. 1991. Purification and characterization of recombinant mouse and herpes simplex virus ribonucleotide reductase R2 subunit. Biochemistry 30:1939-47
46. Mao SS, Holler TP, Yu GX, Bollinger JM, Booker S, et al. 1992. A model for the role of multiple cysteine residues involved in ribonucleotide reductase: amazing and still confusing. Biochemistry 31:9733-43
47. Mao SS, Yu GX, Chalfoun D, 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 possesing novel thioredoxin-like activity. Biochemistry 31: 9752-59
48. Nordlund P, Eklund H. 1993. Structure and function of the Escherichia coli ribonucleotide reductase protein R2. J. Mol. Biol. 232:123-64
49. Nordlund P, Sjöberg B-M, Eklund H. 1990. Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345:593-98
50. Nyholm S, Mann GJ, Johansson AG, Bergeron RJ, Gräslund A, Thelander L. 1993. Role of ribonucleotide reductase in inhibition of mammalian cell growth by potent iron chelators. J. Biol. Chem. 268:26200-5
51. Ochai EI, Mann GJ, Gräslund A, Thelander L. 1990. Tyrosyl free radical formation in the small subunit of mouse ribonucleotide reductase. J. Biol. Chem. 265:15758-61
52. Ormö M, de Maré F, Regnström K, Åberg A, Sahlin M, et al. 1992. Engineering of the iron site in ribonucleotide reductase to a selfhydroxylating monooxygenase. J. Biol. Chem. 267: 8711-14
53. Ormö M, Regnström K, Wang Z, Que L Jr, Sahlin M, Sjöberg B-M. 1995. Residues important for radical stability in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 270: 6570-76
54. Paulsen KE, Liu Y, Fox GF, Lipscomb JD, Münck E, Stankovich MT. 1994. Oxidation-reduction potentials of the methane monooxygenase hydroxylase components from Methylosinus trichosporium OB3b. Biochemistry 33: 713-22
55. Rardin LR, William BT, Lippard SJ. 1991. Monodentate carboxylate complexes and the carboxylate shift: implications for polymetalloprotein structure and function. N. J. Chem. 15: 417-30
56. Ravi N, Bollinger JM, Hahn Huynh B, Edmondson DE, 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. 116:8007-14
57. Reem RC, Solomon EI. 1987. Spectroscopic studies of the binuclear ferrous active site of deoxyhemerythrin: coordination number and probable bridging ligands for the native and ligand bound forms. J. Am. Chem. Soc. 109: 1216-26
58. Reichard P. 1993. From RNA to DNA, why so many ribonucleotide reductases? Science 260:1773-77
59. Rova U, Goodtzova K, Ingmarson R, Behravan G, Gräslund A, Thelander L. 1995. Evidence by site-directed mutagenesis supports long-range electron transfer in mouse ribonucleotide reductase. Biochemistry 34:4267-75
60. Roy B, Decout J-L, Béguin C, Fontecave M, Allard P, et al. 1995. NMR studies of binding of 5-FdUDP and dCDP to ribonucleoside-diphosphate reductase from Escherichia coli. Biochim. Biophys. Acta 1247:284-92
61. Sahlin M, Gräslund A, Petersson L, Ehrenberg A, Sjöberg B-M. 1989. Reduced forms of the iron-containing small subunit of ribonucleotide reductase from Escherichia coli. Biochemistry 28:2618-25
62. Sahlin M, Lassmann G, Pötsch S, Sjöberg B-M, Gräslund A. 1995. Transient free radicals in iron/oxygen reconstitution of the mutant protein R2 Y122F. Possible participants in electron transfer chains in ribonucleotide reductase. J. Biol. Chem. 270: 12361-72
63. Sahlin M, Petersson L, Gräslund A, Ehrenberg A, Sjöberg B-M, Thelander L. 1987. Magnetic interaction between the tyrosyl free radical and the antiferromagnetically coupled iron center in ribonucleotide reductase. Biochemistry 26:5541-48
64. Sahlin M, Sjöberg B-M, Backes G, Loehr T, Sanders-Loehr J. 1990. Activation of the iron-containing B2 protein of ribonucleotide reductase by hydrogen peroxide. Biochem. Biophys. Res. Commun. 167:813-18
65. Salowe S, Bollinger JM, Ator M Jr, Stubbe J, McCracken J et al. 1993. Alternative model for mechanism-based inhibition of E. coli ribonucleotide reductase by 2′-azido-2′-deoxyuridine 5′-diphosphate. Biochemistry 32: 12749-60
66. Silva KE, Elgren TE, Que L Jr, Stankovich MT. 1995. Electron transfer properties of the R2 protein or ribonucleotide reductase from E. coli. Biochemistry 34:14093-14103
67. Sjöberg BM. 1994. The ribonucleotide jigsaw puzzle: a large piece falls into place. Structure 2:793-96
68. Sjöberg B-M. 1995. Structure of ribonucleotide reductase from Escherichia coli. In Nucleic Acids and Molecular Biology, ed. F Eckstein, DMJ Lilley, 9:192-221. Berlin/Heidelberg: Springer-Verlag
69. Sjöberg B-M, Reichard P, Gräslund A, Ehrenberg A. 1978. The tyrosine free radical in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 253:6863-65
70. Stubbe J. 1990. Ribonucleotide reductases: amazing and confusing. J. Biol. Chem. 265:5329-32
71. Uhlin U, Eklund H. 1994. Structure of ribonucleotide reductase protein R1. Nature 370:533-39