Ribonucleotide reductases and radical reactions

Cellular and Molecular Life Sciences

Volumn 54, Issue 7, 1998, Pages 684-695

  Fontecave, M ^a  

^a CEA GRENOBLE   (France)

Author keywords

Glycyl; Hydroxyurea; Nitric oxide; Nucleoside analogues; Radicals; Ribonucleotide reductase; Superoxide radical; Thiyl; Tyrosyl

Indexed keywords

DEOXYRIBONUCLEOTIDE; FREE RADICAL; NITRIC OXIDE; RIBONUCLEOSIDE; RIBONUCLEOTIDE REDUCTASE; SCAVENGER; SUPEROXIDE;

CATALYSIS; DNA SYNTHESIS; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; NONHUMAN; REDUCTION; REVIEW;

BINDING SITES; DNA; ENZYME INHIBITORS; FREE RADICALS; MODELS, MOLECULAR; OXIDATION-REDUCTION; RIBONUCLEOTIDE REDUCTASES; RIBONUCLEOTIDES;

ARCHAEA; ESCHERICHIA COLI; LETHRINIDAE; MAMMALIA; PROKARYOTA;

EID: 0031849153     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s000180050195     Document Type: Review

References (93)

1. Reichard P. (1988) Interactions between deoxyribonucleotide and DNA synthesis. Annu. Rev. Biochem. 57: 349-374
2. Hartwig W. (1983) Modern methods for the radical deoxygenation of alcohols. Tetrahedron 39: 2609-2645
3. Reichard P. (1993) From RNA to DNA, why so many ribonucleotide reductases? Science 260: 1773-1777
4. Reichard P. (1997) The evolution of ribonucleotide reduction. Trends Biochem. Sci. 22: 81-85
5. Riera J., Robb F.T., Weiss R. and Fontecave M. (1997) Ribonucleotide reductase in the archaeon Pyrococcus furiosus: a critical enzyme in the evolution of DNA genomes? Proc. Natl. Acad. Sci. USA 94: 475-478
6. Tauer A. and Benner S. (1997) The B12-dependent ribonucleotide reductase from the archaebacterium Thermoplasma acidophila. An evolutionnary solution to the ribonucleotide reductase conundrum. Proc. Natl. Acad. Sci. USA 94: 53-58
7. Nordlund P. and Eklund H. (1993) Structure and function of the Escherichia coli ribonucleotide reductase. J. Mol. Biol. 232: 123-164
8. Uhlin U. and Eklund H. (1994) Structure of ribonucleotide reductase protein R1. Nature 370: 533-539
9. Sjöberg B.-M. (1994) The ribonucleotide reductase jigsaw puzzle: a large piece falls into place. Structure 2: 793-796
10. Sjöberg B.-M. (1995) Structure of ribonucleotide reductase from Escherichia coli. In: Nucleic Acids and Molecular Biology, vol. 9, pp. 192-221. Eckstein F. and Lilley D. M. J. (eds), Springer, Berlin
11. Fontecave M., Nordlund P., Eklund H. and Reichard P. (1992) The redox centers of ribonucleotide reductase of Escherichia coli. Adv. Enzymol. Relat. Areas Mol. Biol. 65: 147-183
12. Eriksson M., Uhlin U., Ramaswamy S., Ekberg M., Regnström K., Sjöberg B.-M. et al. (1997) Binding of allosteric effectors to ribonucleotide reductase protein R1: reduction of active cysteines promotes substrate binding. Structure 5: 1077-1092
13. Larsson Å. and Sjöberg B.-M. (1986) Identification of the stable free radical tyrosine residue in ribonucleotide reductase. EMBO J. 5: 2037-2040
14. Sjöberg B.-M., Reichard P., Gräslund A. and Ehrenberg A. (1978) The tyrosine free radical in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 253: 6863-6865
15. Sahlin M., Petersson L., Gräslund A., Ehrenberg A., Sjöberg B.-M. and Thelander L. (1987) Magnetic interaction between the tyrosyl free radical and the antiferromagnetically coupled iron center in ribonucleotide reductase. Biochemistry 26: 5541-5548
16. Jordan A., Pontis E., Aslund F., Hellman U., Gibert I. and Reichard P. (1996) The ribonucleotide reductase system from Lactococcus lactis. J. Biol. Chem. 271: 8779-8785
17. Jordan A., Gibert I. and Barbé J. (1994) Cloning and sequencing of the genes from Salmonella typhimurium encoding a new bacterial ribonucleotide reductase. J. Bacteriol. 176: 3420-3427
18. Yang F., Lu G. and Rubin H. (1994) Isolation of ribonucleotide reductase from Mycobacterium tuberculosis and cloning, expression and purification of the large subunit. J. Bacteriol. 176: 6738-6743
19. Jordan A., Aragall E., Gibert I. and Barbé J. (1996) Promoter identification and expression analysis of Salmonella typhimurium and Escherichia coli nrdEF operons encoding one of two class I ribonucleotide reductases present in both bacteria. Mol. Microbiol. 19: 777-790
20. Eliasson R., Pontis E., Jordan A. and Reichard P. (1996) Allosteric regulation of the third ribonucleotide reductase (NrdEF enzyme) from enterobacteriaceae. J. Biol. Chem. 271: 26582-26587
21. Booker S., Licht S., Broderick J. and Stubbe J. (1994) Coenzyme B12-dependent ribonucleotide reductase: evidence for the participation of rive cysteine residues in ribonucleotide reduction. Biochemistry 33: 12676-12685
22. Fontecave M., Eliasson R. and Reichard P. (1989) Oxygen-sensitive ribonucleoside triphosphate reductase is present in anaerobic Escheriehia coli. Proc. Natl. Acad. Sci. USA 86: 2147-2151
23. Young P., Öhman M. and Sjöberg B.-M. (1994) Bacteriophage T4 gene 55.9 encodes an activity required for anaerobic ribonucleotide reduction. J. Biol. Chem. 269: 27815-27818
24. Young P., Andersson J., Sahmin M. and Sjöberg B.-M. (1996) Bacteriophage T4 anaerobic ribonucleotide reductase contains a stable glycyl radical at position 580. J. Biol. Chem. 271: 20770-20775
25. Ollagnier S., Mulliez E., Gaillard J., Eliasson R., Fontecave M. and Reichard P. (1996) The anaerobic Escherichia coli ribonucleotide reductase. J. Biol. Chem. 271: 9410-9416
26. Eliasson R., Pontis E., Sun X. and Reichard P. (1994) Allosteric control of the substrate specificity of the anaerobic ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 269: 26052-26057
27. Sun X., Harder J., Krook M., Jörnvall H., Sjöberg B.-M. and Reichard P. (1993) A possible glycine radical in anaerobic ribonucleotide reductase from Escherichia coli: nucleotide sequence of the cloned nrdD gene. Proc. Natl. Acad. Sci. USA 90: 577-581
28. Sun X., Ollagnier S., Schmidt P. P., Atta M., Mulliez E., Lepape L. et al. (1996) The free radical of the anaerobic ribonucleotide reductase from Escherichia coli is at glycine 681. J. Biol. Chem. 271: 6827-6831
29. Referencce deleted in proof.
30. Willing A., Follmann H. and Auling G. (1988) Ribonucleotide reductase of Brevibacterium ammoniagenes is a manganese enzyme. Eur. J. Biochem. 170: 603-614
31. Mulliez E. and Fontecave M. (1997) Structure and reactivity of the metal centers of ribonucleotide reductases. Chem. Ber. 130: 317-320
32. Ollagnier S., Mulliez F., Schmidt P. P., Eliasson R., Gaillard J., Deronzier C. et al. (1997) Activation of the anaerobic ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 272: 24216-24223
33. Tong W. H., Chen S., Lloyd S. G., Edmondson D. E., Huynh B. H. and Stubbe J. (1996) Mechanism of assembly of the diferric cluster-tyrosyl radical cofactor of Escherichia coli ribonucleotide reductase from the diferrous form of the R2 subunit. J. Am. Chem. Soc. 118: 2107-2108
34. Sturgeon B. E., Burdi D., Chen S., Huynh B. H., Edmondson D. E., Stubbe J. et al. (1996) Reconsideration of X, the diiron intermediate formed during cofactor assembly in E. coli ribonucleotide reductase. J. Am. Chem. Soc. 118: 7551-7557
35. Fontecave M., Eliasson R. and Reichard P. (1987) NAD(P)H:flavin oxidoreductase of Escherichia coli: a ferric reductase participating in the generation of the free radical of ribonucleotide reductase. J. Biol. Chem. 262: 12325-12331
36. Fontecave M., Eliasson R. and Reichard P. (1989) Enzymatic regulation of the radical content of the small subunit of Escherichia coli ribonucleotide reductase involving reduction of its redox centers. J. Biol. Chem. 264: 9164-9170
37. Covès J., Laulhère J. P. and Fontecave M. (1997) The role of exogenous iron in the activation of ribonucleotide reductase from Escherichia coli. J. Biol. Inorg. Chem. 2: 418-426
38. Ochiai E.-I., Mann G. J., Gräslund A. and Thelander L. (1990) Tyrosyl radical formation in the small subunit of mouse ribonucleotide reductase. J. Biol. Chem. 265: 15758-15761
39. Eliasson R., Fontecave M., Jörnvall H., Krook M., Pontis E. and Reichard P. (1990) The anaerobic ribonucleoside triphosphate reductase from Escherichia coli requires S-adenosylmethionine as a cofactor. Proc. Natl. Acad. Sci. USA 87: 3314-3318
40. Mulliez E., Fontecave M., Gaillard J. and Reichard P. (1993) An iron-sulfur center and a free radical in the active anaerobic ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 268: 2296-2299
41. Harder J., Eliasson R., Pontis E., Ballinger M. D. and Reichard P. (1992) Activation of the anaerobic ribonucleotide reductase from Escherichia coli by S-adenosylmethionine. J. Biol. Chem. 267: 25548-25552
42. Licht S., Gerfen G. J. and Stubbe J. (1996) Thiyl radicals in ribonucleotide reductases. Science 271: 477-481
43. Gerfen G. J., Licht S., Willems J.-P., Hoffman B. M. and Stubbe J. (1996) Electron paramagnetic resonance investigations of a kinetically competent intermediate formed in ribonucleotide reduction: evidence for a thiyl radical:cob(II)-alamin interaction. J. Am. Chem. Soc. 118: 8192-8197
44. Stubbe J. and Van der Donk W. (1995) Ribonucleotide reductases: radical enzymes with suicidal tendencies. Chem. Biol. 2: 793-801
45. Persson A. L., Eriksson M., Katterle B., Pötsch S., Sahlin M. and Sjöberg B.-M. (1997) A new mechanism-based radical intermediate in a mutant R1 protein affecting the catalytically essential Glu441 in Escherichia coli ribonucleotide reductase. J. Biol. Chem. 272: 31533-31541
46. Lenz R. and Giese B. (1997) Studies on the mechanism of ribonucleotide reductases. J. Am. Chem. Soc. 119: 2784-2794
47. Åberg A., Hahne S., Karlsson M., Larsson A., Ormö M., Ahgren A. et al. (1989) Evidence for two different classes of redox active cysteines in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 264: 12249-12252
48. Mao S. S., Holler T. P., Yu G. X., Bollinger J. M. Jr., Booker S., Johnston M. I. et al. (1992) A model for the role of multiple cysteine residues involved in ribonucleotide reduction: amazing and still confusing. Biochemistry 31: 9733-9743
49. Robins M. J. and Wilson J. S. (1981) Smooth and efficient deoxygenation of secondary alcohols. J. Am. Chem. Soc. 103:932-933
50. Mao S. S., Yu G. X., Chalfoun D. and Stubbe J. (1992) Characterization of C439SR1, a mutant of Escherichia coli ribonucleotide 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
51. 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. Biochemistry 31: 4801-4807
52. 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
53. 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
54. Lycksell P.-O. and Sahlin M. (1995) Demonstration of segmental mobility in the functionnaly essential carboxyl terminal part of Escherichia coli ribonucleotide reductase. FEBS Lett. 368: 441-444
55. Siegbahn E. M., Blomberg R. A. and Crabtrce R. H. (1998) Hydrogen transfer in the presence of amino acid radicals. Theor. Chem. Acc., in press
56. Eliasson R., Ponlis E., Eckstein F. and Reichard P. (1994) Interactions of 2′-modified azido- and haloanalogs of deoxycytidine 5′-triphosphate with the anaerobic Escherichia coli ribonucleotide reductase. J. Biol. Chem. 269: 26116-26120
57. Eliasson R., Reichard P., Mulliez E., Ollagnier S., Fontecave M., Liepinsh E. et al. (1995) The mechanism of the anaerobic Escherichia coli ribonucleotide reductase investigated with nuclear magnetic resonance spectroscopy. Biochem. Biophys. Res. Commun. 214: 28-35
58. Mulliez E., Ollagnier S., Fontecave M., Eliasson R. and Reichard P. (1995) Formate is the hydrogen donor for the anaerobic Escherichia coli ribonucleotide reductase. Proc. Natl. Acad. Sci. USA 92: 8759-8762
59. Elford H. L., Freese M., Passamani E. and Morris H. P. (1970) Ribonucleotide reductase and cell proliferation. J. Biol. Chem. 245: 5228-5233
60. Takeda E. and Weber G. (1981) Role of ribonueleotide reductase in expression of the neoplastic program. Life Sci. 28: 1007-1014
61. Lankinen H., Gräslund A. and Thelander L. (1982) Induction of a new ribonucleotide reductase after infection of mouse cells with Pseudorabies virus. J. Virol. 41: 893-900
62. Turk S. R., Shipman C. and Drach J. C. (1986) Selective inhibition of herpes simplex virus ribonucleotide reductase by derivatives of 2-acetylpyridine thiosemicarbazone. Biochem. Pharmacol. 35: 1539-1545
63. Colleen Moore E. and Hurlbert R. B. (1985) The inhibition of ribonucleotide reductase by hydroxyurea, guanazole and pyrazoloimidazole. Pharmacol. Ther. 27: 167-196
64. Kjoller-Larsen I., Sjöberg B.-M. and Thelander L. (1982) Characterization of the active site of ribonueleotide reductase of Escherichia coli, bacteriophage T4 and mammalian cells by inhibition studies with hydroxyurea analogues. Eur. J. Biochem. 125: 875-881
65. Elford H. L., Wampler G. L. and Van't Riet B. (1979) New ribonucleotide reductase inhibitors with antineoplastic activity. Cancer Res. 39: 844-851
66. Atta M., Lamarche N., Battioni J. P., Massie B., Langelier Y., Mansuy D. et al. (1993) Escherichia coli and herpes-simplex-virus ribonucleotide reductase R2 subunit. Biochem. J. 290: 807-810
67. Pötsch S., Sahlin M., Langelier Y., Gräslund A. and Lassmann G. (1995) Reduction of the tyrosyl radical and the iron center in protein R2 of ribonucleotide reductase from mouse, herpes simplex virus and E. coli by p-alkoxyphenols. FEBS Lett. 374: 95-99
68. Lassman G., Thelander L. and Gräslund A. (1992) EPR stopped-flow studies of the reaction of the tyrosyl radical of protein R2 from ribonucleotide reductase with hydroxyurea. Biochem. Biophys. Res. Commun. 188: 879-887
69. Karlsson M., Sahlin M. and Sjöberg B.-M. (1992) Escherichia coli ribonucleotide reductase. Radical susceptibility to hydroxyurea is dependent on the regulatory state of the enzyme. J. Biol. Chem. 267: 12622-12626
70. Nyholm S., Thelander L. and Gräslund A. (1993) Reduction and loss of the iron center in the reaction of the small subunit of mouse ribonucleotide reductase with hydroxyurea. Biochemistry 32: 11569-11574
71. Lori F., Malykh A., Cara A., Sun D., Weinstein J. N., Lisziewicz J. et al. Hydroxyurea as an inhibitor of HIV-1 replication. Science 266: 801-805
72. Malley S. D., Grange J. M., Hamedi-Sangsari F. and Vila J. R. (1994) Synergistic anti-HIV-1 effect of hydroxamate compounds with 2′,3′-dideoxyinosine in infected resting lymphocytes. Proc. Natl. Acad. Sci. USA 91: 11017-11021
73. Gao W.-Y., Johns D. G., Chokekijchai S. and Mitsuya H. (1995) Disparate actions of hydroxyurea in potentiation of purine and pyrimidine 2′,3′-dideoxynucleoside activities against replication of HIV. Proc. Natl. Acad. Sci. USA 92: 8333-8337
74. Gao W.-Y., Cara A., Gallo R. C. and Lori F. (1993) Low levels of deoxynucleotides in peripheral blood lymphocytes: a strategy to inhibit HIV-1 replication. Proc. Natl. Acad. Sci. USA 90: 8925-8928
75. Bianchi V., Borella S., Calderazzo F., Ferraro P., Bianchi L. C. and Reichard P. (1994) Inhibition of ribonucleotide reductase by 2′-substituted deoxycytidine analogs: possible application in AIDS treatment. Proc. Natl. Acad. Sci. USA 91: 8403-8407
76. Fontecave M., Lepoivre M., Elleingand E., Gerez C. and Guittet O. (1998) Resveratrol, a remarkable inhibitor of ribonucleotide reductase. FEBS Lett. 421: 277-279
77. Feldman P. L., Griffith O. W. and Stuehr D. J. (1993) The surprising life of nitric oxide. Chem. Eng. News, 20 December, 26-38
78. Lepoivre M., Flamand J. M. and Henry Y. (1992) Early loss of the tyrosyl radical in ribonucleotide reductase of adenocarcinoma cells producing nitric oxide. J. Biol. Chem. 267: 22994-23000
79. Roy B., Lepoivre M., Henry Y. and Fontecave M. (1995) Inhibition of ribonucleotide reductase by nitric oxide from thionitrites: reversible modifications of both subunits. Biochemistry 34: 5411-5418
80. Eiserich J. P., Butler J., Van der Vliet A., Cross C. E. and Halliwell B. (1995) Nitric oxide rapidly scavenges tyrosinc and tryptophan radicals. Biochem. J. 310: 745-749
81. Eliasson R., Jörnvall H. and Reichard P. (1986) Superoxide dismutase participates in the enzymatic formation of the tyrosine radical of ribonucleotide reductase from Escherichia coli. Proc. Natl. Acad. Sci. USA 83: 2373-2377
82. Fontecave M., Gräslund A. and Reichard P. (1987) The function of superoxide dismutase during the enzymatic formation of the free radical of ribonucleotide reductase. J. Biol. Chem. 262: 12332-12336
83. Gaudu P., Nivière V., Pétillot Y., Kauppi B. and Fontecave M. (1996) The irreversible inactivation of ribonucleotide reductase from Escherichia coli by superoxide radicals. FEBS Lett. 387: 137-140
84. Baker C. H., Banzon J., Bollinger J. M., Stubbe J., Samano V., Robins M. J. et al. (1991) 2′-deoxy-2′-methylenecytidine and 2′-deoxy-2′,2′-difluorocytidine 5′-diphosphates: potent mechanism-based inhibitors of ribonucleotide reductase. J. Med. Chem. 34: 1879-1884
85. Van der Donk W. A., Yu G., Silva D. J., Stubbe J., McCarthy J. R., Jarvi E. T. et al. (1996) Inactivation of ribonucleotide reductase by 2′-fluoromethylene-2′-deoxycytidine 5′-diphosphate: a paradigm for nucleotide mechanism-based inhibitors. Biochemistry 35: 8381-8391
86. Covès J., Le Hir de Falloix L., Le Pape L., Décout J. L. and Fontecave M. (1996) Inactivation of Escherichia coli ribonucleotide reductase by 2′-deoxy-2′-mercaptouridine 5′-diphosphate. Electron paramagnetic resonance evidence for a transient protein perthiyl radical. Biochemistry 35: 8595-8602
87. Sjöberg B.-M., Gräslund A. and Eckstein F. (1983) A substrate radical intermediate in the reaction between ribonucleotide reductase from Escherichia coli and 2′-azido-2′-deoxynucleoside diphosphates. J. Biol. Chem. 258: 8060-8067
88. Kaye S. B. (1994) Gemcitabine: current status of phase I and II trials. J. Clin. Oncol. 12: 1527-1531
89. Van der Donk W. A., Stubbe J., Gerfen G. J., Bellew B. F. and Griffin R. G. (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: 8908-8916
90. Ormö M., Regnström K., Wang Z., Que L., Sahlin M. and Sjöberg B.-M. (1995) Residues important for radical stability in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 270: 6570-6576
91. Gerez C., Elleingand E., Kauppi B., Eklund H. and Fontecave M. (1997) Reactivity of the tyrosyl radical of Escherichia coli ribonucleotide reductase. Control by the protein. Eur. J. Biochem. 249: 401-407
92. Fontecave M. and Pierre J. L. (1996) Protein tyrosyl free radicals as active species in metalloenzyme catalysis. Bull. Soc. Chim. 133: 653-660
93. Stubbe J. (1989) Protein radical involvement in biological catalysis. Ann. Rev. Biochem. 58: 257-285