Pre-steady-state and steady-state kinetic analysis of E. coli class I ribonucleotide reductase

Biochemistry

Volumn 42, Issue 34, 2003, Pages 10071-10083

  Ge, Jie ^a   Yu, Guixue ^a,b   Ator, Mark A ^a,c   Stubbe, JoAnne ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

^c CEPHALON INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CONFORMATIONS; ENZYMES; MONOMERS; SUBSTRATES;

ALLOSTERIC EFFECTORS;

ESCHERICHIA COLI;

DISULFIDE; DITHIOL DERIVATIVE; NUCLEOSIDE DERIVATIVE; NUCLEOSIDE DIPHOSPHATE DERIVATIVE; NUCLEOTIDE; RIBONUCLEOTIDE REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SUBUNIT; ESCHERICHIA COLI; NONHUMAN; OXIDATION; PRIORITY JOURNAL; REDUCTION; STEADY STATE; ULTRAVIOLET SPECTROSCOPY;

ADENOSINE TRIPHOSPHATE; AMINO ACID SUBSTITUTION; BINDING SITES; DEOXYCYTOSINE NUCLEOTIDES; ESCHERICHIA COLI; FREE RADICALS; KINETICS; NADP; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PROTEIN SUBUNITS; RIBONUCLEOTIDE REDUCTASES; SPECTROPHOTOMETRY, ULTRAVIOLET; THIOREDOXIN; THIOREDOXIN REDUCTASE (NADPH); TYROSINE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; KOBUS; NEGIBACTERIA;

EID: 0041823734     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi034374r     Document Type: Article

References (65)

1. Licht, S., and Stubbe, J. (1999) in Comprehensive Natural Products Chemistry (Barton, S. D., Nakanishi, K., Meth-Cohn, O., and Poulter, C. D., Eds.) pp 163, Elsevier Science, New York.
2. Jordan, A., and Reichard, P. (1998) Ribonucleotide reductases, Annu. Rev. Biochem. 67, 71-98.
3. Elledge, S. J., Zhou, Z., Allen, J. B., and Navas, T. A. (1993) DNA damage and cell cycle regulation of ribonucleotide reductase, BioEssays 15, 333-9.
4. Stubbe, J. (1998) Ribonucleotide reductases in the twenty-first century, Proc. Natl. Acad. Sci. U.S.A. 95, 2723-4.
5. Stubbe, J., and van der Donk, W. A. (1998) Protein radicals in enzyme catalysis, Chem. Rev. 98, 705-62.
6. Eklund, H., Uhlin, U., Farnegardh, M., Logan, D. T., and Nordlund, P. (2001) Structure and function of the radical enzyme ribonucleotide reductase, Prog. Biophys. Mol. Biol. 77, 177-268.
7. Licht, S. S., Lawrence, C. C., and Stubbe, J. (1999) Class II ribonucleotide reductases catalyze carbon-cobalt bond reformation on every turnover, J. Am. Chem. Soc. 121, 7463-8.
8. Licht, S. S., Booker, S., and Stubbe, J. (1999) Studies on the catalysis of carbon-cobalt bond homolysis by ribonucleoside triphosphate reductase: Evidence for concerted carbon-cobalt bond homolysis and thiyl radical formation, Biochemistry 38, 1221-33.
9. Licht, S. S., Lawrence, C. C., and Stubbe, J. (1999) Thermodynamic and kinetic studies on carbon-cobalt bond homolysis by ribonucleoside triphosphate reductase: The importance of entropy in catalysis, Biochemistry 38, 1234-42.
10. Licht, S., Gerfen, G. J., and Stubbe, J. (1996) Thiyl radicals in ribonucleotide reductases, Science 271, 477-81.
11. Orme-Johnson, W. H., Beinert, H., and Blakley, R. L. (1974) Cobamides and ribonucleotide reduction. XII. The electron paramagnetic resonance spectrum of "active coenzyme B 12", J. Biol. Chem. 249, 2338-43.
12. Tamao, Y., and Blakley, R. L. (1973) Direct spectrophotometric observation of an intermediate formed from deoxyadenosyl-cobalamin in ribonucleotide reduction, Biochemistry 12, 24-34.
13. Thelander, L. (1973) Physicochemical characterization of ribonucleoside diphosphate reductase from Escherichia coli, J. Biol. Chem. 248, 4591-601.
14. Brown, N. C., and Reichard, P. (1969) Ribonucleoside diphosphate reductase. Formation of active and inactive complexes of proteins B1 and B2, J. Mol. Biol. 46, 25-38.
15. Lin, A. N., Ashley, G. W., and Stubbe, J. (1987) Location of the redox-active thiols of ribonucleotide reductase: Sequence similarity between the Escherichia coli and Lactobacillus leichmannii enzymes, Biochemistry 26, 6905-9.
16. Mao, S. S., Johnston, M. I., Bollinger, J. M., and Stubbe, J. (1989) Mechanism-based inhibition of a mutant Escherichia coli ribonucleotide reductase (cysteine-225→serine) by its substrate CDP, Proc. Natl. Acad. Sci. U.S.A. 86, 1485-9.
17. Mao, S. S., Holler, T. P., Bollinger, J. M., Jr., Yu, G. X., Johnston, M. I., and Stubbe, J. (1992) Interaction of C225SR1 mutant subunit of ribonucleotide reductase with R2 and nucleoside diphosphates: Tales of a suicidal enzyme, Biochemistry 31, 9744-51.
18. Mao, S. S., Holler, T. P., Yu, G. X., Bollinger, J. M., Jr., Booker, S., Johnston, M. I., and Stubbe, J. (1992) A model for the role of multiple cysteine residues involved in ribonucleotide reduction: Amazing and still confusing, Biochemistry 31, 9733-43.
19. Mao, S. S., Yu, G. X., Chalfoun, D., and 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 possessing novel thioredoxin-like activity, Biochemistry 31, 9752-9.
20. Åberg, A., Hahne, S., Karlsson, M., Larsson, A., Ormö, M., Ahgren, A., and Sjöberg, B.-M. (1989) Evidence for two different classes of redox-active cysteines in ribonucleotide reductase of Escherichia coli, J. Biol. Chem. 264, 12249-52.
21. Kashlan, O. B., and Cooperman, B. S. (2003) Comprehensive model for allosteric regulation of mammalian ribonucleotide reductase: Refinements and consequences, Biochemistry 42, 1696-706.
22. Kashlan, O. B., Scott, C. P., Lear, J. D., and Cooperman, B. S. (2002) A comprehensive model for the allosteric regulation of mammalian ribonucleotide reductase. Functional consequences of ATP- and dATP-induced oligomerization of the large subunit, Biochemistry 41, 462-74.
23. Brown, N. C., and Reichard, P. (1969) Role of effector binding in allosteric control of ribonucleoside diphosphate reductase, J. Mol. Biol. 46, 39-55.
24. Thelander, L., and Reichard, P. (1979) Reduction of ribonucleotides, Annu. Rev. Biochem. 48, 133-58.
25. Uhlin, U., and Eklund, H. (1994) Structure of ribonucleotide reductase protein R1, Nature 370, 533-9.
26. 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., in press.
27. Nordlund, P., Sjöberg, B.-M., and Eklund, H. (1990) Three-dimensional structure of the free radical protein of ribonucleotide reductase, Nature 345, 593-8.
28. Nordlund, P., and Eklund, H. (1993) Structure and function of the Escherichia coli ribonucleotide reductase protein R2, J. Mol. Biol. 232, 123-64.
29. Erickson, H. K. (2001) Kinetics in the pre-steady state of the formation of cystines in ribonucleoside diphosphate reductase: Evidence for an asymmetric complex, Biochemistry 40, 9631-7.
30. Erickson, H. K. (2000) Formation of the cystine between cysteine 225 and cysteine 462 from ribonucleoside diphosphate reductase is kinetically competent, Biochemistry 39, 9241-50.
31. Lunn, C. A., Kathju, S., Wallace, C., Kushner, S., and Pigiet, V. (1984) Amplification and purification of plasmid-encoded thioredoxin from Escherichia coli K12, J. Biol. Chem. 259, 10469-74.
32. a values of Escherichia coli thioredoxin, Biochemistry 36, 14985-91.
33. Russel, M., and Model, P. (1985) Direct cloning of the trx gene that encodes thioredoxin reductase, J. Bacteriol. 163, 238-42.
34. Salowe, S., Bollinger, J. M., Jr., Ator, M., Stubbe, J., McCraken, J., Peisach, J., Samano, M. C., and Robins, M. J. (1993) Alternative model for mechanism-based inhibition of Escherichia coli ribonucleotide reductase by 2′-azido-2′-deoxyuridine 5′-diphosphate, Biochemistry 32, 12749-60.
35. Thelander, L., Sjöberg, B. R., and Eriksson, S. (1978) Ribonucleoside diphosphate reductase (Escherichia coli), Methods Enzymol. 51, 227-37.
36. Salowe, S. P., and Stubbe, J. (1986) Cloning, overproduction, and purification of the B2 subunit of ribonucleoside-diphosphate reductase, J. Bacteriol. 165, 363-6.
37. Usova, E. V., and Eriksson, S. (1997) The effects of high salt concentrations on the regulation of the substrate specificity of human recombinant deoxycytidine kinase, Eur. J. Biochem. 248, 763-6.
38. Bollinger, J. M., Jr., Tong, W. H., Ravi, N., Huynh, B. H., Edmondson, D. E., and Stubbe, J. A. (1995) Use of rapid kinetics methods to study the assembly of the diferric-tyrosyl radical cofactor of E. coli ribonucleotide reductase, Methods Enzymol. 258, 278-303.
39. Steeper, J. R., and Steuart, C. D. (1970) A rapid assay for CDP reductase activity in mammalian cell extracts, Anal. Biochem. 34, 123-30.
40. Kuzmic, P. (1996) Program DYNAFIT for the analysis of enzyme kinetic data: Application to HIV proteinase, Anal. Biochem. 237, 260-73.
41. Stubbe, J., Ator, M., and Krenitsky, T. (1983) Mechanism of ribonucleoside diphosphate reductase from Escherichia coli. Evidence for 3′ C-H bond cleavage, J. Biol. Chem. 258, 1625-31.
42. Stubbe, J., and Ackles, D. (1980) On the mechanism of ribonucleoside diphosphate reductase from Escherichia coli. Evidence for 3′ C-H bond cleavage, J. Biol. Chem. 255, 8027-30.
43. Thelander, L. (1974) Reaction mechanism of ribonucleoside diphosphate reductase from Escherichia coli. Oxidation-reduction-active disulfides in the B1 subunit, J. Biol. Chem. 249, 4858-62.
44. Sintchak, M. D., Arjara, G., Kellogg, B. A., Stubbe, J., and Drennan, C. L. (2002) The crystal structure of class II ribonucleotide reductase reveals how an allosterically regulated monomer mimics a dimer, Nat. Struct. Biol. 9, 293-300.
45. Booker, S., Licht, S., Broderick, J., and Stubbe, J. (1994) Coenzyme B12-dependent ribonucleotide reductase: Evidence for the participation of five cysteine residues in ribonucleotide reduction, Biochemistry 33, 12676-85.
46. Climent, I., Sjöberg, B.-M., and Huang, C. Y. (1991) Carboxyl-terminal peptides as probes for Escherichia coli ribonucleotide reductase subunit interaction: Kinetic analysis of inhibition studies, Biochemistry 30, 5164-71.
47. 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, 4801-7.
48. Scott, C. P., Kashlan, O. B., Lear, J. D., and Cooperman, B. S. (2001) A quantitative model for allosteric control of purine reduction by murine ribonucleotide reductase, Biochemistry 40, 1651-61.
49. Allard, P., Kuprin, S., Shen, B., and Ehrenberg, A. (1992) Binding of the competitive inhibitor dCDP to ribonucleoside-diphosphate reductase from Escherichia coli studied by 1H NMR. Different properties of the large protein subunit and the holoenzyme, Eur. J. Biochem. 208, 635-42.
50. 1H NMR, Eur. J. Biochem. 208, 631-4.
51. Ormö, M., and Sjöberg, B.-M. (1990) An ultrafiltration assay for nucleotide binding to ribonucleotide reductase, Anal. Biochem. 189, 138-41.
52. Soderman, K., and Reichard, P. (1986) A nitrocellulose filter binding assay for ribonucleotide reductase, Anal. Biochem. 152, 89-93.
53. von Dobeln, U., and Reichard, P. (1976) Binding of substrates to Escherichia coli ribonucleotide reductase, J. Biol. Chem. 251, 3616-22.
54. Ashley, G. W., Harris, G., and Stubbe, J. (1986) The mechanism of Lactobacillus leichmannii ribonucleotide reductase. Evidence for 3′ carbon-hydrogen bond cleavage and a unique role for coenzyme B12, J. Biol. Chem. 261, 3958-64.
55. Lenz, R., and Giese, B. (1997) Studies on the mechanism of ribonucleotide reductases, J. Am. Chem. Soc. 119, 2784-94.
56. Lawrence, C. C., Bennati, M., Obias, H. V., Bar, G., Griffin, R. G., and Stubbe, J. (1999) High-field EPR detection of a disulfide radical anion in the reduction of cytidine 5′-diphosphate by the E441Q R1 mutant of Escherichia coli ribonucleotide reductase, Proc. Natl. Acad. Sci. U.S.A. 96, 8979-84.
57. Northrop, D. B. (1982) Deuterium and tritium kinetic isotope effects on initial rates, Methods Enzymol. 87, 607-25.
58. Swain, C. G., Stivers, E. C., Reuwer, J., Joseph F., and Schaad, L. J. (1958) Use of hydrogen isotope effects to identify the attacking nucleophile in the enolization of ketones catalyzed by acetic acid, J. Am. Chem. Soc. 80, 5885-93.
59. Sjöberg, B.-M., Karlsson, M., and Jörnvall, H. (1987) Half-site reactivity of the tyrosyl radical of ribonucleotide reductase from Escherichia coli, J. Biol. Chem. 262, 9736-43.
60. 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, 20655-9.
61. Ekberg, M., Pötsch, S., Sandin, E., Thunnissen, M., Nordlund, P., Sahlin, M., and Sjöberg, B.-M. (1998) 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, 21003-8.
62. 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, 23746-51.
63. 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, 4267-75.
64. Gray, H. B., and Winkler, J. R. (1997) Electron tunneling in structurally engineered proteins, J. Electroanal. Chem. 438, 43-7.
65. Barshop, B. A., Wrenn, R. F., and Frieden, C. (1983) Analysis of numerical methods for computer simulation of kinetic processes: Development of KINSIM-a flexible, portable system, Anal. Biochem. 130, 134-45.