The First Holocomplex Structure of Ribonucleotide Reductase Gives New Insight into its Mechanism of Action

Journal of Molecular Biology

Volumn 359, Issue 2, 2006, Pages 365-377

  Uppsten, Malin ^a   Färnegårdh, Mathias ^a   Domkin, Vladimir ^a   Uhlin, Ulla ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

crystal structure; holocomplex; R2 C terminus; ribonucleotide reductase; RNR

Indexed keywords

HOLOENZYME; RIBONUCLEOTIDE REDUCTASE;

AMINO ACID SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME MECHANISM; ENZYME STRUCTURE; HYDROPHOBICITY; MOLECULAR INTERACTION; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM; STRUCTURE ANALYSIS;

DNA VIRUSES; MAMMALIA; PROKARYOTA; SALMONELLA TYPHIMURIUM;

EID: 33646176383     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.03.035     Document Type: Article

References (71)

1. Thelander L., and Reichard P. Reduction of ribonucleotides. Annu. Rev. Biochem. 48 (1979) 133-158
2. Reichard P. From RNA to DNA, why so many ribonucleotide reductases?. Science 260 (1993) 1773-1777
3. Sjöberg B.M. Ribonucleotide reductases-a group of enzymes with different metallosites and a similar reaction mechanism. Struct. Bond. 88 (1997) 139-173
4. Jordan A., and Reichard P. Ribonuclotide reductases. Annu. Rev. Biochem. 67 (1998) 71-98
5. Licht S., Gerfen G.J., and Stubbe J. Thiyl radicals in ribonucleotide reductases. Science 271 (1996) 477-481
6. Eklund H., and Fontecave M. Glycyl radical enzymes: a conservative structural basis for radicals. Struct. Fold. Des. 7 (1999) R257-R262
7. Logan D.T., Andersson J., Sjöberg B.M., and Nordlund P. A glycyl radical site in the crystal structure of a class III ribonucleotide reductase. Science 283 (1999) 1499-1504
8. 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
9. Sintchak M.D., Arjara G., Kellogg B.A., Stubbe J., and Drennan C.L. The crystal structure of class II ribonucleotide reductase reveals how an allosterically regulated monomer mimics a dimer. Nature Struct. Biol. 9 (2002) 293-300
10. Eliasson R., Pontis E., Jordan A., and Reichard P. Allosteric regulation of the third ribonucleotide reductase (NrdEF enzyme) from enterobacteriaceae. J. Biol. Chem. 271 (1996) 26582-26587
11. Dawes S.S., Warner D.F., Tsenova L., Timm J., McKinney J.D., Kaplan G., et al. Ribonucleotide reduction in Mycobacterium tuberculosis: function and expression of genes encoding class Ib and class II ribonucleotide reductases. Infect. Immun. 71 (2003) 6124-6131
12. Torrents E., Jordan A., Karlsson M., and Gibert I. Occurrence of multiple ribonucleotide reductase classes in gamma-proteobacteria species. Curr. Microbiol. 41 (2000) 346-351
13. Gräslund A., Sahlin M., and Sjöberg B.-M. The tyrosyl free radical in ribonucleotide reductase. Environ. Health Perspect. 64 (1985) 139-149
14. Larsson A., and Sjöberg B.M. Identification of the stable free radical tyrosine residue in ribonucleotide reductase. EMBO J. 5 (1986) 2037-2040
15. von Döbeln U., and Reichard P. Binding of substrates to Escherichia coli ribonucleotide reductase. J. Biol. Chem. 251 (1976) 3616-3622
16. Åberg A., Hahne S., Karlsson M., Larsson A., Ormö M., Ahgren A., and Sjöberg B.M. Evidence for two different classes of redox-active cysteines in ribonucleotide reductase of Escherichia coli. J. Biol. Chem. 264 (1989) 12249-12252
17. Mao S.S., Holler T.P., Yu G.X., Bollinger Jr. J.M., Booker S., Johnston M.I., and Stubbe J. A model for the role of multiple cysteine residues involved in ribonucleotide reduction: amazing and still confusing. Biochemistry 31 (1992) 9733-9743
18. Mao S.S., Yu G.X., Chalfoun D., and Stubbe J. 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 (1992) 9752-9759
19. Mao S.S., Holler T.P., Bollinger Jr. J.M., Yu G.X., Johnston M.I., and Stubbe J. Interaction of C225SR1 mutant subunit of ribonucleotide reductase with R2 and nucleoside diphosphates: tales of a suicidal enzyme. Biochemistry 31 (1992) 9744-9751
20. Nordlund P., Sjöberg B.M., and Eklund H. Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature 345 (1990) 593-598
21. Petersson L., GrŠslund A., Ehrenberg A., Sjšberg B.-M., and Reichard P. The iron center in ridonucleotide reductase from Escherichia coli. J. Biol. Chem. 255 (1980) 6706-6712
22. Nordlund P., and Eklund H. Structure and function of the Escherichia coli ribonucleotide reductase protein R2. J. Mol. Biol. 232 (1993) 123-164
23. Uhlin U., and Eklund H. Structure of ribonucleotide reductase protein R1. Nature 370 (1994) 533-539
24. Siegbahn P.E.M., Eriksson L., Himo F., and Pavlov M. Hydrogen atom transfer in ribonucleotide reductase (RNR). J. Phys. Chem. B 102 (1998) 10622-10629
25. Schmidt P.P., Rova U., Katterle B., Thelander L., and Graslund A. Kinetic evidence that a radical transfer pathway in protein R2 of mouse ribonucleotide reductase is involved in generation of the tyrosyl free radical. J. Biol. Chem. 273 (1998) 21463-21472
26. 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
27. Rova U., Goodtzova K., Ingemarson R., Behravan G., Gräslund A., and Thelander L. Evidence by site-directed mutagenesis supports long-range electron transfer in mouse ribonucleotide reductase. Biochemistry 34 (1995) 4267-4275
28. Persson B.O., Karlsson M., Climent I., Ling J.S., Loehr J.S., Sahlin M., and Sjöberg B.M. Iron ligand mutants in protein R2 of Escherichia coli ribonucleotide reductase-retention of diiron site, tyrosyl radical and enzymatic activity in mutant proteins lacking an iron-binding side chain. J. Biol. Inorg. Chem. 1 (1996) 247-256
29. 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
30. 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
31. Rova U., Adrait A., Potsch S., Graslund A., and Thelander L. 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 (1999) 23746-23751
32. Ge J., Yu G.X., 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
33. Eriksson M., Uhlin U., Ramaswamy S., Ekberg M., Regnström K., Sjöberg B.M., and Eklund H. Binding of allosteric effectors to ribonucleotide reductase protein R1: reduction of active-site cysteines promotes substrate binding. Structure 5 (1997) 1077-1092
34. Uppsten M., Färnegårdh M., Jordan A., Eliasson R., Eklund H., and Uhlin U. Structure of the large subunit of class Ib ribonucleotide reductase from Salmonella typhimurium and its complexes with allosteric effectors. J. Mol. Biol. 330 (2003) 87-97
35. Jordan A., Gibert I., and Barbe J. Cloning and sequencing of the genes from Salmonella typhimurium encoding a new bacterial ribonucleotide reductase. J. Bacteriol. 176 (1994) 3420-3427
36. Jordan A., Pontis E., Åslund F., Hellman U., Gibert I., and Reichard P. The ribonucleotide reductase system of Lactococcus lactis-characterization of an nrdEF enzyme and a new electron transport protein. J. Biol. Chem. 271 (1996) 8779-8785
37. Scotti C., Valbuzzi A., Perego M., Galizzi A., and Albertini A.M. The Bacillus subtilis genes for ribonucleotide reductase are similar to the genes for the second class I NrdE/NrdF enzymes of Enterobacteriaceae. Microbiology 142 (1996) 2995-3004
38. Fraser C.M., Gocayne J.D., White O., Adams M.D., Clayton R.A., Fleischmann R.D., et al. The minimal gene complement of Mycoplasma genitalium. Science 270 (1995) 397-403
39. Yang F.D., Lu G.Z., and Rubin H. Isolation of ribonucleotide reductase from Mycobacterium tuberculosis and cloning, expression, and purification of the large subunit. J. Bacteriol. 176 (1994) 6738-6743
40. Cohen E.A., Gaudreau P., Brazeau P., and Langlier Y. Specific inhibition of herpes virus ribonucleotide reductase by a nonapeptide derived from the carboxy terminus of subunit 2. Nature 321 (1986) 441-442
41. Dutia B.M., Frame M.C., Subak-Sharpe J.H., Clark W.N., and Marsden H.S. Specific inhibition of herpesvirus ribonucleotide reductase by synthetic peptides. Nature 321 (1986) 439-441
42. Cosentino G., Lavallee P., Rakhit S., Plante R., Gaudette Y., Lawetz C., et al. Specific inhibition of ribonucleotide reductase by peptides corresponding to the C-terminal of their second subunit. Biochem. Cell Biol. 69 (1991) 79-83
43. Sjöberg B.M., Karlsson M., and Jörnvall H. Half-site reactivity of the tyrosyl radical of ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 262 (1987) 9736-9743
44. Climent I., Sjöberg B.-M., and Huang C.Y. Carboxyl-terminal peptides as probes for Escherichia coli ribonucleotide reductase subunit interaction: kinetic analysis of inhibition studies. Biochemistry 30 (1991) 5164-5171
45. Bollinger Jr. J.M., Edmondson D.E., Huynh B.H., Filley J., Norton J.R., and Stubbe J. Mechanism of assembly of the tyrosyl radical-dinuclear iron cluster cofactor of ribonucleotide reductase. Science 253 (1991) 292-298
46. Rova U., Adrait A., Potsch S., Gräslund A., and Thelander L. 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 (1999) 23746-23751
47. Kauppi B., Nielsen B.B., Ramaswamy S., Larsen I.K., Thelander M., Thelander L., and Eklund H. The three-dimensional structure of mammalian ribonucleotide reductase protein R2 reveals a more-accessible iron-radical site than Escherichia coli R2. J. Mol. Biol. 262 (1996) 706-720
48. Voegtli W.C., Ge J., Perlstein D.L., Stubbe J., and Rosenzweig A.C. Structure of the yeast ribonucleotide reductase Y2Y4 heterodimer. Proc. Natl Acad. Sci. USA 98 (2001) 10073-10078
49. Eriksson M., Jordan A., and Eklund H. Structure of Salmonella typhimurium nrdF ribonucleotide reductase in its oxidized and reduced form. Biochemistry 37 (1998) 13359-13369
50. Högbom M., Huque Y., Sjöberg B.M., and Nordlund P. Crystal structure of the di-iron/radical protein of ribonucleotide reductase from Corynebacterium ammoniagenes. Biochemistry 41 (2002) 1381-1389
51. Uppsten M., Davis J., Rubin H., and Uhlin U. Crystal structure of the biologically active form of class Ib ribonucleotide reductase small subunit from Mycobacterium tuberculosis. FEBS Letters 569 (2004) 117-122
52. Lin A.N., Ashley G.W., and Stubbe J. Location of the redox-active thiols of ribonucleotide reductase: sequence similarity between the Escherichia coli and Lactobacillus leichmannii enzymes. Biochemistry 26 (1987) 6905-6909
53. Thelander L. Reaction mechanism of ribonucleoside diphosphate reductase from Escherichia coli. Oxidation-reduction-active disulfides in the B1 subunit. J. Biol. Chem. 249 (1974) 4858-4862
54. Erickson H.K. Kinetics in the pre-steady state of the formation of cystines in ribonucleoside diphosphate reductase: evidence for an asymmetric complex. Biochemistry 40 (2001) 9631-9637
55. Erickson H.K. Formation of the cystine between cysteine 225 and cysteine 462 from ribonucleoside diphosphate reductase is kinetically competent. Biochemistry 39 (2000) 9241-9250
56. 1H NMR. Different properties of the large protein subunit and the holoenzyme. Eur. J. Biochem. 208 (1992) 635-642
57. Roy B., Decout J.L., Beguin C., Fontecave M., Allard P., Kuprin S., and Ehrenberg A. NMR studies of binding of 5-FdUDP and dCDP to ribonucleoside-diphosphate reductase from M. Biochim. Biophys. Acta 1247 (1995) 284-292
58. Kasrayan A., Birgander P.L., Pappalardo L., Regnstrom K., Westman M., Slaby A., et al. Enhancement by effectors and substrate nucleotides of R1-R2 interactions in Escherichia coli class Ia ribonucleotide reductase. J. Biol. Chem. 279 (2004) 31050-31057
59. Chabes A., Domkin V., Larsson G., Liu A., Graslund A., Wijmenga S., and Thelander L. Yeast ribonucleotide reductase has a heterodimeric iron-radical-containing subunit. Proc. Natl Acad. Sci. USA 97 (2000) 2474-2479
60. Uppsten M., Färnegårdh M., Jordan A., Ramaswamy S., and Uhlin U. Expression and preliminary crystallographic studies of R1E, the large subunit of ribonucleotide reductase from Salmonella typhimurium. Acta Crystallog. sect. D 59 (2003) 1081-1083
61. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
62. Read R.J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallog. sect. D 57 (2001) 1373-1382
63. Collabororative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
64. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
65. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A 47 (1991) 110-119
66. Laskowski R.A., Macarthur M.W., Moss D.S., and Thornton J.M. PROCHECK-a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291
67. Vaguine A.A., Richelle J., and Wodak S.J. SFCHECK: a unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Acta Crystallog. sect. D 55 (1999) 191-205
68. Chothia C. Structural invariants of protein folding. Nature 254 (1975) 304-308
69. Lee B., and Richards F. The interpretation of protein structures:estimation of static accessibility. J. Mol. Biol. 55 (1971) 379-400
70. Kleywegt G.J., and Jones T.A. Databases in protein crystallography. Acta Crystallog. sect. D 54 (1998) 1119-1131
71. Brown N.C., and Reichard P. Role of effector binding in allosteric control of ribonucleoside diphosphate reductase. J. Mol. Biol. 46 (1969) 39-55