The dimanganese(II) site of Bacillus subtilis class Ib ribonucleotide reductase

Biochemistry

Volumn 51, Issue 18, 2012, Pages 3861-3871

  Boal, Amie K ^a   Cotruvo, Joseph A ^b   Stubbe, Joanne ^b   Rosenzweig, Amy C ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINOBACTERIA; BACILLUS SUBTILIS; BIOCHEMICAL STUDIES; COFACTORS; COORDINATION GEOMETRY; COORDINATION SPHERE; E. COLI; FLAVODOXIN; METAL CLUSTER; METAL SITES; PROTEIN RESIDUES; PROTEOBACTERIA; RIBONUCLEOTIDE REDUCTASE; RIBONUCLEOTIDES; SECOND GROUP; SEQUENCE ALIGNMENTS; SOLVENT MOLECULES;

BACTERIOLOGY; CARBOXYLATION; ENZYMES; ESCHERICHIA COLI; MANGANESE; POLYPEPTIDES;

MANGANESE COMPOUNDS;

BACTERIAL ENZYME; DEOXYRIBONUCLEOTIDE; MANGANESE DERIVATIVE; RIBONUCLEOTIDE REDUCTASE;

ARTICLE; BACILLUS SUBTILIS; BINDING AFFINITY; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBUNIT; ESCHERICHIA COLI; HYDROGEN BOND; MOLECULE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN CONFORMATION; REDUCTION; SALMONELLA TYPHIMURIUM; STAPHYLOCOCCUS;

BACILLUS SUBTILIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; MANGANESE; RIBONUCLEOTIDE REDUCTASES;

ACTINOBACTERIA; BACILLUS SUBTILIS; ESCHERICHIA COLI; PROTEOBACTERIA; STAPHYLOCOCCUS;

EID: 84860732135     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201925t     Document Type: Article

References (49)

1. Nordlund, P. and Reichard, P. (2006) Ribonucleotide reductases Annu. Rev. Biochem. 75, 681-706 (Pubitemid 44118048)
2. Stubbe, J., Nocera, D. G., Yee, C. S., and Chang, M. C. (2003) Radical initiation in the class I ribonucleotide reductase: Long-range proton-coupled electron transfer? Chem. Rev. 103, 2167-2201
3. Cotruvo, J. A., Jr. and Stubbe, J. (2011) Class I ribonucleotide reductases: Metallocofactor assembly and repair in vitro and in vivo Annu. Rev. Biochem. 80, 733-767
4. Solomon, E. I., Brunold, T. C., Davis, M. I., Kemsley, J. N., Lee, S. K., Lehnert, N., Neese, F., Skulan, A. J., Yang, Y. S., and Zhou, J. (2000) Geometric and electronic structure/function correlations in non-heme iron enzymes Chem. Rev. 100, 235-349
5. Andrews, S. C. (2010) The ferritin-like superfamily: Evolution of the biological iron storeman from a rubrerythrin-like ancestor Biochim. Biophys. Acta 1800, 691-705
6. Atkin, C. L., Thelander, L., Reichard, P., and Lang, G. (1973) Iron and free radical in ribonucleotide reductase. Exchange of iron and Mössbauer spectroscopy of the protein β2 subunit of the Escherichia coli enzyme J. Biol. Chem. 248, 7464-7472
7. Jiang, W., Yun, D., Saleh, L., Barr, E. W., Xing, G., Hoffart, L. M., Maslak, M. A., Krebs, C., and Bollinger, J. M., Jr. (2007) A manganese(IV)/iron(III) cofactor in Chlamydia trachomatis ribonucleotide reductase Science 316, 1188-1191 (Pubitemid 46877480)
8. Jiang, W., Xie, J., Nørgaard, H., Bollinger, J. M., Jr., and Krebs, C. (2008) Rapid and quantitative activation of Chlamydia trachomatis ribonucleotide reductase by hydrogen peroxide Biochemistry 47, 4477-4483 (Pubitemid 351522097)
9. Stubbe, J. and Cotruvo, J. A., Jr. (2011) Control of metallation and active cofactor assembly in the class Ia and Ib ribonucleotide reductases: Diiron or dimanganese? Curr. Opin. Chem. Biol. 15, 284-290
10. Lundin, D., Torrents, E., Poole, A. M., and Sjöberg, B. M. (2009) RNRdb, a curated database of the universal enzyme family ribonucleotide reductase, reveals a high level of misannotation in sequences deposited to Genbank BMC Genomics 10, 589
11. Jordan, A., Pontis, E., Atta, M., Krook, M., Gibert, I., Barbé, J., and Reichard, P. (1994) A second class I ribonucleotide reductase in Enterobacteriaceae: Characterization of the Salmonella typhimurium enzyme Proc. Natl. Acad. Sci. U.S.A. 91, 12892-12896
12. Huque, Y., Fieschi, F., Torrents, E., Gibert, I., Eliasson, R., Reichard, P., Sahlin, M., and Sjöberg, B. M. (2000) The active form of the R2F protein of class Ib ribonucleotide reductase from Corynebacterium ammoniagenes is a diferric protein J. Biol. Chem. 275, 25365-25371
13. Cotruvo, J. A., Jr. and Stubbe, J. (2010) An active dimanganese(III)- tyrosyl radical cofactor in Escherichia coli class Ib ribonucleotide reductase Biochemistry 49, 1297-1309
14. Cox, N., Ogata, H., Stolle, P., Reijerse, E., Auling, G., and Lubitz, W. (2010) A tyrosyl-dimanganese coupled spin system is the native metalloradical cofactor of the R2F subunit of the ribonucleotide reductase of Corynebacterium ammoniagenes J. Am. Chem. Soc. 132, 11197-11213
15. •) involved in ribonucleotide reduction FEBS J. 277, 4849-4862
16. Cotruvo, J. A., Jr. and Stubbe, J. (2011) Escherichia coli class Ib ribonucleotide reductase contains a dimanganese(III)-tyrosyl radical cofactor in vivo Biochemistry 50, 1672-1681
17. Martin, J. E. and Imlay, J. A. (2011) The alternative aerobic ribonucleotide reductase of Escherichia coli, NrdEF, is a manganese-dependent enzyme that enables cell replication during periods of iron starvation Mol. Microbiol. 80, 319-334
18. Zhang, Y. and Stubbe, J. (2011) Bacillus subtilis class Ib ribonucleotide reductase is a dimanganese(III)-tyrosyl radical enzyme Biochemistry 50, 5615-5623
19. Cotruvo, J. A., Jr. and Stubbe, J. (2008) NrdI, a flavodoxin involved in maintenance of the diferric-tyrosyl radical cofactor in Escherichia coli class Ib ribonucleotide reductase Proc. Natl. Acad. Sci. U.S.A. 105, 14383-14388
20. Roca, I., Torrents, E., Sahlin, M., Gibert, I., and Sjöberg, B. M. (2008) NrdI essentiality for class Ib ribonucleotide reduction in Streptococcus pyogenes J. Bacteriol. 190, 4849-4858 (Pubitemid 351994314)
21. Boal, A. K., Cotruvo, J. A., Jr., Stubbe, J., and Rosenzweig, A. C. (2010) Structural basis for activation of class Ib ribonucleotide reductase Science 329, 1526-1530
22. Strand, K. R., Karlsen, S., Kolberg, M., Røhr, A. K., Görbitz, C. H., and Andersson, K. K. (2004) Crystal structural studies of changes in the native dinuclear iron center of ribonucleotide reductase protein R2 from mouse J. Biol. Chem. 279, 46794-46801 (Pubitemid 39518329)
23. Voegtli, W. C., Sommerhalter, M., Saleh, L., Baldwin, J., Bollinger, J. M., Jr., and Rosenzweig, A. C. (2003) Variable coordination geometries at the diiron(II) active site of ribonucleotide reductase R2 J. Am. Chem. Soc. 125, 15822-15830 (Pubitemid 37553699)
24. Högbom, M., Huque, Y., Sjöberg, B. M., and Nordlund, P. (2002) Crystal structure of the di-iron/radical protein of ribonucleotide reductase from Corynebacterium ammoniagenes Biochemistry 41, 1381-1389 (Pubitemid 34083794)
25. Eriksson, M., Jordan, A., and Eklund, H. (1998) Structure of Salmonella typhimurium NrdF ribonucleotide reductase in its oxidized and reduced forms Biochemistry 37, 13359-13369 (Pubitemid 28449581)
26. Uppsten, M., Davis, J., Rubin, H., and Uhlin, U. (2004) Crystal structure of the biologically active form of class Ib ribonucleotide reductase small subunit from Mycobacterium tuberculosis FEBS Lett. 569, 117-122 (Pubitemid 38844603)
27. Logan, D. T., Su, X. D., Aberg, A., Regnström, K., Hajdu, J., Eklund, H., and Nordlund, P. (1996) Crystal structure of reduced protein R2 of ribonucleotide reductase: The structural basis for oxygen activation at a dinuclear iron site Structure 4, 1053-1064 (Pubitemid 26369771)
28. Sazinsky, M. H. and Lippard, S. J. (2006) Correlating structure with function in bacterial multicomponent monooxygenases and related diiron proteins Acc. Chem. Res. 39, 558-566
29. Rardin, R. L., Tolman, W. B., and Lippard, S. J. (1991) Monodentate carboxylate complexes and the carboxylate shift: Implications for polymetalloprotein structure and function New J. Chem. 15, 417-430
30. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
31. McCoy, A. J., Grosse-Kunstleve, R. W., Storoni, L. C., and Read, R. J. (2005) Likelihood-enhanced fast translation functions Acta Crystallogr. D61, 458-464 (Pubitemid 43934606)
32. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132 (Pubitemid 41742764)
33. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255 (Pubitemid 27235885)
34. Laskowski, R. A. (1993) PROCHECK: A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
35. Chen, V. B., Arendall, W. B., III, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr. D66, 12-21
36. Delano, W. L. (2002) The PyMOL molecular graphics system, DeLano Scientific, San Carlos, CA.
37. Zwart, P. H., Afonine, P. V., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., McKee, E., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., Storoni, L. C., Terwilliger, T. C., and Adams, P. D. (2008) Automated structure solution with the PHENIX suite Methods Mol. Biol. 426, 419-435
38. Krissinel, E. and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D60, 2256-2268 (Pubitemid 41742778)
39. Atta, M., Nordlund, P., Aberg, A., Eklund, H., and Fontecave, M. (1992) Substitution of manganese for iron in ribonucleotide reductase from Escherichia coli J. Biol. Chem. 267, 20682-20688
40. Torrents, E., Sahlin, M., Biglino, D., Gräslund, A., and Sjöberg, B. M. (2005) Efficient growth inhibition of Bacillus anthracis by knocking out the ribonucleotide reductase tyrosyl radical Proc. Natl. Acad. Sci. U.S.A. 102, 17946-17951 (Pubitemid 41798482)
41. Johansson, R., Torrents, E., Lundin, D., Sprenger, J., Sahlin, M., Sjöberg, B. M., and Logan, D. T. (2010) High-resolution crystal structures of the flavoprotein NrdI in oxidized and reduced states: An unusual flavodoxin FEBS J. 277, 4265-4277
42. Uhlin, U. and Eklund, H. (1994) Structure of ribonucleotide reductase protein R1 Nature 370, 533-539 (Pubitemid 24264919)
43. Uppsten, M., Farnegardh, M., Domkin, V., and Uhlin, U. (2006) The first holocomplex structure of ribonucleotide reductase gives new insight into its mechanism of action J. Mol. Biol. 359, 365-377
44. Røhr, A. K., Hersleth, H. P., and Andersson, K. K. (2010) Tracking flavin conformations in protein crystal structures with Raman spectroscopy and QM/MM calculations Angew. Chem., Int. Ed. 49, 2324-2327
45. 2 reactivity J. Am. Chem. Soc. 122, 8495-8510
46. Tomter, A. B., Bell, C. B., III, Røhr, A. K., Andersson, K. K., and Solomon, E. I. (2008) Circular dichroism and magnetic circular dichroism studies of the biferrous site of the class Ib ribonucleotide reductase from Bacillus cereus: Comparison to the class Ia enzymes Biochemistry 47, 11300-11309
47. Andersson, M. E., Högbom, M., Rinaldo-Matthis, A., Andersson, K. K., Sjöberg, B. M., and Nordlund, P. (1999) The crystal structure of an azide complex of the diferrous R2 subunit of ribonucleotide reductase displays a novel carboxylate shift with important mechanistic implications for diiron-catalyzed oxygen activation J. Am. Chem. Soc. 121, 2346-2352 (Pubitemid 29153442)
48. Crona, M., Torrents, E., Røhr, A. K., Hofer, A., Furrer, E., Tomter, A. B., Andersson, K. K., Sahlin, M., and Sjöberg, B. M. (2011) NrdH-redoxin mediates high enzyme activity in manganese-reconstituted ribonucleotide reductase from Bacillus anthracis J. Biol. Chem. 286, 33053-33060
49. Landau, M., Mayrose, I., Rosenberg, Y., Glaser, F., Martz, E., Pupko, T., and Ben-Tal, N. (2005) ConSurf 2005: The projection of evolutionary conservation scores of residues on protein structures Nucleic Acids Res. 33, W299-W302