Crystal structure of Bacillus cereus class Ib ribonucleotide reductase di-iron NrdF in complex with NrdI

ACS Chemical Biology

Volumn 9, Issue 2, 2014, Pages 526-537

  Hammerstad, Marta ^a   Hersleth, Hans Petter ^a   Tomter, Ane B ^a   Røhr, Åsmund K ^a   Andersson, K Kristoffer ^a  

^a UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLIC ACID; HOLOENZYME; IRON; METAL ION; RADICAL; RIBONUCLEOTIDE; RIBONUCLEOTIDE REDUCTASE; WATER;

ARTICLE; BACILLUS CEREUS; CRYSTAL STRUCTURE; DISSOCIATION; ESCHERICHIA COLI; GEOMETRY; NONHUMAN; PRIORITY JOURNAL;

BACILLUS CEREUS; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; FLAVOPROTEINS; MOLECULAR DOCKING SIMULATION; PROTEIN BINDING; PROTEIN CONFORMATION; RIBONUCLEOTIDE REDUCTASES;

EID: 84896727015     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400757h     Document Type: Article

References (61)

1. Nordlund, N. and Reichard, P. (2006) Ribonucleotide reductases Annu. Rev. Biochem. 75, 681-706
2. Tomter, A. B., Zoppellaro, G., Andersen, N. H., Hersleth, H. P., Hammerstad, M., Rohr, A. K., Sandvik, G. K., Strand, K. R., Nilsson, G. E., Bell, C. B., Barra, A. L., Blasco, E., Le Pape, L., Solomon, E. I., and Andersson, K. K. (2013) Ribonucleotide reductase class I with different radical generating clusters Coord. Chem. Rev. 257, 3-26
3. Andersson, K. K., Ed. (2008) Ribonucleotide Reductase, Nova Science Publishers, Inc., Hauppauge, NY.
4. Cotruvo, J. A. and Stubbe, J. (2011) Class I ribonucleotide reductases: Metallocofactor assembly and repair in vitro and in vivo Annu. Rev. Biochem. 80, 733-767
5. Tomter, A. B., Zoppellaro, G., Schmitzberger, F., Andersen, N. H., Barra, A. L., Engman, H., Nordlund, P., and Andersson, K. K. (2011) HF-EPR, Raman, UV/VIS light spectroscopic, and DFT studies of the ribonucleotide reductase R2 tyrosyl radical from Epstein-Barr virus PLoS One 6, e25022
6. Kolberg, M., Strand, K. R., Graff, P., and Andersson, K. K. (2004) Structure, function, and mechanism of ribonucleotide reductases Biochim. Biophys. Acta, Proteins Proteomics 1699, 1-34
7. Atkin, C. L., Thelander, L., Reichard, P., and Lang, G. (1973) Iron and free-radical in ribonucleotide reductase-exchange of iron and mossbauer-spectroscopy of protein-b2 subunit of Escherichia-coli enzyme J. Biol. Chem. 248, 7464-7472
8. Jiang, W., Yun, D., Saleh, L., Barr, E. W., Xing, G., Hoffart, L. M., Maslak, M. A., Krebs, C., and Bollinger, J. M. (2007) A manganese(IV)/iron(III) cofactor in Chlamydia trachomatis ribonucleotide reductase Science 316, 1188-1191
9. Hogbom, M., Stenmark, P., Voevodskaya, N., McClarty, G., Graslund, A., and Nordlund, P. (2004) The radical site in chlamydial ribonucleotide reductase defines a new R2 subclass Science 305, 245-248
10. Roshick, C., Iliffe-Lee, E. R., and McClarty, G. (2000) Cloning and characterization of ribonucleotide reductase from Chlamydia trachomatis J. Biol. Chem. 275, 38111-38119
11. Voevodskaya, N., Lendzian, F., Ehrenberg, A., and Graslund, A. (2007) High catalytic activity achieved with a mixed manganese-iron site in protein R2 of Chlamydia ribonucleotide reductase FEBS Lett. 581, 3351-3355
12. Lundin, D., Torrents, E., Poole, A. M., and Sjoberg, 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
13. 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
14. Uhlin, U. and Eklund, H. (1994) Structure of ribonucleotide reductase protein R1 Nature 370, 533-539
15. Logan, D. T. (2011) Closing the circle on ribonucleotide reductases Nat. Struct. Mol. Biol. 18, 251-253
16. Jordan, A., Pontis, E., Atta, M., Krook, M., Gibert, I., Barbe, J., and Reichard, P. (1994) A 2nd class-I ribonucleotide reductase in enterobacteriaceae-characterization of the Salmonella-typhimurium enzyme Proc. Natl. Acad. Sci. U.S.A. 91, 12892-12896
17. Huque, Y., Fieschi, F., Torrents, E., Gibert, I., Eliasson, R., Reichard, P., Sahlin, M., and Sjoberg, 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
18. Cotruvo, J. A. and Stubbe, J. (2010) An active dimanganese(III)-tyrosyl radical cofactor in Escherichia coli class Ib ribonucleotide reductase Biochemistry 49, 1297-1309
19. 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
20. Tomter, A. B., Zoppellaro, G., Bell, C. B., Barra, A. L., Andersen, N. H., Solomon, E. I., and Andersson, K. K. (2012) Spectroscopic studies of the iron and manganese reconstituted tyrosyl radical in Bacillus cereus ribonucleotide reductase R2 protein PLoS One 7, e33436
21. Cotruvo, J. A. 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
22. Johansson, R., Torrents, E., Lundin, D., Sprenger, J., Sahlin, M., Sjoberg, 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
23. Rohr, 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
24. Cotruvo, J. A. and Stubbe, J. (2011) Escherichia coli class Ib ribonucleotide reductase contains a dimanganese(III)-tyrosyl radical cofactor in vivo Biochemistry 50, 1672-1681
25. Boal, A. K., Cotruvo, J. A., Stubbe, J., and Rosenzweig, A. C. (2010) Structural basis for activation of class Ib ribonucleotide reductase Science 329, 1526-1530
26. Cotruvo, J. A., Stich, T. A., Britt, D. R., and Stubbe, J. (2013) Mechanism of assembly of the dimanganese-tyrosyl radical cofactor of class Ib ribonucleotide reductase: Enzymatic generation of superoxide is required for tyrosine oxidation via a Mn(III)Mn(IV) intermediate J. Am. Chem. Soc. 135, 4027-4039
27. Crona, M., Torrents, E., Rohr, A. K., Hofer, A., Furrer, E., Tomter, A. B., Andersson, K. K., Sahlin, M., and Sjoberg, B. M. (2011) NrdH-Redoxin protein mediates high enzyme activity in manganese-reconstituted ribonucleotide reductase from Bacillus anthracis J. Biol. Chem. 286, 33053-33060
28. Tomter, A. B. (2010) Spectroscopic Studies of the Ribonucleotide Reductase R2-subunit from Mammals, Virus, and Bacteria, In Faculty of Mathematics and Natural Sciences, Univeristy of Oslo, Oslo, Norway.
29. Zhang, Y. and Stubbe, J. (2011) Bacillus subtilis class Ib ribonucleotide reductase is a dimanganese(III)-tyrosyl radical enzyme Biochemistry 50, 5615-5623
30. Hogbom, M., Huque, Y., Sjoberg, B. M., and Nordlund, P. (2002) Crystal structure of the di-iron/radical protein of ribonucleotide reductase from Corynebacterium ammoniagenes Biochemistry 41, 1381-1389
31. 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
32. Uppsten, M., Davis, J., Rubin, H., and Uhlin, U. (2004) Crystal structure of the biologically active form of class 1b ribonucleotide reductase small subunit from Mycobacterium tuberculosis FEBS Lett. 569, 117-122
33. Boal, A. K., Cotruvo, J. A., Stubbe, J., and Rosenzweig, A. C. (2012) The dimanganese(II) site of Bacillus subtilis class Ib ribonucleotide reductase Biochemistry 51, 3861-3871
34. Henderson, R. (1990) Cryoprotection of protein crystals against radiation-damage in electron and x-ray-diffraction Proc. R. Soc. London, Ser. B 241, 6-8
35. Hersleth, H.-P. and Andersson, K. K. (2011) How different oxidation states of crystalline myoglobin are influenced by X-rays Biochim. Biophys. Acta, Proteins Proteomics 1814, 785-796
36. Griese, J. J. and Hogbom, M. (2012) X-ray reduction correlates with soaking accessibility as judged from four non-crystallographically related diiron sites Metallomics 4, 894-898
37. Sigfridsson, K. G. V., Chernev, P., Leidel, N., Popovic-Bijelic, A., Graslund, A., and Haumann, M. (2013) Rapid X-ray photoreduction of dimetal-oxygen cofactors in ribonucleotide reductase J. Biol. Chem. 288, 9648-9661
38. Tomter, A. B., Bell, C. B., Rohr, 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
39. Strand, K. R., Karlsen, S., Kolberg, M., Rohr, A. K., Gorbitz, 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
40. Ubbink, M. (2012) Dynamics in transient complexes of redox proteins Biochem. Soc. Trans. 40, 415-418
41. Nordlund, P. and Eklund, H. (1993) Structure and function of the Escherichia-coli ribonucleotide reductase protein R2 J. Mol. Biol. 232, 123-164
42. Smith, P., Zhou, B. S., Ho, N., Yuan, Y. C., Su, L., Tsai, S. C., and Yen, Y. (2009) 2.6 Angstrom X-ray crystal structure of human p53R2, a p53-inducible ribonucleotide reductase Biochemistry 48, 11134-11141
43. Wilmot, C. M., Sjogren, T., Carlsson, G. H., Berglund, G. I., and Hajdu, J. (2002) Defining redox state of X-ray crystal structures by single-crystal ultraviolet-visible microspectrophotometry Methods Enzymol. 353, 301-318
44. Rofougaran, R., Crona, M., Vodnala, M., Sjoberg, B. M., and Hofer, A. (2008) Oligomerization status directs overall activity regulation of the Escherichia coli class Ia ribonucleotide reductase J. Biol. Chem. 283, 35310-35318
45. 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
46. Ando, N., Brignole, E. J., Zimanyi, C. M., Funk, M. A., Yokoyama, K., Asturias, F. J., Stubbe, J., and Drennan, C. L. (2011) Structural interconversions modulate activity of Escherichia coli ribonucleotide reductase Proc. Natl. Acad. Sci. U.S.A. 108, 21046-21051
47. Magnusson, K. E. and Edebo, L. (1976) Influence of cell concentration, temperature, and press performance on flow characterics and disintefration in freeze-pressing of Saccharomycescerevisiae with X-press Biotechnol. Bioeng. 18, 865-883
48. Powell, H. R. (1999) The Rossmann Fourier autoindexing algorithm in MOSFLM Acta Crystallogr., Sect. D: Biol. Crystallogr. 55, 1690-1695
49. Evans, P. (2006) Scaling and assessment of data quality Acta Crystallogr., Sect. D: Biol. Crystallogr. 62, 72-82
50. Evans, P. R. (2011) An introduction to data reduction: space-group determination, scaling and intensity statistics Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 282-292
51. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G. W., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 235-242
52. McCoy, A. J., Grosse-Kunstleve, R. W., Storoni, L. C., and Read, R. J. (2005) Likelihood-enhanced fast translation functions Acta Crystallogr., Sect. D: Biol. Crystallogr. 61, 458-464
53. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling Bioinformatics 22, 195-201
54. Kiefer, F., Arnold, K., Kunzli, M., Bordoli, L., and Schwede, T. (2009) The SWISS-MODEL Repository and associated resources Nucleic Acids Res. 37, D387-D392
55. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255
56. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132
57. Murray, J. W., Garman, E. F., and Ravelli, R. B. G. (2004) X-ray absorption by macromolecular crystals: the effects of wavelength and crystal composition on absorbed dose J. Appl. Crystallogr. 37, 513-522
58. Paithankar, K. S., Owen, R. L., and Garman, E. F. (2009) Absorbed dose calculations for macromolecular crystals: improvements to RADDOSE J. Synchrotron Radiat. 16, 152-162
59. Delano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
60. Ho, B. K. and Gruswitz, F. (2008) HOLLOW: Generating accurate representations of channel and interior surfaces in molecular structures BMC Struct. Biol. 8, 49
61. Owen, R. L., Pearson, A. R., Meents, A., Boehler, P., Thominet, V., and Schulze-Briese, C. (2009) A new on-axis multimode spectrometer for the macromolecular crystallography beamlines of the Swiss Light Source J. Synchrotron Radiat. 16, 173-182