Spectroscopic studies of the iron and manganese reconstituted tyrosyl radical in bacillus cereus ribonucleotide reductase R2 protein

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Tomter, Ane B ^a   Zoppellaro, Giorgio ^a   Bell III, Caleb B ^b   Barra, Anne Laure ^c   Andersen, Niels H ^a   Solomon, Edward I ^b   Andersson, K Kristoffer ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b STANFORD UNIVERSITY   (United States)

^c GRENOBLE HIGH MAGNETIC FIELD LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DEUTERIUM OXIDE; HYDROGEN; IRON; MANGANESE; OXYGEN; OXYGEN 18; PROTEIN R2; RADICAL; RIBONUCLEOTIDE REDUCTASE; TYROSYL RADICAL; UNCLASSIFIED DRUG; FREE RADICAL; RIBONUCLEOTIDE REDUCTASE R2 SUBUNIT; TYROSINE;

ARTICLE; BACILLUS CEREUS; CHEMICAL INTERACTION; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ESCHERICHIA COLI; HYDROGEN BOND; MICROWAVE RADIATION; NONHUMAN; RADICAL REACTION; RAMAN SPECTROMETRY; ANIMAL; CHEMISTRY; ENZYMOLOGY; METABOLISM; MOUSE; TEMPERATURE; ULTRAVIOLET SPECTROPHOTOMETRY;

BACILLUS CEREUS;

ANIMALS; BACILLUS CEREUS; ELECTRON SPIN RESONANCE SPECTROSCOPY; FREE RADICALS; IRON; MANGANESE; MICE; MICROWAVES; RIBONUCLEOTIDE REDUCTASES; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTRUM ANALYSIS, RAMAN; TEMPERATURE; TYROSINE;

EID: 84858231124     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033436     Document Type: Article

References (77)

1. Andersson KK, eds. (2008) Ribonucleotide reductase Hauppauge NY, USA Nova Science publishers, Inc.
2. Jordan A, Reichard P, (1998) Ribonucleotide reductases. Annu Rev Biochem 67: 71-98.
3. Reichard P, (1993) From RNA to DNA, Why So Many Ribonucleotide Reductases. Science 260: 1773-1777.
4. Eklund H, Uhlin U, Farnegardh M, Logan DT, Nordlund P, (2001) Structure and function of the radical enzyme ribonucleotide reductase. Prog Biophys Mol Biol 77: 177-268.
5. Nordlund P, Reichard P, (2006) Ribonucleotide reductases. Annu Rev Biochem 75: 681-706.
6. Shao J, Zhou B, Chu B, Yen Y, (2006) Ribonucleotide reductase inhibitors and future drug design. Current Cancer Drug Targets 6: 409-431.
7. Andersson KK, Graslund A, (1995) Diiron-oxygen proteins. Adv Inorg Chem 43: 359-408.
8. Rofougaran R, Vodnala M, Hofer A, (2006) Enzymatically active mammalian ribonucleotide reductase exists primarily as an alpha(6)beta(2) octamer. J Biol Chem 281: 27705-27711.
9. Fairman JW, Wijerathna SR, Ahmad MF, Xu H, Nakano R, et al. (2011) Structural basis for allosteric regulation of human ribonucleotide reductase by nucleotide-induced oligomerization. Nat Struct Mol Biol 18: 316-322.
10. Bollinger JM, Tong WH, Ravi N, Huynh BH, Edmondson DE, et al. (1995) Use of Rapid Kinetics Methods to Study the Assembly of the Diferric-Tyrosyl Radical Cofactor of Escherichia coli Ribonucleotide Reductase. Meth Enzymol 258: 278-303.
11. Tong WH, Chen S, Lloyd SG, Edmondson DE, Huynh BH, et al. (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.
12. Kolberg M, Strand KR, Graff P, Andersson KK, (2004) Structure, function, and mechanism of ribonucleotide reductases. Biochim Biophys Acta 1699: 1-34.
13. Rova U, Goodtzova K, Ingemarson R, Behravan G, Graslund A, et al. (1995) Evidence by Site-Directed Mutagenesis Supports Long-Range Electron-Transfer in Mouse Ribonucleotide Reductase. Biochemistry 34: 4267-4275.
14. Sjoberg BM, (1997) Ribonucleotide reductases- A group of enzymes with different metallosites and a similar reaction mechanism. Structure and Bonding 88: 139-173.
15. Hogbom M, Stenmark P, Voevodskaya N, McClarty G, Graslund A, et al. (2004) The radical site in chlamydial ribonucleotide reductase defines a new R2 subclass. Science 305: 245-248.
16. Jiang W, Yun D, Saleh L, Barr EW, Xing G, et al. (2007) A manganese(IV)/iron(III) cofactor in Chlamydia trachomatis ribonucleotide reductase. Science 316: 1188-1191.
17. Huque Y, Fieschi F, Torrents E, Gibert I, Eliasson R, et al. (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. Sjoberg BM, (2010) A Never-Ending Story. Science 329: 1475-1476.
19. Willing A, Follmann H, Auling G, (1988) Ribonucleotide Reductase of Brevibacterium-Ammoniagenes Is a Manganese Enzyme. Eur J Biochem 170: 603-611.
20. Cotruvo JA, Stubbe J, (2010) An Active Dimanganese(III)-Tyrosyl Radical Cofactor in Escherichia coli Class Ib Ribonucleotide Reductase. Biochemistry 49: 1297-1309.
21. Cotruvo JA, 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 USA 105: 14383-14388.
22. Zhang Y, Stubbe J, (2011) Bacillus subtilis Class Ib Ribonucleotide Reductase is a Dimanganese(III)-Tyrosyl Radical Enzyme. Biochemistry 50: 5615-5623.
23. Boal AK, Cotruvo JA, Stubbe J, Rosenzweig AC, (2010) Structural Basis for Activation of Class Ib Ribonucleotide Reductase. Science 329: 1526-1530.
24. Rohr AK, Hersleth HP, Andersson KK, (2010) Tracking Flavin Conformations in Protein Crystal Structures with Raman Spectroscopy and QM/MM Calculations. Angewandte Chemie-International Edition 49: 2324-2327.
25. Johansson R, Torrents E, Lundin D, Sprenger J, Sahlin M, et al. (2010) High-resolution crystal structures of the flavoprotein NrdI in oxidized and reduced states - an unusual flavodoxin. FEBS J 277: 4265-4277.
26. Cox N, Ogata H, Stolle P, Reijerse E, Auling G, et al. (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.
27. Jiang W, Bollinger JM, Krebs C, (2007) The active form of Chlamydia trachomatis ribonucleotide reductase R2 protein contains a heterodinuclear Mn(IV)/Fe(III) cluster with S = 1 ground state. J Am Chem Soc 129: 7504-7505.
28. Jiang W, Hoffart LM, Krebs C, Bollinger JM, (2007) A manganese(IV)/iron(IV) intermediate in assembly of the manganese(IV)/iron(III) cofactor of Chlamydia trachomatis ribonucleotide reductase. Biochemistry 46: 8709-8716.
29. Voevodskaya N, Lendzian F, Ehrenberg A, Graslund A, (2007) High catalytic activity achieved with a mixed manganese-iron site in protein R2 of Chlamydia ribonucleotide reductase. FEBS Letters 581: 3351-3355.
30. Ehling-Schulz M, Fricker M, Scherer S, (2004) Bacillus cereus, the causative agent of an emetic type of food-borne illness. Molecular Nutrition & Food Research 48: 479-487.
31. Gallicchio VS, (2005) Ribonucleotide reductase: target therapy for human disease. Expert Opin Ther Pat 15: 659-673.
32. Nocentini G, (1996) Ribonucleotide reductase inhibitors: New strategies for cancer chemotherapy. Crit Rev Oncol Hemat 22: 89-126.
33. Allard P, Barra AL, Andersson KK, Schmidt PP, Atta M, et al. (1996) Characterization of a new tyrosyl free radical in Salmonella typhimurium ribonucleotide reductase with EPR at 9.45 and 245 GHz. J Am Chem Soc 118: 895-896.
34. Andersson KK, Barra AL, (2002) The use of high field/frequency EPR in studies of radical and metal sites in proteins and small inorganic models. Spectrochimica Acta Part a-Molecular and Biomolecular Spectroscopy 58: 1101-1112.
35. Torrents E, Sahlin M, Biglino D, Graslund A, Sjoberg BM, (2005) Efficient growth inhibition of Bacillus anthracis by knocking out the ribonucleotide reductase tyrosyl radical. Proc Natl Acad Sci USA 102: 17946-17951.
36. Lundin D, Torrents E, Poole AM, Sjoberg BM, (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: 1-8.
37. Tomter AB, Bell CB, Rohr AK, Andersson KK, Solomon EI, (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.
38. Rohr AK, (2010) Structural and Spectroscopic Studies of the Flavoprotein NrdI, Thioredoxin BC3987, and Ribonucleotide Reductase Diiron-Protein R2 [Dissertation] Oslo, Norway University of Oslo.
39. Pace CN, Vajdos F, Fee L, Grimsley G, Gray T, (1995) How to Measure and Predict the Molar Absorption-Coefficient of a Protein. Protein Science 4: 2411-2423.
40. Hanson MA, Schmidt PP, Strand KR, Graslund A, Solomon EI, et al. (1999) Resonance Raman evidence for a hydrogen-bonded oxo bridge in the R2 protein of ribonucleotide reductase from mouse. J Am Chem Soc 121: 6755-6756.
41. Castner TG, (1959) Saturation of the Paramagnetic Resonance of a V-Center. Physical Review 115: 1506-1515.
42. Portis AM, (1953) Electronic Structure of F-Centers- Saturation of the Electron Spin Resonance. Physical Review 91: 1071-1078.
43. Zoppellaro G, Harbitz E, Kaur R, Ensign AA, Bren KL, et al. (2008) Modulation of the Ligand-Field Anisotropy in a Series of Ferric Low-Spin Cytochrome c Mutants derived from Pseudomonas aeruginosa Cytochrome c-551 and Nitrosomonas europaea Cytochrome c-552: A Nuclear Magnetic Resonance and Electron Paramagnetic Resonance Study. J Am Chem Soc 130: 15348-15360.
44. Galli C, Innes JB, Hirsh DJ, Brudvig GW, (1996) Effects of dipole-dipole interactions on microwave progressive power saturation of radicals in proteins. J Magn Reson Ser B 110: 284-287.
45. Hirsh DJ, Brudvig GW, (2007) Measuring distances in proteins by saturation-recovery EPR. Nat Protoc 2: 1770-1781.
46. Makinen MW, Wells GB, (1987) Metal Ions in Biological Systems New York, NY Marcel Dekker pp. 129-205 (1987) In:.
47. Himo F, Graslund A, Eriksson LA, (1997) Density functional calculations on model tyrosyl radicals. Biophys J 72: 1556-1567.
48. Svistunenko DA, Cooper CE, (2004) A new method of identifying the site of tyrosyl radicals in proteins. Biophys J 87: 582-595.
49. Barra AL, Graslund A, Andersson KK, (2004) The use of very high frequency EPR (VHF-EPR) in studies in proteins and small inorganic models. Biol Magn Reson 22: 145-164.
50. McCreery RL, eds. (2000) Raman Spectroscopy for Chemical Analysis New York Wiley.
51. Schmidt PP, Andersson KK, Barra AL, Thelander L, Graslund A, (1996) High field EPR studies of mouse ribonucleotide reductase indicate hydrogen bonding of the tyrosyl radical. J Biol Chem 271: 23615-23618.
52. Andersson KK, Schmidt PP, Katterle B, Strand KR, Palmer AE, et al. (2003) Examples of high-frequency EPR studies in bioinorganic chemistry. J Biol Inorg Chem 8: 235-247.
53. Sjoberg BM, Reichard P, Graslund A, Ehrenberg A, (1978) Tyrosine Free-Radical in Ribonucleotide Reductase from Escherichia-Coli. J Biol Chem 253: 6863-6865.
54. Gerfen GJ, Bellew BF, Un S, Bollinger JM, Stubbe J, et al. (1993) High-Frequency (139.5 Ghz) Epr Spectroscopy of the Tyrosyl Radical in Escherichia-Coli Ribonucleotide Reductase. J Am Chem Soc 115: 6420-6421.
55. van Dam PJ, Willems JP, Schmidt PP, Potsch S, Barra AL, et al. (1998) High-frequency EPR and pulsed Q-Band ENDOR studies on the origin of the hydrogen bond in tyrosyl radicals of ribonucleotide reductase R2 proteins from mouse and herpes simplex virus type 1. J Am Chem Soc 120: 5080-5085.
56. Liu A, Potsch S, Davydov A, Barra AL, Rubin H, et al. (1998) The tyrosyl free radical of recombinant ribonucleotide reductase from Mycobacterium tuberculosis is located in a rigid hydrophobic pocket. Biochemistry 37: 16369-16377.
57. Dorlet P, Rutherford AW, Un S, (2000) Orientation of the tyrosyl D, pheophytin anion, and semiquinone Q(A)(center dot-) radicals in photosystem II determined by high-field electron paramagnetic resonance. Biochemistry 39: 7826-7834.
58. Hoganson CW, Sahlin M, Sjoberg BM, Babcock GT, (1996) Electron magnetic resonance of the tyrosyl radical in ribonucleotide reductase from Escherichia coli. J Am Chem Soc 118: 4672-4679.
59. Svistunenko DA, Jones GA, (2009) Tyrosyl radicals in proteins: a comparison of empirical and density functional calculated EPR parameters. Phys Chem Chem Phys 11: 6600-6613.
60. Un S, (2005) The g-values and hyperfine coupling of amino acid radicals in proteins: comparison of experimental measurements with ab initio calculations. Magn Reson Chem 43: S229-S236.
61. Sahlin M, Petersson L, Graslund A, Ehrenberg A, Sjoberg BM, et al. (1987) Magnetic Interaction between the Tyrosyl Free-Radical and the Antiferromagnetically Coupled Iron Center in Ribonucleotide Reductase. Biochemistry 26: 5541-5548.
62. Galli C, Atta M, Andersson KK, Graslund A, Brudvig GW, (1995) Variations of the Diferric Exchange Coupling in the R2-Subunit of Ribonucleotide Reductase from 4 Species as Determined by Saturation- Recovery Epr Spectroscopy. J Am Chem Soc 117: 740-746.
63. Eriksson M, Jordan A, Eklund H, (1998) Structure of Salmonella typhimurium nrdF ribonucleotide reductase in its oxidized and reduced forms. Biochemistry 37: 13359-13369.
64. Hogbom M, Huque Y, Sjoberg BM, Nordlund P, (2002) Crystal structure of the di-iron/radical protein of ribonucleotide reductase from Corynebacterium ammoniagenes. Biochemistry 41: 1381-1389.
65. Strand KR, Karlsen S, Kolberg M, Rohr AK, Gorbitz CH, et al. (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.
66. Uppsten M, Davis J, Rubin H, Uhlin U, (2004) Crystal structure of the biologically active form of class 1b ribonucleotide reductase small subunit from Mycobacterium tuberculosis. FEBS Letters 569: 117-122.
67. Offenbacher AR, Vassiliev IR, Seyedsayamdost MR, Stubbe J, Barry BA, (2009) Redox-Linked Structural Changes in Ribonucleotide Reductase. J Am Chem Soc 131: 7496-7497.
68. Hogbom M, Galander M, Andersson M, Kolberg M, Hofbauer W, et al. (2003) Displacement of the tyrosyl radical cofactor in ribonucleotide reductase obtained by single-crystal high-field EPR and 1.4-angstrom x-ray data. Proc Natl Acad Sci USA 100: 3209-3214.
69. Galander M, Uppsten M, Uhlin U, Lendzian F, (2006) Orientation of the tyrosyl radical in Salmonella typhimurium class Ib ribonucleotide reductase determined by high field EPR of R2F single crystals. J Biol Chem 281: 31743-31752.
70. Wilson EB, (1934) The normal modes and frequencies of vibration of the regular plane hexagon model of the benzene molecule. Physical Review 45: 0706-0714.
71. Tomter AB, Zoppellaro G, Schmitzberger F, Andersen NH, Barra A-L, et al. (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.
72. Backes G, Sahlin M, Sjoberg BM, Loehr TM, Sandersloehr J, (1989) Resonance Raman-Spectroscopy of Ribonucleotide Reductase- Evidence for a Deprotonated Tyrosyl Radical and Photochemistry of the Binuclear Iron Center. Biochemistry 28: 1923-1929.
73. Atta M, Andersson KK, Ingemarson R, Thelander L, Graslund A, (1994) Epr Studies of Mixed-Valent [(Fefeiii)-Fe-Ii] Clusters Formed in the R2 Subunit of Ribonucleotide Reductase from Mouse or Herpes-Simplex Virus- Mild Chemical-Reduction of the Diferric Centers. J Am Chem Soc 116: 6429-6430.
74. Davydov RM, Davydov A, Ingemarson R, Thelander L, Ehrenberg A, et al. (1997) EPR study of the mixed-valent diiron sites in mouse and herpes simplex virus ribonucleotide reductases. Effect of the tyrosyl radical on structure and reactivity of the diferric center. Biochemistry 36: 9093-9100.
75. Tomter AB, (2010) Spectroscopic Studies of the Ribonucleotide Reductase R2-subunits from Mammals, Virus and Bacteria Oslo, Norway University of Oslo.
76. Crona M, Torrents E, Rohr AK, Hofer A, Furrer E, et al. (2011) NrdH-Redoxin Protein Mediates High Enzyme Activity in Manganese-reconstituted Ribonucleotide Reductase from Bacillus anthracis. J Biol Chem 286: 33053-33060.
77. Un S, Gerez C, Elleingand E, Fontecave M, (2001) Sensitivity of tyrosyl radical g-values to changes in protein structure: A high-field EPR study of mutants of ribonucleotide reductase. J Am Chem Soc 123: 3048-3054.