Metal binding and activity of ribonucleotide reductase protein R2 mutants: Conditions for formation of the mixed manganese-iron cofactor

Biochemistry

Volumn 48, Issue 27, 2009, Pages 6532-6539

  Popović Bijelić, Ana ^a   Voevodskaya, Nina ^a   Domkin, Vladimir ^b   Thelander, Lars ^b   Gräslund, Astrid ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHLAMYDIA TRACHOMATIS; COFACTOR; METAL BINDING; METAL CONTENT; RECOMBINANT PROTEIN; RIBONUCLEOTIDE REDUCTASE; SPECIFIC ACTIVITY; TYROSYL RADICALS; WILD TYPES;

AMINO ACIDS; BINDING SITES; ENZYME ACTIVITY; ESCHERICHIA COLI; IRON COMPOUNDS; MANGANESE; PROTEINS;

MANGANESE COMPOUNDS;

IRON; MANGANESE; MUTANT PROTEIN; RECOMBINANT PROTEIN; RIBONUCLEOTIDE REDUCTASE;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CATALYSIS; CHLAMYDIA TRACHOMATIS; ELECTRON SPIN RESONANCE; ENZYME ACTIVATION; ENZYME ACTIVITY; ESCHERICHIA COLI; METAL BINDING; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CHLAMYDIA TRACHOMATIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; IRON; MANGANESE; MICE; MUTATION; PROTEIN BINDING; RIBONUCLEOTIDE REDUCTASES; SPECTROMETRY, FLUORESCENCE;

CHLAMYDIA TRACHOMATIS; ESCHERICHIA COLI;

EID: 67650092935     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900693s     Document Type: Article

References (38)

1. Thelander, L., and Reichard, P. (1979) Ribonucleotide reductase. Annu. Rev. Biochem. 48, 133-158.
2. Sjöberg, B.-M., Reichard, P., Gräslund, A., and Ehrenberg, A. (1978) The tyrosine free radical in ribonucleotide reductase from Escherichia coli. J. Biol. Chem. 253, 6863-6865.
3. Gräslund, A., and Sahlin, M. (1996) Electron paramagnetic resonance and muclear magnetic resonance studies of class I ribonucleotide reductase. Annu. Rev. Biophys. Biomol. Struct. 25, 259-286.
4. 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. 103, 2167-2202.
5. Ḧogbom, M., Stenmark, P., Voevodskaya, N., McClarty, G., Gräslund, A., and Nordlund, P. (2004) The radical site in Chlamydial ribonucleotide reductase defines a new R2 subclass. Science 305, 245-248.
6. 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.
7. Voevodskaya, N., Lendzian, F., Ehrenberg, A., and Gräslund, A. (2007) High catalytic activity achieved with a mixed manganese-iron site in protein R2 of Chlamydia ribonucleotide reductase. FEBS Lett. 581, 3351-3355.
8. Roos, K., and Siegbahn, P. E. M. (2009) Density functional theory study of the manganese-containing ribonucleotide reductase from Chlamydia trachomatis: Why manganese is needed in the active complex. Biochemistry 48, 1878-1887.
9. Bollinger, J. M.Jr., Jiang, W., Green, M. T., and Krebs, C. (2008) The manganese(IV)/iron(III) cofactor of Chlamydia trachomatis ribonucleotide reductase: Structure, assembly, radical initiation, and evolution. Curr. Opin. Struct. Biol. 18, 650-657.
10. Voevodskaya, N., Lendzian, F., Sanganas, O., Grundmeier, A., Gräslund, A., and Haumann, M. (2009) Redox intermediates of the Mn-Fe site in subunit R2 of Chlamydia trachomatis ribonucleotide reductase. An X-ray absorption and EPR study. J. Biol. Chem. 284, 4555-4566.
11. Younker, J. M., Krest, C. M., Jinag, W., Krebs, C., Bollinger, J. M. Jr., and Green, M. T. (2008) Structural analysis of the Mn(IV)/Fe (III) cofactor of Chlamydia trachomatis ribonucleotide reductase by extended X-ray absorption fine structure spectroscopy and density functional theory calculations. J. Am. Chem. Soc. 130, 15022-15027.
12. Jiang, W., Saleh, L., Barr, E. W., Xie, J., Maslak Gardner, M., Krebs, C., and Bollinger, J. M.Jr. (2008) Branched activation- and catalysis-specific pathways for electron relay to the manganese/iron cofactor in ribonucleotide reductase from Chlamydia trachomatis. Biochemistry 47, 8477-8484.
13. Roschick, C., Iliffe-Lee, E. R., and McClarty, G. (2000) Cloning and characterization of ribonucleotide reductase from Chlamydia trachomatis. J. Biol. Chem. 275, 38111-38119.
14. Mann, G. J., Gräslund, A., Ochiai, E.-I., Ingemarson, R., and Thelander, L. (1991) Purification and characterization of recombinant mouse and herpes simplex virus ribonucleotide reductase R2 subunit. Biochemistry 30, 1939-1947.
15. Davis, R., Thelander, M., Mann, G. J., Behravan, G., Soucy, F., Beaulieu, P., Lavallee, P., Graslund, A., and Thelander, A. (1994) Purification, characterization, and localization of subunit interaction area of recombinant mouse ribonucleotide reductase R1 subunit. J. Biol. Chem. 269, 23171-23176.
16. Engström, Y., Eriksson, S., Thelander, L., and Åkerman, M. (1979) Ribonucleotide reductase from calf thymus. Purification and properties. Biochemistry 18, 2941-2948.
17. IV replacement of tyrosyl radical in a class I ribonucleotide reductase. Biochem. Biophys. Res. Commun. 330, 1213-1216.
18. Stoll, S., and Schweiger, A. (2006) EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. J. Magn. Reson. 178, 42-55.
19. Reed, G. H., and Markham, G. D. (1984) EPR of Mn(II) complexes with enzymes and other proteins. Biol. Magn. Reson. 6, 73-142.
20. Von Goldhammer, E., and Zorn, H. (1974) Electron paramagnetic resonance study of manganese ions bound to concanavalin A. Eur. J. Biochem. 44, 195-199.
21. Whiting, A. K., Boldt, Y. R., Hendrich, M. P., Wackett, L. P., and Que, L.Jr. (1996) Manganese(II)-dependent extradiol-cleaving catechol dioxygenase from Arthrobacter globiformis CM-2. Biochemistry 35, 160-170.
22. 1H-ENDOR and X-ray studies. Biochim. Biophys. Acta 1774, 1254-1263.
23. Cooperman, B. S. (2003) Oligopeptide inhibition of class I ribonucleotide reductases. Biopolymers 71, 117-131.
24. Kjoller-Larsen, I., Sjöberg, B.-M., and Thelander, L. (1982) Characterization of the Active Site of Ribonucleotide Reductase of Escherichia coli, Bacteriophage T4 and Mammalian Cells by Inhibition Studies with Hydroxyurea Analogues. Eur. J. Biochem. 125, 75-81.
25. Nyholm, S., Thelander, L., and Gräslund, A. (1993) Reduction and loss of the iron center in the reaction of the small subunit of mouse ribonucleotide reductase with hydroxyurea. Biochemistry 32, 11569-11574.
26. Thelander, L., Gräslund, A., and Thelander, M. (1983) Continual presence of oxygen and iron required for mammalian ribonucleotide reduction: Possible regulation mechanism. Biochem. Biophys. Res. Commun. 110, 859-865.
27. Henriksen, M. A., Cooperman, B. S., Salem, J. S., Li, L.-S., and Rubin, H. (1994) The Stable Tyrosyl Radical in Mouse Ribonucleotide Reductase Is Not Essential for Enzymic Activity. J. Am. Chem. Soc. 116, 9773-9774.
28. Pötsch, S., Lendzian, F., Ingemarson, R., Hörnberg, A., Thelander, L., Lubitz, W., Lassmann, G., and Gräslund, A. (1999) The Iron-Oxygen Reconstitution Reaction in Protein R2-Tyr-177 Mutants of Mouse Ribonucleotide Reductase. J. Biol. Chem. 274, 17696-17704.
29. Abragam, A., and Bleaney, B. (1970) Electron paramagnetic resonance of transition ions , Oxford University Press, London.
30. 31P pulsed ENDOR and ESE-EPR. J. Am. Chem. Soc. 127, 8310-8319.
31. De Vos, D. E., Weckhuysen, B. M., and Bein, T. (1996) ESR fine strucutre of manganese ions in zeolite A detects strong variations of the coordination environment. J. Am. Chem. Soc. 118, 9615-9622.
32. Golombek, A. P., and Hendrich, M. P. (2003) Quantitative analysis of dinuclear manganese(II) EPR spectra. J. Magn. Reson. 165, 33-48.
33. Yévenes, A., González-Nilo, F. D., and Cardemil, E. (2007) Relevance of phenylalanine 216 in the affinity of Saccharomyces cerevisiae phosphoenolpyruvate carboxykinase for Mn(II). Protein J. 26, 135-141.
34. Käss, H., MacMillan, F., Ludwig, B., and Prisner, T. F. (2000) Investigation of the Mn binding site in cytochrome c oxidase from Paracoccus denitrificans by high-frequency EPR. J. Phys. Chem B 104, 5362-5371.
35. Chang, C. H., Svedruzić, D., Ozarowski, A., Walker, L., Yeagle, G., Britt, R. D., Angerhofer, A., and Richards, N. G. J. (2004) EPR Spectroscopic Characterization of the Manganese Center and a Free Radical in the Oxalate Decarboxylase Reaction. J. Biol. Chem. 279, 52840-52849.
36. Frausto da Silva, J. J. R., and Williams, R. J. P. (2006) The biological chemistry of the elements. The inorganic chemistry of life , 2nd ed., Oxford University Press, London.
37. Yévenes, A., Espinoza, R., Rivas-Pardo, J. A., Villarreal, J. M., González-Nilo, F. D., and Cardemil, E. (2006) Site-directed mutagenesis study of the microenvironment characteristics of Lys213 of Saccharomyces cerevisiae phosphoenolpyruvate carboxykinase. Biochimie 88, 663-672.
38. Andersson, C. S., and Högbom, M. (2009) A Mycobacterium tuberculosis ligand-binding Mn/Fe protein reveals a new cofactor in a remodeled R2-protein scaffold. Proc. Natl. Acad. Sci. U.S.A. 106, 5633-5638.