In Situ determination of manganese(II) speciation in deinococcus radiodurans by high magnetic field EPR: Detection of high levels of Mn(II) Bound to proteins

Journal of Biological Chemistry

Volumn 288, Issue 7, 2013, Pages 5050-5055

  Tabares, Leandro C ^a   Un, Sun ^a  

^a SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DEINOCOCCUS RADIODURANS; HIGH MAGNETIC FIELDS; INTACT CELLS; MANGANESE SUPEROXIDE DISMUTASE; SUPEROXIDES;

MANGANESE COMPOUNDS; OXYGEN;

MANGANESE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; FRUCTOSE 1,6 BISPHOSPHATE; FRUCTOSE 6 PHOSPHATE; GLUCOSE 6 PHOSPHATE; HISTIDINE; MANGANESE; MANGANESE SUPEROXIDE DISMUTASE; METAL COMPLEX; NUCLEOTIDE; PHOSPHATE; PYROPHOSPHATE;

ARTICLE; BACTERIAL CELL; CELL GROWTH; CELL LEVEL; CELLULAR PARAMETERS; CHEMICAL REACTION; CONTROLLED STUDY; DEINOCOCCUS RADIODURANS; ELECTRON SPIN RESONANCE; EXPONENTIAL PHASE; HYPERFINE COUPLING; MAGNETIC FIELD; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; SPECIES DIFFERENTIATION; STATIONARY PHASE;

DEINOCOCCUS; DNA; ELECTRON SPIN RESONANCE SPECTROSCOPY; HOMEOSTASIS; IONS; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MANGANESE; NUCLEOTIDES; OXIDATIVE STRESS; PHOSPHATES; PROTEIN BINDING; SUPEROXIDE DISMUTASE; SUPEROXIDES; TIME FACTORS;

EID: 84874064256     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.C112.444992     Document Type: Article

References (36)

1. Daly, M. J. (2009) A new perspective on radiation resistance based on Deinococcus radiodurans. Nat. Rev. Microbiol. 7, 237-245
2. Slade, D., and Radman, M. (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol. Mol. Biol. Rev. 75, 133-191
3. Blasius, M., Sommer, S., and Hübscher, U. (2008) Deinococcus radiodurans: what belongs to the survival kit? Crit. Rev. Biochem. Mol. Biol. 43, 221-238
4. Cox, M. M., and Battista, J. R. (2005) Deinococcus radiodurans - the consummate survivor. Nat. Rev. Microbiol. 3, 882-892
5. Leibowitz, P. J., and Schwartzberg., L. S., and Bruce, A. K. (1976) The in vivo association of manganese with the chromosome of micrococcus radiodurans. Photochem. Photobiol. 23, 45-50
6. Daly, M. J., and Gaidamakova., E. K., Matrosova, V. Y., Vasilenko, A., Zhai, M., Venkateswaran, A., Hess, M., Omelchenko, M. V., and Kostandarithes., H. M., Makarova, K. S., Wackett, L. P., Fredrickson, J. K., and Ghosal, D. (2004) Accumulation of Mn(II) in Deinococcus radiodurans facilitates γ-radiation resistance. Science 306, 1025-1028
7. Horsburgh, M. J., and Wharton., S. J., Karavolos, M., and Foster, S. J. (2002) Manganese: elemental defence for a life with oxygen. Trends Microbiol. 10, 496-501
8. Archibald, F. S., and Fridovich, I. (1981) Manganese and defenses against oxygen toxicity in Lactobacillusplantarum. J. Bacteriol. 145, 442-451
9. Berlett, B. S., and Chock., P. B., Yim, M. B., and Stadtman, E. R. (1990) Manganese(II) catalyzes the bicarbonate-dependent oxidation of amino acids by hydrogen peroxide and the amino acid-facilitated dismutation of hydrogenperoxide. Proc. Natl. Acad. Sci. U.S.A. 87, 389-393
10. Barnese, K., and Gralla., E. B., Cabelli, D. E., and Valentine, J. S. (2008) Manganous phosphate acts as a superoxide dismutase. J. Am. Chem. Soc. 130, 4604-4606
11. Barnese, K., and Gralla., E. B., Valentine, J. S., and Cabelli, D. E. (2012) Biologically relevant mechanism for catalytic superoxide removal by simple manganese compounds. Proc. Natl. Acad. Sci. U.S.A. 109, 6892-6897
12. Daly, M. J., and Gaidamakova., E. K., Matrosova, V. Y., Kiang, J. G., Fukumoto, R., Lee, D.-Y., and Wehr., N. B., Viteri, G. A., Berlett, B. S., and Levine, R. L. (2010) Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS ONE 5, e12570
13. Mounicou, S., Szpunar, J., and Lobinski, R. (2009) Metallomics: the concept and methodology. Chem. Soc. Rev. 38, 1119-1138
14. 2+ speciation and oxidative stress resistance in yeast cells with electron-nuclear double resonance spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 107, 15335-15339
15. Bennati, M., and Prisner, T. F. (2005) New developments in high field electron paramagnetic resonance with applications in structural biology. Rep. Prog. Phys. 68, 411-448
16. Bonacossa de Almeida, C, Coste, G., Sommer, S., and Bailone, A. (2002) Quantification of RecA protein in Deinococcus radiodurans reveals involvement of RecA, but not LexA, in its regulation. Mol. Genet. Genomics 268, 28-41
17. Un, S., Dorlet, P., and Rutherford, A. W. (2001) A high-field EPR tour of radicals in photosystems I and II. Appl. Magn. Reson. 21, 341-361
18. Davies, E. (1974) A new pulse ENDOR technique. Phys. Lett. A 47, 1-2
19. Mims, W. (1965) Pulsed ENDOR experiments. Proc. R. Soc. Lond. A 283, 452-457
20. 2+ complexes of ADP and ATP7S by W-band ENDOR. Appl. Magn. Reson. 30, 461-472
21. Un, S., Tabares, L. C, Cortez, N, Hiraoka, B. Y., and Yamakura, F. (2004) Manganese(II) zero-field interaction in cambialistic and manganese superoxide dismutases and its relationship to the structure of the metal binding site. J. Am. Chem. Soc. 126, 2720-2726
22. Tabares, L. C, Gätjens, J., Hureau, C., Burrell, M. R., Bowater, L., Pecoraro, V. L., Bornemann, S., and Un, S. (2009) pH-dependent structures of the manganese binding sites in oxalate decarboxylase as revealed by high-field electron paramagnetic resonance. J. Phys. Chem. B 113, 9016-9025
23. 2+ binding site in the minimal and tertiary stabilized hammerhead ribozymes. Appl. Magn. Reson. 31, 543-552
24. Bennett, B. D., and Kimball., E. H., Gao, M., Osterhout, R., Van Dien, S. J., and Rabinowitz, J. D. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5, 593-599
25. Tabares, L. C., Gätjens, J., and Un, S. (2010) Understanding the influence of the protein environment on the Mn(II) centers in superoxide dismutases using high-field electron paramagnetic resonance. Biochim. Biophys. Acta 1804, 308-317
26. Imlay, J. A., and Fridovich, I. (1991) Assay of metabolic superoxide production in Escherichia coli. J. Biol. Chem. 266, 6957-6965
27. Volkmer, B., and Heinemann, M. (2011) Condition-dependent cell volume and concentration of Escherichia coli to facilitate data conversion for systems biology modeling. PLoS ONE 6, e23126
28. Lu, P., Vogel, C., Wang, R., Yao, X., and Marcotte, E. M. (2007) Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 25, 117-124
29. Daly, M. J., and Gaidamakova., E. K., Matrosova, V. Y., Vasilenko, A., Zhai, M., and Leapman., R. D., Lai, B., Ravel, B., Li, S.-M. W., Kemner, K. M., and Fredrickson, J. K. (2007) Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol. 5, e92
30. Markillie, L. M., and Varnum., S. M., Hradecky, P., and Wong, K. K. (1999) Targeted mutagenesis by duplication insertion in the radioresistant bacterium Deinococcus radiodurans: radiation sensitivities of catalase (katA) and superoxide dismutase (sodA) mutants. J. Bacteriol. 181, 666-669
31. Robinson, C. K., Webb, K., Kaur, A., Jaruga, P., Dizdaroglu, M., Baliga, N. S., Place, A., and Diruggiero, J. (2011) A major role for nonenzymatic antioxidant processes in the radioresistance of Halobacterium salinarum. J. Bacteriol. 193, 1653-1662
32. Krüger, A., Grüning, N.-M., Wamelink, M. M. C., Kerick, M., Kirpy, A., Parkhomchuk, D., Bluemlein, K., Schweiger, M.-R., Soldatov, A., Lehrach, H., Jakobs, C., and Ralser, M. (2011) The pentose phosphate pathway is a metabolic redox sensor and regulates transcription during the antioxidant response. Antioxid. Redox Signal. 15, 311-324
33. Davey, C. A., and Richmond, T. J. (2002) DNA-dependent divalent cation binding in the nucleosome core particle. Proc. Natl. Acad. Sci. U.S.A. 99, 11169-11174
34. Millonig, H., Pous, J., Gouyette, C., Subirana, J. A., and Campos, J.L. (2009) The interaction of manganese ions with DNA. J. Inorg. Biochem. 103, 876-880
35. Sun, H., Li, M., Xu, G., Chen, H., Jiao, J., Tian, B., Wang, L., and Hua, Y. (2012) Regulation of MntH by a dual Mn(II)-and Fe(II)-dependent transcriptional repressor (DR2539) in Deinococcus radiodurans. PLoS ONE 7, e35057
36. Chen, H., Wu, R., Xu, G., Fang, X., Qiu, X., Guo, H., Tian, B., and Hua, Y. (2010) DR2539 is a novel DtxR-like regulator of Mn/Fe ion homeostasis and antioxidant enzyme in Deinococcus radiodurans. Biochem. Biophys. Res. Commun. 396, 413-418