Role of tyrosine-34 in the anion binding equilibria in manganese(II) superoxide dismutases

Biochemistry

Volumn 46, Issue 32, 2007, Pages 9320-9327

  Tabares, Leandro C ^a,b   Cortez, Néstor ^b   Un, Sun ^a  

^a CEA   (France)

^b UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; ELECTRONIC STRUCTURE; HYDROGEN PEROXIDE; MANGANESE COMPOUNDS; NEGATIVE IONS; PARAMAGNETIC RESONANCE;

ANION BINDING EQUILIBRIA; ANIONIC SUBSTRATES; HIGH FIELD ELECTRON PARAMAGNETIC RESONANCE (HFEPR); TYROSINE;

ENZYME KINETICS;

AMINO ACID; ANION; AZIDE; FLUORIDE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; OXYGEN; PHENYLALANINE; TYROSINE; WATER;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; ELECTRON SPIN RESONANCE; HIGH FIELD ELECTRON PARAMAGNETIC RESONANCE; LOW TEMPERATURE; MEASUREMENT; MOLECULAR INTERACTION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; RHODOBACTER CAPSULATUS;

AMINO ACID SUBSTITUTION; ANIONS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME ACTIVATION; MANGANESE; OXIDATION-REDUCTION; PHENYLALANINE; PROTEIN BINDING; RHODOBACTER CAPSULATUS; SPECTROPHOTOMETRY; SUBSTRATE SPECIFICITY; SUPEROXIDE DISMUTASE; TEMPERATURE; TYROSINE;

EID: 34547905430     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700438j     Document Type: Article

References (48)

1. Fridovich, I. (1995) Superoxide radical and superoxide dismutases, Annu. Rev. Biochem. 64, 97-112.
2. Touati, D. (1997) Superoxide Dismutases in Bacteria and Pathogen Protists, in Oxidative Stress and the Molecular Biology of Antioxidant Defenses (Scandalios, J. G., Ed.) pp 447-493, Cold Spring Harbor Laboratory Press, NY.
3. Bull, C., and Fee, J. A. (1985) Steady-state kinetic studies of superoxide dismutases: properties of the iron containing protein from Escherichia coli, J. Am. Chem. Soc. 107, 3295-3304.
4. Lavelle, F., McAdam, M. E., Fielden, E. M., and Roberts, P. B. (1977) A pulse-radiolysis study of the catalytic mechanism of the iron-containing superoxide dismutase from Photobacterium leiognathi, Biochem. J. 161, 3-11.
5. Klug-Roth, D., Fridovich, I., and Rabani, J. (1973) Pulse radiolytic investigations of superoxide catalyzed disproportionation. Mechanism for bovine superoxide dismutase, J. Am. Chem. Soc. 95, 2786-2790.
6. Kim, E. J., Chung, H. J., Suh, B., Hah, Y. C., and Roe, J. H. (1998) Transcriptional and post-transcriptional regulation by nickel of sodN gene encoding nickel-containing superoxide dismutase from Streptomyces coelicolor Muller, Mol. Microbiol. 27, 187-195.
7. Kim, F. J., Kim, H. P., Hah, Y. C., and Roe, J. H. (1996) Differential expression of superoxide dismutases containing Ni and Fe/Zn in Streptomyces coelicolor, Eur. J. Biochem. 241, 178-185.
8. Stroupe, M. E., DiDonato, M., and Tainer, J. A. (2001) In Handbook of Metalloproteins (Messerschmidt, A., Huber, R., Wieghardt, K., and Paulos, T., Eds.) pp 941-951, Wiley and Sons, Chicester, U.K.
9. Miller, A.-F. (2001) In Handbook of Metalloproteins (Messerschmidt, A., Huber, R., Wieghardt, K., and Paulos, T., Eds.) pp 668-682, Wiley and Sons, Chicester, U.K.
10. Sugio, S., Hiraoka, B. Y., and Yamakura, F. (2000) Crystal structure of cambialistic superoxide dismutase from Porphyromonas gingivalis, Eur. J. Biochem. 267, 3487-3495.
11. Schmidt, B., Meier, B., and Parak, F. (1996) X-ray structure of the cambialistic superoxide dismutase from Propionibacterium shermanii active with Fe or Mn, J. Biol. Inorg. Chem. 1, 532-541.
12. Ose, D. E., and Fridovich, I. (1976) Superoxide dismutase. Reversible removal of manganese and its substitution by cobalt, nickel or zinc, J. Biol. Chem. 251, 1217-1218.
13. Yamakura, F. (1980) Cadmium, chromium, and manganese replacement for iron in iron-superoxide dismutase from Pseudomonas ovalis, J. Biochem. (Tokyo) 88, 191-196.
14. Meier, B., Barra, D., Bossa, F., Calabrese, L., and Rotilio, G. (1982) Synthesis of either Fe- or Mn-superoxide dismutase with an apparently identical protein moiety by an anaerobic bacterium dependent on the metal supplied, J. Biol. Chem. 257, 13977-13980.
15. Amano, A., Shizukuishi, S., Tamagawa, H., Iwakura, K., Tsunasawa, S., and Tsunemitsu, A. (1990) Characterization of superoxide dismutase purified from either anaerobically maintained or aerated Bacteroides gingivalis, J. Bacteriol. 172, 1457-1463.
16. Martin, M. E., Byers, E. B. R., Olson, M. O. J., Salin, M. L., Arceneaux, J. E. L., and Tolbert, C. (1986) A Streptococcus mutans superoxide dismutase that is active with either manganese or iron as a cofactor, J. Biol. Chem. 261, 9361-9367.
17. 2-induced manganese-containing superoxide dismutase from Bacteroides fragilis, Arch. Biochem. Biophys. 238, 83-89.
18. Tabares, L. C., Bittel, C., Carrillo, N., Bortolotti, A., and Cortez, N. (2003) The single superoxide dismutase of Rhodobacter capsulatus is a cambialistic, manganese-containing enzyme, J. Bacteriol. 185, 3223-3227.
19. Miller, A. F., Sorkin, D. L., and Padmakumar, K. (2005) Anion binding properties of reduced and oxidized iron-containing superoxide dismutase reveal no requirement for tyrosine 34, Biochemistry 44, 5969-5981.
20. Whittaker, M. M., and Whittaker, J. W. (1997) Mutagenesis of a proton linkage pathway in Escherichia coli manganese superoxide dismutase, Biochemistry 36, 8923-8931.
21. Tabares, L. C., Cortez, N., Hiraoka, B. Y., Yamakura, F., and Un, S. (2006) Effects of substrate analogues and pH on manganese superoxide dismutases, Biochemistry 45, 1919-1929.
22. Lah, M. S., Dixon, M. M., Pattridge, K. A., Stallings, W. C., Fee, J. A., and Ludwig, M. L. (1995) Structure-function in Escherichia coli iron superoxide dismutase: comparisons with the manganese enzyme from Thermus thermophilus, Biochemistry 34, 1646-1660.
23. Schmidt, M. (1999) Manipulating the coordination mumber of the ferric iron within the cambialistic superoxide dismutase of Propionibacterium shermanii by changing the pH-value. A crystallographic analysis, Eur. J. Biochem. 262, 117-127.
24. Whittaker, J. W., and I., S. E. (1988) Spectroscopic studies on ferrous non-heme iron active sites: magnetic circular dichroism of mononuclear Fe sites in superoxide dismutase and lipoxygenase, J. Am. Chem. Soc. 110, 5329-5339.
25. Whittaker, M. M., and Whittaker, J. W. (1996) Low-temperature thermochromism marks a change in coordination for the metal ion in manganese superoxide dismutase, Biochemistry 35, 6762-6770.
26. Jackson, T. A., Karapetan, A., Miller, A.-F., and Brunold, T. C. (2004) Spectroscopic and computational studies of the azide-adduct of manganese superoxide dismutase: definitive assignment of the ligand responsible for the low-temperature thermochroism, J. Am. Chem. Soc. 126, 12477-12491.
27. Guan, Y., Hickey, M. J., Borgstahl, G. E. O., Hallewell, R. A., Lepock, J. R., O'Conner, D., Hsieh, Y., Nick, H. S., Silvermann, D. N., and Tainer, J. A. (1998) Crystal structure of Y34F mutant human mitochondrial manganese superoxide dismutase and the functional role of tyrosine 34, Biochemistry 37, 4722-4730.
28. Edwards, R. A., Whittaker, M. M., Whittaker, J. W., Baker, E. N., and Jameson, G. B. (2001) Removing a hydrogen bond in the dimer interface of Escherichia coli manganese superoxide dismutase alters structure and reactivity, Biochemistry 40, 4622-4632.
29. Hunter, T., Ikebukuro, K., Bannister, W. H., Bannister, J. V., and Hunter, G. J. (1997) The conserved residue tyrosine 34 is essential for maximal activity of iron-superoxide dismutase from Escherichia coli, Biochemistry 36, 4925-4933.
30. Un, S., Dorlet, P., Voyard, G., Tabares, L. C., and Cortez, N. (2001) High-field EPR characterization of manganese reconstituted superoxide dismutase from Rhodobacter capsulatus, J. Am. Chem. Soc. 123, 10123-10124.
31. 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.
32. Whittaker, M. M., and Whittaker, J. W. (1991) Active site spectral studies on manganese superoxide dismutase, J. Am. Chem. Soc. 113, 5528-5540.
33. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005) Protein Identification and Analysis Tools on the ExPASy Server, in The Proteomics Protocols Handbook (Walker, J. M., Ed.) pp 571-607, Humana Press, Totowa, NJ.
34. Goldring, J. P. D., and Ravaioli, L. (1996) Solubilizarion of protein-dye complexes on nitrocellulose to quantify proteins spectrophotometrically, Anal. Biochem. 242, 197-201.
35. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72, 248-254.
36. McCord, J. M., and Fridovich, I. (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein), J. Biol. Chem. 244, 6049-6055.
37. Beauchamp, C., and Fridovich, I. (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels, Anal. Biochem. 44, 276-287.
38. Un, S., Dorlet, P., and Rutherford, A. W. (2001) A high-field tour of radicals in photosystems I and II, Appl. Magn. Reson. 21, 341-361.
39. -) in reaction centers of Rhodobacter sphaeroides R-26, J. Phys. Chem. 97, 7639-7647.
40. Tabares, L. C., Cortez, N., Agalidis, I., and Un, S. (2005) Temperature-dependent coordination in E. coli manganese superoxide, J. Am. Chem. Soc. 127, 6039-6047.
41. Donahue, J. L., Okpodu, C. M., Cramer, C. L., Grabau, E. A., and Alscher, R. G. (1997) Responses of antioxidants to paraquat in pea leaves (relationships to resistance), Plant Physiol. 113, 249-257.
42. Leveque, V., J.-P., Vance, C. K., Nick, H. S., and Silverman, D. N. (2001) Redox properties of human manganese superoxide dismutase and active-site mutants, Biochemistry 40, 10586-10591.
43. Vance, C. K., and Miller, A. F. (2001) Novel insights into the basis for Escherichia coli superoxide dismutase's metal ion specificity from Mn-substituted FeSOD and its very high E(m), Biochemistry 40, 13079-13087.
44. Borgstahl, G. E., Parge, H. E., Hickey, M. J., Beyer, W. F. J., Hallewell, R. A., and Tainer, J. A. (1992) The structure of human mitochondrial manganese superoxide dismutase reveals a novel tetrameric interface of two 4-helix bundles, Cell 71, 107-118.
45. Edwards, R. A., Baker, H. M., Whittaker, M. M., Whittaker, J. W., Jameson, G. B., and Baker, E. N. (1998) Crystal structure of Escherichia coli manganese superoxide dismutase at 2.1 Å resolution, J. Biol. Inorg. Chem. 3, 161-171.
46. 2O), J. Chem. Phys. 98, 3763-3776.
47. Cleland, W. W., Frey, P. A., and Gerlt, J. A. (1998) The low barrier hydrogen bond in enzymatic catalysis, J. Biol. Chem. 273, 25529-25532.
48. Greenleaf, W. B., Perry, J. J., Hearn, A. S., Cabelli, D. E., Lepock, J. R., Stroupe, M. E., Tainer, J. A., Nick, H. S., and Silverman, D. N. (2004) Role of hydrogen bonding in the active site of human manganese superoxide dismutase, Biochemistry 43, 7038-7045.