Engineering a change in metal-ion specificity of the iron-dependent superoxide dismutase from Mycobacterium tuberculosis X-ray structure analysis of site-directed mutants

European Journal of Biochemistry

Volumn 251, Issue 3, 1998, Pages 795-803

  Bunting, Karen ^b   Cooper, Jon B ^a   Badasso, Mohammed O ^b   Tickle, Ian J ^b   Newton, Melanie ^a   Wood, Steve P ^a   Zhang, Ying ^c   Young, Douglas ^c  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

Mycobacterium tuberculosis; Site directed mutagenesis; Superoxide dismutase; X ray structure

Indexed keywords

IRON; METAL ION; SUPEROXIDE DISMUTASE;

ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME SPECIFICITY; MOLECULAR INTERACTION; MYCOBACTERIUM LEPRAE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

EID: 0032006799     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1998.2510795.x     Document Type: Article

References (47)

1. Amano, A., Shizukuishi, S., Tamagawa, H., Iwakura, K., Tsunasawa, S. & Tsunemitsu, A. (1990) Characterisation of superoxide dismutase purified from either anaerobically maintained or aerated Bacteroides gingivalis, J. Bacteriol. 172, 1457-1463.
2. Ausubel, F. M., Brenet, R., Kingston, R. F., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (1992) Mutagenesis of cloned DNA, in Short protocols in molecular biology, John Wiley & Sons, New York.
3. Beauchamp, C. & Fridovich, I. (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels, Anal. Biochem. 44, 276-287.
4. Blundell, T. L. & Johnson, L. N. (1976) Protein crystallography, Academic Press, London.
5. Borgstahl, G. E. O., Parge, H. E., Hickey, M. J., Beyer, W. F. Jr, Hallewell, R. A. & 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.
6. Brock, C. J. & Harris, J. I. (1977) superoxide dismutase from Bacillus stearothermophilus: reversible removal of manganese and its replacement by other metals, Biochem. Soc. Trans. 5, 1537-1539.
7. CCP4 (1994) The CCP4 suite: programs for protein crystallography, Acta Crystallogr. D50, 760-763.
8. Clemens, D. L. & Horwitz, M. A. (1995) Characterisation of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited, J. Exp. Med. 181, 257-270.
9. Cooper, J. B., Driessen, H. P. C., Wood, S. P., Zhang, Y. & Young, D. (1994) Crystallisation and preliminary X-ray analysis of the superoxide dismutase from Mycobacterium tuberculosis, J. Mol. Biol. 235, 1156-1158.
10. Cooper, J. B., McIntyre, K., Badasso, M. O., Wood, S. P., Zhang, Y., Garbe, T. R. & Young, D. B. (1995) X-ray structure analysis of the iron-dependent superoxide dismutase from Mycobacterium tuberculosis at 2.0 Å resolution reveals novel dimer-dimer interactions, J. Mol. Biol. 246, 531-544.
11. Cotton, F. A. & Wilkinson, G. (1988) Advanced inorganic chemistry - a comprehensive text, Wiley-Interscience, New York.
12. Crowther, R. A. (1972) The last rotation function, in The molecular replacement method (Rossman, M. G., ed.) pp. 173-178, Gordon and Breach, New York.
13. 2 translation function to an asymmetric unit containing two dimers, Acta Crystallogr. B47, 987-997.
14. Escuyer, V., Haddad, N., Frehel, C. & Berche, P. (1996) Molecular characterisation of a surface-exposed superoxide dismutase of Mycobacterium avium, Microb. Pathog. 20, 41-55.
15. Fridovich, I. (1986) Superoxide dismutases, Adv. Enzymol. 58, 61-97.
16. Garbe, T., Barathi, J., Barnini, S., Zhang, Y., Abou-Zeid, C., Tang, D., Mukherjee, R. & Young, D. B. (1994) Transformation of mycobacterial species using hygromycin resistance as selectable marker, Microbiology (Reading) 140, 133-138.
17. Haneef, I., Moss, D. S., Stanford, M. J. & Borkakoti, N. (1985) Restrained structure-factor least-squares refinement of protein structures using a vector-processing computer, Acta Crystallogr. A41, 426-433.
18. Hasan, Z., Schlax, C., Kuhn, L., Lefkovits, I., Young, D., Thole, J. & Pieters, J. (1997) Isolation and characterisation of the mycobacterial phagosome: segregation from the endosomal/lysosomal pathway, Mol. Microbiol. 24, 545-553.
19. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
20. Kusunose, E., Ichihara, K., Noda, Y. & Kusunose, M. (1976) Superoxide dismutase from Mycobacterium tuberculosis, J. Biochem. (Tokyo) 80, 1343-1352.
21. Kusunose, E., Kusunose, M., Ichihara, K. & Izumi, S. (1981) Superoxide dismutase in cell-tree extracts from Mycobacterium leprae grown on armadillo liver, FEMS Microbiol. Lett. 10, 49-52.
22. Lah, M. S., Dixon, M. M., Pattridge, K. A., Stallings, W. C., Fee, J. A. & 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. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291.
24. Leslie, A. G. W. (1991) Molecular data processing, in Crystallographic computing (Moras, D., Podjarny, A. D. & Thierry, J. C., eds) pp. 50-61, IUC Oxford University Press, Oxford.
25. Ludwig, M. L., Metzger A. L., Pattridge, K. A. & Stallings W. C. (1991) Manganese superoxide dismutase from Thermus thermophilus. A structural model refined at 1.8 Å resolution, J. Mol. Biol. 219, 335-358.
26. Martin, M. E., Byers, B. R., Olson, M. O. J., Salin, M. L., Archeneaux, J. K. L. & 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.
27. Matthews, B. W. (1968) Solvent content of protein crystals, J. Mol. Biol. 33, 491-497.
28. McPherson, A. (1982) Preparation and analysis of protein crystals, Wiley, New York
29. Meier, B., Barra, D., Bossa, F., Calabrese, L. & Rotilo, G. (1982) Synthesis of either Fe- or Mn-superoxide dismutase with an apparently identical protein moiety by an anaerobic bacterium dependent on metal supply, J. Biol. Chem. 257, 13977-13980.
30. Meier, B., Sehn, A. P., Schinina, M. E. & Barra, D. (1994) In vivo incorporation of copper into the iron-exchangeable and manganese-exchangeable superoxide dismutase from Propionibacterium shemanii, Eur. J. Biochem. 219, 463-468.
31. Menendez, M. C. Domenech, P., Prieto, J. & Garcia, M. J. (1995) Cloning and expression of Mycobacterium fortuitum superoxide dismutase gene, FEMS Microbiol, Lett. 134, 273-278.
32. O'Gaora, P., Barnini, S., Hayward, C., Filley, E., Rook, G., Young, D. & Thole, J. (1997) Mycobacteria as immunogens: development of expression vectors for use in multiple mycobacterial species, Med. Princ. Pract. 6, 91-96.
33. Ose, D. E. & Fridovich, I. (1979) Manganese-containing superoxide dismutase from Escherichia coli: reversible resolution and metal replacement, Arch. Biochem. Biophys. 194, 360-364.
34. Parker, M. W. & Blake, C. C. F. (1988a) Crystal structure of manganese superoxide dismutase from Bacillus stearothermophilus at 2.4 Å resolution, J. Mol. Biol. 199, 649-661.
35. Parker, M. W. & Blake, C. C. F. (1988b) Iron-containing and manganese-containing superoxide dismutases can be distinguished by analysis of their primary structures, FEBS Lett. 229, 377-382.
36. Pennington, C. D. & Gregory, E. M. (1986) Isolation and reconstitution of iron- and manganese-containing superoxide dismutases from Bacteroides thetaiotaomicron, J. Bacteriol. 166, 528-532.
37. Read, R. J. (1986) Improved Fourier coefficients for maps using phases from partial structures with errors, Acta Crystallogr. A42, 140-149.
38. Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B. & Erlich, H. A. (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase, Science 239, 487-491.
39. Silva, J. J. R. F. da & Williams, R. J. P. (1991) The biological chemistry of the elements: the inorganic chemistry of life, Clarendon Press, Oxford.
40. Stallings, W. C., Powers, T. B., Pattridge, K. A., Fee, J. A. & Ludwig, M. L. (1983) Iron superoxide dismutase from Escherichia coli at 3.1 Å resolution: a structure unlike that of copper/zinc protein at both monomer and dimer levels, Proc. Natl Acad. Sci. USA 80, 3384-3388.
41. Stallings, W. C., Metzger, A. L., Pattridge, K. A., Fee, J. A. & Ludwig, M. L. (1991) Structure-function relationships in iron and manganese superoxide dismutases, Free Radical Res. Commun. 12-13, 259-268.
42. Stoddard, B. L., Howell, P. L., Ringe, D. & Petsko, G. A. (1990) The 2.1 Å resolution structure of iron superoxide dismutase from Pseudomonas ovalis, Biochemistry 29, 8885-8893.
43. Takao, M., Yasui, A. & Oikawa, A. (1991) Unique characteristics of a superoxide dismutase of a strictly anaerobic archaebacterium Methanobacterium thermoautotrophicum, J. Biol. Chem. 266, 14151-14154.
44. Wagner, U. G., Pattridge, K. A., Ludwig, M. L., Stallings, W. C. Werber, M. M., Oefner, C., Frolow, F. & Sussman, J. L. (1993) Comparison of the crystal structures of genetically engineered human manganese superoxide dismutase and manganese superoxide dismutase from Thermus thermophilus: differences in dimer-dimer interaction, Protein Sci. 2, 814-825.
45. Yamakura, F., Kobayashi, K., Tagawa, S., Morita, A., Imai, T., Ohmori, D. & Matsumoto, T. (1995) pH-dependent activity change of superoxide dismutase from Mycobacterium segmatis, Biochem. Mol. Biol. Int. 36, 233-240.
46. Zhang, Y., Lathigra, R., Garbe, T., Catty, D. & Young, D. (1991) Genetic-analysis of superoxide dismutase, the 23 kilodalton antigen of Mycobacterium tuberculosis, Mol. Microbiol. 5, 381-391.
47. Zolg, J. W. & Phillipishulz, S. (1994) The superoxide-dismutase gene, a target for detection and identification of mycobacteria by PCR, J. Clin. Microbiol. 32, 2801-2812.