Structural switching of Cu, Zn-superoxide dismutases at loop VI: Insights from the crystal structure of 2-mercaptoethanol-modified enzyme

Bioscience Reports

Volumn 32, Issue 6, 2012, Pages 539-548

  Ihara, Kentaro ^a   Fujiwara, Noriko ^b   Yamaguchi, Yoshiki ^c   Torigoe, Hidetaka ^d   Wakatsuki, Soichi ^a   Taniguchi, Naoyuki ^c   Suzuki, Keiichiro ^d  

^a HIGH ENERGY ACCELERATOR RESEARCH ORGANIZATION KEK   (Japan)

^b HYOGO COLLEGE OF MEDICINE   (Japan)

^c RIKEN   (Japan)

^d TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

Amyotrophic lateral sclerosis (ALS); Asymmetric configuration; Crystal structure; Superoxide dismutase 1 (SOD1)

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; CYSTEINE; GLYCINE; HISTIDINE; ISOLEUCINE; MERCAPTOETHANOL; SUPEROXIDE DISMUTASE;

ALKYLATION; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; ASYMMETRIC SYNTHESIS; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME METABOLISM; ENZYME MODIFICATION; ENZYME STRUCTURE; GENE MUTATION; GENE SWITCHING; HUMAN; HUMAN CELL; HYDROGEN BOND; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN CROSS LINKING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY;

ALKYLATION; AMINO ACID SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; HUMANS; HYDROGEN BONDING; MERCAPTOETHANOL; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT; SUPEROXIDE DISMUTASE;

EID: 84872381367     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20120029     Document Type: Article

References (51)

1. Deng, H. X., Hentati, A., Tainer, J. A., Zafar, I., Cayabyab, A., Hung, W. Y., Getzoff, E. D., Hu, P., Herzfeldt, B., Roos, R. P. et al. (1993) Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. Science 261, 1047-1051 (Pubitemid 23300865)
2. Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J. P., Deng, H. X. et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362, 59-62 (Pubitemid 23087289)
3. Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., Deng, H. X. et al. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264, 1772-1775 (Pubitemid 24227760)
4. Ripps, M. E., Huntley, G. W., Hof, P. R., Morrison, J. H. and Gordon, J. W. (1995) Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U.S.A. 92, 689-693
5. Valentine, J. S., Doucette, P. A. and Zittin Potter, S. (2005) Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu. Rev. Biochem. 74, 563-593 (Pubitemid 40995518)
6. Seetharaman, S. V., Prudencio, M., Karch, C., Holloway, S. P., Borchelt, D. R. and Hart, P. (2009) Immature copper-zinc superoxide dismutase and familial amyotrophic lateral sclerosis. J. Exp. Biol. Med. 234, 1140-1154
7. Haidet-Phillips, A. M., Hester, M. E., Miranda, C. J., Meyer, K., Braun, L., Frakes, A., Song, S., Likhite, S., Murtha, M. J., Foust, K. D. et al. (2011) Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat. Biotechnol. 29, 824-828
8. Bosco, D. A., Morfini, G., Karabacak, N. M., Song, Y., Gros-Louis, F., Pasinelli, P., Goolsby, H., Fontaine, B. A., Lemay, N., McKenna-Yasek, D. et al. (2010) Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat. Neurosci. 13, 1396-1403
9. Gruzman, A., Wood, W. L., Alpert, E., Prasad, M. D., Miller, R. G., Rothstein, J. D., Bowser, R., Hamilton, R., Wood, T. D., Cleveland, D. W. et al. (2007) Common molecular signature in SOD1 for both sporadic and familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U.S.A. 104, 12524-12529 (Pubitemid 47206171)
10. Zetterström, P., Graffmo, K. S., Andersen, P. M., Brännström, T. and Marklund, S. L. (2011) Proteins that bind to misfolded mutant superoxide dismutase-1 in spinal cords from transgenic amyotrophic lateral sclerosis (ALS) model mice. J. Biol. Chem. 286, 20130-20136
11. Fujiwara, N., Miyamoto, Y., Ogasahara, K., Takahashi, M., Ikegami, T., Takamiya, R., Suzuki, K. and Taniguchi, N. (2005) Different immunoreactivity against monoclonal antibodies between wild-type and mutant copper/zinc superoxide dismutase linked to amyotrophic lateral sclerosis. J. Biol. Chem. 280, 5061-5070 (Pubitemid 40288682)
12. Tainer, J. A., Getzoff, E. D., Beem, K. M., Richardson, J. S. and Richardson, D. C. (1982) Determination and analysis of the 2 A-structure of copper, zinc superoxide dismutase. J. Mol. Biol. 160, 181-217 (Pubitemid 13239300)
13. Parge, H. E., Hallewell, R. A. and Tainer, J. A. (1992) Atomic structures of wild-type and thermostable mutant recombinant human Cu,Zn superoxide dismutase. Proc. Natl. Acad. Sci. U.S.A. 89, 6109-6113
14. Fukuhara, R., Tezuka, T. and Kageyama, T. (2002) Structure, molecular evolution, and gene expression of primate superoxide dismutases. Gene 296, 99-109 (Pubitemid 35287328)
15. Fink, R. C. and Scandaliios, J. G. (2002) Molecular evolution and structure-function relationships of the superoxide dismutase gene families in angiosperms and their relationship to other eukaryotic and prokaryotic superoxide dismutases. Arch. Biochem. Biophys. 399, 19-36 (Pubitemid 34848307)
16. Repock, J. R., Frey, H. E. and Hallewell, R. A. (1990) Contribution of conformational stability and reversibility of unfolding to the increased thermostability of human and bovine superoxide dismutase mutated at free cysteines. J. Biol. Chem. 265, 21612-21618 (Pubitemid 120014203)
17. Fujiwara, N., Nakano, M., Kato, S., Yoshihara, D., Ookawara, T., Eguchi, H., Taniguchi, N. and Suzuki, K. (2007) Oxidative modification to cysteine sulfonic acid of Cys111 in human copper-zinc superoxide dismutase. J. Biol. Chem. 282, 35933-35944 (Pubitemid 350277101)
18. Okado-Matsumoto, A., Guan, Z. and Fridovich, I. (2006) Modification of cysteine 111 in human Cu,Zn-superoxide dismutase. Free Radical Biol. Med. 41, 1837-1846 (Pubitemid 44839144)
19. Liu, H., Zhu, H., Eggers, D. K., Nersissian, A. M., Faull, K. F., Goto, J. J., Ai, J., Sanders-Loehr, J., Gralla, E. B. and Valentine, J. S. (2000) Copper(2 +) binding to the surface residue cysteine 111 of His46Arg human copper-zinc superoxide dismutase, a familial amyotrophic lateral sclerosis mutant. Biochemistry 39, 8125-8132 (Pubitemid 30460961)
20. Hiraki, M., Kato, R., Nagai, M., Satoh, T., Hirano, S. and Ihara, K. (2006) Development of an automated large-scale protein-crystallization and monitoring system for high-throughput protein-structure analyses. Acta Crystallogr. D: Biol. Crystallogr. 62, 1058-1065 (Pubitemid 44337380)
21. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
22. Vagin, A. and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025 (Pubitemid 127485985)
23. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
24. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
25. Jones, T. A., Zou, J. Y., Cowan, S. W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. Sect. A Found. Crystallogr. 47, A110-A119
26. Perrakis, A., Sixma, T. K., Wilson, K. S. and Lamzin, V. S. (1997) wARP: improvement and extension of crystallographic phases by weighted averaging of multiple-refined dummy atomic models. Acta Crystallogr. Sect. D Biol. Crystallogr. 53, 448-455 (Pubitemid 27340643)
27. Murshudov, G. N., Vagin, A. A. and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. Sect. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
28. Sayle, R. A. and Milner-White, E. J. (1995) RASMOL: biomolecular graphics for all. Trends Biochem. Sci. 20, 374-376
29. Kraulis, P. J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950
30. Merritt, E. A. and Murphy, M. E. P. (1994) Raster3D Version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. Sect D Biol. Crystallogr. 50, 869-873 (Pubitemid 2161308)
31. Auclair, J. R., Boggio, K. J., Petsko, G. A., Ringe, D. and Agar, J. N. (2010) Strategies for stabilizing superoxide dismutase (SOD1), the protein destabilized in the most common form of familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U.S.A. 107, 21394-21399
32. Blackburn, N. J., Hasnain, S. S., Binsted, N., Diakun, G. P., Garner, C. D. and Knowles, P. F. (1984) An extended-X-ray-absorption-finestructure study of bovine erythrocyte superoxide dismutase in aqueous solution. Direct evidence for three-co-ordinate Cu(I) in reduced enzyme. Biochem. J. 219, 985-990
33. Ogihara, N. L., Parge, H. E., Hart, P. J., Weiss, M. S., Goto, J. J., Crane, B. R., Tsang, J., Slater, K., Roe, J. A., Valentine, J. S. et al. (1996) Unusual trigonal-planar copper configuration revealed in the atomic structure of yeast copper-zinc superoxide dismutase. Biochemistry 35, 2316-2321 (Pubitemid 26071664)
34. Seetharaman, S. V., Winkler, D. D., Taylor, A. B., Cao, X., Whitson, L. J., Doucette, P. A., Valentine, J. S., Sfiurf, V., Demeler, B., Carroll, M. C. et al. (2010) Disrupted zinc-binding sites in structures of pathogenic SOD1 variants D124V and H80R. Biochemistry 49, 5714-5725
35. Hough, M. A., Grossmann, J. G., Antonyuk, S. V, Strange, R. W., Doucette, P. A., Rodriguez, J. A., Whitson, L. J., Hart, P. J., Hayward, L. J., Valentine, J. S. and Hasnain, S. S. (2004) Dimer destabilization in superoxide dismutase may result in disease-causing properties: structures of motor neuron disease mutants. Proc. Natl. Acad. Sci. U.S.A. 101, 5976-5981
36. Banci, L., Bertini, I., D'Amelio, N., Libralesso, E., Turano, P. and Valentine, J. S. (2007) Metalation of the amyotrophic lateral sclerosis mutant glycine 37 to arginine superoxide dismutase (SOD1) apoprotein restores its structural and dynamical properties in solution to those of metalated wild-type SOD1. Biochemistry 46, 9953-9962 (Pubitemid 47378585)
37. DiDonato, M., Craig, L., Huff, M. E., Thayer, M. M., Cardoso, R. M., Kassmann, C. J., Lo, T. P., Bruns, C. K., Powers, E. T., Kelly, J. W., Getzoff, E. D. and Tainer, J. A. (2003) ALS mutants of human superoxide dismutase form fibrous aggregates via framework destabilization. J. Mol. Biol. 332, 601-615 (Pubitemid 37075984)
38. Elam, J. S., Taylor, A. B., Strange, R., Antonyuk, A., Doucette, P. A., Rodriguez, J. A., Hasnain, S. S., Hayward, L. J., Valentine, J. S., Yeates, T. O. and Hart, P. J. (2003) Amyloid-like filaments and water-filled nanotubes formed by SOD1 mutant proteins linked to familial ALS. Nat. Struct. Biol. 10, 461-467 (Pubitemid 36637644)
39. Antonyuk, S., Elam, J. S., Hough, M. A., Strange, R. W., Doucette, P. A., Rodriguez, J. A., Hayward, L. J., Valentine, J. S., Hart, P. J. and Hasnain, S. S. (2005) Structural consequences of the familial amyotrophic lateral sclerosis SOD1 mutant His46Arg. Protein Sci. 14, 1201-1213 (Pubitemid 40577800)
40. Cao, X., Antonyuk, S. V., Seetharaman, S. V., Whitson, L. J., Taylor, A. B., Holloway, S. P., Strange, R. W., Doucette, P. A., Valentine, J. S., Tiwari, A. et al. (2008) Structures of the G85R variant of SOD1 in familial amyotrophic lateral sclerosis. J. Biol. Chem. 283, 16169-16177
41. Cardoso, R. M., Thayer, M. M., DiDonato, M., Lo, T. P., Bruns, C. K., Getzoff, E. D. and Tainer, J. A. (2002) Insights into Lou Gehrig's disease from the structure and instability of the A4V mutant of human Cu,Zn superoxide dismutase. J. Mol. Biol. 324, 247-256 (Pubitemid 35379025)
42. Getzoff, E. D., Tainer, J. A., Stempien, M. M., Bell, G. I. and Hallewell, R. A. (1989) Evolution of CuZn superoxide dismutase and the Greek key beta-barrel structural motif. Proteins 5, 322-336 (Pubitemid 19189328)
43. Schmidlin, T., Kennedy, B. K. and Daggett, V. (2009) Structural changes to monomeric CuZn superoxide dismutase caused by the familial amyotrophic lateral sclerosis-associated mutation A4V. Biophys. J. 97, 104-111
44. Furukawa, Y., Kaneko, K., Yamanaka, K. and Nukina, N. (2010) Mutation-dependent polymorphism of Cu,Zn-superoxide dismutase aggregates in the familial form of amyotrophic lateral sclerosis. J. Biol. Chem. 285, 22221-22231
45. Arnesano, F., Banci, L., Bertini, I., Martinelli, M., Furukawa, Y. and O'Hallorann, T. V. (2004) The unusually stable quaternary structure of human Cu,Zn-superoxide dismutase 1 is controlled by both metal occupancy and disulfide status. J. Biol. Chem. 279, 47998-48003 (Pubitemid 39540952)
46. Takeuchi, S., Fujiwara, N., Ido, A., Ono, M., Takeuchi, Y., Tateno, M., Suzuki, K., Takahashi, R., Tooyama, I., Taniguchi, N. et al. (2010) Induction of protective immunity by vaccination with wild-type apo superoxide dismutase 1 in mutant SOD1 transgenic mice. J. Neuropathol. Exp. Neurol. 69, 1044-1056
47. Rakhit, R., Crow, J. P., Lepock, J. R., Kondejewski, L. H., Cashman, N. R. and Chakrabartty, A. (2004) Monomeric Cu,Zn-superoxide dismutase is a common misfolding intermediate in the oxidation models of sporadic and familial amyotrophic lateral sclerosis. J. Biol. Chem. 279, 15499-15504 (Pubitemid 38618950)
48. Furukawa, Y., Kaneko, K., Yamanaka, K., O'Halloran, T. V. and Nukina, N. (2008) Complete loss of post-translational modifications triggers fibrillar aggregation of SOD1 in the familial form of amyotrophic lateral sclerosis. J. Biol. Chem. 283, 24167-24176
49. Polymenidou, M. and Cleveland, D. W. (2011) The seeds of neurodegeneration: prion-like spreading in ALS. Cell 147, 498-508
50. Henriksen, A., Aghajari, N., Jensen, K. F. and Gajhede, M. (1996) A flexible loop at the dimer interface is a part of the active site of the adjacent monomer of Escherichia coli orotate phosphoribosyltransferase. Biochemistry 35, 3803-3809 (Pubitemid 26102170)
51. Lee, M., Maher, M. J., Christopherson, R. I. and Guss, J. M. (2007) Kinetic and structural analysis of mutant Escherichia coli dihydroorotases: a flexible loop stabilizes the transition state. Biochemistry 37, 10538-10550 (Pubitemid 47417249)