The Coupling between Disulphide Status, Metallation and Dimer Interface Strength in Cu/Zn Superoxide Dismutase

Journal of Molecular Biology

Volumn 365, Issue 2, 2007, Pages 333-342

  Hörnberg, Andreas ^a   Logan, Derek T ^b   Marklund, Stefan L ^c   Oliveberg, Mikael ^d  

^a UMEÅ UNIVERSITY   (Sweden)

^b Department of Molecular Biophysics ^*  (Sweden)

^c UMEÅ UNIVERSITY HOSPITAL   (Sweden)

^d STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

ALS; dimerisation; disulphide bond; loop entropy; protein folding

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DIMERIZATION; DISULFIDE BOND; ENTROPY; ENZYME ACTIVITY; ENZYME STABILITY; METALLATION; PRIORITY JOURNAL; PROTEIN FOLDING;

EID: 33751536847     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.09.048     Document Type: Article

References (70)

1. Deng H.X., Hentati A., Tainer J.A., Iqbal Z., Cayabyab A., Hung W.Y., et al. Science 261 (1993) 1047-1051
2. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362 (1993) 59-62
3. Andersen P.M., Sims K.B., Xin W.W., Kiely R., O'Neill G., Ravits J., et al. Sixteen novel mutations in the Cu/Zn superoxide dismutase gene in amyotrophic lateral sclerosis: a decade of discoveries, defects and disputes. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 4 (2003) 62-73
4. Tandan R., and Bradley W.G. Amyotrophic lateral sclerosis: Part 1. Clinical features, pathology, and ethical issues in management. Ann. Neurol. 18 (1985) 271-280
5. Mulder D.W., Kurland L.T., Offord K.P., and Beard C.M. Familial adult motor neuron disease: amyotrophic lateral sclerosis. Neurology 36 (1986) 511-5117
6. Cudkowicz M.E., McKenna-Yasek D., Sapp P.E., Chin W., Geller B., Hayden D.L., et al. Epidemiology of mutations in superoxide dismutase in amyotrophic lateral sclerosis. Ann. Neurol. 41 (1997) 210-221
7. Haverkamp L.J., Appel V., and Appel S.H. Natural history of amyotrophic lateral sclerosis in a database population. Validation of a scoring system and a model for survival prediction. Brain 118 (1995) 707-719
8. Liochev S.I., and Fridovich I. Mutant Cu,Zn superoxide dismutases and familial amyotrophic lateral sclerosis: evaluation of oxidative hypotheses. Free Radic. Biol. Med. 34 (2003) 1383-1389
9. Wood J.D., Beaujeux T.P., and Shaw P.J. Protein aggregation in motor neurone disorders. Neuropathol. Appl. Neurobiol. 29 (2003) 529-545
10. Watanabe M., Dykes-Hoberg M., Culotta V.C., Price D.L., Wong P.C., and Rothstein J.D. Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol. Dis. 8 (2001) 933-941
11. Lynch S.M., Boswell S.A., and Colon W. Kinetic stability of Cu/Zn superoxide dismutase is dependent on its metal ligands: implications for ALS. Biochemistry 43 (2004) 16525-16531
12. Chung J., Yang H., de Beus M.D., Ryu C.Y., Cho K., and Colon W. Cu/Zn superoxide dismutase can form pore-like structures. Biochem. Biophys. Res. Commun. 312 (2003) 873-876
13. Lindberg M.J., Normark J., Holmgren A., and Oliveberg M. Folding of human superoxide dismutase: disulfide reduction prevents dimerization and produces marginally stable monomers. Proc. Natl Acad. Sci. USA 101 (2004) 15893-15898
14. Lindberg M.J., Bystrom R., Boknas N., Andersen P.M., and Oliveberg M. Systematically perturbed folding patterns of amyotrophic lateral sclerosis (ALS)-associated SOD1 mutants. Proc. Natl Acad. Sci. USA 102 (2005) 9754-9759
15. Rosenzweig A.C., and O'Halloran T.V. Structure and chemistry of the copper chaperone proteins. Curr. Opin. Chem. Biol. 4 (2000) 140-147
16. Tiwari A., and Hayward L.J. Familial amyotrophic lateral sclerosis mutants of copper/zinc superoxide dismutase are susceptible to disulfide reduction. J. Biol. Chem. 278 (2003) 5984-5992
17. Arnesano F., Banci L., Bertini I., Martinelli M., Furukawa Y., and O'Halloran T.V. 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 (2004) 47998-48003
18. Furukawa Y., and O'Halloran T.V. Amyotrophic lateral sclerosis mutations have the greatest destabilizing effect on the apo- and reduced form of SOD1, leading to unfolding and oxidative aggregation. J. Biol. Chem. 280 (2005) 17266-17274
19. Khare S.D., Caplow M., and Dokholyan N.V. The rate and equilibrium constants for a multistep reaction sequence for the aggregation of superoxide dismutase in amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 101 (2004) 15094-15099
20. Rakhit R., Crow J.P., Lepock J.R., Kondejewski L.H., Cashman N.R., and Chakrabartty A. 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 (2004) 15499-15504
21. Furukawa Y., Torres A.S., and O'Halloran T.V. Oxygen-induced maturation of SOD1: a key role for disulfide formation by the copper chaperone CCS. EMBO J. 23 (2004) 2872-2881
22. Hough M.A., Grossmann J.G., Antonyuk S.V., Strange R.W., Doucette P.A., Rodriguez J.A., et al. Dimer destabilization in superoxide dismutase may result in disease-causing properties: structures of motor neuron disease mutants. Proc. Natl Acad. Sci. USA 101 (2004) 5976-5981
23. Lindberg M.J., Tibell L., and Oliveberg M. Common denominator of Cu/Zn superoxide dismutase mutants associated with amyotrophic lateral sclerosis: decreased stability of the apo state. Proc. Natl Acad. Sci. USA 99 (2002) 16607-16612
24. Tainer J.A., Getzoff E.D., Beem K.M., Richardson J.S., and Richardson D.C. Determination and analysis of the 2 Å-structure of copper, zinc superoxide dismutase. J. Mol. Biol. 160 (1982) 181-217
25. Strange R.W., Antonyuk S., Hough M.A., Doucette P.A., Rodriguez J.A., Hart P.J., et al. The structure of holo and metal-deficient wild-type human Cu, Zn superoxide dismutase and its relevance to familial amyotrophic lateral sclerosis. J. Mol. Biol. 328 (2003) 877-891
26. Ramachandran G.N., and Sasisekharan V. Conformation of polypeptides and proteins. Adv. Protein Chem. 23 (1968) 283-438
27. Laskowski R.A., Moss D.S., and Thornton J.M. Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231 (1993) 1049-1067
28. Ogihara N.L., Parge H.E., Hart P.J., Weiss M.S., Goto J.J., Crane B.R., et al. Unusual trigonal-planar copper configuration revealed in the atomic structure of yeast copper-zinc superoxide dismutase. Biochemistry 35 (1996) 2316-2321
29. Murphy L.M., Strange R.W., and Hasnain S.S. A critical assessment of the evidence from XAFS and crystallography for the breakage of the imidazolate bridge during catalysis in CuZn superoxide dismutase. Structure 5 (1997) 371-379
30. Hart P.J., Liu H., Pellegrini M., Nersissian A.M., Gralla E.B., Valentine J.S., and Eisenberg D. Subunit asymmetry in the three-dimensional structure of a human CuZnSOD mutant found in familial amyotrophic lateral sclerosis. Protein Sci. 7 (1998) 545-555
31. Hough M.A., and Hasnain S.S. Crystallographic structures of bovine copper-zinc superoxide dismutase reveal asymmetry in two subunits: functionally important three and five coordinate copper sites captured in the same crystal. J. Mol. Biol. 287 (1999) 579-592
32. Strange R.W., Antonyuk S.V., Hough M.A., Doucette P.A., Valentine J.S., and Hasnain S.S. Variable metallation of human superoxide dismutase: atomic resolution crystal structures of Cu-Zn, Zn-Zn and as-isolated wild-type enzymes. J. Mol. Biol. 356 (2006) 1152-1162
33. Ferraroni M., Rypniewski W., Wilson K.S., Viezzoli M.S., Banci L., Bertini I., and Mangani S. The crystal structure of the monomeric human SOD mutant F50E/G51E/E133Q at atomic resolution. The enzyme mechanism revisited. J. Mol. Biol. 288 (1999) 413-426
34. Parge H.E., Hallewell R.A., and Tainer J.A. Atomic structures of wild-type and thermostable mutant recombinant human Cu,Zn superoxide dismutase. Proc. Natl Acad. Sci. USA 89 (1992) 6109-6113
35. DiDonato M., Craig L., Huff M.E., Thayer M.M., Cardoso R.M., Kassmann C.J., et al. ALS mutants of human superoxide dismutase form fibrous aggregates via framework destabilization. J. Mol. Biol. 332 (2003) 601-615
36. Cardoso R.M., Thayer M.M., DiDonato M., Lo T.P., Bruns C.K., Getzoff E.D., and Tainer J.A. 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 (2002) 247-256
37. Lindberg M., Tangrot J., and Oliveberg M. Complete change of the protein folding transition state upon circular permutation. Nature Struct. Biol. 9 (2002) 818-822
38. Banci L., Bertini I., Cantini F., D'Amelio N., and Gaggelli E. Human SOD1 before harboring the catalytic metal: solution structure of copper-depleted, disulfide-reduced form. J. Biol. Chem. 281 (2006) 2333-2337
39. Bertini I., Piccioli M., Viezzoli M.S., Chiu C.Y., and Mullenbach G.T. A spectroscopic characterization of a monomeric analog of copper, zinc superoxide dismutase. Eur. Biophys. J. 23 (1994) 167-176
40. Flory P.J. Theory of elastic mechanisms in fibrous proteins. J. Am. Chem. Soc. 78 (1956) 5222-5235
41. Banci L., Bertini I., Cramaro F., Del Conte R., and Viezzoli M.S. Solution structure of Apo Cu,Zn superoxide dismutase: role of metal ions in protein folding. Biochemistry 42 (2003) 9543-9553
42. Banci L., Bertini I., Cantini F., D'Onofrio M., and Viezzoli M.S. Structure and dynamics of copper-free SOD: the protein before binding copper. Protein Sci. 11 (2002) 2479-2492
43. Banci L., Benedetto M., Bertini I., Del Conte R., Piccioli M., and Viezzoli M.S. Solution structure of reduced monomeric Q133M2 copper, zinc superoxide dismutase (SOD). Why is SOD a dimeric enzyme?. Biochemistry 37 (1998) 11780-11791
44. Getzoff E.D., Tainer J.A., Weiner P.K., Kollman P.A., Richardson J.S., and Richardson D.C. Electrostatic recognition between superoxide and copper, zinc superoxide dismutase. Nature 306 (1983) 287-290
45. Getzoff E.D., Cabelli D.E., Fisher C.L., Parge H.E., Viezzoli M.S., Banci L., and Hallewell R.A. Faster superoxide dismutase mutants designed by enhancing electrostatic guidance. Nature 358 (1992) 347-351
46. Banci L., Bertini I., Del Conte R., Fadin R., Mangani S., and Viezzoli M.S. The solution structure of a monomeric, reduced form of human copper,zinc superoxide dismutase bearing the same charge as the native protein. J. Biol. Inorg. Chem. 4 (1999) 795-803
47. Banci L., Bertini I., Cramaro F., Del Conte R., Rosato A., and Viezzoli M.S. Backbone dynamics of human Cu,Zn superoxide dismutase and of its monomeric F50E/G51E/E133Q mutant: the influence of dimerization on mobility and function. Biochemistry 39 (2000) 9108-9118
48. Malinowski D.P., and Fridovich I. Chemical modification of arginine at the active site of the bovine erythrocyte superoxide dismutase. Biochemistry 18 (1979) 5909-5917
49. Fisher C.L., Cabelli D.E., Tainer J.A., Hallewell R.A., and Getzoff E.D. The role of arginine 143 in the electrostatics and mechanism of Cu,Zn superoxide dismutase: computational and experimental evaluation by mutational analysis. Proteins: Struct. Funct. Genet. 19 (1994) 24-34
50. Beyer Jr W.F., Fridovich I., Mullenbach G.T., and Hallewell R. Examination of the role of arginine-143 in the human copper and zinc superoxide dismutase by site-specific mutagenesis. J. Biol. Chem. 262 (1987) 11182-11187
51. Dupeyrat F., Vidaud C., Lorphelin A., and Berthomieu C. Long distance charge redistribution upon Cu,Zn-superoxide dismutase reduction: significance for dismutase function. J. Biol. Chem. 279 (2004) 48091-48101
52. Maxwell K.L., Wildes D., Zarrine-Afsar A., De Los Rios M.A., Brown A.G., Friel C.T., et al. Protein folding: defining a "standard" set of experimental conditions and a preliminary kinetic data set of two-state proteins. Protein Sci. 14 (2005) 602-616
53. Jonsson P.A., Graffmo K.S., Andersen P.M., Brannstrom T., Lindberg M., Oliveberg M., and Marklund S.L. Disulphide-reduced superoxide dismutase-1 in CNS of transgenic amyotrophic lateral sclerosis models. Brain 129 (2006) 451-464
54. Ahl I.M., Lindberg M.J., and Tibell L.A. Co-expression of yeast copper chaperone (yCCS) and CuZn-superoxide dismutases in Escherichia coli yields protein with high copper contents. Protein Expr. Purif. 37 (2004) 311-319
55. Sutter B., Bounds P.L., and Koppenol W.H. The preparation of apo-Cu,Zn superoxide dismutase by ion-exchange chromatography on iminodiacetic acid-sepharose. Protein Expr. Purif. 19 (2000) 53-56
56. McPherson A. Preparation and Analysis of Protein Crystals (1982), John Wiley and Sons, New York
57. Leslie A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography 26 (1992)
58. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallog. 26 (1993) 795-800
59. Collaborative Computational Project, N. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D 50 (1994) 760-763
60. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D 54 (1998) 905-921
61. Brünger A.T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355 (1992) 472-475
62. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A 47 (1991) 110-119
63. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
64. Schomaker V., and Trueblood K.N. On the rigid-body motion of molecules in crystals. Acta Crystallog. sect. B 24 (1968) 63-76
65. Kleywegt G.J., and Jones T.A. A super position. CCP4/ESF-EACBM Newsletter on Protein Crystallography 31 (1994) 9-14
66. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24 (1991) 946-950
67. Merritt E.A., and Bacon D.J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277 (1997) 505-524
68. Koradi, R., Billeter, M., & Wuthrich, K. (1996). MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55, 29-32.
69. Marklund S., and Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 47 (1974) 469-474
70. Engh R.A., and Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A 47 (1991) 392-400