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

Volumn 46, Issue 35, 2007, Pages 9953-9962

  Banci, Lucia ^a,b   Bertini, Ivano ^a   D'Amelio, Nicola ^a   Libralesso, Elisa ^a   Turano, Paola ^a   Valentine, Joan Selverstone ^c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b FiorGen Foundation   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISEASES; MOLECULAR STRUCTURE; MUTAGENESIS; PLASTICITY; TOXICITY;

AMYOTROPHIC LATERAL SCLEROSIS MUTANT GLYCINE 37; METALATION; MUTANT PROTEIN;

PROTEINS;

APOPROTEIN; ARGININE; COPPER ZINC SUPEROXIDE DISMUTASE; GLYCINE; MUTANT PROTEIN; SUPEROXIDE DISMUTASE; TRIFLUOROETHANOL;

ALPHA HELIX; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BETA CHAIN; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME STABILITY; ENZYME STRUCTURE; MUTATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION;

AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; APOENZYMES; ARGININE; COPPER; ELECTRON SPIN RESONANCE SPECTROSCOPY; GLYCINE; HUMANS; HYDROGEN BONDING; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTAGENESIS; MUTATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; SUPEROXIDE DISMUTASE; TRANSITION TEMPERATURE; TRIFLUOROETHANOL; ZINC;

EID: 34548513550     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700620r     Document Type: Article

References (38)

1. Pasinelli, P., and Brown, R. H. (2006) Molecular biology of amyotrophic lateral sclerosis: insights from genetics, Nat. Rev. Neurosci. 7, 710-723.
2. Boillee, S., Vande Velde, C., and Cleveland, D. W. (2006) ALS: A disease of motor neurons and their nonneuronal neighbors, Neuron 52, 39-59.
3. Wang, J., Xu, G., and Borchelt, D. R. (2006) Mapping Superoxide Dismutase 1 Domains of Non-Native Interaction: Roles of Intra-and Intermolecular Disulfide Bonding in Aggregation, J. Neurochem. 96, 1277-1288.
4. Wang, J., Xu, G. L., Slunt, H. H., Gonzales, V., Coonfield, M., Fromholt, D., Copeland, N. G., Jenkins, N. A., and Borchelt, D. R. (2005) Coincident thresholds of mutant protein for paralytic disease and protein aggregation caused by restrictively expressed superoxide dismutase cDNA, Neurobiol. Dis. 20, 943-952.
5. Valentine, J. S., Doucette, P. A., and Potter, S. Z. (2005) Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis, Annu. Rev. Biochem. 74, 563-593.
6. Elam, J. S., Taylor, A. B., Strange, R., Antonyuk, S., 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, Nature Struct. Biol. 10, 461-467.
7. 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.
8. Hart, P. J., Liu, H., Pellegrini, M., Nersissian, A. M., Gralla, E. B., Valentine, J. S., and Eisenberg, D. (1998) Subunit asymmetry in the three-dimensional structure of a human CuZnSOD mutant found in familial amyotrophic lateral sclerosis, Protein Sci. 7, 545-555.
9. 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.
10. Rodriguez, J. A., Valentine, J. S., Eggers, D. K., Roe, J. A., Tiwari, A., Brown, R. H. J., and Hayward, L. J. (2002) Familial amyotrophic lateral sclerosis-associated mutations decrease the thermal stability of distinctly metallated species of human copper-zinc superoxide dismutase, J. Biol. Chem. 277, 15932-15937.
11. Rodriguez, J. A., Shaw, B. F., Durazo, A., Sohn, S. H., Doucette, P. A., Nersissian, A. M., Faull, K. F., Eggers, D. K., Tiwari, A., Hayward, L. J., and Valentine, J. S. (2005) Destabilization of apoprotein is insufficient to explain Cu,Zn-superoxide dismutase-linked ALS pathogenesis, Proc. Natl. Acad. Sci. U.S.A. 102, 10516-10521.
12. Julien, J. P., and Kriz, J. (2006) Transgenic mouse models of amyotrophic lateral sclerosis, Biochim. Biophys. Acta 1762, 1013-1024.
13. Wang, J., Slunt, H., Gonzales, V., Fromholt, D., Coonfield, M., Copeland, N. G., Jenkins, N. A., and Borchelt, D. R. (2003) Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature, Hum. Mol. Genet. 12, 2753-2764.
14. Ferri, A., Cozzolino, M., Crosio, C., Nencini, M., Casciati, A., Gralla, E. B., Rotilio, G., Valentine, J. S., and Carri, M. T. (2006) Familial ALS-superoxide dismutases associate with mitochondria and shift their redox potentials, Proc. Natl. Acad. Sci. U.S.A. 103, 13860-13865.
15. Shipp, E., Cantini, F., Bertini, I., Valentine, J. S., and Banci, L. (2003) Dynamic properties of the G93A mutant of copper-zinc superoxide dismutase as detected by NMR spectroscopy: implications for the pathology of familial amyotrophic lateral sclerosis, Biochemistry 42, 1890-1899.
16. Banci, L., Bertini, I., D'Amelio, N., Gaggelli, E., Libralesso, E., Matecko, I., Turano, P., and Valentine, J. S. (2005) Fully metallated S134N Cu,Zn-Superoxide Dismutase displays abnormal mobility and intermolecular contacts in solution, J. Biol. Chem. 280, 35815-35821.
17. Hallewell, R. A., Imlay, K. C., Laria, I., Gallegos, C., Fong, N. M., Irvine, B., Cabelli, D. E., Bielski, B. H. J., Olson, P., Mullenbach, G. T., and Cousens, L. S. (1991) Thermostabilization of recombinant CuZn superoxide dismutases by replacement of free cysteines, Biochem. Biophys. Res. Commun. 181, 474-480.
18. Lepock, 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.
19. 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, 6109-6114.
20. Banci, L., Benedetto, M., Bertini, I., Del Conte, R., Piccioli, M., Richert, T., and Viezzoli, M. S. (1997) Assignment of backbone NMR resonances and secondary structural elements of a reduced monomeric mutant of copper/zinc superoxide dismutase, Magn. Reson. Chem. 35, 845-853.
21. Getzoff, E. D., Cabelli, D. E., Fisher, C. L., Parge, H. E., Viezzoli, M. S., Banci, L., and Hallewell, R. A. (1992) Faster Superoxide Dismutase Mutants designed by Enhancing Electrostatic Guidance, Nature 358, 347-351.
22. McCord, J. M., and Fridovich, I. (1969) The utility of superoxide dismutase in studying free radical reactions. I. Radicals generated by the interaction of sulfite, dimethyl sulfoxide, and oxygen, J. Biol. Chem. 244, 6056-6063.
23. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single quantum NMR spectroscopy of aqueous solutions, J. Biomol. NMR 2, 661-666.
24. Van Dijk, A. A., Scheek, R. M., Dijkstra, K., Wolters, G. K., and Robillard, G. T. (1992) Characterization of the protonation and hydrogen bonding state of the histidine residues in IIAmtl, a domain of the phospohenolypyruvate-dependent mannitol-specific transport protein, Biochemistry 31, 9063-9072.
25. 15N-labeled histidine in aqueous solution, J. Am. Chem. Soc. 99, 8149-8159.
26. 1H NMR investigation, Biochemistry 34, 12265-12275.
27. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease, Biochemistry 28, 8972-8979.
28. Palmer, A. G., III, Skelton, N. J., Chazin, W. J., Wright, P. E., and Rance, M. (1992) Suppression of the effects of cross-correlation between dipolar and anisotropic chemical shift relaxation mechanisms in the measurements of spin-spin relaxation rates, Mol. Phys. 75, 699-711.
29. 15N relaxation using inverse detected two-dimensional NMR spectroscopy; the central helix is flexible, Biochemistry 31, 5269-5278.
30. 2 values in proteins, J. Magn. Reson. 97, 359-375.
31. Peng, J. W., and Wagner, G. (1992) Mapping of spectral density function using heteronuclear NMR relaxation measurements, J. Magn. Reson. 98, 308-332.
32. Pelton, J. G., Torchia, D. A., Meadow, N. D., and Roseman, S. (1993) Tautomeric states of the active-site histidines of phosphorylated and unphospohorylated IIIglc, a signal transducing protein from Escherichia coli, using two dimesnional heteronuclear NMR techniques, Protein Sci. 2, 543-558.
33. Assfalg, M., Banci, L., Bertini, I., Turano, P., and Vasos, P. R. (2003) Superoxide dismutase folding/unfolding pathway: role of the metal ions in modulating structural and dynamical features, J. Mol. Biol. 330, 145-158.
34. Strange, R. W., Antonyuk, S. V., Hough, M. A., Doucette, P. A., Valentine, J. S., and Hasnain, S. S. (2006) 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, 1152-1162.
35. Banci, L., Bertini, I., Cramaro, F., Del Conte, R., and Viezzoli, M. S. (2003) Solution structure of apo Cu,Zn superoxide dismutase: the role of metal ions in protein folding, Biochemistry 42, 9543-9553.
36. Tainer, J. A., Getzoff, E. D., Beem, K. M., Richardson, J. S., and Richardson, D. C. (1982) Determination and Analysis of 2 A Structure of Copper Zinc Superoxide Dismutase, J. Mol. Biol. 160, 181-217.
37. Starzyk, A., Barber-Armstrong, W., Sridharan, M., and Decatur, S. M. (2005) Spectroscopic evidence for backbone desolvation of helical peptides by 2,2,2-trifluoroethanol: An isotope-edited FTIR study, Biochemistry 44, 369-376.
38. Banci, L., Bertini, I., Girotto, S., Martinelli, M., Vieru, M., Whitelegge, J., Durazo, A., and Valentine, J. S. (2007) Metal-free SOD1 forms amyloid-like oligomers: a possible general mechanism for familial ALS; Proc. Natl. Acad. Sci. U.S.A. 104, 11263-11267.