Glutathionylation potentiates benign superoxide dismutase 1 variants to the toxic forms associated with amyotrophic lateral sclerosis

Scientific Reports

Volumn 3, Issue , 2013, Pages

  McAlary, Luke ^a,b   Yerbury, Justin J ^a,b   Aquilina, J Andrew ^a,b  

^a ILLAWARRA HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE; RECOMBINANT PROTEIN; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CHEMISTRY; GENETICS; HUMAN; KINETICS; MASS SPECTROMETRY; METABOLISM; PROTEIN MULTIMERIZATION;

AMYOTROPHIC LATERAL SCLEROSIS; GLUTATHIONE; HUMANS; KINETICS; MASS SPECTROMETRY; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; SUPEROXIDE DISMUTASE;

EID: 84888218077     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep03275     Document Type: Article

References (27)

1. Valentine, J. S., Doucette, P. A. & Potter, S. Z. Copper-zinc superoxide dismutase and amyotrophic lateral sclerosis. Annu. Rev. Biochem 74, 563-593 (2005). (Pubitemid 40995518)
2. Sibata, N., Asayama, K.,Hirano, A. & Kobayashi, M. Immunohistochemical study on superoxide dismutases in spinal cords from autopsied patients with amyotrophic lateral sclerosis. Dev. Neurosci. 18, 492-498 (1996). (Pubitemid 26371593)
3. Bosco, D. A. et al.Wild-Type andMutant SOD1 Share an Aberrant Conformation and a Common Pathogenic Pathway in ALS. Nat. Neurosci 13, 1396-1403 (2010).
4. Forsberg, K. et al.Novel antibodies reveal inclusions containing non-native SOD1 in sporadic ALS patients. PLoS ONE 5, e11552 (2010).
5. Pokrishevsky, E. et al. Aberrant localization of FUS and TDP43 is associated with misfolding of SOD1 in Amyotrophic lateral sclerosis. PLoS ONE 7, e35050 (2012).
6. Rakhit, R. et al. 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 (2004). (Pubitemid 38618950)
7. Svensson, A. E. et al.Metal-free ALS variants of dimeric human Cu,Zn-superoxide dismutase have enhanced populations of monomeric species. PLoS ONE 5, 1-10 (2010).
8. Ray, S. S. et al. An intersubunit disulfide bond prevents in vitro aggregation of a superoxide dismutase-1 mutant linked to familial Amyotrophic lateral sclerosis. Biochem 43, 4899-4905 (2004). (Pubitemid 38544443)
9. Wilcox, K. C. et al. Modifications of Superoxide Disumutase (SOD1) in Human Erythrocytes: a Possible Role in Amyotrophic Lateral Sclerosis. J. Biol. Chem 284, 13940-13947 (2009).
10. Auclair, J. R., Boggio, K. J., Petsko, G. A., Ringe, D. & Agar, J. N. Strategies for stabilizing superoxide dismutase (SOD1), the protein destabilized in the most common form of familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 107, 21394-21399 (2010).
11. Redler, R. et al. Glutathionylation at Cys-111 Induces Dissocation of Wild Type and FALS Mutant SOD1 Dimers. Biochem 50, 7057-7066 (2011).
12. Sobott, F., Hernandez, H., McCammon, M. G., Tito, M. A. & Robinson, C. V. A tandem mass spectrometer for improved transmission and analysis of large macromolecular assemblies. Anal. Chem. 74 (2002).
13. Rostom, A. A., Tame, J. R. H., Ladbury, J. E. & Robinson, C. V. Specificity and interactions of the protein OppA: Partioning solvent binding effects using mass spectrometry. J. Mol. Biol. 296, 269-279 (2000).
14. Furukawa, Y., Torres, A. S. & O'Halloran, T. V. Oxygen-induced maturation of SOD1: A key role for disulfide formation by the copper chaperone (CCS). EMBO J. 23, 2872-2881 (2004). (Pubitemid 39013559)
15. Leinweber, B. et al.Aggregation of ALSmutant superoxide dismutase expressed in Escherichia coli. Free Radic. Biol. Med 36, 911-918 (2004). (Pubitemid 38352907)
16. Lindberg, M. J., Normark, J., Holmgren, A. & Oliveberg, M. Folding of human superoxide dismutase: disulfide reduction prevents dimerization and produces marginally stable monomers. Proc. Natl. Acad. Sci. USA 101, 15893-15898 (2004). (Pubitemid 39507898)
17. Tainer, J. A., Getzoff, E. D., Beem, K. M., Richardson, J. S. & Richardson, D. C. Determination and analysis of the 2A? structure of copper, zinc superoxide dismutase. J. Mol. Bio 160, 181-217 (1982). (Pubitemid 13239300)
18. Wang, Q., Johnson, J. L. & Agar, N. Y. R. N. A. J. Protein Aggregation and Protein Instability Govern Familial Amyotrophic Lateral Sclerosis Patient Survival. PLoS Bio 6, 1508-1526 (2008).
19. Rumfeldt, J. A. O., Stathopulos, P. B., Chakrabartty, A., Lepock, J. R. & Meiering, E. M. Mechanism and thermodynamics of guanidinium cholride-induced denaturation of ALS-associated mutant Cu,Zn superoxide dismutases. J. Mol. Bio 355, 106-123 (2006). (Pubitemid 41774143)
20. Perry, J. J. P., Shin, D. S., Getzoff, E. D. & Tainer, J. A. The structural biochemistry of the superoxide dismutases. Biochim. Biophys. Acta 1804, 245-262 (2010).
21. Weisberg, S. J. et al. Compartmentalization of superoxide dismutase 1 (SOD1G93A) aggregates determines their toxicity. Proc. Natl. Acad. Sci. 109, 15811-15816 (2012).
22. Barber, S. C.&Shaw, P. J. Oxidative stress in ALS: Key role in motor neuron injury and therapeutic target. Free. Radic. Biol. Med. 48, 629-641 (2010).
23. Dalle-Donne, I., Rossi, R., Giustarini, D., Colombo, R. & Milzani, A. Sglutathionylation in protein redox regulation. Free. Radic. Biol. Med 43, 883-898 (2007).
24. Tohgi, H. et al. Increase in oxidized NO products and reduction in oxidized glutathione in cerebrospinal fluid from patients with sporadic form of amyotrophic lateral sclerosis. Neurosci. Lett. 260, 204-206 (1999). (Pubitemid 29089196)
25. Stansell, M. J. & Deutsch, H. F. The levels of catalase and of erythrocuprein in human erythrocytes. Clin. Chim. Acta 14, 598-607 (1966).
26. Ruotolo, B. T., Benesch, J. L. P., Sandercock, A. M., Hyung, S. & Robinson, C. V. Ion mobility-mass spectrometry analysis of large protein complexes. Nat. Protoc 3, 1139-1152 (2008).
27. Rose, R. J. et al. Quantitative analysis of the interaction strength and dynamics of human IgG4 half molecules by native mass spectrometry. Structure 19, 1274-1282 (2011).