Role of mutant SOD1 disulfide oxidation and aggregation in the pathogenesis of familial ALS

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 19, 2009, Pages 7774-7779

  Karch, Celeste M ^a   Prudencio, Mercedes ^a   Winkler, Duane D ^b   Hart, P John ^b,c   Borchelt, David R ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Neurodegenerative disease; Protein misfolding

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CROSS LINKING; DEGENERATIVE DISEASE; DISULFIDE BOND; MOUSE; NONHUMAN; OXIDATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DISEASE MODELS, ANIMAL; DISULFIDES; HUMANS; MICE; MICE, TRANSGENIC; MUTATION; NEURONS; OXIDATIVE STRESS; SOLUBILITY; SUPEROXIDE DISMUTASE;

MUS; MUS MUSCULUS;

EID: 66049156169     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0902505106     Document Type: Article

References (33)

1. Rosen DR, et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62. (Pubitemid 23087289)
2. Borchelt DR, et al. (1994) Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Natl Acad Sci USA 91:8292-8296. (Pubitemid 24253933)
3. Potter SZ, Valentine JS (2003) The perplexing role of copper-zinc superoxide dismutase in amyotrophic lateral sclerosis (Lou Gehrig's disease). J Biol Inorg Chem 8:373-380. (Pubitemid 36578189)
4. Valentine JS, Hart PJ (2003) Misfolded CuZnSOD and amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 100:3617-3622. (Pubitemid 36418082)
5. Ratovitski T, et al. (1999) Variation in the biochemical/biophysical properties of mutant superoxide dismutase 1 enzymes and the rate of disease progression in familial amyotrophic lateral sclerosis kindreds. Hum Mol Genet 8:1451-1460. (Pubitemid 29374078)
6. Reaume AG, et al. (1996) Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat Genet 13:43-47. (Pubitemid 26139292)
7. Johnston JA, Dalton MJ, Gurney ME, Kopito RR (2000) Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 97:12571-12576.
8. Wang J, et al. (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. (Pubitemid 37407112)
9. Turner BJ, Talbot K (2008) Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog Neurobiol 85:94-134.
10. Wang J, Xu G, Borchelt DR (2002) High molecular weight complexes of mutant superoxide dismutase 1: Age-dependent and tissue-specific accumulation. Neurobiol Dis 9:139-148. (Pubitemid 34261210)
11. Jonsson PA, et al. (2006) Disulphide-reduced superoxide dismutase-1 in CNS of transgenic amyotrophic lateral sclerosis models. Brain 129:451-464. (Pubitemid 43164368)
12. Furukawa Y, et al. (2006) Disulfide cross-linked protein represents a significant fraction of ALS-associated Cu, Zn-superoxide dismutase aggregates in spinal cords of model mice. Proc Natl Acad Sci USA 103:7148-7153.
13. Karch CM, Borchelt DR (2008) A limited role for disulfide cross-linking in the aggregation of mutant SOD1 linked to familial amyotrophic lateral sclerosis. J Biol Chem 283:13528-13537.
14. Jonsson PA, et al. (2004) Minute quantities of misfolded mutant superoxide dismutase-1 cause amyotrophic lateral sclerosis. Brain 127:73-88. (Pubitemid 38055347)
15. Banci L, et al. (2007) Metal-free superoxide dismutase forms soluble oligomers under physiological conditions: A possible general mechanism for familial ALS. Proc Natl Acad Sci USA 104:11263-11267. (Pubitemid 47175129)
16. Zetterstrom P, et al. (2007) Soluble misfolded subfractions of mutant superoxide dismutase-1s are enriched in spinal cords throughout life in murine ALS models. Proc Natl Acad Sci USA 104:14157-14162. (Pubitemid 350003351)
17. Wang J, Xu G, Borchelt DR (2006) Mapping superoxide dismutase 1 domains of non-native interaction: Roles of intra- and intermolecular disulfide bonding in aggregation. J Neurochem 96:1277-1288.
18. Furukawa Y, et al. (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.
19. Chattopadhyay M, et al. (2008) Initiation and elongation in fibrillation of ALS-linked superoxide dismutase. Proc Natl Acad Sci USA 105:18663-18668.
20. Wang J, et al. (2007) Disease-associated mutations at copper ligand histidine residues of superoxide dismutase 1 diminish the binding of copper and compromise dimer stability. J Biol Chem 282:345-352. (Pubitemid 47076602)
21. Furukawa Y, Torres AS, O'Halloran TV (2004) Oxygen-induced maturation of SOD1: A key role for disulfide formation by the copper chaperone CCS. EMBO J 23:2872-2881. (Pubitemid 39013559)
22. Hart PJ (2006) Pathogenic superoxide dismutase structure, folding, aggregation and turnover. Curr Opin Chem Biol 10:131-138.
23. Proescher JB, Son M, Elliott JL, Culotta VC (2008) Biological effects of CCS in the absence of SOD1 enzyme activation: Implications for disease in a mouse model for ALS. Hum Mol Genet 17:1728-1737.
24. Wang J, et al. (2002) Fibrillar inclusions and motor neuron degeneration in transgenic mice expressing superoxide dismutase 1 with a disrupted copper-binding site. Neurobiol Dis 10:128-138.
25. Fischer LR, et al. (2004) Amyotrophic lateral sclerosis is a distal axonopathy: Evidence in mice and man. Exp Neurol 185:232-240. (Pubitemid 38084849)
26. Kennel PF, Finiels F, Revah F, Mallet J (1996) Neuromuscular function impairment is not caused by motor neurone loss in FALS mice: An electromyographic study. NeuroReport 7:1427-1431. (Pubitemid 26281007)
27. Hegedus J, Putman CT, Gordon T (2007) Time course of preferential motor unit loss in the SOD1 G93A mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 28:154-164. (Pubitemid 47615455)
28. Borchelt DR, et al. (1998) Axonal transport of mutant superoxide dismutase 1 and focal axonal abnormalities in the proximal axons of transgenic mice. Neurobiol Dis 5:27-35. (Pubitemid 28361649)
29. Watanabe M, et al. (2001) Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol Dis 8:933-941. (Pubitemid 34017087)
30. Son M, et al. (2007) Overexpression of CCS in G93A-SOD1 mice leads to accelerated neurological deficits with severe mitochondrial pathology. Proc Natl Acad Sci USA 104:6072-6077. (Pubitemid 47175660)
31. Wong PC, et al. (1995) An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14:1105-1116.
32. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
33. Bruijn LI, et al. (1997) ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18:327-338. (Pubitemid 27111114)