Mutant SOD1 forms ion channel: Implications for ALS pathophysiology

Neurobiology of Disease

Volumn 45, Issue 3, 2012, Pages 831-838

  Allen, Michael J ^a   Lacroix, Jérome J ^a   Ramachandran, Srinivasan ^b   Capone, Ricardo ^b   Whitlock, Jenny L ^a   Ghadge, Ghanashyam D ^a   Arnsdorf, Morton F ^a   Roos, Raymond P ^a   Lal, Ratnesh ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

A4V; Amyotrophic lateral sclerosis; Atomic force microscopy; DiBAC 4(3) membrane potential measurement; Fluo 4 calcium assay; Protein misfolding; Superoxide dismutase

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; ION CHANNEL; PROTEOLIPOSOME;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GENE MUTATION; HOMEOSTASIS; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; ULTRACENTRIFUGATION;

ALANINE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BIOPHYSICAL PHENOMENA; BIOPHYSICS; CALCIUM; CELL LINE, TUMOR; ELECTRIC STIMULATION; HUMANS; ION CHANNEL GATING; LIPID BILAYERS; MEMBRANE POTENTIALS; MEMBRANES, ARTIFICIAL; MICE; MICROSCOPY, ATOMIC FORCE; MUTATION; NEUROBLASTOMA; PATCH-CLAMP TECHNIQUES; PROTEIN CONFORMATION; SUPEROXIDE DISMUTASE; TIME FACTORS; TRANSFECTION; VALINE;

EID: 84856569186     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.08.031     Document Type: Article

References (51)

1. Alexianu M.E., et al. The role of calcium-binding proteins in selective motoneuron vulnerability in amyotrophic lateral sclerosis. Ann. Neurol. 1994, 36:846-858.
2. Arimura K., et al. Isaacs' syndrome as a potassium channelopathy of the nerve. Muscle Nerve Suppl. 2002, 11:S55-S58.
3. Arispe N., et al. Giant multilevel cation channels formed by Alzheimer disease amyloid beta-protein [A beta P-(1-40)] in bilayer membranes. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:10573-10577.
4. Arispe N., et al. Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:567-571.
5. Barber S.C., et al. Oxidative stress in ALS: a mechanism of neurodegeneration and a therapeutic target. Biochim. Biophys. Acta 2006, 1762:1051-1067.
6. Beal M.F. Mitochondria and the pathogenesis of ALS. Brain 2000, 123(Pt 7):1291-1292.
7. Beers D.R., et al. Parvalbumin overexpression alters immune-mediated increases in intracellular calcium, and delays disease onset in a transgenic model of familial amyotrophic lateral sclerosis. J. Neurochem. 2001, 79:499-509.
8. Boillee S., et al. ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 2006, 52:39-59.
9. Borthwick G.M., et al. Mitochondrial enzyme activity in amyotrophic lateral sclerosis: implications for the role of mitochondria in neuronal cell death. Ann. Neurol. 1999, 46:787-790.
10. Bruening W., et al. Up-regulation of protein chaperones preserves viability of cells expressing toxic Cu/Zn-superoxide dismutase mutants associated with amyotrophic lateral sclerosis. J. Neurochem. 1999, 72:693-699.
11. Bruijn L.I., et al. Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 1998, 281:1851-1854.
12. Bruijn L.I., et al. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 2004, 27:723-749.
13. Camerino D.C., et al. Ion channel pharmacology. Neurotherapeutics 2007, 4:184-198.
14. Capone R., et al. Antimicrobial protegrin-1 forms ion channels: molecular dynamic simulation, atomic force microscopy, and electrical conductance studies. Biophys. J. 2010, 98:2644-2652.
15. Cleveland D.W., Rothstein J.D. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2001, 2:806-819.
16. Elam J.S., et al. Amyloid-like filaments and water-filled nanotubes formed by SOD1 mutant proteins linked to familial ALS. Nat. Struct. Biol. 2003, 10:461-467.
17. Engel A., Gaub H.E. Structure and mechanics of membrane proteins. Annu. Rev. Biochem. 2008, 77:127-148.
18. Ezzi S.A., et al. Wild-type superoxide dismutase acquires binding and toxic properties of ALS-linked mutant forms through oxidation. J. Neurochem. 2007, 102:170-178.
19. Galaleldeen A., et al. Structural and biophysical properties of metal-free pathogenic SOD1 mutants A4V and G93A. Arch. Biochem. Biophys. 2009, 492:40-47.
20. Getzoff E.D., Tainer J.A. Superoxide dismutase as a model ion channel. Ion Channel Reconstitution 1986, 57-74. Plenum Press, New York. C. Miller (Ed.).
21. Ghadge G.D., et al. Truncated wild-type SOD1 and FALS-linked mutant SOD1 cause neural cell death in the chick embryo spinal cord. Neurobiol. Dis. 2006, 21:194-205.
22. Grosskreutz J., et al. Role of mitochondria in kainate-induced fast Ca2+ transients in cultured spinal motor neurons. Cell Calcium 2007, 42:59-69.
23. Gruzman A., et al. Common molecular signature in SOD1 for both sporadic and familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:12524-12529.
24. Gurney M.E., et al. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 1994, 264:1772-1775.
25. Hayward L.J., et al. Decreased metallation and activity in subsets of mutant superoxide dismutases associated with familial amyotrophic lateral sclerosis. J. Biol. Chem. 2002, 277:15923-15931.
26. Hirakura Y., et al. Alzheimer amyloid abeta1-42 channels: effects of solvent, pH, and Congo Red. J. Neurosci. Res. 1999, 57:458-466.
27. Ionov I.D. Survey of ALS-associated factors potentially promoting Ca2+ overload of motor neurons. Amyotroph. Lateral Scler. 2007, 8:260-265.
28. Israelson A., et al. Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS. Neuron 2010, 67:575-587.
29. Jang H., et al. Truncated beta-amyloid peptide channels provide an alternative mechanism for Alzheimer's Disease and Down syndrome. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:6538-6543.
30. Jang H., et al. Structural convergence among diverse, toxic beta-sheet ion channels. J. Phys. Chem. B 2010, 114:9445-9451.
31. Johnston J.A., et al. 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. U.S.A. 2000, 97:12571-12576.
32. Kabashi E., et al. Oxidized/misfolded superoxide dismutase-1: the cause of all amyotrophic lateral sclerosis?. Ann. Neurol. 2007, 62:553-559.
33. Kuwabara S., Kanai K. Altered axonal ion channel function in amyotrophic lateral sclerosis. Brain Nerve 2007, 59:1109-1115.
34. Lin H., et al. Amyloid beta protein forms ion channels: implications for Alzheimer's disease pathophysiology. FASEB J. 2001, 15:2433-2444.
35. Marambaud P., et al. Calcium signaling in neurodegeneration. Mol. Neurodegener. 2009, 4:20.
36. Menzies F.M., et al. Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis. Brain 2002, 125:1522-1533.
37. Mueller P., et al. Reconstitution of cell membrane structure in vitro and its transformation into an excitable system. Nature 1962, 194:979-980.
38. Pasinelli P., et al. Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron 2004, 43:19-30.
39. Pieri M., et al. Altered excitability of motor neurons in a transgenic mouse model of familial amyotrophic lateral sclerosis. Neurosci. Lett. 2003, 351:153-156.
40. Quist A., et al. Amyloid ion channels: a common structural link for protein-misfolding disease. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:10427-10432.
41. Reaume A.G., et al. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 1996, 13:43-47.
42. Rosen D.R., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
43. Sandelin E., et al. Amyotrophic lateral sclerosis-associated copper/zinc superoxide dismutase mutations preferentially reduce the repulsive charge of the proteins. J. Biol. Chem. 2007, 282:21230-21236.
44. Scholle M.D., et al. In vivo biotinylated proteins as targets for phage-display selection experiments. Protein Expr. Purif. 2004, 37:243-252.
45. Seetharaman S.V., et al. Disrupted zinc-binding sites in structures of pathogenic SOD1 variants D124V and H80R. Biochemistry 2010, 49:5714-5725.
46. Shirwany N.A., et al. The amyloid beta ion channel hypothesis of Alzheimer's disease. Neuropsychiatr. Dis. Treat. 2007, 3:597-612.
47. Tiwari A., et al. Aberrantly increased hydrophobicity shared by mutants of Cu,Zn-superoxide dismutase in familial amyotrophic lateral sclerosis. J. Biol. Chem. 2005, 280:29771-29779.
48. Urushitani M., et al. N-methyl-D-aspartate receptor-mediated mitochondrial Ca(2+) overload in acute excitotoxic motor neuron death: a mechanism distinct from chronic neurotoxicity after Ca(2+) influx. J. Neurosci. Res. 2001, 63:377-387.
49. Urushitani M., et al. The endoplasmic reticulum-Golgi pathway is a target for translocation and aggregation of mutant superoxide dismutase linked to ALS. FASEB J. 2008, 22:2476-2487.
50. Vande Velde C., et al. Selective association of misfolded ALS-linked mutant SOD1 with the cytoplasmic face of mitochondria. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4022-4027.
51. Zhao W., et al. Extracellular mutant SOD1 induces microglial-mediated motoneuron injury. Glia 2010, 58:231-243.