ALS-causing SOD1 mutations promote production of copper-deficient misfolded species

Journal of Molecular Biology

Volumn 409, Issue 5, 2011, Pages 839-852

  Ip, Philbert ^a   Mulligan, Vikram Khipple ^a   Chakrabartty, Avijit ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

amyotrophic lateral sclerosis; Cu,Zn superoxide dismutase; metal binding; misfolding; protein folding kinetics

Indexed keywords

COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; DIMER; GUANIDINE; MONOMER; TRYPTOPHAN; ZINC;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CONFORMATIONAL TRANSITION; COPPER DEFICIENCY; FLUORESCENCE; HUMAN; HUMAN TISSUE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN STRUCTURE; PROTEIN UNFOLDING; SIGNAL TRANSDUCTION; SPECIES; WILD TYPE; ZINC DEFICIENCY;

EID: 79958070512     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.04.027     Document Type: Article

References (66)

1. Mitchell J.D., and Borasio G.D. Amyotrophic lateral sclerosis Lancet 369 2007 2031 2041
2. Majoor-Krakauer D., Willems P.J., and Hofman A. Genetic epidemiology of amyotrophic lateral sclerosis Clin. Genet. 63 2003 83 101 (Pubitemid 36949902)
3. Rakhit R., and Chakrabartty A. Structure, folding, and misfolding of Cu,Zn superoxide dismutase in amyotrophic lateral sclerosis Biochim. Biophys. Acta 1762 2006 1025 1037 (Pubitemid 44781177)
4. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., and Hentati A. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis Nature 362 1993 59 62 (Pubitemid 23087289)
5. Deng H.X., Hentati A., Tainer J.A., Iqbal Z., Cayabyab A., and Hung W.Y. Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase Science 261 1993 1047 1051 (Pubitemid 23300865)
6. McCord J.M., and Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) J. Biol. Chem. 244 1969 6049 6055
7. Borchelt D.R., Lee M.K., Slunt H.S., Guarnieri M., Xu Z.S., and Wong P.C. Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity Proc. Natl Acad. Sci. USA 91 1994 8292 8296 (Pubitemid 24253933)
8. Reaume A.G., Elliott J.L., Hoffman E.K., Kowall N.W., Ferrante R.J., and Siwek D.F. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury Nat. Genet. 13 1996 43 47 (Pubitemid 26139292)
9. Gurney M.E., Pu H., Chiu A.Y., Dal Canto M.C., Polchow C.Y., and Alexander D.D. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation Science 264 1994 1772 1775 (Pubitemid 24227760)
10. Crow J.P., Sampson J.B., Zhuang Y., Thompson J.A., and Beckman J.S. Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite J. Neurochem. 69 1997 1936 1944 (Pubitemid 27452740)
11. Estevez A.G., Crow J.P., Sampson J.B., Reiter C., Zhuang Y., and Richardson G.J. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase Science 286 1999 2498 2500
12. Wang J., Slunt H., Gonzales V., Fromholt D., Coonfield M., and Copeland N.G. Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature Hum. Mol. Genet. 12 2003 2753 2764 (Pubitemid 37407112)
13. Kerman A., Liu H.N., Croul S., Bilbao J., Rogaeva E., and Zinman L. Amyotrophic lateral sclerosis is a non-amyloid disease in which extensive misfolding of SOD1 is unique to the familial form Acta Neuropathol. 119 2010 335 344
14. Ince P.G., Lowe J., and Shaw P.J. Amyotrophic lateral sclerosis: current issues in classification, pathogenesis and molecular pathology Neuropathol. Appl. Neurobiol. 24 1998 104 117 (Pubitemid 28175040)
15. Shibata N., Hirano A., Kobayashi M., Siddique T., Deng H.X., and Hung W.Y. Intense superoxide dismutase-1 immunoreactivity in intracytoplasmic hyaline inclusions of familial amyotrophic lateral sclerosis with posterior column involvement J. Neuropathol. Exp. Neurol. 55 1996 481 490 (Pubitemid 26112102)
16. Shibata N., Hirano A., Kobayashi M., Sasaki S., Kato T., and Matsumoto S. Cu/Zn superoxide dismutase-like immunoreactivity in Lewy body-like inclusions of sporadic amyotrophic lateral sclerosis Neurosci. Lett. 179 1994 149 152 (Pubitemid 24298580)
17. Lowe J. New pathological findings in amyotrophic lateral sclerosis J. Neurol. Sci. 124 1994 38 51
18. Takahashi K., Nakamura H., and Okada E. Hereditary amyotrophic lateral sclerosis. Histochemical and electron microscopic study of hyaline inclusions in motor neurons Arch. Neurol. 27 1972 292 299
19. Liu H.N., Sanelli T., Horne P., Pioro E.P., Strong M.J., and Rogaeva E. Lack of evidence of monomer/misfolded superoxide dismutase-1 in sporadic amyotrophic lateral sclerosis Ann. Neurol. 66 2009 75 80
20. Rakhit R., Robertson J., Vande Velde C., Horne P., Ruth D.M., and Griffin J. An immunological epitope selective for pathological monomer-misfolded SOD1 in ALS Nat. Med. 13 2007 754 759 (Pubitemid 46889748)
21. Hwang Y.M., Stathopulos P.B., Dimmick K., Yang H., Badiei H.R., and Tong M.S. Non-amyloid aggregates arising from mature Cu/Zn superoxide dismutases resemble those observed in amyotrophic lateral sclerosis J. Biol. Chem. 285 2010 41701 41711
22. Stathopulos P.B., Rumfeldt J.A., Scholz G.A., Irani R.A., Frey H.E., and Hallewell R.A. Cu/Zn superoxide dismutase mutants associated with amyotrophic lateral sclerosis show enhanced formation of aggregates in vitro Proc. Natl Acad. Sci. USA 100 2003 7021 7026 (Pubitemid 36706386)
23. 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 (Pubitemid 38618950)
24. Rakhit R., Cunningham P., Furtos-Matei A., Dahan S., Qi X.F., and Crow J.P. Oxidation-induced misfolding and aggregation of superoxide dismutase and its implications for amyotrophic lateral sclerosis J. Biol. Chem. 277 2002 47551 47556 (Pubitemid 36159274)
25. Kirkitadze M.D., Bitan G., and Teplow D.B. Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: the emerging role of oligomeric assemblies J. Neurosci. Res. 69 2002 567 577 (Pubitemid 34966869)
26. Carrell R.W., and Gooptu B. Conformational changes and disease-serpins, prions and Alzheimer's Curr. Opin. Struct. Biol. 8 1998 799 809 (Pubitemid 29004679)
27. Biliaderis C.G., Weselake R.J., Petkau A., and Friesen A.D. A calorimetric study of human CuZn superoxide dismutase Biochem. J. 248 1987 981 984 (Pubitemid 18012737)
28. Rodriguez J.A., Valentine J.S., Eggers D.K., Roe J.A., Tiwari A., Brown Jr.R.H., and Hayward L.J. Familial amyotrophic lateral sclerosis-associated mutations decrease the thermal stability of distinctly metallated species of human copper/zinc superoxide dismutase J. Biol. Chem. 277 2002 15932 15937 (Pubitemid 34967874)
29. 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 (Pubitemid 36034020)
30. Stathopulos P.B., Rumfeldt J.A., Karbassi F., Siddall C.A., Lepock J.R., and Meiering E.M. Calorimetric analysis of thermodynamic stability and aggregation for apo and holo amyotrophic lateral sclerosis-associated Gly-93 mutants of superoxide dismutase J. Biol. Chem. 281 2006 6184 6193 (Pubitemid 43847548)
31. Vassall K.A., Stathopulos P.B., Rumfeldt J.A., Lepock J.R., and Meiering E.M. Equilibrium thermodynamic analysis of amyotrophic lateral sclerosis-associated mutant apo Cu,Zn superoxide dismutases Biochemistry 45 2006 7366 7379 (Pubitemid 43877423)
32. Rodriguez J.A., Shaw B.F., Durazo A., Sohn S.H., Doucette P.A., and Nersissian A.M. Destabilization of apoprotein is insufficient to explain Cu,Zn-superoxide dismutase-linked ALS pathogenesis Proc. Natl Acad. Sci. USA 102 2005 10516 10521 (Pubitemid 41061586)
33. 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 (Pubitemid 40993641)
34. Nordlund A., and Oliveberg M. Folding of Cu/Zn superoxide dismutase suggests structural hotspots for gain of neurotoxic function in ALS: parallels to precursors in amyloid disease Proc. Natl Acad. Sci. USA 103 2006 10218 10223 (Pubitemid 44051147)
35. Svensson A.K., Bilsel O., Kayatekin C., Adefusika J.A., Zitzewitz J.A., and Matthews C.R. Metal-free ALS variants of dimeric human Cu,Zn-superoxide dismutase have enhanced populations of monomeric species PLoS One 5 2010 e10064
36. Svensson A.K., Bilsel O., Kondrashkina E., Zitzewitz J.A., and Matthews C.R. Mapping the folding free energy surface for metal-free human Cu,Zn superoxide dismutase J. Mol. Biol. 364 2006 1084 1102 (Pubitemid 44765032)
37. 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 (Pubitemid 39540952)
38. Doucette P.A., Whitson L.J., Cao X., Schirf V., Demeler B., and Valentine J.S. Dissociation of human copper-zinc superoxide dismutase dimers using chaotrope and reductant. Insights into the molecular basis for dimer stability J. Biol. Chem. 279 2004 54558 54566 (Pubitemid 40053198)
39. Kayatekin C., Zitzewitz J.A., and Matthews C.R. Zinc binding modulates the entire folding free energy surface of human Cu,Zn superoxide dismutase J. Mol. Biol. 384 2008 540 555
40. Potter S.Z., Zhu H., Shaw B.F., Rodriguez J.A., Doucette P.A., and Sohn S.H. Binding of a single zinc ion to one subunit of copper-zinc superoxide dismutase apoprotein substantially influences the structure and stability of the entire homodimeric protein J. Am. Chem. Soc. 129 2007 4575 4583 (Pubitemid 46648756)
41. Tiwari A., Liba A., Sohn S.H., Seetharaman S.V., Bilsel O., and Matthews C.R. Metal deficiency increases aberrant hydrophobicity of mutant superoxide dismutases that cause amyotrophic lateral sclerosis J. Biol. Chem. 284 2009 27746 27758
42. 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 (Pubitemid 40041065)
43. Lynch S.M., and Colon W. Dominant role of copper in the kinetic stability of Cu/Zn superoxide dismutase Biochem. Biophys. Res. Commun. 340 2006 457 461 (Pubitemid 43021770)
44. Rumfeldt J.A., Lepock J.R., and Meiering E.M. Unfolding and folding kinetics of amyotrophic lateral sclerosis-associated mutant Cu,Zn superoxide dismutases J. Mol. Biol. 385 2009 278 298
45. Rumfeldt J.A., Stathopulos P.B., Chakrabarrty A., Lepock J.R., and Meiering E.M. Mechanism and thermodynamics of guanidinium chloride-induced denaturation of ALS-associated mutant Cu,Zn superoxide dismutases J. Mol. Biol. 355 2006 106 123 (Pubitemid 41774143)
46. Maret W. Zinc and sulfur: a critical biological partnership Biochemistry 43 2004 3301 3309 (Pubitemid 38396774)
47. Rae T.D., Schmidt P.J., Pufahl R.A., Culotta V.C., and O'Halloran T.V. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase Science 284 1999 805 808 (Pubitemid 29291346)
48. Mulligan V.K., Kerman A., Ho S., and Chakrabartty A. Denaturational stress induces formation of zinc-deficient monomers of Cu,Zn superoxide dismutase: implications for pathogenesis in amyotrophic lateral sclerosis J. Mol. Biol. 383 2008 424 436
49. Hough M.A., Grossmann J.G., Antonyuk S.V., Strange R.W., Doucette P.A., and Rodriguez J.A. 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 (Pubitemid 38520513)
50. Ripps M.E., Huntley G.W., Hof P.R., Morrison J.H., and Gordon J.W. Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis Proc. Natl Acad. Sci. USA 92 1995 689 693
51. Wong P.C., Pardo C.A., Borchelt D.R., Lee M.K., Copeland N.G., and Jenkins N.A. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria Neuron 14 1995 1105 1116
52. Banci L., Bertini I., Ciofi-Baffoni S., Kozyreva T., Zovo K., and Palumaa P. Affinity gradients drive copper to cellular destinations Nature 465 2010 645 648
53. 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 (Pubitemid 39391724)
54. Vassall K.A., Stubbs H.R., Primmer H.A., Tong M.S., Sullivan S.M., and Sobering R. Decreased stability and increased formation of soluble aggregates by immature superoxide dismutase do not account for disease severity in ALS Proc. Natl Acad. Sci. USA 108 2011 2210 2215
55. Pantoliano M., McDonnell P.J., and Valentine J.S. Reversible loss of metal ions from the zinc binding site of copper-zinc superoxide dismutase: the low pH transition J. Am. Chem. Soc. 101 1979 6454 6456
56. Pantoliano M., Valentine J.S., Mammone R.J., and Scholler D.M. pH dependence of metal ion binding to the native zinc site of bovine erythrocuprein (superoxide dismutase) J. Am. Chem. Soc. 104 1982 1717 1723
57. Lepock J.R., Frey H.E., and Hallewell R.A. 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 1990 21612 21618 (Pubitemid 120014203)
58. Calabrese L., Federici G., Bannister W.H., Bannister J.V., Rotilio G., and Finazzi-Agro A. Labile sulfur in human superoxide dismutase Eur. J. Biochem. 56 1975 305 309
59. Carrico R.J., and Deutsch H.F. Isolation of human hepatocuprein and cerebrocuprein. Their identity with erythrocuprein J. Biol. Chem. 244 1969 6087 6093
60. de Beus M.D., Chung J., and Colon W. Modification of cysteine 111 in Cu/Zn superoxide dismutase results in altered spectroscopic and biophysical properties Protein Sci. 13 2004 1347 1355 (Pubitemid 38526100)
61. You Z., Cao X., Taylor A.B., Hart P.J., and Levine R.L. Characterization of a covalent polysulfane bridge in copper-zinc superoxide dismutase Biochemistry 49 2010 1191 1198
62. Bond J.M., Bannister J.V., and Bannister W.H. Polymers of Cu/Zn superoxide dismutase produced by cross-linking with glutaraldehyde Free Radical Res. Commun. 12-13 1991 545 551
63. Lai Z., McCulloch J., Lashuel H.A., and Kelly J.W. Guanidine hydrochloride-induced denaturation and refolding of transthyretin exhibits a marked hysteresis: equilibria with high kinetic barriers Biochemistry 36 1997 10230 10239 (Pubitemid 27357734)
64. Fersht A. Enzyme Structure and Mechanism 1977 W. H. Freeman and Company Reading, MA
65. Ikai A., and Tanford C. Kinetic evidence for incorrectly folded intermediate states in the refolding of denatured proteins Nature 230 1971 100 102
66. Ikai A., and Tanford C. Kinetics of unfolding and refolding of proteins: I. Mathematical analysis J. Mol. Biol. 73 1973 145 163