Skip to main content
Top
Published in: Molecular Neurodegeneration 1/2013

Open Access 01-12-2013 | Research article

Features of wild-type human SOD1 limit interactions with misfolded aggregates of mouse G86R Sod1

Authors: David A Qualls, Mercedes Prudencio, Brittany LT Roberts, Keith Crosby, Hilda Brown, David R Borchelt

Published in: Molecular Neurodegeneration | Issue 1/2013

Login to get access

Abstract

Mutations in the gene encoding superoxide dismutase 1 (SOD1) account for about 20% of the cases of familial amyotrophic lateral sclerosis (fALS). It is well established that mutations in SOD1, associated with fALS, heighten the propensity of the protein to misfold and aggregate. Although aggregation appears to be a factor in the toxicity of mutant SOD1s, the precise nature of this toxicity has not been elucidated. A number of other studies have now firmly established that raising the levels of wild-type (WT) human SOD1 (hSOD1) proteins can in some manner augment the toxicity of mutant hSOD1 proteins. However, a recent study demonstrated that raising the levels of WT-hSOD1 did not affect disease in mice that harbor a mouse Sod1 gene (mSod1) encoding a well characterized fALS mutation (G86R). In the present study, we sought a potential explanation for the differing effects with WT-hSOD1 on the toxicity of mutant hSOD1 versus mutant mSod1. In the cell culture models used here, we observe poor interactions between WT-hSOD1 and misfolded G86R-mSod1, possibly explaining why over-expression of WT-hSOD1 does not synergize with mutant mSod1 to accelerate the course of the disease in mice.
Appendix
Available only for authorised users
Literature
1.
go back to reference Fridovich I: Superoxide dismutases. Adv Enzymol Relat Areas Mol Biol. 1974, 41: 35-97.PubMed Fridovich I: Superoxide dismutases. Adv Enzymol Relat Areas Mol Biol. 1974, 41: 35-97.PubMed
2.
go back to reference Parge HE, Hallewell RA, Tainer JA: Atomic structures of wild- type and thermostable mutant recombinant human Cu, Zn superoxide dismutase. Proc Natl Acad Sci USA. 1992, 89: 6109-6113. 10.1073/pnas.89.13.6109.PubMedCentralCrossRefPubMed Parge HE, Hallewell RA, Tainer JA: Atomic structures of wild- type and thermostable mutant recombinant human Cu, Zn superoxide dismutase. Proc Natl Acad Sci USA. 1992, 89: 6109-6113. 10.1073/pnas.89.13.6109.PubMedCentralCrossRefPubMed
3.
go back to reference Ogihara NL, Parge HE, Hart PJ, Weiss MS, Goto JJ, Crane BR, Tsang J, Slater K, Roe JA, Valentine JS, et al: Unusual trigonal-planar copper configuration revealed in the atomic structure of yeast copper-zinc superoxide dismutase. Biochemistry. 1996, 35: 2316-2321. 10.1021/bi951930b.CrossRefPubMed Ogihara NL, Parge HE, Hart PJ, Weiss MS, Goto JJ, Crane BR, Tsang J, Slater K, Roe JA, Valentine JS, et al: Unusual trigonal-planar copper configuration revealed in the atomic structure of yeast copper-zinc superoxide dismutase. Biochemistry. 1996, 35: 2316-2321. 10.1021/bi951930b.CrossRefPubMed
4.
go back to reference Bruijn LI, Miller TM, Cleveland DW: Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci. 2004, 27: 723-749. 10.1146/annurev.neuro.27.070203.144244.CrossRefPubMed Bruijn LI, Miller TM, Cleveland DW: Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu Rev Neurosci. 2004, 27: 723-749. 10.1146/annurev.neuro.27.070203.144244.CrossRefPubMed
5.
go back to reference Prudencio M, Hart PJ, Borchelt DR, Andersen PM: Variation in aggregation propensities among ALS-associated variants of SOD1: correlation to human disease. Hum Mol Genet. 2009, 18: 3217-3226. 10.1093/hmg/ddp260.PubMedCentralCrossRefPubMed Prudencio M, Hart PJ, Borchelt DR, Andersen PM: Variation in aggregation propensities among ALS-associated variants of SOD1: correlation to human disease. Hum Mol Genet. 2009, 18: 3217-3226. 10.1093/hmg/ddp260.PubMedCentralCrossRefPubMed
6.
go back to reference Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng H-X, et al: Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science. 1994, 264: 1772-1775. 10.1126/science.8209258.CrossRefPubMed Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng H-X, et al: Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science. 1994, 264: 1772-1775. 10.1126/science.8209258.CrossRefPubMed
7.
go back to reference Deng HX, Shi Y, Furukawa Y, Zhai H, Fu R, Liu E, Gorrie GH, Khan MS, Hung WY, Bigio EH, et al: Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. Proc Natl Acad Sci U S A. 2006, 103: 7142-7147. 10.1073/pnas.0602046103.PubMedCentralCrossRefPubMed Deng HX, Shi Y, Furukawa Y, Zhai H, Fu R, Liu E, Gorrie GH, Khan MS, Hung WY, Bigio EH, et al: Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. Proc Natl Acad Sci U S A. 2006, 103: 7142-7147. 10.1073/pnas.0602046103.PubMedCentralCrossRefPubMed
8.
go back to reference Deng HX, Jiang H, Fu R, Zhai H, Shi Y, Liu E, Hirano M, Dal Canto MC, Siddique T: Molecular dissection of ALS-associated toxicity of SOD1 in transgenic mice using an exon-fusion approach. Hum Mol Genet. 2008, 17: 2310-2319. 10.1093/hmg/ddn131.CrossRefPubMed Deng HX, Jiang H, Fu R, Zhai H, Shi Y, Liu E, Hirano M, Dal Canto MC, Siddique T: Molecular dissection of ALS-associated toxicity of SOD1 in transgenic mice using an exon-fusion approach. Hum Mol Genet. 2008, 17: 2310-2319. 10.1093/hmg/ddn131.CrossRefPubMed
9.
go back to reference Jaarsma D, Teuling E, Haasdijk ED, De Zeeuw CI, Hoogenraad CC: Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J Neurosci. 2008, 28: 2075-2088. 10.1523/JNEUROSCI.5258-07.2008.CrossRefPubMed Jaarsma D, Teuling E, Haasdijk ED, De Zeeuw CI, Hoogenraad CC: Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J Neurosci. 2008, 28: 2075-2088. 10.1523/JNEUROSCI.5258-07.2008.CrossRefPubMed
10.
go back to reference Wang L, Deng HX, Grisotti G, Zhai H, Siddique T, Roos RP: Wild-type SOD1 overexpression accelerates disease onset of a G85R SOD1 mouse. Hum Mol Genet. 2009, 18: 1642-1651. 10.1093/hmg/ddp085.PubMedCentralCrossRefPubMed Wang L, Deng HX, Grisotti G, Zhai H, Siddique T, Roos RP: Wild-type SOD1 overexpression accelerates disease onset of a G85R SOD1 mouse. Hum Mol Genet. 2009, 18: 1642-1651. 10.1093/hmg/ddp085.PubMedCentralCrossRefPubMed
11.
go back to reference Prudencio M, Durazo A, Whitelegge JP, Borchelt DR: An examination of wild-type SOD1 in modulating the toxicity and aggregation of ALS-associated mutant SOD1. Hum Mol Genet. 2010, 19: 4774-4789. 10.1093/hmg/ddq408.PubMedCentralCrossRefPubMed Prudencio M, Durazo A, Whitelegge JP, Borchelt DR: An examination of wild-type SOD1 in modulating the toxicity and aggregation of ALS-associated mutant SOD1. Hum Mol Genet. 2010, 19: 4774-4789. 10.1093/hmg/ddq408.PubMedCentralCrossRefPubMed
12.
go back to reference Bruijn LI, Houseweart MK, Kato S, Anderson KL, Anderson SD, Ohama E, Reaume AG, Scott RW, Cleveland DW: Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science. 1998, 281: 1851-1854.CrossRefPubMed Bruijn LI, Houseweart MK, Kato S, Anderson KL, Anderson SD, Ohama E, Reaume AG, Scott RW, Cleveland DW: Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science. 1998, 281: 1851-1854.CrossRefPubMed
13.
go back to reference Audet JN, Gowing G, Julien JP: Wild-type human SOD1 overexpression does not accelerate motor neuron disease in mice expressing murine Sod1 G86R. Neurobiol Dis. 2010, 40: 245-250. 10.1016/j.nbd.2010.05.031.CrossRefPubMed Audet JN, Gowing G, Julien JP: Wild-type human SOD1 overexpression does not accelerate motor neuron disease in mice expressing murine Sod1 G86R. Neurobiol Dis. 2010, 40: 245-250. 10.1016/j.nbd.2010.05.031.CrossRefPubMed
14.
go back to reference Ripps ME, Huntley GW, Hof PR, Morrison JH, Gordon JW: Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA. 1995, 92: 689-693. 10.1073/pnas.92.3.689.PubMedCentralCrossRefPubMed Ripps ME, Huntley GW, Hof PR, Morrison JH, Gordon JW: Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc Natl Acad Sci USA. 1995, 92: 689-693. 10.1073/pnas.92.3.689.PubMedCentralCrossRefPubMed
15.
go back to reference Prudencio M, Borchelt DR: Superoxide dismutase 1 encoding mutations linked to ALS adopts a spectrum of misfolded states. Mol Neurodegener. 2011, 6: 77-10.1186/1750-1326-6-77.PubMedCentralCrossRefPubMed Prudencio M, Borchelt DR: Superoxide dismutase 1 encoding mutations linked to ALS adopts a spectrum of misfolded states. Mol Neurodegener. 2011, 6: 77-10.1186/1750-1326-6-77.PubMedCentralCrossRefPubMed
17.
go back to reference Wang J, Slunt H, Gonzales V, Fromholt D, Coonfield M, Copeland NG, Jenkins NA, Borchelt DR: Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum Mol Genet. 2003, 12: 2753-2764. 10.1093/hmg/ddg312.CrossRefPubMed Wang J, Slunt H, Gonzales V, Fromholt D, Coonfield M, Copeland NG, Jenkins NA, Borchelt DR: Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum Mol Genet. 2003, 12: 2753-2764. 10.1093/hmg/ddg312.CrossRefPubMed
18.
go back to reference Karch CM, Prudencio M, Winkler DD, Hart PJ, Borchelt DR: Role of mutant SOD1 disulfide oxidation and aggregation in the pathogenesis of familial ALS. Proc Natl Acad Sci U S A. 2009, 106: 7774-7779. 10.1073/pnas.0902505106.PubMedCentralCrossRefPubMed Karch CM, Prudencio M, Winkler DD, Hart PJ, Borchelt DR: Role of mutant SOD1 disulfide oxidation and aggregation in the pathogenesis of familial ALS. Proc Natl Acad Sci U S A. 2009, 106: 7774-7779. 10.1073/pnas.0902505106.PubMedCentralCrossRefPubMed
19.
go back to reference Prudencio M, Durazo A, Whitelegge JP, Borchelt DR: Modulation of mutant superoxide dismutase 1 aggregation by co-expression of wild-type enzyme. J Neurochem. 2009, 108: 1009-1018. 10.1111/j.1471-4159.2008.05839.x.PubMedCentralCrossRefPubMed Prudencio M, Durazo A, Whitelegge JP, Borchelt DR: Modulation of mutant superoxide dismutase 1 aggregation by co-expression of wild-type enzyme. J Neurochem. 2009, 108: 1009-1018. 10.1111/j.1471-4159.2008.05839.x.PubMedCentralCrossRefPubMed
20.
go back to reference Karch CM, Borchelt DR: A limited role for disulfide cross-linking in the aggregation of mutant SOD1 linked to familial amyotrophic lateral sclerosis. J Biol Chem. 2008, 283: 13528-13537. 10.1074/jbc.M800564200.PubMedCentralCrossRefPubMed Karch CM, Borchelt DR: A limited role for disulfide cross-linking in the aggregation of mutant SOD1 linked to familial amyotrophic lateral sclerosis. J Biol Chem. 2008, 283: 13528-13537. 10.1074/jbc.M800564200.PubMedCentralCrossRefPubMed
21.
go back to reference Stevens JC, Chia R, Hendriks WT, Bros-Facer V, Van MJ, Martin JE, Jackson GS, Greensmith L, Schiavo G, Fisher EM: Modification of superoxide dismutase 1 (SOD1) properties by a GFP tag--implications for research into amyotrophic lateral sclerosis (ALS). PLoS ONE. 2010, 5: e9541-10.1371/journal.pone.0009541.PubMedCentralCrossRefPubMed Stevens JC, Chia R, Hendriks WT, Bros-Facer V, Van MJ, Martin JE, Jackson GS, Greensmith L, Schiavo G, Fisher EM: Modification of superoxide dismutase 1 (SOD1) properties by a GFP tag--implications for research into amyotrophic lateral sclerosis (ALS). PLoS ONE. 2010, 5: e9541-10.1371/journal.pone.0009541.PubMedCentralCrossRefPubMed
22.
go back to reference Francis G, Kerem Z, Makkar HP, Becker K: The biological action of saponins in animal systems: a review. Br J Nutr. 2002, 88: 587-605. 10.1079/BJN2002725.CrossRefPubMed Francis G, Kerem Z, Makkar HP, Becker K: The biological action of saponins in animal systems: a review. Br J Nutr. 2002, 88: 587-605. 10.1079/BJN2002725.CrossRefPubMed
23.
go back to reference Qualls DA, Crosby K, Brown H, Borchelt DR: An analysis of interactions between fluorescently-tagged mutant and wild-type SOD1 in intracellular inclusions. PLoS One. in press Qualls DA, Crosby K, Brown H, Borchelt DR: An analysis of interactions between fluorescently-tagged mutant and wild-type SOD1 in intracellular inclusions. PLoS One. in press
24.
go back to reference Rakhit R, Robertson J, Vande VC, Horne P, Ruth DM, Griffin J, Cleveland DW, Cashman NR, Chakrabartty A: An immunological epitope selective for pathological monomer-misfolded SOD1 in ALS. Nat Med. 2007, 13: 754-759. 10.1038/nm1559.CrossRefPubMed Rakhit R, Robertson J, Vande VC, Horne P, Ruth DM, Griffin J, Cleveland DW, Cashman NR, Chakrabartty A: An immunological epitope selective for pathological monomer-misfolded SOD1 in ALS. Nat Med. 2007, 13: 754-759. 10.1038/nm1559.CrossRefPubMed
25.
go back to reference Bertini I, Piccioli M, Viezzoli MS, Chiu CY, Mullenbach GT: A spectroscopic characterization of a monomeric analog of copper, zinc superoxide dismutase. Eur Biophys J. 1994, 23: 167-176. 10.1007/BF01007608.CrossRefPubMed Bertini I, Piccioli M, Viezzoli MS, Chiu CY, Mullenbach GT: A spectroscopic characterization of a monomeric analog of copper, zinc superoxide dismutase. Eur Biophys J. 1994, 23: 167-176. 10.1007/BF01007608.CrossRefPubMed
26.
go back to reference Banci L, Benedetto M, Bertini I, Del Conte R, Piccioli M, Viezzoli MS: Solution structure of reduced monomeric Q133M2 copper, zinc superoxide dismutase (SOD). Why is SOD a dimeric enzyme?. Biochemistry. 1998, 37: 11780-11791. 10.1021/bi9803473.CrossRefPubMed Banci L, Benedetto M, Bertini I, Del Conte R, Piccioli M, Viezzoli MS: Solution structure of reduced monomeric Q133M2 copper, zinc superoxide dismutase (SOD). Why is SOD a dimeric enzyme?. Biochemistry. 1998, 37: 11780-11791. 10.1021/bi9803473.CrossRefPubMed
27.
go back to reference Kim SB, Sato M, Tao H: Split Gaussia luciferase-based bioluminescence template for tracing protein dynamics in living cells. Anal Chem. 2009, 81: 67-74. 10.1021/ac801658y.CrossRefPubMed Kim SB, Sato M, Tao H: Split Gaussia luciferase-based bioluminescence template for tracing protein dynamics in living cells. Anal Chem. 2009, 81: 67-74. 10.1021/ac801658y.CrossRefPubMed
28.
go back to reference Rakhit R, Crow JP, Lepock JR, Kondejewski LH, Cashman NR, 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. 2004, 279: 15499-15504. 10.1074/jbc.M313295200.CrossRefPubMed Rakhit R, Crow JP, Lepock JR, Kondejewski LH, Cashman NR, 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. 2004, 279: 15499-15504. 10.1074/jbc.M313295200.CrossRefPubMed
29.
go back to reference Khare SD, Caplow M, Dokholyan NV: FALS mutations in Cu, Zn superoxide dismutase destabilize the dimer and increase dimer dissociation propensity: a large-scale thermodynamic analysis. Amyloid. 2006, 13: 226-235. 10.1080/13506120600960486.CrossRefPubMed Khare SD, Caplow M, Dokholyan NV: FALS mutations in Cu, Zn superoxide dismutase destabilize the dimer and increase dimer dissociation propensity: a large-scale thermodynamic analysis. Amyloid. 2006, 13: 226-235. 10.1080/13506120600960486.CrossRefPubMed
30.
go back to reference Svensson AK, Bilsel O, Kayatekin C, Adefusika JA, Zitzewitz JA, Matthews CR: Metal-free ALS variants of dimeric human Cu, Zn-superoxide dismutase have enhanced populations of monomeric species. PLoS ONE. 2010, 5: e10064-10.1371/journal.pone.0010064.PubMedCentralCrossRefPubMed Svensson AK, Bilsel O, Kayatekin C, Adefusika JA, Zitzewitz JA, Matthews CR: Metal-free ALS variants of dimeric human Cu, Zn-superoxide dismutase have enhanced populations of monomeric species. PLoS ONE. 2010, 5: e10064-10.1371/journal.pone.0010064.PubMedCentralCrossRefPubMed
31.
go back to reference Auclair JR, Boggio KJ, Petsko GA, Ringe D, Agar JN: Strategies for stabilizing superoxide dismutase (SOD1), the protein destabilized in the most common form of familial amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A. 2010, 107: 21394-21399. 10.1073/pnas.1015463107.PubMedCentralCrossRefPubMed Auclair JR, Boggio KJ, Petsko GA, Ringe D, Agar JN: Strategies for stabilizing superoxide dismutase (SOD1), the protein destabilized in the most common form of familial amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A. 2010, 107: 21394-21399. 10.1073/pnas.1015463107.PubMedCentralCrossRefPubMed
32.
go back to reference Ray SS, Nowak RJ, Strokovich K, Brown RH, Walz T, Lansbury PT: An intersubunit disulfide bond prevents in vitro aggregation of a superoxide dismutase-1 mutant linked to familial amytrophic lateral sclerosis. Biochemistry. 2004, 43: 4899-4905. 10.1021/bi030246r.CrossRefPubMed Ray SS, Nowak RJ, Strokovich K, Brown RH, Walz T, Lansbury PT: An intersubunit disulfide bond prevents in vitro aggregation of a superoxide dismutase-1 mutant linked to familial amytrophic lateral sclerosis. Biochemistry. 2004, 43: 4899-4905. 10.1021/bi030246r.CrossRefPubMed
Metadata
Title
Features of wild-type human SOD1 limit interactions with misfolded aggregates of mouse G86R Sod1
Authors
David A Qualls
Mercedes Prudencio
Brittany LT Roberts
Keith Crosby
Hilda Brown
David R Borchelt
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Molecular Neurodegeneration / Issue 1/2013
Electronic ISSN: 1750-1326
DOI
https://doi.org/10.1186/1750-1326-8-46

Other articles of this Issue 1/2013

Molecular Neurodegeneration 1/2013 Go to the issue

Reviewer acknowledgement

Reviewer acknowledgement