Direct and indirect mechanisms for wild-type SOD1 to enhance the toxicity of mutant SOD1 in bigenic transgenic mice

Human Molecular Genetics

Volumn 24, Issue 4, 2015, Pages 1019-1035

  Xu, Guilian ^a,b   Ayers, Jacob I ^a   Roberts, Brittany L ^a   Brown, Hilda ^a,b   Fromholt, Susan ^a,b   Green, Cameron ^a   Borchelt, David R ^a,b  

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

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; COPPER ZINC SUPEROXIDE DISMUTASE; HISTIDINE; UBIQUITIN; YELLOW FLUORESCENT PROTEIN; MESSENGER RNA; MUTANT PROTEIN; PROTEIN BINDING; SUPEROXIDE DISMUTASE;

AGE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RETRIEVAL; ARTICLE; BINDING AFFINITY; CELL LOSS; CELL LYSATE; CONTROLLED STUDY; DISEASE SEVERITY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MOLECULAR WEIGHT; MOTONEURON; MOTOR NEURON DISEASE; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SPINAL PARALYSIS; STEADY STATE; TOXICITY; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL; CELL LINE; CHEMISTRY; DISEASE MODEL; FEMALE; GENE EXPRESSION; GENETICS; HUMAN; MALE; METABOLISM; MORTALITY; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; HUMANS; MALE; MICE; MICE, TRANSGENIC; MOTOR NEURONS; MUTANT PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TRANSPORT; RNA, MESSENGER; SUPEROXIDE DISMUTASE;

EID: 84922477400     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu517     Document Type: Article

References (46)

1. Rosen, D.R., Siddique, T., Patterson, D., Figlewicz, D.A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., O'Regan, J.P. and Deng, H.X. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature, 362, 59-62.
2. Borchelt, D.R., Guarnieri, M., Wong, P.C., Lee, M.K., Slunt, H.S., Xu, Z.S., Sisodia, S.S., Price, D.L. and Clevel, D.W. (1995) Superoxide dismutase 1 subunits with mutations linked to familial amyotrophic lateral sclerosis do not affect wild-type subunit function. J. Biol. Chem., 270, 3234-3238.
3. Fridovich, I. (1974) Superoxide dismutases. Adv. Enzymol. Relat. Areas Mol. Biol., 41, 35-97.
4. Williamson, T.L., Corson, L.B., Huang, L., Burlingame, A., Liu, J., Bruijn, L.I. and Cleveland, D.W. (2000) Toxicity of ALS-linked SOD1 mutants. Science, 288, 399a-399a.
5. Bruijn, L.I., Miller, T.M. and Clevel, D.W. (2004) Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci., 27, 723-749.
6. Prudencio, M. and Borchelt, D.R. (2011) Superoxide dismutase 1 encoding mutations linked to ALS adopts a spectrum of misfolded states. Mol. Neurodegener., 6, 77.
7. Prudencio, M., Hart, P.J., Borchelt, D.R. and Andersen, P.M. (2009) Variation in aggregation propensities among ALS-associated variants of SOD1: Correlation to human disease. Hum. Mol. Genet., 18, 3217-3226.
8. Bruijn, L.I., Houseweart, M.K., Kato, S., Anderson, K.L., Anderson, S.D., Ohama, E., Reaume, A.G., Scott, R.W. and Clevel, D.W. (1998) Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science, 281, 1851-1854.
9. Deng, H.X., Shi, Y., Furukawa, Y., Zhai, H., Fu, R., Liu, E., Gorrie, G.H., Khan, M.S., Hung, W.Y., Bigio, E.H. et al. (2006) Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. Proc. Natl. Acad. Sci. USA, 103, 7142-7147.
10. Prudencio, M., Durazo, A., Whitelegge, J.P. and Borchelt, D.R. (2010) An examination of wild-type SOD1 in modulating the toxicity and aggregation of ALS-associated mutant SOD1. Hum. Mol. Genet., 19, 4774-4789.
11. Jaarsma, D., Teuling, E., Haasdijk, E.D., De Zeeuw, C.I. and Hoogenraad, C.C. (2008) Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J. Neurosci., 28, 2075-2088.
12. Deng, H.X., Jiang, H., Fu, R., Zhai, H., Shi, Y., Liu, E., Hirano, M., Dal Canto, M.C. and Siddique, T. (2008) Molecular dissection of ALS-associated toxicity of SOD1 in transgenic mice using an exon-fusion approach. Hum. Mol. Genet., 17, 2310-2319.
13. Wang, L., Deng, H.X., Grisotti, G., Zhai, H., Siddique, T. and Roos, R.P. (2009) Wild-typeSOD1overexpression accelerates disease onset of a G85R SOD1 mouse. Hum. Mol. Genet., 18, 1642-1651.
14. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., Polchow, C.Y., Alexander, D.D., Caliendo, J., Hentati, A., Kwon, Y.W. and Deng, H.X. (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science, 264, 1772-1775.
15. Wang, J., Xu, G., Slunt, H.H., Gonzales, V., Coonfield, M., Fromholt, D., Copeland, N.G., Jenkins, N.A. and Borchelt, D.R. (2005) Coincident thresholds of mutant protein for paralytic disease and protein aggregation caused by restrictively expressed superoxide dismutase cDNA. Neurobiol. Dis., 20, 943-952.
16. Wong, P.C., Pardo, C.A., Borchelt, D.R., Lee, M.K., Copeland, N.G., Jenkins, N.A., Sisodia, S.S., Cleveland, D.W. and Price, D.L. (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.
17. Maquat, L.E. (1995) When cells stop making sense: Effects of nonsense codons on RNA metabolism in vertebrate cells. RNA, 1, 453-465.
18. Wang, J., Xu, G., Li, H., Gonzales, V., Fromholt, D., Karch, C., Copeland, N.G., Jenkins, N.A. and Borchelt, D.R. (2005) Somatodendritic accumulation of misfolded SOD1-L126Z in motor neurons mediates degeneration: {Alpha}B-crystallin modulates aggregation. Hum. Mol. Genet., 14, 2335-2347.
19. Jonsson, P.A., Ernhill, K., Andersen, P.M., Bergemalm, D., Brannstrom, T., Gredal, O., Nilsson, P. and Marklund, S.L. (2004) Minute quantities of misfolded mutant superoxide dismutase-1 cause amyotrophic lateral sclerosis. Brain, 127, 73-88.
20. Wang, J., Xu, G. and Borchelt, D.R. (2006) Mapping superoxide dismutase 1 domains of non-native interaction: roles of intra-and intermolecular disulfide bonding in aggregation. J. Neurochem., 96, 1277-1288.
21. Wang, J., Xu, G., Gonzales, V., Coonfield, M., Fromholt, D., Copeland, N.G., Jenkins, N.A. and Borchelt, D.R. (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.
22. Ratovitski, T., Corson, L.B., Strain, J., Wong, P., Cleveland, D.W., Culotta, V.C. and Borchelt, D.R. (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.
23. Urushitani, M., Ezzi, S.A. and Julien, J.P. (2007) Therapeutic effects of immunization with mutant superoxide dismutase in mice models of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA, 104, 2495-2500.
24. Ayers, J.I., Xu, G., Pletnikova, O., Troncoso, J.C., Hart, P.J. and Borchelt, D.R. (2014) Conformatonal specificity of the C4F6 SOD1 antibody; low frequency of reactivity in sporadic ALS cases. Acta Neuropathol. Commun., 2, 55.
25. Rakhit, R., Robertson, J., Vande, V.C., Horne, P., Ruth, D.M., Griffin, J., Cleveland, D.W., Cashman, N.R. and Chakrabartty, A. (2007) An immunological epitope selective for pathological monomer-misfolded SOD1 in ALS. Nat. Med., 13, 754-759.
26. Rotunno, M.S., Auclair, J.R., Maniatis, S., Shaffer, S.A., Agar, J. and Bosco, D.A. (2014) Identification of a misfolded region in superoxide dismutase 1 that is exposed in amyotrophic lateral sclerosis. J. Biol. Chem., 289, 28527-28538.
27. Bruijn, L.I., Becher, M.W., Lee, M.K., Anderson, K.L., Jenkins, N.A., Copeland, N.G., Sisodia, S.S., Rothstein, J.D., Borchelt, D.R., Price, D.L. et al. (1997) ALS-linkedSOD1mutantG85Rmediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron, 18, 327-338.
28. Wang, J., Farr, G.W., Zeiss, C.J., Rodriguez-Gil, D.J., Wilson, J.H., Furtak, K., Rutkowski, D.T., Kaufman, R.J., Ruse, C.I., Yates, J.R. III et al. (2009) Progressive aggregation despite chaperone associations of a mutant SOD1-YFPin transgenic mice that developALS.Proc. Natl. Acad. Sci.USA, 106, 1392-1397.
29. Kim, S.B., Sato, M. and Tao, H. (2009) Split gaussia luciferase-based bioluminescence template for tracing protein dynamics in living cells. Anal. Chem., 81, 67-74.
30. Bertini, I., Piccioli, M., Viezzoli, M.S., Chiu, C.Y. and Mullenbach, G.T. (1994) A spectroscopic characterization of a monomeric analog of copper, zinc superoxide dismutase. Eur. Biophys. J., 23, 167-176.
31. Qualls, D.A., Crosby, K., Brown, H. and Borchelt, D.R. (2013) An analysis of interactions between fluorescently-tagged mutant and wild-type SOD1 in intracellular inclusions. PLoS ONE, 8, e83981.
32. Driegen, S., Ferreira, R., van Zon, A., Strouboulis, J., Jaegle, M., Grosveld, F., Philipsen, S. and Meijer, D. (2005) A generic tool for biotinylation of tagged proteins in transgenic mice. Transgenic Res., 14, 477-482.
33. Weichert, A., Besemer, A.S., Liebl, M., Hellmann, N., Koziollek-Drechsler, I., Ip, P., Decker, H., Robertson, J., Chakrabartty, A., Behl, C. et al. (2014) Wildtype cu/zn superoxide dismutase 1 stabilizes mutant variants by heterodimerization. Neurobiol. Dis., 62, 479-488.
34. Zetterstrom, P., Graffmo, K.S., Andersen, P.M., Brannstrom, T. and Marklund, S.L. (2013) Composition of soluble misfolded superoxide dismutase-1 in murine models of amyotrophic lateral sclerosis. Neuromolecular Med., 15, 147-158.
35. Schagger, H. and von Jagow, G. (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem., 199, 223-231.
36. Borchelt, D.R., Lee, M.K., Slunt, H.S., Guarnieri, M., Xu, Z.S., Wong, P.C., Brown, R.H. Jr, Price, D.L., Sisodia, S.S. and Cleveland, D.W. (1994) Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc. Natl. Acad. Sci.USA, 91, 8292-8296.
37. Grad, L.I., Yerbury, J.J., Turner, B.J., Guest, W.C., Pokrishevsky, E., O'Neill, M.A., Yanai, A., Silverman, J.M., Zeineddine, R., Corcoran, L. et al. (2014) Intercellular propagated misfolding of wild-type cu/zn superoxide dismutase occurs via exosome-dependent and-independent mechanisms. Proc. Natl. Acad. Sci. USA, 111, 3620-3625.
38. Prudencio, M., Lelie, H., Brown, H.H., Whitelegge, J.P., Valentine, J.S. and Borchelt, D.R. (2012) A novel variant of human SOD1 harboring ALS-associated and experimental mutations in metal-binding residues and free cysteines lacks toxicity in vivo. J. Neurochem., 121, 305-314.
39. Karch, C.M., Prudencio, M., Winkler, D.D., Hart, P.J. and Borchelt, D.R. (2009) Role of mutant SOD1 disulfide oxidation and aggregation in the pathogenesis of familial ALS. Proc. Natl. Acad. Sci. USA, 106, 7774-7779.
40. Prudencio, M., Durazo, A., Whitelegge, J.P. and Borchelt, D.R. (2009) Modulation of mutant superoxide dismutase 1 aggregation by co-expression of wild-type enzyme. J. Neurochem., 108, 1009-1018.
41. Graffmo, K.S., Forsberg, K., Bergh, J., Birve, A., Zetterstrom, P., Andersen, P.M., Marklund, S.L. and Brannstrom, T. (2013) Expression of wild-type human superoxide dismutase-1 in mice causes amyotrophic lateral sclerosis. Hum. Mol. Genet., 22, 51-60.
42. Bosco, D.A., Morfini, G., Karabacak, N.M., Song, Y., Gros-Louis, F., Pasinelli, P., Goolsby, H., Fontaine, B.A., Lemay, N., McKenna-Yasek, D. et al. (2010) Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat. Neurosci., 13, 1396-1403.
43. Brotherton, T.E., Li, Y., Cooper, D., Gearing, M., Julien, J.P., Rothstein, J.D., Boylan, K. and Glass, J.D. (2012) Localization of a toxic form of superoxide dismutase 1 protein to pathologically affected tissues in familial ALS. Proc. Natl. Acad. Sci. USA, 109, 5505-5510.
44. Forsberg, K., Jonsson, P.A., Andersen, P.M., Bergemalm, D., Graffmo, K.S., Hultdin, M., Jacobsson, J., Rosquist, R., Marklund, S.L. and Brannstrom, T. (2010) Novel antibodies reveal inclusions containing non-native SOD1 in sporadic ALS patients. PLoS ONE, 5, e11552.
45. Brown, H.H. and Borchelt, D.R. (2014) Analysis of mutant SOD1 electrophoretic mobility by blue native gel electrophoresis; evidence for soluble multimeric assemblies. PLoS ONE, 9, e104583.
46. Danzer, K.M., Kranich, L.R., Ruf, W.P., Cagsal-Getkin, O., Winslow, A.R., Zhu, L., Vanderburg, C.R. and McLean, P.J. (2012) Exosomal cell-to-cell transmission of alpha synuclein oligomers. Mol. Neurodegener., 7, 42.