Experimental transmissibility of mutant SOD1 motor neuron disease

Acta Neuropathologica

Volumn 128, Issue 6, 2014, Pages 791-803

  Ayers, Jacob I ^a   Fromholt, Susan ^a   Koch, Morgan ^a   DeBosier, Adam ^a   McMahon, Ben ^a   Xu, Guilian ^a,b   Borchelt, David R ^a,b  

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

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Amyotrophic lateral sclerosis; Motor neuron disease; Seeding; Superoxide dismutase 1; Transmissibility

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; HYBRID PROTEIN; MUTANT PROTEIN; PROTEIN VARIANT; YELLOW FLUORESCENT PROTEIN; BACTERIAL PROTEIN; PHOTOPROTEIN; SUPEROXIDE DISMUTASE; YELLOW FLUORESCENT PROTEIN, BACTERIA;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE TRANSMISSION; MOTOR NEURON DISEASE; MOUSE; NEWBORN; NONHUMAN; PARALYSIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD; SPINE DISEASE; TISSUE HOMOGENATE; TISSUE PREPARATION; TRANSGENIC MOUSE; ANIMAL; C3H MOUSE; C57BL MOUSE; CELL INCLUSION; DISEASE MODEL; FLUORESCENCE MICROSCOPY; GENETIC PREDISPOSITION; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANIMALS, NEWBORN; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; INCLUSION BODIES; KAPLAN-MEIER ESTIMATE; LUMINESCENT PROTEINS; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; MOTOR NEURON DISEASE; MUTATION; PARALYSIS; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 84921935837     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-014-1342-7     Document Type: Article

References (46)

1. Aguzzi A, Heikenwalder M, Polymenidou M (2007) Insights into prion strains and neurotoxicity. Nat Rev Mol Cell Biol 8:552–561. doi:10.1038/nrm2204
2. Ayers J, Kincaid AE, Bartz JC (2009) Prion strain targeting independent of strain-specific neuronal tropism. J Virol 83:81–87. doi:10.1128/JVI.01745-08
3. Ayers J, Xu G, Pletnikova O, Troncoso JC, Hart PJ, Borchelt DR (2014) Conformational specificity of the C4F6 SOD1 antibody; low frequency of reactivity in sporadic ALS cases. Acta Neuropathol Commun 2:55. doi:10.1186/2051-5960-2-55
4. Banci L, Bertini I, Durazo A, Girotto S, Gralla EB, Martinelli M, Valentine JS, Vieru M, Whitelegge JP (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. doi:10.1073/pnas.0704307104
5. Bandyopadhyay U, Nagy M, Fenton WA, Horwich AL (2014) Absence of lipofuscin in motor neurons of SOD1-linked ALS mice. Proc Natl Acad Sci USA. doi:10.1073/pnas.1409314111
6. Bartz JC, Kincaid AE, Bessen RA (2002) Retrograde transport of transmissible mink encephalopathy within descending motor tracts. J Virol 76:5759–5768
7. Bessen RA, Marsh RF (1992) Identification of two biologically distinct strains of transmissible mink encephalopathy in hamsters. J Gen Virol 73(Pt 2):329–334
8. Borchelt DR, Guarnieri M, Wong PC, Lee MK, Slunt HS, Xu ZS, Sisodia SS, Price DL, Cleveland DW (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
9. Borchelt DR, Lee MK, Slunt HS, Guarnieri M, Xu ZS, Wong PC, Brown RH, Price DL, Sisodia SS, Cleveland DW (1994) Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Natl Acad Sci USA 91:8292–8296
10. Brooks BR (1991) The role of axonal transport in neurodegenerative disease spread: a meta-analysis of experimental and clinical poliomyelitis compares with amyotrophic lateral sclerosis. Can J Neurol Sci 18:435–438
11. Bruce M, Chree A, McConnell I, Foster J, Pearson G, Fraser H (1994) Transmission of bovine spongiform encephalopathy and scrapie to mice: strain variation and the species barrier. Philos Trans R Soc Lond B Biol Sci 343:405–411. doi:10.1098/rstb.1994.0036
12. Bruijn LI, Houseweart MK, Kato S, Anderson KL, Anderson SD, Ohama E, Reaume AG, Scott RW, Cleveland DW (1998) Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 281:1851–1854
13. Chattopadhyay M, Durazo A, Sohn SH, Strong CD, Gralla EB, Whitelegge JP, Valentine JS (2008) Initiation and elongation in fibrillation of ALS-linked superoxide dismutase. Proc Natl Acad Sci USA 105:18663–18668. doi:10.1073/pnas.0807058105
14. Chia R, Tattum MH, Jones S, Collinge J, Fisher EMC, Jackson GS (2010) Superoxide dismutase 1 and tgSOD1 mouse spinal cord seed fibrils, suggesting a propagative cell death mechanism in amyotrophic lateral sclerosis. PLoS One 5:e10627. doi:10.1371/journal.pone.0010627
15. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, Fraser G, Stalder AK, Beibel M, Staufenbiel M, Jucker M, Goedert M, Tolnay M (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11:909–913. doi:10.1038/ncb1901
16. Dickinson AG, Meikle VM (1971) Host-genotype and agent effects in scrapie incubation: change in allelic interaction with different strains of agent. Mol Gen Genet 112:73–79
17. Fraser JR (1996) Infectivity in extraneural tissues following intraocular scrapie infection. J Gen Virol 77(Pt 10):2663–2668
18. Grad LI, Yerbury JJ, Turner BJ, Guest WC, Pokrishevsky E, O’Neill MA, Yanai A, Silverman JM, Zeineddine R, Corcoran L, Kumita JR, Luheshi LM, Yousefi M, Coleman BM, Hill AF, Plotkin SS, Mackenzie IR, Cashman NR (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. doi:10.1073/pnas.1312245111
19. Graffmo KS, Forsberg K, Bergh J, Birve A, Zetterstrom P, Andersen PM, Marklund SL, Brannstrom T (2012) Expression of wild-type human superoxide dismutase-1 in mice causes amyotrophic lateral sclerosis. Hum Mol Genet 22:51–60. doi:10.1093/hmg/dds399
20. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264:1772–1775
21. Hsiao KK, Groth D, Scott M, Yang SL, Serban H, Rapp D, Foster D, Torchia M, Dearmond SJ, Prusiner SB (1994) Serial transmission in rodents of neurodegeneration from transgenic mice expressing mutant prion protein. Proc Natl Acad Sci USA 91:9126–9130
22. Jaarsma D, Rognoni F, van Duijn W, Verspaget HW, Haasdijk ED, Holstege JC (2001) CuZn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol 102:293–305. doi:10.1007/s004010100399
23. 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. doi:10.1073/pnas.220417997
24. Jonsson PA, Graffmo KS, Andersen PM, Brännström T, Lindberg M, Oliveberg M, Marklund SL (2006) Disulphide-reduced superoxide dismutase-1 in CNS of transgenic amyotrophic lateral sclerosis models. Brain 129:451–464. doi:10.1093/brain/awh704
25. Kanouchi T, Ohkubo T, Yokota T (2012) Can regional spreading of amyotrophic lateral sclerosis motor symptoms be explained by prion-like propagation? J Neurol Neurosurg Psychiatry 83:739–745. doi:10.1136/jnnp-2011-301826
26. Karch CM, Prudencio M, Winkler DD, Hart PJ, Borchelt DR (2009) Role of mutant SOD1 disulfide oxidation and aggregation in the pathogenesis of familial ALS. Proc Natl Acad Sci USA 106:7774–7779. doi:10.1073/pnas.0902505106
27. McBride PA, Schulz-Schaeffer WJ, Donaldson M, Bruce M, Diringer H, Kretzschmar HA, Beekes M (2001) Early spread of scrapie from the gastrointestinal tract to the central nervous system involves autonomic fibers of the splanchnic and vagus nerves. J Virol 75:9320–9327. doi:10.1128/JVI.75.19.9320-9327.2001
28. McKinley MP, Dearmond SJ, Torchia M, Mobley WC, Prusiner SB (1989) Acceleration of scrapie in neonatal Syrian hamsters. Neurology 39:1319–1324
29. Meyer-Luehmann M (2006) Exogenous induction of cerebral-amyloidogenesis is governed by agent and host. Science 313:1781–1784. doi:10.1126/science.1131864
30. Monari L, Chen SG, Brown P, Parchi P, Petersen RB, Mikol J, Gray F, Cortelli P, Montagna P, Ghetti B (1994) Fatal familial insomnia and familial Creutzfeldt–Jakob disease: different prion proteins determined by a DNA polymorphism. Proc Natl Acad Sci USA 91:2839–2842
31. Mougenot A-L, Nicot S, Bencsik A, Morignat E, Verchere J, Lakhdar L, Legastelois S, Baron T (2012) Prion-like acceleration of a synucleinopathy in a transgenic mouse model. Neurobiol Aging 33:2225–2228. doi:10.1016/j.neurobiolaging.2011.06.022
32. Münch C, O’Brien J, Bertolotti A (2011) Prion-like propagation of mutant superoxide dismutase-1 misfolding in neuronal cells. Proc Natl Acad Sci USA 108:3548–3553. doi:10.1073/pnas.1017275108
33. Oztug Durer ZA, Cohlberg JA, Dinh P, Padua S, Ehrenclou K, Downes S, Tan JK, Nakano Y, Bowman CJ, Hoskins JL, Kwon C, Mason AZ, Rodriguez JA, Doucette PA, Shaw BF, Valentine JS (2009) Loss of metal ions, disulfide reduction and mutations related to familial ALS promote formation of amyloid-like aggregates from superoxide dismutase. PLoS One 4:e5004. doi:10.1371/journal.pone.0005004
34. Peretz D, Scott MR, Groth D, Williamson RA, Burton DR, Cohen FE, Prusiner SB (2001) Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci 10:854–863. doi:10.1110/ps.39201
35. Prudencio M, Borchelt DR (2011) Superoxide dismutase 1 encoding mutations linked to ALS adopts a spectrum of misfolded states. Mol Neurodegener 6:77. doi:10.1186/1750-1326-6-77
36. Prudencio M, Durazo A, Whitelegge JP, Borchelt DR (2010) An examination of wild-type SOD1 in modulating the toxicity and aggregation of ALS-associated mutant SOD1. Hum Mol Genet 19:4774–4789. doi:10.1093/hmg/ddq408
37. Prudencio M, Hart PJ, Borchelt DR, Andersen PM (2009) Variation in aggregation propensities among ALS-associated variants of SOD1: correlation to human disease. Hum Mol Genet 18:3217–3226. doi:10.1093/hmg/ddp260
38. Qualls DA, Crosby K, Brown H, Borchelt DR (2013) An analysis of interactions between fluorescently-tagged mutant and wild-type SOD1 in intracellular inclusions. PLoS One 8:e83981. doi:10.1371/journal.pone.0083981.s024
39. Ravits J, Paul P, Jorg C (2007) Focality of upper and lower motor neuron degeneration at the clinical onset of ALS. Neurology 68:1571–1575. doi:10.1212/01.wnl.0000260965.20021.47
40. Ravits JM, La Spada AR (2009) ALS motor phenotype heterogeneity, focality, and spread: deconstructing motor neuron degeneration. Neurology 73:805–811. doi:10.1212/WNL.0b013e3181b6bbbd
41. Schneider K, Fangerau H, Michaelsen B, Raab WH-M (2008) The early history of the transmissible spongiform encephalopathies exemplified by scrapie. Brain Res Bull 77:343–355. doi:10.1016/j.brainresbull.2008.09.012
42. Taraboulos A, Jendroska K, Serban D, Yang SL, Dearmond SJ, Prusiner SB (1992) Regional mapping of prion proteins in brain. Proc Natl Acad Sci USA 89:7620–7624
43. Wang J, Farr GW, Zeiss CJ, Rodriguez-Gil DJ, Wilson JH, Furtak K, Rutkowski DT, Kaufman RJ, Ruse CI, Yates JR, Perrin S, Feany MB, Horwich AL (2009) Progressive aggregation despite chaperone associations of a mutant SOD1-YFP in transgenic mice that develop ALS. Proc Natl Acad Sci USA 106:1392–1397. doi:10.1073/pnas.0813045106
44. Wang J, Slunt H, Gonzales V, Fromholt D, Coonfield M, Copeland NG, Jenkins NA, Borchelt DR (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. doi:10.1093/hmg/ddg312
45. Wang J, Xu G, Slunt HH, Gonzales V, Coonfield M, Fromholt D, Copeland NG, Jenkins NA, Borchelt DR (2005) Coincident thresholds of mutant protein for paralytic disease and protein aggregation caused by restrictively expressed superoxide dismutase cDNA. Neurobiol Dis 20:943–952. doi:10.1016/j.nbd.2005.06.005
46. Wong PC, Pardo CA, Borchelt DR, Lee MK, Copeland NG, Jenkins NA, Sisodia SS, Cleveland DW, Price DL (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