Prion-like activity of Cu/Zn superoxide dismutase Implications for amyotrophic lateral sclerosis

Prion

Volumn 8, Issue 1, 2014, Pages

  Grad, Leslie I ^a   Cashman, Neil R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Amyotrophic lateral sclerosis; Intercellular transmission; Neurodegenerative disease; Prion like; Protein misfolding; Superoxide dismutase 1

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; PRION PROTEIN; PRION; SUPEROXIDE DISMUTASE;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; CELL DEATH; CELL TRANSPORT; CHRONIC WASTING DISEASE; DEGENERATIVE DISEASE; ENZYME ACTIVITY; EXOSOME; HUMAN; MOTONEURON; MOTOR NEURON DISEASE; MULTIVESICULAR BODY; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRION DISEASE; PROTEIN FOLDING; REVIEW; SECRETORY PATHWAY; WILD TYPE; CHEMISTRY; GENETICS; METABOLISM; PRION;

AMYOTROPHIC LATERAL SCLEROSIS; HUMANS; PRIONS; PROTEIN FOLDING; SUPEROXIDE DISMUTASE;

EID: 84896970296     PISSN: 19336896     EISSN: 1933690X     Source Type: Journal    
DOI: 10.4161/pri.27602     Document Type: Review

References (107)

1. Cleveland DW, Rothstein JD. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2001; 2:806-19; PMID:11715057; http://dx.doi. org/10.1038/35097565 (Pubitemid 33674062)
2. Bradley WG. Updates on amyotrophic lateral sclerosis: improving patient care. Ann Neurol 2009; 65(Suppl 1):S1-2; PMID:19191303; http://dx.doi. org/10.1002/ana.21546
3. Strong M, Rosenfeld J. Amyotrophic lateral sclerosis: a review of current concepts. Amyotroph Lateral Scler Other Motor Neuron Disord 2003; 4:136-43; PMID:13129799; http://dx.doi. org/10.1080/14660820310011250 (Pubitemid 37184881)
4. Elden AC, Kim HJ, Hart MP, Chen-Plotkin AS, Johnson BS, Fang X, Armakola M, Geser F, Greene R, Lu MM, et al. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 2010; 466:1069-75; PMID:20740007; http://dx.doi.org/10.1038/ nature09320
5. Haverkamp LJ, Appel V, Appel SH. Natural history of amyotrophic lateral sclerosis in a database population. Validation of a scoring system and a model for survival prediction. Brain 1995; 118:707-19; PMID:7600088; http://dx.doi.org/10.1093/ brain/118.3.707
6. Mutation Database ALS. http://reseq.biosciencedbc. jp/resequence/ SearchDisease.do?targetId=1. The University of Tokyo, 2007.
7. Deng HX, Chen W, Hong ST, Boycott KM, Gorrie GH, Siddique N, Yang Y, Fecto F, Shi Y, Zhai H, et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011; 477:211-5; PMID:21857683; http:// dx.doi.org/10.1038/nature10353
8. Wu CH, Fallini C, Ticozzi N, Keagle PJ, Sapp PC, Piotrowska K, Lowe P, Koppers M, McKenna-Yasek D, Baron DM, et al. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 2012; 488:499-503; PMID:22801503; http://dx.doi. org/10.1038/nature11280
9. Stewart H, Rutherford NJ, Briemberg H, Krieger C, Cashman N, Fabros M, Baker M, Fok A, DeJesus-Hernandez M, Eisen A, et al. Clinical and pathological features of amyotrophic lateral sclerosis caused by mutation in the C9ORF72 gene on chromosome 9p. Acta Neuropathol 2012; 123:409-17; PMID:22228244; http://dx.doi.org/10.1007/ s00401-011-0937-5
10. Rosen DR. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993; 364:362; PMID:8332197; http://dx.doi.org/10.1038/364362c0 (Pubitemid 23265284)
11. Andersen PM. Genetic factors in the early diagnosis of ALS. Amyotroph Lateral Scler Other Motor Neuron Disord 2000; 1(Suppl 1):S31-42; PMID:11464924; http://dx.doi.org/10.1080/14660820052415899
12. Robberecht W. Genetics of amyotrophic lateral sclerosis. J Neurol 2000; 247:2-6; PMID:11200702; http://dx.doi.org/10.1007/PL00007785 (Pubitemid 32038222)
13. Andersen PM, Sims KB, Xin WW, Kiely R, O'Neill G, Ravits J, Pioro E, Harati Y, Brower RD, Levine JS, et al. Sixteen novel mutations in the Cu/Zn superoxide dismutase gene in amyotrophic lateral sclerosis: a decade of discoveries, defects and disputes. Amyotroph Lateral Scler Other Motor Neuron Disord 2003; 4:62-73; PMID:14506936; http:// dx.doi.org/10.1080/ 14660820310011700 (Pubitemid 36874774)
14. Cashman NR, Chakrabartty A, Rakhit R, Ostermann JB. EP 2495327 A3. Methods and compositions to treat and detect misfolded SOD1 mediated diseases 2007.
15. Rakhit R, Crow JP, Lepock JR, Kondejewski LH, Cashman NR, Chakrabartty A. Monomeric Cu,Znsuperoxide dismutase is a common misfolding intermediate in the oxidation models of sporadic and familial amyotrophic lateral sclerosis. J Biol Chem 2004; 279:15499-504; PMID:14734542; http:// dx.doi.org/10.1074/jbc. M313295200 (Pubitemid 38618950)
16. Rakhit R, Robertson J, Vande Velde C, 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; 13:754-9; PMID:17486090; http:// dx.doi.org/10.1038/nm1559 (Pubitemid 46889748)
17. Rakhit R, Cunningham P, Furtos-Matei A, Dahan S, Qi XF, Crow JP, Cashman NR, Kondejewski LH, Chakrabartty A. Oxidation-induced misfolding and aggregation of superoxide dismutase and its implications for amyotrophic lateral sclerosis. J Biol Chem 2002; 277:47551-6; PMID:12356748; http://dx.doi. org/10.1074/jbc.M207356200 (Pubitemid 36159274)
18. Casoni F, Basso M, Massignan T, Gianazza E, Cheroni C, Salmona M, Bendotti C, Bonetto V. Protein nitration in a mouse model of familial amyotrophic lateral sclerosis: possible multifunctional role in the pathogenesis. J Biol Chem 2005; 280:16295-304; PMID:15699043; http://dx.doi.org/10.1074/ jbc.M413111200 (Pubitemid 40616757)
19. Kato S, Takikawa M, Nakashima K, Hirano A, Cleveland DW, Kusaka H, Shibata N, Kato M, Nakano I, Ohama E. New consensus research on neuropathological aspects of familial amyotrophic lateral sclerosis with superoxide dismutase 1 (SOD1) gene mutations: inclusions containing SOD1 in neurons and astrocytes. Amyotroph Lateral Scler Other Motor Neuron Disord 2000; 1:163-84; PMID:11464950; http://dx.doi.org/10.1080/14660820050515160
20. Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins NA, Copeland NG, Sisodia SS, Rothstein JD, Borchelt DR, Price DL, et al. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 1997; 18:327-38; PMID:9052802; http://dx.doi.org/10.1016/ S0896-6273(00)80272-X (Pubitemid 27111114)
21. Durham HD, Roy J, Dong L, Figlewicz DA. Aggregation of mutant Cu/Zn superoxide dismutase proteins in a culture model of ALS. J Neuropathol Exp Neurol 1997; 56:523-30; PMID:9143265; http:// dx.doi.org/10.1097/00005072- 199705000-00008 (Pubitemid 27463093)
22. Matias-Guiu J, Galan L, Garcia-Ramos R, Barcia JA. Superoxide dismutase: the cause of all amyotrophic lateral sclerosis? Ann Neurol 2008; 64:356-7, author reply 358; PMID:18350588; http://dx.doi. org/10.1002/ana.21373
23. Synofzik M, Ronchi D, Keskin I, Basak AN, Wilhelm C, Gobbi C, Birve A, Biskup S, Zecca C, Fernández- Santiago R, et al. Mutant superoxide dismutase-1 indistinguishable from wild-type causes ALS. Hum Mol Genet 2012; 21:3568-74; PMID:22595972; http://dx.doi.org/10.1093/hmg/dds188
24. Shibata N, Hirano A, Kobayashi M, Sasaki S, Kato T, Matsumoto S, Shiozawa Z, Komori T, Ikemoto A, Umahara T, et al. Cu/Zn superoxide dismutase-like immunoreactivity in Lewy body-like inclusions of sporadic amyotrophic lateral sclerosis. Neurosci Lett 1994; 179:149-52; PMID:7845611; http://dx.doi. org/10.1016/0304-3940(94)90956-3 (Pubitemid 24298580)
25. Chou SM, Wang HS, Komai K. Colocalization of NOS and SOD1 in neurofilament accumulation within motor neurons of amyotrophic lateral sclerosis: an immunohistochemical study. J Chem Neuroanat 1996; 10:249-58; PMID:8811414; http:// dx.doi.org/10.1016/0891-0618(96)00137-8 (Pubitemid 26196652)
26. Chou SM, Wang HS, Taniguchi A. Role of SOD-1 and nitric oxide/cyclic GMP cascade on neurofilament aggregation in ALS/MND. J Neurol Sci 1996; 139(Suppl):16-26; PMID:8899653; http://dx.doi. org/10.1016/0022-510X(96)00090-1
27. Gruzman A, Wood WL, Alpert E, Prasad MD, Miller RG, Rothstein JD, Bowser R, Hamilton R, Wood TD, Cleveland DW, et al. Common molecular signature in SOD1 for both sporadic and familial amyotrophic lateral sclerosis. Proc Natl Acad Sci U S A 2007; 104:12524-9; PMID:17636119; http://dx.doi. org/10.1073/pnas. 0705044104 (Pubitemid 47206171)
28. Broom WJ, Greenway M, Sadri-Vakili G, Russ C, Auwarter KE, Glajch KE, Dupre N, Swingler RJ, Purcell S, Hayward C, et al. 50bp deletion in the promoter for superoxide dismutase 1 (SOD1) reduces SOD1 expression in vitro and may correlate with increased age of onset of sporadic amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2008; 9:229-37; PMID:18608091; http://dx.doi. org/10.1080/17482960802103107
29. Forsberg K, Jonsson PA, Andersen PM, Bergemalm D, Graffmo KS, Hultdin M, Jacobsson J, Rosquist R, Marklund SL, Brännström T. Novel antibodies reveal inclusions containing non-native SOD1 in sporadic ALS patients. PLoS One 2010; 5:e11552; PMID:20644736; http://dx.doi.org/10.1371/journal. pone.0011552
30. Bosco DA, Morfini G, Karabacak NM, Song Y, Gros-Louis F, Pasinelli P, Goolsby H, Fontaine BA, Lemay N, McKenna-Yasek D, et al. Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat Neurosci 2010; 13:1396-403; PMID:20953194; http://dx.doi. org/10.1038/nn.2660
31. Pokrishevsky E, Grad LI, Yousefi M, Wang J, Mackenzie IR, Cashman NR. Aberrant localization of FUS and TDP43 is associated with misfolding of SOD1 in amyotrophic lateral sclerosis. PLoS One 2012; 7:e35050; PMID:22493728; http://dx.doi. org/10.1371/journal.pone.0035050
32. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996; 271:C1424-37; PMID:8944624
33. Shefner JM, Reaume AG, Flood DG, Scott RW, Kowall NW, Ferrante RJ, Siwek DF, Upton-Rice M, Brown RH Jr. Mice lacking cytosolic copper/ zinc superoxide dismutase display a distinctive motor axonopathy. Neurology 1999; 53:1239-46; PMID:10522879; http://dx.doi.org/10.1212/ WNL.53.6.1239 (Pubitemid 29480082)
34. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994; 264:1772-5; PMID:8209258; http://dx.doi.org/10.1126/ science.8209258 (Pubitemid 24227760)
35. Andersen PM, Nilsson P, Ala-Hurula V, Keränen ML, Tarvainen I, Haltia T, Nilsson L, Binzer M, Forsgren L, Marklund SL. Amyotrophic lateral sclerosis associated with homozygosity for an Asp90Ala mutation in CuZn-superoxide dismutase. Nat Genet 1995; 10:61-6; PMID:7647793; http://dx.doi. org/10.1038/ng0595-61
36. Reaume AG, Elliott JL, Hoffman EK, Kowall NW, Ferrante RJ, Siwek DF, Wilcox HM, Flood DG, Beal MF, Brown RH Jr., et al. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat Genet 1996; 13:43-7; PMID:8673102; http://dx.doi.org/10.1038/ng0596-43
37. Said Ahmed M, Hung WY, Zu JS, Hockberger P, Siddique T. Increased reactive oxygen species in familial amyotrophic lateral sclerosis with mutations in SOD1. J Neurol Sci 2000; 176:88-94; PMID:10930589; http://dx.doi.org/10. 1016/ S0022-510X(00)00317-8 (Pubitemid 30621604)
38. Beckman JS, Carson M, Smith CD, Koppenol WH. ALS, SOD and peroxynitrite. Nature 1993; 364:584; PMID:8350919; http://dx.doi. org/10.1038/364584a0
39. Beckman JS, Estévez AG, Crow JP, Barbeito L. Superoxide dismutase and the death of motoneurons in ALS. Trends Neurosci 2001; 24(Suppl):S15-20; PMID:11881740; http://dx.doi.org/10.1016/ S0166-2236(00)01981-0
40. Cleveland DW, Liu J. Oxidation versus aggregation - how do SOD1 mutants cause ALS? Nat Med 2000; 6:1320-1; PMID:11100110; http://dx.doi. org/10.1038/82122 (Pubitemid 32001005)
41. Bendotti C, Marino M, Cheroni C, Fontana E, Crippa V, Poletti A, De Biasi S. Dysfunction of constitutive and inducible ubiquitin-proteasome system in amyotrophic lateral sclerosis: implication for protein aggregation and immune response. Prog Neurobiol 2012; 97:101-26; PMID:22033150; http://dx.doi.org/10. 1016/j.pneurobio.2011.10.001
42. Bard F, Fox M, Friedrich S, Seubert P, Schenk D, Kinney GG, Yednock T. Sustained levels of antibodies against A? in amyloid-rich regions of the CNS following intravenous dosing in human APP transgenic mice. Exp Neurol 2012; 238:38-43; PMID:22892246; http://dx.doi.org/10.1016/j. expneurol.2012.07.022
43. Ravits J, Paul P, Jorg C. Focality of upper and lower motor neuron degeneration at the clinical onset of ALS. Neurology 2007; 68:1571-5; PMID:17485643; http://dx.doi.org/10.1212/01. wnl.0000260965.20021.47 (Pubitemid 46717980)
44. Ravits JM, La Spada AR. ALS motor phenotype heterogeneity, focality, and spread: deconstructing motor neuron degeneration. Neurology 2009; 73:805-11; PMID:19738176; http://dx.doi.org/10.1212/ WNL.0b013e3181b6bbbd
45. Luk KC, Kehm V, Carroll J, Zhang B, O'Brien P, Trojanowski JQ, Lee VM. Pathological ?-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 2012; 338:949-53; PMID:23161999; http://dx.doi.org/10.1126/ science.1227157
46. Eisele YS, Bolmont T, Heikenwalder M, Langer F, Jacobson LH, Yan ZX, Roth K, Aguzzi A, Staufenbiel M, Walker LC, et al. Induction of cerebral beta-amyloidosis: intracerebral versus systemic Abeta inoculation. Proc Natl Acad Sci U S A 2009; 106:12926-31; PMID:19622727; http://dx.doi.org/10.1073/ pnas.0903200106
47. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science 1982; 216:136-44; PMID:6801762; http://dx.doi.org/10.1126/ science.6801762 (Pubitemid 12089840)
48. Ratovitski T, Corson LB, Strain J, Wong P, Cleveland DW, Culotta VC, Borchelt DR. 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 1999; 8:1451-60; PMID:10400992; http://dx.doi.org/10.1093/hmg/8.8.1451 (Pubitemid 29374078)
49. Chia R, Tattum MH, Jones S, Collinge J, Fisher EM, Jackson GS. Superoxide dismutase 1 and tgSOD1 mouse spinal cord seed fibrils, suggesting a propagative cell death mechanism in amyotrophic lateral sclerosis. PLoS One 2010; 5:e10627; PMID:20498711; http://dx.doi.org/10.1371/journal.pone.0010627
50. 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; 18:3217-26; PMID:19483195; http://dx.doi.org/10. 1093/hmg/ ddp260
51. Wang J, Xu G, Gonzales V, Coonfield M, Fromholt D, Copeland NG, Jenkins NA, Borchelt DR. Fibrillar inclusions and motor neuron degeneration in transgenic mice expressing superoxide dismutase 1 with a disrupted copper-binding site. Neurobiol Dis 2002; 10:128-38; PMID:12127151; http://dx.doi. org/10.1006/nbdi.2002.0498 (Pubitemid 34775466)
52. Furukawa Y, Kaneko K, Yamanaka K, O'Halloran TV, Nukina N. Complete loss of post-translational modifications triggers fibrillar aggregation of SOD1 in the familial form of amyotrophic lateral sclerosis. J Biol Chem 2008; 283:24167-76; PMID:18552350; http://dx.doi.org/10.1074/jbc.M802083200
53. Kerman A, Liu HN, Croul S, Bilbao J, Rogaeva E, Zinman L, Robertson J, Chakrabartty A. Amyotrophic lateral sclerosis is a non-amyloid disease in which extensive misfolding of SOD1 is unique to the familial form. Acta Neuropathol 2010; 119:335-44; PMID:20111867; http://dx.doi.org/10.1007/ s00401-010-0646-5
54. Jaarsma D, Haasdijk ED, Grashorn JA, Hawkins R, van Duijn W, Verspaget HW, London J, Holstege JC. Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol Dis 2000; 7(6 Pt B):623-43; PMID:11114261; http://dx.doi.org/10.1006/ nbdi.2000.0299 (Pubitemid 32044287)
55. 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; 18:1642-51; PMID:19233858; http:// dx.doi.org/10.1093/hmg/ddp085
56. Fukada K, Nagano S, Satoh M, Tohyama C, Nakanishi T, Shimizu A, Yanagihara T, Sakoda S. Stabilization of mutant Cu/Zn superoxide dismutase (SOD1) protein by coexpressed wild SOD1 protein accelerates the disease progression in familial amyotrophic lateral sclerosis mice. Eur J Neurosci 2001; 14:2032-6; PMID:11860498; http://dx.doi. org/10.1046/j.0953-816x.2001.01828.x (Pubitemid 35463690)
57. 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; 103:7142-7; PMID:16636275; http://dx.doi.org/10.1073/pnas.0602046103
58. 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; 281:1851-4; PMID:9743498; http://dx.doi.org/10.1126/ science.281.5384.1851 (Pubitemid 28450505)
59. Grad LI, Guest WC, Yanai A, Pokrishevsky E, O'Neill MA, Gibbs E, Semenchenko V, Yousefi M, Wishart DS, Plotkin SS, et al. Intermolecular transmission of superoxide dismutase 1 misfolding in living cells. Proc Natl Acad Sci U S A 2011; 108:16398-403; PMID:21930926; http://dx.doi. org/10.1073/pnas.1102645108
60. Taylor DM, Gibbs BF, Kabashi E, Minotti S, Durham HD, Agar JN. Tryptophan 32 potentiates aggregation and cytotoxicity of a copper/zinc superoxide dismutase mutant associated with familial amyotrophic lateral sclerosis. J Biol Chem 2007; 282:16329-35; PMID:17389599; http://dx.doi.org/10.1074/jbc. M610119200 (Pubitemid 47100349)
61. Raymond GJ, Bossers A, Raymond LD, O'Rourke KI, McHolland LE, Bryant PK 3rd, Miller MW, Williams ES, Smits M, Caughey B. Evidence of a molecular barrier limiting susceptibility of humans, cattle and sheep to chronic wasting disease. EMBO J 2000; 19:4425-30; PMID:10970836; http://dx.doi. org/10.1093/emboj/19.17. 4425
62. 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; 40:245-50; PMID:20573565; http://dx.doi.org/10.1016/j.nbd. 2010.05.031
63. 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; 108:1009-18; PMID:19077113; http://dx.doi.org/10.1111/j.1471- 4159.2008.05839.x
64. Münch C, O'Brien J, Bertolotti A. Prion-like propagation of mutant superoxide dismutase-1 misfolding in neuronal cells. Proc Natl Acad Sci U S A 2011; 108:3548-53; PMID:21321227; http://dx.doi. org/10.1073/pnas.1017275108
65. Horwich AL, Weissman JS. Deadly conformations- protein misfolding in prion disease. Cell 1997; 89:499-510; PMID:9160742; http://dx.doi. org/10.1016/S0092-8674(00)80232-9 (Pubitemid 27511761)
66. Witan H, Gorlovoy P, Kaya AM, Koziollek-Drechsler I, Neumann H, Behl C, Clement AM. Wild-type Cu/ Zn superoxide dismutase (SOD1) does not facilitate, but impedes the formation of protein aggregates of amyotrophic lateral sclerosis causing mutant SOD1. Neurobiol Dis 2009; 36:331-42; PMID:19660548; http://dx.doi.org/10.1016/j.nbd.2009.07.024
67. 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; 19:4774-89; PMID:20871097; http://dx.doi.org/ 10.1093/hmg/ ddq408
68. Aguzzi A, Rajendran L. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 2009; 64:783-90; PMID:20064386; http://dx.doi. org/10.1016/j.neuron.2009.12.016
69. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002; 297:353-6; PMID:12130773; http://dx.doi.org/10.1126/ science.1072994 (Pubitemid 34790756)
70. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, Kilger E, Neuenschwander A, Abramowski D, Frey P, Jaton AL, et al. Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 2006; 313:1781-4; PMID:16990547; http://dx.doi.org/10.1126/ science.1131864 (Pubitemid 44454153)
71. Luk KC, Song C, O'Brien P, Stieber A, Branch JR, Brunden KR, Trojanowski JQ, Lee VM. Exogenous alpha-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci U S A 2009; 106:20051-6; PMID:19892735; http://dx.doi.org/10.1073/ pnas.0908005106
72. Münch C, Bertolotti A. Exposure of hydrophobic surfaces initiates aggregation of diverse ALScausing superoxide dismutase-1 mutants. J Mol Biol 2010; 399:512-25; PMID:20399791; http://dx.doi. org/10.1016/j.jmb.2010.04.019
73. Wang Q, Johnson JL, Agar NY, Agar JN. Protein aggregation and protein instability govern familial amyotrophic lateral sclerosis patient survival. PLoS Biol 2008; 6:e170; PMID:18666828; http://dx.doi. org/10.1371/journal.pbio. 0060170
74. Elam JS, Taylor AB, Strange R, Antonyuk S, Doucette PA, Rodriguez JA, Hasnain SS, Hayward LJ, Valentine JS, Yeates TO, et al. Amyloid-like filaments and water-filled nanotubes formed by SOD1 mutant proteins linked to familial ALS. Nat Struct Biol 2003; 10:461-7; PMID:12754496; http:// dx.doi.org/10.1038/ nsb935 (Pubitemid 36637644)
75. Furukawa Y, Kaneko K, Watanabe S, Yamanaka K, Nukina N. Intracellular seeded aggregation of mutant Cu,Zn-superoxide dismutase associated with amyotrophic lateral sclerosis. FEBS Lett 2013; 587:2500-5; PMID:23831581; http://dx.doi.org/10.1016/j. febslet.2013.06.046
76. Grad LI, Yerbury JJ, Turner BJ, Guest WC, Pokrishevsky E, O'Neill MA, Yanai A, Silverman JM, Zeineddine R, Corcoran L, et al. Intercellular propagated misfolding of wild-type Cu/Zn superoxide dismutase occurs via exosome-dependent and -independent mechanisms. Proc Natl Acad Sci U S A 2014; PMID:24550511; http://dx.doi.org/10.1073/ pnas.1312245111.
77. Guest WC, Plotkin SS, Cashman NR. Toward a mechanism of prion misfolding and structural models of PrP(Sc): current knowledge and future directions. J Toxicol Environ Health A 2011; 74:154-60; PMID:21218344; http://dx.doi.org/10. 1080/152873 94.2011.529065
78. Haass C, Selkoe DJ. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 2007; 8:101-12; PMID:17245412; http://dx.doi.org/10.1038/ nrm2101 (Pubitemid 46432529)
79. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003; 300:486-9; PMID:12702875; http://dx.doi.org/10.1126/ science.1079469 (Pubitemid 36444329)
80. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH. A specific amyloidbeta protein assembly in the brain impairs memory. Nature 2006; 440:352-7; PMID:16541076; http:// dx.doi.org/10.1038/ nature04533
81. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 2008; 14:837-42; PMID:18568035; http://dx.doi. org/10.1038/nm1782
82. El-Agnaf OM, Salem SA, Paleologou KE, Curran MD, Gibson MJ, Court JA, Schlossmacher MG, Allsop D. Detection of oligomeric forms of alphasynuclein protein in human plasma as a potential biomarker for Parkinson's disease. FASEB J 2006; 20:419-25; PMID:16507759; http://dx.doi. org/10.1096/fj.03-1449com (Pubitemid 44933318)
83. Lashuel HA, Petre BM, Wall J, Simon M, Nowak RJ, Walz T, Lansbury PT Jr. Alpha-synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J Mol Biol 2002; 322:1089-102; PMID:12367530; http:// dx.doi.org/10.1016/S0022-2836(02)00735-0
84. Keller S, Sanderson MP, Stoeck A, Altevogt P. Exosomes: from biogenesis and secretion to biological function. Immunol Lett 2006; 107:102-8; PMID:17067686; http://dx.doi.org/10.1016/j. imlet.2006.09.005 (Pubitemid 44779821)
85. Flanagan J, Middeldorp J, Sculley T. Localization of the Epstein-Barr virus protein LMP 1 to exosomes. J Gen Virol 2003; 84:1871-9; PMID:12810882; http://dx.doi.org/10.1099/vir.0.18944-0 (Pubitemid 36805923)
86. Gould SJ, Booth AM, Hildreth JE. The Trojan exosome hypothesis. Proc Natl Acad Sci U S A 2003; 100:10592-7; PMID:12947040; http://dx.doi. org/10.1073/pnas.1831413100 (Pubitemid 37140073)
87. Nguyen DG, Booth A, Gould SJ, Hildreth JE. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J Biol Chem 2003; 278:52347-54; PMID:14561735; http://dx.doi.org/10.1074/jbc.M309009200 (Pubitemid 38035824)
88. Perez-Gonzalez R, Gauthier SA, Kumar A, Levy E. The exosome secretory pathway transports amyloid precursor protein carboxyl-terminal fragments from the cell into the brain extracellular space. J Biol Chem 2012; 287:43108-15; PMID:23129776; http:// dx.doi.org/10.1074/jbc.M112.404467
89. Emmanouilidou E, Melachroinou K, Roumeliotis T, Garbis SD, Ntzouni M, Margaritis LH, Stefanis L, Vekrellis K. Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J Neurosci 2010; 30:6838-51; PMID:20484626; http://dx.doi.org/10.1523/ JNEUROSCI.5699-09.2010
90. Danzer KM, Kranich LR, Ruf WP, Cagsal- Getkin O, Winslow AR, Zhu L, Vanderburg CR, McLean PJ. Exosomal cell-to-cell transmission of alpha synuclein oligomers. Mol Neurodegener 2012; 7:42; PMID:22920859; http://dx.doi. org/10.1186/1750-1326-7-42
91. Fevrier B, Vilette D, Archer F, Loew D, Faigle W, Vidal M, Laude H, Raposo G. Cells release prions in association with exosomes. Proc Natl Acad Sci U S A 2004; 101:9683-8; PMID:15210972; http://dx.doi. org/10.1073/pnas. 0308413101
92. Coleman BM, Hassen E, Lawson VA, Hill AF. Prion-infected cells regulate the release of exosomes with distinct ultrastructural features. FASEB J 2012; 26:4160-73; PMID:22767229; http://dx.doi. org/10.1096/fj.11-202077
93. Kim DK, Kang B, Kim OY, Choi DS, Lee J, Kim SR, Go G, Yoon YJ, Kim JH, Jang SC, et al. EVpedia: an integrated database of high-throughput data for systemic analyses of extracellular vesicles. J Extracell Vesicles 2013; 2.
94. Turner BJ, Atkin JD, Farg MA, Zang DW, Rembach A, Lopes EC, Patch JD, Hill AF, Cheema SS. Impaired extracellular secretion of mutant superoxide dismutase 1 associates with neurotoxicity in familial amyotrophic lateral sclerosis. J Neurosci 2005; 25:108-17; PMID:15634772; http://dx.doi. org/10.1523/JNEUROSCI.4253-04.2005 (Pubitemid 40110771)
95. Gomes C, Palma AS, Almeida R, Regalla M, McCluskey LF, Trojanowski JQ, Costa J. Establishment of a cell model of ALS disease: Golgi apparatus disruption occurs independently from apoptosis. Biotechnol Lett 2008; 30:603-10; PMID:18004513; http://dx.doi.org/10.1007/ s10529-007-9595-z
96. Gomes C, Keller S, Altevogt P, Costa J. Evidence for secretion of Cu,Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis. Neurosci Lett 2007; 428:43-6; PMID:17942226; http://dx.doi.org/10. 1016/j.neulet.2007.09.024 (Pubitemid 47633803)
97. Urushitani M, Sik A, Sakurai T, Nukina N, Takahashi R, Julien JP. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci 2006; 9:108-18; PMID:16369483; http://dx.doi. org/10.1038/nn1603 (Pubitemid 43011916)
98. Urushitani M, Ezzi SA, Matsuo A, Tooyama I, Julien JP. The endoplasmic reticulum-Golgi pathway is a target for translocation and aggregation of mutant superoxide dismutase linked to ALS. FASEB J 2008; 22:2476-87; PMID:18337461; http://dx.doi. org/10.1096/fj.07-092783 (Pubitemid 351948665)
99. Basso M, Pozzi S, Tortarolo M, Fiordaliso F, Bisighini C, Pasetto L, Spaltro G, Lidonnici D, Gensano F, Battaglia E, et al. Mutant copper-zinc superoxide dismutase (SOD1) induces protein secretion pathway alterations and exosome release in astrocytes: implications for disease spreading and motor neuron pathology in amyotrophic lateral sclerosis. J Biol Chem 2013; 288:15699-711; PMID:23592792; http:// dx.doi.org/10.1074/jbc.M112.425066
100. Kabashi E, Valdmanis PN, Dion P, Rouleau GA. Oxidized/misfolded superoxide dismutase-1: the cause of all amyotrophic lateral sclerosis? Ann Neurol 2007; 62:553-9; PMID:18074357; http://dx.doi. org/10.1002/ana.21319
101. Haidet-Phillips AM, Hester ME, Miranda CJ, Meyer K, Braun L, Frakes A, Song S, Likhite S, Murtha MJ, Foust KD, et al. Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat Biotechnol 2011; 29:824-8; PMID:21832997; http://dx.doi.org/10.1038/nbt.1957
102. Legname G, Nguyen HO, Baskakov IV, Cohen FE, Dearmond SJ, Prusiner SB. Strain-specified characteristics of mouse synthetic prions. Proc Natl Acad Sci U S A 2005; 102:2168-73; PMID:15671162; http:// dx.doi.org/10.1073/pnas. 0409079102 (Pubitemid 40262030)
103. Irwin DJ, Abrams JY, Schonberger LB, Leschek EW, Mills JL, Lee VM, Trojanowski JQ. Evaluation of potential infectivity of Alzheimer and Parkinson disease proteins in recipients of cadaver-derived human growth hormone. JAMA Neurol 2013; 70:462-8; PMID:23380910; http://dx.doi.org/10.1001/ jamaneurol.2013.1933
104. Eisele YS, Obermüller U, Heilbronner G, Baumann F, Kaeser SA, Wolburg H, Walker LC, Staufenbiel M, Heikenwalder M, Jucker M. Peripherally applied Abeta-containing inoculates induce cerebral beta-amyloidosis. Science 2010; 330:980-2; PMID:20966215; http://dx.doi.org/10.1126/ science.1194516
105. Weichert A, Besemer AS, Liebl M, Hellmann N, Koziollek-Drechsler I, Ip P, Decker H, Robertson J, Chakrabartty A, Behl C, et al. Wild-type Cu/Zn superoxide dismutase stabilizes mutant variants by heterodimerization. Neurobiol Dis 2014; 62:479-88; PMID:24200866; http://dx.doi.org/10.1016/j. nbd.2013.10.027
106. Furukawa Y, Kaneko K, Watanabe S, Yamanaka K, Nukina N. A seeding reaction recapitulates intracellular formation of Sarkosyl-insoluble transactivation response element (TAR) DNA-binding protein-43 inclusions. J Biol Chem 2011; 286:18664-72; PMID:21454603; http://dx.doi.org/10.1074/jbc. M111.231209
107. Nonaka T, Masuda-Suzukake M, Arai T, Hasegawa Y, Akatsu H, Obi T, Yoshida M, Murayama S, Mann DM, Akiyama H, et al. Prion-like properties of pathological TDP-43 aggregates from diseased brains. Cell Rep 2013; 4:124-34; PMID:23831027; http:// dx.doi.org/10.1016/j.celrep.2013.06.007