Ataxin-1 oligomers induce local spread of pathology and decreasing them by passive immunization slows spinocerebellar ataxia type 1 phenotypes

eLife

Volumn 4, Issue DECEMBER2015, 2015, Pages

  Lasagna Reeves, Cristian A ^a,b   Rousseaux, Maxime W C ^a,b   Guerrero Munoz, Marcos J ^c   Vilanova Velez, Luis ^a,b   Park, Jeehye ^a,b   See, Lauren ^a,b   Jafar Nejad, Paymaan ^a,b   Richman, Ronald ^a,b   Orr, Harry T ^d   Kayed, Rakez ^c   Zoghbi, Huda Y ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Texas Children's Hospital   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOTOR COORDINATION; MOUSE; NEUROPATHOLOGY; NONHUMAN; PASSIVE IMMUNIZATION; PATHOLOGY; PHENOTYPE; PROTEIN EXPRESSION; ROTAROD TEST; STEREOTACTIC PROCEDURE; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; SPINOCEREBELLAR ATAXIAS; TREATMENT OUTCOME;

ANIMALS; ATAXIN-1; DISEASE MODELS, ANIMAL; IMMUNIZATION, PASSIVE; MICE; SPINOCEREBELLAR ATAXIAS; TREATMENT OUTCOME;

EID: 84988638319     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10891     Document Type: Article

References (23)

1. Banks WA, Farr SA, Morley JE, Wolf KM, Geylis V, Steinitz M. 2007. Anti-amyloid beta protein antibody passage across the blood-brain barrier in the SAMP8 mouse model of alzheimer’s disease: an age-related selective uptake with reversal of learning impairment. Experimental Neurology 206:248-256. doi: 10.1016/j.expneurol.2007.05.005
2. Castillo-Carranza DL, Sengupta U, Guerrero-Munoz MJ, Lasagna-Reeves CA, Gerson JE, Singh G, Estes DM, Barrett ADT, Dineley KT, Jackson GR, Kayed R. 2014. Passive immunization with tau oligomer monoclonal antibody reverses tauopathy phenotypes without affecting hyperphosphorylated neurofibrillary tangles. Journal of Neuroscience 34:4260-4272. doi: 10.1523/JNEUROSCI.3192-13.2014
3. Chai X, Wu S, Murray TK, Kinley R, Cella CV, Sims H, Buckner N, Hanmer J, Davies P, O’Neill MJ, Hutton ML, Citron M. 2011. Passive immunization with anti-tau antibodies in two transgenic models: reduction of Tau pathology and delay of disease progression. Journal of Biological Chemistry 286:34457-34467. doi: 10.1074/jbc.M111.229633
4. de Calignon A, Polydoro M, Suárez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, Pitstick R, Sahara N, Ashe KH, Carlson GA, Spires-Jones TL, Hyman BT. 2012. Propagation of tau pathology in a model of early alzheimer’s disease. Neuron 73:685-697. doi: 10.1016/j.neuron.2011.11.033
5. Frost B, Jacks RL, Diamond MI. 2009. Propagation of tau misfolding from the outside to the inside of a cell. Journal of Biological Chemistry 284:12845-12852. doi: 10.1074/jbc.M808759200
6. Games D, Valera E, Spencer B, Rockenstein E, Mante M, Adame A, Patrick C, Ubhi K, Nuber S, Sacayon P, Zago W, Seubert P, Barbour R, Schenk D, Masliah E. 2014. Reducing c-terminal-truncated alpha-synuclein by immunotherapy attenuates neurodegeneration and propagation in parkinson’s disease-like models. Journal of Neuroscience 34:9441-9454. doi: 10.1523/JNEUROSCI.5314-13.2014
7. Guo JL, Lee VMY. 2014. Cell-to-cell transmission of pathogenic proteins in neurodegenerative diseases. Nature Medicine 20:130-138. doi: 10.1038/nm.3457
8. Hardy J, Revesz T. 2012. The spread of neurodegenerative disease. New England Journal of Medicine 366:2126-2128. doi: 10.1056/NEJMcibr1202401
9. Harris JA, Devidze N, Verret L, Ho K, Halabisky B, Thwin MT, Kim D, Hamto P, Lo I, Yu G-Q, Palop JJ, Masliah E, Mucke L. 2010. Transsynaptic progression of amyloid-b-induced neuronal dysfunction within the entorhinal- hippocampal network. Neuron 68:428-441. doi: 10.1016/j.neuron.2010.10.020
10. Holmes BB, Diamond MI. 2012. Cellular mechanisms of protein aggregate propagation. Current Opinion in Neurology 25:721-726. doi: 10.1097/WCO.0b013e32835a3ee0
11. Kayed R. 2003. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300:486-489. doi: 10.1126/science.1079469
12. Lasagna-Reeves CA, Rousseaux MWC, Guerrero-Muñoz MJ, Park J, Jafar-Nejad P, Richman R, Lu N, Sengupta U, Litvinchuk A, Orr HT, Kayed R, Zoghbi HY. 2015. A native interactor scaffolds and stabilizes toxic ATAXIN-1 oligomers in SCA1. eLife 4. doi: 10.7554/eLife.07558
13. Liu L, Drouet V, Wu JW, Witter MP, Small SA, Clelland C, Duff K, Ikezu T. 2012. Trans-synaptic spread of tau pathology in vivo. PLoS ONE 7:e31302. doi: 10.1371/journal.pone.0031302
14. Lorenzetti D. 2000. Repeat instability and motor incoordination in mice with a targeted expanded CAG repeat in the Sca1 locus. Human Molecular Genetics 9:779-785. doi: 10.1093/hmg/9.5.779
15. Masliah E, Rockenstein E, Mante M, Crews L, Spencer B, Adame A, Patrick C, Trejo M, Ubhi K, Rohn TT, Mueller-Steiner S, Seubert P, Barbour R, McConlogue L, Buttini M, Games D, Schenk D, McAlonan GM. 2011. Passive immunization reduces behavioral and neuropathological deficits in an alpha-synuclein transgenic model of lewy body disease. PLoS ONE 6:e19338. doi: 10.1371/journal.pone.0019338
16. Munch C, O’Brien J, Bertolotti A. 2011. Prion-like propagation of mutant superoxide dismutase-1 misfolding in neuronal cells. Proceedings of the National Academy of Sciences of the United States of America 108:3548-3553. doi: 10.1073/pnas.1017275108
17. Park J, Al-Ramahi I, Tan Q, Mollema N, Diaz-Garcia JR, Gallego-Flores T, Lu H-C, Lagalwar S, Duvick L, Kang H, Lee Y, Jafar-Nejad P, Sayegh LS, Richman R, Liu X, Gao Y, Shaw CA, Arthur JSC, Orr HT, Westbrook TF, Botas J, Zoghbi HY. 2013. RAS-MAPK-MSK1 pathway modulates ataxin 1 protein levels and toxicity in SCA1. Nature 498:325-331. doi: 10.1038/nature12204
18. Pecho-Vrieseling E, Rieker C, Fuchs S, Bleckmann D, Esposito MS, Botta P, Goldstein C, Bernhard M, Galimberti I, Müller M, Lüthi A, Arber S, Bouwmeester T, van der Putten H, Di Giorgio FP. 2014. Transneuronal propagation of mutant huntingtin contributes to non-cell autonomous pathology in neurons. Nature Neuroscience 17:1064-1072. doi: 10.1038/nn.3761
19. Pedersen JS, Christensen G, Otzen DE. 2004. Modulation of S6 fibrillation by unfolding rates and gatekeeper residues. Journal of Molecular Biology 341:575-588. doi: 10.1016/j.jmb.2004.06.020
20. Serio TR. 2000. Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289:1317-1321. doi: 10.1126/science.289.5483.1317
21. Tran HT, Chung CH-Y, Iba M, Zhang B, Trojanowski JQ, Luk KC, Lee VMY. 2014. a-synuclein immunotherapy blocks uptake and templated propagation of misfolded a-synuclein and neurodegeneration. Cell Reports 7: 2054-2065. doi: 10.1016/j.celrep.2014.05.033
22. Watase K, Weeber EJ, Xu B, Antalffy B, Yuva-Paylor L, Hashimoto K, Kano M, Atkinson R, Sun Y, Armstrong DL, Sweatt JD, Orr HT, Paylor R, Zoghbi HY. 2002. A long CAG repeat in the mouse Sca1 locus replicates SCA1 features and reveals the impact of protein solubility on selective neurodegeneration. Neuron 34:905-919. doi: 10.1016/S0896-6273(02)00733-X
23. Yanamandra K, Kfoury N, Jiang H, Mahan TE, Ma S, Maloney SE, Wozniak DF, Diamond MI, Holtzman DM. 2013. Anti-tau antibodies that block tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Neuron 80:402-414. doi: 10.1016/j.neuron.2013.07.046