Seeding induced by α-synuclein oligomers provides evidence for spreading of α-synuclein pathology

Journal of Neurochemistry

Volumn 111, Issue 1, 2009, Pages 192-203

  Danzer, Karin M ^a,b   Krebs, Simon K ^a   Wolff, Michael ^b   Birk, Gerald ^b   Hengerer, Bastian ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

Author keywords

synuclein; Aggregation; Neurodegeneration; Oligomers; Parkinson's disease; Seeding

Indexed keywords

ALPHA SYNUCLEIN; DODECYL SULFATE; LITHIUM; MEMBRANE PROTEIN; OLIGOMER;

ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CELL LINE; EMBRYO; IN VITRO STUDY; MOUSE; NERVE CELL CULTURE; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION;

ANIMALS; CALCIUM; CELLS, CULTURED; CEREBRAL CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MICE; MUTATION; NEUROBLASTOMA; NEURONS; PEPTIDE FRAGMENTS; STATISTICS, NONPARAMETRIC; TIME FACTORS; TRANSFECTION;

EID: 70349223775     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06324.x     Document Type: Article

References (40)

1. Ahn K. J., Paik S. R., Chung K. C. Kim J. (2006) Amino acid sequence motifs and mechanistic features of the membrane translocation of αsynuclein. J. Neurochem. 97, 265 279.
2. Auluck P. K., Chan H. Y., Trojanowski J. Q., Lee V. M. Bonini N. M. (2002) Chaperone suppression of αsynuclein toxicity in a Drosophila model for Parkinson's disease. Science 295, 865 868.
3. Bodner R. A., Outeiro T. F., Altmann S. et al. (2006) Pharmacological promotion of inclusion formation: a therapeutic approach for Huntington's and Parkinson's diseases. Proc. Natl Acad. Sci. USA 103, 4246 4251.
4. Braak H. Braak E. (2000) Pathoanatomy of Parkinson's disease. J. Neurol. 247 (Suppl. 2 II3 II10.
5. Braak H., de Vos R. A., Jansen E. N., Bratzke H. Braak E. (1998) Neuropathological hallmarks of Alzheimer's and Parkinson's diseases. Prog. Brain Res. 117, 267 285.
6. Braak H., Del T. K., Rub U., de Vos R. A., Jansen Steur E. N. Braak E. (2003a) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 24, 197 211.
7. Braak H., Rub U., Gai W. P. Del T. K. (2003b) Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J. Neural Transm. 110, 517 536.
8. Braak H., Bohl J. R., Muller C. M., Rub U., de Vos R. A. Del T. K. (2006) Stanley Fahn Lecture 2005: the staging procedure for the inclusion body pathology associated with sporadic Parkinson's disease reconsidered. Mov. Disord. 21, 2042 2051.
9. Brundin P., Li J. Y., Holton J. L., Lindvall O. Revesz T. (2008) Research in motion: the enigma of Parkinson's disease pathology spread. Nat. Rev. Neurosci. 9, 741 745.
10. Bucciantini M., Calloni G., Chiti F., Stefani M., Formigli L., Nosi D. Dobson C. M. (2004) Prefibrillar amyloid protein aggregates share common features of cytotoxicity. J. Biol. Chem. 279, 31374 31382.
11. Danzer K. M., Haasen D., Karow A. R., Moussaud S., Habeck M., Kretzschmar H., Giese A., Hengerer B. Kostka M. (2007) Different species of αsynuclein oligomers induce calcium influx and seeding. J. Neurosci. 27, 9220 9232.
12. Dauer W. Przedborski S. (2003) Parkinson's disease: mechanisms and models. Neuron 39, 889 909.
13. El-Agnaf O. M., Salem S. A., Paleologou K. E., Curran M. D., Gibson M. J., Court J. A., Schlossmacher M. G. Allsop D. (2006) Detection of oligomeric forms of αsynuclein protein in human plasma as a potential biomarker for Parkinson's disease. FASEB J. 20, 419 425.
14. Goedert M. (2001) αSynuclein and neurodegenerative diseases. Nat. Rev. Neurosci. 2, 492 501.
15. Haasen D., Wolff M., Valler M. J. Heilker R. (2006) Comparison of G-protein coupled receptor desensitization-related beta-arrestin redistribution using confocal and non-confocal imaging. Comb. Chem. High Throughput Screen. 9, 37 47.
16. Hardy J. Selkoe D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353 356.
17. Hoyer W., Antony T., Cherny D., Heim G., Jovin T. M. Subramaniam V. (2002) Dependence of αsynuclein aggregate morphology on solution conditions. J. Mol. Biol. 322, 383 393.
18. Jensen P. H., Islam K., Kenney J., Nielsen M. S., Power J. Gai W. P. (2000) Microtubule-associated protein 1B is a component of cortical Lewy bodies and binds alpha-synuclein filaments. J. Biol. Chem. 275, 21500 21507.
19. Kayed R., Head E., Thompson J. L., McIntire T. M., Milton S. C., Cotman C. W. Glabe C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486 489.
20. Krueger R., Kuhn W., Muller T. et al. (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 18, 106 108.
21. Kordower J. H., Chu Y., Hauser R. A., Freeman T. B. Olanow C. W. (2008) Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat. Med. 14, 504 506.
22. Lee H. J., Choi C. Lee S. J. (2002) Membrane-bound αsynuclein has a high aggregation propensity and the ability to seed the aggregation of the cytosolic form. J. Biol. Chem. 277, 671 678.
23. Lee H. J., Patel S. Lee S. J. (2005) Intravesicular localization and exocytosis of αsynuclein and its aggregates. J. Neurosci. 25, 6016 6024.
24. Lee H. J., Suk J. E., Bae E. J., Lee J. H. Paik S. R. (2008) Assembly-dependent endocytosis and clearance of extracellular αsynuclein. Int. J. Biochem. Cell Biol. 40, 1835 1849.
25. Li J. Y., Englund E., Holton J. L. et al. (2008) Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat. Med. 14, 501 503.
26. Liu J., Zhang J. P., Shi M., Quinn T., Bradner J., Beyer R., Chen S. Zhang J. (2009) Rab11a and HSP90 regulate recycling of extracellular αsynuclein. J. Neurosci. 29, 1480 1485.
27. Mendez I., Viñuela A., Astradsson A. et al. (2008) Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nat. Med. 14, 507 509.
28. Munishkina L. A., Phelan C., Uversky V. N. Fink A. L. (2003) Conformational behavior and aggregation of αsynuclein in organic solvents: modeling the effects of membranes. Biochemistry 42, 2720 2730.
29. Murray I. V. J. (2003) Role of αsynuclein carboxy-terminus on fibril formation in vitro. Biochemistry 42, 8530 8540.
30. Nuscher B., Kamp F., Mehnert T., Odoy S., Haass C., Kahle P. J. Beyer K. (2004) αSynuclein has a high affinity for packing defects in a bilayer membrane: a thermodynamics study. J. Biol. Chem. 279, 21966 21975.
31. Outeiro T. F., Putcha P., Tetzlaff J. E., Spoelgen R., Koker M., Carvalho F., Hyman B. T. McLean P. J. (2008) Formation of toxic oligomeric αsynuclein species in living cells. PLoS ONE 3, 1867.
32. Park J. Y. Lansbury P. T. Jr. (2003) Beta-synuclein inhibits formation of αsynuclein protofibrils: a possible therapeutic strategy against Parkinson's disease. Biochemistry 42, 3696 3700.
33. Polymeropoulos M. H., Lavedan C., Leroy E. et al. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276, 2045 2047.
34. Pountney D. L., Voelcker N. H. Gai W. P. (2005) Annular αsynuclein oligomers are potentially toxic agents in alpha-synucleinopathy. Hypothesis. Neurotox. Res. 7, 59 67.
35. Surguchov A. (2008) Molecular and cellular biology of synucleins. Int. Rev. Mol. Biol. 270, 225 317.
36. Tanaka M., Kim Y. M., Lee G., Junn E., Mouradian M. M. Iwatsubo T. (2004) Aggresomes formed by αsynuclein and synphilin-1 are cytoprotective. J. Biol. Chem. 279, 4625 4631.
37. Taylor J. P., Hardy J. Fischbeck K. H. (2002) Toxic proteins in neurodegenerative disease. Science 296, 1991 1995.
38. Unterberger U., Voigtlander T. Budka H. (2005) Pathogenesis of prion diseases. Acta Neuropathol. 109, 32 48.
39. Uversky V. N., Li J. Fink A. L. (2001) Metal-triggered structural transformations, aggregation, and fibrillation of human alpha-synuclein. A possible molecular NK between Parkinson's disease and heavy metal exposure. J. Biol. Chem. 276, 44284 44296.
40. Wolff M., Haasen D., Merk S. et al. (2006) Automated high content screening for phosphoinositide 3 kinase inhibition using an AKT 1 redistribution assay. Comb. Chem. High Throughput Screen. 9, 339 350.