Propagation of prions causing synucleinopathies in cultured cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 35, 2015, Pages E4949-E4958

  Woerman, Amanda L ^a   Stöhr, Jan ^a,b   Aoyagi, Atsushi ^a,c   Rampersaud, Ryan ^a   Krejciova, Zuzana ^a   Watts, Joel C ^a,b,h   Ohyama, Takao ^c   Patel, Smita ^a   Widjaja, Kartika ^a   Oehler, Abby ^b   Sanders, David W ^d   Diamond, Marc I ^d   Seeley, William W ^b   Middleton, Lefkos T ^e   Gentleman, Steve M ^e   Mordes, Daniel A ^f   Südhof, Thomas C ^g   Giles, Kurt ^a,b   Prusiner, Stanley B ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DAIICHI SANKYO CO   (Japan)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF TORONTO   (Canada)

Author keywords

Multiple system atrophy; Neurodegeneration; Parkinson's disease; Strains; synuclein

Indexed keywords

ALPHA SYNUCLEIN; PRION PROTEIN; TAU PROTEIN; YELLOW FLUORESCENT PROTEIN; PRION;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN HOMOGENATE; BRAIN LEVEL; CELL COUNT; CELL CULTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; FLUORESCENCE MICROSCOPY; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN CONTENT; PROTEIN PURIFICATION; SHY DRAGER SYNDROME; ANIMAL; DEGENERATIVE DISEASE; METABOLISM; PATHOLOGY; PRION;

ALPHA-SYNUCLEIN; ANIMALS; HEK293 CELLS; HUMANS; MICE; NEURODEGENERATIVE DISEASES; PRIONS;

EID: 84940969467     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1513426112     Document Type: Article

References (75)

1. Parkinson J (1817) An Essay on the Shaking Palsy (Sherwood, Neely, and Jones, London).
2. Forster E, Lewy FH (1912) Paralysis agitans. Pathologische Anatomie. Handbuch der Neurologie, ed Lewandowsky M (Springer, Berlin), pp 920-933.
3. Polymeropoulos MH, et al. (1997) Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 276(5321):2045-2047.
4. Singleton AB, et al. (2003) α-Synuclein locus triplication causes Parkinson's disease. Science 302(5646):841.
5. Chartier-Harlin MC, et al. (2004) Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet 364(9440):1167-1169.
6. Spillantini MG, et al. (1997) Alpha-synuclein in Lewy bodies. Nature 388(6645):839-840.
7. Baba M, et al. (1998) Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am J Pathol 152(4):879-884.
8. Spillantini MG, et al. (1998) Filamentous α-synuclein inclusions link multiple system atrophy with Parkinson's disease and dementia with Lewy bodies. Neurosci Lett 251(3):205-208.
9. Nalls MA, et al.; International Parkinson's Disease Genomics Consortium (IPDGC); Parkinson's Study Group (PSG) Parkinson's Research: The Organized GENetics Initiative (PROGENI); 23andMe; GenePD; NeuroGenetics Research Consortium (NGRC); Hussman Institute of Human Genomics (HIHG); Ashkenazi Jewish Dataset Investigator; Cohorts for Health and Aging Research in Genetic Epidemiology (CHARGE); North American Brain Expression Consortium (NABEC); United Kingdom Brain Expression Consortium (UKBEC); Greek Parkinson's Disease Consortium; Alzheimer Genetic Analysis Group (2014) Large-scale meta-analysis of genome-wide association data identifies six new risk loci for Parkinson's disease.Nat Genet 46(9):989-993.
10. Wakabayashi K, Yoshimoto M, Tsuji S, Takahashi H (1998) α-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett 249(2-3):180-182.
11. Tu PH, et al. (1998) Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble α-synuclein. Ann Neurol 44(3):415-422.
12. Papp MI, Kahn JE, Lantos PL (1989) Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J Neurol Sci 94(1-3):79-100.
13. Fernagut P-O, Ghorayeb I, Diguet E, Tison F (2005) In vivo models of multiple system atrophy. Mov Disord 20(Suppl 12):S57-S63.
14. Kordower JH, Chu Y, Hauser RA, Freeman TB, Olanow CW (2008) Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med 14(5):504-506.
15. Li JY, et al. (2008) Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat Med 14(5):501-503.
16. Olanow CW, Prusiner SB (2009) Is Parkinson's disease a prion disorder? Proc Natl Acad Sci USA 106(31):12571-12572.
17. Aguzzi A, Rajendran L (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64(6):783-790.
18. Braak H, et al. (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 24(2):197-211.
19. Giasson BI, et al. (2002) Neuronal α-synucleinopathy with severe movement disorder in mice expressing A53T human α-synuclein. Neuron 34(4):521-533.
20. Mougenot A-L, et al. (2012) Prion-like acceleration of a synucleinopathy in a transgenic mouse model. Neurobiol Aging 33(9):2225-2228.
21. Luk KC, et al. (2012) Intracerebral inoculation of pathological α-synuclein initiates a rapidly progressive neurodegenerative α-synucleinopathy in mice. J Exp Med 209(5):975-986.
22. Watts JC, et al. (2013) Transmission of multiple system atrophy prions to transgenic mice. Proc Natl Acad Sci USA 110(48):19555-19560.
23. Prusiner SB, et al. Evidence for α-synuclein prions causing multiple system atrophy in humans with parkinsonism. Proc Natl Acad Sci USA, 10.1073/pnas.1514475112.
24. Recasens A, et al. (2014) Lewy body extracts from Parkinson disease brains trigger α-synuclein pathology and neurodegeneration in mice and monkeys. Ann Neurol 75(3):351-362.
25. Masuda-Suzukake M, et al. (2013) Prion-like spreading of pathological α-synuclein in brain. Brain 136(Pt 4):1128-1138.
26. Kfoury N, Holmes BB, Jiang H, Holtzman DM, Diamond MI (2012) Trans-cellular propagation of Tau aggregation by fibrillar species. J Biol Chem 287(23):19440-19451.
27. Sanders DW, et al. (2014) Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron 82(6):1271-1288.
28. Burré J, Sharma M, Südhof TC (2012) Systematic mutagenesis of α-synuclein reveals distinct sequence requirements for physiological and pathological activities. J Neurosci 32(43):15227-15242.
29. Holmes BB, et al. (2014) Proteopathic tau seeding predicts tauopathy in vivo. Proc Natl Acad Sci USA 111(41):E4376-E4385.
30. Luk KC, et al. (2009) Exogenous alpha-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci USA 106(47):20051-20056.
31. Sc) molecules with different conformations. Nat Med 4(10):1157-1165.
32. Levine DJ, et al. (2015) Mechanism of scrapie prion precipitation with phosphotungstate anions. ACS Chem Biol 10(5):1269-1277.
33. Bruce ME, McBride PA, Farquhar CF (1989) Precise targeting of the pathology of the sialoglycoprotein, PrP, and vacuolar degeneration in mouse scrapie. Neurosci Lett 102(1):1-6.
34. Hecker R, et al. (1992) Replication of distinct scrapie prion isolates is region specific in brains of transgenic mice and hamsters. Genes Dev 6(7):1213-1228.
35. Wenning GK, Braune S (2001) Multiple system atrophy: Pathophysiology and management. CNS Drugs 15(11):839-852.
36. Watanabe H, et al. (2002) Progression and prognosis in multiple system atrophy: An analysis of 230 Japanese patients. Brain 125(Pt 5):1070-1083.
37. Race RE, Fadness LH, Chesebro B (1987) Characterization of scrapie infection in mouse neuroblastoma cells. J Gen Virol 68(Pt 5):1391-1399.
38. Butler DA, et al. (1988) Scrapie-infected murine neuroblastoma cells produce protease-resistant prion proteins. J Virol 62(5):1558-1564.
39. Mahal SP, et al. (2007) Prion strain discrimination in cell culture: The cell panel assay. Proc Natl Acad Sci USA 104(52):20908-20913.
40. Ghaemmaghami S, et al. (2007) Cell division modulates prion accumulation in cultured cells. Proc Natl Acad Sci USA 104(46):17971-17976.
41. Bian J, et al. (2006) GFP-tagged PrP supports compromised prion replication in transgenic mice. Biochem Biophys Res Commun 340(3):894-900.
42. Barmada SJ, Harris DA (2005) Visualization of prion infection in transgenic mice expressing green fluorescent protein-tagged prion protein. J Neurosci 25(24):5824-5832.
43. Frost B, Jacks RL, Diamond MI (2009) Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 284(19):12845-12852.
44. Safar JG, et al. (2005) Diagnosis of human prion disease. Proc Natl Acad Sci USA 102(9):3501-3506.
45. Luk KC, et al. (2012) Pathological α-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 338(6109):949-953.
46. Guo JL, et al. (2013) Distinct α-synuclein strains differentially promote tau inclusions in neurons. Cell 154(1):103-117.
47. Bousset L, et al. (2013) Structural and functional characterization of two alpha-synuclein strains. Nat Commun 4:2575.
48. Peelaerts W, et al. (2015) α-Synuclein strains cause distinct synucleinopathies after local and systemic administration. Nature 522(7556):340-344.
49. Giasson BI, et al. (2000) Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290(5493):985-989.
50. Shimura H, et al. (2001) Ubiquitination of a new form of α-synuclein by parkin from human brain: Implications for Parkinson's disease. Science 293(5528):263-269.
51. Fujiwara H, et al. (2002) alpha-Synuclein is phosphorylated in synucleinopathy lesions. Nat Cell Biol 4(2):160-164.
52. Krumova P, et al. (2011) Sumoylation inhibits α-synuclein aggregation and toxicity. J Cell Biol 194(1):49-60.
53. Hardy J, Cai H, Cookson MR, Gwinn-Hardy K, Singleton A (2006) Genetics of Parkinson's disease and parkinsonism. Ann Neurol 60(4):389-398.
54. Pasanen P, et al. (2014) Novel α-synuclein mutation A53E associated with atypical multiple system atrophy and Parkinson's disease-type pathology. Neurobiol Aging 35(9):2180.e1-2180.e5.
55. Kiely AP, et al. (2013) α-Synucleinopathy associated with G51D SNCA mutation: A link between Parkinson's disease and multiple system atrophy? Acta Neuropathol 125(5):753-769.
56. Lesage S, et al.; French Parkinson's Disease Genetics Study Group (2013) G51D α-synuclein mutation causes a novel parkinsonian-pyramidal syndrome. Ann Neurol 73(4):459-471.
57. nd Ed.
58. Prusiner SB (2014) Madness and Memory (Yale Univ Press, New Haven, CT).
59. Walker LC, Jucker M (2015) Neurodegenerative diseases: Expanding the prion concept. Annu Rev Neurosci 38:87-103.
60. Arriagada PV, Growdon JH, Hedley-Whyte ET, Hyman BT (1992) Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42(3 Pt 1):631-639.
61. Cohen RM, et al. (2013) A transgenic Alzheimer rat with plaques, tau pathology, behavioral impairment, oligomeric aβ, and frank neuronal loss. J Neurosci 33(15):6245-6256.
62. Choi SH, et al. (2014) A three-dimensional human neural cell culture model of Alzheimer's disease. Nature 515(7526):274-278.
63. Murray ME, et al. (2015) Clinicopathologic and11 C-Pittsburgh compound B implications of Thal amyloid phase across the Alzheimer's disease spectrum. Brain 138(Pt 5):1370-1381.
64. Stöhr J, et al. (2014) Distinct synthetic Aβ prion strains producing different amyloid deposits in bigenic mice. Proc Natl Acad Sci USA 111(28):10329-10334.
65. Watts JC, et al. (2014) Serial propagation of distinct strains of Aβ prions from Alzheimer's disease patients. Proc Natl Acad Sci USA 111(28):10323-10328.
66. th Ed.
67. Mackenzie IR, et al. (2010) Nomenclature and nosology for neuropathologic subtypes of frontotemporal lobar degeneration: An update. Acta Neuropathol 119(1):1-4.
68. Kim E-J, et al. (2012) Selective frontoinsular von Economo neuron and fork cell loss in early behavioral variant frontotemporal dementia. Cereb Cortex 22(2):251-259.
69. Gilman S, et al. (2008) Second consensus statement on the diagnosis of multiple system atrophy. Neurology 71(9):670-676.
70. Alafuzoff I, et al. (2009) Staging/typing of Lewy body related alpha-synuclein pathology: A study of the BrainNet Europe Consortium. Acta Neuropathol 117(6):635-652.
71. Alafuzoff I, et al. (2008) Staging of neurofibrillary pathology in Alzheimer's disease: A study of the BrainNet Europe Consortium. Brain Pathol 18(4):484-496.
72. Ghoshal N, et al. (2002) Tau conformational changes correspond to impairments of episodic memory in mild cognitive impairment and Alzheimer's disease. Exp Neurol 177(2):475-493.
73. Barghorn S, Biernat J, Mandelkow E (2005) Purification of recombinant tau protein and preparation of Alzheimer-paired helical filaments in vitro. Methods Mol Biol 299:35-51.
74. Stöhr J, et al. (2012) Purified and synthetic Alzheimer's amyloid beta (Aβ) prions. Proc Natl Acad Sci USA 109(27):11025-11030.
75. Chandler RL, Fisher J (1963) Experimental transmission of scrapie to rats. Lancet 2(7318):1165.