The propagation of prion-like protein inclusions in neurodegenerative diseases

Trends in Neurosciences

Volumn 33, Issue 7, 2010, Pages 317-325

  Goedert, Michel ^a   Clavaguera, Florence ^b   Tolnay, Markus ^b  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; COPPER ZINC SUPEROXIDE DISMUTASE; HUNTINGTIN; PRION PROTEIN; TAU PROTEIN; PRION;

ALZHEIMER DISEASE; DEGENERATIVE DISEASE; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; REVIEW; ANIMAL; CELL INCLUSION; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PRION; PRION DISEASE;

ANIMALS; HUMANS; INCLUSION BODIES; NEURODEGENERATIVE DISEASES; PRION DISEASES; PRIONS; PROTEIN FOLDING; TAU PROTEINS;

EID: 77954385676     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tins.2010.04.003     Document Type: Review

References (109)

1. Prusiner S.B. Novel proteinaceous infectious particles cause scrapie. Science 1982, 216:136-144.
2. Hsiao K., et al. Linkage of a prion protein missense variant to Gerstmann-Sträussler syndrome. Nature 1989, 388:342-345.
3. Collinge J., Clarke A.R. A general model of prion strains and their pathogenicity. Science 2007, 318:930-936.
4. Wickner R.B., et al. Prions of fungi: inherited structures and biological roles. Nat. Rev. Microbiol. 2007, 5:611-618.
5. Colby D.W., et al. Design and construction of diverse mammalian prion strains. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20417-20422.
6. Goedert M., Spillantini M.G. A century of Alzheimer's disease. Science 2006, 314:777-781.
7. Goate A., et al. Segregation of missense mutation in the amyloid precursor gene with familial Alzheimer's disease. Nature 1991, 349:704-706.
8. Murrell J., et al. A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease. Science 1991, 254:97-99.
9. Polymeropoulos M.H., et al. Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 1997, 276:2045-2047.
10. Poorkaj P., et al. Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann. Neurol. 1998, 43:815-825.
11. Hutton M., et al. Association of missense and 5'-splice-site mutations in tau with inherited dementia FTDP-17. Nature 1998, 393:702-705.
12. Spillantini M.G., et al. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:7737-7741.
13. Rosen D.R., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
14. Sreedharan J., et al. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319:1668-1672.
15. Kwiatkowski T.J., et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
16. Vance C., et al. Mutations in FUS, an RNA-processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
17. The Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72, 971-983.
18. Braak H., Braak E. Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
19. Braak H., et al. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 2003, 24:197-211.
20. Wisniewski H.M., et al. Infectious etiology of neuritic (senile) plaques in mice. Science 1975, 190:1108-1110.
21. Van den Bosch Aguilar P., et al. Transplantation of human cortex with Alzheimer's disease into rat occipital cortex: a model for the study of Alzheimer disease. Experientia 1984, 40:402-403.
22. Baker H.F., et al. Induction of β(A4)-amyloid in primates by injection of Alzheimer's disease brain homogenate. Mol. Neurobiol. 1994, 8:25-39.
23. Brown P., et al. Human spongiform encephalopathy: The National Institutes of Health series of 300 cases of experimentally transmitted disease. Ann. Neurol. 1994, 35:513-529.
24. Kane M.D., et al. Evidence for seeding of β-amyloid by intracerebral infusion of Alzheimer brain extracts in β-amyloid precursor protein-transgenic mice. J. Neurosci. 2000, 20:3606-3611.
25. Yang W., et al. Aggregated polyglutamine peptides delivered to nuclei are toxic to mammalian cells. Hum. Mol. Genet. 2001, 11:2905-2917.
26. Urushitani M., et al. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat. Neurosci. 2006, 9:108-118.
27. Meyer-Luehmann M., et al. Exogenous induction of cerebral β-amyloidogenesis is governed by agent and host. Science 2006, 313:1781-1784.
28. Ren P.-H., et al. Cytoplasmic penetration and persistent infection of mammalian cells by polyglutamine aggregates. Nat. Cell Biol. 2009, 11:219-225.
29. Clavaguera F., et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat. Cell Biol. 2009, 11:909-913.
30. Frost B., et al. Propagation of tau misfolding from the outside to the inside of a cell. J. Biol. Chem. 2009, 284:12845-12852.
31. Eisele Y.S., et al. Induction of cerebral β-amyloidogenesis: Intracerebral versus systemic Aβ inoculation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:12926-12931.
32. Desplats P., et al. Inclusion formation and neuronal cell death through neuron-to-neuron transmission of α-synuclein. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13010-13015.
33. Luk K.C., et al. Exogenous α-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20051-20056.
34. Hu X., et al. Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-β peptide. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20324-20329.
35. Aguzzi A. Beyond the prion principle. Nature 2009, 459:924-925.
36. Aguzzi A., Rajendran L. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 2009, 64:783-790.
37. Zhao W., et al. Extracellular mutant SOD1 induces microglial-mediated motoneuron injury. Glia 2010, 58:231-243.
38. Frost B., Diamond M.I. Prion-like mechanisms in neurodegenerative diseases. Nat. Rev. Neurosci. 2010, 11:155-159.
39. Crowther R.A., Goedert M. Abnormal tau-containing filaments in neurodegenerative diseases. J. Struct. Biol. 2000, 130:271-279.
40. Conrad C., et al. Genetic evidence for the involvement of tau in progressive supranuclear palsy. Ann. Neurol. 1997, 41:277-281.
41. Baker M., et al. Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Hum. Mol. Genet. 1999, 8:711-715.
42. Di Maria E., et al. Corticobasal degeneration shares a common genetic background with progressive supranuclear palsy. Ann. Neurol. 2000, 47:374-377.
43. Stefansson H., et al. A common inversion under selection in Europeans. Nat. Genet. 2005, 37:129-137.
44. Koolen D.A., et al. A new chromosome 17q21.31 microdeletion syndrome associated with a common inversion polymorphism. Nat. Genet. 2006, 38:999-1001.
45. Shaw-Smith C., et al. Microdeletion encompassing MAPT at chromosome 17q21.3 is associated with developmental delay and learning disability. Nat. Genet. 2006, 38:1032-1037.
46. Sharp A.J., et al. Discovery of previously unidentified genomic disorders from the duplication architecture of the human genome. Nat. Genet. 2006, 38:1038-1042.
47. Goedert M., et al. Multiple isoforms of human microtubule-associated protein tau: Sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989, 3:519-526.
48. Kovacs G.G., et al. White matter tauopathy with globular glial inclusions: A distinct sporadic frontotemporal lobar degeneration. J. Neuropathol. Exp. Neurol. 2008, 67:963-975.
49. Saito Y., et al. Staging of argyrophilic grains: An age-associated tauopathy. J. Neuropathol. Exp. Neurol. 2004, 63:911-918.
50. Tolnay M., Clavaguera F. Argyrophilic grain disease: a late-onset dementia with distinctive features among tauopathies. Neuropathology 2004, 24:269-283.
51. Allen B., et al. Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J. Neurosci. 2002, 22:9340-9351.
52. Frank S., et al. Tauopathy models and human neuropathology: similarities and differences. Acta Neuropathol. 2008, 115:39-53.
53. Frost B., et al. Conformational diversity of wild-type tau fibrils specified by templated conformation change. J. Biol. Chem. 2009, 284:3546-3551.
54. Magalhaes A.C., et al. Uptake and neuritic transport of scrapie prion protein coincident with infection of neuronal cells. J. Neurosci. 2005, 25:5207-5216.
55. Krammer C., et al. The yeast Sup35NM domain propagates as a prion in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:462-467.
56. Russo C., et al. Presenilin-1 mutations in Alzheimer's disease. Nature 2000, 405:531-532.
57. Petkova A.T., et al. Self-propagating, molecular-level polymorphism in Alzheimer's β-amyloid fibrils. Science 2005, 307:262-265.
58. Bolmont T., et al. Induction of tau pathology by intracerebral infusion of amyloid-β-containing brain extract and by amyloid-β deposition in APP×Tau transgenic mice. Am. J. Pathol. 2007, 171:2012-2020.
59. Lewis J., et al. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 2001, 293:1487-1491.
60. Götz J., et al. Formation of neurofibrillary tangles in P301L tau transgenic mice induced by Aβ42 fibrils. Science 2001, 293:1491-1495.
61. Boutajangout A., et al. Characterization of cytoskeletal abnormalities in mice transgenic for wild-type human tau and familial Alzheimer's disease mutants of APP and presenilin-1. Neurobiol. Dis. 2004, 15:47-60.
62. Spillantini M.G., et al. α-Synuclein in Lewy bodies. Nature 1997, 388:839-840.
63. Spillantini M.G., et al. α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6469-6473.
64. Papp M.I., et al. Glial cytoplasmic inclusions in the CNS of patients with multiple system atrophy (striatonigral degeneration, olivopontocerebellar atrophy and Shy-Drager syndrome). J. Neurol. Sci. 1989, 94:79-100.
65. Spillantini M.G., et al. Filamentous α-synuclein inclusions link multiple system atrophy with Parkinson's disease and dementia with Lewy bodies. Neurosci. Lett. 1998, 251:205-208.
66. Yonetani M., et al. Conversion of wild-type α-synuclein into mutant-type fibrils and its propagation in the presence of A30P mutant. J. Biol. Chem. 2009, 284:7940-7950.
67. Singleton A.B., et al. α-Synuclein locus triplication causes Parkinson's disease. Science 2003, 302:841.
68. Chiba-Falek O., Nussbaum R.L. Effect of allelic variation at the NACP-Rep1 repeat upstream of the α-synuclein gene (SNCA) on transcription in a cell culture luciferase reporter system. Hum. Mol. Genet. 2001, 10:3101-3109.
69. Scholz S.W., et al. SNCA variants are associated with increased risk of multiple system atrophy. Ann. Neurol. 2009, 65:610-614.
70. Satake W., et al. Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat. Genet. 2009, 41:1303-1307.
71. Simón-Sánchez J., et al. Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat. Genet. 2009, 41:1308-1312.
72. Pastor P., et al. Significant association between the tau gene A0/A0 genotype and Parkinson's disease. Ann. Neurol. 2000, 47:242-245.
73. Ueda K., et al. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:11282-11286.
74. Jakes R., et al. Identification of two distinct synucleins from human brain. FEBS Lett. 1994, 345:27-32.
75. Davidson W.S., et al. Stabilization of α-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 1998, 273:9443-9449.
76. Miake H., et al. Biochemical characterization of the core structure of α-synuclein filaments. J. Biol. Chem. 2002, 277:19213-19219.
77. Chandra S., et al. α-Synuclein cooperates with CSPα in preventing neurodegeneration. Cell 2005, 123:383-396.
78. Dickson D.W., et al. Evidence that incidental Lewy body disease is pre-symptomatic Parkinson's disease. Acta Neuropathol. 2008, 115:437-444.
79. Fujishiro H., et al. Glial cytoplasmic inclusions in neurologically normal elderly: prodromal multiple system atrophy?. Acta Neuropathol. 2008, 116:269-275.
80. Lees A.J., et al. Parkinson's disease. Lancet 2009, 373:2055-2066.
81. Braak H., et al. Gastric α-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci. Lett. 2006, 396:67-72.
82. Bloch A., et al. α-Synuclein pathology of the spinal and peripheral autonomic nervous system in neurologically unimpaired elderly subjects. Neuropathol. Appl. Neurobiol. 2006, 12:284-295.
83. Braak H., et al. Idiopathic Parkinson's disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J. Neural Transm. 2003, 110:517-536.
84. Aguzzi A., Calella A.M. Prions: protein aggregation and infectious diseases. Physiol. Rev. 2009, 89:1105-1152.
85. Pan-Montojo F., et al. Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS ONE 2010, 5:e8762.
86. Li J.Y., et al. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat. Med. 2008, 14:501-503.
87. Kordower J.H., et al. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat. Med. 2008, 14:504-506.
88. Kordower J.H., et al. Transplanted dopaminergic neurons develop PD pathologic changes: a second case report. Mov. Disord. 2008, 23:2303-2306.
89. Li, J.Y. et al. (2010) Characterization of Lewy body pathology in 12- and 16-year-old intrastriatal mesencephalic grafts surviving in a patient with Parkinson's disease. Mov. Disord. doi:10.1002/mds.23012.
90. Greffard S., et al. A stable proportion of Lewy body-bearing neurons in the substantia nigra suggests a model in which the Lewy body causes neuronal death. Neurobiol. Aging 2010, 31:99-103.
91. Lee H.-J., et al. Intravesicular localization and exocytosis of α-synuclein and its aggregates. J. Neurosci. 2005, 25:6016-6024.
92. Ilieva H., et al. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J. Cell Biol. 2009, 187:761-772.
93. Gros-Louis F., et al. Chromogranin B P413L variant as risk factor and modifier of disease onset for amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:21777-21782.
94. Thurston T.L.M., et al. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nat. Immunol. 2009, 10:1215-1221.
95. Heiseke A., et al. Autophagy, prion infection and their mutual interactions. Curr. Issues Mol. Biol. 2010, 12:87-98.
96. Renna M., et al. Chemical inducers of autophagy that enhance the clearance of mutant proteins in neurodegenerative diseases. J. Biol. Chem. 2010, 285:11061-11067.
97. Fevrier B., et al. Cells release prions in association with exosomes. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9683-9688.
98. Gousset K., et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 2009, 11:328-336.
99. Kanu N., et al. Transfer of scrapie prion infectivity by cell contact in culture. Curr. Biol. 2002, 12:523-530.
100. Simons M., Raposo G. Exosomes - vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 2009, 21:575-581.
101. Fader C.M., et al. Induction of autophagy promotes fusion of multivesicular bodies with autophagic vacuoles in K562 cells. Traffic 2008, 9:230-250.
102. Rajendran L., et al. Alzheimer's disease β-amyloid peptides are released in association with exosomes. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:11172-11177.
103. Davis D.M., Sowinski S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nat. Rev. Mol. Cell Biol. 2008, 9:431-436.
104. Sandvig K., van Deurs B. Entry of ricin and Shiga toxin into cells: molecular mechanisms and medical perspectives. EMBO J. 2000, 19:5943-5950.
105. Tsai B. Penetration of nonenveloped viruses into the cytoplasm. Annu. Rev. Cell Dev. Biol. 2007, 23:23-43.
106. Masliah E., et al. Effects of α-synuclein immunization in a mouse model of Parkinson's disease. Neuron 2005, 46:857-868.
107. Urushitani M., et al. Therapeutic effects of immunization with mutant superoxide dismutase in mice models of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2495-2500.
108. Asuni A.A., et al. Immunotherapy targeting pathological tau conformers in a tangle mouse model reduces brain pathology with associated functional improvements. J. Neurosci. 2007, 27:9115-9129.
109. Bugiani O., et al. Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in Tau. J. Neuropathol. Exp. Neurol. 1999, 58:667-677.