Protein aggregate spreading in neurodegenerative diseases: Problems and perspectives

Neuroscience Research

Volumn 70, Issue 4, 2011, Pages 339-348

  Lee, Seung Jae ^a,b   Lim, Hee Sun ^a,b   Masliah, Eliezer ^c   Lee, He Jin ^a,b  

^a Konkuk University   (South Korea)

^b Konkuk University   (South Korea)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; Huntington's disease; Parkinson's disease; Prion; Protein aggregation

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; POLYGLUTAMINE; PRION PROTEIN;

ALZHEIMER DISEASE; ANIMAL MODEL; CELL AGGREGATION; DEGENERATIVE DISEASE; DIAGNOSTIC PROCEDURE; ENDOSOME; EXPERIMENTAL MODEL; EXTRACELLULAR SPACE; HUMAN; HUNTINGTON CHOREA; IMMUNIZATION; IN VIVO STUDY; LEWY BODY; LYSOSOME; NEUROFIBRILLARY TANGLE; NEUROPIL THREAD; NEUROTOXICITY; NEUROTRANSMISSION; NONHUMAN; PARKINSON DISEASE; PATHOLOGY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN HOMEOSTASIS; PROTEIN POLYMERIZATION; REVIEW; SYNAPTIC TRANSMISSION; TAUOPATHY;

ANIMALS; HUMANS; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; PROTEIN FOLDING; PROTEOSTASIS DEFICIENCIES;

EID: 79959923467     PISSN: 01680102     EISSN: 18728111     Source Type: Journal    
DOI: 10.1016/j.neures.2011.05.008     Document Type: Review

References (104)

1. Aguzzi A., Baumann F., Bremer J. The prion's elusive reason for being. Annu. Rev. Neurosci. 2008, 31:439-477.
2. Alvarez-Erviti L., Seow Y., Schapira A.H., Gardiner C., Sargent I.L., Wood M.J., Cooper J.M. Lysosomal dysfunction increases exosome-mediated alpha-synuclein release and transmission. Neurobiol. Dis. 2011.
3. Arrasate M., Mitra S., Schweitzer E.S., Segal M.R., Finkbeiner S. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 2004, 431:805-810.
4. Bahr B.A., Bendiske J. The neuropathogenic contributions of lysosomal dysfunction. J. Neurochem. 2002, 83:481-489.
5. Balch W.E., Morimoto R.I., Dillin A., Kelly J.W. Adapting proteostasis for disease intervention. Science 2008, 319:916-919.
6. Bence N.F., Sampat R.M., Kopito R.R. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001, 292:1552-1555.
7. Borchelt D.R., Koliatsos V.E., Guarnieri M., Pardo C.A., Sisodia S.S., Price D.L. Rapid anterograde axonal transport of the cellular prion glycoprotein in the peripheral and central nervous systems. J. Biol. Chem. 1994, 269:14711-14714.
8. Braak H., Alafuzoff I., Arzberger T., Kretzschmar H., Del Tredici K. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 2006, 112:389-404.
9. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
10. Braak H., Del Tredici K. Alzheimer's disease: intraneuronal alterations precede insoluble amyloid-beta formation. Neurobiol. Aging 2004, 25:713-718. discussion 743-746.
11. Braak H., Del Tredici K., Rub U., de Vos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 2003, 24:197-211.
12. Brody D.L., Holtzman D.M. Active and passive immunotherapy for neurodegenerative disorders. Annu. Rev. Neurosci. 2008, 31:175-193.
13. Burke R.E., Dauer W.T., Vonsattel J.P. A critical evaluation of the Braak staging scheme for Parkinson's disease. Ann. Neurol. 2008, 64:485-491.
14. Busch C., Bohl J., Ohm T.G. Spatial, temporal and numeric analysis of Alzheimer changes in the nucleus coeruleus. Neurobiol. Aging 1997, 18:401-406.
15. Caughey B., Baron G.S., Chesebro B., Jeffrey M. Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions. Annu. Rev. Biochem 2009, 78:177-204.
16. Cirrito J.R., Kang J.E., Lee J., Stewart F.R., Verges D.K., Silverio L.M., Bu G., Mennerick S., Holtzman D.M. Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo. Neuron 2008, 58:42-51.
17. Cirrito J.R., Yamada K.A., Finn M.B., Sloviter R.S., Bales K.R., May P.C., Schoepp D.D., Paul S.M., Mennerick S., Holtzman D.M. Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 2005, 48:913-922.
18. Clavaguera F., Bolmont T., Crowther R.A., Abramowski D., Frank S., Probst A., Fraser G., Stalder A.K., Beibel M., Staufenbiel M., et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat. Cell Biol. 2009, 11:909-913.
19. Crouch P.J., Harding S.M., White A.R., Camakaris J., Bush A.I., Masters C.L. Mechanisms of A beta mediated neurodegeneration in Alzheimer's disease. Int. J. Biochem. Cell Biol. 2008, 40:181-198.
20. Danzer K.M., Krebs S.K., Wolff M., Birk G., Hengerer B. Seeding induced by alpha-synuclein oligomers provides evidence for spreading of alpha-synuclein pathology. J. Neurochem. 2009, 111:192-203.
21. Danzer K.M., Ruf W.P., Putcha P., Joyner D., Hashimoto T., Glabe C., Hyman B.T., McLean P.J. Heat-shock protein 70 modulates toxic extracellular alpha-synuclein oligomers and rescues trans-synaptic toxicity. FASEB J. 2010, 25:326-336.
22. Desplats P., Lee H.J., Bae E.J., Patrick C., Rockenstein E., Crews L., Spencer B., Masliah E., Lee S.J. Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13010-13015.
23. DiFiglia M., Sapp E., Chase K.O., Davies S.W., Bates G.P., Vonsattel J.P., Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997, 277:1990-1993.
24. Eisele Y.S., Bolmont T., Heikenwalder M., Langer F., Jacobson L.H., Yan Z.X., Roth K., Aguzzi A., Staufenbiel M., Walker L.C., Jucker M. Induction of cerebral beta-amyloidosis: intracerebral versus systemic Abeta inoculation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:12926-12931.
25. Eisele Y.S., Obermuller U., Heilbronner G., Baumann F., Kaeser S.A., Wolburg H., Walker L.C., Staufenbiel M., Heikenwalder M., Jucker M. Peripherally applied Abeta-containing inoculates induce cerebral beta-amyloidosis. Science 2010, 330:980-982.
26. El-Agnaf O.M., Salem S.A., Paleologou K.E., Cooper L.J., Fullwood N.J., Gibson M.J., Curran M.D., Court J.A., Mann D.M., Ikeda S., et al. Alpha-synuclein implicated in Parkinson's disease is present in extracellular biological fluids, including human plasma. FASEB J. 2003, 17:1945-1947.
27. El-Agnaf O.M., Salem S.A., Paleologou K.E., Curran M.D., Gibson M.J., Court J.A., Schlossmacher M.G., Allsop D. Detection of oligomeric forms of alpha-synuclein protein in human plasma as a potential biomarker for Parkinson's disease. FASEB J. 2006, 20:419-425.
28. Emmanouilidou E., Melachroinou K., Roumeliotis T., Garbis S.D., Ntzouni M., Margaritis L.H., Stefanis L., Vekrellis K. Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J. Neurosci. 2010, 30:6838-6851.
29. Federoff H.J. Development of vaccination approaches for the treatment of neurological diseases. J. Comp. Neurol. 2009, 515:4-14.
30. 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, 101:9683-9688.
31. Fortin D.L., Nemani V.M., Voglmaier S.M., Anthony M.D., Ryan T.A., Edwards R.H. Neural activity controls the synaptic accumulation of {alpha}-synuclein. J. Neurosci. 2005, 25:10913-10921.
32. Frost B., Jacks R.L., Diamond M.I. Propagation of tau misfolding from the outside to the inside of a cell. J. Biol. Chem. 2009, 284:12845-12852.
33. Frost B., Ollesch J., Wille H., Diamond M.I. Conformational diversity of wild-type Tau fibrils specified by templated conformation change. J. Biol. Chem. 2009, 284:3546-3551.
34. Futerman A.H., van Meer G. The cell biology of lysosomal storage disorders. Nat. Rev. Mol. Cell Biol. 2004, 5:554-565.
35. Gao H.M., Kotzbauer P.T., Uryu K., Leight S., Trojanowski J.Q., Lee V.M. Neuroinflammation and oxidation/nitration of alpha-synuclein linked to dopaminergic neurodegeneration. J. Neurosci. 2008, 28:7687-7698.
36. Gidalevitz T., Ben-Zvi A., Ho K.H., Brignull H.R., Morimoto R.I. Progressive disruption of cellular protein folding in models of polyglutamine diseases. Science 2006, 311:1471-1474.
37. Glabe C.G. Structural classification of toxic amyloid oligomers. J. Biol. Chem. 2008, 283:29639-29643.
38. Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat. Rev. Neurosci. 2001, 2:492-501.
39. Gomez-Tortosa E., Newell K., Irizarry M.C., Albert M., Growdon J.H., Hyman B.T. Clinical and quantitative pathologic correlates of dementia with Lewy bodies. Neurology 1999, 53:1284-1291.
40. Gousset K., Schiff E., Langevin C., Marijanovic Z., Caputo A., Browman D.T., Chenouard N., de Chaumont F., Martino A., Enninga J., et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 2009, 11:328-336.
41. Guo J.L., Lee V.M. Seeding of normal tau by pathological tau conformers drives pathogenesis of Alzheimer-like tangles. J. Biol. Chem. 2011, 286:15317-15331.
42. Gutekunst C.A., Li S.H., Yi H., Mulroy J.S., Kuemmerle S., Jones R., Rye D., Ferrante R.J., Hersch S.M., Li X.J. Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J. Neurosci. 1999, 19:2522-2534.
43. Halliday G.M., Stevens C.H. Glia: initiators and progressors of pathology in Parkinson's disease. Mov. Disord. 2011, 26:6-17.
44. Hansen C., Angot E., Bergstrom A.L., Steiner J.A., Pieri L., Paul G., Outeiro T.F., Melki R., Kallunki P., Fog K., et al. alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J. Clin. Invest. 2011, 121:715-725.
45. Hardy J. A hundred years of Alzheimer's disease research. Neuron 2006, 52:3-13.
46. Holmes C., Boche D., Wilkinson D., Yadegarfar G., Hopkins V., Bayer A., Jones R.W., Bullock R., Love S., Neal J.W., et al. Long-term effects of Abeta42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial. Lancet 2008, 372:216-223.
47. Hu X., Crick S.L., Bu G., Frieden C., Pappu R.V., Lee J.M. Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc. Natl. Acad. Sci. U. S. A. 2009.
48. Jang A., Lee H.J., Suk J.E., Jung J.W., Kim K.P., Lee S.J. Non-classical exocytosis of alpha-synuclein is sensitive to folding states and promoted under stress conditions. J. Neurochem. 2010, 113:1263-1274.
49. Jarrett J.T., Lansbury P.T. Seeding " one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie?. Cell 1993, 73:1055-1058.
50. Jayasinghe S.A., Langen R. Membrane interaction of islet amyloid polypeptide. Biochim. Biophys. Acta 2007, 1768:2002-2009.
51. Jellinger K.A. A critical reappraisal of current staging of Lewy-related pathology in human brain. Acta Neuropathol. 2008, 116:1-16.
52. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., Malinow R. APP processing and synaptic function. Neuron 2003, 37:925-937.
53. Kane M.D., Lipinski W.J., Callahan M.J., Bian F., Durham R.A., Schwarz R.D., Roher A.E., Walker L.C. Evidence for seeding of beta-amyloid by intracerebral infusion of Alzheimer brain extracts in beta-amyloid precursor protein-transgenic mice. J. Neurosci. 2000, 20:3606-3611.
54. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003, 300:486-489.
55. Koenigsknecht J., Landreth G. Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J. Neurosci. 2004, 24:9838-9846.
56. Koistinaho M., Lin S., Wu X., Esterman M., Koger D., Hanson J., Higgs R., Liu F., Malkani S., Bales K.R., Paul S.M. Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-beta peptides. Nat. Med. 2004, 10:719-726.
57. Kordower J.H., Chu Y., Hauser R.A., Freeman T.B., Olanow C.W. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat. Med. 2008, 14:504-506.
58. Kordower J.H., Chu Y., Hauser R.A., Olanow C.W., Freeman T.B. Transplanted dopaminergic neurons develop PD pathologic changes: a second case report. Mov. Disord. 2008, 23:2303-2306.
59. Lee H.-J., Patel S., Lee S.-J. Intravesicular localization and exocytosis of alpha-synuclein and its aggregates. J. Neurosci. 2005, 25:6016-6024.
60. Lee H.-J., Suk J.E., Bae E.J., Lee J.H., Paik S.R., Lee S.-J. Assembly-dependent endocytosis and clearance of extracellular alpha-synuclein. Int. J. Biochem. Cell Biol. 2008, 40:1835-1849.
61. Lee H.-J., Suk J.E., Bae E.J., Lee S.-J. Clearance and deposition of extracellular alpha-synuclein aggregates in microglia. Biochem. Biophys. Res. Commun. 2008, 372:423-428.
62. Lee H.J., Suk J.E., Patrick C., Bae E.J., Cho J.H., Rho S., Hwang D., Masliah E., Lee S.J. Direct transfer of alpha-synuclein from neuron to astroglia causes inflammatory responses in synucleinopathies. J. Biol. Chem. 2010, 285:9262-9272.
63. Lee S.J., Lee H.J., Masliah E. Multiple non-cell autonomous actions of alpha-synuclein in neurodegenerative diseases: is there a direct link?. Cell Cycle 2010, 9:2696-2697.
64. Legname G., Baskakov I.V., Nguyen H.O., Riesner D., Cohen F.E., DeArmond S.J., Prusiner S.B. Synthetic mammalian prions. Science 2004, 305:673-676.
65. Li J.Y., Englund E., Holton J.L., Soulet D., Hagell P., Lees A.J., Lashley T., Quinn N.P., Rehncrona S., Bjorklund A., 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.
66. Li W., Hoffman P.N., Stirling W., Price D.L., Lee M.K. Axonal transport of human alpha-synuclein slows with aging but is not affected by familial Parkinson's disease-linked mutations. J. Neurochem. 2004, 88:401-410.
67. Luk K.C., Song C., O'Brien P., Stieber A., Branch J.R., Brunden K.R., Trojanowski J.Q., Lee V.M. Exogenous {alpha}-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20051-20056.
68. Magalhaes A.C., Baron G.S., Lee K.S., Steele-Mortimer O., Dorward D., Prado M.A., Caughey B. Uptake and neuritic transport of scrapie prion protein coincident with infection of neuronal cells. J. Neurosci. 2005, 25:5207-5216.
69. Mandrekar S., Jiang Q., Lee C.Y., Koenigsknecht-Talboo J., Holtzman D.M., Landreth G.E. Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J. Neurosci. 2009, 29:4252-4262.
70. Masliah E., Rockenstein E., Adame A., Alford M., Crews L., Hashimoto M., Seubert P., Lee M., Goldstein J., Chilcote T., et al. Effects of alpha-synuclein immunization in a mouse model of Parkinson's disease. Neuron 2005, 46:857-868.
71. Mawuenyega K.G., Sigurdson W., Ovod V., Munsell L., Kasten T., Morris J.C., Yarasheski K.E., Bateman R.J. Decreased clearance of CNS beta-amyloid in Alzheimer's disease. Science 2011, 330:1774.
72. Mendez I., Vinuela A., Astradsson A., Mukhida K., Hallett P., Robertson H., Tierney T., Holness R., Dagher A., Trojanowski J.Q., Isacson O. Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nat. Med. 2008, 14:507-509.
73. Meyer-Luehmann M., Coomaraswamy J., Bolmont T., Kaeser S., Schaefer C., Kilger E., Neuenschwander A., Abramowski D., Frey P., Jaton A.L., et al. Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 2006, 313:1781-1784.
74. Moya K.L., Hassig R., Creminon C., Laffont I., Di Giamberardino L. Enhanced detection and retrograde axonal transport of PrPc in peripheral nerve. J. Neurochem. 2004, 88:155-160.
75. Nonaka T., Watanabe S.T., Iwatsubo T., Hasegawa M. Seeded aggregation and toxicity of {alpha}-synuclein and tau: cellular models of neurodegenerative diseases. J. Biol. Chem. 2010, 285:34885-34898.
76. Parihar M.S., Parihar A., Fujita M., Hashimoto M., Ghafourifar P. Mitochondrial association of alpha-synuclein causes oxidative stress. Cell. Mol. Life Sci. 2008, 65:1272-1284.
77. Petkova A.T., Leapman R.D., Guo Z., Yau W.M., Mattson M.P., Tycko R. Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 2005, 307:262-265.
78. Prusiner S.B. Shattuck lecture - neurodegenerative diseases and prions. N. Engl. J. Med. 2001, 344:1516-1526.
79. Rajendran L., Honsho M., Zahn T.R., Keller P., Geiger K.D., Verkade P., Simons K. Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:11172-11177.
80. Ren P.H., Lauckner J.E., Kachirskaia I., Heuser J.E., Melki R., Kopito R.R. Cytoplasmic penetration and persistent infection of mammalian cells by polyglutamine aggregates. Nat. Cell Biol. 2009, 11:219-225.
81. Richard K.L., Filali M., Prefontaine P., Rivest S. Toll-like receptor 2 acts as a natural innate immune receptor to clear amyloid beta 1-42 and delay the cognitive decline in a mouse model of Alzheimer's disease. J. Neurosci. 2008, 28:5784-5793.
82. Rinne J.O., Brooks D.J., Rossor M.N., Fox N.C., Bullock R., Klunk W.E., Mathis C.A., Blennow K., Barakos J., Okello A.A., et al. 11C-PiB PET assessment of change in fibrillar amyloid-beta load in patients with Alzheimer's disease treated with bapineuzumab: a phase 2, double-blind, placebo-controlled, ascending-dose study. Lancet Neurol. 2010, 9:363-372.
83. Rosas H.D., Salat D.H., Lee S.Y., Zaleta A.K., Pappu V., Fischl B., Greve D., Hevelone N., Hersch S.M. Cerebral cortex and the clinical expression of Huntington's disease: complexity and heterogeneity. Brain 2008, 131:1057-1068.
84. Ross C.A., Poirier M.A. Protein aggregation and neurodegenerative disease. Nat. Med. 2004, 10(Suppl.):S10-S17.
85. Roy S., Winton M.J., Black M.M., Trojanowski J.Q., Lee V.M. Rapid and intermittent cotransport of slow component-b proteins. J. Neurosci. 2007, 27:3131-3138.
86. Saito Y., Kawashima A., Ruberu N.N., Fujiwara H., Koyama S., Sawabe M., Arai T., Nagura H., Yamanouchi H., Hasegawa M., et al. Accumulation of phosphorylated alpha-synuclein in aging human brain. J. Neuropathol. Exp. Neurol. 2003, 62:644-654.
87. Sandberg M.K., Al-Doujaily H., Sharps B., Clarke A.R., Collinge J. Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 2011, 470:540-542.
88. Sassin I., Schultz C., Thal D.R., Rub U., Arai K., Braak E., Braak H. Evolution of Alzheimer's disease-related cytoskeletal changes in the basal nucleus of Meynert. Acta Neuropathol. 2000, 100:259-269.
89. Selkoe D.J. Folding proteins in fatal ways. Nature 2003, 426:900-904.
90. Selkoe D.J. Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat. Cell Biol. 2004, 6:1054-1061.
91. Sigurdsson E.M. Immunotherapy targeting pathological tau protein in Alzheimer's disease and related tauopathies. J. Alzheimers Dis. 2008, 15:157-168.
92. Silveira J.R., Raymond G.J., Hughson A.G., Race R.E., Sim V.L., Hayes S.F., Caughey B. The most infectious prion protein particles. Nature 2005, 437:257-261.
93. Solomon A., Richey T., Murphy C.L., Weiss D.T., Wall J.S., Westermark G.T., Westermark P. Amyloidogenic potential of foie gras. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:10998-11001.
94. Sponarova J., Nystrom S.N., Westermark G.T. AA-amyloidosis can be transferred by peripheral blood monocytes. PLoS One 2008, 3:e3308.
95. Sung J.Y., Park S.M., Lee C.H., Um J.W., Lee H.J., Kim J., Oh Y.J., Lee S.T., Paik S.R., Chung K.C. Proteolytic cleavage of extracellular secreted {alpha}-synuclein via matrix metalloproteinases. J. Biol. Chem. 2005, 280:25216-25224.
96. Tahara K., Kim H.D., Jin J.J., Maxwell J.A., Li L., Fukuchi K. Role of toll-like receptor signalling in Abeta uptake and clearance. Brain 2006, 129:3006-3019.
97. Tampellini D., Rahman N., Gallo E.F., Huang Z., Dumont M., Capetillo-Zarate E., Ma T., Zheng R., Lu B., Nanus D.M., et al. Synaptic activity reduces intraneuronal Abeta, promotes APP transport to synapses, and protects against Abeta-related synaptic alterations. J. Neurosci. 2009, 29:9704-9713.
98. Tanzi R.E., Moir R.D., Wagner S.L. Clearance of Alzheimer's Abeta peptide: the many roads to perdition. Neuron 2004, 43:605-608.
99. Tao-Cheng J.H. Activity-related redistribution of presynaptic proteins at the active zone. Neuroscience 2006, 141:1217-1224.
100. Tyedmers J., Mogk A., Bukau B. Cellular strategies for controlling protein aggregation. Nat. Rev. Mol. Cell Biol. 2010, 11:777-788.
101. Vandermeeren M., Mercken M., Vanmechelen E., Six J., van de Voorde A., Martin J.J., Cras P. Detection of tau proteins in normal and Alzheimer's disease cerebrospinal fluid with a sensitive sandwich enzyme-linked immunosorbent assay. J. Neurochem. 1993, 61:1828-1834.
102. Waxman E.A., Giasson B.I. A novel, high-efficiency cellular model of fibrillar alpha-synuclein inclusions and the examination of mutations that inhibit amyloid formation. J. Neurochem. 2010, 113:374-388.
103. Wyss-Coray T., Loike J.D., Brionne T.C., Lu E., Anankov R., Yan F., Silverstein S.C., Husemann J. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat. Med. 2003, 9:453-457.
104. Yonetani M., Nonaka T., Masuda M., Inukai Y., Oikawa T., Hisanaga S., Hasegawa M. Conversion of wild-type alpha-synuclein into mutant-type fibrils and its propagation in the presence of A30P mutant. J. Biol. Chem. 2009, 284:7940-7950.