Effects of α-synuclein immunization in a mouse model of Parkinson's disease

Neuron

Volumn 46, Issue 6, 2005, Pages 857-868

  Masliah, Eliezer ^a,b   Rockenstein, Edward ^a   Adame, Anthony ^a   Alford, Michael ^a   Crews, Leslie ^a   Hashimoto, Makoto ^a   Seubert, Peter ^c   Lee, Michael ^c   Goldstein, Jason ^c   Chilcote, Tamie ^c   Games, Dora ^c   Schenk, Dale ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ELAN PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIFFUSE LEWY BODY DISEASE; GENE TARGETING; IMMUNE RESPONSE; IMMUNIZATION; LYSOSOME; MOUSE; NERVE CELL; NERVE DEGENERATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; VACCINATION;

ALPHA-SYNUCLEIN; ANIMALS; ANTIBODIES; BLOTTING, WESTERN; CATHEPSIN D; CEREBRAL CORTEX; DIAGNOSTIC IMAGING; DISEASE MODELS, ANIMAL; EPITOPE MAPPING; HUMANS; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; INCLUSION BODIES; LYSOSOMES; MICE; MICE, TRANSGENIC; MODELS, IMMUNOLOGICAL; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; PARKINSON DISEASE; PRESYNAPTIC TERMINALS; SUBCELLULAR FRACTIONS; SYNAPTOPHYSIN; SYNUCLEINS;

EID: 20444413356     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2005.05.010     Document Type: Article

References (82)

1. M. Alford, E. Masliah, L. Hansen, and R. Terry A simple dot-immunobinding assay for the quantification of synaptophysin-like immunoreactivity in human brain J. Histochem. Cytochem. 42 1994 283 287
2. J. Bainbridge, and B. Walker Cell mediated immune responses against human prion protein Clin. Exp. Immunol. 133 2003 310 317
3. F. Bard, R. Barbour, C. Cannon, R. Carretto, M. Fox, D. Games, T. Guido, K. Hoenow, K. Hu, and K. Johnson-Wood Epitope and isotype specificities of antibodies to Aβ peptide for protection against AD-like neuropathology Proc. Natl. Acad. Sci. USA 100 2003 2023 2028
4. E.J. Benner, R.L. Mosley, C.J. Destache, T.B. Lewis, V. Jackson-Lewis, S. Gorantla, C. Nemachek, S.R. Green, S. Przedborski, and H.E. Gendelman Therapeutic immunization protects dopaminergic neurons in a mouse model of Parkinson's disease Proc. Natl. Acad. Sci. USA 101 2004 9435 9440
5. R. Betarbet, T.B. Sherer, G. MacKenzie, M. Garcia-Osuna, A.V. Panov, and J.T. Greenamyre Chronic systemic pesticide exposure reproduces features of PD Nat. Neurosci. 3 2000 1301 1306
6. H. Braak, K. Del Tredici, H. Bratzke, J. Hamm-Clement, D. Sandmann-Keil, and U. Rub Staging of the intracerebral inclusion body pathology associated with idiopathic PD (preclinical and clinical stages) J. Neurol. Suppl. 3 2002 1 5
7. E.A. Burton, J.C. Glorioso, and D.J. Fink Gene therapy progress and prospects: PD Gene Ther. 10 2003 1721 1727
8. T. Coleman, S. Ellis, I. Martin, M. Lennard, and G. Tucker 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) is N-demethylated by cytochromes P450 2D6, 1A2 and 3A4 - implications for susceptibility to PD J. Pharmacol. Exp. Ther. 277 1996 685 690
9. A.M. Cuervo Autophagy: in sickness and in health Trends Cell Biol. 14 2004 70 77
10. A.M. Cuervo, L. Stefanis, R. Fredenburg, P.T. Lansbury, and D. Sulzer Impaired degradation of mutant α-syn by chaperone-mediated autophagy Science 305 2004 1292 1295
11. R. D'Amato, Z. Lipman, and S. Snyder Selectivity of the parkinsonian neurotoxin MPTP: toxic metabolite MPP+ binds to neuromelanin Science 231 1986 987 989
12. C. Dixon, N. Mathias, R.M. Zweig, D.A. Davis, and D.S. Gross α-Syn targets the plasma membrane via the Secretory pathway and induces toxicity in yeast Genetics 170 2005 47 59 10.1534/genetics.104.035493 Published on March 21, 2005
13. P. Dodd, J.A. Hardy, A.E. Oakley, and A.J. Strong Synaptosomes prepared from fresh human cerebral cortex; morphology, respiration and release of transmitter amino acids Brain Res. 224 1981 419 425
14. P.R. Dodd, J.A. Hardy, A.E. Oakley, J.A. Edwardson, E.K. Perry, and J.P. Delaunoy A rapid method for preparing synaptosomes: comparison, with alternative procedures Brain Res. 226 1981 107 118
15. D. Eliezer, E. Kutluay, R. Bussell Jr., and G. Browne Conformational properties of α-syn in its free and lipid-associated states J. Mol. Biol. 307 2001 1061 1073
16. S. Emadi, R. Liu, B. Yuan, P. Schulz, C. McAllister, Y. Lyubchenko, A. Messer, and M.R. Sierks Inhibiting aggregation of α-syn with human single chain antibody fragments Biochemistry 43 2004 2871 2878
17. R.H. Fabian Uptake of antineuronal IgM by CNS neurons: comparison with antineuronal IgG Neurology 40 1990 419 422
18. R.H. Fabian, and G. Petroff Intraneuronal IgG in the central nervous system: uptake by retrograde axonal transport Neurology 37 1987 1780 1784
19. M. Feany, and W. Bender A Drosophila model of PD Nature 404 2000 394 398
20. I. Ferrer, M. Boada Rovira, M.L. Sanchez Guerra, M.J. Rey, and F. Costa-Jussa Neuropathology and pathogenesis of encephalitis following Aβ immunization in AD Brain Pathol. 14 2004 11 20
21. L. Forno, L. DeLanney, I. Irwin, and J. Langston Electron microscopy of Lewy bodies in the amygdala-parahippocamapal region. Comparison with inclusion bodies in the MPTP-treated squirrel monkey L. Battistin G. Scarlato T. Caraceni S. Ruggieri Advances in Neurology 1996 Lippincott-Raven Publishers Philadelphia 217 228
22. D. Frenkel, and B. Solomon Towards Alzheimer's Aβ vaccination Biologicals 29 2001 243 247
23. D. Games, F. Bard, H. Grajeda, T. Guido, K. Khan, F. Soriano, N. Vasquez, N. Wehner, K. Johnson-Wood, and T. Yednock Prevention and reduction of AD-type pathology in PDAPP mice immunized with Aβ1-42 Ann. N Y Acad. Sci. 920 2000 274 284
24. J. Garzon, J. DeFelipe, J.R. Rodriguez, I. DeAntonio, A. Garcia-Espana, and P. Sanchez-Blazquez Transport of CSF antibodies to Gα subunits across neural membranes requires binding to the target protein and protein kinase C activity Brain Res. Mol. Brain Res. 65 1999 151 166
25. S.L. Gonias, L. Wu, and A.M. Salicioni Low density lipoprotein receptor-related protein: regulation of the plasma membrane proteome Thromb. Haemost. 91 2004 1056 1064
26. L.A. Hansen, and D. Galasko Lewy body disease Curr. Opin. Neurol. Neurosurg. 5 1992 889 894
27. L. Hansen, D. Salmon, D. Galasko, E. Masliah, R. Katzman, R. DeTeresa, L. Thal, M. Pay, R. Hofstetter, and M. Klauber The Lewy body variant of AD: a clinical and pathologic entity Neurology 40 1990 1 7
28. M. Hashimoto, and E. Masliah α-Syn in LBD and AD Brain Pathol. 9 1999 707 720
29. M. Hashimoto, S. Hernandez-Ruiz, L. Hsu, A. Sisk, Y. Xia, A. Takeda, M. Sundsmo, and E. Masliah Human recombinant NACP/α-syn is aggregated and fibrillated in vitro: Relevance for LBD Brain Res. 799 1998 301 306
30. M. Hashimoto, E. Rockenstein, M. Mante, M. Mallory, and E. Masliah β-Syn inhibits α-syn aggregation: a possible role as an anti-parkinsonian factor Neuron 32 2001 213 223
31. M. Hashimoto, Y. Sagara, I.P. Everall, M. Mallory, A. Everson, D. Langford, and E. Masliah FGF1 regulates signaling via the GSK3β pathway: implications for neuroprotection J. Biol. Chem. 277 2002 32985 32991
32. M. Hashimoto, E. Rockenstein, M. Mante, L. Crews, P. Bar-On, F.H. Gage, R. Marr, and E. Masliah An antiaggregation gene therapy strategy for LBD utilizing β-syn lentivirus in a transgenic model Gene Ther. 11 2004 1713 1723
33. J. Herz, R.C. Kowal, Y.K. Ho, M.S. Brown, and J.L. Goldstein Low density lipoprotein receptor-related protein mediates endocytosis of monoclonal antibodies in cultured cells and rabbit liver J. Biol. Chem. 265 1990 21355 21362
34. C. Hock, U. Konietzko, A. Papassotiropoulos, A. Wollmer, J. Streffer, R.C. von Rotz, G. Davey, E. Moritz, and R.M. Nitsch Generation of antibodies specific for Aβ by vaccination of patients with Alzheimer disease Nat. Med. 8 2002 1270 1275
35. M.M. Hussain Structural, biochemical and signaling properties of the low-density lipoprotein receptor gene family Front. Biosci. 6 2001 D417 D428
36. A. Iwai Properties of NACP/α-syn and its role in AD Biochim. Biophys. Acta 1502 2000 95 109
37. A. Iwai, E. Masliah, M. Yoshimoto, R. De Silva, N. Ge, A. Kittel, and T. Saitoh The precursor protein of non-Aβ component of AD amyloid (NACP) is a presynaptic protein of the central nervous system Neuron 14 1994 467 475
38. T. Iwatsubo, H. Yamaguchi, M. Fujimuro, H. Yokosawa, Y. Ihara, J.Q. Trojanowski, and V.-M. Lee Purification and characterization of Lewy bodies from brains of patients with diffuse LBD Am. J. Pathol. 148 1996 1517 1529
39. C. Janus, J. Pearson, J. McLaurin, P.M. Mathews, Y. Jiang, S.D. Schmidt, M.A. Chishti, P. Horne, D. Heslin, and J. French Aβ peptide immunization reduces behavioural impairment and plaques in a model of AD Nature 408 2000 979 982
40. P. Jenner Oxidative mechanisms in nigral cell death in PD Mov. Disord. 13 1998 24 34
41. D.W. Kim Efficient induction of dopaminergic neurons from embryonic stem cells for application to PD Yonsei Med. J. 45 Suppl 2004 23 27
42. T.D. Kim, S.R. Paik, and C.H. Yang Structural and functional implications of C-terminal regions of α-syn Biochemistry 41 2002 13782 13790
43. D. Kirik, B. Georgievska, and A. Bjorklund Localized striatal delivery of GDNF as a treatment for Parkinson disease Nat. Neurosci. 7 2004 105 110
44. K. Kosaka, M. Yoshimura, K. Ikeda, and H. Budka Diffuse type of LBD. Progressive dementia with abundant cortical Lewy bodies and senile changes of varying degree - A new disease? Clin. Neuropathol. 3 1984 183 192
45. M. Kounnas, R. Moir, G. Rebeck, A. Bush, W. Argaves, R. Tanzi, B. Hyman, and D. Strickland LDL receptor-related protein, a multifunctional apoE receptor, binds secreted Aβ precursor protein and mediates its degradation Cell 82 1995 331 340
46. R. Kruger, W. Kuhn, T. Muller, D. Woitalla, M. Graeber, S. Kosel, H. Przuntek, J. Epplen, L. Schols, and O. Reiss Ala30Pro mutation in the gene encoding α-syn in Parkinsons's disease Nat. Genet. 18 1998 106 108
47. P.T.J. Lansbury Evolution of amyloid: What normal protein folding may tell us about fibrillogenesis and disease Proc. Natl. Acad. Sci. USA 96 1999 3342 3344
48. M.K. Lee, W. Stirling, Y. Xu, X. Xu, D. Qui, A.S. Mandir, T.M. Dawson, N.G. Copeland, N.A. Jenkins, and D.L. Price Human α-syn-harboring familial PD-linked Ala-53 → Thr mutation causes neurodegenerative disease with α-syn aggregation in transgenic mice Proc. Natl. Acad. Sci. USA 99 2002 8968 8973
49. H.J. Lee, F. Khoshaghideh, S. Patel, and S.J. Lee Clearance of α-syn oligomeric intermediates via the lysosomal degradation pathway J. Neurosci. 24 2004 1888 1896
50. V.M. Lee, B.I. Giasson, and J.Q. Trojanowski More than just two peas in a pod: common amyloidogenic properties of tau and α-syn in neurodegenerative diseases Trends Neurosci. 27 2004 129 134
51. C.A. Lemere, E.T. Spooner, J.F. Leverone, C. Mori, M. Iglesias, J.K. Bloom, and T.J. Seabrook Amyloid-β immunization in AD transgenic mouse models and wildtype mice Neurochem. Res. 28 2003 1017 1027
52. R. Luthi-Carter Progress towards a vaccine for Huntington's disease Mol. Ther. 7 2003 569 570
53. R.A. Marr, E. Rockenstein, A. Mukherjee, M.S. Kindy, L.B. Hersh, F.H. Gage, I.M. Verma, and E. Masliah Neprilysin gene transfer reduces human amyloid pathology in transgenic mice J. Neurosci. 23 2003 1992 1996
54. E. Masliah, E. Rockenstein, I. Veinbergs, M. Mallory, M. Hashimoto, A. Takeda, Y. Sagara, A. Sisk, and L. Mucke Dopaminergic loss and inclusion body formation in α-syn mice: Implications for neurodegenerative disorders Science 287 2000 1265 1269
55. E. Masliah, E. Rockenstein, I. Veinbergs, Y. Sagara, M. Mallory, M. Hashimoto, and L. Mucke β-Amyloid peptides enhance α-syn accumulation and neuronal deficits in a transgenic mouse model linking AD and PD Proc. Natl. Acad. Sci. USA 98 2001 12245 12250
56. I.G. McKeith Spectrum of PD, Parkinson's dementia, and Lewy body dementia Neurol. Clin. 18 2000 865 902
57. P.J. McLean, H. Kawamata, S. Ribich, and B.T. Hyman Membrane association and protein conformation of α-syn in intact neurons. Effect of PD-linked mutations J. Biol. Chem. 275 2000 8812 8816
58. M.L. Meeker, R.B. Meeker, and J.N. Hayward Accumulation of circulating endogenous and exogenous immunoglobulins by hypothalamic magnocellular neurons Brain Res. 423 1987 45 55
59. T.W. Miller, T.L. Shirley, W.J. Wolfgang, X. Kang, and A. Messer DNA vaccination against mutant huntingtin ameliorates the HDR6/2 diabetic phenotype Mol. Ther. 7 2003 572 579
60. D. Morgan, D. Diamond, P. Gottschall, K. Ugen, C. Dickey, J. Hardy, K. Duff, P. Jantzen, G. DiCarlo, and D. Wilcock Aβ peptide vaccination prevents memory loss in an animal model of AD Nature 408 2000 982 985
61. L. Mucke, E. Masliah, G.Q. Yu, M. Mallory, E.M. Rockenstein, G. Tatsuno, K. Hu, D. Kholodenko, K. Johnson-Wood, and L. McConlogue High-level neuronal expression of Aβ1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation J. Neurosci. 20 2000 4050 4058
62. M. Polymeropoulos, C. Lavedan, E. Leroy, S. Ide, A. Dehejia, A. Dutra, B. Pike, H. Root, J. Rubenstein, and R. Boyer Mutation in the α-syn gene identified in families with PD Science 276 1997 2045 2047
63. E. Rockenstein, M. Mallory, M. Hashimoto, D. Song, C.W. Shults, I. Lang, and E. Masliah Differential neuropathological alterations in transgenic mice expressing α-syn from the platelet-derived growth factor and Thy-1 promoters J. Neurosci. Res. 68 2002 568 578
64. D.P. Salmon, D. Galasko, L.A. Hansen, E. Masliah, N. Butters, L.J. Thal, and R. Katzman Neuropsychological deficits associated with diffuse Lewy body disease Brain Cogn. 31 1996 148 165
65. D. Schenk, R. Barbour, W. Dunn, G. Gordon, H. Grajeda, T. Guido, K. Hu, J. Huang, K. Johnson-Wood, and K. Khan Immunization with Aβ attenuates Alzheimer-disease-like pathology in the PDAPP mouse Nature 400 1999 173 177
66. W.J. Schneider, and J. Nimpf LDL receptor relatives at the crossroad of endocytosis and signaling Cell. Mol. Life Sci. 60 2003 892 903
67. B.S. Shastry Parkinson disease: etiology, pathogenesis and future of gene therapy Neurosci. Res. 41 2001 5 12
68. E.M. Sigurdsson, D.R. Brown, M. Daniels, R.J. Kascsak, R. Kascsak, R. Carp, H.C. Meeker, B. Frangione, and T. Wisniewski Immunization delays the onset of prion disease in mice Am. J. Pathol. 161 2002 13 17
69. A.B. Singleton, M. Farrer, J. Johnson, A. Singleton, S. Hague, J. Kachergus, M. Hulihan, T. Peuralinna, A. Dutra, and R. Nussbaum α-Syn locus triplication causes PD Science 302 2003 841
70. M. Spillantini, M. Schmidt, V.-Y. Lee, J. Trojanowski, R. Jakes, and M. Goedert α-Syn in Lewy bodies Nature 388 1997 839 840
71. A. Takeda, M. Hashimoto, M. Mallory, M. Sundsmo, L. Hansen, A. Sisk, and E. Masliah Abnormal distribution of the non-Aβ component of AD amyloid precursor/α-syn in LBD as revealed by proteinase K and formic acid pretreatment Lab. Invest. 78 1998 1169 1177
72. A. Takeda, M. Mallory, M. Sundsmo, W. Honer, L. Hansen, and E. Masliah Abnormal accumulation of NACP/α-syn in neurodegenerative disorders Am. J. Pathol. 152 1998 367 372
73. A. Takeda, M. Hashimoto, M. Mallory, M. Sundsmo, L. Hansen, and E. Masliah C-terminal α-syn immunoreactivity in structures other than Lewy bodies in neurodegenerative disorders Acta Neuropathol. (Berl.) 99 2000 296 304
74. J. Trojanowski, and V. Lee Aggregation of neurofilament and α-syn proteins in Lewy bodies: implications for pathogenesis of Parkinson disease and Lewy body dementia Arch. Neurol. 55 1998 151 152
75. J. Trojanowski, M. Goedert, T. Iwatsubo, and V. Lee Fatal attractions: abnormal protein aggregation and neuron death in PD and lewy body dementia Cell Death Differ. 5 1998 832 837
76. S. Ubol, B. Levine, S.H. Lee, N.S. Greenspan, and D.E. Griffin Roles of immunoglobulin valency and the heavy-chain constant domain in antibody-mediated downregulation of Sindbis virus replication in persistently infected neurons J. Virol. 69 1995 1990 1993
77. B. Veldman, A. Wijn, N. Knoers, P. Praamstra, and M. Horstink Genetic and environmental risk factors in PD Clin. Neurol. Neurosurg. 100 1998 15 26
78. K. Wakabayashi, K. Matsumoto, K. Takayama, M. Yoshimoto, and H. Takahashi NACP, a presynaptic protein, immunoreactivity in Lewy bodies in PD Neurosci. Lett. 239 1997 45 48
79. A.R. White, and S.H. Hawke Immunotherapy as a therapeutic treatment for neurodegenerative disorders J. Neurochem. 87 2003 801 808
80. A.R. White, P. Enever, M. Tayebi, R. Mushens, J. Linehan, S. Brandner, D. Anstee, J. Collinge, and S. Hawke Monoclonal antibodies inhibit prion replication and delay the development of prion disease Nature 422 2003 80 83
81. T. Yoshizaki, M. Inaji, H. Kouike, T. Shimazaki, K. Sawamoto, K. Ando, I. Date, K. Kobayashi, T. Suhara, Y. Uchiyama, and H. Okano Isolation and transplantation of dopaminergic neurons generated from mouse embryonic stem cells Neurosci. Lett. 363 2004 33 37
82. C. Zhou, S. Emadi, M.R. Sierks, and A. Messer A human single-chain Fv intrabody blocks aberrant cellular effects of overexpressed α-syn Mol. Ther. 10 2004 1023 1031