Tau gene transfer, but not alpha-synuclein, induces both progressive dopamine neuron degeneration and rotational behavior in the rat

Neurobiology of Disease

Volumn 20, Issue 1, 2005, Pages 64-73

  Klein, Ronald L ^a,c   Dayton, Robert D ^a   Lin, Wen Lang ^b   Dickson, Dennis W ^b  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b MAYO CLINIC   (United States)

^c LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

Synuclein; Adeno associated virus; Neurodegeneration; Neurofibrillary tangles; Substantia nigra; Tau

Indexed keywords

ALPHA SYNUCLEIN; AMPHETAMINE; DOPAMINE; TAU PROTEIN; VIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CIRCLING BEHAVIOR; CONTROLLED STUDY; DOPAMINE BRAIN LEVEL; DOPAMINERGIC NERVE CELL; EXPERIMENTAL MODEL; GENE FUNCTION; GENE TRANSFER; MALE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA; VIRUS MUTANT; WILD TYPE;

ALPHA-SYNUCLEIN; ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; DOPAMINE; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; MALE; MOTOR ACTIVITY; MOVEMENT DISORDERS; MUTATION; NERVE DEGENERATION; NEUROFIBRILLARY TANGLES; RATS; RATS, SPRAGUE-DAWLEY; ROTATION; SUBSTANTIA NIGRA; TAU PROTEINS; TAUOPATHIES;

EID: 24044494918     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2005.02.001     Document Type: Article

References (50)

1. B. Allen, E. Ingram, M. Takao, M.J. Smith, R. Jakes, K. Virdee, H. Yoshida, M. Holzer, M. Craxton, P.C. Emson, C. Atzori, A. Migheli, R.A. Crowther, B. Ghetti, M.G. Spillantini, and M. Goedert Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein J. Neurosci. 22 2002 9340 9351
2. C. Andorfer, Y. Kress, M. Espinoza, R. de Silva, K.L. Tucker, Y.A. Barde, K. Duff, and P. Davies Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms J. Neurochem. 86 2003 582 890
3. M. Baker, I. Litvan, H. Houlden, J. Adamson, D. Dickson, J. Perez-Tur, J. Hardy, T. Lynch, E. Bigio, and M. Hutton Association of an extended haplotype in the tau gene with progressive supranuclear palsy Hum. Mol. Genet. 8 1999 711 715
4. C. Bancher, C. Brunner, H. Lassmann, H. Budka, K. Jellinger, F. Seitelberger, I. Grundke-Iqbal, K. Iqbal, and H.M. Wisniewski Tau and ubiquitin immunoreactivity at different stages of formation of Alzheimer neurofibrillary tangles Prog. Clin. Biol. Res. 317 1989 837 848
5. E. Braak, D. Sandmann-Keil, U. Rub, W.P. Gai, R.A. de Vos, E.N. Steur, K. Arai, and H. Braak Alpha-synuclein immunopositive Parkinson's disease-related inclusion bodies in lower brain stem nuclei Acta Neuropathol. (Berl) 101 2001 195 201
6. M.C. Chartier-Harlin, J. Kachergus, C. Roumier, V. Mouroux, X. Douay, S. Lincoln, C. Levecque, L. Larvor, J. Andrieux, M. Hulihan, N. Waucquier, L. Defebvre, P. Amouyel, M. Farrer, and A. Destee Alpha-synuclein locus duplication as a cause of familial Parkinson's disease Lancet 364 2004 1167 1169
7. A. Crowe, H. Ksiezak-Reding, W.K. Liu, D.W. Dickson, and S.H. Yen The N terminal region of human tau is present in Alzheimer's disease protein A68 and is incorporated into paired helical filaments Am. J. Pathol. 139 1991 1463 1470
8. E. Di Maria, M. Tabaton, T. Vigo, G. Abbruzzese, E. Bellone, C. Donati, E. Frasson, R. Marchese, P. Montagna, D.G. Munoz, P.P. Pramstaller, G. Zanusso, F. Ajmar, and P. Mandich Corticobasal degeneration shares a common genetic background with progressive supranuclear palsy Ann. Neurol. 47 2000 374 377
9. D.W. Dickson, H. Ksiezak-Reding, W.K. Liu, P. Davies, A. Crowe, and S.H. Yen Immunocytochemistry of neurofibrillary tangles with antibodies to subregions of tau protein: identification of hidden and cleaved tau epitopes and a new phosphorylation site Acta Neuropathol. (Berl) 84 1992 596 605
10. F. Dou, W.J. Netzer, K. Tanemura, F. Li, F.U. Hartl, A. Takashima, G.K. Gouras, P. Greengard, and H. Xu Chaperones increase association of tau protein with microtubules Proc. Natl. Acad. Sci. U. S. A. 100 2003 721 726
11. J.E. Duda, B.I. Giasson, M.E. Mabon, D.C. Miller, L.I. Golbe, V.M. Lee, and J.Q. Trojanowski Concurrence of α-synuclein and tau brain pathology in the Contursi kindred Acta Neuropathol. 104 2002 7 11
12. A.J. Dunn Neurochemical methods for evaluating cerebral biogenic amine responses to cytokines and their involvement in the central actions of interleukin-1 E.B. De Souza Methods in neurosciences Neurobiology of cytokines vol. 17 Part B 1993 Academic Press San Diego 209 222
13. M. Farrer, D.M. Maraganore, P. Lockhart, A. Singleton, T.G. Lesnick, M. de Andrade, A. West, R. de Silva, J. Hardy, and D. Hernandez Alpha-synuclein gene haplotypes are associated with Parkinson's disease Hum. Mol. Genet. 10 2001 1847 1851
14. B.I. Giasson, J.E. Duda, S.M. Quinn, B. Zhang, J.Q. Trojanowski, and V.M. Lee Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-syuclein Neuron 34 2002 521 533
15. J. Götz, J.R. Streffer, D. David, A. Schild, F. Hoerndli, L. Pennanen, P. Kurosinki, and F. Chen Transgenic models of Alzheimer's disease and related disorders: histopathology, behavior and therapy Mol. Psychiatry 9 2004 664 683
16. D. Grimm, A. Kern, K. Rittner, and J.A. Kleinschmidt Novel tools for production and purification of recombinant adeno-associated virus vectors Hum. Gene Ther. 9 1998 2745 2760
17. K. Gwin-Hardy, N.D. Mehta, M. Farrer, D. Maraganore, M. Muenter, S.-H. Yen, J. Hardy, and D.W. Dickson Distinctive neuropathology revealed by α-synuclein antibodies in hereditary parkinsonism and dementia linked to chromosome 4p Acta Neuropathol. 99 2000 663 672
18. D.G. Healy, P.M. Abou-Sleiman, A.J. Lees, J.P. Casas, N. Quinn, K. Bhatia, A.D. Hingorani, and N.W. Wood Tau gene and Parkinson's disease: a case-control study and meta-analysis J. Neurol. Neurosurg. Psychiatry 75 2004 962 965
19. M. Hutton, C.L. Lendon, P. Rizzu, M. Baker, S. Froelich, H. Houlden, S. Pickering-Brown, S. Chakraverty, A. Isaacs, A. Grover, J. Hackett, J. Adamson, S. Lincoln, D. Dickson, P. Davies, R.C. Petersen, M. Stevens, E. de Graaff, E. Wauters, J. van Baren, M. Hillebrand, M. Joosse, J.M. Kwon, P. Nowotny, L.K. Che, J. Norton, J.C. Morris, L.A. Reed, J. Trojanowski, H. Basun, L. Lannfelt, M. Neystat, S. Fahn, F. Dark, T. Tannenberg, P.R. Dodd, N. Hayward, J.B.J. Kwok, P.R. Schofield, A. Andreadis, J. Snowden, D. Craufurd, D. Neary, F. Owen, B.A. Oostra, J. Hardy, A. Goate, J.V. Swieten, D. Mann, T. Lynch, and P. Heutink Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17 Nature 393 1998 702 705
20. T. Ishizawa, P. Mattila, P. Davies, D. Wang, and D.W. Dickson Colocalization of tau and alpha-synuclein in Lewy bodies J. Neuropathol. Exp. Neurol. 62 2003 389 397
21. G.A. Jicha, A. O'Donnell, C. Weaver, R. Angeletti, and P. Davies Hierarchical phosphorylation of recombinant tau by the paired-helical filament-associated protein kinase is dependent on cyclic AMP-dependent protein kinase J. Neurochem. 72 1999 214 224
22. D. Kirik, C. Rosenblad, A. Bjorklund, and R.J. Mandel Long-term rAAV-mediated gene transfer of GDNF in the rat Parkinson's model: intrastriatal but not intranigral transduction promotes functional regeneration in the lesioned nigrostriatal system J. Neurosci. 20 2000 4686 4700
23. D. Kirik, C. Rosenblad, C. Burger, C. Lundberg, T.E. Johansen, N. Muzyczka, R.J. Mandel, and A. Bjorklund Parkinson-like neurodegeneration induced by targeted overexpression of alpha-synuclein in the nigrostriatal system J. Neurosci. 22 2002 2780 2791
24. R.L. Klein, M.A. King, M.E. Hamby, and E.M. Meyer Dopaminergic cell loss induced by human A30P alpha-synuclein gene transfer to the rat substantia nigra Hum. Gene Ther. 13 2002 605 612
25. R.L. Klein, M.E. Hamby, Y. Gong, A.C. Hirko, S. Wang, J.A. Hughes, M.A. King, and E.M. Meyer Dose and promoter effects of adeno-associated viral vector for GFP expression in the rat brain Exp. Neurol. 176 2002 66 74
26. R.L. Klein, M.E. Hamby, C.F. Sonntag, W.J. Millard, M.A. King, and E.M. Meyer Measurements of vector-derived neurotrophic factor and green fluorescent protein levels in the brain Methods 28 2002 286 292
27. R.L. Klein, W.L. Lin, D.W. Dickson, J. Lewis, M. Hutton, K. Duff, E.M. Meyer, and M.A. King Rapid neurofibrillary tangle formation after localized gene transfer of mutated tau Am. J. Pathol. 164 2004 347 353
28. M.K. Lee, W. Stirling, Y. Xu, X. Xu, D. Qui, AS. Mandir, T.M. Dawson, N.G. Copeland, N.A. Jenkins, and D.L. Price Human alpha-synuclein-harboring familial Parkinson's disease-linked Ala-53 to Thr mutation causes neurodegenerative disease with alpha-synuclein aggregation in transgenic mice Proc. Natl. Acad. Sci. U. S. A. 99 2002 8968 8973
29. J. Lewis, E. McGowan, J. Rockwood, H. Melrose, P. Nacharaju, M. Van Slegtenhorst, K. Gwinn-Hardy, M. Paul Murphy, M. Baker, X. Yu, K. Duff, J. Hardy, A. Corral, W.L. Lin, S.H. Yen, D.W. Dickson, P. Davies, and M. Hutton Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein Nat. Genet. 25 2000 402 405
30. W.L. Lin, J. Lewis, S.H. Yen, M. Hutton, and D.W. Dickson Filamentous tau in oligodendrocytes and astrocytes of transgenic mice expressing the human tau isoform with the P301L mutation Am. J. Pathol. 162 2003 213 218
31. W.L. Lin, J. Lewis, S.H. Yen, M. Hutton, and D.W. Dickson Ultrastructural neuronal pathology in transgenic mice expressing mutant (P301L) tau J. Neurocytol. 32 2003 1091 1105
32. W.L. Lin, M.W. DeLucia, and D.W. Dickson Alpha-synuclein immunoreactivity in neuronal nuclear inclusions and neurites in multiple system atrophy Neurosci. Lett. 354 2004 99 102
33. C. Lo Bianco, J.L. Ridet, B.L. Schneider, N. Deglon, and P. Aebischer Alpha-synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease Proc. Natl. Acad. Sci. U. S. A. 99 2002 10813 10818
34. J.E. Loeb, W.S. Cordier, M.E. Harris, M.D. Weitzman, and T.J. Hope Enhanced expression of transgenes from adeno-associated virus vectors with the woodchuck hepatitis virus posttranscriptional regulatory element: implications for gene therapy Hum. Gene Ther. 10 1999 2295 2305
35. E.R. Martin, W.K. Scott, M.A. Nance, R.L. Watts, J.P. Hubble, W.C. Koller, K. Lyons, R. Pahwa, M.B. Stern, A. Colcher, B.C. Hiner, J. Jankovic, W.G. Ondo, F.H. Allen Jr., C.G. Goetz, G.W. Small, D. Masterman, F. Mastaglia, N.G. Laing, J.M. Stajich, R.C. Ribble, M.W. Booze, A. Rogala, M.A. Hauser, F. Zhang, R.A. Gibson, L.T. Middleton, A.D. Roses, J.L. Haines, B.L. Scott, M.A. Pericak-Vance, and J.M. Vance Association of single-nucleotide polymorphisms of the tau gene with late-onset Parkinson disease JAMA 286 2001 2245 2250
36. S.S. Mirra, J.R. Murrell, M. Gearing, M.G. Spillantini, M. Goedert, R.A. Crowther, A.I. Levey, R. Jones, J. Green, J.M. Shoffner, B.H. Wainer, M.L. Schmidt, J.Q. Trojanowski, and B. Ghetti Tau pathology in a family with dementia and a P301L mutation in tau J. Neuropathol. Exp. Neurol. 58 1999 335 345
37. P. Nacharaju, J. Lewis, C. Easson, S. Yen, J. Hackett, M. Hutton, and S.H. Yen Accelerated filament formation from tau protein with specific FTDP-17 missense mutations FEBS Lett. 447 1999 195 199
38. M. Neumann, P.J. Kahle, B.I. Giasson, L. Ozmen, E. Borroni, W. Spooren, V. Muller, S. Odoy, H. Fujiwara, M. Hasegawa, T. Iwatsubo, J.Q. Trojanowski, H.A. Kretzschmar, and C. Haass Misfolded proteinase K-resistant hyperphosphorylated alpha-synuclein in aged transgenic mice with locomotor deterioration and in human alpha-synucleinopathies J. Clin. Invest. 110 2002 1429 1439
39. H. Niwa, K. Yamamura, and J. Miyazaki Efficient selection for high-expression transfectants with a novel eukaryotic vector Gene 108 1991 193 199
40. J.C. Paterna, and H. Bueler Recombinant adeno-associated virus vector design and gene expression in the mammalian brain Methods 28 2002 208 218
41. G. Paxinos, and C. Watson The rat brain in stereotaxic coordinates 1998 Academic Press San Diego
42. L. Petrucelli, D. Dickson, K. Kehoe, J. Taylor, H. Snyder, A. Grover, E. McGowan, J. Lewis, W.H. Dillmann, S.E. Browne, R. Voellmy, Y. Tsuboi, T.M. Dawson, B. Wolozin, J. Hardy, and M. Hutton CHIP and Hsp70 regulate Tau ubiquitination, degradation and aggregation Hum. Mol. Genet. 13 2004 703 714
43. P. Poorkaj, N.A. Muma, V. Zhukareva, E.J. Cochran, K.M. Shannon, H. Hurtig, W.C. Koller, T.D. Bird, J.Q. Trojanowski, V.M. Lee, and G.D. Schellenberg An R5L tau mutation in a subject with a progressive supranuclear palsy phenotype Ann. Neurol. 52 2002 511 516
44. J.A. Schneider, J.L. Bienias, D.W. Gilley, D.E. Kvarnberg, E.J. Mufson, and D.A. Bennett Improved detection of substantia nigra pathology in Alzheimer's disease J. Histochem. Cytochem. 50 2002 99 106
45. A.B. Singleton, M. Farrer, J. Johnson, A. Singleton, S. Hague, J. Kachergus, M. Hulihan, T. Peuralinna, A. Dutra, R. Nussbaum, S. Lincoln, A. Crawley, M. Hanson, D. Maraganore, C. Adler, M.R. Cookson, M. Muenter, M. Baptista, D. Miller, J. Blancato, J. Hardy, and K. Gwinn-Hardy Alpha-synuclein locus triplication causes Parkinson's disease Science 302 2003 841
46. L.A. Sternberger, and N.H. Sternberger Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ Proc. Natl. Acad. Sci. U. S. A. 80 1983 6126 6130
47. I. Tsunoda, L.Q. Kuang, J.E. Libbey, and R.S. Fujinami Axonal injury heralds virus-induced demyelination Am. J. Pathol. 162 2003 1259 1269
48. K. Wakabayashi, K. Oyanagi, T. Makifuchi, F. Ikuta, A. Homma, Y. Homma, Y. Horikawa, and S. Tokiguchi Corticobasal degeneration: etiopathological significance of the cytoskeletal alterations Acta Neuropathol. 87 1994 545 553
49. S.H. Yen, A. Crowe, and D.W. Dickson Monoclonal antibodies to Alzheimer neurofibrillary tangles: I. Identification of polypeptides Am. J. Pathol. 120 1985 282 291
50. C. Zehr, K. Goodwin, W.L. Lin, D.W. Dickson, E. McGowan, J. Lewis, and M. Hutton Axonal degeneration in P301L tau transgenic mice. Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17 Neurobiol. Aging 25 Suppl. 2 2004 S243