Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein

Acta Neuropathologica

Volumn 99, Issue 5, 2000, Pages 469-481

  Probst, A ^a   Tolnay, M ^a   Mistl, C ^a   Gotz J ^b   Wiederhold, K H ^c   Jaton, A L ^c   Hong, M ^d   Ishihara, T ^d   Lee, V M Y ^d   Trojanowski, J Q ^d   Jakes, R ^e   Crowther, R A ^e   Goedert, M ^e   Spillantini, M G ^f   Burki K ^b  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c NOVARTIS PHARMA AG   (Switzerland)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Amyotrophy; Axonopathy; Neurofilaments; Tau protein; Transgenic mice

Indexed keywords

TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; DENDRITE; HUMAN; MOTOR PERFORMANCE; MOUSE; MUSCLE ATROPHY; MUSCLE WEAKNESS; NERVE DEGENERATION; NEUROFILAMENT; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; TRANSGENIC MOUSE;

EID: 0342803685     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004010051148     Document Type: Article

References (57)

1. Andreadis A, Brown WM, Kosik KS (1992) Structure and novel exons of the human tau gene. Biochemistry 31 : 10626-10633
2. Arriagada PV, Growdon JH, Hedley-White ET, Hyman BT (1992) Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 82 : 239-259
3. Braak E, Braak H, Mandelkow EM (1994) A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 87 : 554-567
4. Brion JP, Tremp G, Octave JN (1999) Transgenic expression of the shortest human tau affects its compartmentalization and its phosphorylation as in the pretangle stage of Alzheimer's disease. Am J Pathol 154 : 255-270
5. Buée-Scherrer V, Condamines O, Mourton-Gilles C, Jakes R, Goedert M, Pau B, Delacourte A (1996) AD2, a phosphorylation-dependent monoclonal antibody directed against tau proteins found in Alzheimer's disease. Mol Brain Res 39 : 79-88
6. Carpenter S (1968) Proximal axonal enlargement in motor neuron disease. Neurology 18 : 842-851
7. Chou SM, Hartmann HA (1965) Electron microscopy of focal neuroaxonal lesions produced by β,β'-iminodipropionitrile (IDPN) in rats. Acta Neuropathol 4 : 590-603
8. Collard JF, Coté F, Julien JP (1995) Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375 : 61-64
9. Clark LN, Poorkaj P, Wszolek Z, et al (1998) Pathogenic implications of mutations in the tau gene in pallido-ponto-nigral degeneration and related neurodegenerative disorders linked to chromosome 17. Proc Natl Acad Sci USA 95 : 13 103-13 107
10. Coté F, Collard JF, Julien JP (1993) Progressive neuronopathy in transgenic mice expressing the human neurofilament heavy gene: a mouse model of amyotrophic lateral sclerosis. Cell 73 : 35-46
11. D'Souza I, Poorkaj P, Hong M, Nochlin D, Lee VM-Y, Bird TD, Schellenberg GD (1999) Missense and silent tau gene mutations cause frontotemporal dementia with parkinsonism-chromosome 17 type, by affecting multiple alternative RNA splicing regulatory elements. Proc Natl Acad Sci USA 96 : 5598-5603
12. Ebneth A, Godemann R, Stamer K, Illenberger S, Trinczek B, Mandelkow EM, Mandelkow E (1998) Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J Cell Biol 143 : 777-794
13. Gallyas F (1971) Silver staining of Alzheimer's neurofibrillary changes by means of physical development. Acta Morphol Acad Sci Hung 19 : 1-8
14. Goedert M, Jakes R (1990) Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J 9 : 4225-4230
15. Goedert M, Wischik CM, Crowther RA, Walker JE, Klug A (1988) Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau. Proc Natl Acad Sci USA 85 : 4051-4055
16. Goedert M, Spillantini MG, Potier MC, Ulrich J, Crowther RA (1989) Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in brain. EMBO J 8 : 393-399
17. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3 : 519-526
18. Goedert M, Spillantini MG, Cairns NJ, Crowther RA (1992) Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8 : 159-168
19. Goedert M, Jakes R, Crowther RA, Cohen P, Vanmechelen E, Vandermeeren M, Cras P (1994) Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: identification of phosphorylation sites in tau protein. Biochem J 301 : 871-877
20. Goedert M, Jakes R, Vanmechelen E (1995) Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci Lett 189 : 167-170
21. Goedert M, Crowther RA, Spillantini MG (1998) Tau mutations cause frontotemporal dementias. Neuron 21 : 955-958
22. Goedert M, Spillantini MG, Crowther RA, Chen SG, Parchi P, Tabaton M, Lanska DJ, Markesbery WR, Wilhelmsen KC, Dickson DW, Petersen RB, Gambetti P (1999) Tau gene mutation in familial progressive subcortical gliosis. Nat Med 5 : 454-457
23. Goode BL, Feinstein SC (1994) Identification of a novel microtubule binding and assembly domain in the developmentally regulated inter-repeat region of tau. J Cell Biol 124 : 769-782
24. Götz J, Probst A, Spillantini MG, Schäfer T, Jakes R, Bürki K, Goedert M (1995) Somatodendritic localisation and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform. EMBO J 14 : 1304-1313
25. Greenberg SG, Davies P (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci USA 87 : 5827-5831
26. Griffin JW, Hoffman PN, Clark AW, Carroll PT, Price DL (1978) Slow axonal transport of neurofilament proteins: impairment by β,β′-iminodipropionitrile administration. Science 202 : 633-635
27. Grover A, Houlden H, Baker M, Adamson J, Lewis J, Prihar G, Pickering-Brown S, Duff K, Hutton M (1999) 5′ Splice site mutations in tau associated with the inherited dementia FTDP-17 affect a stem-loop structure that regulates alternative splicing of exon 10. J Biol Chem 274 : 15 134-15 143
28. Gustke N, Trinczek B, Biernat J, Mandelkow EM, Mandelkow E (1994) Domains of tau protein and interaction with microtubules. Biochemistry 33 : 9511-9522
29. Hasegawa M, Jakes R, Crowther RA, Lee VM-Y, Ihara Y, Goedert M (1996) Characterization of mAb AP422, a novel phosphorylation-dependent monoclonal antibody against tau protein. FEBS Lett 384 : 25-30
30. Hasegawa M, Smith MJ, Goedert M (1998) Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett 437 : 207-210
31. Hasegawa M, Smith MJ, Iijima M, Tabira T, Goedert M (1999) FTDP-17 mutations N279K and S305N in tau produce increased splicing of exon 10. FEBS Lett 443 : 93-96
32. Hirano A, Nakano I, Kurland LT, Mulder DW, Holley PW, Saccomanno G (1984) Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 43 : 471-480
33. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, Miller BI, Geschwind DH, Bird TD, McKeel D, Goate A, Morris JC, Wilhelmsen KC, Schellenberg GD, Trojanowski JQ, Lee VM-Y (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282 : 1914-1917
34. Hutton M, Lendon CL, Rizzu P, et al (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393 : 702-705
35. Jaton AL, Giger R, Vigouret JM, Enz A, Frick W, Closse A, Markstein R (1986) Pharmacological profile of the abeorphine 201-678 a potent orally active and long lasting dopamine agonist. Life Sci 38 : 155-164
36. Kampers T, Pangalos M, Geerts H, Wiech H, Mandelkow E (1999) Assembly of paired helical filaments from mouse tau: implications for the neurofibrillary pathology in transgenic mouse models for Alzheimer's disease. FEBS Lett 451 : 39-44
37. Kosik KS, Orecchio LD, Binder LI, Trojanowski JQ, Lee VM-Y, Lee G (1988) Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1 : 817-825
38. Lüthi A, Putten H van der, Botteri FM, Mansuy IM, Meins M, Frey U, Sansig G, Portet C, Schmutz M, Schröder M, Nitsch C, Laurent JP, Monard D (1997) Endogenous serine protease inhibitor modulates epileptic activity and hippocampal long-term potentiation. J Neurosci 17 : 4688-4698
39. Lynch T, Sano M, Marder KS, Bell KL, Foster NL, Defendini RF, Sima AAF, Keohane C, Nygaard TG, Fahn S, Mayeux R, Rowland LP, Wilhelmsen KC (1994) Clinical characteristics of a family with chromosome 17-linked disinhibition-dementia-parkinsonism-amyotrophy complex. Neurology 44 : 1878-1884
40. Matsumoto S, Hirano A, Goto S (1990) Spinal cord neurofibrillary tangles of Guamanian amyotrophic lateral sclerosis and parkinsonism-dementia complex. Neurology 40 : 975-979
41. Miyasaka H, Okabe S, Ishiguro K, Uchida YT, Hirokawa N (1993) Interaction of the tail domain of high molecular weight subunits of neurofilaments with the COOH-terminal region of tubulin and its regulation by the tau protein kinase II. J Biol Chem 268 : 22695-22702
42. Munoz DG, Greene C, Perl DP, Selkoe DJ (1988) Accumulation of phosphorylated neurofilaments in anterior horn motoneurons in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 47 : 9-18
43. Otvos L, Feiner L, Lang E, Szendrei GI, Goedert M, Lee VM-Y (1994) Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. J Neurosci Res 39 : 669-673
44. Poorkaj P, Bird TD, Wijsman E, Nemens E, Garruto RM, Anderson L, Andreadis A, Wiederholt WC, Raskind M, Schellenberg GD (1998) Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 43 : 815-825
45. Rouleau GA, Clark AW, Rooke K, Pramatarova A, Krizus A, Suchowersky O, Julien JP, Figlewicz D (1996) SODI mutation is associated with accumulation of neurofilaments in amyotrophic lateral sclerosis. Ann Neurol 39 : 128-131
46. Seubert P, Mawal-Dewan M, Barbour R, Jakes R, Goedert M, Johnson GVW, Litersky JM, Schenk D, Lieberburg I, Trojanowski JQ, Lee VM-Y (1995) Detection of phosphorylated Ser262 in fetal tau, adult tau and paired helical filament tau. J Biol Chem 270 : 18917-18922
47. Sima AAF, Defendini R, Keohane C, D'Amato C, Foster NL, Parchi P, Gambetti P, Lynch T, Wilhelmsen KC (1996) The neuropathology of chromosome 17-linked dementia. Ann Neurol 39 : 734-743
48. Spillantini MG, Goedert M (1998) Tau protein pathology in neurodegenerative diseases. Trends Neurosci 21 : 428-433
49. Spillantini MG, Goedert M, Crowther RA, Murrell JR, Farlow MR, Ghetti B (1997) Familial multiple system tauopathy with presenile dementia: a disease with abundant neuronal and glial tau filaments. Proc Natl Acad Sci USA 94 : 4113-4118
50. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B (1998) Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci USA 95 : 7737-7741
51. Tashiro T, Imai R, Komiya Y (1994) Early effects of β,β′-iminodipropionitrile on tubulin solubility and neurofilament phosphorylation in the axon. J Neurochem 63 : 291-300
52. Tashiro T, Sun X, Tsuda M, Komiya Y (1996) Differential axonal transport of soluble and insoluble tau in the rat sciatic nerve. J Neurochem 67 : 1566-1574
53. Trojanowski JQ, Schuck T, Schmidt ML, Lee VM-Y (1989) Distribution of tau proteins in the normal human central and peripheral nervous system. J Histochem Cytochem 37 : 209-215
54. Tu PH, Robinson KA, Snoo F de, Ever J, Peterson A, Lee VM-Y, Trojanowski JQ (1997) Selective degeneration of Purkinje cells with Lewy body-like inclusions in aged NFHLACZ transgenic mice. J Neurosci 17 : 2664-2674
55. Varani L, Hasegawa M, Spillantini MG, Smith MJ, Murrell JR, Ghetti B, Klug A, Goedert M, Varani G (1999) Structure of tau exon 10 splicing regulatory element RNA and destabilization by mutations of frontotemporal dementia and parkinsonism linked to chromosome 17. Proc Natl Acad Sci USA 96 : 8229-8234
56. Xu Z, Cork LC, Griffin JW, Cleveland DW (1993) Increased expression of neurofilament subunit NF-L produces morphological alterations that resemble the pathology of human motor neuron disease. Cell 73 : 23-33
57. Zhou L, Miller BL, McDaniel CH, Kelly L. Kim OJ, Miller CA (1998) Frontotemporal dementia: neuropil spheroids and presynaptic terminal degeneration. Ann Neurol 44 : 99-109