Tau gene mutation G389R causes a tauopathy with abundant pick body-like inclusions and axonal deposits

Journal of Neuropathology and Experimental Neurology

Volumn 58, Issue 12, 1999, Pages 1207-1226

  Murrell, Jill R ^a   Spillantini, Maria Grazia ^b   Zolo, Paolo ^c   Guazzelli, Mario ^d   Smith, Michael J ^e   Hasegawa, Masato ^e   Redi, Francesco ^c   Crowther, R Anthony ^e   Pietrini, Pietro ^d   Ghetti, Bernardino ^a   Goedert, Michel ^e  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c IRCCS POLICLINICO SAN DONATO   (Italy)

^d UNIVERSITY OF PISA   (Italy)

^e Med Res Cncl Lab of Molec B   (United Kingdom)

Author keywords

Axonal tau deposits; Brain metabolism; Frontotemporal dementia; Pick body like inclusions; Tauopathy

Indexed keywords

TAU PROTEIN;

ADULT; AMNESIA; APATHY; APHASIA; ARTICLE; BRAIN ATROPHY; CASE REPORT; CELL INCLUSION; DENTATE GYRUS; DEPHOSPHORYLATION; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; HUMAN; HUMAN TISSUE; HYPERPHAGIA; MALE; MICROTUBULE ASSEMBLY; NEOCORTEX; NERVE FIBER; NUCLEAR MAGNETIC RESONANCE IMAGING; PICK PRESENILE DEMENTIA; PRIORITY JOURNAL;

EID: 0032763203     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-199912000-00002     Document Type: Article

References (77)

1. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA. Multiple isoforms of human microtubule-associated protein tau: Sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989;3:519-26
2. Spillantini MG, Bird T, Ghetti B. Frontotemporal dementia and parkinsonism linked to chromosome 17: A new group of tauopathies. Brain Pathol 1998;8:387-402
3. Kertesz A, Munoz D. Pick's disease, frontotemporal dementia, and Pick complex: Emerging concepts. Arch Neurol 1998;55:302-4
4. Poorkaj P, Bird TD, Wijsman E, et al. Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 1998;43: 815-25
5. Hutton M, Lendon CL, Rizzu P, et al. Association of missense and 5′-splice-site mutations in tau with inherited dementia FTDP-17. Nature 1998;393:702-5
6. Spillantini MG, Murrell J, Goedert M, Farlow MR, Klug A. Ghetti B. Mutation in the tau gene in familial system tauopathy with presenile dementia. Proc Natl Acad Sci USA 1998;95:7737-41
7. Dumanchin C, Camuzat A, Campion D, et al. Segregation of a missense mutation in the microtubule-associated protein tau gene with familial frontotemporal dementia and parkinsonism. Hum Mol Genet 1998;7:1825-29
8. Clark LN, Poorkaj P, Wszolek Z, et al. 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 1998;98:13103-7
9. Rizzu P, Van Swieten JC, Joosse M, et al. High prevalence of mutations in the microtubule-associated protein tau in a population study of frontotemporal dementia in the Netherlands. Am J Hum Genet 1999;64:414-21
10. Iijima M, Tabira T, Poorkaj P, et al. A distinct familial presenile dementia with a novel missense mutation in the tau gene. NeuroReport 1999;10:497-501
11. Morris HR, Perez-Tur J, Janssen JC, et al. Mutation in the tau exon 10 splice site region in familial frontotemporal dementia. Ann Neural 1999;45:270-71
12. Goedert M, Spillantini MG, Crowther RA, et al. Tau gene mutation in familial progressive subcortical gliosis. Nature Med 1999;5: 454-57
13. Mirra SS, Murrell JR, Gearing M, et al. Tau pathology in a family with dementia and a P301L mutation in tau. J Neuropathol Exp Neurol 1999;58:335-45
14. Bird TD, Nochlin D, Poorkaj P, et al. A clinical pathological comparison of three families with frontotemporal dementia and identical mutations in the tau gene (P301L). Brain 1999;122:741-56
15. D'Souza I, Poorkaj P, Hong, M, et al. 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 1999;96:5598-603
16. Bugiani O, Murrell JR, Giaccone G, et al. Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau. J Neuropathol Exp Neurol 1999;58:667-77
17. Nasreddine ZS, Loginov M, Clark LN, et al. From genotype to phenotype: A clinical, pathological, and biochemical investigation of frontotemporal dementia and parkinsonism (FTDP-17) caused by the P301L tau mutation. Ann Neurol 1999;45:704-15
18. Delisle MB, Murrell JR, Richardson R, et al. A mutation at codon 279 (N279K) in exon 10 of the Tau gene causes a tauopathy with dementia and supranuclear palsy. Acta Neuropathol 1999;98:62-77
19. Van Swieten JC, Stevens M, Rosso SM, et al. Phenotypic variation in hereditary frontotemporal dementia with tau mutations. Ann Neurol 1999;46:617-26
20. Goedert M, Spillantini MG, Potier MC, Ulrich J, Crowther RA. 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 human brain. EMBO J 1989;8:393-99
21. Gustke N, Trinczek B, Biernat J, Mandelkow EM, Mandelkow E. Domains of tau protein and interactions with microtubules. Biochemistry 1994;33:9511-22
22. Goode BL, Feinstein SC. Identification of a novel microtubule binding and assembly domain in the developmentally regulated inter-repeat region of tau. J Cell Biol 1994;124:769-82
23. Goedert M, Jakes R. Expression of separate isoforms of human tau protein: Correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J 1990;9:4225-30
24. Goedert M, Spillantini MG, Cairns NJ, Crowther RA. Tau proteins of Alzheimer paired helical filaments: Abnormal phosphorylation of all six brain isoforms. Neuron 1992;8:159-68
25. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, et al. Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 1998;282:1914-17
26. Hasegawa M, Smith MJ, Iijima M, Tabira T, Goedert M. FTDP-17 mutations N279K and S305N in tau produce increased splicing of exon 10. FEBS Lett 1999;443:93-96
27. Grover A, Houlden H, Baker M, et al. 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 1999;274:15134-43
28. Varani L, Hasegawa M, Spillantini MG, et al. 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 1999;96:8229-34
29. Reed LA, Schmidt ML, Wszolek ZK, et al. The neuropathology of a chromosome 17-linked autosomal dominant parkinsonism and dementia ("pallido-ponto-nigral degeneration"). J Neuropathol Exp Neurol 1998;57:588-601
30. Spillantini MG, Goedert M, Crowther RA, Murrell JR, Farlow MR, Ghetti B. Familial multiple system tauopathy with presenile dementia: A disease with abundant neuronal and glial tau filaments. Proc Natl Acad Sci USA 1997;94:4113-18
31. Hasegawa M, Smith MJ, Goedert M. Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett 1998;437:207-10
32. Dayanandan R, Van Slegtenhorst M, Mack TGA, et al. Mutations in tau reduce its microtubule binding properties in intact cells and affect its phosphorylation. FEBS Lett 1999;446:228-32
33. Nacharaju P, Lewis J, Easson C, et al. Accelerated filament formation from tau protein with specific FTDP-17 missense mutations. FEBS Lett 1999;447:195-99
34. Goedert M, Jakes R, Crowther RA. Effects of frontotemporal dementia FTDP-17 mutations on heparin-induced assembly of tau filaments. FEBS Lett 1999;450:306-11
35. Goedert M, Crowther RA, Spillantini MG. Tau mutations cause frontotemporal dementias. Neuron 1998;21:955-58
36. Spillantini MG, Crowther RA, Goedert M. Comparison of the neurofibrillary pathology in Alzheimer's disease and familial presenile dementia with tangles. Acta Neuropathol 1996;92:42-48
37. Pietrini P, Furey ML, Graff-Radford N, et al. Preferential metabolic involvement of visual cortical areas in a subtype of Alzheimer's disease: Clinical implications. Am J Psychiat 1996;153:1261-68
38. Pietrini P, Azari NP, Grady CL, et al. Pattern of cerebral metabolic interactions in a subject at risk for Alzheimer's disease. Dementia 1993;4:94-101
39. 14C)-deoxyglucose method for the measurement of local cerebral glucose utilization: Theory, procedure and normal values in the conscious and anesthetized albino rat. J Neurochem 1977;28:897-916
40. Goedert M, Jakes R, Crowther RA, et al. Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: Identification of phosphorylation sites in tau protein. Biochem J 1994;301:871-77
41. Goedert M, Jakes R, Vanmechelen E. Monoclonal antibody AT8 recognizes tau protein phosphorylated at both serine 202 and threonine 205. Neurosci Lett 1995;189:167-70
42. Zheng-Fischhöfer Q, Biernat J, Mandelkow EM, Illenberger S, Godemann R, Mandelkow E. Sequential phosphorylation of tau by glycogen synthase kinase-3β and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical-filament-like conformation. Eur J Biochem 1998;252:542-52
43. Seubert P, Mawal-Dewan M, Harbour R, et al. Detection of phosphorylated Ser262 in fetal tau, adult tau, and paired helical filament tau. J Biol Chem 1995;270:18917-22
44. Otvos L, Feiner L, Lang E, Szendrei GI, Goedert M, Lee VMY. Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. J Neurosci Res 1994;39:669-73
45. Hasegawa M, Jakes R, Crowther RA, Lee VMY, Ihara Y, Goedert M. Characterization of Mab AP422, a novel phosphorylation-dependent monoclonal antibody against tau protein. FEBS Lett 1996;384:25-30
46. Carmel G, Mager EM, Binder LI, Kuret J. The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J Biol Chem 1996;277:32789-95
47. Sergeant N, David JP, Goedert M, et al. Two-dimensional characterization of paired helical filament-tau from Alzheimer's disease: Demonstration of an additional 74-kDa component and age-related biochemical modifications. J Neurochem 1997;69:834-44
48. Szendrei GI, Lee VMY, Otvos L. Recognition of the minimal epitope of monoclonal antibody Tau-1 depends upon the presence of a phosphate group but not its location. J Neurosci 1993;34:243-49
49. Madisen L, Hoar DI, Holroyd CD, Crisp M, Hodes ME. DNA banking: The effect of storage of blood and isolated DNA on the integrity of DNA. Am J Med Genet 1987;27:379-90
50. Young K, Jones CK, Piccardo P, et al. Gerstmann-Sträussler-Scheinker disease with mutation at codon 102 and methionine at codon 129 of PRNP in previously unreported patients. Neurology 1995;45:1127-34
51. Baker M, Litvan I, Houlden H, et al. Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Hum Mol Genet 1999;8:711-15
52. Crowther, RA. Straight and paired helical filaments in Alzheimer disease have a common structural unit. Proc Natl Acad Sci USA 1992;88:2288-92
53. Hasegawa M, Crowther RA, Jakes R, Goedert M. Alzheimer-like changes in microtubule-associated protein tau induced by sulfated glycosaminoglycans. Inhibition of microtubule binding, stimulation of phosphorylation and filament assembly depend on the degree of sulfation. J Biol Chem 1997;272:33118-24
54. Folstein MF, Folstein SE, McHugh PR. Mini-Mental State: A practical method for grading the cognitive state of patients for the clinician. J Psychiat Res 1975;12:189-98
55. Wechsler D. Manual for the Wechsler Adult Intelligence Scale. New York: Psychological Corporation, 1955.
56. Buschke H, Fuld PA. Evaluating storage, retention and retrieval in disordered memory and learning. Neurology 1974;24:1019-25
57. Osterrieth PA. Le test de copie d'une figure complexe. Arch Psychol 1944;30:286-356
58. Benton AL, Hamsher KD, Varney NR, Spreen O. Contributions to neuropsychological assessment. New York: Oxford University Press, 1983
59. Conrad C, Andreadis A, Trojanowski JQ, et al. Genetic evidence of the involvement of tau in progressive supranuclear palsy. Ann Neurol 1997;41:277-81
60. Fuster JM. The prefrontal cortex: Anatomy, physiology and neuropsychology of the frontal lobe. New York: Raven Press, 1989
61. Pick A. Über die Beziehungen der senilen Hirnatrophie zur Aphasie. Prager Med Wochenschr 1892;16:765-67
62. Pick A. Zur Symptomatologie der linksseitigen Schläfenlappenatrophie. Monatsschr Psychiat Neurol 1904;16:378-88
63. Binetti G, Growdon JH, Vonsattel J-PG. Pick's Disease. In: Growdon JH, Rossor MN, eds. The dementias. Boston: Butterworth Heinemann, 1998:7-44
64. Pietrini P, Alexander GE, Furey ML, Guazzelli M. The neurometabolic landscape of cognitive decline: In vivo studies with positron emission tomography in Alzheimer's disease. Int J Psychophysiol (in press)
65. Schenk VWD. Re-examination of a family with Pick's disease. Ann Hum Genet 1959;23:325-33
66. Groen JJ, Endtz LJ. Hereditary Pick's disease. Second re-examination of a large family and discussion of other hereditary cases, with particular reference to electroencephalography and computerized tomography. Brain 1982;105:443-59
67. Heutink P, Stevens M, Rizzu P, et al. Hereditary fronto-temporal dementia is linked to chromosome 17q21-22: A genetic and clinico-pathological study of three Dutch families. Ann Neurol 1997;41:150-59
68. Spillantini MG, Crowther RA, Kamphorst W, Heutink P, van Swieten JC. Tau pathology in two Dutch families with mutations in the microtubule-binding region of tau. Am J Pathol 1998;153:1359-63
69. Alzheimer A: Über eigenartige Krankheitsfälle des späteren Alters. Z Neurol Psychiat 1911;4:356-85
70. Probst A, Tolnay M, Langui D, Goedert M, Spillantini MG. Pick's disease: Hyperphosphorylated tau protein segregates to the somatoaxonal compartment. Acta Neuropathol 1996;92:588-96
71. Delacourte A, Sergeant N, Wattez A, Gauvreau D, Robitaille Y. Vulnerable neuronal subsets in Alzheimer's and Pick's disease are distinguished by their tau isoform distribution and phosphorylation. Ann Neurol 1998;43:193-204
72. Murayama S, Mori H, Ihara Y, Tomonaga M. Immunocytochemical and ultrastructural studies of Pick's disease. Ann Neurol 1990;27: 394-404
73. Delacourte A, Robitaille Y, Sergeant N, et al. Specific pathological tau protein variants characterize Pick's disease. J Neuropathol Exp Neurol 1996;55:159-68
74. Sergeant N, David JP, Lefranc D, Vermersch P, Wattez A, Delacourte A. Different distribution of phosphorylated tau protein isoforms in Alzheimer's and Pick's disease. FEBS Lett 1997;412: 578-82
75. Shibayama H, Kitoh J, Marui Y, et al. An unusual case of Pick's disease. Acta Neuropathol 1983;59:79-87
76. Munoz-Garcia D, Ludwin SK. Classic and generalized variants of Pick's disease: A clinico-pathological, ultrastructural and immunocytochemical comparative study. Ann Neurol 1984;16:467-80
77. Kato S, Nakamura H. Presence of two different fibril subtypes in the Pick body: An immunoelectron microscopic study. Acta Neuropathol 1990;81:125-29