Book contents
- Frontmatter
- Contents
- List of contributors
- Preface
- Part I Genes and behaviour
- Part II Brain development
- Part III New ways of imaging the brain
- Part VI Imaging the normal and abnormal mind
- Part V Consciousness and will
- Part IV Recent advances in dementia
- 12 The neurobiology of the tauopathies
- 13 Advances in early diagnosis and differentiation of the dementias
- Part VII Affective illness
- Part VIII Aggression
- Part IX Drug use and abuse
- Index
- Plate section
- References
12 - The neurobiology of the tauopathies
from Part IV - Recent advances in dementia
Published online by Cambridge University Press: 19 January 2010
Book contents
- Frontmatter
- Contents
- List of contributors
- Preface
- Part I Genes and behaviour
- Part II Brain development
- Part III New ways of imaging the brain
- Part VI Imaging the normal and abnormal mind
- Part V Consciousness and will
- Part IV Recent advances in dementia
- 12 The neurobiology of the tauopathies
- 13 Advances in early diagnosis and differentiation of the dementias
- Part VII Affective illness
- Part VIII Aggression
- Part IX Drug use and abuse
- Index
- Plate section
- References
Summary
Introduction
Current concepts of neurodegenerative diseases began to develop over a century ago, when the German school of neuropathologists described the salient histological features of what we now know to be the most common of these diseases. In 1907, Alois Alzheimer described the neuritic plaques and neurofibrillary lesions in the disease that was subsequently named after him (Alzheimer 1907). In 1911, Alzheimer also described the presence of Pick bodies as the characteristic neuropathological lesion of Pick's disease, a form of frontotemporal dementia (Alzheimer 1911). In 1912, Friederich Lewy described the inclusions characteristic of Parkinson's disease, the so-called ‘Lewy bodies’ (Lewy 1912). In the 1960s, electron microscopy was used to show that the above inclusions are made of abnormal filaments (Kidd 1963; Duffy and Tennyson 1965; Rewcastle and Ball 1968). At the time, the identification of these lesions was instrumental in establishing the various diseases as discrete entities. However, this work did not indicate a role for the lesions in the aetiology and pathogenesis of neurodegeneration. Over the past 20 years, a direct correspondence between the formation of the neuropathological lesions and the degenerative process has emerged. Besides the above diseases, this is also true of the prion diseases, of Huntington's disease and the other glutamine repeat diseases, as well as of several other, rarer conditions.
Progress was made possible by the merging of two independent lines of research. On the one hand, the biochemical study of the neuropathological lesions led to the identification of their main molecular components.
- Type
- Chapter
- Information
- Disorders of Brain and Mind , pp. 245 - 261Publisher: Cambridge University PressPrint publication year: 2003
References
, , et al. (2000). Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc Natl Acad Sci USA, 97, 2910–915Google Scholar
(1907). Über eine eigenartige Erkrankung der Hirnrinde. Allg Z Psychiatrie psychiatrisch-gerichtliche Med, 64, 146–8Google Scholar
(1911). Über eigenartige Krankheitsfälle des späteren Alters. Z Neurol Psychiatrie, 4, 356–85Google Scholar
, and (1992). Structure and novel exons of the human tau gene. Biochemistry, 31, 10626–33Google Scholar
, , et al. (1999). Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Hum Mol Genet, 8, 711–15Google Scholar
, , et al. (2000). No association between TAU haplotype and Alzheimer's disease in population or clinic based series or in familial disease. Neurosci Lett, 285, 147–9Google Scholar
, , et al. (2000). Structure, microtubule interactions, and paired helical filament aggregation by tau mutants of frontotemporal dementias. Biochemistry, 39, 11714–21Google Scholar
, and (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, 255–70Google Scholar
, , et al. (1999). Frontotemporal dementia and corticobasal degeneration in a family with a P301S mutation in tau. J Neuropathol Exp Neurol, 58, 667–77Google Scholar
, , , , and (2000). Alzheimer-like neurodegeneration in aged anti-nerve growth factor transgenic mice. Proc Natl Acad Sci USA, 97, 6826–31Google Scholar
, , 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, 13103–7Google Scholar
, , et al. (1997). Genetic evidence for the involvement of tau in progressive supranuclear palsy. Ann Neurol, 41, 277–81Google Scholar
and (2000). Abnormal tau-containing filaments in neurodegenerative diseases. J Struct Biol, 130, 271–9Google Scholar
, , et al. (1999). Mutations in tau reduce its microtubule binding properties in intact cells and affect its phosphorylation. FEBS Lett 446, 228–32Google Scholar
, , et al. (2000). Missense tau mutations identified in FTDP-17 have a small effect on tau-microtubule interactions. Brain Res, 853, 5–14Google Scholar
, , et al. (2000). Corticobasal degeneration shares a common genetic background with progressive supranuclear palsy. Ann Neurol, 47, 374–7Google Scholar
and (2000). Determinants of 4-repeat tau expression. Coordination between enhancing and inhibitory splicing sequences for exon 10 inclusion. J Biol Chem, 275, 17700–9Google Scholar
, , et al. (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, 5598–603Google Scholar
and (1965). Phase and electron microscopic observations of Lewy bodies and melanin granules in the substantia nigra and locus coeruleus in Parkinson's disease. J Neuropathol Exp Neurol, 24, 398–414Google Scholar
, and (1996). Neuropathologic overlap of progressive supranuclear palsy, Pick's disease and corticobasal degeneration. J Neuropathol Exp Neurol, 55, 53–67Google Scholar
, , , and (1991). Abnormal tau proteins in progressive supranuclear palsy. Similarities and differences with the neurofibrillary degeneration of the Alzheimer type. Acta Neuropathol, 81, 591–6Google Scholar
, , et al. (1997). Frontotemporal dementia and parkinsonism linked to chromosome 17: a consensus statement. Ann Neurol, 41, 706–15Google Scholar
, , et al. (2000). In vitro polymerization of tau protein monitored by laser light scattering: method and application to the study of FTDP-17 mutants. Biochemistry, 39, 6136–44Google Scholar
, , , , and (2000). Complex regulation of tau exon 10, whose missplicing causes frontotemporal dementia. J Neurochem, 74, 490–500Google Scholar
and (1990). Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J, 9, 4225–30Google Scholar
, , , and (1988). Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease. Proc Natl Acad Sci USA, 85, 4051–5Google Scholar
, , , and (1989 a). Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron, 3, 519–26Google Scholar
, , , and (1989 b). 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, 8, 393–9Google Scholar
, , and (1992 a). MAP kinase phosphorylation sites in microtubule-associated protein tau are dephosphorylated by protein phosphatase 2A1. Implications for Alzheimer's disease. FEBS Lett, 312, 95–9Google Scholar
, , and (1992 b). Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron, 8, 159–68Google Scholar
, and (1999 a). Effects of frontotemporal dementia FTDP-17 mutations on heparin-induced assembly of tau filaments. FEBS Lett, 450, 306–11Google Scholar
, , et al. (1999 b). Tau gene mutation in familial progressive subcortical gliosis. Nat Med, 5, 454–7Google Scholar
, , , , , and (2000). Reduced binding of protein phosphatase 2A to tau protein with frontotemporal dementia and parkinsonism linked to chromosome 17 mutations. J Neurochem, 75, 2155–62Google Scholar
and (1994). Identification of a novel microtubule binding and assembly domain in the developmentally regulated interrepeat region of tau. J Cell Biol, 124, 769–82Google Scholar
, , , , , and (1995). Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice overexpressing the longest human brain tau isoform. EMBO J, 14, 1304–13Google Scholar
, , and (2001 a). Tau filament formation in transgenic mice expressing P301L tau. J Biol Chem, 276, 529–34Google Scholar
, , and (2001 b). Formation of neurofibrillary tangles in P301L tau transgenic mice induced by Aβ42 fibrils. Science, 293, 1491–4Google Scholar
, , et al. (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, 15134–43Google Scholar
, and (1997). Tau overexpressed in identified lamprey neurons in situ is spatially segregated by phosphorylation state, forms hyperphosphorylated, dense aggregates and induces neurodegeneration. Proc Natl Acad Sci USA, 94, 4733–8Google Scholar
, , and (2000). Human tau filaments induce microtubule and synapse loss in an in vivo model of neurofibrillary degenerative disease. J Cell Sci, 113, 1373–87Google Scholar
, , et al. (2001). Regulation of alternative splicing of human tau exon 10 by phosphorylation of splicing factors. Mol Cell Neurosci, 18, 80–90Google Scholar
, and (1998). Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett, 437, 207–10Google Scholar
, , , and (1999). FTDP-17 mutations N279K and S305N in tau produce increased splicing of exon 10. FEBS Lett, 443, 93–6Google Scholar
, , et al. (1998). Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science, 282, 1914–17Google Scholar
, , et al. (2001). Corticobasal degeneration and progressive supranuclear palsy share a common tau haplotype. Neurology, 56, 1702–6Google Scholar
, , et al. (1998). Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature, 393, 702–5Google Scholar
, , et al. (1999). A distinct familial presenile dementia with a novel missense mutation in the tau gene. Neuroreport, 10, 497–501Google Scholar
, , et al. (2001). Familial frontotemporal dementia and parkinsonism with a novel N296H mutation in exon 10 of the tau gene and a widespread tau accumulation in the glial cells. Acta Neuropathol, 102, 285–92Google Scholar
, , et al. (1999). Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron, 24, 751–62Google Scholar
, , , , and (2001). Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mice. Am J Pathol, 158, 555–62Google Scholar
, , , and (2000). Aberrant splicing of tau pre-mRNA caused by intronic mutations associated with the inherited dementia frontotemporal dementia with parkinsonism linked to chromosome 17. Mol Cell Biol, 20, 4036–48Google Scholar
(1963). Paired helical filaments in electron microscopy of Alzheimer's disease. Nature, 197, 192–3Google Scholar
, , et al. (1994). Ultrastructure and biochemical composition of paired helical filaments in corticobasal degeneration. Am J Pathol, 145, 1496–508Google Scholar
, , et al. (2000). Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet, 25, 402–5Google Scholar
, , et al. (2001). Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science, 293, 1487–91Google Scholar
Lewy F (1912). Paralysis agitans. I. Pathologische Anatomie. In Handbuch der Neurologie, Vol. 3, ed. M Lewandowski and G Abelsdorff, pp. 920–33. Berlin: Springer Verlag
, , et al. (2000). Frontotemporal dementia with novel tau pathology and a Glu342Val tau mutation. Ann Neurol, 48, 850–8Google Scholar
, and (1999). Stable expression in Chinese hamster ovary cells of mutated tau genes causing frontotemporal dementia and parkinsonism linked to chromosome 17 (FTDP-17). Am J Pathol, 154, 1649–56Google Scholar
, , et al. (2001). Familial frontotemporal dementia and parkinsonism with a novel mutation at an intron 10 + 11-splice site in the tau gene. Ann Neurol, 50, 117–20Google Scholar
, , et al. (2001 a). Molecular analysis of mutant and wild-type tau deposited in the brain affected by the FTDP-17 R406W mutation. Am J Pathol, 158, 373–9Google Scholar
, , , , and (2001 b). Selective deposition of mutant tau in the FTDP-17 brain affected by the P301L mutation. J Neuropathol Exp Neurol, 60, 872–84Google Scholar
, , et al. (1999). Tau gene mutation G389R causes a tauopathy with abundant Pick body-like inclusions and axonal deposits. J Neuropathol Exp Neurol, 58, 1207–26Google Scholar
, , et al. (1999). Accelerated filament formation from tau protein with specific FTDP-17 mutations. FEBS Lett, 447, 195–9Google Scholar
, , et al. (2001). Pick's disease associated with the novel tau gene mutation K369I. Ann Neurol, 50, 503–13Google Scholar
, , et al. (2000). Significant association between the tau gene A0/A0 genotype and Parkinson's disease. Ann Neurol, 47, 242–5Google Scholar
, , et al. (2001). Familial atypical progressive supranuclear palsy associated with homozygosity for the delN296 mutation in the tau gene. Ann Neurol, 49, 263–7Google Scholar
, , et al. (1998). Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol, 43, 815–25Google Scholar
, , et al. (2000). Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathol, 99, 469–81Google Scholar
and (1968). Electron microscopic structure of the ‘inclusion bodies’ in Pick's disease. Neurology, 18, 1205–13Google Scholar
, , et al. (2000). Tau gene mutation K257T causes a tauopathy similar to Pick's disease. J Neuropathol Exp Neurol, 58, 1207–26Google Scholar
, , et al. (1999). High prevalence of mutations in the microtubule-associated protein tau in a population study of frontotemporal dementia in the Netherlands. Am J Hum Genet, 64, 414–21Google Scholar
, , et al. (2000). Mutation-dependent aggregation of tau protein and its selective depletion from the soluble fraction in brain of P301L FTDP-17 patients. Hum Mol Genet, 9, 3075–82Google Scholar
, , et al. (2002). A novel tau mutation, S320F, causes a tauopathy with inclusions similar to those in Pick's disease. Ann Neurol, 51, 373–6Google Scholar
, , et al. (2001). The extended haplotype of the microtubule associated protein tau gene is not associated with Pick's disease. Neurosci Lett, 299, 156–8Google Scholar
, and (1999). Neurofibrillary degeneration in progressive supranuclear palsy and corticobasal degeneration: tau pathologies with exclusively ‘exon 10’ isoforms. J Neurochem, 72, 1243–9Google Scholar
, and (2000). The natural osmolyte trimethylamine N-oxide (TMAO) restores the ability of mutant tau to promote microtubule assembly. FEBS Lett, 484, 265–70Google Scholar
, , et al. (1999). Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J Biol Chem, 274, 25490–8Google Scholar
, and (1996). Comparison of the neurofibrillary pathology in Alzheimer's disease and familial presenile dementia with tangles. Acta Neuropathol, 92, 42–8Google Scholar
, , , , and (1997). Familial multiple system tauopathy with presenile dementia: a disease with abundant neuronal and glial tau filaments. Proc Natl Acad Sci USA, 94, 4113–18Google Scholar
, and (1998 a). Frontotemporal dementia and parkinsonism linked to chromosome 17: a new group of tauopathies. Brain Pathol, 8, 387–402Google Scholar
, , , and (1998 b). Tau pathology in two Dutch families with mutations in the microtubule-binding region of tau. Am J Pathol 153, 1359–63Google Scholar
, , , , and (1998 c). Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci USA, 95, 7737–41Google Scholar
, , et al. (2000). A novel tau mutation (N296N) in familial dementia with swollen achromatic neurons and corticobasal inclusion bodies. Ann Neurol, 48, 939–93Google Scholar
, , et al. (1999). Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol, 155, 2153–65Google Scholar
St George-Hyslop P H, Farrer L A and Goedert M (2001). Alzheimer disease and the frontotemporal dementias: diseases with cerebral deposition of fibrillar proteins. In The Metabolic and Molecular Bases of Inherited Disease, 8th edn, ed. C R Scriver, A L Beaudet, W S Sly and D Valle, pp. 5875–99. New York: McGraw-Hill
, , et al. (2000). Progressive supranuclear palsy pathology caused by a novel silent mutation in exon 10 of the tau gene. Brain, 123, 880–93Google Scholar
, , , , and (2000). Expression of human apolipoprotein E4 in neurons causes hyperphosphorylation of protein tau in the brains of transgenic mice. Am J Pathol, 156, 951–64Google Scholar
, , et al. (1999). Phenotypic variation in hereditary frontotemporal dementia with tau mutations. Ann Neurol, 46, 617–26Google Scholar
, , et al. (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, 8229–34Google Scholar
, , and (2000). Structural basis for recognition of the RNA major groove in the tau exon 10 splicing regulatory element by aminoglycoside antibiotics. Nucleic Acids Res, 28, 710–19Google Scholar
, , et al. (2000). Distinct FTDP-17 missense mutations in tau produce tau aggregates and other pathological phenotypes in transfected CHO cells. Mol Biol Cell, 11, 4093–104Google Scholar
, , , and (1994). Localization of disinhibition-dementia-Parkinsonism-amyotrophy complex to 17q21-22. Am J Hum Genet, 55, 1159–65Google Scholar
, , et al. (2001). Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science, 293, 711–14Google Scholar
, , et al. (1999). A mutation in the microtubule-associated protein tau in pallido-nigro-luysian degeneration. Neurology, 53, 864–8Google Scholar
, , et al. (2000). A novel mutation at position +12 in the intron following exon 10 of the tau gene in familial frontotemporal dementia (FTD-Kumamoto). Ann Neurol, 47, 422–9Google Scholar