Acta Neuropathologica

, Volume 106, Issue 3, pp 251–260 | Cite as

4-repeat tauopathy sharing pathological and biochemical features of corticobasal degeneration and progressive supranuclear palsy

  • Omi Katsuse
  • Eizo Iseki
  • Tetsuaki Arai
  • Haruhiko Akiyama
  • Takashi Togo
  • Hirotake Uchikado
  • Masanori Kato
  • Rohan de Silva
  • Andrew Lees
  • Kenji Kosaka
Regular Paper

Abstract

We report a 67-year-old man with 4-repeat (4R) tauopathy sharing both features of corticobasal degeneration (CBD) and progressive supranuclear palsy (PSP). Although CBD and PSP have a common pathological feature that 4R tau accumulates in neurons and glia, recent pathological studies have confirmed differences between the two disorders. Clinical features of the present case were asymmetrical apraxia, parkinsonism, memory disturbance, disorientation and left limb myoclonus with a 5-year history. Pathological features were the widespread occurrence of 4R tau-positive structures including pre-tangles, neurofibrillary tangles, astrocytic plaques, tufted astrocytes, coiled bodies and argyrophilic threads. Biochemically, immunoblotting of insoluble tau demonstrated the low molecular fragments of 37 kDa and 33 kDa observed in typical CBD and PSP, respectively, in addition to the presence of 4R tau isoforms. The present case shared tau-related pathological and biochemical features of CBD and PSP. These findings support that CBD and PSP are closely associated disorders having a pathogenesis common to 4R tauopathy.

Keywords

4-repeat tauopathy Corticobasal degeneration Progressive supranuclear palsy Astrocytic plaque Tufted astrocyte 

References

  1. 1.
    Arai T, Ikeda K, Akiyama H, Tsuchiya K, Yagishita S, Takamatsu J (2001) Intracellular processing of aggregated tau differs between corticobasal degeneration and progressive supranuclear palsy. NeuroReport 12:935–938PubMedGoogle Scholar
  2. 2.
    Arai T, Ikeda K, Akiyama H, Shikamoto Y, Tsuchiya K, Yagishita S, Beach T, Rogers J, Schwab C, McGeer PL (2001) Distinct isoforms of tau aggregated in neurons and glial cells in brains of patients with Pick's disease, corticobasal degeneration and progressive supranuclear palsy. Acta Neuropathol 101:167–173PubMedGoogle Scholar
  3. 3.
    Arima K, Nakamura M, Sunohara N, Ogawa M, Anno M, Izumiyama Y, Hirai S, Ikeda K (1997) Ultrastructural characterization of the tau-immunoreactive tubules in the oligodendroglial perikarya and their inner loop processes in progressive supranuclear palsy. Acta Neuropathol 93:558–566CrossRefPubMedGoogle Scholar
  4. 4.
    Bancher C, Brunner C, Lassmann H, Budka H, Jellinger K, Wiche G, Seitelberger F, Grundke-Iqbal I, Iqbal K, Wisniewski HM (1989) Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res 477:90–99PubMedGoogle Scholar
  5. 5.
    Buee L, Delacourte A (1999) Comparative biochemistry of tau in progressive supranuclear palsy, corticobasal degeneration, FTDP-17 and Pick's disease. Brain Pathol 9:681–693PubMedGoogle Scholar
  6. 6.
    Collins SJ, Ahlskog JE, Parisi JE, Maraganore DM (1995) Progressive supranuclear palsy: neuropathologically based diagnostic clinical criteria. J Neurol Neurosurg Psychiatry 58:167–173PubMedGoogle Scholar
  7. 7.
    De Silva R, Lashley T, Gibb G, Hanger D, Hope A, Reid A, Bandopadhyay R, Utton M, Strand C, Jowett T, Khan N, Anderton B, Wood N, Holton J, Revesz T, Lees A (2003) Pathological inclusion bodies in tauopathies contain distinct complements of tau with three or four microtubule-binding repeat domains as demonstrated by new specific monoclonal antibodies. Neuropathol Appl Neurobiol (in press)Google Scholar
  8. 8.
    Delacourte A, Sergeant N, Wattez A, Gauvreau D, Robitaille Y (1998) Vulnerable neuronal subsets in Alzheimer's and Pick's disease are distinguished by their tau isoform distribution and phosphorylation. Ann Neurol 43:193–204PubMedGoogle Scholar
  9. 9.
    Di Maria E, Tabaton M, Vigo T, Abbruzzese G, Bellone E, Donati C, Frasson E, Marchese R, Montagna P, Munoz DG, Pramstaller PP, Zanusso G, Ajmar F, Mandich P (2000) Corticobasal degeneration shares a common genetic background with progressive supranuclear palsy. Ann Neurol 47:374–377PubMedGoogle Scholar
  10. 10.
    Dickson DW (1999) Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration. J Neurol 246:6–15CrossRefPubMedGoogle Scholar
  11. 11.
    Dickson DW, Bergeron C, Chin SS, Duyckaerts C, Horoupian D, Ikeda K, Jellinger K, Lantos PL, Lippa CF, Mirra SS, Tabaton M, Vonsattel JP, Wakabayashi K, Litvan I (2002) Office of Rare Diseases neuropathologic criteria for corticobasal degeneration. J Neuropathol Exp Neurol 61:935–946PubMedGoogle Scholar
  12. 12.
    Goedert M, Spillantini MG, Cairns NJ, Crowther RA (1992) Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8:159–168PubMedGoogle Scholar
  13. 13.
    Hauw JJ, Verny M, Delaere P, Cervera P, He Y, Duyckaerts C (1990) Constant neurofibrillary changes in the neocortex in progressive supranuclear palsy. Basic differences with Alzheimer's disease and aging. Neurosci Lett 119:182–186PubMedGoogle Scholar
  14. 14.
    Hauw JJ, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL, McKee A, Tabaton M, Litvan I (1994) Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 44:2015–2019PubMedGoogle Scholar
  15. 15.
    Houlden H, Baker M, Morris HR, MacDonald N, Pickering-Brown S, Adamson J, Lees AJ, Rossor MN, Quinn NP, Kertesz A, Khan MN, Hardy J, Lantos PL, St George-Hyslop P, Munoz DG, Mann D, Lang AE, Bergeron C, Bigio EH, Litvan I, Bhatia KP, Dickson D, Wood NW, Hutton M (2001) Corticobasal degeneration and progressive supranuclear palsy share a common tau haplotype. Neurology 56:1702–1706PubMedGoogle Scholar
  16. 16.
    Ikeda K, Akiyama H, Haga C, Kondo H, Arima K, Oda T (1994) Argyrophilic thread-like structure in corticobasal degeneration and supranuclear palsy. Neurosci Lett 174:157–159PubMedGoogle Scholar
  17. 17.
    Ikeda K, Akiyama H, Arai T, Nishimura T (1998) Glial tau pathology in neurodegenerative diseases: their nature and comparison with neuronal tangles. Neurobiol Aging 19:S85–91CrossRefPubMedGoogle Scholar
  18. 18.
    Iseki E, Li F, Kosaka K, Nishimura T, Akiyama H, Ikeda K, Kato M (1997) Tau-immunohistochemical and -immunoelectron microscopical investigation of astrocytic plaques in progressive supranuclear palsy. Biomed Res 18:145–148Google Scholar
  19. 19.
    Iseki E, Togo T, Suzuki K, Katsuse O, Marui W, Silva R de, Lees A, Yamamoto T, Kosaka K (2003) Dementia with Lewy bodies from the perspective of tauopathy. Acta Neuropathol 105:265–270PubMedGoogle Scholar
  20. 20.
    Komori T, Arai N, Oda M, Nakayama H, Mori H, Yagishita S, Takahashi T, Amano N, Murayama S, Murakami S, Shibata N, Kobayashi M, Sasaki S, Iwata M (1998) Astrocytic plaques and tufts of abnormal fibers do not coexist in corticobasal degeneration and progressive supranuclear palsy. Acta Neuropathol 96:401–408CrossRefPubMedGoogle Scholar
  21. 21.
    Lang AE, Riley DE, Bergeron C (1994) Cortical-basal ganglionic degeneration. In: Calne DB (ed) Neurodegenerative disease. Saunders, Philadelphia, pp 877–894Google Scholar
  22. 22.
    Li F, Iseki E, Kosaka K, Ikeda K (1998) Immunohistochemical and immunoelectron microscopical investigation of tau-positive neurons lacking tangle-formation in progressive supranuclear palsy. Biomed Res 19:145–149Google Scholar
  23. 23.
    Li F, Iseki E, Odawara T, Kosaka K, Yagishita S, Amano N (1998) Regional quantitative analysis of tau-positive neurons in progressive supranuclear palsy: comparison with Alzheimer's disease. J Neurol Sci 159:73–81CrossRefPubMedGoogle Scholar
  24. 24.
    Litvan I, Agid Y, Jankovic J, Goetz C, Brandel JP, Lai EC, Wenning G, D'Olhaberriague L, Verny M, Chaudhuri KR, McKee A, Jellinger K, Bartko JJ, Mangone CA, Pearce RK (1996) Accuracy of clinical criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Neurology 46:922–930PubMedGoogle Scholar
  25. 25.
    Litvan I, Agid Y, Goetz C, Jankovic J, Wenning GK, Brandel JP, Lai EC, Verny M, Ray-Chaudhuri K, McKee A, Jellinger K, Pearce RK, Bartko JJ (1997) Accuracy of the clinical diagnosis of corticobasal degeneration: a clinicopathologic study. Neurology 48:119–125PubMedGoogle Scholar
  26. 26.
    Litvan I, Grimes DA, Lang AE, Jankovic J, McKee A, Verny M, Jellinger K, Chaudhuri KR, Pearce RK (1999) Clinical features differentiating patients with postmortem confirmed progressive supranuclear palsy and corticobasal degeneration. J Neurol 246:1–5CrossRefGoogle Scholar
  27. 27.
    Mizusawa H, Yen S-H, Hirano A, Llena JF (1989) Pathology of the dentate nucleus in progressive supranuclear palsy: a histological, immunohistochemical and ultrastructural study. Acta Neuropathol 78:419–428PubMedGoogle Scholar
  28. 28.
    Nishimura M, Namba Y, Ikeda K, Oda M (1992) Glial fibrillary tangles with straight tubules in the brains of patients with progressive supranuclear palsy. Neurosci Lett 143:35–38CrossRefPubMedGoogle Scholar
  29. 29.
    Nishimura M, Tomimoto H, Suenaga T, Namba Y, Ikeda K, Akiguchi I, Kimura J (1995) Immunocytochemical characterization of glial fibrillary tangles in Alzheimer's disease brain. Am J Pathol 146:1052–1058PubMedGoogle Scholar
  30. 30.
    Otvos L Jr, Feiner L, Lang E, Szendrei GI, Goedert M, Lee VM (1994) Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. J Neurosci Res 39:669–673PubMedGoogle Scholar
  31. 31.
    Rebeiz JJ, Kolodny EH, Richardson EP Jr (1967) Corticodentatonigral degeneration with neuronal achromasia: a progressive disorder of late adult life. Trans Am Neurol Assoc 92:23–26PubMedGoogle Scholar
  32. 32.
    Sergeant N, David JP, Goedert M, Jakes R, Vermersch P, Buee L, Lefranc D, Wattez A, Delacourte A (1997) 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 69:834–844PubMedGoogle Scholar
  33. 33.
    Sergeant N, Wattez A, Delacourte A (1999) Neurofibrillary degeneration in progressive supranuclear palsy and corticobasal degeneration: tau pathologies with exclusively "exon 10" isoforms. J Neurochem 72:1243–1249CrossRefPubMedGoogle Scholar
  34. 34.
    Steele JC, Richardson JC, Olszewski J (1964) Progressive supranuclear palsy. Arch Neurol10:333–359Google Scholar
  35. 35.
    Tellez-Nagel I, Wisniewski HM (1973) Ultrastructure of neurofibrillary tangles in Steele-Richardson-Olszewski syndrome. Arch Neurol 29:324–327PubMedGoogle Scholar
  36. 36.
    Togo T, Dickson DW (2002) Ballooned neurons in progressive supranuclear palsy are usually due to concurrent argyrophilic grain disease. Acta Neuropathol 104:53–56CrossRefPubMedGoogle Scholar
  37. 37.
    Togo T, Sahara N, Yen SH, Cookson N, Ishizawa T, Hutton M, Silva R de, Lees A, Dickson DW (2002) Argyrophilic grain disease is a sporadic 4-repeat tauopathy. J Neuropathol Exp Neurol 61:547–556PubMedGoogle Scholar
  38. 38.
    Verny M, Duyckaerts C, Agid Y, Hauw JJ (1996) The significance of cortical pathology in progressive supranuclear palsy. Clinico-pathological data in 10 cases. Brain 119:1123–1136PubMedGoogle Scholar
  39. 39.
    Yamada T, McGeer PL, McGeer EG (1992) Appearance of paired nucleated, Tau-positive glia in patients with progressive supranuclear palsy brain tissue. Neurosci Lett 135:99–102PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Omi Katsuse
    • 1
  • Eizo Iseki
    • 1
  • Tetsuaki Arai
    • 2
  • Haruhiko Akiyama
    • 2
  • Takashi Togo
    • 1
  • Hirotake Uchikado
    • 1
  • Masanori Kato
    • 3
  • Rohan de Silva
    • 4
  • Andrew Lees
    • 4
  • Kenji Kosaka
    • 1
  1. 1.Department of PsychiatryYokohama City University School of MedicineYokohamaJapan
  2. 2.Department of PsychogeriatricsTokyo Institute of PsychiatryTokyoJapan
  3. 3.Soga HospitalOdawaraJapan
  4. 4.Reta Lila Weston Institute of Neurological StudiesUniversity College LondonLondonUK

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