Journal of the Neurological Sciences
Volume 208, Issue 1 , Pages 17-24 , 15 April 2003

Association of phosphorylation site of tau protein with neuronal apoptosis in Alzheimer's disease

  • Katsuji Kobayashi

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +81-76-265-2301; fax: +81-76-234-4254.
    • Department of Psychiatry and Neurobiology, Graduate School of Medical Sciences, Kanazawa University, 13-1, Takara-machi, Kanazawa, Ishikawa 920-8641, Japan
    • ,
  • Hiroyuki Nakano

      Affiliations

    • Department of Psychiatry and Neurobiology, Graduate School of Medical Sciences, Kanazawa University, 13-1, Takara-machi, Kanazawa, Ishikawa 920-8641, Japan
    • ,
  • Masahiro Hayashi

      Affiliations

    • National Sanatorium Hokuriku Hospital, Nobusue, Jouhana-machi, Toyama, Japan
    • ,
  • Masao Shimazaki

      Affiliations

    • Department of Psychiatry and Neurobiology, Graduate School of Medical Sciences, Kanazawa University, 13-1, Takara-machi, Kanazawa, Ishikawa 920-8641, Japan
    • ,
  • Yuken Fukutani

      Affiliations

    • Department of Psychiatry, Fukui Medical University, Matsuoka-tyou, Fukui, Japan
    • ,
  • Kazuo Sasaki

      Affiliations

    • Department of Psychiatry, Fukui Medical University, Matsuoka-tyou, Fukui, Japan
    • ,
  • Kaoru Sugimori

      Affiliations

    • Department of Psychiatry and Neurobiology, Graduate School of Medical Sciences, Kanazawa University, 13-1, Takara-machi, Kanazawa, Ishikawa 920-8641, Japan
    • ,
  • Yoshifumi Koshino

      Affiliations

    • Department of Psychiatry and Neurobiology, Graduate School of Medical Sciences, Kanazawa University, 13-1, Takara-machi, Kanazawa, Ishikawa 920-8641, Japan

Received 17 June 2002 ,Revised 16 October 2002 ,Accepted 16 October 2002.

References 

  1. Su JH, Anderson JA, Cummings BJ, Cotman CW. Immunohistochemical evidence of apoptosis in Alzheimer's disease. Neuroreport. 1994;5:2529–2533
  2. Cotman CW, Anderson AJ. A potential role for apoptosis in neurodegeneration and Alzheimer's disease. Mol. Neurobiol. 1995;10:10–45
  3. Lassmann H, Bancher C, Breitschopf H, Wegiel J, Bobinski M, Jellinger KA, et al.  Cell death in Alzheimer's disease evaluated by DNA fragmentation in situ. Acta Neuropathol. (Berl). 1995;89:35–41
  4. Cotman CW, Su JH. Mechanisms of neuronal death in Alzheimer's disease. Brain Pathol. 1996;6:493–506
  5. Smale G, Nichols NR, Brady DR, Finch CE, Horton WE. Evidence for apoptotic cell death in Alzheimer's disease. Exp. Neurol. 1995;133:225–230
  6. Troncoso JC, Sukhov RR, Kawas CH, Koliatsos VE. In situ labeling of dying cortical neurons in normal ageing and Alzheimer's disease: correlations with senile plaques and disease progression. J. Neuropathol. Exp. Neurol. 1996;55:1134–1142
  7. Lucassen PJ, Chung WC, Kamphorst W, Swaab DF. DNA damage distribution in the human brain as shown by in situ end labeling; area-specific differences in ageing and Alzheimer's disease in the absence of apoptotic morphology. J. Neuropathol. Exp. Neurol. 1997;56:887–900
  8. Li WP, Chan WY, Lai HWL, Yew DT. Terminal dUTP nick end labeling (TUNEL) positive cells in the different regions of the brain in normal aging and Alzheimer patients. J. Mol. Neurosci. 1997;8:75–82
  9. Sugaya K, Reeves M, McKinney M. Topographic associations between DNA fragmentation and Alzheimer's disease neuropathology in the hippocampus. Neurochem. Int. 1997;31:275–281
  10. Sheng JG, Mrak RE, Griffin WST. Progressive neuronal DNA damage associated with neurofibrillary tangle formation in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 1998;57:323–328
  11. Sheng JG, Xue QZ, Mrak RE, Griffin WST. Progressive neuronal injury associated with amyloid plaque formation in Alzheimer disease. J. Neuropathol. Exp. Neurol. 1998;57:714–717
  12. Jellinger KA, Bancher C. Neuropathology of Alzheimer's disease: a critical update. J. Neural. Transm. 1998;54:77–95 [Supplement]
  13. Stadelmann C, Bruck W, Bancher C, Jellinger KA, Lassmann H. Alzheimer's disease: DNA fragmentation indicates increased neuronal vulnerability, but not apoptosis. J. Neuropathol. Exp. Neurol. 1998;57:456–464
  14. Selkoe DJ. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature. 1999;399:A23–A31 [Supplement]
  15. Behl C. Apoptosis and Alzheimer's disease. J. Neural. Transm. 2000;107:1325–1344
  16. Ferrer I, Blanco R, Carmona M, Ribera R, Goutan E, Puig B, et al.  Phosphorylated MAP kinase (ERK1, ERK2) expression is associated with early tau deposition in neurons and glial cells, but not with increased nuclear DNA vulnerability and cell death, in Alzheimer disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Brain Pathol. 2001;11:144–158
  17. Ferrer I, Puig B, Krupinsk J, Carmona M, Blanco R. Fas and Fas ligand expression in Alzheimer's disease. Acta Neuropathol. (Berl). 2001;102:121–131
  18. Broe M, Schepherd CE, Milward EA, Halliday GM. Relationship between DNA fragmentation, morphological changes and neuronal loss in Alzheimer's disease and dementia with Lewy bodies. Acta Neuropathol. (Berl). 2001;101:616–624
  19. Ugolini G, Cattaneo A, Novak M. Co-localization of truncated tau and DNA fragmentation in Alzheimer's disease neurons. Neuroreport. 1997;8:3709–3712
  20. Nagy Z, Esiri MM. Apoptosis-related protein expression in the hippocampus in Alzheimer's disease. Neurobiol. Aging. 1997;18:565–571
  21. Giannakopoulos P, Kovari E, Savioz A, De Bilbao F, Dubois-Dauphin M, Hof PR, et al.  Differential distribution of presenilin-1, Bax, and Bcl-Xl in Alzheimer's disease and frontotemporal dementia. Acta Neuropathol. (Berl). 1999;98:141–149
  22. Shirley BS, Johnson GV. Tau and HMW tau phosphorylation and compartmentalization in apoptotic neuronal PC12 cells. J. Neurosci. Res. 2001;66:203–213
  23. Mookherjee P, Johnson GV. Tau phosphorylation during apoptosis of human SH-SY5Y neuroblastoma cells. Brain Res. 2001;921:31–43
  24. Raina AK, Hochman A, Zhu X, Rottkamp CA, Numomura A, Siedlak SL, et al.  Abortive apoptosis in Alzheimer's disease. Acta Neuropathol. (Berl). 2001;101:305–310
  25. Kobayashi K, Hayashi M, Nakano H, Fukutani Y, Sasaki K, Shimazaki M, et al.  Apoptosis of astrocytes with enhanced lysosomal activity and oligodendrocytes in white matter lesions in Alzheimer's disease. Neuropathol. Appl. Neurobiol. 2002;28:238–251
  26. Bancher C, Brunner C, Lassmann H, Budka H, Jellinger K, Wiche G, et al.  Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res. 1989;477:90–99
  27. Braak E, Braak H, Mandelkow EM. A sequence of cytoskeletal changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol. (Berl). 1994;87:554–567
  28. Uchihara T, Nakamura A, Yamazaki M, Mori O. Evolution from pretangle neurons to neurofibrillary tangles monitored by thiazin red combined with Gallyas method and double immunofluorescence. Acta Neuropathol. (Berl). 2001;101:535–539
  29. Kimura T, Ono T, Takamatsu J, Yamamoto H, Ikegami K, Kondo A, et al.  Sequential changes of tau-site-specific phosphorylation during development of paired helical filaments. Dementia. 1996;7:177–181
  30. Su JH, Cummings BJ, Cotman CW. Early phosphorylation of tau in Alzheimer's disease occurs at Ser-202 and is preferentially located within neurites. Neuroreport. 1994;5:2358–2362
  31. Mercken M, Vandermeeren M, Lübke U, Six J, Boons J, Van de Voorde A, et al.  Monoclonal antibodies with selective specificity for Alzheimer tau are directed against phosphatase-sensitive epitopes. Acta Neuropathol. (Berl). 1992;84:265–272
  32. Szendrei GI, Lee VM-Y, 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. Res. 1993;34:243–249
  33. Papasozomenos SC. Tau protein immunoreactivity in dementia of the Alzheimer type: II. Electron microscopy and pathogenetic implications. Effects of fixation on the morphology of the Alzheimer's abnormal filaments. Lab. Invest. 1989;60:375–389
  34. Dickson DW, Ksiezak-Reding H, Liu WK, Davies P, Crowe A, Yen SH. 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). 1992;84:596–605
  35. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, et al.  participating CERAD neuropathologists   The Consortium to Establish a Registry for Alzheimer's disease (CERAD): Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology. 1991;41:479–486
  36. Khachaturian ZS. Diagnosis of Alzheimer's disease. Arch. Neurol. 1985;42:1097–1105
  37. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. (Berl). 1991;82:239–259
  38. Anderson AJ, Stoltzner S, Lai F, Su J, Nixon RA. Morphological and biochemical assessment of DNA damage and apoptosis in Down syndrome and Alzheimer disease, and effect of postmortem tissue archival on TUNEL. Neurobiol. Aging. 2000;21:511–524
  39. Busciglio J, Lorenzo A, Yeh J, Yankner BA. β-Amyloid fibrils induces tau phosphorylation and loss of microtubule binding. Neuron. 1995;14:879–888
  40. de la Monte SM, Carlson RI, Brown NV, Wands JR. Profiles of neuronal threads protein expression in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 1996;55:1038–1050
  41. de la Monte SM, Wands JR. Alzheimer-associated neuronal threads protein-induced apoptosis and impaired mitochondrial function in human central nervous system-derived neuronal cells. J. Neuropathol. Exp. Neurol. 2001;60:195–207

PII: S0022-510X(02)00410-0

doi: 10.1016/S0022-510X(02)00410-0

Journal of the Neurological Sciences
Volume 208, Issue 1 , Pages 17-24 , 15 April 2003

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