Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease: Evidence for apoptotic cell death

American Journal of Pathology

Volumn 155, Issue 5, 1999, Pages 1459-1466

  Stadelmann, Christine ^a   Deckwerth, Thomas L ^b   Srinivasan, Anu ^b   Bancher, Christian ^c   Brück, Wolfgang ^d   Jellinger, Kurt ^e   Lassmann, Hans ^a,f  

^a UNIVERSITY OF VIENNA   (Austria)

^b PFIZER INC   (United States)

^c GENERAL HOSPITAL LINZ   (Austria)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

^f Brain Research Institute   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; DNA FRAGMENT;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL GRANULE; CONTROLLED STUDY; DOWN SYNDROME; ENZYME ACTIVATION; HUMAN; HUMAN TISSUE; NERVE CELL NECROSIS; NEUROPROTECTION; PRIORITY JOURNAL;

EID: 0032747486     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)65460-0     Document Type: Article

References (73)

1. Yamatsuji T, Matsui T, Okamoto T, Komatsuzaki K, Takeda S, Fukumoto H, Iwatsubo T, Suzuki N, Asami-Odaka A, Ireland S, Kinane B, Giambarella U, Nishimoto I: G-protein-mediated neuronal DNA fragmentation induced by familial Alzheimer's disease-associated mutants of APP. Science 1996, 272:1349-1352
2. Guo Q, Sopher BL, Furukawa K, Pham DG, Robinson N, Martin GM, Mattson MP: Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid β-peptide: involvement of calcium and oxyradicals. J Neurosci 1997, 17:4212-4222
3. 2+-binding protein ALG-2 and Alzheimer's disease gene ALG-3. Science 1996, 271:521-524
4. Wolozin B, Iwasaki K, Vito P, Ganjei JK, Lacaná E, Sunderland T, Zhao B, Kusiak JW, Wasco W, D'Adamio L: Participation of presenilin 2 in apoptosis: enhanced basal activity conferred by an Alzheimer mutation. Science 1996, 274:1710-1713
5. Gschwind M, Huber G: Apoptotic cell death induced by β-amyloid 1-42 peptide is cell type dependent. J Neurochem 1995, 65:292-300
6. Li YP, Bushnell AF, Lee CM, Perlmutter LS, Wong SK: Beta-amyloid induces apoptosis in human-derived neurotypic SH-SY5Y cells. Brain Res 1996, 738:196-204
7. Busciglio J, Yankner BA: Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature 1995, 378:776-779
8. Guo Q, Fu W, Xie J, Luo H, Sells SF, Geddes JW, Bondada V, Rangnekar VM, Mattson MP: Par-4 is a mediator of neuronal degeneration associated with the pathogenesis of Alzheimer's disease. Nat Med 1998, 4:957-962
9. Su JH, Deng G, Cotman CW: Bax protein expression is increased in Alzheimer's brain: correlations with DNA damage, bcl-2 expression, and brain pathology. J Neuropathol Exp Neurol 1997, 56:86-93
10. Su JH, Satou T, Andersen AJ, Cotman CW: Up-regulation of Bcl-2 is associated with neuronal DNA damage in Alzheimer's disease. Neuroreport 1996, 7:437-440
11. Kitamura Y, Shimohama S, Kamoshima W, Matsuoka Y, Nomura Y, Taniguchi T: Changes of p53 in the brains of patients with Alzheimer's disease. Biochem Biophys Res Commun 1997, 232:418-421
12. Nishimura T, Akiyama H, Yonehara S, Kondo H, Ikeda K, Kato M, Iseki E, Kosaka K: Fas antigen expression in brains of patients with Alzheimer-type dementia. Brain Res 1995, 695:137-145
13. Kitamura Y, Shimohama S, Kamoshima W, Ota T, Matsuoka Y, Nomura Y, Smith MA, Perry G, Whitehouse PJ, Taniguchi T: Alteration of proteins regulating apoptosis, Bcl-2, Bcl-x, Bax, Bak, Bad, ICH-1 and CPP32, in Alzheimer's disease. Brain Res 1998, 780:260-269
14. Shimohama S, Tanino H, Fujimoto S: Changes in caspase expression in Alzheimer's disease: comparison with development and aging. Biochem Biophys Res Common 1999, 256:381-384
15. Dragunow M, Faull RL, Lawlor P, Beilharz EJ, Singleton K, Walker EB, Mee E: In situ evidence for DNA fragmentation in Huntington's disease striatum, and Alzheimer's disease temporal lobes. Neuroreport 1995, 6:1053-1057
16. Lassmann H, Bancher C, Breitschopf H, Wegiel J, Bobinski M, Jellinger K, Wisniewski HM: Cell death in Alzheimer's disease evaluated by DNA fragmentation in situ. Acta Neuropathol (Berl) 1995, 89: 35-41
17. Lucassen PJ, Chung WCJ, Kamphorst W, Swaab DF: DNA damage distribution in the human brain as shown by in situ end labeling; area-specific differences in aging and Alzheimer's disease in the absence of apoptotic morphology. J Neuropathol Exp Neurol 1997, 56:887-900
18. Migheli A, Cavalla P, Marino S, Schiffer D: A study of apoptosis in normal and pathologic nervous tissue after in situ end-labeling of DNA strand breaks. J Neuropathol Exp Neurol 1994, 53:606-616
19. Smale G, Nichols NR, Brady DR, Finch CE, Horton Jr WE: Evidence for apoptotic cell death in Alzheimer's disease. Exp Neurol 1995, 133:225-230
20. Stadelmann C, Bruck W, Bancher C, Jellinger K, Lassmann H: Alzheimer disease: DNA fragmentation indicates increased neuronal vulnerability, but not apoptosis. J Neuropathol Exp Neurol 1998, 5:456-464
21. Su JH, Anderson AJ, Cummings BJ, Cotman CW: Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 1994, 5:2529-2533
22. Troncoso JC, Sukhov RR, Kawas CH, Koliatsos VE: In situ labeling of dying cortical neurons in normal aging, and in Alzheimer's disease: correlations with senile plaques and disease progression J Neuropathol Exp Neurol 1996, 55:1134-1142
23. Perry G, Nunomura A, Smith MA: A suicide note from Alzheimer's disease neurons? (commentary) Nat Med 1998, 4:897-898
24. Perry G, Nunomura A, Lucassen P, Lassmann H, Smith MA: Apoptosis and Alzheimer's disease. (letter) Science 1998, 282:1268-1269
25. Srinivasan A, Roth KA, Sayers RO, Shindler KS, Wong AM, Fritz LC, Tomaselli K: In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death Differ 1998, 5:1004-1016
26. Thornberry NA, Lazebnik Y: Caspases: enemies within. Science 1998, 281:1312-1316
27. Schulz JB, Weller M, Moskowitz MA: Caspases as treatment targets in stroke and neurodegenerative diseases. Ann Neurol 1999, 45:421-429
28. Simchowicz T: Histologische Studien über die senile Demenz. Histologische und histopathologische. Arbeiten über die Grosshirnrinde 1911, 4:267-444
29. Brück Y, Brück W, Kretzschmar HA, Lassmann H: Evidence for neuronal apoptosis in pontosubicular neuron necrosis. Neuropathol Appl Neurobiol 1996, 22:23-29
30. Friede RL: Ponto-subicular lesions in perinatal anoxia. Arch Pathol 1972, 94:343-354
31. Khatchaturian ZS: Diagnosis of Alzheimer's disease. Arch Neurol 1995, 42:1097-1105
32. Mirra SS, Heyman A. McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L: The consortium to establish a registry for Alzheimer's disease (CERAD). II. Standardization of the neuropathological assessment of Alzheimer's disease. Neurology 1991, 41:479-486
33. Chenghua G, Casaccia-Bonnefil P, Srinivasan A, Chao MV: Oligodendrocyte apoptosis mediated by caspase activation. J Neurosci 1999, 19:3043-3049
34. Mercken M, Vandermeeren M, Lübke U, Six J, Boons J, Van de Voorde A, Martin J-J, Gheuens J: Monoclonal antibodies with selective specificity for Alzheimer tau are directed against phosphatase-sensitive epitopes. Acta Neuropathol (Berl) 1992, 84:265-272
35. Biernat J, Mandelkow EM, Schroter C, Lichtenberg-Kraag B, Steiner B, Berling B, Meyer H, Mercken M, Vandermeeren A, Goedert M, Mandelkow E: The switch of tau protein to an Alzheimer-like state includes the phosphorylation of two serine-proline motifs upstream of the microtubule binding region. EMBO J 1992, 11:1593-1597
36. Goedert M, Jakes R, Crowther RA, Six J, Lübke U, Vandermeeren M, Cras P, Trojanowski JQ, Lee VM-Y: The abnormal phosphorylation of tau protein at Ser-202 in Alzheimer disease recapitulates phosphorylation during development. Proc Natl Acad Sci USA 1993, 90:5066-5070
37. Sheng JG, Mrak RE, Griffin WS: Progressive neuronal DNA damage associated with neurofibrillary tangle formation in Alzheimer disease. J Neuropathol Exp Neurol 1998, 57:323-328
38. Bancher C, Brunner C, Lassmann H, Budka H, Jellinger K, Wiche G, Seitelberger F, Grundke-Iqbal I, Iqbal K, Wisniewski HM: Accumulation of abnormally phophorylated τ precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res 1989, 477:90-99
39. Braak E, Braak H, Mandelkow E-M: A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol (Berl) 1994, 87:554-567
40. Cotman CW, Su JH: Mechanisms of neuronal cell death in Alzheimer's disease. Brain Pathol 1996, 6:493-506
41. Keller JN, Guo Q, Holtsberg FW, Bruce-Keller AJ, Mattson MP: Increased sensitivity to mitochondrial toxin-induced apoptosis in neural cells expressing mutant presenilin-1 is linked to perturbed calcium homeostasis and enhanced oxyradical production. J Neurosci 1998, 18:4439-4450
42. Guo Q, Sebastian L, Sopher BL, Miller MW, Ware CB, Martin GM, Mattson MP: Increased vunerability of hippocampal neurons from presenilin-1 mutant knock-in mice to amyloid β-peptide toxicity: central roles of superoxide production and caspase activation. J Neurochem 1999, 72:1019-1029
43. Guo Q, Fu W, Sopher BL, Miller MW, Ware CB, Martin GM, Mattson MP: Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knock-in mice. Nat Med 1999, 5:101-106
44. Vito P, Ghayur T, D'Adamio L: Generation of anti-apoptotic presenilin-2 polypeptides by alternative transcription, proteolysis, and caspase-3 cleavage. J Biol Chem 1997, 272:28315-28320
45. Walter J, Schindzielorz A, Grunberg J, Haass C: Phosphorylation of presenilin-2 regulates its cleavage by caspases and retards progression of apoptosis Proc Natl Acad Sci USA 1999, 96:1391-1396
46. Vezina J, Tschopp-C, Andersen E, Muller K: Overexpression of a C-terminal fragment of presenilin 1 delays anti-Fas induced apoptosis in Jurkat cells, Neurosci Lett 1999, 263:65-68
47. Anderson AJ, Su JH, Cotman CW: DNA damage and apoptosis in Alzheimer's disease: colocalization with c-Jun immunoreactivity, relationship to brain area, and effect of postmortem delay. J Neurosci 1996, 16:1710-1719
48. Arendt T, Holzer M, Gartner U: Neuronal expression of cycline dependent kinase inhibitors of the INK4 family in Alzheimer's disease. J Neural Transm 1998, 105:949-960
49. McShea A, Harris PLR, Webster KR, Wahl AF, Smith MA: Abnormal expression of the cell cycle regulators P16 and CDK4 in Alzheimer's disease. Am J Pathol 1997, 150:1933-1939
50. Nagy ZS, Esiri MM, Cato A-M, Smith AD: Cell cycle markers in the hippocampus in Alzheimer's disease. Acta Neuropathol (Berl) 1997, 94:6-15
51. Ross ME: Cell division and the nervous system: regulating the cycle from neural differentiation to death. Trends Neurosci 1996, 19:62-68
52. Vincent I, Jicha G, Rosado M, Dickson DW: Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J Neurosci 1997, 17:3588-3598
53. Kim TW, Pettingell WH, Jung YK, Kovacs DM, Tanzi RE: Alternative cleavage of Alzheimer-associated presenilins during apoptosis by a caspase-3 family protease. Science 1997, 277:373-376
54. Loetscher H, Deuschle U, Brockhaus M, Reinhardt D, Nelboeck P, Mous J, Grunberg J, Haass C, Jacobsen H: Presenilins are processed by caspase-type proteases. J Biol Chem 1997, 272:20655-20659
55. Barnes NY, Li L, Yoshikawa K, Schwartz LM, Oppenheim RW, Milligan CE: Increased production of amyloid precursor protein provides a substrate for caspase-3 in dying motoneurons. J Neurosci 1998, 18:5869-5880
56. Weidemann A, Paliga K, Durrwang U, Reinhard FBM, Schuckert O, Evin G, Masters CL: Proteolytic processing of the Alzheimer's disease amyloid precursor protein within its cytoplasmic domain by caspase-like proteases. J Biol Chem 1999, 274:5823-5829
57. van de Craen M, de Jonghe C, van den Brande I, Deolercq W, van Gassen G, van Criekinge W, Vanderhoeven I, Fiers W, van Broeckhoven C, Hendriks L, Vandenabeele P: Identification of caspases that cleave presenilin-1 and presenilin-2: five presenilin-1 (PS1) mutations do not alter the sensitivity of PS1 to caspases. FEBS Lett 1999, 445:149-154
58. Gervais FG, Xu D, Robertson GS, Vaillancourt JP, Zhu Y, Huang JQ, LeBlanc A, Smith D, Rigby M, Shearman MS, Clarke EE, Zheng H, Van der Ploeg LHT, Ruffolo SC, Thornberry NA, Xanthoudakis S, Zamboni RJ, Roy S, Nicholson DW: Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-β precursor protein and amyloidogenic Aβ peptide formation. Cell 1999, 97:395-406
59. Masliah E, Mallory M, Alford M, Tanaka S, Hansen LA: Caspase dependent DNA fragmentation might be associated with excitotoxicity in Alzheimer disease. J Neuropathol Exp Neurol 1998, 57:1041-1052
60. Wisniewski HM, Terry RD: Morphology of the aging brain, human and animal. Progress in Brain Research, vol 40. Edited by Ford DM. Amsterdam, Elsevier, 1973, pp 167-186
61. de Estable-Puig RF, Estable-Puig JF: Vacuolar degeneration in neurones of aging rats. Virchows Arch B Cell Pathol 1975, 17:337-346
62. Mann DMA: Granulovacuolar degeneration in pyramidal cells of the hippocampus. Acta Neuropathol (Berl) 1978, 42:149-151
63. Okamoto K, Hirai S, Iizuka, Yanagisawa, Watanabe M: Reexamination of granulovacuolar degeneration. Acta Neuropathol (Berl) 1991, 82: 340-345
64. Schotte P, van Criekinge W, van de Craen M, van Loo G, Desmedt M, Grooten J, Cornelissen M, de Bidder L, Vandekerckhove J, Fiers W, Vandenabeele P, Beyaert R: Cathepsin B-mediated activation of the proinflammatory caspase-11. Biochem Biophys Res Commun 1998, 251:379-387
65. Ishisaka R, Utsumi T, Yabuki M, Kanno T, Furuno T, Inoue M, Utsumi K: Activation of caspase-3 like protease by digitonin treated lysosomes. FEBS Lett 1998, 435:233-236
66. Monney L, Olivier R, Otter I, Jansen B, Poirier GG, Borner C: Role of an acidic compartment in tumor-necrosis-factor-α-induced production of ceramide, activation of caspase-3 and apoptosis. Eur J Biochem 1998, 251:295-303
67. Bursch W, Ellinger A, Török L, Parzefall W, Coulibaly S, Hochegger K, Schörkhuber M, Partik G, Marian B, Walker R, Sikorska M, Schulte-Hermann R: In vitro studies on subtypes, and regulation of active cell death. Toxicol In Vitro 1997, 11:579-588
68. Clarke PGH: Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 1990, 181:195-213
69. Hammond EM, Brunet CL, Johnson GD, Parkhill J, Milner AE, Brady G, Gregory CD, Grand RJA: Homology between a human apoptosis specific protein and the product of APG5, a gene involved in autophagy in yeast. FEBS Lett 1998, 425:391-395
70. Tomlinson BE, Kitchener D: Granulovacuolar degeneration of hippocampal pyramidal cells. J Pathol 1972, 106:165-185
71. Ball MJ: Topographic distribution of neurofibrillary tangles and granulovacuolar degeneration in hippocampal cortex of aging and demented patients. A quantitative study. Acta Neuropathol (Berl) 1978, 42:73-80
72. Bondareff W, Wischik CM, Novak M, Roth M: Sequestration of tau by granulovacuolar degeneration in Alzheimer's disease. Am J Pathol 1991, 139:641-647
73. Dickson DW, Ksiezwak-Reding H, Davies P, Yen SH: A monoclonal antibody that recognizes a phosphorylated epitope in Alzheimer neurofibrillary tangles, neurofilaments and tau proteins immunostains granulovacuolar degeneration. Acta Neuropathol (Berl) 1987, 73: 254-258