Alzheimer disease: DNA fragmentation indicates increased neuronal vulnerability, but not apoptosis

Journal of Neuropathology and Experimental Neurology

Volumn 57, Issue 5, 1998, Pages 456-464

  Stadelmann, Christine ^a   Brück, Wolfgang ^b   Bancher, Christian ^c   Jellinger, Kurt ^c   Lassmann, Hans ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c GENERAL HOSPITAL LINZ   (Austria)

Author keywords

Alzheimer disease; Apoptosis; Apoptosis specific protein; c Jun; DNA fragmentation; Neuronal cell death; Pontosubicular neuron necrosis

Indexed keywords

ALPHA CRYSTALLIN; BETA CRYSTALLIN; DNA FRAGMENT; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 65; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; ONCOPROTEIN; PROTEIN BCL 2; UBIQUITIN;

ADULT; AGED; ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; CHROMATIN CONDENSATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL NECROSIS; PRIORITY JOURNAL;

EID: 2642680857     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-199805000-00009     Document Type: Article

References (68)

1. Gómez-Isla T, Hollister R, West H, et al. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann Neurol 1997;41:17-24
2. Mann DMA, Yates PO, Marcynuik B. Some morphometric observations on the cerebral cortex and hippocampus in presenile Alzheimer's disease, senile dementia of Alzheimer type and Down's syndrome in middle age. J Neurol Sci 1985;69:139-59
3. De Kosky ST, Scheff SW. Synapse loss in frontal lobe biopsies in Alzheimer's disease: Correlation with cognitive severity. Ann Neurol 1990;27:457-64
4. Terry RD, Masliah E, Salmon DP, et al. Physical basis of cognitive alterations in Alzheimer's disease: Synaptic loss is a major correlate of cognitive impairment. Ann Neurol 1991;30:572-80
5. Mullaart E, Boerrigter METI, Ravid R, Swaab DF, Vijg J. Increased levels of DNA breaks in cerebral cortex of Alzheimer's disease pa-tients. Neurobiol Aging 1990;11:169-73
6. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501
7. Gold R, Schmied M, Giegerich G, Breitschopf H, Hartung HP, Toyka K, Lassmann H. Differentiation between cellular apoptosis and necrosis by combined use of in situ tailing and nick translation techniques. Lab Invest 1994;71:219-25
8. 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;6:1053-57
9. 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 1995;89:35-41
10. 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
11. 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;53:606-16
12. Portera-Cailliau C, Hedreen JC, Price DL, Koliatsos VE. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J Neurosci 1995;15:3775-87
13. Smale G, Nichols NR, Brady DR, Finch CE, Horton Jr. WE. Evidence for apoptotic cell death in Alzheimer's disease. Exp Neurol 1995;133:225-30
14. Su JH, Anderson AJ, Cummings BJ, Cotman CW. Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 1994;5:2529-33
15. Tompkins MM, Basgall EJ, Zamrini E, Hill WD. Apoptotic-like changes in Lewy-body-associated disorders and normal aging in substantia nigral neurons. Am J Pathol 1997;150:119-31
16. 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;55:1134-42
17. Bredesen DE. Neural apoptosis. Ann Neurol 1995;38:839-51
18. Yankner BA. Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 1996;16:921-32
19. 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; 17:4212-22
20. Haass C. Presenilins: Genes for life and death. Neuron 1997;18:687-90
21. 2+-binding protein ALG-2 and Alzheimer's disease gene ALG-3. Science 1996;271:521-54
22. Wolozin B, Iwasaki K, Vito R et al. Participation of presenilin 2 in apoptosis: Enhanced basal activity conferred by an Alzheimer mutation. Science 1996;274:1710-13
23. Yamatsuji T, Matsui T, Okamoto T, et al. G-protein-mediated neuronal DNA fragmentation induced by familial Alzheimer's disease-associated mutants of APP. Science 1996;272:1349-52
24. Busciglio J, Yankner BA. Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature 1995;378:776-79
25. Paradis E, Douillard H, Koutroumanis M, Goodyer C, LeBlanc A. Amyloid β peptide of Alzheimer's disease downregulates Bcl-2 and upregulates Bax expression in human neurons. J Neurosci 1996;16: 7533-39
26. 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
27. Su JH, Satou T, Anderson AJ, Cotman CW. Up-regulation of Bcl-2 is associated with neuronal DNA damage in Alzheimer's disease. Neuroreport 1996;7:437-40
28. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson Jr. EM. Altered gene expression in neurons during programmed cell death: Identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 1994;127:1717-27
29. Ham J, Babij C, Whitfield J, Pharr CM, Lallemand D, Yaniv M. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 1995;14:927-39
30. Herdegen T, Skene P, Bähr M. The c-Jun transcription factor -bipotential mediator of neuronal death, survival and regeneration. Trends Neurosci 1997;20:227-31
31. Morgan JI, Curran T. Stimulus-transcription coupling in the nervous system: Involvement of the inducible proto-oncogenes fos and jun. Ann Rev Neurosci 1991;14:421-51
32. 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;16:1710-19
33. Wyllie AH, Kerr JFR, Currie AR. Cell death: The significance of apoptosis. Int Rev Cytol 1980;68:251-306
34. Grand RJA, Milner AE, Mustoe T, Johnson GD, Owen D, Grant ML, Gregory CD. A novel protein expressed in mammalian cells undergoing apoptosis. Exp Cell Res 1995;218:439-51
35. Brück Y, Brück W, Kretzschmar HA, Lassmann H. Evidence for neuronal apoptosis in pontosubicular neuron necrosis. Neuropathol Appl Neurobiol 1996;22:23-29
36. Friede RL. Ponto-subicular lesions in perinatal anoxia. Arch Pathol 1972;94:343-54
37. Khatchaturian ZS. Diagnosis of Alzheimer's disease. Arch Neurol 1985;42:1097-1105
38. Mirra SS, Heyman A, McKeel D, et al. The consortium to establish a registry for Alzheimer's disease (CERAD). Part II. Standardization of the neuropathological assessment of Alzheimer's disease. Neurology 1991;41:479-86
39. Wang GP, Grundke-Iqbal I, Kascak RJ, Iqbal K, Wisniewski HM. Alzheimer neurofibrillary tangles: Monoclonal antibodies to inherent antigen(s). Acta Neuropathol 1984;62:268-75
40. Lassmann H. Patterns of synaptic and nerve cell pathology in Alzheimer's disease. Behav Brain Res 1996;78:9-14
41. Selkoe DJ. Alzheimer's disease: Genotypes, phenotype, and treatments. Science 1997;275:630-31
42. Cotman CW, Su JH. Mechanisms of neuronal cell death in Alzheimer's disease. Brain Pathol 1996;6:493-506
43. Mu X, He J, Anderson DW, Trojanowski JQ, Springer JE. Altered expression of bcl-2 and bax mRNA in amyotrophic lateral sclerosis spinal cord motor neurons. Ann Neurol 1996;40:379-86
44. 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;150:1933-39
45. Nagy Zs, Esiri MM, Cato A-M, Smith AD. Cell cycle markers in the hippocampus in Alzheimer's disease. Acta Neuropathol 1997; 94:6-15
46. Ross ME. Cell division and the nervous system: Regulating the cycle from neural differentiation to death. Trends Neurosci 1996; 19:62-68
47. 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;17:3588-98
48. Harlan RE, Garcia MM. Charting of Jun family member proteins in the rat forebrain and midbrain: Immunocytochemical evidence for a new Jun-related antigen. Brain Res 1995;692:1-22
49. Björkerud S, Björkerud B. Apoptosis is abundant in human athero-sclerotic lesions, especially in inflammatory cells (macrophages and T cells), and may contribute to the accumulation of gruel and plaque instability. Am J Pathol 1996;149:367-80
50. Anderson AJ, Cummings BJ, Cotman CW. Increased immunoreactivity for Jun- and Fos-related proteins in Alzheimer's disease: Association with pathology. Exp Neurol 1994;125:286-95
51. Ferrer I, Seguí J, Planas AM. Amyloid deposition is associated with c-Jun expression in Alzheimer's disease and amyloid angiopathy. Neuropathol Appl Neurobiol 1996;22:521-26
52. Virgo L, de Belleroche J. Induction of the immediate early gene c-jun in human spinal cord in amyotrophic lateral sclerosis with concomitant loss of NMDA receptor NR-1 and glycine transporter mRNA. Brain Res 1995;676:196-204
53. Martín G, Seguí J, Díaz-Villoslada P, Montalbán X, Planas AM, Ferrer I. Jun expression is found in neurons located in the vicinity of subacute plaques in patients with multiple sclerosis. Neurosci Lett 1996;212:95-98
54. Migheli A, Cavalla P, Piva R, Giordana MT, Schiffer D. Bcl-2 protein expression in aged brain and neurodegenerative diseases. Neuroreport 1994;5:1906-8
55. O'Barr S, Schultz J, Rogers J. Expression of the protooncogene bcl-2 in Alzheimer's disease brain. Neurobiol Aging 1995;17: 131-36
56. Satou T, Cummings BJ, Cotman CW. Immunoreactivity for Bcl-2 protein within neurons in the Alzheimer's disease brain increases with disease severity. Brain Res 1995;697:35-43
57. Mailhos C, Howard MK, Latchman DS. Heat shock protects neuronal cells from programmed cell death by apoptosis. Neuroscience 1993;55:621-27
58. Mehlen P, Schulze-Osthoff K, Arrigo A-P. Small stress proteins as novel regulators of apoptosis. J Biol Chem 1996;271:16510-14
59. Polla BS, Kantengwa S, Francois D, Salvioli S, Franceschi C, Marsac C, Cossarizza A. Mitochondria are selective targets for the protective effects of heat shock against oxidative injury. Proc Natl Acad Sci USA 1996;93:6458-63
60. Samali A, Cotter TC. Heat shock proteins increase resistance to apoptosis. Exp Cell Research 1996;223:163-70
61. Petito CK, Roberts B. Effect of postmortem interval on in situ end-labeling of DNA oligonucleosomes. J Neuropathol Exp Neurol 1995;54:761-65
62. Robbins JH, Otsuka F, Tarone RD, et al. Radiosensitivity in Alzheimer's disease and Parkinson disease [letter]. Lancet 1983;1: 468-69
63. Robison SH, Munzer JS, Tandan R, Bradley WG. Alzheimer's disease cells exhibit defective repair of alkylating agent-induced DNA damage. Ann Neurol 1987;21:250-58
64. Parshad R, Sanford KK, Price FM, et al. Fluorescent light-induced chromatid breaks distinguish Alzheimer disease cells from normal cells in tissue culture. Proc Natl Acad Sci USA 1996;93:5146-50
65. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P. Glutamate-induced neuronal death: A succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995;15:961-73
66. Beal MF. Aging, energy, and oxidative stress in neurodegenerative diseases. Ann Neurol 1995;38:357-66
67. Hoyer S. Oxidative metabolism deficiencies in brains of patients with Alzheimer's disease. Acta Neurol Scand Suppl 1996;165: 18-24
68. Sheehan JP, Swerdlow RH, Miller SW, Davis RE, Parks JK, Parker WD, Tuttle JB. Calcium homeostasis and reactive oxygen species production in cells transformed by mitochondria from individuals with sporadic Alzheimer's disease. J Neurosci 1997;17:4612-22