Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms

Journal of Neuroscience

Volumn 25, Issue 22, 2005, Pages 5446-5454

  Andorfer, Cathy ^a   Acker, Christopher M ^a   Kress, Yvonne ^a   Hof, Patrick R ^b   Duff, Karen ^c   Davies, Peter ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

Author keywords

Cell cycle; Cell death; Neurodegeneration; Neurofibrillary tangle; Nonmutant tau; Transgenic

Indexed keywords

CELL CYCLE PROTEIN; TAU PROTEIN;

ADOLESCENT; AGED; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL DEATH; DEGENERATIVE DISEASE; DNA SYNTHESIS; FEMALE; MALE; MICROTUBULE; MOUSE; MUTATION; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TAUOPATHY; TRANSGENIC MOUSE;

AGING; ANIMALS; BRAIN; BROMODEOXYURIDINE; CELL CYCLE; CELL DEATH; DNA FRAGMENTATION; HUMANS; MICE; MICE, TRANSGENIC; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NEUROFIBRILLARY TANGLES; NEURONS; PROTEIN ISOFORMS; TAU PROTEINS;

EID: 20044367108     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4637-04.2005     Document Type: Article

References (75)

1. Andorfer C, Kress Y, Espinoza M, de Silva R, Tucker KL, Barde YA, Duff K, Davies P (2003) Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J Neurochem 86:582-590.
2. Andorfer CA, Davies P (2000) PKA phosphorylations on tau: developmental studies in the mouse. Dev Neurosci 22:303-309.
3. Augustinack JC, Schneider A, Mandelkow EM, Hyman BT (2002) Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease. Acta Neuropathol (Berl) 103:26-35.
4. Behl C (2000) Apoptosis and Alzheimer's disease. J Neural Transm 107:1325-1344.
5. Bunker JM, Wilson L, Jordan MA, Feinstein SC (2004) Modulation of microtubule dynamics by tau in living cells: implications for development and neurodegeneration. Mol Biol Cell 15:2720-2728.
6. Busser J, Geldmacher DS, Herrup K (1998) Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J Neurosci 18:2801-2807.
7. Coqueret O (2002) Linking cyclins to transcriptional control. Gene 299:35-55.
8. Cotman CW, Anderson AJ (1995) A potential role for apoptosis in neurodegeneration and Alzheimer's disease. Mol Neurobiol 10:19-45.
9. Duff K, Knight H, Refolo LM, Sanders S, Yu X, Picciano M, Malester B, Hutton M, Adamson J, Goedert M, Burki K, Davies P (2000) Characterization of pathology in transgenic mice over-expressing human genomic and cDNA tau transgenes. Neurobiol Dis 7:87-98.
10. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
11. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
12. Giannakakou P, Robey R, Fojo T, Blagosklonny MV (2001) Low concentrations of paclitaxel induce cell type-dependent p53, p21 and G1/G2 arrest instead of mitotic arrest: molecular determinants of paclitaxel-induced cytotoxicity. Oncogene 20:3806-3813.
13. Goedert M, Wischik CM, Crowther RA, Walker JE, Klug A (1988) Cloning and sequencing of the cDNA encoding a core protein of the paired helical filament of Alzheimer disease: identification as the microtubule-associated protein tau. Proc Natl Acad Sci USA 85:4051-4055.
14. Goedert M, Spillantini MG, Potier MC, Ulrich J, Crowther RA (1989) 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 8:393-399.
15. Goldstein LS (2003) Do disorders of movement cause movement disorders and dementia? Neuron 40:415-425.
16. Gomez-Isla T, Hollister R, West H, Mui S, Growdon JH, Petersen RC, Parisi JE, Hyman BT (1997) Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann Neurol 41:17-24.
17. Goode BL, Feinstein SC (1994) Identification of a novel microtubule binding and assembly domain in the developmentally regulated inter-repeat region of tau. J Cell Biol 124:769-782.
18. Gould E, Tanapat P, McEwen BS, Flugge G, Fuchs E (1998) Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci USA 95:3168-3171.
19. Greenberg SG, Davies P (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci USA 87:5827-5831.
20. Gunawardena S, Goldstein LS (2001) Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila, Neuron 32:389-401.
21. Gunawardena S, Her LS, Brusch RG, Laymon RA, Niesman IR, Gordesky-Gold B, Sintasath L, Bonini NM, Goldstein LS (2003) Disruption of axonal transport by loss of huntingtin or expression of pathogenic polyQ proteins in Drosophila. Neuron 40:25-40.
22. Hardy JA, Higgins GA (1992) Alzheimer's disease: the amyloid cascade hypothesis. Science 256:184-185.
23. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770-776.
24. Herrup K, Arendt T (2002) Re-expression of cell cycle proteins induces neuronal cell death during Alzheimer's disease. J Alzheimers Dis 4:243-247.
25. Herrup K, Yang Y (2001) Pictures in molecular medicine: Contemplating Alzheimer's disease as cancer: a loss of cell-cycle control. Trends Mol Med 7:527.
26. Himmler A (1989) Structure of the bovine tau gene: alternatively spliced transcripts generate a protein family. Mol Cell Biol 9:1389-1396.
27. Hof PR (2000) Comparative cytoarchitectonic atlas of the C57BL/6 and 129/Sv mouse brains. Amsterdam: Elsevier.
28. Honer WG, Dickson DW, Gleeson J, Davies P (1992) Regional synaptic pathology in Alzheimer's disease. Neurobiol Aging 13:375-382.
29. Hutton M (2001) Missense and splice site mutations in tau associated with FTDP-17: multiple pathogenic mechanisms. Neurology 56:S21-S25.
30. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Adamson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaff E, Wauters E, van Baren J, et al. (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393:702-705.
31. Ishihara T, Hong M, Zhang B, Nakagawa Y, Lee MK, Trojanowski JQ, Lee VM (1999) Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 24:751-762.
32. Jackson GR, Wiedau-Pazos M, Sang TK, Wagle N, Brown CA, Massachi S, Geschwind DH (2002) Human wild-type tau interacts with wingless pathway components and produces neurofibrillary pathology in Drosophila. Neuron 34:509-519.
33. Jicha GA, Bowser R, Kazam IG, Davies P (1997a) Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J Neurosci Res 48:128-132.
34. Jicha GA, Lane E, Vincent I, Otvos Jr L, Hoffmann R, Davies P (1997b) A conformation- and phosphorylation-dependent antibody recognizing the paired helical filaments of Alzheimer's disease. J Neurochem 69:2087-2095.
35. Jicha GA, Rockwood JM, Berenfeld B, Hutton M, Davies P (1999) Altered conformation of recombinant frontotemporal dementia-17 mutant tau proteins. Neurosci Lett 260:153-156.
36. Jordan MA, Wendell K, Gardiner S, Derry WB, Copp H, Wilson L (1996) Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res 56:816-825.
37. Kerr JF (1972) Shrinkage necrosis of adrenal cortical cells. J Pathol 107:217-219.
38. Kimura T, Ono T, Takamatsu J, Yamamoto H, Ikegami K, Kondo A, Hasegawa M, Ihara Y, Miyamoto E, Miyakawa T (1996) Sequential changes of tau-site-specific phosphorylation during development of paired helical filaments. Dementia 7:177-181.
39. Kuan CY, Schloemer AJ, Lu A, Burns KA, Weng WL, Williams MT, Strauss KI, Vorhees CV, Flavell RA, Davis RJ, Sharp FR, Rakic P (2004) Hypoxia-ischemia induces DNA synthesis without cell proliferation in dying neurons in adult rodent brain. J Neurosci 24:10763-10772.
40. LaMonte BH, Wallace KE, Holloway BA, Shelly SS, Ascano J, Tokito M, Van Winkle T, Howland DS, Holzbaur EL (2002) Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 34:715-727.
41. Lassmann H, Bancher C, Breitschopf H, Wegiel J, Bobinski M, Jellinger K, Wisniewski HM (1995) Cell death in Alzheimer's disease evaluated by DNA fragmentation in situ. Acta Neuropathol (Berl) 89:35-41.
42. Lee G, Cowan N, Kirschner M (1988) The primary structure and heterogeneity of tau protein from mouse brain. Science 239:285-288.
43. Leist M, Jaattela M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2:589-598.
44. Lew J, Qi Z, Huang QQ, Paudel H, Matsuura I, Matsushita M, Zhu X, Wang JH (1995) Structure, function, and regulation of neuronal Cdc2-like protein kinase. Neurobiol Aging 16:263-268, discussion 268-270.
45. Lucassen PJ, Chung WC, Kamphorst W, Swaab DF (1997) DNA damage distribution in the human brain as shown by in situ end labeling; area-specific differences in aging and Alzheimer disease in the absence of apoptotic morphology. J Neuropathol Exp Neurol 56:887-900.
46. Maga G, Hubscher U (2003) Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 116:3051-3060.
47. Michaelis ML, Dobrowsky RT, Li G (2002) Tau neurofibrillary pathology and microtubule stability. J Mol Neurosci 19:289-293.
48. Nagy Z, Esiri MM, Cato AM, Smith AD (1997) Cell cycle markers in the hippocampus in Alzheimer's disease. Acta Neuropathol (Berl) 94:6-15.
49. Nakanishi T, Ikawa M, Yamada S, Toshimori K, Okabe M (2001) Alkalinization of acrosome measured by GFP as a pH indicator and its relation to sperm capacitation. Dev Biol 237:222-231.
50. Otvos Jr L, 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 39:669-673.
51. Panda D, Goode BL, Feinstein SC, Wilson L (1995) Kinetic stabilization of microtubule dynamics at steady state by tau and microtubule-binding domains of tau. Biochemistry 34:11117-11127.
52. Panda D, Samuel JC, Massie M, Feinstein SC, Wilson L (2003) Differential regulation of microtubule dynamics by three- and four-repeat tau: implications for the onset of neurodegenerative disease. Proc Natl Acad Sci USA 100:9548-9553.
53. Poorkaj P, Grossman M, Steinbart E, Payami H, Sadovnick A, Nochlin D, Tabira T, Trojanowski JQ, Borson S, Galasko D, Reich S, Quinn B, Schellenberg G, Bird TD (2001) Frequency of tau gene mutations in familial and sporadic cases of non-Alzheimer dementia. Arch Neurol 58:383-387.
54. Schluter C, Duchrow M, Wohlenberg C, Becker MH, Key G, Flad HD, Gerdes J (1993) The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol 123:513-522.
55. Schmitz C, Hof PR (2000) Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J Chem Neuroanat 20:93-114.
56. Scholzen T, Gerdes J (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182:311-322.
57. Sgonc R, Wick G (1994) Methods for the detection of apoptosis. Int Arch Allergy Immunol 105:327-332.
58. Spillantini MG, Goedert M (1998) Tau protein pathology in neurodegenerative diseases. Trends Neurosci 21:428-433.
59. Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B (1998) Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc Natl Acad Sci USA 95:7737-7741.
60. Srivastava RK, Srivastava AR, Korsmeyer SJ, Nesterova M, Cho-Chung YS, Longo DL (1998) Involvement of microtubules in the regulation of Bcl2 phosphorylation and apoptosis through cyclic AMP-dependent protein kinase. Mol Cell Biol 18:3509-3517.
61. Stadelmann C, Bruck W, Bancher C, Jellinger K, Lassmann H (1998) Alzheimer disease: DNA fragmentation indicates increased neuronal vulnerability, but not apoptosis. J Neuropathol Exp Neurol 57:456-464.
62. Su JH, Anderson AJ, Cummings BJ, Cotman CW (1994) Immunohistochemical evidence for apoptosis in Alzheimer's disease. NeuroReport 5:2529-2533.
63. Taylor JP, Hardy J, Fischbeck KH (2002) Toxic proteins in neurodegenerative disease. Science 296:1991-1995.
64. Troncoso JC, Martin LJ, Dal Forno G, Kawas CH (1996) Neuropathologyin controls and demented subjects from the Baltimore Longitudinal Study of Aging. Neurobiol Aging 17:365-371.
65. Tucker KL, Meyer M, Barde YA (2001) Neurotrophins are required for nerve growth during development. Nat Neurosci 4:29-37.
66. Vincent I, Pae CI, Hallows JL (2003) The cell cycle and human neurodegenerative disease. Prog Cell Cycle Res 5:31-41.
67. Weaver CL, Espinoza M, Kress Y, Davies P (2000) Conformational change as one of the earliest alterations of tau in Alzheimer's disease. Neurobiol Aging 21:719-727.
68. Wen Y, Yang S, Liu R, Brun-Zinkernagel AM, Koulen P, Simpkins JW (2004) Transient cerebral ischemia induces aberrant neuronal cell cycle re-entry and Alzheimer's disease-like tauopathy in female rats. J Biol Chem 279:22684-22692.
69. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
70. Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, Hutton M, Feany MB (2001) Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 293:711-714.
71. Yang Y, Geldmacher DS, Herrup K (2001) DNA replication precedes neuronal cell death in Alzheimer's disease. J Neurosci 21:2661-2668.
72. Yang Y, Mufson EJ, Herrup K (2003) Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J Neurosci 23:2557-2563.
73. Ye K, Zhou J, Landen JW, Bradbury EM, Joshi HC (2001) Sustained activation of p34(cdc2) is required for noscapine-induced apoptosis. J Biol Chem 276:46697-46700.
74. Yvon AM, Wadsworth P, Jordan MA (1999) Taxol suppresses dynamics of individual microtubules in living human tumor cells. Mol Biol Cell 10:947-959.
75. Zehr C, Lewis J, McGowan E, Crook J, Lin WL, Godwin K, Knight J, Dickson DW, Hutton M (2004) Apoptosis in oligodendrocytes is associated with axonal degeneration in P301L tau mice. Neurobiol Dis 15:553-562.