Tau-4R suppresses proliferation and promotes neuronal differentiation in the hippocampus of tau knockin/knockout mice

FASEB Journal

Volumn 21, Issue 9, 2007, Pages 2149-2161

  Sennvik, Kristina ^a   Boekhoorn, Karin ^b   Lasrado, Reena ^a   Terwel, Dick ^a   Verhaeghe, Steven ^a   Korr, Hubert ^c   Schmitz, Christoph ^c   Tomiyama, Takami ^d   Mori, Hiroshi ^d   Krugers, Harm ^b   Joels, Marian ^b   Ramakers, Ger J A ^e   Lucassen, Paul J ^b   Van Leuven, Fred ^a,f  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d OSAKA UNIVERSITY   (Japan)

^e NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^f KULeuven Campus Gasthuisberg ON1 06602 ^*  (Belgium)

Author keywords

Cognition; Neurogenesis; Primary cultures; Transgenic mice

Indexed keywords

PROTEIN; PROTEIN TAU 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL COUNT; CELL PROLIFERATION; CELL SURVIVAL; CELL VOLUME; CONTROLLED STUDY; HIPPOCAMPUS; KNOCKOUT MOUSE; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; CROSSES, GENETIC; EMBRYO TRANSFER; EMBRYONIC STEM CELLS; EXPLORATORY BEHAVIOR; GENETIC VECTORS; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROINJECTIONS; NEURITES; NEURONS; ORGAN SIZE; PROTEIN ISOFORMS; RECOGNITION (PSYCHOLOGY); RECOMBINANT FUSION PROTEINS; STEM CELLS; TAU PROTEINS; TRANSDUCTION, GENETIC;

MURINAE; MUS; MUS MUSCULUS;

EID: 34347387536     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7735com     Document Type: Article

References (33)

1. Goedert, M. (1996) Tau protein and the neurofibrillary pathology of Alzheimer's disease. Ann. N. Y. Acad. Sci. 777, 121-131
2. Lee, V. M., Goedert, M., and Trojanowski, J. Q. (2001) Neurodegenerative tauopathies. Annu. Rev. Neurosci. 24, 1121-1159
3. Buée, L., Bussière, T., Buée-Scherrer, V., Delacourte, A., and Hof, P. (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain. Res. Rev. 33, 95-130
4. Larcher, J. C., Boucher, D., Ginzburg, I., Gros, F., and Denoulet, P. (1992) Heterogeneity of Tau proteins during mouse brain development and differentiation of cultured neurons. Dev. Biol. 154, 195-204
5. Takuma, H., Shigeki, A., and Mori, H. (2003) Isoform changes of tau protein during development in various species. Dev. Brain. Res. 142, 121-127
6. Andorfer, C., Kress, Y., Espinoza, M., de Silva, R., Tucker, K. L., Barde, Y.-A., Duff, K., and Davies, P. (2003) Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J. Neurochem. 86, 582-590
7. Gotz, J., Streffer, J. R., David, D., Schild, A., Hoerndli, F., Pennanen, L., Kurosinski, P., and Chen, F. (2004) Transgenic animal models of Alzheimer's disease and related disorders: histopathology, behavior and therapy. Mol. Psych. 9, 664-683
8. Spittaels, K., Van den Haute, C., Van Dorpe, J., Bruynseels, K., Vandezande, K., Laenen, I., Geerts, H., Mercken, M., Sciot, R., Van Lommel, A., et al. (1999) Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am. J. Pathol. 155, 2153-2165
9. Terwel, D., Lasrado, R., Snauwaert, J., Vandeweert, E., Van Haesendonck, C., Borghgraef, P., and Van Leuven, F. (2005) Changed conformation of mutant tau-P301L underlies the moribund tauopathy, absent in progressive non-lethal axonopathy of tau-4R/2N transgenic mice. J. Biol. Chem. 280, 3963-3973
10. Umans, L., Serneels, L., Lorent, K., Dewachter, I., Tesseur, I., Moechars, D., and F., V. L. (1999) Lipoprotein receptor-related protein in brain and in cultured neurons of mice deficient in receptor-associated protein and transgenic for apolipoprotein E4 or amyloid precursor protein. Neuroscience 94, 315-321
11. Harada, A., Oguchi, K., Okabo, S., Kuno, J., Terada, S., Ohsima, T., Sato-Yoshitake, R., Takei, Y., Noda, T., and Hirokawa, N. (1994) Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature 369, 488-491
12. Dewachter, I., Reversé, D., Caluwaerts, N., Ris, L., Kuiperi, C., Van den Haute, C., Spittaels, K., Umans, L., Serneels, L., and Thiry, E., et al. (2002) Neuronal deficiency of presenilin 1 inhibits amyloid plaque formation and corrects hippocampal long-term potentiation but not a cognitive defect of amyloid precursor protein [V717I] transgenic mice. J. Neurosci. 22, 3445-3453
13. West, M. J. (1993) New stereological methods for counting neurons. Neurobiol. Aging 14, 275-285
14. Schmitz, C. (2000) Towards the use of state-of-the-art stereology in experimental gerontology. Exp. Gerontol. 35, 429-431
15. Boekhoorn, K., Terwel, D., Biemans, B., Borghgraef, P., Wiegert, O., Ramakers, G. J. A., de Vos, K., Krugers, H., Joels, M., Van Leuven, F., et al. (2006) Improved long-term potentiation and memory function in young Tau-P301L transgenic mice prior to the onset of hyperphosphorylation and tauopathy. (2006) J. Neurosci. 26, 3514-3523
16. Heine, V. M., Maslam, S., Joels, M., and Lucassen, P. J. (2004) Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation. Neurobiol. Aging 25, 361-375
17. Lucassen, P. J., Fuchs, E., and Czeh, B. (2004) Antidepressant treatment with tianeptine reduces apoptosis in the tree shrew hippocampal dentate gyrus and temporal cortex. Biol. Psych. 55, 789-796
18. Ramakers, G. J., Winter, J., Hoogland, T. M., Lequin, M. B., Van Hulten, P., Van Pelt, J., and Pool, C. W. (1998) Depolarization stimulates lamellipodia formation and axonal but not dendritic branching in cultured rat cerebral cortex neurons. Brain. Res. Dev. Brain. Res. 108, 205-216
19. Banker, G. A., and Cowan, W. M. (1977) Rat hippocampal neurons in dispersed cell culture. Brain. Res. 126, 397-342
20. Dawson, H. N., Ferreira, A., Eyster, M. V., Ghoshal, N., Binder, L. I., and Vitek, M. P. (2001) Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J. Cell Sci. 114, 1179-1187
21. Vandebroek, T., Vanhelmont, T., Terwel, D., Borghgraef, P., Lemaire, K., Snauwaert, J., Wera, S., Van Leuven, F., and Winderickx, J. (2005) Identification and isolation of a hyperphosphorylated, conformationally changed intermediate of human protein tau expressed in yeast. Biochemistry 44, 11466-11475
22. Spittaels, K., Van den Haute, C., Van Dorpe, J., Terwel, D., Vandezande, K., Lasrado, R., Bruynseels, K., Irizarry, M., Verhoye, M., Van Lint, J., et al. (2002) Neonatal neuronal overexpression of glycogen synthase kinase-3 beta reduces brain size in transgenic mice. Neuroscience 113, 797-808
23. van Praag, H., Christie, B. R., Sejnowski, T. J., and Gage, F. H. (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U. S. A. 96, 13427-13431
24. Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., and Gould, E. (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12, 578-584
25. Kempermann, G., Wiskott, L., and Gage, F. H. (2004) Functional significance of adult neurogenesis. Curr. Opin. Neurobiol. 14, 186-191
26. Andorfer, C. A., and Davies, P. (2000) PKA phosphorylations on tau: developmental studies in the mouse. Dev. Neurosci. 22, 303-309
27. Goedert, M., Spillantini, M. G., Jakes, R., Rutherford, D., and Crowther, R. A. (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3, 519-526
28. Stanfield, B. B., and Cowan, W. M. (1979) The development of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185, 423-459
29. Caceres, A., and Kosik, K. S. (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461-463
30. Liu, C. W., G., L., and Jay, D. G. (1999) Tau is required for neurite outgrowth and growth cone motility of chick sensory neurons. Cell Motil. Cytoskel. 43, 232-242
31. Takei, Y., Teng, J., Harada, A., and Hirokawa, N. (2000) Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J. Cell Biol. 150, 989-1000
32. Utton, M. A., Graham, M. G., Burdett, I. D. J., Anderton, B. H., and Vandecandelaere, A. (2001) Functional differences of tau isoforms containing 3 or 4 C-terminal repeat regions and the influence of oxidative stress. J. Biol. Chem. 276, 34288-34297
33. Levy, S. F., LeBoeuf, A. C., Massie, M. R., Jordan, M. A., Wilson, L., and Feinstein, S. F. (2005) Three- and four-repeat tau regulate the dynamic instability of two distinct microtubule subpopulations in qualitatively different manners. J. Biol. Chem. 280, 13520-13528