Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy

Journal of Neuroscience

Volumn 26, Issue 13, 2006, Pages 3514-3523

  Boekhoorn, Karin ^a   Terwel, Dick ^b   Biemans, Barbara ^b   Borghgraef, Peter ^b   Wiegert, Olof ^a   Ramakers, Ger J A ^c   De Vos, Koos ^c   Krugers, Harm ^a   Tomiyama, Takami ^d   Mori, Hiroshi ^d   Joels, Marian ^a   Van Leuven, Fred ^b   Lucassen, Paul J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

Dendate gyrus; Golgi impregnation; LTP; Memory; Neurodegeneration; Neurogenesis

Indexed keywords

TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DATA ANALYSIS; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MALE; MEMORY; MENTAL PERFORMANCE; MORPHOLOGY; MOUSE; MUTATION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PARAMETER; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TAUOPATHY; TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MEMORY; MICE; MICE, TRANSGENIC; NEURONS; PHOSPHORYLATION; TAU PROTEINS; TAUOPATHIES; TIME FACTORS;

EID: 33645454579     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5425-05.2006     Document Type: Article

References (65)

1. Alfarez DN, Joels M, Krugers HJ (2003) Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur J Neurosci 17:1928-1934.
2. Andorfer C, Davies P (2000) PKA phosphorylation on tau: developmental studies in the mouse. Dev Neurosci 4:303-309.
3. Andorfer C, Acker CM, Kress Y, Hof PR, Duff K, Davies P (2005) Cell-cycle reentry and cell death in transgenic mice expressing wild-type human tau isoforms. J Neurosci 25:5446-5454.
4. Angelo M, Plattner F, Irvine EE, Giese KP (2003) Improved reversal learning and altered fear conditioning in transgenic mice with regionally restricted p25 expression. Eur J Neurosci 18:423-431.
5. Arendash GW, Lewis J, Leighty RE, McGowan E, Cracchiolo JR, Hutton M, Garcia MF (2004) Multi-metric behavioral comparison of APPsw and P301L models for Alzheimer's disease: linkage of poorer cognitive performance to tau pathology in forebrain. Brain Res 1012:29-41.
6. Bast T, da Silva BM, Morris RG (2005) Distinct contributions of hippocampal NMDA and AMPA receptors to encoding and retrieval of one-trial place memory. J Neurosci 25:5845-5856.
7. Bronner IF, Ter Meulen BC, Azmani A, Severijnen LA, Willemsen R, Kamphorst W, Ravid R, Heutink P, van Swieten JC (2005) Hereditary Pick's disease with the G272V tau mutation shows predominant three-repeat tau pathology. Brain 128:2645-2653.
8. Buée L, Bussiere T, Buée-Scherrer V, Delacourte A, Hof PR (2000) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 33:95-130.
9. Bussey TJ, Muir JL, Aggleton JP (1999) Functionally dissociating aspects of event memory: the effects of combined perirhinal and postrhinal cortex lesions on object and place memory in the rat. J Neurosci 19:495-502.
10. Chen YG (2005) Specific tau phosphorylation sites in hippocampus correlate with impairment of step-down inhibitory avoidance task in rats. Behav Brain Res 158:277-284.
11. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21:1-14.
12. Crusio WE (2001) Genetic dissection of mouse exploratory behaviour. Behav Brain Res 125:127-132.
13. Davis S, Butcher SP, Morris RG (1992) The NMDA receptor antagonist D-2-amino-5-phosphonopentanoate (D-AP-5) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. J Neurosci 12:21-34.
14. Dawson HN, Ferreira A, Eyster MV, Ghoshal N, Binder LI, Vitek MP (2001) Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J Cell Sci 114:1179-1187.
15. Decker MW, Curzon P, Brioni JD (1995) Influence of separate and combined septal and amygdala lesions on memory, acoustic startle, anxiety, and locomotor activity in rats. Neurobiol Learn Mem 64:156-168.
16. Dewachter I, Reverse D, Caluwaerts N, Ris L, Kuiperi C, Van Den Haute C, Spittaels K, Umans L, Serneels L, Thiry E, Moechars D, Mercken M, Godaux E, Van Leuven F (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.
17. Duchrow M, Schmidt MH, Zingler M, Anemuller S, Bruch HP, Broll R (2001) Suppression of cell division by pKi-67 antisense-RNA and recombinant protein. Cell Physiol Biochem 11:331-338.
18. Endl E, Gerdes J (2000) The Ki-67 protein: fascinating forms and an unknown function. Exp Cell Res 257:231-237.
19. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H, 4 (1984) Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 133:1710-1715.
20. Goedert M, Jakes R (2005) Mutations causing neurodegenerative tauopathies. Biochim Biophys Acta 1739:240-250.
21. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
22. Hammond RS, Tull LE, Stackman RW (2004) On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol Learn Mem 82:26-34.
23. Harley CW, Martin GM (1999) Open field motor patterns and object marking, but not object sniffing, are altered by ibotenate lesions of the hippocampus. Neurobiol Learn Mem 72:202-214.
24. Heine VM, Maslam S, Joels M, Lucassen PJ (2004a) 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.
25. Heine VM, Maslam S, Zareno J, Joels M, Lucassen PJ, 1 (2004b) Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci 19:131-144.
26. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, Miller BI, Geschwind DH, Bird TD, McKeel D, Goate A, Morris JC, Wilhelmsen KC, Schellenberg GD, Trojanowski JQ, Lee VM (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282:1914-1917.
27. Ikeda M, Shoji M, Kawarai T, Kawarabayashi T, Matsubara E, Murakami T, Sasaki A, Tomidokoro Y, Ikarashi Y, Kuribara H, Ishiguro K, Hasegawa M, Yen SH, Chishti MA, Harigaya Y, Abe K, Okamoto K, St George-Hyslop P, Westaway D (2005) Accumulation of filamentous tau in the cerebral cortex of human tau R406W transgenic mice. Am J Pathol 166:521-531.
28. Ingram EM, Spillantini MG (2002) Tau gene mutations: dissecting the pathogenesis of FTDP-17. Trends Mol Med 8:555-562.
29. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, Greenberg DA (2004) Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci USA 101:343-347.
30. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115:97-105.
31. Kesner RP, Ravindranathan A, Jackson P, Giles R, Chiba AA (2001) Aneural circuit analysis of visual recognition memory: role of perirhinal, medial, and lateral entorhinal cortex. Learn Mem 8:87-95.
32. Kobayashi K, Kidani T, Ujike H, Hayashi M, Ishihara T, Miyazu K, Kuroda S, Koshino Y (2003) Another phenotype of frontotemporal dementia and parkinsonism linked to chromosome-17 (FTDP-17) with a missense mutation of S305N closely resembling Pick's disease. J Neurol 250:990-992.
33. Lee VM, Kenyon TK, Trojanowski JQ (2005) Transgenic animal models of tauopathies. Biochim Biophys Acta 1739:251-259.
34. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van Slegtenhorst M, Gwinn-Hardy K, Paul Murphy M, Baker M, Yu X, Duff K, Hardy J, Corral A, Lin WL, Yen SH, Dickson DW, Davies P, Hutton M (2000) Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 25:402-405.
35. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
36. Miller S, Yasuda M, Coats JK, Jones Y, Martone ME, Mayford M (2002) Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36:507-519.
37. Mumby DG (2001) Perspectives on object-recognition memory following hippocampal damage: lessons from studies in rats. Behav Brain Res 127:159-181.
38. Pennanen L, Welzl H, D'Adamo P, Nitsch RM, Gotz J (2004) Accelerated extinction of conditioned taste aversion in P301L tau transgenic mice. Neurobiol Dis 15:500-509.
39. Perez M, Lim F, Arrasate M, Avila J (2000) The FTDP-17-linked mutation R406W abolishes the interaction of phosphorylated tau with microtubules. J Neurochem 74:2583-2589.
40. Pugh PL, Ahmed SF, Smith MI, Upton N, Hunter AJ (2004) A behavioral characterization of the FVB/N mouse strain. Behav Brain Res 155:283-289.
41. Ramakers GJ, Winter J, Hoogland TM, Lequin MB, van Hulten P, van Pelt J, Pool CW (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.
42. Santa Cruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, Guimaraes A, DeTure M, Ramsden M, McGowan E, Forster C, Yue M, Orne J, Janus C, Mariash A, Kuskowski M, Hyman B, Hutton M, Ashe KH (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309:476-481.
43. Selkoe DJ (2005) Defining molecular targets to prevent Alzheimer disease. Arch Neurol 62:192-195.
44. Setou M, Nakagawa T, Seog DH, Hirokawa N (2000) Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288:1796-1802.
45. Setou M, Seog DH, Tanaka Y, Kanai Y, Takei Y, Kawagishi M, Hirokawa N (2002) Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature 417:83-87.
46. Shors TJ (2004) Memory traces of trace memories: neurogenesis, synaptogenesis and awareness. Trends Neurosci 27:250-256.
47. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.
48. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12:578-584.
49. Spittaels K, Van den Haute C, Van Dorpe J, Bruynseels K, Vandezande K, Laenen I, Geerts H, Mercken M, Sciot R, Van Lommel A, Loos R, Van Leuven F (1999) Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol 155:2153-2165.
50. Spittaels K, Van den Haute C, Van Dorpe J, Geerts H, Mercken M, Bruynseels K, Lasrado R, Vandezande K, Laenen I, Boon T, Van Lint J, Vandenheede J, Moechars D, Loos R, Van Leuven F (2000) Glycogen synthase kinase-3beta phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J Biol Chem 275:41340-41349.
51. Sun L, Wang X, Liu S, Wang Q, Wang J, Bennecib M, Gong CX, Sengupta A, Grundke-Iqbal I, Iqbal K (2005) Bilateral injection of isoproterenol into hippocampus induces Alzheimer-like hyperphosphorylation of tau and spatial memory deficit in rat. FEBS Lett 579:251-258.
52. Takei Y, Teng J, Harada A, Hirokawa N (2000) Defects in axonal elongation and neuronal migration in mice with disrupted tau and map1b genes. J Cell Biol 150:989-1000.
53. Takuma H, Arawaka S, Mori H (2003) Isoforms changes of tau protein during development in various species. Brain Res Dev Brain Res 142:121-127.
54. Tanemura K, Murayama M, Akagi T, Hashikawa T, Tominaga T, Ichikawa M, Yamaguchi H, Takashima A (2002) Neurodegeneration with tau accumulation in a transgenic mouse expressing V337M human tau. J Neurosci 22:133-141.
55. Tatebayashi Y, Miyasaka T, Chui DH, Akagi T, Mishima K, Iwasaki K, Fujiwara M, Tanemura K, Murayama M, Ishiguro K, Planel E, Sato S, Hashikawa T, Takashima A (2002) Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau. Proc Natl Acad Sci USA 99:13896-13901.
56. Terwel D, Lasrado R, Snauwaert J, Vandeweert E, Van Haesendonck C, Borghgraef P, 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.
57. Tolnay M, Probst A (1999) Tau protein pathology in Alzheimer's disease and related disorders. Neuropathol Appl Neurobiol 25:171-187.
58. Tsai LH, Lee MS, Cruz J (2004) Cdk5, a therapeutic target for Alzheimer's disease? Biochim Biophys Acta 1697:137-142.
59. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427-13431.
60. van Swieten JC, Stevens M, Rosso SM, Rizzu P, Joosse M, de Koning I, Kamphorst W, Ravid R, Spillantini MG, Niermeijer, Heutink P (1999) Phenotypic variation in hereditary frontotemporal dementia with tau mutations. Ann Neurol 46:617-626.
61. Wang H, Ferguson GD, Pineda VV, Cundiff PE, Storm DR (2004) Overexpression of type-1 adenylyl cyclase in mouse forebrain enhances recognition memory and LTP. Nat Neurosci 7:635-642.
62. Yuen EY, Jiang Q, Feng J, Yan Z (2005) Microtubule regulation of N-methyl-D-aspartate receptor channels in neurons. J Biol Chem 280:29420-29427.
63. Zhang B, Higuchi M, Yoshiyama Y, Ishihara T, Forman MS, Martinez D, Joyce S, Trojanowski JQ, Lee VM (2004) Retarded axonal transport of R406W mutant tau in transgenic mice with a neurodegenerative tauopathy. J Neurosci 24:4657-4667.
64. Zhang B, Maiti A, Shively S, Lakhani F, McDonald-Jones G, Bruce J, Lee EB, Xie SX, Joyce S, Li C, Toleikis PM, Lee VM, Trojanowski JQ (2005) Microtubule-binding drugs offset tau sequestration by stabilizing microtubules and reversing fast axonal transport deficits in a tauopathy model. Proc Natl Acad Sci USA 102:227-231.
65. Zhao Z, Ho L, Suh J, Qin W, Pyo H, Pompl P, Ksiezak-Reding H, Pasinetti GM (2003) A role of P301L tau mutant in anti-apoptotic gene expression, cell cycle and apoptosis. Mol Cell Neurosci 24:367-379.