Cognition and hippocampal synaptic plasticity in mice with a homozygous tau deletion

Neurobiology of Aging

Volumn 35, Issue 11, 2014, Pages 2474-2478

  Ahmed, Tariq ^a   Van der Jeugd, Ann ^a   Blum, David ^b,c,d   Galas, Marie Christine ^b,c,d   D'Hooge, Rudi ^a   Buee, Luc ^b,c,d   Balschun, Detlef ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b INSERM   (France)

^c UNIV LILLE   (France)

^d JEAN PIERRE AUBERT RESEARCH CENTER   (France)

Author keywords

Alzheimer's disease; Cognition; Hippocampus; Long term depression; Morris water maze; Synaptic plasticity; Tau knock out mice

Indexed keywords

TAU PROTEIN;

ANIMAL EXPERIMENT; ANXIETY; ARTICLE; COGNITION; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; FACILITATION; HIPPOCAMPAL CA1 REGION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MORRIS WATER MAZE TEST; MOTOR PERFORMANCE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; SPATIAL LEARNING; SYNAPTIC TRANSMISSION; WILD TYPE; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENE DELETION; HIPPOCAMPUS; HOMOZYGOTE; KNOCKOUT MOUSE; METABOLISM; MICROTUBULE; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; TAUOPATHY;

ANIMALS; COGNITION; DISEASE MODELS, ANIMAL; GENE DELETION; HIPPOCAMPUS; HOMOZYGOTE; LONG-TERM POTENTIATION; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULES; NEURONAL PLASTICITY; SPATIAL LEARNING; SYNAPTIC TRANSMISSION; TAU PROTEINS; TAUOPATHIES;

EID: 84922913225     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.05.005     Document Type: Article

References (35)

1. Ahmed T., Sabanov V., D'Hooge R., Balschun D. An N-methyl-D-aspartate-receptor dependent, late-phase long-term depression in middle-aged mice identifies no GluN2-subunit bias. Neuroscience 2011, 185:27-38. Epub 2011 Apr 12, 27-38.
2. Ashe K.H., Zahs K.R. Probing the biology of Alzheimer's disease. Neuron 2010, 66:631-645.
3. Bailey C.H., Giustetto M., Huang Y.Y., Hawkins R.D., Kandel E.R. Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory?. Nat. Rev. Neurosci. 2000, 1:11-20.
4. Balschun D., Wolfer D.P., Gass P., Mantamadiotis T., Welzl H., Schütz G., Frey J.U., Lipp H.P. Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory?. J.Neurosci. 2003, 23:6304-6314.
5. Bear M.F., Abraham W.C. Long-term depression in hippocampus. Annu. Rev. Neurosci. 1996, 19:437-462.
6. Boekhoorn K., Terwel D., Biemans B., Borghgraef P., Wiegert O., Ramakers G.J., de Vos K., Krugers H., Tomiyama T., Mori H., Joels M., van Leuven F., Lucassen P.J. Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy. J.Neurosci. 2006, 26:3514-3523.
7. Buee L., Bussiere T., Buee-Scherrer V., Delacourte A., Hof P.R. Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res. Rev. 2000, 33:95-130.
8. Burnouf S., Martire A., Derisbourg M., Laurent C., Belarbi K., Leboucher A., Fernandez-Gomez F.J., Troquier L., Eddarkaoui S., Grosjean M.E., Demeyer D., Muhr-Tailleux A., Buisson A., Sergeant N., Hamdane M., Humez S., Popoli P., Buee L., Blum D. NMDA receptor dysfunction contributes to impaired brain-derived neurotrophic factor-induced facilitation of hippocampal synaptic transmission in a Tau transgenic model. Aging Cell 2013, 12:11-23.
9. Cuchillo-Ibanez I., Seereeram A., Byers H.L., Leung K.-Y., Ward M.A., Anderton B.H., Hanger D.P. Phosphorylation of tau regulates its axonal transport by controlling its binding to kinesin. FASEB J. 2008, 22:3186-3195.
10. Dawson H.N., Ferreira A., Eyster M.V., Ghoshal N., Binder L.I., Vitek M.P. Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J.Cell Sci 2001, 114:1179-1187.
11. Dawson H.N., Cantillana V., Jansen M., Wang H., Vitek M.P., Wilcock D.N., Lynch J.R., Laskowitz D.T. Loss of tau elicits axonal degeneration in a mouse model of Alzheimer's disease. Neurosci 2010, 169:516-531.
12. Denk F., Wade-Martins R. Knockout and transgenic mouse models of tauopathies. Neurobiol. Aging 2009, 30:1-13.
13. D'Hooge R., Lullmann-Rauch R., Beckers T., Balschun D., Schwake M., Reiss K., vonFigura K., Saftig P. Neurocognitive and psychotiform behavioral alterations and enhanced hippocampal long-term potentiation in transgenic mice displaying neuropathological features of human alpha-mannosidosis. J.Neurosci. 2005, 25:6539-6549.
14. Dubey M., Pulkit C.P., Kabiru H., Shea T.B. Tau inhibits anterograde axonal transport and perturbs stability in growing axonal neurites in part by displacing kinesin cargo: neurofilaments attenuate tau-mediated neurite instability. Cell Motil. Cytoskeleton 2008, 65:89-99.
15. Fedulov V., Rex C.S., Simmons D.A., Palmer L., Gall C.M., Lynch G. Evidence that long-term potentiation occurs within individual hippocampal synapses during learning. J.Neurosci. 2007, 27:8031-8039.
16. Goddyn H., Leo S., Meert T., D'Hooge R. Differences in behavioural test battery performance between mice with hippocampal and cerebellar lesions. Behav. Brain Res. 2006, 173:138-147.
17. Harada A., Oguchi K., Okabe S., Kuno J., Terada S., Ohshima T., Sato-Yoshitake R., Takei Y., Noda T., Hirokawa N. Altered microtubule organisation in small-calibre axons of mice lacking tau protein. Nature 1994, 369:488-491.
18. Ikegami S., Harad A., Hirokawa N. Muscle weakness, hyperactivity and impairement in fear conditioning in tau-deficient mice. Neurosci. Lett. 2000, 279:129-132.
19. Ittner L.M., Ke Y.D., Delerue F., Bi M., Gladbach A., van E.J., Wolfing H., Chieng B.C., Christie M.J., Napier I.A., Eckert A., Staufenbiel M., Hardeman E., Gotz J. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010, 142:387-397.
20. Janus C. Conditionally inducible tau mice - designing a better mouse model of neurodegenerative diseases. Gene Brain Behav. 2008, 7:12-27.
21. Kimura T., Whitcomb D.J., Jo J., Regan P., Piers T., Heo S., Brown C., Hashikawa T., Murayama M., Seok H., Sotiropoulos I., Kim E., Collingridge G.L., Takashima A., Cho K. Microtubule-associated protein tau is essential for long-term depression in the hippocampus. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2014, 369:20130144.
22. Lo A.C., Iscru E., Blum D., Tesseur I., Callaerts-Vegh Z., Buée L., De Strooper B., Balschun D., D'Hooge R. Amyloid and tau neuropathology differentially affect prefrontal synaptic plasticity and cognitive performance in mouse models of Alzheimer's disease. J.Alzheimers Dis. 2013, 37:109-125.
23. Martin S.J., Grimwood P.D., Morris R.G.M. Synaptic plasticity and memory. Ann. Rev. Neurosci. 2000, 23:649-711.
24. Meiri N., Sun M.-K., Segal Z., Alkon D.L. Memory and long-term potentiation (LTP) dissociated: normal spatial memory despite CA1 LTP elimination with Kv1.4 antisense. Proc. Natl. Acad. Sci. U.S.A 1998, 95:15037-15042.
25. Morris M., Hamto P., Adame A., Devidze N., Masliah E., Mucke L. Age-appropriate cognition and subtle dopamine-independent motor deficits in aged Tau knockout mice. Neurobiol. Aging 2013, 34:1523-1529.
26. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992, 106:274-285.
27. Roberson E.D., Scearce-Levie K., Palop J.J., Yan F., Cheng I.H., Wu T., Gerstein H., Yu G.Q., Mucke L. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 2007, 316:750-754.
28. Sergeant N., Bretteville A., Hamdane M., Caillet-Boudin M.L., Grognet P., Bombois S., Blum D., Delacourte A., Pasquier F., Vanmechelen E., Schraen-Maschke S., Buée L. Biochemistry of tau in Alzheimer's disease and related neurological disorders. Exp. Rev. Proteomics 2008, 5:207-224.
29. Shipton O.A., Leitz J.R., Dworzak J., Acton C.E., Tunbridge E.M., Denk F., Dawson H.N., Vitek M.P., Wade-Martins R., Paulsen O., Vargas-Caballero M. Tau protein is required for amyloid (beta)-induced impairment of hippocampal long-term potentiation. J.Neurosci. 2011, 31:1688-1692.
30. Spires-Jones T.L., Stoothoff W.H., de Calignon A., Jones P.B., Hyman B.T. Tau pathophysiology in neurodegeneration: a tangled issue. Trend Neurosci. 2009, 32:150-159.
31. Tucker K.L., Meyer M., Barde Y.A. Neurotrophins are required for nerve growth during development. Nat. Neurosci. 2001, 4:29-37.
32. Van der Jeugd A., Ahmed T., Burnouf S., Belarbi K., Hamdame M., Grosjean M.-E., Humez S., Balschun D., Blum D., Buée L., D'Hooge R. Hippocampal tauopathy in tau transgenic mice coincides with impaired hippocampus-dependent learning and memory, and attenuated late-phase long-term depression of synaptic transmission. Neurobiol. Learn Mem. 2010, 95:296-304.
33. Weingarten M.D., Lockwood A.D., Hwo S.-Y., Kirschener M.W. Aprotein factor essential for microtubule assembly. Proc. Nat. Acad. Sci. U.S.A 1975, 72:1858-1862.
34. Whitlock J.R., Heynen A.J., Shuler M.G., Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 2006, 313:1093-1097.
35. Wilsch V.W., Behnisch T., Jäger T., Reymann K.G., Balschun D. When are class I metabotropic glutamate receptors necessary for long-term potentiation?. J.Neurosci. 1998, 18:6071-6080.