Human P301L-Mutant Tau Expression in Mouse Entorhinal-Hippocampal Network Causes Tau Aggregation and Presynaptic Pathology but No Cognitive Deficits

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Harris, Julie A ^a,b   Koyama, Akihiko ^a   Maeda, Sumihiro ^a,b   Ho, Kaitlyn ^a   Devidze, Nino ^a   Dubal, Dena B ^a,b   Yu, Gui Qiu ^a   Masliah, Eliezer ^c,d   Mucke, Lennart ^a,b  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPSIN; TAU PROTEIN;

AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DENTATE GYRUS; ENTORHINAL CORTEX; FEMALE; GRANULE CELL; HIPPOCAMPUS; LEARNING; MALE; MEMORY; MOUSE; NERVE ENDING; NONHUMAN; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SYNAPSE; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ALZHEIMER DISEASE; ANIMALS; DENTATE GYRUS; ENTORHINAL CORTEX; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; HUMANS; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MILD COGNITIVE IMPAIRMENT; MUTATION, MISSENSE; PATTERN RECOGNITION, VISUAL; PERFORANT PATHWAY; RECOGNITION (PSYCHOLOGY); SYNAPSES; TAU PROTEINS;

MUS;

EID: 84866681445     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045881     Document Type: Article

References (67)

1. Huang Y, Mucke L, (2012) Alzheimer mechanisms and therapeutic strategies. Cell 148: 1204-1222.
2. Bertram L, Lill CM, Tanzi RE, (2010) The genetics of Alzheimer disease: back to the future. Neuron 68: 270-281.
3. Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, et al. (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393: 702-705.
4. Reed LA, Wszolek ZK, Hutton M, (2001) Phenotypic correlations in FTDP-17. Neurobiol Aging 22: 89-107.
5. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, et al. (2000) Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 25: 402-405.
6. SantaCruz K, Lewis J, Spires T, Paulson J, Kotilinek L, et al. (2005) Tau suppression in a neurodegenerative mouse model improves memory function. Science 309: 476-481.
7. Braak H, Braak E, (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239-259.
8. Braak H, Rüb U, Schultz C, Del Tredici K, (2006) Vulnerability of cortical neurons to Alzheimer's and Parkinson's diseases. J Alzheimers Dis 9: 35-44.
9. Braak H, Del Tredici K, (2011) The pathological process underlying Alzheimer's disease in individuals under thirty. Acta Neuropathol 121: 171-181.
10. Braak H, Braak E, Yilmazer D, de Vos RAI, Jansen ENH, et al. (1996) Pattern of brain destruction in Parkinson's and Alzheimer's diseases. J Neural Transm 103: 455-490.
11. Braak H, Braak E, (1997) Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol Aging 18: 351-357.
12. Gomez-Isla T, Price JL, McKeel DW Jr, Morris JC, Growdon JH, et al. (1996) Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 16: 4491-4500.
13. Masdeu JC, Zubieta JL, Arbizu J, (2005) Neuroimaging as a marker of the onset and progression of Alzheimer's disease. J Neurol Sci 236: 55-64.
14. Eichenbaum H, Lipton PA, (2008) Towards a functional organization of the medial temporal lobe memory system: role of the parahippocampal and medial entorhinal cortical areas. Hippocampus 18: 1314-1324.
15. Squire LR, Stark CE, Clark RE, (2004) The medial temporal lobe. Annu Rev Neurosci 27: 279-306.
16. deIpolyi AR, Rankin KP, Mucke L, Miller BL, Gorno-Tempini ML, (2007) Spatial cognition and the human navigation network in AD and MCI. Neurology 69: 986-997.
17. Monacelli AM, Cushman LA, Kavcic V, Duffy CJ, (2003) Spatial disorientation in Alzheimer's disease: The remembrance of things passed. Neurology 61: 1491-1497.
18. Frost B, Jacks RL, Diamond MI, (2009) Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 284: 12845-12852.
19. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, et al. (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11: 909-913.
20. Sydow A, Mandelkow EM, (2010) 'Prion-like' propagation of mouse and human tau aggregates in an inducible mouse model of tauopathy. Neurodegener Dis 7: 28-31.
21. Guo JL, Lee VM, (2011) Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J Biol Chem 286: 15317-15331.
22. Lee SJ, Lim HS, Masliah E, Lee HJ, (2011) Protein aggregate spreading in neurodegenerative diseases: Problems and perspectives. Neurosci Res 70: 339-348.
23. Harris JA, Devidze N, Verret L, Ho K, Halabisky B, et al. (2010) Transsynaptic progression of amyloid-beta-induced neuronal dysfunction within the entorhinal-hippocampal network. Neuron 68: 428-441.
24. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, et al. (2005) Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci 25: 10637-10647.
25. Yasuda M, Mayford MR, (2006) CaMKII activation in the entorhinal cortex disrupts previously encoded spatial memory. Neuron 50: 309-318.
26. Harris JA, Devidze N, Halabisky B, Lo I, Thwin MT, et al. (2010) Many neuronal and behavioral impairments in transgenic mouse models of Alzheimer's disease are independent of caspase cleavage of the amyloid precursor protein. J Neurosci 30: 372-381.
27. Sun A, Nguyen XV, Bing G, (2002) Comparative analysis of an improved thioflavin-s stain, Gallyas silver stain, and immunohistochemistry for neurofibrillary tangle demonstration on the same sections. J Histochem Cytochem 50: 463-472.
28. Spencer B, Marr RA, Gindi R, Potkar R, Michael S, et al. (2011) Peripheral delivery of a CNS targeted, metalo-protease reduces abeta toxicity in a mouse model of Alzheimer's disease. PLoS One 6: e16575.
29. Ubhi K, Rockenstein E, Doppler E, Mante M, Adame A, et al. (2009) Neurofibrillary and neurodegenerative pathology in APP-transgenic mice injected with AAV2-mutant TAU: neuroprotective effects of Cerebrolysin. Acta Neuropathol 117: 699-712.
30. Berger Z, Roder H, Hanna A, Carlson A, Rangachari V, et al. (2007) Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. J Neurosci 27: 3650-3662.
31. Young ME, Clark MH, Goffus A, Hoane MR (2009) Mixed Effects Modeling of Morris Water Maze Data: Advantages and Cautionary Notes. Learning and Motivation, v40 n2 p160-177.
32. Schindowski K, Bretteville A, Leroy K, Begard S, Brion JP, et al. (2006) Alzheimer's disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. Am J Pathol 169: 599-616.
33. Takeuchi H, Iba M, Inoue H, Higuchi M, Takao K, et al. (2011) P301S mutant human tau transgenic mice manifest early symptoms of human tauopathies with dementia and altered sensorimotor gating. PLoS One 6: e21050.
34. Tatebayashi Y, Miyasaka T, Chui DH, Akagi T, Mishima K, et al. (2002) Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau. Proc Natl Acad Sci U S A 99: 13896-13901.
35. Cisse M, Halabisky B, Harris J, Devidze N, Dubal DB, et al. (2011) Reversing EphB2 depletion rescues cognitive functions in Alzheimer model. Nature 469: 47-52.
36. Jicha GA, Bowser R, Kazam IG, Davies P, (1997) 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.
37. Sze CI, Troncoso JC, Kawas C, Mouton P, Price DL, et al. (1997) Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J Neuropathol Exp Neurol 56: 933-944.
38. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, et al. (1991) Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann Neurol 30: 572-580.
39. Chin J, Palop J, Puoliväli J, Massaro C, Yu G-Q, et al. (2004) Overexpression of fyn kinase exacerbates cellular and behavioral deficits in human amyloid precursor protein transgenic mice. Neurobiol Aging 25: 18.
40. Hsia A, Masliah E, McConlogue L, Yu G, Tatsuno G, et al. (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96: 3228-3233.
41. Mucke L, Masliah E, Yu G-Q, Mallory M, Rockenstein EM, et al. (2000) High-level neuronal expression of Aβ1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation. J Neurosci 20: 4050-4058.
42. Tomiyama T, Matsuyama S, Iso H, Umeda T, Takuma H, et al. (2010) A mouse model of amyloid {beta} oligomers: their contribution to synaptic alteration, abnormal tau phosphorylation, glial activation, and neuronal loss in vivo. J Neurosci 30: 4845-4856.
43. Ashe KH, Zahs KR, (2010) Probing the biology of Alzheimer's disease in mice. Neuron 66: 631-645.
44. Morris M, Maeda S, Vossel K, Mucke L, (2011) The many faces of tau. Neuron 70: 410-426.
45. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, et al. (2007) Reducing endogenous tau ameliorates amyloid β-induced deficits in an Alzheimer's disease mouse model. Science 316: 750-754.
46. Roberson ED, Halabisky B, Yoo JW, Yao J, Chin J, et al. (2011) Amyloid-beta/Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease. J Neurosci 31: 700-711.
47. Vossel KA, Zhang K, Brodbeck J, Daub AC, Sharma P, et al. (2010) Tau reduction prevents Abeta-induced defects in axonal transport. Science 330: 198.
48. Shipton OA, Leitz JR, Dworzak J, Acton CE, Tunbridge EM, et al. (2011) Tau protein is required for amyloid {beta}-induced impairment of hippocampal long-term potentiation. J Neurosci 31: 1688-1692.
49. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, et al. (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 142: 387-397.
50. Kimura T, Yamashita S, Fukuda T, Park JM, Murayama M, et al. (2007) Hyperphosphorylated tau in parahippocampal cortex impairs place learning in aged mice expressing wild-type human tau. EMBO J 26: 5143-5152.
51. Steffenach HA, Witter M, Moser MB, Moser EI, (2005) Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45: 301-313.
52. Remondes M, Schuman EM, (2004) Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 431: 699-703.
53. Verret L, Mann EO, Hang GB, Barth AM, Cobos I, et al. (2012) Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149: 708-721.
54. Dayton RD, Wang DB, Cain CD, Schrott LM, Ramirez JJ, et al. (2012) Frontotemporal lobar degeneration-related proteins induce only subtle memory-related deficits when bilaterally overexpressed in the dorsal hippocampus. Exp Neurol 233: 807-814.
55. Giannakopoulos P, Herrmann FR, Bussiere T, Bouras C, Kovari E, et al. (2003) Tangle and neuron numbers, but not amyloid load, predict cognitive status in Alzheimer's disease. Neurology 60: 1495-1500.
56. Murakami T, Paitel E, Kawarabayashi T, Ikeda M, Chishti MA, et al. (2006) Cortical neuronal and glial pathology in TgTauP301L transgenic mice: neuronal degeneration, memory disturbance, and phenotypic variation. Am J Pathol 169: 1365-1375.
57. Boekhoorn K, Terwel D, Biemans B, Borghgraef P, Wiegert O, et al. (2006) Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy. J Neurosci 26: 3514-3523.
58. Kremer A, Maurin H, Demedts D, Devijver H, Borghgraef P, et al. (2011) Early improved and late defective cognition is reflected by dendritic spines in Tau.P301L mice. J Neurosci 31: 18036-18047.
59. Frost B, Diamond MI, (2010) Prion-like mechanisms in neurodegenerative diseases. Nat Rev Neurosci 11: 155-159.
60. Goedert M, Clavaguera F, Tolnay M, (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 33: 317-325.
61. Braak H, Del Tredici K, (2011) Alzheimer's pathogenesis: is there neuron-to-neuron propagation? Acta Neuropathol 121: 589-595.
62. Barten DM, Cadelina GW, Hoque N, DeCarr LB, Guss VL, et al. (2011) Tau transgenic mice as models for cerebrospinal fluid tau biomarkers. J Alzheimers Dis 24 (Suppl 2): 127-141.
63. Liu L, Drouet V, Wu JW, Witter MP, Small SA, et al. (2012) Trans-synaptic spread of tau pathology in vivo. PLoS One 7: e31302.
64. de Calignon A, Polydoro P, Suarez-Calvet M, William C, Adamowicz DH, et al. (2012) Propagation of Tau Pathology in a Model of Early Alzheimer's Disease. Neuron 73: 685-697.
65. Callahan LM, Selski DJ, Martzen MR, Cheetham JE, Coleman PD, (1994) Preliminary evidence: decreased GAP-43 message in tangle-bearing neurons relative to adjacent tangle-free neurons in Alzheimer's disease parahippocampal gyrus. Neurobiol Aging 15: 381-386.
66. Miyasaka T, Morishima-Kawashima M, Ravid R, Kamphorst W, Nagashima K, et al. (2001) Selective deposition of mutant tau in the FTDP-17 brain affected by the P301L mutation. J Neuropathol Exp Neurol 60: 872-884.
67. Aoyagi H, Hasegawa M, Tamaoka A, (2007) Fibrillogenic nuclei composed of P301L mutant tau induce elongation of P301L tau but not wild-type tau. J Biol Chem 282: 20309-20318.