Human Truncated Tau Induces Mature Neurofibrillary Pathology in a Mouse Model of Human Tauopathy

Journal of Alzheimer's Disease

Volumn 54, Issue 2, 2016, Pages 831-843

  Zimova, Ivana ^a,b   Brezovakova, Veronika ^a   Hromadka, Tomas ^a,b   Weisova, Petronela ^b   Cubinkova, Veronika ^a,b   Valachova, Bernadeta ^a,b   Filipcik, Peter ^a,b   Jadhav, Santosh ^a   Smolek, Tomas ^a,b   Novak, Michal ^a,b   Zilka, Norbert ^a,b  

^a INSTITUTE OF NEUROIMMUNOLOGY   (Slovakia)

^b Axon Neuroscience RandD Services SE ^*  (Slovakia)

Author keywords

Alzheimer's disease; neurofibrillary degeneration; tauopathies; transgenic mouse; truncated tau protein

Indexed keywords

PEPTIDE VACCINE; PROTEIN TYROSINE PHOSPHATASE; SARKOSYL INSOLUBLE TAU PROTEIN; TAU PROTEIN; TAU VACCINE; UNCLASSIFIED DRUG; MAPT PROTEIN, HUMAN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL ANALYSIS; BRAIN REGION; BRAIN STEM; CELL MATURATION; CLINICAL ASSESSMENT; CLINICAL FEATURE; CONTROLLED STUDY; FEMALE; GAIT DISORDER; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LIFESPAN; LOCOMOTION; MALE; MOTOR DYSFUNCTION; MOUSE; NEUROFIBRILLARY TANGLE; NEUROFILAMENT; NEUROPIL THREAD; NONHUMAN; PRECLINICAL STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SENSORY DYSFUNCTION; TAUOPATHY; THERAPY; TRANSGENIC MOUSE; ANIMAL; BIOSYNTHESIS; BRAIN; C57BL MOUSE; DISEASE MODEL; METABOLISM; PATHOLOGY;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROFIBRILLARY TANGLES; TAU PROTEINS; TAUOPATHIES;

EID: 84986630229     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-160347     Document Type: Article

References (34)

1. Reitz C, Mazeux R (2014) Alzheimer disease: Epidemiology, diagnostic criteria, risk factors and biomarkers. Biochem Pharmacol 15, 640-651.
2. Ingelsson M, Fukumoto H, Newell KL, Growdon JH, Hedley-Whyte ET, Frosch MP, Albert MS, Hyman BT, Irizarry MC (2004) Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation inADbrain. Neurology 62, 925-931.
3. Di J, Cohen LS, Corbo CP, Phillips GR, El Idrissi A, Alonso AD (2016) Abnormal tau induces cognitive impairment through two different mechanisms: Synaptic dysfunction and neuronal loss. Sci Rep 6, 20833.
4. Golde TE (2014) Open questions for Alzheimer's disease immunotherapy. Alzheimers Res Ther 6, 3.
5. Jadhav S, Zilka N, Novak M (2013) Protein truncation as a common denominator of human neurodegenerative foldopathies. Mol Neurobiol 48, 516-532.
6. Zilka N, Filipcik P, Koson P, Fialova L, Skrabana R, Zilkova M, Rolkova G, Kontsekova E, Novak M (2006) Truncated tau from sporadic Alzheimer's disease suffices to drive neurofibrillary degeneration in vivo. FEBS Lett 580, 3582-3588.
7. Filipcik P, Zilka N, Bugos O, Kucerak J, Koson P, Novak P, NovakM(2012) First transgenic rat model developing progressive cortical neurofibrillary tangles. Neurobiol Aging 33, 1448-1456.
8. Kontsekova E, Zilka N, Kovacech B, Skrabana R, Novak M (2014) Identification of structural determinants on tau protein essential for its pathological function: Novel therapeutic target for tau immunotherapy in Alzheimer's disease. Alzheimers Res Ther 6, 45.
9. Gallyas F (1971) Silver staining of Alzheimer's neurofibrillary changes by means of physical development. Acta Morphol Acad Hung 19, 1-8.
10. Jadhav S, Katina S,KovacA, Kazmerova Z, NovakM, Zilka N (2015) Truncated tau deregulates synaptic markers in rat model for human tauopathy. Front Cell Neurosci 23, 9-24.
11. Moller KA, Berge OG, Hamers FP (2008) Using the Cat-Walk method to assess weight-bearing and pain behaviour in walking rats with ankle joint monoarthritis induced by carrageenan: Effect of morphine and rofecoxib. J Neurosci Methods 174, 1-9.
12. Chiang CHY, Sheu ML, Cheng FC, Chen CH, Su H, Sheehan J, Pan H (2013) Comprehensive analysis of neurobehavior associated with histomorphological alterations in a chronic constrictive nerve injury model through use of the CatWalk XT system. J Neurosurg 120, 250-262.
13. Koopmans GC, Deumens R, Honig WM, Hamers FP, SteinbuschHW, Joosten EA (2005) The assessment of locomotor function in spinal cord injured rats: The importance of objective analysis of coordination. J Neurotrauma 22, 214-225.
14. Do Carmo S, Cuello AC (2013) Modeling Alzheimer's disease in transgenic rats. Mol Neurodegener 8, 27.
15. Asuni AA, Boutajangout A, Quartermain D, Sigurdsson EM (2007) Immunotherapy targeting pathological tau conformers in a tangle mouse model reduces brain pathology with associated functional improvements. J Neurosci 27, 9115-9129.
16. Bi M, Ittner A, Ke YD, Gotz J, Ittner LM (2011) Tau-targeted immunization impedes progression of neurofibrillary histopathology in aged P301L tau transgenic mice. PloS One 6, e26860.
17. Castillo-Carranza DL, Sengupta U, Guerrero-Munoz MJ, Lasagna-Reeves CA, Gerson JE, Singh G, Estes DM, Barrett AD, Dineley KT, Jackson GR, Kayer R (2014) Passive immunization with tau oligomer monoclonal antibody reverses tauopathy phenotypes without affecting hyperphosphorylated neurofibrillary tangles. J Neurosci 34, 4260-4272.
18. Allen B, Ingram E, Takao M, Smith MJ, Jakes R, Virdee K, Yashida H, Holyer M, Craxton M, Emson PC, Atzori C, Migheli A, Crowther RA, Ghetti B, Spinallantini MG, GoedertM(2002) Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 22, 9340-9351.
19. Richter M, Mewes A, Fritsch M, Krugel U, Hoffman R, SingerD(2014) Doubly phosphorylated peptide vaccines to protect transgenic P301S mice against Alzheimer's disease like tau aggregation. Vaccines 2, 601-623.
20. Chai X, Wu S, Murray TK, Kinley R, Cella CV, Sims H, Bruckner N, Hanmer J, Davies P, O'Neill MJ, Hutton ML, Citron M (2011) Passive immunization with anti-Tau antibodies in two transgenic models: Reduction of Tau pathology and delay of disease progression. J Biol Chem 286, 34457-34467.
21. Troquier L, Caillierez R, Burnouf S, Fernandez-Gomez FJ, Grosjean ME, Zommer N, Sergeant N, Schraen-Maschke S, Blum D, Buee L (2012) Targeting phosphor-Ser422 by active tau immunotherapy in the THYTau22 mouse model: Asuitable therapeutic approach. Curr Alzheimer Res 9, 397-405.
22. Dai CL, Cen X, Kazim SF, Liu F, Gong CX, Grundke-Iqbal I, Iqbal K (2014) Passive immunization targeting the N-terminal projection domain of tau decreases tau pathology and improves cognition in a transgenic mouse model of Alzheimer disease and tauopathies. J Neural Transm 122, 607-617.
23. Walls KC, Ager RR, Vasilevko V, Cheng D, Medeiros R, LaFerla FM (2014) p-Tau immunotherapy reduces soluble and insoluble tau in aged 3xTg-AD mice. Neurosci Lett 575, 96-100.
24. Collin L, Bohrmann B, Gopfert U, Oroszlan-Szovik K, Ozmen L, Gruninger F (2014) Neuronal uptake of tau/pS422 antibody and reduced progression of tau pathology in a mouse model of Alzheimer's disease. Brain 137, 2834-2846.
25. Sigurdsson EM (2008) Immunotherapy targeting pathological tau protein in Alzheimer's disease and related tauopathies. J Alzheimers Dis 15, 157-168.
26. Boutajangout A, Quartemain D, Sigurdsson EM (2010) Immunotherapy targeting pathological tau prevents cognitive decline in a new tangle mouse model. J Neurosci 30, 16559-16566.
27. Terwel D, Lasrado R, Snauwaert J,Vaneweert E,Van Haeendonck C, Borghgraef P, Van Leuven F (2005) Changed conformation of mutant Tau-P301L underlies the moribund tauopathy, absent in progressive, nonlethal axonopathy of Tau-4R/2N transgenic mice. J Biol Chem 280, 3963-3973.
28. Ramsden M, Kotilinek L, Forster C, Paulson J, McGowan E, SantaCruz K, Guimaraes A, Yue M, Lewis J, Carlson G, Hutton M, Ashe KH (2005) Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J Neurosci 25, 10637-10647.
29. Lewis J, McGowan E, Rockwood J, Melrose H, Nachraju P, Van Slegtenhorst M, Gwinn-Hardy K, Paul Murphy M, Baker M,Yu X, DuffK, 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.
30. Sahara N, Lewis J, DeTure M, McGowan E, Dickson DW, Hutton M,Yen SH(2002) Assembly of tau in transgenic animals expressing P301L tau: Alteration of phosphorylation and solubility. J Neurochem 83, 1498-1508.
31. Takeuchi H, Iba M, Inoue H, Higuch M, Takao K, Tsukita K, Karatsu Y, Iwamoto Y, Miyakawa T, Suhara T, Trojanowski JQ, Lee V, Takahashi R (2005) P301S mutant human tau transgenic mice manifest early symptoms of human tauopathies with dementia and altered sensorimotor gating. PloS One 6, e21050.
32. Brook SP, Dunnett SB (2009) Tests to assess motor phenotype in mice: A user's guide. Nat Rev Neurosci 10, 519-529.
33. 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.
34. Koson P, Zilka N, Kovac A, Kovacech B, Korenova M, Filipcik P, Novak M (2008) Truncated tau expression levels determine life span of a rat model of tauopathy without causing neuronal loss or correlating with terminal neurofibrillary tangle load. Eur J Neurosci 28, 239-246.