Long-Term In Vivo Imaging of Fibrillar Tau in the Retina of P301S Transgenic Mice

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Schön, Christian ^a,b   Hoffmann, Nadine A ^a,b   Ochs, Simon M ^a   Burgold, Steffen ^a,b   Filser, Severin ^a   Steinbach, Sonja ^a   Seeliger, Mathias W ^c   Arzberger, Thomas ^b   Goedert, Michel ^d   Kretzschmar, Hans A ^b   Schmidt, Boris ^e   Herms, Jochen ^a  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^e DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; BIOACCUMULATION; CELL FATE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIAGNOSTIC VALUE; DISEASE ASSOCIATION; EXPERIMENTAL MOUSE; HUMAN; HUMAN TISSUE; IN VIVO STUDY; MOLECULAR IMAGING; MOUSE; NEUROFIBRILLARY TANGLE; NEUROFILAMENT; NEUROPATHOLOGY; NONHUMAN; PROGRESSIVE SUPRANUCLEAR PALSY; PROTEIN AGGREGATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RETINA; TAUOPATHY; TISSUE DISTRIBUTION; TRANSGENIC MOUSE;

ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MIDDLE AGED; PHOSPHORYLATION; RETINA; TAU PROTEINS; TAUOPATHIES;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 84871812476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053547     Document Type: Article

References (46)

1. Goedert M, (2004) Tau protein and neurodegeneration. Semin Cell Dev Biol 15: 45-49.
2. Hasegawa M, Smith MJ, Goedert M, (1998) Tau proteins with FTDP-17 mutations have a reduced ability to promote microtubule assembly. FEBS Lett 437: 207-210.
3. Hong M, Zhukareva V, Vogelsberg-Ragaglia V, Wszolek Z, Reed L, et al. (1998) Mutation-specific functional impairments in distinct tau isoforms of hereditary FTDP-17. Science 282: 1914-1917.
4. Goedert M, Jakes R, (2005) Mutations causing neurodegenerative tauopathies. Biochim Biophys Acta 1739: 240-250.
5. Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, et al. (2011) Alzheimer's disease. Lancet 377: 1019-1031.
6. Fox NC, Freeborough PA, Rossor MN, (1996) Visualisation and quantification of rates of atrophy in Alzheimer's disease. Lancet 348: 94-97.
7. Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, et al. (2004) Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound-B. Ann Neurol 55: 306-319.
8. Nordberg A, (2004) PET imaging of amyloid in Alzheimer's disease. Lancet Neurol 3: 519-527.
9. Iseri PK, Altinas O, Tokay T, Yuksel N, (2006) Relationship between cognitive impairment and retinal morphological and visual functional abnormalities in Alzheimer disease. J Neuroophthalmol 26: 18-24.
10. Lu Y, Li Z, Zhang X, Ming B, Jia J, et al. (2010) Retinal nerve fiber layer structure abnormalities in early Alzheimer's disease: evidence in optical coherence tomography. Neurosci Lett 480: 69-72.
11. Paquet C, Boissonnot M, Roger F, Dighiero P, Gil R, et al. (2007) Abnormal retinal thickness in patients with mild cognitive impairment and Alzheimer's disease. Neurosci Lett 420: 97-99.
12. Berisha F, Feke GT, Trempe CL, McMeel JW, Schepens CL, (2007) Retinal abnormalities in early Alzheimer's disease. Invest Ophthalmol Vis Sci 48: 2285-2289.
13. Koronyo-Hamaoui M, Koronyo Y, Ljubimov AV, Miller CA, Ko MK, et al. (2011) Identification of amyloid plaques in retinas from Alzheimer's patients and noninvasive in vivo optical imaging of retinal plaques in a mouse model. Neuroimage 54Suppl 1: 204-217.
14. Liu B, Rasool S, Yang Z, Glabe CG, Schreiber SS, et al. (2009) Amyloid-peptide vaccinations reduce {beta}-amyloid plaques but exacerbate vascular deposition and inflammation in the retina of Alzheimer's transgenic mice. Am J Pathol 175: 2099-2110.
15. Ning A, Cui J, To E, Ashe KH, Matsubara J, (2008) Amyloid-beta deposits lead to retinal degeneration in a mouse model of Alzheimer disease. Invest Ophthalmol Vis Sci 49: 5136-5143.
16. Perez SE, Lumayag S, Kovacs B, Mufson EJ, Xu S, (2009) Beta-amyloid deposition and functional impairment in the retina of the APPswe/PS1DeltaE9 transgenic mouse model of Alzheimer's disease. Invest Ophthalmol Vis Sci 50: 793-800.
17. Allen B, Ingram E, Takao M, Smith MJ, Jakes R, et al. (2002) Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 22: 9340-9351.
18. Gasparini L, Crowther RA, Martin KR, Berg N, Coleman M, et al. (2011) Tau inclusions in retinal ganglion cells of human P301S tau transgenic mice: effects on axonal viability. Neurobiol Aging 32: 419-433.
19. Magnani E, Fan J, Gasparini L, Golding M, Williams M, et al. (2007) Interaction of tau protein with the dynactin complex. EMBO J 26: 4546-4554.
20. Bull ND, Guidi A, Goedert M, Martin KR, Spillantini MG, (2012) Reduced axonal transport and increased excitotoxic retinal ganglion cell degeneration in mice transgenic for human mutant P301S tau. PLoS One 7: e34724.
21. Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K, (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112: 389-404.
22. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, et al. (1991) The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41: 479-486.
23. Seeliger MW, Beck SC, Pereyra-Munoz N, Dangel S, Tsai JY, et al. (2005) In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy. Vision Res 45: 3512-3519.
24. Velasco A, Fraser G, Delobel P, Ghetti B, Lavenir I, et al. (2008) Detection of filamentous tau inclusions by the fluorescent Congo red derivative FSB [(trans, trans)-1-fluoro-2,5-bis(3-hydroxycarbonyl-4-hydroxy)styrylbenzene]. FEBS Lett 582: 901-906.
25. Otvos L Jr, Feiner L, Lang E, Szendrei GI, Goedert M, et al. (1994) Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404. J Neurosci Res 39: 669-673.
26. Charbel Issa P, Singh MS, Lipinski DM, Chong NV, Delori FC, et al. (2012) Optimization of in vivo confocal autofluorescence imaging of the ocular fundus in mice and its application to models of human retinal degeneration. Invest Ophthalmol Vis Sci 53: 1066-1075.
27. Xu H, Chen M, Manivannan A, Lois N, Forrester JV, (2008) Age-dependent accumulation of lipofuscin in perivascular and subretinal microglia in experimental mice. Aging Cell 7: 58-68.
28. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, et al. (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51.
29. Walsh MK, Quigley HA, (2008) In vivo time-lapse fluorescence imaging of individual retinal ganglion cells in mice. J Neurosci Methods 169: 214-221.
30. Koronyo Y, Salumbides BC, Black KL, Koronyo-Hamaoui M, (2012) Alzheimer's disease in the retina: imaging retinal abeta plaques for early diagnosis and therapy assessment. Neurodegener Dis 10: 285-293.
31. Blanks JC, Hinton DR, Sadun AA, Miller CA, (1989) Retinal ganglion cell degeneration in Alzheimer's disease. Brain Res 501: 364-372.
32. Hinton DR, Sadun AA, Blanks JC, Miller CA, (1986) Optic-nerve degeneration in Alzheimer's disease. N Engl J Med 315: 485-487.
33. Leger F, Fernagut PO, Canron MH, Leoni S, Vital C, et al. (2011) Protein aggregation in the aging retina. J Neuropathol Exp Neurol 70: 63-68.
34. Bolander A, Kieser D, Voss C, Bauer S, Schon C, et al. (2012) Bis(arylvinyl)pyrazines,-pyrimidines, and-pyridazines As Imaging Agents for Tau Fibrils and beta-Amyloid Plaques in Alzheimer's Disease Models. J Med Chem.
35. Higuchi M, Iwata N, Matsuba Y, Sato K, Sasamoto K, et al. (2005) 19F and 1H MRI detection of amyloid beta plaques in vivo. Nat Neurosci 8: 527-533.
36. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM, (2003) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 24: 1063-1070.
37. Radde R, Bolmont T, Kaeser SA, Coomaraswamy J, Lindau D, et al. (2006) Abeta42-driven cerebral amyloidosis in transgenic mice reveals early and robust pathology. EMBO Rep 7: 940-946.
38. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, et al. (2001) Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 276: 21562-21570.
39. de Calignon A, Fox LM, Pitstick R, Carlson GA, Bacskai BJ, et al. (2010) Caspase activation precedes and leads to tangles. Nature 464: 1201-1204.
40. 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.
41. Condello C, Schain A, Grutzendler J, (2011) Multicolor time-stamp reveals the dynamics and toxicity of amyloid deposition. Sci Rep 1: 19.
42. Oka T, Tagawa K, Ito H, Okazawa H, (2011) Dynamic changes of the phosphoproteome in postmortem mouse brains. PLoS One 6: e21405.
43. Maurage CA, Ruchoux MM, de Vos R, Surguchov A, Destee A, (2003) Retinal involvement in dementia with Lewy bodies: a clue to hallucinations? Ann Neurol 54: 542-547.
44. Surguchov A, McMahan B, Masliah E, Surgucheva I, (2001) Synucleins in ocular tissues. J Neurosci Res 65: 68-77.
45. Gupta N, Fong J, Ang LC, Yucel YH, (2008) Retinal tau pathology in human glaucomas. Can J Ophthalmol 43: 53-60.
46. Wostyn P, Audenaert K, De Deyn PP, (2009) Alzheimer's disease and glaucoma: is there a causal relationship? Br J Ophthalmol 93: 1557-1559.