Staging of Alzheimer's pathology in triple transgenic mice: A light and electron microscopic analysis

International Journal of Alzheimer's Disease

Volumn , Issue , 2010, Pages

  Mufson, Elliott J ^a   Oh, Kwang Jin ^a   Perez, Sylvia E ^a   Lagalwar, Sarita ^b   Vana, Laurel ^b   Binder, Lester ^b  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; LEUCINE; METHIONINE; PRESENILIN 1; PROLINE; TAU PROTEIN; VALINE;

AGING; ALZHEIMER DISEASE; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CYTOPLASM; DISEASE SEVERITY; ELECTRON MICROSCOPY; FEMALE; FLUORESCENCE MICROSCOPY; GENE MUTATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MICROSCOPY; MOUSE; MUTANT; NERVE CELL; NEUROPATHOLOGY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SUBICULUM;

EID: 77955953363     PISSN: None     EISSN: 20900252     Source Type: Journal    
DOI: 10.4061/2010/780102     Document Type: Article

References (70)

1. Eriksen J. L., Janus C. G., Plaques, tangles, and memory loss in mouse models of neurodegeneration Behavior Genetics 2007 37 1 79 100
2. Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clemens J., Donaldson T., Gillespie F., Guido T., Hagoplan S., Johnson-Wood K., Khan K., Lee M., Leibowitz P., Lieberburg I., Little S., Masliah E., Alzheimer-type neuropathology in transgenic mice overexpressing V717F -amyloid precursor protein Nature 1995 373 6514 523 527
3. Oddo S., Caccamo A., Tran L., Lambert M. P., Glabe C. G., Klein W. L., LaFerla F. M., Temporal profile of amyloid- (A ) oligomerization in an in vivo model of Alzheimer disease: a link between A and tau pathology Journal of Biological Chemistry 2006 281 3 1599 1604
4. Gtz J., Deters N., Doldissen A., Bokhari L., Ke Y., Wiesner A., Schonrock N., Ittner L. M., A decade of tau transgenic animal models and beyond Brain Pathology 2007 17 1 91 103
5. Gtz J., Streffer J. R., David D., Schild A., Hoerndli F., Pennanen L., Kurosinski P., Chen F., Transgenic animal models of Alzheimer's disease and related disorders: histopathology, behavior and therapy Molecular Psychiatry 2004 9 7 664 683
6. Spires T. L., Hyman B. T., Transgenic models of Alzheimer's disease: learning from animals NeuroRx 2005 2 3 423 437
7. Allen B., Ingram E., Takao M., Smith M. J., Jakes R., Virdee K., Yoshida H., Holzer M., Craxton M., Emson P. C., Atzori C., Migheli A., Anthony Crowther R., Ghetti B., Spillantini M. G., Goedert M., Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301s tau protein Journal of Neuroscience 2002 22 21 9340 9351
8. Gtz J., Chen F., Barmettler R., Nitsch R. M., Tau filament formation in transgenic mice expressing P301L tau Journal of Biological Chemistry 2001 276 1 529 534
9. Lewis J., McGowan E., Rockwood J., Melrose H., Nacharaju P., Van Slegtenhorst M., Gwinn-Hardy K., Murphy M. P., Baker M., Yu X., Duff K., Hardy J., Corral A., Lin W.-L., Yen S.-H., Dickson D. W., Davies P., Hutton M., Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L)tau protein Nature Genetics 2000 25 4 402 405
10. Lin W.-L., Lewis J., Yen S.-H., Hutton M., Dickson D. W., Ultrastructural neuronal pathology in transgenic mice expressing mutant (P301L) human tau Journal of Neurocytology 2003 32 9 1091 1105
11. Billings L. M., Oddo S., Green K. N., McGaugh J. L., LaFerla F. M., Intraneuronal A causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice Neuron 2005 45 5 675 688
12. Oddo S., Caccamo A., Kitazawa M., Tseng B. P., LaFerla F. M., Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease Neurobiology of Aging 2003 24 8 1063 1070
13. Oddo S., Caccamo A., Shepherd J. D., Murphy M. P., Golde T. E., Kayed R., Metherate R., Mattson M. P., Akbari Y., LaFerla F. M., Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular A and synaptic dysfunction Neuron 2003 39 3 409 421
14. Oddo S., Caccamo A., Smith I. F., Green K. N., LaFerla F. M., A dynamic relationship between intracellular and extracellular pools of A American Journal of Pathology 2006 168 1 184 194
15. Overk C. R., Kelley C. M., Mufson E. J., Brainstem Alzheimer's-like pathology in the triple transgenic mouse model of Alzheimer's disease Neurobiology of Disease 2009 35 3 415 425
16. Hirata-Fukae C., Li H.-F., Hoe H.-S., Gray A. J., Minami S. S., Hamada K., Niikura T., Hua F., Tsukagoshi-Nagai H., Horikoshi-Sakuraba Y., Mughal M., Rebeck G. W., LaFerla F. M., Mattson M. P., Iwata N., Saido T. C., Klein W. L., Duff K. E., Aisen P. S., Matsuoka Y., Females exhibit more extensive amyloid, but not tau, pathology in an Alzheimer transgenic model Brain Research 2008 1216 92 103
17. Mastrangelo M. A., Bowers W. J., Detailed immunohistochemical characterization of temporal and spatial progression of Alzheimer's disease-related pathologies in male triple-transgenic mice BMC Neuroscience 2008 9, article 81
18. Conti C. J., Larcher F., Chesner J., Aldaz C. M., Polyacrylamide gel electrophoresis and immunoblotting of proteins extracted from paraffin-embedded tissue sections Journal of Histochemistry and Cytochemistry 1988 36 5 547 550
19. Matsuo E. S., Shin R.-W., Billingsley M. L., Van DeVoorde A., O'Connor M., Trojanowski J. Q., Lee V. M.-Y., Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau Neuron 1994 13 4 989 1002
20. Fox C. H., Johnson F. B., Whiting J., Roller P. P., Formaldehyde fixation Journal of Histochemistry and Cytochemistry 1985 33 8 845 853
21. Pollock N. J., Wood J. G., Differential sensitivity of the microtubule-associated protein, tau, in Alzheimer's disease tissue to formalin fixation Journal of Histochemistry and Cytochemistry 1988 36 9 1117 1121
22. Riederer B. M., Antigen preservation tests for immunocytochemical detection of cytoskeletal proteins: influence of aldehyde fixatives Journal of Histochemistry and Cytochemistry 1989 37 5 675 681
23. Riederer B. M., Porchet R., Marugg R. A., Binder L. I., Solubility of cytoskeletal proteins in immunohistochemistry and the influence of fixation Journal of Histochemistry and Cytochemistry 1993 41 4 609 616
24. Trojanowski J. Q., Obrocka M. A., Lee V. M.-Y., Distribution of neurofilament subunits in neurons and neuronal processes: immunohistochemical studies of bovine cerebellum with subunit-specific monoclonal antibodies Journal of Histochemistry and Cytochemistry 1985 33 6 557 563
25. Trojanowski J. Q., Schuck T., Schmidt M. L., Lee V. M.-Y., Distribution of tau proteins in the normal human central and peripheral nervous system Journal of Histochemistry and Cytochemistry 1989 37 2 209 215
26. Vickers J. C., Riederer B. M., Marugg R. A., Alterations in neurofilament protein immunoreactivity in human hippocampal neurons related to normal aging and Alzheimer's disease Neuroscience 1994 62 1 1 13
27. Goedert M., Jakes R., Crowther R. A., Cohen P., Vanmechelen E., Vandermeeren M., Cras P., Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: identification of phosphorylation sites in tau protein Biochemical Journal 1994 301 3 871 877
28. Mercken M., Vandermeeren M., Lubke U., Six J., Boons J., Van de Voorde A., Martin J.-J., Gheuens J., Monoclonal antibodies with selective specificity for Alzheimer Tau are directed against phosphatase-sensitive epitopes Acta Neuropathologica 1992 84 3 265 272
29. Goedert M., Jakes R., Vanmechelen E., Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205 Neuroscience Letters 1995 189 3 167 169
30. Greenberg S. G., Davies P., A preparation of Alzheimer paired helical filaments that displays distinct proteins by polyacrylamide gel electrophoresis Proceedings of the National Academy of Sciences of the United States of America 1990 87 15 5827 5831
31. Lang E., Szendrei G. I., Lee V. M.-Y., Otvos L. Jr., Immunological and conformational characterization of a phosphorylated immunodominant epitope on the paired helical filaments found in Alzheimer's disease Biochemical and Biophysical Research Communications 1992 187 2 783 790
32. Otvos L. Jr., Feiner L., Lang E., Szendrei G. I., Goedert M., Lee V. M.-Y., Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404 Journal of Neuroscience Research 1994 39 6 669 673
33. Carmel G., Mager E. M., Binder L. I., Kuret J., The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology Journal of Biological Chemistry 1996 271 51 32789 32795
34. Jicha G. A., Berenfeld B., Davies P., Sequence requirements for formation of conformational variants of tau similar to those found in Alzheimer's disease Journal of Neuroscience Research 1999 55 6 713 723
35. Jicha G. A., Bowser R., Kazam I. G., Davies P., Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau Journal of Neuroscience Research 1997 48 2 128 132
36. Wolozin B. L., Pruchnicki A., Dickson D. W., Davies P., A neuronal antigen in the brains of Alzheimer patients Science 1986 232 4750 648 650
37. Rye D. B., Leverenz J., Greenberg S. G., Davies P., Saper C. B., The distribution of Alz-50 immunoreactivity in the normal human brain Neuroscience 1993 56 1 109 127
38. Yan S. D., Yan S. F., Chen X., Fu J., Chen M., Kuppusamy P., Smith M. A., Perry G., Godman G. C., Nawroth P., Zweier J. L., Stern D., Non-enzymatically glycated tau in Alzheimer's disease induces neuronal oxidant stress resulting in cytokine gene expression and release of amyloid -peptide Nature Medicine 1995 1 7 693 699
39. De Felice F. G., Velasco P. T., Lambert M. P., Viola K., Fernandez S. J., Ferreira S. T., Klein W. L., A oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine Journal of Biological Chemistry 2007 282 15 11590 11601
40. De Felice F. G., Wu D., Lambert M. P., Fernandez S. J., Velasco P. T., Lacor P. N., Bigio E. H., Jerecic J., Acton P. J., Shughrue P. J., Chen-Dodson E., Kinney G. G., Klein W. L., Alzheimer's disease-type neuronal tau hyperphosphorylation induced by A oligomers Neurobiology of Aging 2008 29 9 1334 1347
41. Ferreira S. T., Vieira M. N. N., De Felice F. G., Soluble protein oligomers as emerging toxins in Alzheimer's and other amyloid diseases IUBMB Life 2007 59 4-5 332 345
42. Glabe C. G., Structural classification of toxic amyloid oligomers Journal of Biological Chemistry 2008 283 44 29639 29643
43. Lacor P. N., Buniel M. C., Furlow P. W., Clemente A. S., Velasco P. T., Wood M., Viola K. L., Klein W. L., A oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease Journal of Neuroscience 2007 27 4 796 807
44. Lambert M. P., Velasco P. T., Chang L., Viola K. L., Fernandez S., Lacor P. N., Khuon D., Gong Y., Bigio E. H., Shaw P., De Felice F. G., Krafft G. A., Klein W. L., Monoclonal antibodies that target pathological assemblies of A Journal of Neurochemistry 2007 100 1 23 35
45. Shankar G. M., Bloodgood B. L., Townsend M., Walsh D. M., Selkoe D. J., Sabatini B. L., Natural oligomers of the Alzheimer amyloid- protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway Journal of Neuroscience 2007 27 11 2866 2875
46. Walsh D. M., Hartley D. M., Condron M. M., Selkoe D. J., Teplow D. B., In vitro studies of amyloid -protein fibril assembly and toxicity provide clues to the aetiology of Flemish variant (Ala692 → Gly) Alzheimer's disease Biochemical Journal 2001 355 3 869 877
47. Walsh D. M., Selkoe D. J., A oligomersa decade of discovery Journal of Neurochemistry 2007 101 5 1172 1184
48. Hirata-Fukae C., Li H.-F., Ma L., Hoe H.-S., Rebeck G. W., Aisen P. S., Matsuoka Y., Levels of soluble and insoluble tau reflect overall status of tau phosphorylation in vivo Neuroscience Letters 2009 450 1 51 55
49. Carroll J. C., Rosario E. R., Chang L., Stanczyk F. Z., Oddo S., LaFerla F. M., Pike C. J., Progesterone and estrogen regulate Alzheimer-like neuropathology in female 3xTg-AD mice Journal of Neuroscience 2007 27 48 13357 13365
50. Garver T. D., Harris K. A., Lehman R. A. W., Lee V. M.-Y., Trojanowski J. Q., Billingsley M. L., Phosphorylation in human, primate, and rat brain: evidence that a pool of is highly phosphorylated in vivo and is rapidly dephosphorylated in vitro Journal of Neurochemistry 1994 63 6 2279 2287
51. Trojanowski J. Q., Lee V. M.-Y., Phosphorylation of paired helical filament tau in Alzheimer's disease neurofibrillary lesions: focusing on phosphatases FASEB Journal 1995 9 15 1570 1576
52. Liang Z., Liu F., Iqbal K., Grundke-Iqbal I., Wegiel J., Gong C.-X., Decrease of protein phosphatase 2A and its association with accumulation and hyperphosphorylation of tau in Down syndrome Journal of Alzheimer's Disease 2008 13 3 295 302
53. Wang J.-Z., Grundke-Iqbal I., Iqbal K., Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration European Journal of Neuroscience 2007 25 1 59 68
54. Liu F., Grundke-Iqbal I., Iqbal K., Gong C.-X., Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation European Journal of Neuroscience 2005 22 8 1942 1950
55. Souli C., Lpagnol J., Delacourte A., Caillet-Boudin M. L., Dephosphorylation studies of SKNSH-SY 5Y cell Tau proteins by endogenous phosphatase activity Neuroscience Letters 1996 206 2-3 189 192
56. Lavenex P., Lavenex P. B., Bennett J. L., Amaral D. G., Postmortem changes in the neuroanatomical characteristics of the primate brain: hippocampal formation Journal of Comparative Neurology 2009 512 1 27 51
57. Movsesyan N., Ghochikyan A., Mkrtichyan M., Petrushina I., Davtyan H., Olkhanud P. B., Head E., Biragyn A., Cribbs D. H., Agadjanyan M. G., Reducing AD-like pathology in 3xTg-AD mouse model by DNA epitope vaccinea novel immunotherapeutic strategy PLoS ONE 2008 3 5, article e2124
58. Oddo S., Billings L., Kesslak J. P., Cribbs D. H., LaFerla F. M., A immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome Neuron 2004 43 3 321 332
59. Lewis J., Dickson D. W., Lin W.-L., Chisholm L., Corral A., Jones G., Yen S.-H., Sahara N., Skipper L., Yager D., Eckman C., Hardy J., Hutton M., McGowan E., Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP Science 2001 293 5534 1487 1491
60. Ramsden M., Kotilinek L., Forster C., Paulson J., McGowan E., SantaCruz K., Guimaraes A., Yue M., Lewis J., Carlson G., Hutton M., Ashe K. H., Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L) Journal of Neuroscience 2005 25 46 10637 10647
61. Augustinack J. C., Schneider A., Mandelkow E.-M., Hyman B. T., Specific tau phosphorylation sites correlate with severity of neuronal cytopathology in Alzheimer's disease Acta Neuropathologica 2002 103 1 26 35
62. Binder L. I., Guillozet-Bongaarts A. L., Garcia-Sierra F., Berry R. W., Tau, tangles, and Alzheimer's disease Biochimica et Biophysica Acta 2005 1739 2 216 223
63. Luna-Muoz J., Chvez-Macas L., Garca-Sierra F., Mena R., Earliest stages of tau conformational changes are related to the appearance of a sequence of specific phospho-dependent tau epitopes in Alzheimer's disease Journal of Alzheimer's Disease 2007 12 4 365 375
64. Luna-Muoz J., Garca-Sierra F., Falcn V., Menndez I., Chvez-Macas L., Mena R., Regional conformational change involving phosphorylation of tau protein at the Thr231, precedes the structural change detected by Alz-50 antibody in Alzheimer's disease Journal of Alzheimer's Disease 2005 8 1 29 41
65. Alonso A. D. C., Zaidi T., Novak M., Grundke-Iqbal I., Iqbal K., Hyperphosphorylation induces self-assembly of into tangles of paired helical filaments/straight filaments Proceedings of the National Academy of Sciences of the United States of America 2001 98 12 6923 6928
66. Goedert M., Tau gene mutations and their effects Movement Disorders 2005 20 12 S45 S52
67. Braak E., Braak H., Mandelkow E.-M., A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads Acta Neuropathologica 1994 87 6 554 567
68. Sassin I., Schultz C., Thal D. R., Rb U., Arai K., Braak E., Braak H., Evolution of Alzheimer's disease-related cytoskeletal changes in the basal nucleus of Meynert Acta Neuropathologica 2000 100 3 259 269
69. Duff K., Knight H., Refolo L. M., Sanders S., Yu X., Picciano M., Malester B., Hutton M., Adamson J., Goedert M., Burki K., Davies P., Characterization of pathology in transgenic mice over-expressing human genomic and cDNA tau transgenes Neurobiology of Disease 2000 7 2 87 98
70. Ginsberg S. D., Che S., Counts S. E., Mufson E. J., Shift in the ratio of three-repeat tau and four-repeat tau mRNAs in individual cholinergic basal forebrain neurons in mild cognitive impairment and Alzheimer's disease Journal of Neurochemistry 2006 96 5 1401 1408