TOC1: A valuable tool in assessing disease progression in the rTg4510 mouse model of tauopathy

Neurobiology of Disease

Volumn 67, Issue , 2014, Pages 37-48

  Ward, Sarah M ^a,d   Himmelstein, Diana S ^a   Ren, Yan ^b   Fu, Yifan ^a   Yu, Xiao Wen ^a   Roberts, Kaleigh ^a   Binder, Lester I ^a,d   Sahara, Naruhiko ^b,c  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^d MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Filament; Neurodegenerative diseases; Oligomer; Oxidation; Reduction; Tauopathies

Indexed keywords

AB39 ANTIBODY; CP13 ANTIBODY; MC1 ANTIBODY; MONOCLONAL ANTIBODY; OLIGOMER; TAU OLIGOMER COMPLEX 1; TAU OLIGOMER COMPLEX 1 ANTIBODY; TAU PROTEIN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; MAPT PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DIMERIZATION; DISEASE COURSE; IMMUNOREACTIVITY; MOUSE; NEUROFIBRILLARY TANGLE; NONHUMAN; OLIGOMERIZATION; OXIDATION REDUCTION STATE; PATHOLOGY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TAUOPATHY; ANIMAL; BRAIN; CHEMISTRY; DISEASE MODEL; HUMAN; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL; BIOLOGICAL MARKERS; BRAIN; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; HUMANS; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; PROTEIN MULTIMERIZATION; TAU PROTEINS; TAUOPATHIES;

EID: 84897520975     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.03.002     Document Type: Article

References (51)

1. Alonso A.C., Zaidi T., Grundke-Iqbal I., Iqbal K. Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:5562-5566.
2. Andorfer C., Acker C.M., Kress Y., Hof P.R., Duff K., Davies P. Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J. Neurosci. 2005, 25:5446-5454.
3. Arriagada P.V., Growdon J.H., Hedley-Whyte E.T., Hyman B.T. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 1992, 42:631-639.
4. Berger Z., Roder H., Hanna A., Carlson A., Rangachari V., Yue M., Wszolek Z., Ashe K., Knight J., Dickson D., et al. Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. J. Neurosci. 2007, 27:3650-3662.
5. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
6. Carmel G., Leichus B., Cheng X., Patterson S.D., Mirza U., Chait B.T., Kuret J. Expression, purification, crystallization, and preliminary X-ray analysis of casein kinase-1 from Schizosaccharomyces pombe. J. Biol. Chem. 1994, 269:7304-7309.
7. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., Lansbury P.T. Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:571-576.
8. Dickson D.W., Ksiezak-Reding H., Liu W.K., Davies P., Crowe A., Yen S.H. Immunocytochemistry of neurofibrillary tangles with antibodies to subregions of tau protein: identification of hidden and cleaved tau epitopes and a new phosphorylation site. Acta Neuropathol. 1992, 84:596-605.
9. Ferrer I., Santpere G., van Leeuwen F.W. Argyrophilic grain disease. Brain 2008, 131:1416-1432.
10. Gamblin T.C., King M.E., Dawson H., Vitek M.P., Kuret J., Berry R.W., Binder L.I. In vitro polymerization of tau protein monitored by laser light scattering: method and application to the study of FTDP-17 mutants. Biochemistry 2000, 39:6136-6144.
11. Gamblin T.C., King M.E., Kuret J., Berry R.W., Binder L.I. Oxidative regulation of fatty acid-induced tau polymerization. Biochemistry 2000, 39:14203-14210.
12. Gamblin T.C., Berry R.W., Binder L.I. Modeling tau polymerization in vitro: a review and synthesis. Biochemistry 2003, 42:15009-15017.
13. Gamblin T.C., Chen F., Zambrano A., Abraha A., Lagalwar S., Guillozet A.L., Lu M., Fu Y., Garcia-Sierra F., LaPointe N., et al. Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10032-10037.
14. Garcia-Sierra F., Ghoshal N., Quinn B., Berry R.W., Binder L.I. Conformational changes and truncation of tau protein during tangle evolution in Alzheimer's disease. J. Alzheimer's Dis. 2003, 5:65-77.
15. Goedert M., Spillantini M.G., Jakes R., Rutherford D., Crowther R.A. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989, 3:519-526.
16. Gomez-Isla T., Hollister R., West H., Mui S., Growdon J.H., Petersen R.C., Parisi J.E., Hyman B.T. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann. Neurol. 1997, 41:17-24.
17. Guillozet-Bongaarts A.L., Garcia-Sierra F., Reynolds M.R., Horowitz P.M., Fu Y., Wang T., Cahill M.E., Bigio E.H., Berry R.W., Binder L.I. Tau truncation during neurofibrillary tangle evolution in Alzheimer's disease. Neurobiol. Aging 2005, 26:1015-1022.
18. Guillozet-Bongaarts A.L., Cahill M.E., Cryns V.L., Reynolds M.R., Berry R.W., Binder L.I. Pseudophosphorylation of tau at serine422 inhibits caspase cleavage: in vitro evidence and implications for tangle formation in vivo. J. Neurochem. 2006, 97:1005-1014.
19. Iqbal K., Alonso Adel C., Chen S., Chohan M.O., El-Akkad E., Gong C.X., Khatoon S., Li B., Liu F., Rahman A., et al. Tau pathology in Alzheimer disease and other tauopathies. Biochim. Biophys. Acta 2005, 1739:198-210.
20. Janocko N.J., Brodersen K.A., Soto-Ortolaza A.I., Ross O.A., Liesinger A.M., Duara R., Graff-Radford N.R., Dickson D.W., Murray M.E. Neuropathologically defined subtypes of Alzheimer's disease differ significantly from neurofibrillary tangle-predominant dementia. Acta Neuropathol. 2012, 124:681-692.
21. 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. J. Neurosci. Res. 1997, 48:128-132.
22. Khlistunova I., Biernat J., Wang Y., Pickhardt M., von Bergen M., Gazova Z., Mandelkow E., Mandelkow E.M. Inducible expression of Tau repeat domain in cell models of tauopathy: aggregation is toxic to cells but can be reversed by inhibitor drugs. J. Biol. Chem. 2006, 281:1205-1214.
23. Lasagna-Reeves C.A., Castillo-Carranza D.L., Guerrero-Muoz M.J., Jackson G.R., Kayed R. Preparation and characterization of neurotoxic tau oligomers. Biochemistry 2010, 49:10039-10041.
24. Lasagna-Reeves C.A., Castillo-Carranza D.L., Sengupta U., Guerrero-Munoz M.J., Kiritoshi T., Neugebauer V., Jackson G.R., Kayed R. Alzheimer brain-derived tau oligomers propagate pathology from endogenous tau. Sci. Rep. 2012, 2:700.
25. Lasagna-Reeves C.A., Castillo-Carranza D.L., Sengupta U., Sarmiento J., Troncoso J., Jackson G.R., Kayed R. Identification of oligomers at early stages of tau aggregation in Alzheimer's disease. FASEB J. 2012, 26(5):1946-1959.
26. Lee V.M., Goedert M., Trojanowski J.Q. Neurodegenerative tauopathies. Annu. Rev. Neurosci. 2001, 24:1121-1159.
27. Lewis J., McGowan E., Rockwood J., Melrose H., Nacharaju P., Van Slegtenhorst M., Gwinn-Hardy K., Paul Murphy M., Baker M., Yu X., et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat. Genet. 2000, 25:402-405.
28. Maeda S., Sahara N., Saito Y., Murayama M., Yoshiike Y., Kim H., Miyasaka T., Murayama S., Ikai A., Takashima A. Granular tau oligomers as intermediates of tau filaments. Biochemistry 2007, 46:3856-3861.
29. Meraz-Rios M.A., Lira-De Leon K.I., Campos-Pena V., De Anda-Hernandez M.A., Mena-Lopez R. Tau oligomers and aggregation in Alzheimer's disease. J. Neurochem. 2010, 112:1353-1367.
30. Morsch R., Simon W., Coleman P.D. Neurons may live for decades with neurofibrillary tangles. J. Neuropathol. Exp. Neurol. 1999, 58:188-197.
31. Novak M. Truncated tau protein as a new marker for Alzheimer's disease. Acta Virol. 1994, 38:173-189.
32. Novitskaya V., Bocharova O.V., Bronstein I., Baskakov I.V. Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons. J. Biol. Chem. 2006, 281:13828-13836.
33. 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 Abeta and synaptic dysfunction. Neuron 2003, 39:409-421.
34. Patterson K.R., Remmers C., Fu Y., Brooker S., Kanaan N.M., Vana L., Ward S., Reyes J.F., Philibert K., Glucksman M.J., et al. Characterization of prefibrillar tau oligomers in vitro and in Alzheimer disease. J. Biol. Chem. 2011, 286:23063-23076.
35. Ramsden M., Kotilinek L., Forster C., Paulson J., McGowan E., SantaCruz K., Guimaraes A., Yue M., Lewis J., Carlson G., et al. Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L). J. Neurosci. 2005, 25:10637-10647.
36. Reyes J.F., Reynolds M.R., Horowitz P.M., Fu Y., Guillozet-Bongaarts A.L., Berry R., Binder L.I. A possible link between astrocyte activation and tau nitration in Alzheimer's disease. Neurobiol. Dis. 2008, 31:198-208.
37. Sahara N., Lewis J., DeTure M., McGowan E., Dickson D.W., Hutton M., Yen S.H. Assembly of tau in transgenic animals expressing P301L tau: alteration of phosphorylation and solubility. J. Neurochem. 2002, 83:1498-1508.
38. Sahara N., Murayama M., Mizoroki T., Urushitani M., Imai Y., Takahashi R., Murata S., Tanaka K., Takashima A. In vivo evidence of CHIP up-regulation attenuating tau aggregation. J. Neurochem. 2005, 94:1254-1263.
39. Sahara N., Maeda S., Murayama M., Suzuki T., Dohmae N., Yen S.H., Takashima A. Assembly of two distinct dimers and higher-order oligomers from full-length tau. Eur. J. Neurosci. 2007, 25:3020-3029.
40. Sahara N., Maeda S., Takashima A. Tau oligomerization: a role for tau aggregation intermediates linked to neurodegeneration. Curr. Alzheimer Res. 2008, 5:591-598.
41. Sahara N., Deture M., Ren Y., Ebrahim A.S., Kang D., Knight J., Volbracht C., Pedersen J.T., Dickson D.W., Yen S.H., et al. Characteristics of TBS-extractable hyperphosphorylated tau species: aggregation intermediates in rTg4510 mouse brain. J. Alzheimers Dis. 2013, 33(1):249-263.
42. Santacruz K., Lewis J., Spires T., Paulson J., Kotilinek L., Ingelsson M., Guimaraes A., DeTure M., Ramsden M., McGowan E., et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005, 309:476-481.
43. Schweers O., Mandelkow E.M., Biernat J., Mandelkow E. Oxidation of cysteine-322 in the repeat domain of microtubule-associated protein tau controls the in vitro assembly of paired helical filaments. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:8463-8467.
44. Spires T.L., Orne J.D., SantaCruz K., Pitstick R., Carlson G.A., Ashe K.H., Hyman B.T. Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am. J. Pathol. 2006, 168:1598-1607.
45. Vana L., Kanaan N.M., Ugwu I.C., Wuu J., Mufson E.J., Binder L.I. Progression of tau pathology in cholinergic basal forebrain neurons in mild cognitive impairment and Alzheimer's disease. Am. J. Pathol. 2011, 179:2533-2550.
46. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
47. Ward S.M., Himmelstein D.S., Lancia J.K., Fu Y., Patterson K.R., Binder L.I. TOC1: characterization of a selective oligomeric tau antibody. J. Alzheimers Dis. 2013, 37(3):593-602.
48. Weingarten M.D., Lockwood A.H., Hwo S.Y., Kirschner M.W. A protein factor essential for microtubule assembly. Proc. Natl. Acad. Sci. U. S. A. 1975, 72:1858-1862.
49. Yao T., Tomoo K., Ishida T., Hasegawa H., Sasaki M., Taniguchi T. Aggregation analysis of the microtubule binding domain n tau protein by spectroscopic methods. J. Biochem. (Tokyo) 2003, 134:91-99.
50. Yen S.H., Dickson D.W., Crowe A., Butler M., Shelanski M.L. Alzheimer's neurofibrillary tangles contain unique epitopes and epitopes in common with the heat-stable microtubule associated proteins tau and MAP2. Am. J. Pathol. 1987, 126:81-91.
51. Yoshiyama Y., Higuchi M., Zhang B., Huang S.M., Iwata N., Saido T.C., Maeda J., Suhara T., Trojanowski J.Q., Lee V.M. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007, 53:337-351.