Abnormal tau induces cognitive impairment through two different mechanisms: Synaptic dysfunction and neuronal loss

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Di, J ^a   Cohen, L S ^a   Corbo, C P ^b   Phillips, G R ^a   El Idrissi, A ^a   Alonso, A D ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b WAGNER COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL; BIOSYNTHESIS; CELL DEATH; COGNITIVE DEFECT; DISEASE MODEL; GENETICS; GLIOSIS; HIPPOCAMPAL CA1 REGION; HUMAN; METABOLISM; MOUSE; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; SYNAPSE; TRANSGENIC MOUSE; TUMOR CELL LINE;

ALZHEIMER DISEASE; ANIMALS; CA1 REGION, HIPPOCAMPAL; CELL DEATH; CELL LINE, TUMOR; COGNITIVE DYSFUNCTION; DISEASE MODELS, ANIMAL; GLIOSIS; HUMANS; MICE; MICE, TRANSGENIC; NEURONS; PHOSPHORYLATION; SYNAPSES; TAU PROTEINS;

EID: 84959036980     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20833     Document Type: Article

References (63)

1. Lee, V. M., Goedert, M., Trojanowski, J. Q. Neurodegenerative tauopathies. Annu Rev Neurosci 24, 1121-1159 (2001).
2. Iqbal, K., Liu, F., Gong, C. X., Alonso, A. D., Grundke-Iqbal, I. Mechanisms of tau-induced neurodegeneration. Acta Neuropathol 118, 53-69 (2009).
3. McKee, A. C. et al. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J Neuropathol Exp Neurol 68, 709-735 (2009).
4. Murray, M. E. et al. Clinicopathologic and 11C-Pittsburgh compound B implications of Thal amyloid phase across the Alzheimer's disease spectrum. Brain 138, 1370-1381 (2015).
5. Alonso, A. D., Zaidi, T., Novak, M., Grundke-Iqbal, I., Iqbal, K. Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc Natl Acad Sci USA. 98, 6923-6928 (2001).
6. LaFerla, F. M., Green, K. N. Animal models of Alzheimer disease. Cold Spring Harb Perspect Med 2, a006320, doi: 10.1101/cshperspect.a006320 (2012).
7. Platt, T. L., Reeves, V. L., Murphy, M. P. Transgenic models of Alzheimer's disease: better utilization of existing models through viral transgenesis. Biochim Biophys Acta 1832, 1437-1448 (2013).
8. Berger, Z. et al. Accumulation of pathological tau species and memory loss in a conditional model of tauopathy. J Neurosci 27, 3650-3662 (2007).
9. Roberson, E. D. et al. 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 (2011).
10. Sydow, A. et al. Tau-induced defects in synaptic plasticity, learning, and memory are reversible in transgenic mice after switching off the toxic Tau mutant. J Neurosci 31, 2511-2525 (2011).
11. Lasagna-Reeves, C. A., Castillo-Carranza, D. L., Sengupta, U., Clos, A. L., Jackson, G. R., Kayed, R. Tau oligomers impair memory and induce synaptic and mitochondrial dysfunction in wild-type mice. Mol Neurodegener 6, 39 (2011).
12. Eckermann, K. et al. The beta-propensity of Tau determines aggregation and synaptic loss in inducible mouse models of tauopathy. J Biol Chem 282, 31755-31765 (2007).
13. Webster, S. J., Bachstetter, A. D., Nelson, P. T., Schmitt, F. A., Van Eldik, L. J. Using mice to model Alzheimer's dementia: an overview of the clinical disease and the preclinical behavioral changes in 10 mouse models. Front Genet 5, 88 (2014).
14. Research Models Database. http://www.alzforum.org/research-models. (accessed June 16, 2014)
15. Lewis, J. et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 25, 402-405 (2000).
16. Lewis, J. et al. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293, 1487-1491 (2001).
17. Tanemura, K. et al. Formation of filamentous tau aggregations in transgenic mice expressing V337M human tau. Neurobiol Dis 8, 1036-1045 (2001).
18. Tanemura, K. et al. Neurodegeneration with tau accumulation in a transgenic mouse expressing V337M human tau. J Neurosci 22, 133-141 (2002).
19. Tatebayashi, Y. et al. Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau. Proc Natl Acad Sci USA 99, 13896-13901 (2002).
20. Santacruz, K. et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science 309, 476-481 (2005).
21. Schindowski, K. et al. 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 (2006).
22. Yoshiyama, Y. et al. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 53, 337-351 (2007).
23. Hundelt, M. et al. Altered phosphorylation but no neurodegeneration in a mouse model of tau hyperphosphorylation. Neurobiol Aging 32, 991-1006 (2011).
24. Flunkert, S. et al. Elevated levels of soluble total and hyperphosphorylated tau result in early behavioral deficits and distinct changes in brain pathology in a new tau transgenic mouse model. Neurodegener Dis 11, 194-205 (2013).
25. 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 Neuropathol 103, 26-35 (2002).
26. Alonso, A. D., Mederlyova, A., Novak, M., Grundke-Iqbal, I., Iqbal, K. Promotion of hyperphosphorylation by frontotemporal dementia tau mutations. J Biol Chem 279, 34873-34881 (2004).
27. Stoothoff, W. H., Johnson, G. V. Tau phosphorylation: physiological and pathological consequences. Biochim Biophys Acta 1739, 280-297 (2005).
28. Buee, L. et al. From tau phosphorylation to tau aggregation: what about neuronal death?Biochem Soc Trans 38, 967-972 (2010).
29. Alonso, A. D. et al. Phosphorylation of tau at Thr212, Thr231, and Ser262 combined causes neurodegeneration. J Biol Chem 285, 30851-30860 (2010).
30. Beharry, C., Alaniz, M. E., Alonso, A. D. Expression of Alzheimer-like pathological human tau induces a behavioral motor and olfactory learning deficit in Drosophila melanogaster. J Alzheimers Dis 37, 539-550 (2013).
31. Itoh, N. et al. Large-scale, multicenter study of cerebrospinal fluid tau protein phosphorylated at serine 199 for the antemortem diagnosis of Alzheimer's disease. Ann Neurol 50, 150-156 (2001).
32. Ryoo, S. R. et al. DYRK1A-mediated hyperphosphorylation of Tau. A functional link between Down syndrome and Alzheimer disease. J Biol Chem 282, 34850-34857 (2007).
33. Ryoo, S. R. et al. Dual-specificity tyrosine(Y)-phosphorylation regulated kinase 1A-mediated phosphorylation of amyloid precursor protein: evidence for a functional link between Down syndrome and Alzheimer's disease. J Neurochem 104, 1333-1344 (2008).
34. Sengupta, A., Novak, M., Grundke-Iqbal, I., Iqbal, K. Regulation of phosphorylation of tau by cyclin-dependent kinase 5 and glycogen synthase kinase-3 at substrate level. FEBS Lett 580, 5925-5933 (2006).
35. Israel, M. A. et al. Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482, 216-220 (2012).
36. Rissman, R. et al. Caspase-cleavage of tau is an early event in Alzheimer disease tangle pathology. J Clin Invest 114, 121-130 (2004).
37. Petry, F. R. et al. Specificity of anti-tau antibodies when analyzing mice models of Alzheimer's disease: problems and solutions. PLoS One 9, e94251 (2014).
38. Sagne, C., Isambert, M. F., Henry, J. P., Gasnier, B. SDS-resistant aggregation of membrane proteins: application to the purification of the vesicular monoamine transporter. Biochem J 316(Pt 3), 825-831 (1996).
39. Lasagna-Reeves, C. A. et al. Identification of oligomers at early stages of tau aggregation in Alzheimer's disease. FASEB J 26, 1946-1959 (2012).
40. Alonso, A. D., Grundke-Iqbal, I., Iqbal, K. Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat Med 2, 783-787 (1996).
41. Flores-Rodriguez, P. et al. The relationship between truncation and phosphorylation at the C-terminus of tau protein in the paired helical filaments of Alzheimer's disease. Front Neurosci 9, 33 (2015).
42. Vincent, A. J., Gasperini, R., Foa, L., Small, D. H. Astrocytes in Alzheimer's disease: emerging roles in calcium dysregulation and synaptic plasticity. J Alzheimers Dis 22, 699-714 (2010).
43. Brady, R. M., Zinkowski, R. P., Binder, L. I. Presence of tau in isolated nuclei from human brain. Neurobiol Aging 16, 479-486 (1995).
44. Sultan, A. et al. Nuclear tau, a key player in neuronal DNA protection. J Biol Chem 286, 4566-4575 (2011).
45. Fernandez-Nogales, M. et al. Huntington's disease is a four-repeat tauopathy with tau nuclear rods. Nat Med 20, 881-885 (2014).
46. Frost, B., Hemberg, M., Lewis, J., Feany, M. B. Tau promotes neurodegeneration through global chromatin relaxation. Nat Neurosci 17, 357-366 (2014).
47. Lasagna-Reeves, C. A. et al. The formation of tau pore-like structures is prevalent and cell specific: possible implications for the disease phenotypes. Acta Neuropathol Commun 2, 56 (2014).
48. Rajan, K. B., Wilson, R. S., Weuve, J., Barnes, L. L., Evans, D. A. Cognitive impairment 18 years before clinical diagnosis of Alzheimer disease dementia. Neurology 85(10), 898-904 (2015).
49. Beharry, C., Cohen, L. S., Di, J., Ibrahim, K., Briffa-Mirabella, S., Alonso, A. D. Tau-induced neurodegeneration: mechanisms and targets. Neurosci Bull 30, 346-358 (2014).
50. Small, G. W. et al. PET scanning of brain tau in retired national football league players: preliminary findings. Am J Geriatr Psychiatry 21, 138-144 (2013).
51. Guillozet-Bongaarts, A. L. et al. Tau truncation during neurofibrillary tangle evolution in Alzheimer's disease. Neurobiol Aging 26, 1015-1022 (2005).
52. De Calignon, A. et al. Caspase activation precedes and leads to tangles. Nature 464, 1201-1204 (2010).
53. Garcia-Sierra, F. et al. Ubiquitin is associated with early truncation of tau protein at aspartic acid(421) during the maturation of neurofibrillary tangles in Alzheimer's disease. Brain Pathol 22, 240-250 (2012).
54. Delobel, P. et al. Analysis of tau phosphorylation and truncation in a mouse model of human tauopathy. Am J Pathol 172, 123-131 (2008).
55. Mondragon-Rodriguez, S. et al. Cleavage and conformational changes of tau protein follow phosphorylation during Alzheimer's disease. Int J Exp Path 89, 81-90 (2008).
56. Serrano-Pozo, A. et al. Reactive glia not only associates with plaques but also parallels tangles in Alzheimer's disease. Am J Pathol 179, 1373-1384 (2011).
57. Plouffe, V. et al. Hyperphosphorylation and cleavage at D421 enhance tau secretion. PLoS One 7, e36873 (2012).
58. Chun, W., Johnson, G. V. Activation of glycogen synthase kinase 3beta promotes the intermolecular association of tau. The use of fluorescence resonance energy transfer microscopy. J Biol Chem 282, 23410-23417 (2007).
59. Sarsoza, F. et al. A fibril-specific, conformation-dependent antibody recognizes a subset of Abeta plaques in Alzheimer disease, Down syndrome and Tg2576 transgenic mouse brain. Acta Neuropathol 118, 505-517 (2009).
60. Luna-Munoz, J., Peralta-Ramirez, J., Chavez-Macias, L., Harrington, C. R., Wischik, C. M., Mena, R. Thiazin red as a neuropathological tool for the rapid diagnosis of Alzheimer's disease in tissue imprints. Acta Neuropathol 116, 507-515 (2008).
61. Antunes, M., Biala, G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 13, 93-110 (2012).
62. Dobkin, C. et al. Fmr1 knockout mouse has a distinctive strain-specific learning impairment. Neuroscience 100, 423-429 (2000).
63. El Idrissi, A. Taurine improves learning and retention in aged mice. Neurosci Lett 436, 19-22 (2008).