Tau association with synaptic vesicles causes presynaptic dysfunction

Nature Communications

Volumn 8, Issue , 2017, Pages

  Zhou, Lujia ^a,b   McInnes, Joseph ^a,b   Wierda, Keimpe ^a,b   Holt, Matthew ^a,b   Herrmann, Abigail G ^c   Jackson, Rosemary J ^c   Wang, Yu Chun ^a,b   Swerts, Jef ^a,b   Beyens, Jelle ^a,b   Miskiewicz, Katarzyna ^a,b   Vilain, Sven ^a,b   Dewachter, Ilse ^d,e   Moechars, Diederik ^f   Strooper, Bart De ^a,b   Spires Jones, Tara L ^c   Wit, Joris De ^a,b   Verstreken, Patrik ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^e HASSELT UNIVERSITY   (Belgium)

^f JANSSEN RESEARCH FOUNDATION   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

TAU PROTEIN; ACTIN;

CHEMICAL BINDING; FLY; MEMBRANE; MOBILITY; NERVOUS SYSTEM DISORDER; NEUROLOGY; PATHOLOGY; RODENT; TOXICITY;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DIPTERA; NERVE ENDING; NEUROTOXICITY; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC DYSFUNCTION; PROTEIN BINDING; PROTEIN LOCALIZATION; RAT; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TAUOPATHY; ANIMAL; CHEMISTRY; DROSOPHILA MELANOGASTER; GENETICS; HIPPOCAMPUS; HUMAN; METABOLISM; MUTATION; NERVE CELL; PROTEIN DOMAIN; PROTEIN TRANSPORT; ULTRASTRUCTURE;

RATTUS;

ACTINS; ANIMALS; DROSOPHILA MELANOGASTER; HIPPOCAMPUS; HUMANS; MUTATION; NEURONS; PRESYNAPTIC TERMINALS; PROTEIN DOMAINS; PROTEIN TRANSPORT; RATS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TAU PROTEINS;

EID: 85032677914     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms15295     Document Type: Article

References (70)

1. Morris, M., Maeda, S., Vossel, K. & Mucke, L. The many faces of tau. Neuron70, 410-426 (2011).
2. Ballatore, C., Lee, V. M. & Trojanowski, J. Q. Tau-mediated neurodegenerationin Alzheimer's disease and related disorders. Nat. Rev. Neurosci. 8, 663-672(2007).
3. Wang, Y. & Mandelkow, E. Tau in physiology and pathology. Nat. Rev.Neurosci. 17, 22-35 (2016).
4. Kwok, J. B., et al. Tau haplotypes regulate transcription and are associated withParkinson's disease. Ann. Neurol. 55, 329-334 (2004).
5. Refenes, N., et al. Role of the H1 haplotype of microtubule-associated proteintau (MAPT) gene in Greek patients with Parkinson's disease. BMC Neurol. 9,26 (2009).
6. Allen, M., et al. Association of MAPT haplotypes with Alzheimer's diseaserisk and MAPT brain gene expression levels. Alzheimers Res. Ther. 6, 39(2014).
7. Liu, T., et al. Amyloid-beta-induced toxicity of primary neurons is dependentupon differentiation-associated increases in tau and cyclin-dependent kinase 5expression. J. Neurochem. 88, 554-563 (2004).
8. Rapoport, M., Dawson, H. N., Binder, L. I., Vitek, M. P. & Ferreira, A. Tau isessential to beta-amyloid-induced neurotoxicity. Proc. Natl Acad. Sci. USA 99,6364-6369 (2002).
9. Nussbaum, J. M., et al. Prion-like behaviour and tau-dependent cytotoxicity ofpyroglutamylated amyloid-b. Nature 485, 651-655 (2012).
10. Roberson, E. D., et al. Reducing endogenous tau ameliorates amyloid betainduceddeficits in an Alzheimer's disease mouse model. Science 316, 750-754(2007).
11. Holth, J. K., et al. Tau loss attenuates neuronal network hyperexcitability inmouse and Drosophila genetic models of epilepsy. J. Neurosci. 33, 1651-1659(2013).
12. DeVos, S. L., et al. Antisense reduction of tau in adult mice protects againstseizures. J. Neurosci. 33, 12887-12897 (2013).
13. Masliah, E., et al. Altered expression of synaptic proteins occurs early duringprogression of Alzheimer's disease. Neurology 56, 127-129 (2001).
14. Bellucci, A., Navarria, L., Zaltieri, M., Missale, C. & Spano, P. a-Synucleinsynaptic pathology and its implications in the development of novel therapeuticapproaches to cure Parkinson's disease. Brain Res. 1432, 95-113 (2012).
15. Milnerwood, A. J. & Raymond, L. A. Early synaptic pathophysiology inneurodegeneration: Insights from Huntington's disease. Trends Neurosci. 33,513-523 (2010).
16. Scheff, S. W., Price, D. A., Schmitt, F. A. & Mufson, E. J. Hippocampal synapticloss in early Alzheimer's disease and mild cognitive impairment. Neurobiol.Aging 27, 1372-1384 (2006).
17. Yoshiyama, Y., et al. Synapse loss and microglial activation precede tangles in aP301S tauopathy mouse model. Neuron 53, 337-351 (2007).
18. Crimins, J. L., Rocher, A. B. & Luebke, J. I. Electrophysiological changesprecede morphological changes to frontal cortical pyramidal neurons in therTg4510 mouse model of progressive tauopathy. Acta Neuropathol. 124,777-795 (2012).
19. Polydoro, M., et al. Soluble pathological tau in the entorhinal cortex leads topresynaptic deficits in an early Alzheimer's disease model. Acta Neuropathol.127, 257-270 (2014).
20. Sydow, A., et al. Tau-induced defects in synaptic plasticity, learning, andmemory are reversible in transgenic mice after switching off the toxic Taumutant. J. Neurosci. 31, 2511-2525 (2011).
21. Hoover, B. R., et al. Tau mislocalization to dendritic spines mediates synapticdysfunction independently of neurodegeneration. Neuron 68, 1067-1081(2010).
22. Erez, H., Shemesh, O. A. & Spira, M. E. Rescue of tau-induced synaptictransmission pathology by paclitaxel. Front. Cell Neurosci. 8, 34 (2014).
23. Menkes-Caspi, N., et al. Pathological tau disrupts ongoing network activity.Neuron 85, 959-966 (2015).
24. Santacruz, K., et al. Tau suppression in a neurodegenerative mouse modelimproves memory function. Science 309, 476-481 (2005).
25. Hong, M., et al. Mutation-specific functional impairments in distinct tauisoforms of hereditary FTDP-17. Science 282, 1914-1917 (1998).
26. Fein, J. A., et al. Co-localization of amyloid beta and tau pathology inAlzheimer's disease synaptosomes. Am. J. Pathol. 172, 1683-1692 (2008).
27. Sokolow, S., et al. Pre-synaptic C-terminal truncated tau is released fromcortical synapses in Alzheimer's disease. J. Neurochem. 133, 368-379 (2015).
28. Henkins, K. M., et al. Extensive p-tau pathology and SDS-stable p-tau oligomersin Alzheimer's cortical synapses. Brain Pathol. 22, 826-833 (2012).
29. Tai, H. C., et al. The synaptic accumulation of hyperphosphorylated tauoligomers in Alzheimer disease is associated with dysfunction of the ubiquitinproteasomesystem. Am. J. Pathol. 181, 1426-1435 (2012).
30. Sahara, N., Murayama, M., Higuchi, M., Suhara, T. & Takashima, A.Biochemical distribution of Tau protein in synaptosomal fraction of transgenicmice expressing human P301L Tau. Front. Neurol. 5, 26 (2014).
31. Harris, J. A., et al. Human P301L-mutant tau expression in mouse entorhinalhippocampalnetwork causes tau aggregation and presynaptic pathology but nocognitive deficits. PLoS ONE 7, e45881 (2012).
32. Ittner, L. M., et al. Dendritic function of tau mediates amyloid-beta toxicity inAlzheimer's disease mouse models. Cell 142, 387-397 (2010).
33. Lloyd, T. E., et al. A genome-wide search for synaptic vesicle cycle proteins inDrosophila. Neuron 26, 45-50 (2000).
34. Hadley, D., et al. Patterns of sequence conservation in presynaptic neural genes.Genome Biol. 7, R105 (2006).
35. Dias-Santagata, D., Fulga, T. A., Duttaroy, A. & Feany, M. B. Oxidative stressmediates tau-induced neurodegeneration in Drosophila. J. Clin. Invest. 117,236-245 (2007).
36. Frost, B., Hemberg, M., Lewis, J. & Feany, M. B. Tau promotesneurodegeneration through global chromatin relaxation. Nat. Neurosci. 17,357-366 (2014).
37. Khurana, V., et al. TOR-mediated cell-cycle activation causesneurodegeneration in a Drosophila tauopathy model. Curr. Biol. 16, 230-241(2006).
38. Wittmann, C. W., et al. Tauopathy in Drosophila: Neurodegeneration withoutneurofibrillary tangles. Science 293, 711-714 (2001).
39. Kawasaki, F., Hazen, M. & Ordway, R. W. Fast synaptic fatigue in shibiremutants reveals a rapid requirement for dynamin in synaptic vesicle membranetrafficking. Nat. Neurosci. 3, 859-860 (2000).
40. Verstreken, P., et al. Endophilin mutations block clathrin-mediated endocytosisbut not neurotransmitter release. Cell 109, 101-112 (2002).
41. Saheki, Y. & De Camilli, P. Synaptic vesicle endocytosis. Cold Spring Harb.Perspect. Biol. 4, a005645 (2012).
42. Sara, Y., Mozhayeva, M. G., Liu, X. & Kavalali, E. T. Fast vesicle recyclingsupports neurotransmission during sustained stimulation at hippocampalsynapses. J. Neurosci. 22, 1608-1617 (2002).
43. Verstreken, P., et al. Synaptic mitochondria are critical for mobilization ofreserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47,365-378 (2005).
44. Alabi, A. A. & Tsien, R. W. Synaptic vesicle pools and dynamics. Cold SpringHarb. Perspect. Biol. 4, a013680 (2012).
45. Fernández-Alfonso, T. & Ryan, T. A. The kinetics of synaptic vesicle pooldepletion at CNS synaptic terminals. Neuron 41, 943-953 (2004).
46. Gaffield, M. A., Rizzoli, S. O. & Betz, W. J. Mobility of synaptic vesicles indifferent pools in resting and stimulated frog motor nerve terminals. Neuron51, 317-325 (2006).
47. Miesenböck, G., De Angelis, D. A. & Rothman, J. E. Visualizing secretion andsynaptic transmission with pH-sensitive green fluorescent proteins. Nature 394,192-195 (1998).
48. Fulga, T. A., et al. Abnormal bundling and accumulation of F-actin mediatestau-induced neuronal degeneration in vivo. Nat. Cell Biol. 9, 139-148 (2007).
49. He, H. J., et al. The proline-rich domain of tau plays a role in interactions withactin. BMC Cell Biol. 10, 81 (2009).
50. Shupliakov, O., Haucke, V. & Pechstein, A. How synapsin I may clustersynaptic vesicles. Semin. Cell Dev. Biol. 22, 393-399 (2011).
51. Steinhilb, M. L., Dias-Santagata, D., Fulga, T. A., Felch, D. L. & Feany, M. B.Tau phosphorylation sites work in concert to promote neurotoxicity in vivo.Mol. Biol. Cell 18, 5060-5068 (2007).
52. Bekkers, J. M. & Stevens, C. F. Excitatory and inhibitory autaptic currents inisolated hippocampal neurons maintained in cell culture. Proc. Natl Acad. Sci.USA 88, 7834-7838 (1991).
53. Chouhan, A. K., et al. Uncoupling neuronal death and dysfunction inDrosophila models of neurodegenerative disease. Acta Neuropathol. Commun.4, 62 (2016).
54. Diao, J., et al. Native a-synuclein induces clustering of synaptic-vesicle mimics viabinding to phospholipids and synaptobrevin-2/VAMP2. Elife 2, e00592 (2013).
55. Wang, L., et al. a-synuclein multimers cluster synaptic vesicles and attenuaterecycling. Curr. Biol. 24, 2319-2326 (2014).
56. Fioravante, D., Liu, R. Y., Netek, A. K., Cleary, L. J. & Byrne, J. H. Synapsinregulates Basal synaptic strength, synaptic depression, and serotonin-inducedfacilitation of sensorimotor synapses in Aplysia. J. Neurophysiol. 98, 3568-3580(2007).
57. Vasileva, M., Renden, R., Horstmann, H., Gitler, D. & Kuner, T.Overexpression of synapsin Ia in the rat calyx of Held accelerates short-termplasticity and decreases synaptic vesicle volume and active zone area. Front. CellNeurosci. 7, 270 (2013).
58. Zhao, X., et al. Caspase-2 cleavage of tau reversibly impairs memory. Nat. Med.22, 1268-1276 (2016).
59. Penzes, P., et al. Rapid induction of dendritic spine morphogenesis by transsynapticephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37,263-274 (2003).
60. Rao, A., Cha, E. M. & Craig, A. M. Mismatched appositions of presynaptic andpostsynaptic components in isolated hippocampal neurons. J. Neurosci. 20,8344-8353 (2000).
61. Crimins, J. L., et al. Homeostatic responses by surviving cortical pyramidal cellsin neurodegenerative tauopathy. Acta Neuropathol. 122, 551-564 (2011).
62. Decker, J. M., et al. Pro-aggregant Tau impairs mossy fiber plasticity due tostructural changes and Ca(\+\+) dysregulation. Acta Neuropathol. Commun. 3,23 (2015).
63. Rocher, A. B., et al. Structural and functional changes in tau mutant miceneurons are not linked to the presence of NFTs. Exp. Neurol. 223, 385-393(2010).
64. Crone, N. E., Korzeniewska, A. & Franaszczuk, P. J. Cortical g responses:searching high and low. Int. J. Psychophysiol. 79, 9-15 (2011).
65. Herrmann, C. S., Munk, M. H. & Engel, A. K. Cognitive functions of gammabandactivity: Memory match and utilization. Trends Cogn. Sci. 8, 347-355(2004).
66. Lachaux, J. P., Axmacher, N., Mormann, F., Halgren, E. & Crone, N. E. Highfrequencyneural activity and human cognition: Past, present and possiblefuture of intracranial EEG research. Prog Neurobiol. 98, 279-301 (2012).
67. Ferreira, A. & Bigio, E. H. Calpain-mediated tau cleavage: A mechanism leadingto neurodegeneration shared by multiple tauopathies. Mol. Med. 17, 676-685(2011).
68. Vilain, S., et al. Fast and efficient Drosophila melanogaster gene knock-ins usingMiMIC transposons. G3 4, 2381-2387 (2014).
69. Uytterhoeven, V., Kuenen, S., Kasprowicz, J., Miskiewicz, K. & Verstreken, P.Loss of skywalker reveals synaptic endosomes as sorting stations for synapticvesicle proteins. Cell 145, 117-132 (2011).
70. Holt, M., Riedel, D., Stein, A., Schuette, C. & Jahn, R. Synaptic vesicles areconstitutively active fusion machines that function independently of Ca2\+.Curr. Biol. 18, 715-722 (2008).