Motor Deficit in a Tauopathy Model Is Induced by Disturbances of Axonal Transport Leading to Dying-Back Degeneration and Denervation of Neuromuscular Junctions

American Journal of Pathology

Volumn 185, Issue 10, 2015, Pages 2685-2697

  Audouard, Emilie ^a   Van Hees, Laura ^a   Suain, Valérie ^a   Yilmaz, Zehra ^a   Poncelet, Luc ^a   Leroy, Karelle ^a   Brion, Jean Pierre ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN; TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEGENERATION; DENERVATION; GENE EXPRESSION; INNERVATION; MOTONEURON; MOTOR DYSFUNCTION; MOUSE; MUSCLE DENERVATION; MUTANT; NERVE ENDING; NERVE FIBER; NERVE FIBER TRANSPORT; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SCIATIC NERVE; SYNAPSE VESICLE; TAUOPATHY; ANIMAL; AXON; BRAIN; DISEASE MODEL; GENETICS; METABOLISM; NERVE DEGENERATION; NEUROMUSCULAR JUNCTION; PATHOLOGY; PHYSIOLOGY; PROCEDURES; SPINAL CORD; TRANSGENIC MOUSE;

ANIMALS; AXONAL TRANSPORT; AXONS; BRAIN; DENERVATION; DISEASE MODELS, ANIMAL; MICE; MICE, TRANSGENIC; NERVE DEGENERATION; NEUROMUSCULAR JUNCTION; SPINAL CORD; SYNAPTIC VESICLES; TAUOPATHIES;

EID: 84943637989     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.06.011     Document Type: Article

References (47)

1. V.M. Lee, M. Goedert, and J.Q. Trojanowski Neurodegenerative tauopathies Annu Rev Neurosci 24 2001 1121 1159
2. D. Neary, J.S. Snowden, D.M. Mann, B. Northen, P.J. Goulding, and N. Macdermott Frontal lobe dementia and motor neuron disease J Neurol Neurosurg Psychiatry 53 1990 23 32
3. A. Hirano, N. Malamud, T.S. Elizan, and L.T. Kurland Amyotrophic lateral sclerosis and Parkinsonism-dementia complex on Guam. Further pathologic studies Arch Neurol 15 1966 35 51
4. M. Goedert, and M.G. Spillantini Pathogenesis of the tauopathies J Mol Neurosci 45 2011 425 431
5. G.M. McKhann, M.S. Albert, M. Grossman, B. Miller, D. Dickson, J.Q. Trojanowski Work Group on Frontotemporal Dementia and Pick's Disease Clinical and pathological diagnosis of frontotemporal dementia: report of the Work Group on Frontotemporal Dementia and Pick's Disease Arch Neurol 58 2001 1803 1809
6. L. Buee, T. Bussiere, V. Buee-Scherrer, A. Delacourte, and P.R. Hof Tau protein isoforms, phosphorylation and role in neurodegenerative disorders Brain Res Brain Res Rev 33 2000 95 130
7. J.Z. Wang, and F. Liu Microtubule-associated protein tau in development, degeneration and protection of neurons Prog Neurobiol 85 2008 148 175
8. J. Gotz, J.R. Streffer, D. David, A. Schild, F. Hoerndli, L. Pennanen, P. Kurosinski, and F. Chen Transgenic animal models of Alzheimer's disease and related disorders: histopathology, behavior and therapy Mol Psychiatry 9 2004 664 683
9. B. Allen, E. Ingram, M. Takao, M.J. Smith, R. Jakes, K. Virdee, H. Yoshida, M. Holzer, M. Craxton, P.C. Emson, C. Atzori, A. Migheli, R.A. Crowther, B. Ghetti, M.G. Spillantini, and M. Goedert Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein J Neurosci 22 2002 9340 9351
10. K. Leroy, A. Bretteville, K. Schindowski, E. Gilissen, M. Authelet, R. De Decker, Z. Yilmaz, L. Buee, and J.P. Brion Early axonopathy preceding neurofibrillary tangles in mutant tau transgenic mice Am J Pathol 171 2007 976 992
11. K. Schindowski, A. Bretteville, K. Leroy, S. Begard, J.P. Brion, M. Hamdane, and L. Buee 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 2006 599 616
12. K. Ando, K. Leroy, C. Heraud, Z. Yilmaz, M. Authelet, V. Suain, R. De Decker, and J.P. Brion Accelerated human mutant tau aggregation by knocking out murine tau in a transgenic mouse model Am J Pathol 178 2011 803 816
13. N. Besalduch, M. Tomas, M.M. Santafe, N. Garcia, J. Tomas, and M.A. Lanuza Synaptic activity-related classical protein kinase C isoform localization in the adult rat neuromuscular synapse J Comp Neurol 518 2010 211 228
14. M.A. Lanuza, M.X. Li, M. Jia, S. Kim, R. Davenport, V. Dunlap, and P.G. Nelson Protein kinase C-mediated changes in synaptic efficacy at the neuromuscular junction in vitro: the role of postsynaptic acetylcholine receptors J Neurosci Res 61 2000 616 625
15. E. Audouard, O. Schakman, F. Rene, R.E. Huettl, A.B. Huber, J.P. Loeffler, P. Gailly, and F. Clotman The Onecut transcription factor HNF-6 regulates in motor neurons the formation of the neuromuscular junctions PLoS One 7 2012 e50509
16. X. Paez-Colasante, B. Seaberg, T.L. Martinez, L. Kong, C.J. Sumner, and M. Rimer Improvement of neuromuscular synaptic phenotypes without enhanced survival and motor function in severe spinal muscular atrophy mice selectively rescued in motor neurons PLoS One 8 2013 e75866
17. K. Leroy, K. Ando, V. Laporte, R. Dedecker, V. Suain, M. Authelet, C. Heraud, N. Pierrot, Z. Yilmaz, J.N. Octave, and J.P. Brion Lack of tau proteins rescues neuronal cell death and decreases amyloidogenic processing of APP in APP/PS1 mice Am J Pathol 181 2012 1928 1940
18. N. Kuninaka, M. Kawaguchi, M. Ogawa, A. Sato, K. Arima, S. Murayama, and Y. Saito Simplification of the modified Gallyas method Neuropathology 35 2015 10 15
19. B. Boland, A. Kumar, S. Lee, F.M. Platt, J. Wegiel, W.H. Yu, and R.A. Nixon Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease J Neurosci 28 2008 6926 6937
20. Y. Iguchi, M. Katsuno, J. Niwa, S. Takagi, S. Ishigaki, K. Ikenaka, K. Kawai, H. Watanabe, K. Yamanaka, R. Takahashi, H. Misawa, S. Sasaki, F. Tanaka, and G. Sobue Loss of TDP-43 causes age-dependent progressive motor neuron degeneration Brain 136 2013 1371 1382
21. M. Vidal, R. Morris, F. Grosveld, and E. Spanopoulou Tissue-specific control elements of the Thy-1 gene EMBO J 9 1990 833 840
22. H. Warita, Y. Itoyama, and K. Abe Selective impairment of fast anterograde axonal transport in the peripheral nerves of asymptomatic transgenic mice with a G93A mutant SOD1 gene Brain Res 819 1999 120 131
23. D.C. Rubinsztein The roles of intracellular protein-degradation pathways in neurodegeneration Nature 443 2006 780 786
24. Z. Yue, Q.J. Wang, and M. Komatsu Neuronal autophagy: going the distance to the axon Autophagy 4 2008 94 96
25. K. Katsumata, J. Nishiyama, T. Inoue, N. Mizushima, J. Takeda, and M. Yuzaki Dynein- and activity-dependent retrograde transport of autophagosomes in neuronal axons Autophagy 6 2010 378 385
26. R.A. Nixon The role of autophagy in neurodegenerative disease Nat Med 19 2013 983 997
27. K. Belarbi, K. Schindowski, S. Burnouf, R. Caillierez, M.E. Grosjean, D. Demeyer, M. Hamdane, N. Sergeant, D. Blum, and L. Buee Early tau pathology involving the septo-hippocampal pathway in a tau transgenic model: relevance to Alzheimer's disease Curr Alzheimer Res 6 2009 152 157
28. F. Chee, A. Mudher, T.A. Newman, M. Cuttle, S. Lovestone, and D. Shepherd Overexpression of tau results in defective synaptic transmission in Drosophila neuromuscular junctions Biochem Soc Trans 34 2006 88 90
29. M. Coleman Axon degeneration mechanisms: commonality amid diversity Nat Rev Neurosci 6 2005 889 898
30. S. Roy, B. Zhang, V.M. Lee, and J.Q. Trojanowski Axonal transport defects: a common theme in neurodegenerative diseases Acta Neuropathol 109 2005 5 13
31. K.J. De Vos, A.J. Grierson, S. Ackerley, and C.C. Miller Role of axonal transport in neurodegenerative diseases Annu Rev Neurosci 31 2008 151 173
32. G.A. Morfini, M. Burns, L.I. Binder, N.M. Kanaan, N. LaPointe, D.A. Bosco, R.H. Brown Jr., H. Brown, A. Tiwari, L. Hayward, J. Edgar, K.A. Nave, J. Garberrn, Y. Atagi, Y. Song, G. Pigino, and S.T. Brady Axonal transport defects in neurodegenerative diseases J Neurosci 29 2009 12776 12786
33. X.A. Liu, V. Rizzo, and S.V. Puthanveettil Pathologies of axonal transport in neurodegenerative diseases Transl Neurosci 3 2012 355 372
34. G.T. Banks, and E.M. Fisher Cytoplasmic dynein could be key to understanding neurodegeneration Genome Biol 9 2008 214
35. M. Hafezparast, R. Klocke, C. Ruhrberg, A. Marquardt, A. Ahmad-Annuar, S. Bowen, and et al. Mutations in dynein link motor neuron degeneration to defects in retrograde transport Science 300 2003 808 812
36. G.B. Stokin, C. Lillo, T.L. Falzone, R.G. Brusch, E. Rockenstein, S.L. Mount, R. Raman, P. Davies, E. Masliah, D.S. Williams, and L.S.B. Goldstein Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease Science 307 2005 1282 1288
37. J. Gotz, L.M. Ittner, and S. Kins Do axonal defects in tau and amyloid precursor protein transgenic animals model axonopathy in Alzheimer's disease? J Neurochem 98 2006 993 1006
38. E. Vicario-Orri, C.M. Opazo, and F.J. Munoz The pathophysiology of axonal transport in Alzheimer's disease J Alzheimers Dis 43 2015 1097 1113
39. K. Stamer, R. Vogel, E. Thies, E. Mandelkow, and E.M. Mandelkow Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress J Cell Biol 156 2002 1051 1063
40. K.A. Vossel, K. Zhang, J. Brodbeck, A.C. Daub, P. Sharma, S. Finkbeiner, B. Cui, and L. Mucke Tau reduction prevents Abeta-induced defects in axonal transport Science 330 2010 198
41. N.M. Kanaan, G.A. Morfini, N.E. LaPointe, G.F. Pigino, K.R. Patterson, Y. Song, A. Andreadis, Y. Fu, S.T. Brady, and L.I. Binder Pathogenic forms of tau inhibit kinesin-dependent axonal transport through a mechanism involving activation of axonal phosphotransferases J Neurosci 31 2011 9858 9868
42. M. Morel, C. Heraud, C. Nicaise, V. Suain, and J.P. Brion Levels of kinesin light chain and dynein intermediate chain are reduced in the frontal cortex in Alzheimer's disease: implications for axoplasmic transport Acta Neuropathol 123 2012 71 84
43. D. Yu, N.E. LaPointe, E. Guzman, V. Pessino, L. Wilson, S.C. Feinstein, and M.T. Valentine Tau proteins harboring neurodegeneration-linked mutations impair kinesin translocation in vitro J Alzheimers Dis 39 2014 301 314
44. L.M. Ittner, Y.D. Ke, F. Delerue, M. Bi, A. Gladbach, J. van Eersel, H. Wolfing, B.C. Chieng, M.J. Christie, I.A. Napier, A. Eckert, M. Staufenbiel, E. Hardeman, and J. Gotz Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models Cell 142 2010 387 397
45. S. Burnouf, A. Martire, M. Derisbourg, C. Laurent, K. Belarbi, A. Leboucher, F.J. Fernandez-Gomez, L. Troquier, S. Eddarkaoui, M.E. Grosjean, D. Demeyer, A. Muhr-Tailleux, A. Buisson, N. Sergeant, M. Hamdane, S. Humez, P. Popoli, L. Buée, and D. Blum NMDA receptor dysfunction contributes to impaired brain-derived neurotrophic factor-induced facilitation of hippocampal synaptic transmission in a Tau transgenic model Aging Cell 12 2013 11 23
46. N.M. Kanaan, G.F. Pigino, S.T. Brady, O. Lazarov, L.I. Binder, and G.A. Morfini Axonal degeneration in Alzheimer's disease: when signaling abnormalities meet the axonal transport system Exp Neurol 246 2013 44 53
47. J.M. Decker, L. Kruger, A. Sydow, S. Zhao, M. Frotscher, E. Mandelkow, and E.M. Mandelkow Pro-aggregant Tau impairs mossy fiber plasticity due to structural changes and Ca++ dysregulation Acta Neuropathol Commun 3 2015 23