Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2016 (2016), Article ID 4145708, 15 pages
http://dx.doi.org/10.1155/2016/4145708
Research Article

Amyloid-Beta Induced Changes in Vesicular Transport of BDNF in Hippocampal Neurons

1Institute of Physiology, Medical Faculty, Otto-von-Guericke-University, 39120 Magdeburg, Germany
2Institute of Clinical Chemistry and Pathobiochemistry, Medical Faculty, Otto-von-Guericke-University, 39120 Magdeburg, Germany
3German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany
4Institute of Physiological Chemistry, University Medical Center of the Johannes Gutenberg University, 55128 Mainz, Germany
5Center of Behavioral Brain Sciences (CBBS), 39106 Magdeburg, Germany

Received 18 September 2015; Revised 26 November 2015; Accepted 29 November 2015

Academic Editor: Pablo Munoz

Copyright © 2016 Bianca Seifert et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Edelmann, E. Cepeda-Prado, M. Franck, P. Lichtenecker, T. Brigadski, and V. Leßmann, “Theta burst firing recruits BDNF release and signaling in postsynaptic CA1 neurons in spike-timing-dependent LTP,” Neuron, vol. 86, no. 4, pp. 1041–1054, 2015. View at Publisher · View at Google Scholar
  2. E. J. Huang and L. F. Reichardt, “Neurotrophins: roles in neuronal development and function,” Annual Review of Neuroscience, vol. 24, pp. 677–736, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Klein, “Role of neurotrophins in mouse neuronal development,” The FASEB Journal, vol. 8, no. 10, pp. 738–744, 1994. View at Google Scholar · View at Scopus
  4. V. Lessmann and R. Heumann, “Modulation of unitary glutamatergic synapses by neurotrophin-4/5 or brain-derived neurotrophic factor in hippocampal microcultures: presynaptic enhancement depends on pre-established paired-pulse facilitation,” Neuroscience, vol. 86, no. 2, pp. 399–413, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Park and M.-M. Poo, “Neurotrophin regulation of neural circuit development and function,” Nature Reviews Neuroscience, vol. 14, no. 1, pp. 7–23, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Connor and M. Dragunow, “The role of neuronal growth factors in neurodegenerative disorders of the human brain,” Brain Research Reviews, vol. 27, no. 1, pp. 1–39, 1998. View at Publisher · View at Google Scholar · View at Scopus
  7. L. Tapia-Arancibia, E. Aliaga, M. Silhol, and S. Arancibia, “New insights into brain BDNF function in normal aging and Alzheimer disease,” Brain Research Reviews, vol. 59, no. 1, pp. 201–220, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Zuccato and E. Cattaneo, “Brain-derived neurotrophic factor in neurodegenerative diseases,” Nature Reviews Neurology, vol. 5, no. 6, pp. 311–322, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. K. Schindowski, K. Belarbi, and L. Buée, “Neurotrophic factors in Alzheimer's disease: role of axonal transport,” Genes, Brain and Behavior, vol. 7, supplement 1, pp. 43–56, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Adachi, T. Numakawa, M. Richards, S. Nakajima, and H. Kunugi, “New insight in expression, transport, and secretion of brain-derived neurotrophic factor: Implications in brain-related diseases,” World Journal of Biological Chemistry, vol. 5, no. 4, pp. 409–428, 2014. View at Publisher · View at Google Scholar
  11. P. Harjes and E. E. Wanker, “The hunt for huntingtin function: interaction partners tell many different stories,” Trends in Biochemical Sciences, vol. 28, no. 8, pp. 425–433, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Kruttgen, S. Saxena, M. E. Evangelopoulos, and J. Weis, “Neurotrophins and neurodegenerative diseases: receptors stuck in traffic?” Journal of Neuropathology and Experimental Neurology, vol. 62, no. 4, pp. 340–350, 2003. View at Google Scholar · View at Scopus
  13. C. A. Altar and P. S. Distefano, “Neurotrophin trafficking by anterograde transport,” Trends in Neurosciences, vol. 21, no. 10, pp. 433–437, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. L. R. Gauthier, B. C. Charrin, M. Borrell-Pagès et al., “Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules,” Cell, vol. 118, no. 1, pp. 127–138, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Vermehren-Schmaedick, W. Krueger, T. Jacob et al., “Heterogeneous intracellular trafficking dynamics of brain-derived neurotrophic factor complexes in the neuronal soma revealed by single quantum dot tracking,” PLoS ONE, vol. 9, no. 4, Article ID e95113, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Caleo, E. Menna, S. Chierzi, M. C. Cenni, and L. Maffei, “Brain-derived neurotrophic factor is an anterograde survival factor in the rat visual system,” Current Biology, vol. 10, no. 19, pp. 1155–1161, 2000. View at Publisher · View at Google Scholar · View at Scopus
  17. K. L. Spalding, M. M. L. Tan, I. A. Hendry, and A. R. Harvey, “Anterograde transport and trophic actions of BDNF and NT-4/5 in the developing rat visual system,” Molecular and Cellular Neuroscience, vol. 19, no. 4, pp. 485–500, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. H. B. Rind, R. Butowt, and C. S. von Bartheld, “Synaptic targeting of retrogradely transported trophic factors in motoneurons: comparison of glial cell line-derived neurotrophic factor, brain-derived neurotrophic factor, and cardiotrophin-1 with tetanus toxin,” Journal of Neuroscience, vol. 25, no. 3, pp. 539–549, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. J. J. Park, N. X. Cawley, and Y. P. Loh, “A bi-directional carboxypeptidase E-driven transport mechanism controls BDNF vesicle homeostasis in hippocampal neurons,” Molecular and Cellular Neuroscience, vol. 39, no. 1, pp. 63–73, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. D. M. Kwinter, K. Lo, P. Mafi, and M. A. Silverman, “Dynactin regulates bidirectional transport of dense-core vesicles in the axon and dendrites of cultured hippocampal neurons,” Neuroscience, vol. 162, no. 4, pp. 1001–1010, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. N. Adachi, K. Kohara, and T. Tsumoto, “Difference in trafficking of brain-derived neurotrophic factor between axons and dendrites of cortical neurons, revealed by live-cell imaging,” BMC Neuroscience, vol. 6, article 42, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. W. W. Poon, A. J. Carlos, B. L. Aguilar et al., “β-Amyloid (Aβ) oligomers impair brain-derived neurotrophic factor retrograde trafficking by down-regulating ubiquitin C-terminal hydrolase, UCH-L1,” The Journal of Biological Chemistry, vol. 288, no. 23, pp. 16937–16948, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. W. W. Poon, M. Blurton-Jones, C. H. Tu et al., “β-Amyloid impairs axonal BDNF retrograde trafficking,” Neurobiology of Aging, vol. 32, no. 5, pp. 821–833, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Brigadski, M. Hartmann, and V. Lessmann, “Differential vesicular targeting and time course of synaptic secretion of the mammalian neurotrophins,” Journal of Neuroscience, vol. 25, no. 33, pp. 7601–7614, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. W. Haubensak, F. Narz, R. Heumann, and V. Leßmann, “BDNF-GFP containing secretory granules are localized in the vicinity of synaptic junctions of cultured cortical neurons,” Journal of Cell Science, vol. 111, no. 11, pp. 1483–1493, 1998. View at Google Scholar · View at Scopus
  26. C. Kaether, P. Skehel, and C. G. Dotti, “Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons,” Molecular Biology of the Cell, vol. 11, no. 4, pp. 1213–1224, 2000. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Hartmann, R. Heumann, and V. Lessmann, “Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses,” The EMBO Journal, vol. 20, no. 21, pp. 5887–5897, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. W. L. Klein, “Aβ toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets,” Neurochemistry International, vol. 41, no. 5, pp. 345–352, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Rönicke, M. Mikhaylova, S. Rönicke et al., “Early neuronal dysfunction by amyloid β oligomers depends on activation of NR2B-containing NMDA receptors,” Neurobiology of Aging, vol. 32, no. 12, pp. 2219–2228, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. R. Kolarow, T. Brigadski, and V. Lessmann, “Postsynaptic secretion of BDNF and NT-3 from hippocampal neurons depends on calcium—calmodulin kinase II signaling and proceeds via delayed fusion pore opening,” The Journal of Neuroscience, vol. 27, no. 39, pp. 10350–10364, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Lison, M. F. K. Happel, F. Schneider et al., “Disrupted cross-laminar cortical processing in β amyloid pathology precedes cell death,” Neurobiology of Disease, vol. 63, pp. 62–73, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Oakley, S. L. Cole, S. Logan et al., “Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation,” Journal of Neuroscience, vol. 26, no. 40, pp. 10129–10140, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. F. Schneider, K. Baldauf, W. Wetzel, and K. G. Reymann, “Behavioral and EEG changes in male 5xFAD mice,” Physiology and Behavior, vol. 135, pp. 25–33, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. L. Holcomb, M. N. Gordon, E. Mcgowan et al., “Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes,” Nature Medicine, vol. 4, no. 1, pp. 97–100, 1998. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Caroni, “Overexpression of growth-associated proteins in the neurons of adult transgenic mice,” Journal of Neuroscience Methods, vol. 71, no. 1, pp. 3–9, 1997. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Porrero, P. Rubio-Garrido, C. Avendaño, and F. Clascá, “Mapping of fluorescent protein-expressing neurons and axon pathways in adult and developing Thy1-eYFP-H transgenic mice,” Brain Research, vol. 1345, pp. 59–72, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. J. S. Liu, C. R. Schubert, X. Fu et al., “Molecular basis for specific regulation of neuronal kinesin-3 motors by doublecortin family proteins,” Molecular Cell, vol. 47, no. 5, pp. 707–721, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Nakata, S. Terada, and N. Hirokawa, “Visualization of the dynamics of synaptic vesicle and plasma membrane proteins in living axons,” Journal of Cell Biology, vol. 140, no. 3, pp. 659–674, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Kamal, G. B. Stokin, Z. Yang, C.-H. Xia, and L. S. B. Goldstein, “Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I,” Neuron, vol. 28, no. 2, pp. 449–459, 2000. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Kamal, A. Almenar-Queralt, J. F. LeBlanc, E. A. Roberts, and L. S. B. Goldstein, “Kinesin-mediated axonal transport of a membrane compartment containing β-secretase and presenilin-1 requires APP,” Nature, vol. 414, no. 6864, pp. 643–648, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. O. Lazarov, G. A. Morfini, E. B. Lee et al., “Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited,” Journal of Neuroscience, vol. 25, no. 9, pp. 2386–2395, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. J. L. Wittnam, E. Portelius, H. Zetterberg et al., “Pyroglutamate amyloid β(aβ) aggravates behavioral deficits in transgenic amyloid mouse model for Alzheimer disease,” The Journal of Biological Chemistry, vol. 287, no. 11, pp. 8154–8162, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Lu, “BDNF and activity-dependent synaptic modulation,” Learning and Memory, vol. 10, no. 2, pp. 86–98, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Gottmann, T. Mittmann, and V. Lessmann, “BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses,” Experimental Brain Research, vol. 199, no. 3-4, pp. 203–234, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. V. Lessmann, “Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS,” General Pharmacology, vol. 31, no. 5, pp. 667–674, 1998. View at Publisher · View at Google Scholar · View at Scopus
  46. V. Lessmann and T. Brigadski, “Mechanisms, locations, and kinetics of synaptic BDNF secretion: an update,” Neuroscience Research, vol. 65, no. 1, pp. 11–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. S. J. Mowla, H. F. Farhadi, S. Pareek et al., “Biosynthesis and post-translational processing of the precursor to brain-derived neurotrophic factor,” The Journal of Biological Chemistry, vol. 276, no. 16, pp. 12660–12666, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Yang, C.-J. Siao, G. Nagappan et al., “Neuronal release of proBDNF,” Nature Neuroscience, vol. 12, no. 2, pp. 113–115, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. G. Nagappan, E. Zaitsev, V. V. Senatorov Jr., J. Yang, B. L. Hempstead, and B. Lu, “Control of extracellular cleavage of ProBDNF by high frequency neuronal activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 4, pp. 1267–1272, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Thinakaran and E. H. Koo, “Amyloid precursor protein trafficking, processing, and function,” The Journal of Biological Chemistry, vol. 283, pp. 29615–29619, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Haass and D. J. Selkoe, “Cellular processing of β-amyloid precursor protein and the genesis of amyloid β-peptide,” Cell, vol. 75, no. 6, pp. 1039–1042, 1993. View at Publisher · View at Google Scholar · View at Scopus
  52. V. Muresan, N. H. Varvel, B. T. Lamb, and Z. Muresan, “The cleavage products of amyloid-β precursor protein are sorted to distinct carrier vesicles that are independently transported within neurites,” Journal of Neuroscience, vol. 29, no. 11, pp. 3565–3578, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. U. C. Müller and H. Zheng, “Physiological functions of APP family proteins,” Cold Spring Harbor Perspectives in Medicine, vol. 2, no. 2, Article ID a006288, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. B. De Strooper and W. Annaert, “Proteolytic processing and cell biological functions of the amyloid precursor protein,” Journal of Cell Science, vol. 113, no. 11, pp. 1857–1870, 2000. View at Google Scholar · View at Scopus
  55. C. Haass, C. Kaether, G. Thinakaran, and S. Sisodia, “Trafficking and proteolytic processing of APP,” Cold Spring Harbor Perspectives in Medicine, vol. 2, no. 5, Article ID a006270, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Brunholz, S. Sisodia, A. Lorenzo, C. Deyts, S. Kins, and G. Morfini, “Axonal transport of APP and the spatial regulation of APP cleavage and function in neuronal cells,” Experimental Brain Research, vol. 217, no. 3-4, pp. 353–364, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Ferreira, A. Caceres, and K. S. Kosik, “Intraneuronal compartments of the amyloid precursor protein,” The Journal of Neuroscience, vol. 13, no. 7, pp. 3112–3123, 1993. View at Google Scholar · View at Scopus
  58. R. Butowt and C. S. von Bartheld, “Conventional kinesin-I motors participate in the anterograde axonal transport of neurotrophins in the visual system,” Journal of Neuroscience Research, vol. 85, no. 12, pp. 2546–2556, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. E. Colin, D. Zala, G. Liot et al., “Huntingtin phosphorylation acts as a molecular switch for anterograde/retrograde transport in neurons,” The EMBO Journal, vol. 27, no. 15, pp. 2124–2134, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. J. P. Dompierre, J. D. Godin, B. C. Charrin et al., “Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation,” The Journal of Neuroscience, vol. 27, no. 13, pp. 3571–3583, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. N. Hirokawa, S. Niwa, and Y. Tanaka, “Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease,” Neuron, vol. 68, no. 4, pp. 610–638, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Kins, N. Lauther, A. Szodorai, and K. Beyreuther, “Subcellular trafficking of the amyloid precursor protein gene family and its pathogenic role in Alzheimer's disease,” Neurodegenerative Diseases, vol. 3, no. 4-5, pp. 218–226, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. M. Kondo, Y. Takei, and N. Hirokawa, “Motor protein KIF1A is essential for hippocampal synaptogenesis and learning enhancement in an enriched environment,” Neuron, vol. 73, no. 4, pp. 743–757, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. K. Y. Lo, A. Kuzmin, S. M. Unger, J. D. Petersen, and M. A. Silverman, “KIF1A is the primary anterograde motor protein required for the axonal transport of dense-core vesicles in cultured hippocampal neurons,” Neuroscience Letters, vol. 491, no. 3, pp. 168–173, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Tang, D. A. Scott, U. Das et al., “Early and selective impairments in axonal transport kinetics of synaptic cargoes induced by soluble amyloid β-protein oligomers,” Traffic, vol. 13, no. 5, pp. 681–693, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. M.-M. Fu and E. L. F. Holzbaur, “JIP1 regulates the directionality of APP axonal transport by coordinating kinesin and dynein motors,” Journal of Cell Biology, vol. 202, no. 3, pp. 495–508, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. H. Inomata, Y. Nakamura, A. Hayakawa et al., “A scaffold protein JIP-1b enhances amyloid precursor protein phosphorylation by JNK and its association with kinesin light chain 1,” Journal of Biological Chemistry, vol. 278, no. 25, pp. 22946–22955, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. Z. Muresan and V. Muresan, “Coordinated transport of phosphorylated amyloid-β precursor protein and c-Jun NH2-terminal kinase–interacting protein-1,” The Journal of Cell Biology, vol. 171, no. 4, pp. 615–625, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. C. Goldsbury, M.-M. Mocanu, E. Thies et al., “Inhibition of APP trafficking by tau protein does not increase the generation of amyloid-β peptides,” Traffic, vol. 7, no. 7, pp. 873–888, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. 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,” Journal of Cell Biology, vol. 156, no. 6, pp. 1051–1063, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. H. Decker, K. Y. Lo, S. M. Unger, S. T. Ferreira, and M. A. Silverman, “Amyloid-β peptide oligomers disrupt axonal transport through an NMDA receptor-dependent mechanism that is mediated by glycogen synthase kinase 3β in primary cultured hippocampal neurons,” Journal of Neuroscience, vol. 30, no. 27, pp. 9166–9171, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. E. M. Ramser, K. J. Gan, H. Decker et al., “Amyloid-β oligomers induce tau-independent disruption of BDNF axonal transport via calcineurin activation in cultured hippocampal neurons,” Molecular Biology of the Cell, vol. 24, no. 16, pp. 2494–2505, 2013. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Zala, M.-V. Hinckelmann, H. Yu et al., “Vesicular glycolysis provides on-board energy for fast axonal transport,” Cell, vol. 152, no. 3, pp. 479–491, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. L. Mucke and D. J. Selkoe, “Neurotoxicity of amyloid β-protein: synaptic and network dysfunction,” Cold Spring Harbor Perspectives in Medicine, vol. 2, no. 7, Article ID a006338, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. A. C. Paula-Lima, J. Brito-Moreira, and S. T. Ferreira, “Deregulation of excitatory neurotransmission underlying synapse failure in Alzheimer's disease,” Journal of Neurochemistry, vol. 126, no. 2, pp. 191–202, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. J. de Wit, R. F. Toonen, J. Verhaagen, and M. Verhage, “Vesicular trafficking of semaphorin 3A is activity-dependent and differs between axons and dendrites,” Traffic, vol. 7, no. 8, pp. 1060–1077, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. S. V. Puthanveettil, F. J. Monje, M. C. Miniaci et al., “A new component in synaptic plasticity: upregulation of kinesin in the neurons of the gill-withdrawal reflex,” Cell, vol. 135, no. 5, pp. 960–973, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. H. Hiruma, K. Shimizu, T. Takenami, H. Sugie, and T. Kawakami, “Effects of clonidine on lidocaine-induced inhibition of axonal transport in cultured mouse dorsal root ganglion neurones,” British Journal of Anaesthesia, vol. 101, no. 5, pp. 659–665, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. K. Lardong, C. Maas, and M. Kneussel, “Neuronal depolarization modifies motor protein mobility,” Neuroscience, vol. 160, no. 1, pp. 1–5, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. G. Morfini, G. Szebenyi, R. Elluru, N. Ratner, and S. T. Brady, “Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility,” The EMBO Journal, vol. 21, no. 3, pp. 281–293, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. G. Morfini, G. Szebenyi, H. Brown et al., “A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons,” The EMBO Journal, vol. 23, no. 11, pp. 2235–2245, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. J. M. Nussbaum, S. Schilling, H. Cynis et al., “Prion-like behaviour and tau-dependent cytotoxicity of pyroglutamylated amyloid-beta,” Nature, vol. 485, no. 7400, pp. 651–655, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. I. Benilova, E. Karran, and B. De Strooper, “The toxic Aβ oligomer and Alzheimer's disease: an emperor in need of clothes,” Nature Neuroscience, vol. 15, no. 3, pp. 349–357, 2012. View at Publisher · View at Google Scholar
  84. D. J. Selkoe, “Soluble oligomers of the amyloid β-protein impair synaptic plasticity and behavior,” Behavioural Brain Research, vol. 192, no. 1, pp. 106–113, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. G. Pigino, G. Morfini, A. Pelsman, M. P. Mattson, S. T. Brady, and J. Busciglio, “Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport,” Journal of Neuroscience, vol. 23, no. 11, pp. 4499–4508, 2003. View at Google Scholar · View at Scopus
  86. H. Bros, A. Hauser, F. Paul, R. Niesner, and C. Infante-Duarte, “Assessing mitochondrial movement within neurons: manual versus automated tracking methods,” Traffic, vol. 16, no. 8, pp. 906–917, 2015. View at Publisher · View at Google Scholar
  87. D. Horiuchi, C. A. Collins, P. Bhat, R. V. Barkus, A. Diantonio, and W. M. Saxton, “Control of a kinesin-cargo linkage mechanism by JNK pathway kinases,” Current Biology, vol. 17, no. 15, pp. 1313–1317, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. K. Hensley, D. A. Butterfield, N. Hall et al., “Reactive oxygen species as causal agents in the neurotoxicity of the Alzheimer's disease-associated amyloid beta peptide,” Annals of the New York Academy of Sciences, vol. 786, pp. 120–134, 1996. View at Publisher · View at Google Scholar · View at Scopus
  89. A. Maruszak and C. Zekanowski, “Mitochondrial dysfunction and Alzheimer's disease,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 35, no. 2, pp. 320–330, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. X. Gu, J. Sun, S. Li, X. Wu, and L. Li, “Oxidative stress induces DNA demethylation and histone acetylation in SH-SY5Y cells: potential epigenetic mechanisms in gene transcription in Aβ production,” Neurobiology of Aging, vol. 34, no. 4, pp. 1069–1079, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. E. Edelmann, V. Leßmann, and T. Brigadski, “Pre- and postsynaptic twists in BDNF secretion and action in synaptic plasticity,” Neuropharmacology, vol. 76, pp. 610–627, 2014. View at Publisher · View at Google Scholar · View at Scopus
  92. B.-K. Choi, J.-Y. Kim, M.-Y. Cha, I. Mook-Jung, Y.-K. Shin, and N. K. Lee, “β-Amyloid and α-synuclein cooperate to block SNARE-dependent vesicle fusion,” Biochemistry, vol. 54, no. 9, pp. 1831–1840, 2015. View at Publisher · View at Google Scholar
  93. Y. Yang, J. Kim, H. Y. Kim et al., “Amyloid-β oligomers may impair SNARE-mediated exocytosis by direct binding to syntaxin 1a,” Cell Reports, vol. 12, no. 8, pp. 1244–1251, 2015. View at Publisher · View at Google Scholar
  94. L. Groth-Pedersen, S. Aits, E. Corcelle-Termeau, N. H. T. Petersen, J. Nylandsted, and M. Jäättelä, “Identification of cytoskeleton-associated proteins essential for lysosomal stability and survival of human cancer cells,” PLoS ONE, vol. 7, no. 10, Article ID e45381, 2012. View at Publisher · View at Google Scholar · View at Scopus