Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2016, Article ID 2371970, 19 pages
http://dx.doi.org/10.1155/2016/2371970
Review Article

Regulation of the Postsynaptic Compartment of Excitatory Synapses by the Actin Cytoskeleton in Health and Its Disruption in Disease

1Neurodegeneration and Repair Unit, School of Medical Sciences, University of New South Wales, Sydney, NSW 2052, Australia
2Translational Neuroscience Facility, School of Medical Sciences, University of New South Wales, Sydney, NSW 2052, Australia

Received 9 December 2015; Accepted 9 March 2016

Academic Editor: Zygmunt Galdzicki

Copyright © 2016 Holly Stefen 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. S. W. Scheff, D. A. Price, F. A. Schmitt, and E. J. Mufson, “Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment,” Neurobiology of Aging, vol. 27, no. 10, pp. 1372–1384, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. S. T. DeKosky and S. W. Scheff, “Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity,” Annals of Neurology, vol. 27, no. 5, pp. 457–464, 1990. View at Publisher · View at Google Scholar · View at Scopus
  3. R. D. Terry, E. Masliah, D. P. Salmon et al., “Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment,” Annals of Neurology, vol. 30, no. 4, pp. 572–580, 1991. View at Publisher · View at Google Scholar · View at Scopus
  4. T. Arendt, “Synaptic degeneration in Alzheimer's disease,” Acta Neuropathologica, vol. 118, no. 1, pp. 167–179, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. B. C. Dickerson and R. A. Sperling, “Large-scale functional brain network abnormalities in Alzheimer's disease: insights from functional neuroimaging,” Behavioural Neurology, vol. 21, no. 1-2, pp. 63–75, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Herholz, S. Westwood, C. Haense, and G. Dunn, “Evaluation of a calibrated 18F-FDG PET score as a biomarker for progression in alzheimer disease and mild cognitive impairment,” Journal of Nuclear Medicine, vol. 52, no. 8, pp. 1218–1226, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. K. M. Harris and S. B. Kater, “Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function,” Annual Review of Neuroscience, vol. 17, pp. 341–371, 1994. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Noguchi, M. Matsuzaki, G. C. R. Ellis-Davies, and H. Kasai, “Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites,” Neuron, vol. 46, no. 4, pp. 609–622, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. J. M. Power and P. Sah, “Dendritic spine heterogeneity and calcium dynamics in basolateral amygdala principal neurons,” Journal of Neurophysiology, vol. 112, no. 7, pp. 1616–1627, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Sheng and E. Kim, “The postsynaptic organization of synapses,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 12, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Okabe, “Molecular dynamics of the excitatory synapse,” Advances in Experimental Medicine and Biology, vol. 970, pp. 131–152, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. K. E. Sorra and K. M. Harris, “Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines,” Hippocampus, vol. 10, no. 5, pp. 501–511, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Peters and I. R. Kaiserman-Abramof, “The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines,” American Journal of Anatomy, vol. 127, no. 4, pp. 321–355, 1970. View at Publisher · View at Google Scholar · View at Scopus
  14. E. A. Nimchinsky, B. L. Sabatini, and K. Svoboda, “Structure and function of dendritic spines,” Annual Review of Physiology, vol. 64, pp. 313–353, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. N. Honkura, M. Matsuzaki, J. Noguchi, G. C. R. Ellis-Davies, and H. Kasai, “The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines,” Neuron, vol. 57, no. 5, pp. 719–729, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Noguchi, A. Nagaoka, S. Watanabe et al., “In vivo two-photon uncaging of glutamate revealing the structure-function relationships of dendritic spines in the neocortex of adult mice,” The Journal of Physiology, vol. 589, no. 10, pp. 2447–2457, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Bosch and Y. Hayashi, “Structural plasticity of dendritic spines,” Current Opinion in Neurobiology, vol. 22, no. 3, pp. 383–388, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Meyer, T. Bonhoeffer, and V. Scheuss, “Balance and stability of synaptic structures during synaptic plasticity,” Neuron, vol. 82, no. 2, pp. 430–443, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. K. M. Harris and J. K. Stevens, “Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics,” The Journal of Neuroscience, vol. 9, no. 8, pp. 2982–2997, 1989. View at Google Scholar · View at Scopus
  20. M. Matsuzaki, G. C. R. Ellis-Davies, T. Nemoto, Y. Miyashita, M. Iino, and H. Kasai, “Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons,” Nature Neuroscience, vol. 4, no. 11, pp. 1086–1092, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. J. T. Trachtenberg, B. E. Chen, G. W. Knott et al., “Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex,” Nature, vol. 420, no. 6917, pp. 788–794, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Matsuzaki, N. Honkura, G. C. R. Ellis-Davies, and H. Kasai, “Structural basis of long-term potentiation in single dendritic spines,” Nature, vol. 429, no. 6993, pp. 761–766, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Holtmaat, L. Wilbrecht, G. W. Knott, E. Welker, and K. Svoboda, “Experience-dependent and cell-type-specific spine growth in the neocortex,” Nature, vol. 441, no. 7096, pp. 979–983, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Spacek and K. M. Harris, “Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat,” Journal of Neuroscience, vol. 17, no. 1, pp. 190–203, 1997. View at Google Scholar · View at Scopus
  25. A. J. G. D. Holtmaat, J. T. Trachtenberg, L. Wilbrecht et al., “Transient and persistent dendritic spines in the neocortex in vivo,” Neuron, vol. 45, no. 2, pp. 279–291, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Yoshihara, M. De Roo, and D. Muller, “Dendritic spine formation and stabilization,” Current Opinion in Neurobiology, vol. 19, no. 2, pp. 146–153, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Fifková and R. I. Delay, “Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity,” The Journal of Cell Biology, vol. 95, no. 1, pp. 345–350, 1982. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Korobova and T. M. Svitkina, “Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis,” Molecular Biology of the Cell, vol. 21, no. 1, pp. 165–176, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Hotulainen and C. C. Hoogenraad, “Actin in dendritic spines: connecting dynamics to function,” Journal of Cell Biology, vol. 189, no. 4, pp. 619–629, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. E. N. Star, D. J. Kwiatkowski, and V. N. Murthy, “Rapid turnover of actin in dendritic spines and its regulation by activity,” Nature Neuroscience, vol. 5, no. 3, pp. 239–246, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. K.-I. Okamoto, T. Nagai, A. Miyawaki, and Y. Hayashi, “Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity,” Nature Neuroscience, vol. 7, no. 10, pp. 1104–1112, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. N. A. Frost, H. Shroff, H. Kong, E. Betzig, and T. A. Blanpied, “Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines,” Neuron, vol. 67, no. 1, pp. 86–99, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. U. V. Nägerl, K. I. Willig, B. Hein, S. W. Hell, and T. Bonhoeffer, “Live-cell imaging of dendritic spines by STED microscopy,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 48, pp. 18982–18987, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. H. D. MacGillavry and C. C. Hoogenraad, “The internal architecture of dendritic spines revealed by super-resolution imaging: what did we learn so far?” Experimental Cell Research, vol. 335, no. 2, pp. 180–186, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. H. E. Lu, H. D. MacGillavry, N. A. Frost, and T. A. Blanpied, “Multiple spatial and kinetic subpopulations of CaMKII in spines and dendrites as resolved by single-molecule tracking PALM,” Journal of Neuroscience, vol. 34, no. 22, pp. 7600–7610, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Okamoto, M. Bosch, and Y. Hayashi, “The roles of CaMKII and F-actin in the structural plasticity of dendritic spines: a potential molecular identity of a synaptic tag?” Physiology, vol. 24, no. 6, pp. 357–366, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Tønnesen, G. Katona, B. Rózsa, and U. V. Nägerl, “Spine neck plasticity regulates compartmentalization of synapses,” Nature Neuroscience, vol. 17, no. 5, pp. 678–685, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. E. S. Harris and H. N. Higgs, “Actin cytoskeleton: formins lead the way,” Current Biology, vol. 14, no. 13, pp. R520–R522, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. B. L. Goode and M. J. Eck, “Mechanism and function of formins in the control of actin assembly,” Annual Review of Biochemistry, vol. 76, pp. 593–627, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Watanabe, T. Kato, A. Fujita, T. Ishizaki, and S. Narumiya, “Cooperation between mDia1 and ROCK in Rho-induced actin reorganization,” Nature Cell Biology, vol. 1, no. 3, pp. 136–143, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Aspenström, N. Richnau, and A.-S. Johansson, “The diaphanous-related formin DAAM1 collaborates with the Rho GTPases RhoA and Cdc42, CIP4 and Src in regulating cell morphogenesis and actin dynamics,” Experimental Cell Research, vol. 312, no. 12, pp. 2180–2194, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Matusek, R. Gombos, A. Szécsényi et al., “Formin proteins of the DAAM subfamily play a role during axon growth,” The Journal of Neuroscience, vol. 28, no. 49, pp. 13310–13319, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Hotulainen, O. Llano, S. Smirnov et al., “Defning mechanisms of actin polymerization and depolymerization during Dendritic spine morphogenesis,” Journal of Cell Biology, vol. 185, no. 2, pp. 323–339, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Chazeau, A. Mehidi, D. Nair et al., “Nanoscale segregation of actin nucleation and elongation factors determines dendritic spine protrusion,” EMBO Journal, vol. 33, no. 23, pp. 2745–2764, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. I. Rouiller, X.-P. Xu, K. J. Amann et al., “The structural basis of actin filament branching by the Arp2/3 complex,” The Journal of Cell Biology, vol. 180, no. 5, pp. 887–895, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. F. Korobova and T. Svitkina, “Arp2/3 complex is important for filopodia formation, growth cone motility, and neuritogenesis in neuronal cells,” Molecular Biology of the Cell, vol. 19, no. 4, pp. 1561–1574, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. B. Rácz and R. J. Weinberg, “Organization of the Arp2/3 complex in hippocampal spines,” Journal of Neuroscience, vol. 28, no. 22, pp. 5654–5659, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. Q. Yang, X.-F. Zhang, T. D. Pollard, and P. Forscher, “Arp2/3 complex-dependent actin networks constrain myosin II function in driving retrograde actin flow,” Journal of Cell Biology, vol. 197, no. 7, pp. 939–956, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. J. D. Rotty, C. Wu, and J. E. Bear, “New insights into the regulation and cellular functions of the ARP2/3 complex,” Nature Reviews Molecular Cell Biology, vol. 14, no. 1, pp. 7–12, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. S. N. Duleh and M. D. Welch, “WASH and the Arp2/3 complex regulate endosome shape and trafficking,” Cytoskeleton, vol. 67, no. 3, pp. 193–206, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Suarez, R. T. Carroll, T. A. Burke et al., “Profilin regulates F-Actin network homeostasis by favoring formin over Arp2/3 complex,” Developmental Cell, vol. 32, no. 1, pp. 43–53, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. E. D. Korn, M.-F. Carlier, and D. Pantaloni, “Actin polymerization and ATP hydrolysis,” Science, vol. 238, no. 4827, pp. 638–644, 1987. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Muhlrad, D. Pavlov, Y. M. Peyser, and E. Reisler, “Inorganic phosphate regulates the binding of cofilin to actin filaments,” FEBS Journal, vol. 273, no. 7, pp. 1488–1496, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. B. W. Bernstein and J. R. Bamburg, “ADF/Cofilin: a functional node in cell biology,” Trends in Cell Biology, vol. 20, no. 4, pp. 187–195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Arber, F. A. Barbayannis, H. Hanser et al., “Regulation of actin dynamics through phosphorylation of cofilin by LIM- kinase,” Nature, vol. 393, no. 6687, pp. 805–809, 1998. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Yang, O. Higuchi, K. Ohashi et al., “Cofflin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization,” Nature, vol. 393, no. 6687, pp. 809–812, 1998. View at Publisher · View at Google Scholar · View at Scopus
  57. V. E. Galkin, A. Orlova, D. S. Kudryashov et al., “Remodeling of actin filaments by ADF/cofilin proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 51, pp. 20568–20572, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. J.-H. Chen, Y. Kellner, M. Zagrebelsky, M. Grunwald, M. Korte, and P. J. Walla, “Two-photon correlation spectroscopy in single dendritic spines reveals fast actin filament reorganization during activity-dependent growth,” PLoS ONE, vol. 10, no. 5, Article ID e0128241, 2015. View at Publisher · View at Google Scholar · View at Scopus
  59. B. K. Garvalov, K. C. Flynn, D. Neukirchen et al., “Cdc42 regulates cofilin during the establishment of neuronal polarity,” Journal of Neuroscience, vol. 27, no. 48, pp. 13117–13129, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. Ashish, M. S. Paine, P. B. Perryman, L. Yang, H. L. Yin, and J. K. Krueger, “Global structure changes associated with Ca2+ activation of full-length human plasma gelsolin,” Journal of Biological Chemistry, vol. 282, no. 35, pp. 25884–25892, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. H. Choe, L. D. Burtnick, M. Mejillano, H. L. Yin, R. C. Robinson, and S. Choe, “The calcium activation of gelsolin: insights from the 3Å structure of the G4-G6/actin complex,” Journal of Molecular Biology, vol. 324, no. 4, pp. 691–702, 2002. View at Google Scholar
  62. L. D. Burtnick, D. Urosev, E. Irobi, K. Narayan, and R. C. Robinson, “Structure of the Nterminal half of gelsolin bound to actin: roles in severing, apoptosis and FAF,” The EMBO Journal, vol. 23, no. 14, pp. 2713–2722, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. P. A. Janmey, C. Chaponnier, S. E. Lind, K. S. Zaner, T. P. Stossel, and H. L. Yin, “Interactions of gelsolin and gelsolin-actin complexes with actin. Effects of calcium on actin nucleation, filament severing, and end blocking,” Biochemistry, vol. 24, no. 14, pp. 3714–3723, 1985. View at Publisher · View at Google Scholar · View at Scopus
  64. H. J. Kinosian, J. Newman, B. Lincoln, L. A. Selden, L. C. Gershman, and J. E. Estes, “Ca2+ regulation of gelsolin activity: binding and severing of F-actin,” Biophysical Journal, vol. 75, no. 6, pp. 3101–3109, 1998. View at Publisher · View at Google Scholar · View at Scopus
  65. P. Silacci, L. Mazzolai, C. Gauci, N. Stergiopulos, H. L. Yin, and D. Hayoz, “Gelsolin superfamily proteins: key regulators of cellular functions,” Cellular and Molecular Life Sciences, vol. 61, no. 19-20, pp. 2614–2623, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. P. A. Janmey and T. P. Stossel, “Modulation of gelsolin function by phosphatidylinositol 4,5-bisphosphate,” Nature, vol. 325, no. 6102, pp. 362–364, 1987. View at Publisher · View at Google Scholar · View at Scopus
  67. J. H. Hartwig, G. M. Bokoch, C. L. Carpenter et al., “Thrombin receptor ligation and activated rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets,” Cell, vol. 82, no. 4, pp. 643–653, 1995. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Nag, M. Larsson, R. C. Robinson, and L. D. Burtnick, “Gelsolin: the tail of a molecular gymnast,” Cytoskeleton, vol. 70, no. 7, pp. 360–384, 2013. View at Publisher · View at Google Scholar · View at Scopus
  69. E. J. Furnish, W. Zhou, C. C. Cunningham, J. A. Kas, and C. E. Schmidt, “Gelsolin overexpression enhances neurite outgrowth in PC12 cells,” FEBS Letters, vol. 508, no. 2, pp. 282–286, 2001. View at Publisher · View at Google Scholar · View at Scopus
  70. H.-T. Hu and Y.-P. Hsueh, “Calcium influx and postsynaptic proteins coordinate the dendritic filopodium-spine transition,” Developmental Neurobiology, vol. 74, no. 10, pp. 1011–1029, 2014. View at Publisher · View at Google Scholar · View at Scopus
  71. A. Ivanov, M. Esclapez, C. Pellegrino, T. Shirao, and L. Ferhat, “Drebrin A regulates dendritic spine plasticity and synaptic function in mature cultured hippocampal neurons,” Journal of Cell Science, vol. 122, no. 4, pp. 524–534, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Ishikawa, K. Katoh, A. Takahashi et al., “Drebrin attenuates the interaction between actin and myosin-V,” Biochemical and Biophysical Research Communications, vol. 359, no. 2, pp. 398–401, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. M. A. Mikati, E. E. Grintsevich, and E. Reisler, “Drebrin-induced stabilization of actin filaments,” Journal of Biological Chemistry, vol. 288, no. 27, pp. 19926–19938, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Sharma, E. E. Grintsevich, M. L. Phillips, E. Reisler, and J. K. Gimzewski, “Atomic force microscopy reveals drebrin induced remodeling of F-actin with subnanometer resolution,” Nano Letters, vol. 11, no. 2, pp. 825–827, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. E. E. Grintsevich and E. Reisler, “Drebrin inhibits cofilin-induced severing of F-actin,” Cytoskeleton, vol. 71, no. 8, pp. 472–483, 2014. View at Publisher · View at Google Scholar · View at Scopus
  76. P. W. Gunning, G. Schevzov, A. J. Kee, and E. C. Hardeman, “Tropomyosin isoforms: divining rods for actin cytoskeleton function,” Trends in Cell Biology, vol. 15, no. 6, pp. 333–341, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. X. Li, K. C. Holmes, W. Lehman, H. Jung, and S. Fischer, “The shape and flexibility of tropomyosin coiled coils: implications for actin filament assembly and regulation,” Journal of Molecular Biology, vol. 395, no. 2, pp. 327–339, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. X. Li, L. S. Tobacman, J. Y. Mun, R. Craig, S. Fischer, and W. Lehman, “Tropomyosin position on F-actin revealed by EM reconstruction and computational chemistry,” Biophysical Journal, vol. 100, no. 4, pp. 1005–1013, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. K. Guven, P. Gunning, and T. Fath, “TPM3 and TPM4 gene products segregate to the postsynaptic region of central nervous system synapses,” Bioarchitecture, vol. 1, no. 6, pp. 284–289, 2011. View at Publisher · View at Google Scholar
  80. G. Schevzov, S. P. Whittaker, T. Fath, J. J. Lin, and P. W. Gunning, “Tropomyosin isoforms and reagents,” Bioarchitecture, vol. 1, pp. 135–164, 2011. View at Google Scholar
  81. W. Lehman, V. Hatch, V. Korman et al., “Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments,” Journal of Molecular Biology, vol. 302, no. 3, pp. 593–606, 2000. View at Publisher · View at Google Scholar · View at Scopus
  82. N. S. Bryce, G. Schevzov, V. Ferguson et al., “Specification of actin filament function and molecular composition by tropomyosin isoforms,” Molecular Biology of the Cell, vol. 14, no. 3, pp. 1002–1016, 2003. View at Publisher · View at Google Scholar · View at Scopus
  83. G. Schevzov, N. S. Bryce, R. Almonte-Baldonado et al., “Specific features of neuronal size and shape are regulated by tropomyosin isoforms,” Molecular Biology of the Cell, vol. 16, no. 7, pp. 3425–3437, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. G. Schevzov, T. Fath, B. Vrhovski et al., “Divergent regulation of the sarcomere and the cytoskeleton,” The Journal of Biological Chemistry, vol. 283, no. 1, pp. 275–283, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. T. Fath, Y.-K. Agnes Chan, B. Vrhovski et al., “New aspects of tropomyosin-regulated neuritogenesis revealed by the deletion of Tm5NM1 and 2,” European Journal of Cell Biology, vol. 89, no. 7, pp. 489–498, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. Fan, X. Tang, E. Vitriol, G. Chen, and J. Q. Zheng, “Actin capping protein is required for dendritic spine development and synapse formation,” Journal of Neuroscience, vol. 31, no. 28, pp. 10228–10233, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. M. Hertzog, F. Milanesi, L. Hazelwood et al., “Molecular basis for the dual function of Eps8 on actin dynamics: bundling and capping,” PLoS Biology, vol. 8, no. 6, Article ID e1000387, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. E. Stamatakou, A. Marzo, A. Gibb, and P. C. Salinas, “Activity-dependent spine morphogenesis: a role for the actin-capping protein Eps8,” The Journal of Neuroscience, vol. 33, no. 6, pp. 2661–2670, 2013. View at Publisher · View at Google Scholar · View at Scopus
  89. D. Gremm and A. Wegner, “Gelsolin as a calcium-regulated actin filament-capping protein,” European Journal of Biochemistry, vol. 267, no. 14, pp. 4339–4345, 2000. View at Publisher · View at Google Scholar · View at Scopus
  90. M. A. Hartman and J. A. Spudich, “The myosin superfamily at a glance,” Journal of Cell Science, vol. 125, no. 7, pp. 1627–1632, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. M. L. Walker, S. A. Burgess, J. R. Sellers et al., “Two-headed binding of a processive myosin to F-actin,” Nature, vol. 405, no. 6788, pp. 804–807, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. J. N. Forkey, M. E. Quinlan, M. A. Shaw, J. E. T. Corrie, and Y. E. Goldman, “Three-dimensional structural dynamics of myosin V by single-molecule fluorescence polarization,” Nature, vol. 422, no. 6930, pp. 399–404, 2003. View at Publisher · View at Google Scholar · View at Scopus
  93. G. E. Snyder, T. Sakamoto, J. A. Hammer III, J. R. Sellers, and P. R. Selvin, “Nanometer localization of single fluorescent proteins: evidence that myosin V walks hand-over-hand via telemark configuration,” Biophysical Journal, vol. 87, no. 3, pp. 1776–1783, 2004. View at Publisher · View at Google Scholar · View at Scopus
  94. D. M. Warshaw, G. G. Kennedy, S. S. Work, E. B. Krementsova, S. Beck, and K. M. Trybus, “Differential labeling of myosin V heads with quantum dots allows direct visualization of hand-over-hand processivity,” Biophysical Journal, vol. 88, no. 5, pp. L30–L32, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. E. Osterweil, D. G. Wells, and M. S. Mooseker, “A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis,” Journal of Cell Biology, vol. 168, no. 2, pp. 329–338, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. Z. Wang, J. G. Edwards, N. Riley et al., “Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity,” Cell, vol. 135, no. 3, pp. 535–548, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. N. L. Rochefort and A. Konnerth, “Dendritic spines: from structure to in vivo function,” EMBO Reports, vol. 13, no. 8, pp. 699–708, 2012. View at Publisher · View at Google Scholar · View at Scopus
  98. R. C. Malenka and M. F. Bear, “LTP and LTD: an embarrassment of riches,” Neuron, vol. 44, no. 1, pp. 5–21, 2004. View at Publisher · View at Google Scholar · View at Scopus
  99. Y. Yang, X.-B. Wang, M. Frerking, and Q. Zhou, “Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 32, pp. 11388–11393, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. Q. Zhou, K. J. Homma, and M.-M. Poo, “Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses,” Neuron, vol. 44, no. 5, pp. 749–757, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi, “Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo,” Neuron, vol. 38, no. 3, pp. 447–460, 2003. View at Publisher · View at Google Scholar · View at Scopus
  102. T. Krucker, G. R. Siggins, and S. Halpain, “Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 12, pp. 6856–6861, 2000. View at Publisher · View at Google Scholar · View at Scopus
  103. H. Udo, I. Jin, J.-H. Kim et al., “Serotonin-induced regulation of the actin network for learning-related synaptic growth requires Cdc42, N-WASP, and PAK in Aplysia sensory neurons,” Neuron, vol. 45, no. 6, pp. 887–901, 2005. View at Publisher · View at Google Scholar · View at Scopus
  104. F. Huang, J. K. Chotiner, and O. Steward, “Actin polymerization and ERK phosphorylation are required for Arc/Arg3.1 mRNA targeting to activated synaptic sites on dendrites,” Journal of Neuroscience, vol. 27, no. 34, pp. 9054–9067, 2007. View at Publisher · View at Google Scholar · View at Scopus
  105. B. Ramachandran and J. U. Frey, “Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro,” The Journal of Neuroscience, vol. 29, no. 39, pp. 12167–12173, 2009. View at Publisher · View at Google Scholar · View at Scopus
  106. R. Fonseca, “Activity-dependent actin dynamics are required for the maintenance of long-term plasticity and for synaptic capture,” The European Journal of Neuroscience, vol. 35, no. 2, pp. 195–206, 2012. View at Publisher · View at Google Scholar · View at Scopus
  107. W. Morishita, H. Marie, and R. C. Malenka, “Distinct triggering and expression mechanisms underlie LTD of AMPA and NMDA synaptic responses,” Nature Neuroscience, vol. 8, no. 8, pp. 1043–1050, 2005. View at Publisher · View at Google Scholar · View at Scopus
  108. R. Lamprecht, “The actin cytoskeleton in memory formation,” Progress in Neurobiology, vol. 117, pp. 1–19, 2014. View at Publisher · View at Google Scholar · View at Scopus
  109. L. Y. Chen, C. S. Rex, M. S. Casale, C. M. Gall, and G. Lynch, “Changes in synaptic morphology accompany actin signaling during LTP,” Journal of Neuroscience, vol. 27, no. 20, pp. 5363–5372, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. M. Bosch, J. Castro, T. Saneyoshi, H. Matsuno, M. Sur, and Y. Hayashi, “Structural and molecular remodeling of dendritic spine substructures during long-term potentiation,” Neuron, vol. 82, no. 2, pp. 444–459, 2014. View at Publisher · View at Google Scholar · View at Scopus
  111. A. Reichenbach, A. Derouiche, and F. Kirchhoff, “Morphology and dynamics of perisynaptic glia,” Brain Research Reviews, vol. 63, no. 1-2, pp. 11–25, 2010. View at Publisher · View at Google Scholar · View at Scopus
  112. Y. Bernardinelli, J. Randall, E. Janett et al., “Activity-dependent structural plasticity of perisynaptic astrocytic domains promotes excitatory synapse stability,” Current Biology, vol. 24, no. 15, pp. 1679–1688, 2014. View at Publisher · View at Google Scholar · View at Scopus
  113. M. Horak, R. S. Petralia, M. Kaniakova, and N. Sans, “ER to synapse trafficking of NMDA receptors,” Frontiers in Cellular Neuroscience, vol. 8, article 394, 2014. View at Publisher · View at Google Scholar · View at Scopus
  114. R. L. Huganir and R. A. Nicoll, “AMPARs and synaptic plasticity: the last 25 years,” Neuron, vol. 80, no. 3, pp. 704–717, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. L. Ladépêche, J. P. Dupuis, and L. Groc, “Surface trafficking of NMDA receptors: gathering from a partner to another,” Seminars in Cell and Developmental Biology, vol. 27, pp. 3–13, 2014. View at Publisher · View at Google Scholar · View at Scopus
  116. M.-F. Lisé, T. P. Wong, A. Trinh et al., “Involvement of myosin Vb in glutamate receptor trafficking,” The Journal of Biological Chemistry, vol. 281, no. 6, pp. 3669–3678, 2006. View at Publisher · View at Google Scholar · View at Scopus
  117. S. S. Correia, S. Bassani, T. C. Brown et al., “Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation,” Nature Neuroscience, vol. 11, no. 4, pp. 457–466, 2008. View at Publisher · View at Google Scholar · View at Scopus
  118. K. R. Tovar and G. L. Westbrook, “Mobile NMDA receptors at hippocampal synapses,” Neuron, vol. 34, no. 2, pp. 255–264, 2002. View at Publisher · View at Google Scholar · View at Scopus
  119. A. Sergé, L. Fourgeaud, A. Hémar, and D. Choquet, “Active surface transport of metabotropic glutamate receptors through binding to microtubules and actin flow,” Journal of Cell Science, vol. 116, no. 24, pp. 5015–5022, 2003. View at Publisher · View at Google Scholar · View at Scopus
  120. G. L. Collingridge, R. W. Olsen, J. Peters, and M. Spedding, “A nomenclature for ligand-gated ion channels,” Neuropharmacology, vol. 56, no. 1, pp. 2–5, 2009. View at Publisher · View at Google Scholar · View at Scopus
  121. M. L. Mayer and N. Armstrong, “Structure and function of glutamate receptor ion channels,” Annual Review of Physiology, vol. 66, pp. 161–181, 2004. View at Publisher · View at Google Scholar · View at Scopus
  122. W. Lu, Y. Shi, A. C. Jackson et al., “Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach,” Neuron, vol. 62, no. 2, pp. 254–268, 2009. View at Publisher · View at Google Scholar · View at Scopus
  123. D. W. Allison, V. I. Gelfand, I. Spector, and A. M. Craig, “Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors,” The Journal of Neuroscience, vol. 18, no. 7, pp. 2423–2436, 1998. View at Google Scholar · View at Scopus
  124. Q. Zhou, M.-Y. Xiao, and R. A. Nicoll, “Contribution of cytoskeleton to the internalization of AMPA receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 3, pp. 1261–1266, 2001. View at Publisher · View at Google Scholar · View at Scopus
  125. P. Penzes and M. E. Cahill, “Deconstructing signal transduction pathways that regulate the actin cytoskeleton in dendritic spines,” Cytoskeleton, vol. 69, no. 7, pp. 426–441, 2012. View at Publisher · View at Google Scholar · View at Scopus
  126. D. A. Applewhite, M. Barzik, S.-I. Kojima, T. M. Svitkina, F. B. Gertler, and G. G. Borisy, “Ena/VASP proteins have an anti-capping independent function in filopodia formation,” Molecular Biology of the Cell, vol. 18, no. 7, pp. 2579–2591, 2007. View at Publisher · View at Google Scholar · View at Scopus
  127. L. Pasic, T. Kotova, and D. A. Schafer, “Ena/VASP proteins capture actin filament barbed ends,” Journal of Biological Chemistry, vol. 283, no. 15, pp. 9814–9819, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. S. D. Hansen and R. D. Mullins, “VASP is a processive actin polymerase that requires monomeric actin for barbed end association,” Journal of Cell Biology, vol. 191, no. 3, pp. 571–584, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. W.-H. Lin, C. A. Nebhan, B. R. Anderson, and D. J. Webb, “Vasodilator-stimulated phosphoprotein (VASP) induces actin assembly in dendritic spines to promote their development and potentiate synaptic strength,” The Journal of Biological Chemistry, vol. 285, no. 46, pp. 36010–36020, 2010. View at Publisher · View at Google Scholar · View at Scopus
  130. D. L. Rocca, S. Martin, E. L. Jenkins, and J. G. Hanley, “Inhibition of Arp2/3-mediated actin polymerization by PICK1 regulates neuronal morphology and AMPA receptor endocytosis,” Nature Cell Biology, vol. 10, no. 3, pp. 259–271, 2008. View at Publisher · View at Google Scholar · View at Scopus
  131. D. L. Rocca, M. Amici, A. Antoniou et al., “The small GTPase Arf1 modulates Arp2/3-mediated actin polymerization via PICK1 to regulate synaptic plasticity,” Neuron, vol. 79, no. 2, pp. 293–307, 2013. View at Publisher · View at Google Scholar · View at Scopus
  132. A. Citri, S. Bhattacharyya, C. Ma et al., “Calcium binding to PICK1 is essential for the intracellular retention of AMPA receptors underlying long-term depression,” The Journal of Neuroscience, vol. 30, no. 49, pp. 16437–16452, 2010. View at Publisher · View at Google Scholar · View at Scopus
  133. J. A. Hammer III and W. Wagner, “Functions of class V myosins in neurons,” The Journal of Biological Chemistry, vol. 288, no. 40, pp. 28428–28434, 2013. View at Publisher · View at Google Scholar · View at Scopus
  134. W. Wagner, S. D. Brenowitz, and J. A. Hammer III, “Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons,” Nature Cell Biology, vol. 13, no. 1, pp. 40–47, 2011. View at Publisher · View at Google Scholar · View at Scopus
  135. S. H. Lee, A. Simonetta, and M. Sheng, “Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons,” Neuron, vol. 43, no. 2, pp. 221–236, 2004. View at Publisher · View at Google Scholar · View at Scopus
  136. M. Park, E. C. Penick, J. G. Edwards, J. A. Kauer, and M. D. Ehlers, “Recycling endosomes supply AMPA receptors for LTP,” Science, vol. 305, no. 5692, pp. 1972–1975, 2004. View at Publisher · View at Google Scholar · View at Scopus
  137. L. A. Lapierre, R. Kumar, C. M. Hales et al., “Myosin Vb is associated with plasma membrane recycling systems,” Molecular Biology of the Cell, vol. 12, no. 6, pp. 1843–1857, 2001. View at Google Scholar
  138. A. L. Wells, A. W. Lin, L.-Q. Chen et al., “Myosin VI is an actin-based motor that moves backwards,” Nature, vol. 401, no. 6752, pp. 505–508, 1999. View at Publisher · View at Google Scholar · View at Scopus
  139. J. Ménétrey, A. Bahloul, A. L. Wells et al., “The structure of the myosin VI motor reveals the mechanism of directionality reversal,” Nature, vol. 435, no. 7043, pp. 779–785, 2005. View at Publisher · View at Google Scholar · View at Scopus
  140. H. Wu, J. E. Nash, P. Zamorano, and C. C. Garner, “Interaction of SAP97 with minus-end-directed actin motor myosin VI. Implications for AMPA receptor trafficking,” The Journal of Biological Chemistry, vol. 277, no. 34, pp. 30928–30934, 2002. View at Publisher · View at Google Scholar · View at Scopus
  141. J. Gu, C. W. Lee, Y. Fan et al., “ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity,” Nature Neuroscience, vol. 13, no. 10, pp. 1208–1215, 2010. View at Publisher · View at Google Scholar · View at Scopus
  142. E. Y. Yuen, W. Liu, T. Kafri, H. van Praag, and Z. Yan, “Regulation of AMPA receptor channels and synaptic plasticity by cofilin phosphatase Slingshot in cortical neurons,” Journal of Physiology, vol. 588, no. 13, pp. 2361–2371, 2010. View at Publisher · View at Google Scholar · View at Scopus
  143. Y. Wang, Q. Dong, X.-F. Xu et al., “Phosphorylation of cofilin regulates extinction of conditioned aversive memory via AMPAR trafficking,” The Journal of Neuroscience, vol. 33, no. 15, pp. 6423–6433, 2013. View at Publisher · View at Google Scholar · View at Scopus
  144. K. Kato, T. Shirao, H. Yamazaki, K. Imamura, and Y. Sekino, “Regulation of AMPA receptor recruitment by the actin binding protein drebrin in cultured hippocampal neurons,” Journal of Neuroscience and Neuroengineering, vol. 1, no. 2, pp. 153–160, 2012. View at Publisher · View at Google Scholar
  145. L. D. Walensky, S. Blackshaw, D. Liao et al., “A novel neuron-enriched homolog of the erythrocyte membrane cytoskeletal protein 4.1,” The Journal of Neuroscience, vol. 19, no. 15, pp. 6457–6467, 1999. View at Google Scholar · View at Scopus
  146. L. Shen, F. Liang, L. D. Walensky, and R. L. Huganir, “Regulation of AMPA receptor GluR1 subunit surface expression by a 4.1 N-linked actin cytoskeletal association,” The Journal of Neuroscience, vol. 20, no. 21, pp. 7932–7940, 2000. View at Google Scholar · View at Scopus
  147. L. C. Kapitein and C. C. Hoogenraad, “Which way to go? Cytoskeletal organization and polarized transport in neurons,” Molecular and Cellular Neuroscience, vol. 46, no. 1, pp. 9–20, 2011. View at Publisher · View at Google Scholar · View at Scopus
  148. Y. Bu, N. Wang, S. Wang et al., “Myosin IIb-dependent regulation of actin dynamics is required for N-Methyl-D-aspartate receptor trafficking during synaptic plasticity,” Journal of Biological Chemistry, vol. 290, no. 42, pp. 25395–25410, 2015. View at Publisher · View at Google Scholar · View at Scopus
  149. M. Sheng, “Molecular organization of the postsynaptic specialization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 13, pp. 7058–7061, 2001. View at Publisher · View at Google Scholar · View at Scopus
  150. J. M. Montgomery, J. C. Selcher, J. E. Hanson, and D. V. Madison, “Dynamin-dependent NMDAR endocytosis during LTD and its dependence on synaptic state,” BMC Neuroscience, vol. 6, article 48, 2005. View at Publisher · View at Google Scholar · View at Scopus
  151. M. Wyszynski, J. Lin, A. Rao et al., “Competitive binding of α-actinin and calmodulin to the NMDA receptor,” Nature, vol. 385, no. 6615, pp. 439–442, 1997. View at Publisher · View at Google Scholar · View at Scopus
  152. A. W. Dunah, M. Wyszynski, D. M. Martin, M. Sheng, and D. G. Standaert, “α-Actinin-2 in rat striatum: localization and interaction with NMDA glutamate receptor subunits,” Molecular Brain Research, vol. 79, no. 1-2, pp. 77–87, 2000. View at Publisher · View at Google Scholar · View at Scopus
  153. J. Peng, M. J. Kim, D. Cheng, D. M. Duong, S. P. Gygi, and M. Sheng, “Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry,” The Journal of Biological Chemistry, vol. 279, no. 20, pp. 21003–21011, 2004. View at Publisher · View at Google Scholar · View at Scopus
  154. T. Nakagawa, J. A. Engler, and M. Sheng, “The dynamic turnover and functional roles of α-actinin in dendritic spines,” Neuropharmacology, vol. 47, no. 5, pp. 734–745, 2004. View at Publisher · View at Google Scholar · View at Scopus
  155. W. Nörenberg, F. Hofmann, P. Illes, K. Aktories, and D. K. Meyer, “Rundown of somatodendritic N-methyl-D-aspartate (NMDA) receptor channels in rat hippocampal neurones: evidence for a role of the small GTPase RhoA,” British Journal of Pharmacology, vol. 127, no. 5, pp. 1060–1063, 1999. View at Publisher · View at Google Scholar · View at Scopus
  156. C. Rosenmund and G. L. Westbrook, “Calcium-induced actin depolymerization reduces NMDA channel activity,” Neuron, vol. 10, no. 5, pp. 805–814, 1993. View at Publisher · View at Google Scholar · View at Scopus
  157. K. Furukawa, W. Fu, Y. Li, W. Witke, D. J. Kwiatkowski, and M. P. Mattson, “The actin-severing protein gelsolin modulates calcium channel and NMDA receptor activities and vulnerability to excitotoxicity in hippocampal neurons,” Journal of Neuroscience, vol. 17, no. 21, pp. 8178–8186, 1997. View at Google Scholar · View at Scopus
  158. E. B. Merriam, M. Millette, D. C. Lumbard et al., “Synaptic regulation of microtubule dynamics in dendritic spines by calcium, F-actin, and drebrin,” The Journal of Neuroscience, vol. 33, no. 42, pp. 16471–16482, 2013. View at Publisher · View at Google Scholar · View at Scopus
  159. S. K. Ultanir, J.-E. Kim, B. J. Hall, T. Deerinck, M. Ellisman, and A. Ghosh, “Regulation of spine morphology and spine density by NMDA receptor signaling in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 49, pp. 19553–19558, 2007. View at Publisher · View at Google Scholar · View at Scopus
  160. C. G. Pontrello, M.-Y. Sun, A. Lin, T. A. Fiacco, K. A. DeFea, and I. M. Ethell, “Cofilin under control of β-arrestin-2 in NMDA-dependent dendritic spine plasticity, long-term depression (LTD), and learning,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 7, pp. E442–E451, 2012. View at Publisher · View at Google Scholar · View at Scopus
  161. M.-Y. Xiao, B. Gustafsson, and Y.-P. Niu, “Metabotropic glutamate receptors in the trafficking of ionotropic glutamate and GABAA receptors at central synapses,” Current Neuropharmacology, vol. 4, no. 1, pp. 77–86, 2006. View at Publisher · View at Google Scholar · View at Scopus
  162. R. Luján, Z. Nusser, J. D. B. Roberts, R. Shigemoto, and P. Somogyi, “Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus,” European Journal of Neuroscience, vol. 8, no. 7, pp. 1488–1500, 1996. View at Publisher · View at Google Scholar · View at Scopus
  163. J. L. Esseltine, F. M. Ribeiro, and S. S. G. Ferguson, “Rab8 modulates metabotropic glutamate receptor subtype 1 intracellular trafficking and signaling in a protein kinase C-dependent manner,” The Journal of Neuroscience, vol. 32, no. 47, pp. 16933–16942, 2012. View at Publisher · View at Google Scholar · View at Scopus
  164. L. J. Volk, C. A. Daly, and K. M. Huber, “Differential roles for group 1 mGluR subtypes in induction and expression of chemically induced hippocampal long-term depression,” Journal of Neurophysiology, vol. 95, no. 4, pp. 2427–2438, 2006. View at Publisher · View at Google Scholar · View at Scopus
  165. U. Finckh, C. Kuschel, M. Anagnostouli et al., “Novel mutations and repeated findings of mutations in familial Alzheimer disease,” Neurogenetics, vol. 6, no. 2, pp. 85–89, 2005. View at Publisher · View at Google Scholar · View at Scopus
  166. M. J. Ball, V. Hachinski, A. Fox et al., “A new definition of Alzheimer's disease: a hippocampal dementia,” The Lancet, vol. 325, no. 8419, pp. 14–16, 1985. View at Publisher · View at Google Scholar · View at Scopus
  167. W. G. Honer, D. W. Dickson, J. Gleeson, and P. Davies, “Regional synaptic pathology in Alzheimer's disease,” Neurobiology of Aging, vol. 13, no. 3, pp. 375–382, 1992. View at Publisher · View at Google Scholar · View at Scopus
  168. H. B. M. Uylings and J. M. De Brabander, “Neuronal changes in normal human aging and Alzheimer's disease,” Brain and Cognition, vol. 49, no. 3, pp. 268–276, 2002. View at Publisher · View at Google Scholar · View at Scopus
  169. K. K. Leung, J. W. Bartlett, J. Barnes, E. N. Manning, S. Ourselin, and N. C. Fox, “Cerebral atrophy in mild cognitive impairment and Alzheimer disease: rates and acceleration,” Neurology, vol. 80, no. 7, pp. 648–654, 2013. View at Publisher · View at Google Scholar · View at Scopus
  170. M. Grundman, D. Sencakova, C. R. Jack Jr. et al., “Brain MRI hippocampal volume and prediction of clinical status in a mild cognitive impairment trial,” Journal of Molecular Neuroscience, vol. 19, no. 1-2, pp. 23–27, 2002. View at Publisher · View at Google Scholar · View at Scopus
  171. E. Frankó and O. Joly, “Evaluating Alzheimer’s disease progression using rate of regional hippocampal atrophy,” PLoS ONE, vol. 8, no. 8, Article ID e71354, 2013. View at Publisher · View at Google Scholar · View at Scopus
  172. J. P. Lerch, J. C. Pruessner, A. Zijdenbos, H. Hampel, S. J. Teipel, and A. C. Evans, “Focal decline of cortical thickness in Alzheimer's disease identified by computational neuroanatomy,” Cerebral Cortex, vol. 15, no. 7, pp. 995–1001, 2005. View at Publisher · View at Google Scholar · View at Scopus
  173. V. Singh, H. Chertkow, J. P. Lerch, A. C. Evans, A. E. Dorr, and N. J. Kabani, “Spatial patterns of cortical thinning in mild cognitive impairment and Alzheimer's disease,” Brain, vol. 129, no. 11, pp. 2885–2893, 2006. View at Publisher · View at Google Scholar · View at Scopus
  174. P. J. Hsu, H. Shou, T. Benzinger et al., “Amyloid burden in cognitively normal elderly is associated with preferential hippocampal subfield volume loss,” Journal of Alzheimer's Disease, vol. 45, no. 1, pp. 27–33, 2015. View at Publisher · View at Google Scholar · View at Scopus
  175. J. M. Schott, N. C. Fox, C. Frost et al., “Assessing the onset of structural change in familial Alzheimer's disease,” Annals of Neurology, vol. 53, no. 2, pp. 181–188, 2003. View at Publisher · View at Google Scholar · View at Scopus
  176. J. H. Morra, Z. Tu, L. G. Apostolova et al., “Automated 3D mapping of hippocampal atrophy and its clinical correlates in 400 subjects with Alzheimer's disease, mild cognitive impairment, and elderly controls,” Human Brain Mapping, vol. 30, no. 9, pp. 2766–2788, 2009. View at Publisher · View at Google Scholar · View at Scopus
  177. F. Kamenetz, T. Tomita, H. Hsieh et al., “APP processing and synaptic function,” Neuron, vol. 37, no. 6, pp. 925–937, 2003. View at Publisher · View at Google Scholar · View at Scopus
  178. G. M. Shankar, S. Li, T. H. Mehta et al., “Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory,” Nature Medicine, vol. 14, no. 8, pp. 837–842, 2008. View at Publisher · View at Google Scholar · View at Scopus
  179. H. W. Querfurth and F. M. LaFerla, “Alzheimer's disease,” The New England Journal of Medicine, vol. 362, no. 4, pp. 329–344, 2010. View at Publisher · View at Google Scholar · View at Scopus
  180. L. M. Ittner, Y. D. Ke, F. Delerue et al., “Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models,” Cell, vol. 142, no. 3, pp. 387–397, 2010. View at Publisher · View at Google Scholar · View at Scopus
  181. O. A. Shipton, J. R. Leitz, J. Dworzak et al., “Tau protein is required for amyloid β-induced impairment of hippocampal long-term potentiation,” Journal of Neuroscience, vol. 31, no. 5, pp. 1688–1692, 2011. View at Publisher · View at Google Scholar · View at Scopus
  182. M. E. Seward, E. Swanson, A. Norambuena et al., “Amyloid-β signals through tau to drive ectopic neuronal cell cycle re-entry in alzheimer's disease,” Journal of Cell Science, vol. 126, no. 5, pp. 1278–1286, 2013. View at Publisher · View at Google Scholar · View at Scopus
  183. D. E. Hurtado, L. Molina-Porcel, M. Iba et al., “Aβ accelerates the spatiotemporal progression of tau pathology and augments tau amyloidosis in an Alzheimer mouse model,” American Journal of Pathology, vol. 177, no. 4, pp. 1977–1988, 2010. View at Publisher · View at Google Scholar · View at Scopus
  184. M. A. Chabrier, D. Cheng, N. A. Castello, K. N. Green, and F. M. LaFerla, “Synergistic effects of amyloid-beta and wild-type human tau on dendritic spine loss in a floxed double transgenic model of Alzheimer's disease,” Neurobiology of Disease, vol. 64, pp. 107–117, 2014. View at Publisher · View at Google Scholar · View at Scopus
  185. K. T. Dineley, A. A. Pandya, and J. L. Yakel, “Nicotinic ACh receptors as therapeutic targets in CNS disorders,” Trends in Pharmacological Sciences, vol. 36, no. 2, pp. 96–108, 2015. View at Publisher · View at Google Scholar · View at Scopus
  186. M. L. Giuffrida, F. Caraci, B. Pignataro et al., “β-Amyloid monomers are neuroprotective,” The Journal of Neuroscience, vol. 29, no. 34, pp. 10582–10587, 2009. View at Publisher · View at Google Scholar · View at Scopus
  187. M. Guglielmotto, D. Monteleone, A. Piras et al., “Aβ1-42 monomers or oligomers have different effects on autophagy and apoptosis,” Autophagy, vol. 10, no. 10, pp. 1827–1843, 2014. View at Publisher · View at Google Scholar · View at Scopus
  188. C. Ye, D. M. Walsh, D. J. Selkoe, and D. M. Hartley, “Amyloid β-protein induced electrophysiological changes are dependent on aggregation state: N-methyl-D-aspartate (NMDA) versus non-NMDA receptor/channel activation,” Neuroscience Letters, vol. 366, no. 3, pp. 320–325, 2004. View at Publisher · View at Google Scholar · View at Scopus
  189. B. J. Cummings and C. W. Cotman, “Image analysis of β-amyloid load in Alzheimer's disease and relation to dementia severity,” The Lancet, vol. 346, no. 8989, pp. 1524–1528, 1995. View at Publisher · View at Google Scholar · View at Scopus
  190. C. M. Kirkwood, J. Ciuchta, M. D. Ikonomovic et al., “Dendritic spine density, morphology, and fibrillar actin content surrounding amyloid-β plaques in a mouse model of amyloid-β deposition,” Journal of Neuropathology and Experimental Neurology, vol. 72, no. 8, pp. 791–800, 2013. View at Publisher · View at Google Scholar · View at Scopus
  191. L. Mucke, E. Masliah, G.-Q. Yu et al., “High-level neuronal expression of Aβ(1–42) in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation,” The Journal of Neuroscience, vol. 20, no. 11, pp. 4050–4058, 2000. View at Google Scholar · View at Scopus
  192. C. A. McLean, R. A. Cherny, F. W. Fraser et al., “Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease,” Annals of Neurology, vol. 46, no. 6, pp. 860–866, 1999. View at Publisher · View at Google Scholar · View at Scopus
  193. A. J. Furst, G. D. Rabinovici, A. H. Rostomian et al., “Cognition, glucose metabolism and amyloid burden in Alzheimer's disease,” Neurobiology of Aging, vol. 33, no. 2, pp. 215–225, 2012. View at Publisher · View at Google Scholar · View at Scopus
  194. S. Zhu, J. He, R. Zhang et al., “Therapeutic effects of quetiapine on memory deficit and brain β-amyloid plaque pathology in a transgenic mouse model of Alzheimer's disease,” Current Alzheimer Research, vol. 10, no. 3, pp. 270–278, 2013. View at Publisher · View at Google Scholar · View at Scopus
  195. A.-G. Xuan, X.-B. Pan, P. Wei et al., “Valproic acid alleviates memory deficits and attenuates amyloid-β deposition in transgenic mouse model of Alzheimer’s disease,” Molecular Neurobiology, vol. 51, no. 1, pp. 300–312, 2014. View at Publisher · View at Google Scholar · View at Scopus
  196. P. E. Cramer, J. R. Cirrito, D. W. Wesson et al., “ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models,” Science, vol. 335, no. 6075, pp. 1503–1506, 2012. View at Publisher · View at Google Scholar · View at Scopus
  197. E. J. Mufson, E.-Y. Chen, E. J. Cochran, L. A. Beckett, D. A. Bennett, and J. H. Kordower, “Entorhinal cortex β-amyloid load in individuals with mild cognitive impairment,” Experimental Neurology, vol. 158, no. 2, pp. 469–490, 1999. View at Publisher · View at Google Scholar · View at Scopus
  198. P. N. Lacor, M. C. Buniel, P. W. Furlow et al., “Aβ oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease,” The Journal of Neuroscience, vol. 27, no. 4, pp. 796–807, 2007. View at Publisher · View at Google Scholar · View at Scopus
  199. K. H. Gylys, J. A. Fein, F. Yang, D. Wiley, C. A. Miller, and G. M. Cole, “Synaptic changes in Alzheimer's disease accompanied by decreased PSD-95 fluorescence,” American Journal of Pathology, vol. 165, no. 5, pp. 1809–1817, 2004. View at Google Scholar
  200. B. Calabrese, G. M. Shaked, I. V. Tabarean, J. Braga, E. H. Koo, and S. Halpain, “Rapid, concurrent alterations in pre- and postsynaptic structure induced by naturally-secreted amyloid-β protein,” Molecular and Cellular Neuroscience, vol. 35, no. 2, pp. 183–193, 2007. View at Publisher · View at Google Scholar · View at Scopus
  201. D. M. Walsh, I. Klyubin, J. V. Fadeeva et al., “Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo,” Nature, vol. 416, no. 6880, pp. 535–539, 2002. View at Publisher · View at Google Scholar · View at Scopus
  202. H.-W. Wang, J. F. Pasternak, H. Kuo et al., “Soluble oligomers of β amyloid (1–42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus,” Brain Research, vol. 924, no. 2, pp. 133–140, 2002. View at Publisher · View at Google Scholar · View at Scopus
  203. S. Li, S. Hong, N. E. Shepardson, D. M. Walsh, G. M. Shankar, and D. Selkoe, “Soluble oligomers of amyloid β protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake,” Neuron, vol. 62, no. 6, pp. 788–801, 2009. View at Publisher · View at Google Scholar · View at Scopus
  204. S. Petratos, Q.-X. Li, A. J. George et al., “The β-amyloid protein of Alzheimer's disease increases neuronal CRMP-2 phosphorylation by a Rho-GTP mechanism,” Brain, vol. 131, no. 1, pp. 90–108, 2008. View at Publisher · View at Google Scholar · View at Scopus
  205. A. Schmandke, A. Schmandke, and S. Strittmatter, “ROCK and Rho: biochemistry and neuronal functions of Rho-associated protein kinases,” Neurology, vol. 13, no. 5, pp. 454–469, 2010. View at Google Scholar
  206. B. Niederöst, T. Oertle, J. Fritsche, R. A. McKinney, and C. E. Bandtlow, “Nogo-A and myelin-associated glycoprotein mediate neurite growth inhibition by antagonistic regulation of RhoA and Rac1,” The Journal of Neuroscience, vol. 22, no. 23, pp. 10368–10376, 2002. View at Google Scholar · View at Scopus
  207. C. Hofmann, M. Shepelev, and J. Chernoff, “The genetics of Pak,” Journal of Cell Science, vol. 117, no. 19, pp. 4343–4354, 2004. View at Publisher · View at Google Scholar · View at Scopus
  208. J. Pozueta, R. Lefort, and M. L. Shelanski, “Synaptic changes in Alzheimer's disease and its models,” Neuroscience, vol. 251, pp. 51–65, 2013. View at Publisher · View at Google Scholar · View at Scopus
  209. L. Zhao, Q.-L. Ma, F. Calon et al., “Role of p21-activated kinase pathway defects in the cognitive deficits of Alzheimer disease,” Nature Neuroscience, vol. 9, no. 2, pp. 234–242, 2006. View at Publisher · View at Google Scholar · View at Scopus
  210. M. T. Maloney, L. S. Minamide, A. W. Kinley, J. A. Boyle, and J. R. Bamburg, “β-secretase-cleaved amyloid precursor protein accumulates at actin inclusions induced in neurons by stress or amyloid β: a feedforward mechanism for alzheimer's disease,” Journal of Neuroscience, vol. 25, no. 49, pp. 11313–11321, 2005. View at Publisher · View at Google Scholar · View at Scopus
  211. A. Mendoza-Naranjo, E. Contreras-Vallejos, D. R. Henriquez et al., “Fibrillar amyloid-β1-42 modifies actin organization affecting the cofilin phosphorylation state: a role for Rac1/cdc42 effector proteins and the slingshot phosphatase,” Journal of Alzheimer's Disease, vol. 29, no. 1, pp. 63–77, 2012. View at Publisher · View at Google Scholar · View at Scopus
  212. S. Simó and J. A. Cooper, “Regulation of dendritic branching by Cdc42 GAPs,” Genes and Development, vol. 26, no. 15, pp. 1653–1658, 2012. View at Publisher · View at Google Scholar · View at Scopus
  213. L. S. Minamide, A. M. Striegl, J. A. Boyle, P. J. Meberg, and J. R. Bamburg, “Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function,” Nature Cell Biology, vol. 2, no. 9, pp. 628–636, 2000. View at Publisher · View at Google Scholar · View at Scopus
  214. J. R. Bamburg, B. W. Bernstein, R. C. Davis et al., “ADF/Cofilin-actin rods in neurodegenerative diseases,” Current Alzheimer Research, vol. 7, no. 3, pp. 241–250, 2010. View at Publisher · View at Google Scholar · View at Scopus
  215. J. Cichon, C. Sun, B. Chen et al., “Cofilin aggregation blocks intracellular trafficking and induces synaptic loss in hippocampal neurons,” Journal of Biological Chemistry, vol. 287, no. 6, pp. 3919–3929, 2012. View at Publisher · View at Google Scholar · View at Scopus
  216. E. Nielsen, F. Severin, J. M. Backer, A. A. Hyman, and M. Zerial, “Rab5 regulates motility of early endosomes on microtubules,” Nature Cell Biology, vol. 1, no. 6, pp. 376–382, 1999. View at Publisher · View at Google Scholar · View at Scopus
  217. K. S. Shim and G. Lubec, “Drebrin, a dendritic spine protein, is manifold decreased in brains of patients with Alzheimer's disease and Down syndrome,” Neuroscience Letters, vol. 324, no. 3, pp. 209–212, 2002. View at Publisher · View at Google Scholar · View at Scopus
  218. E. Perez-Gracia, R. Blanco, M. Carmona, E. Carro, and I. Ferrer, “Oxidative stress damage and oxidative stress responses in the choroid plexus in Alzheimer's disease,” Acta Neuropathologica, vol. 118, no. 4, pp. 497–504, 2009. View at Publisher · View at Google Scholar · View at Scopus
  219. A. Güntert, J. Campbell, M. Saleem et al., “Plasma gelsolin is decreased and correlates with rate of decline in Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 21, no. 2, pp. 585–596, 2010. View at Publisher · View at Google Scholar · View at Scopus
  220. Y. Matsuoka, M. Saito, J. LaFrancois et al., “Novel therapeutic approach for the treatment of Alzheimer's disease by peripheral administration of agents with an affinity to beta-amyloid,” The Journal of Neuroscience, vol. 23, no. 1, pp. 29–33, 2003. View at Google Scholar · View at Scopus
  221. M. D. Ehlers, “Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting,” Neuron, vol. 28, no. 2, pp. 511–525, 2000. View at Publisher · View at Google Scholar · View at Scopus
  222. G. M. Shankar, B. L. Bloodgood, M. Townsend, D. M. Walsh, D. J. Selkoe, and B. L. Sabatini, “Natural oligomers of the Alzheimer amyloid-β protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway,” The Journal of Neuroscience, vol. 27, no. 11, pp. 2866–2875, 2007. View at Publisher · View at Google Scholar · View at Scopus
  223. M. Esteves da Silva, M. Adrian, P. Schätzle et al., “Positioning of AMPA receptor-containing endosomes regulates synapse architecture,” Cell Reports, vol. 13, no. 5, pp. 933–943, 2015. View at Publisher · View at Google Scholar
  224. G. Jung, E.-J. Kim, A. Cicvaric et al., “Drebrin depletion alters neurotransmitter receptor levels in protein complexes, dendritic spine morphogenesis and memory-related synaptic plasticity in the mouse hippocampus,” Journal of Neurochemistry, vol. 134, no. 2, pp. 327–339, 2015. View at Publisher · View at Google Scholar · View at Scopus
  225. H. Takahashi, T. Mizui, and T. Shirao, “Down-regulation of drebrin A expression suppresses synaptic targeting of NMDA receptors in developing hippocampal neurones,” Journal of neurochemistry, vol. 97, no. 1, pp. 110–115, 2006. View at Publisher · View at Google Scholar · View at Scopus
  226. P. G. Galloway, G. Perry, and P. Gambetti, “Hirano body filaments contain actin and actin-associated proteins,” Journal of Neuropathology and Experimental Neurology, vol. 46, no. 2, pp. 185–199, 1987. View at Publisher · View at Google Scholar · View at Scopus
  227. P. G. Galloway, P. Mulvihill, S. Siedlak et al., “Immunochemical demonstration of tropomyosin in the neurofibrillary pathology of Alzheimer's disease,” American Journal of Pathology, vol. 137, no. 2, pp. 291–300, 1990. View at Google Scholar · View at Scopus
  228. B. Pianu, R. Lefort, L. Thuiliere, E. Tabourier, and F. Bartolini, “The Aβ1-42 peptide regulates microtubule stability independently of tau,” Journal of Cell Science, vol. 127, no. 5, pp. 1117–1127, 2014. View at Publisher · View at Google Scholar · View at Scopus
  229. J. R. Stehn, N. K. Haass, T. Bonello et al., “A novel class of anticancer compounds targets the actin cytoskeleton in tumor cells,” Cancer Research, vol. 73, no. 16, pp. 5169–5182, 2013. View at Publisher · View at Google Scholar · View at Scopus