Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2016 (2016), Article ID 7969272, 19 pages
http://dx.doi.org/10.1155/2016/7969272
Review Article

Emerging Link between Alzheimer’s Disease and Homeostatic Synaptic Plasticity

1Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA
2Neuroscience Program, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA

Received 14 December 2015; Accepted 31 January 2016

Academic Editor: Victor Anggono

Copyright © 2016 Sung-Soo Jang and Hee Jung Chung. 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. D. O. Hebb, The Organization of Behavior: A Neuropsychological Theory, John Wiley & Sons, New York, NY, USA, 1949.
  2. T. V. P. Bliss and T. Lomo, “Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path,” The Journal of Physiology, vol. 232, no. 2, pp. 331–356, 1973. View at Publisher · View at Google Scholar · View at Scopus
  3. J. R. Whitlock, A. J. Heynen, M. G. Shuler, and M. F. Bear, “Learning induces long-term potentiation in the hippocampus,” Science, vol. 313, no. 5790, pp. 1093–1097, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. M. A. Lynch, “Long-term potentiation and memory,” Physiological Reviews, vol. 84, no. 1, pp. 87–136, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. 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
  6. G. Neves, S. F. Cooke, and T. V. P. Bliss, “Synaptic plasticity, memory and the hippocampus: a neural network approach to causality,” Nature Reviews Neuroscience, vol. 9, no. 1, pp. 65–75, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. D. E. Feldman, “Synaptic mechanisms for plasticity in neocortex,” Annual Review of Neuroscience, vol. 32, pp. 33–55, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. L. F. Abbott and S. B. Nelson, “Synaptic plasticity: taming the beast,” Nature Neuroscience, vol. 3, pp. 1178–1183, 2000. View at Publisher · View at Google Scholar
  9. G. G. Turrigiano and S. B. Nelson, “Hebb and homeostasis in neuronal plasticity,” Current Opinion in Neurobiology, vol. 10, no. 3, pp. 358–364, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. L. N. Cooper and M. F. Bear, “The BCM theory of synapse modification at 30: interaction of theory with experiment,” Nature Reviews Neuroscience, vol. 13, no. 11, pp. 798–810, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Marder and A. A. Prinz, “Current compensation in neuronal homeostasis,” Neuron, vol. 37, no. 1, pp. 2–4, 2003. View at Publisher · View at Google Scholar · View at Scopus
  12. G. W. Davis, “Homeostatic control of neural activity: from phenomenology to molecular design,” Annual Review of Neuroscience, vol. 29, pp. 307–323, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. G. G. Turrigiano, “The self-tuning neuron: synaptic scaling of excitatory synapses,” Cell, vol. 135, no. 3, pp. 422–435, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Pozo and Y. Goda, “Unraveling mechanisms of homeostatic synaptic plasticity,” Neuron, vol. 66, no. 3, pp. 337–351, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. G. Turrigiano, “Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function,” Cold Spring Harbor Perspectives in Biology, vol. 4, no. 1, Article ID a005736, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. G. McKhann, D. Drachman, and M. Folstein, “Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease,” Neurology, vol. 34, no. 7, pp. 939–944, 1984. View at Publisher · View at Google Scholar · View at Scopus
  17. P. F. Chapman, G. L. White, M. W. Jones et al., “Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice,” Nature Neuroscience, vol. 2, no. 3, pp. 271–276, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. S. M. Fitzjohn, R. A. Morton, F. Kuenzi et al., “Age-related impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein,” The Journal of Neuroscience, vol. 21, no. 13, pp. 4691–4698, 2001. View at Google Scholar · View at Scopus
  19. J. S. Jacobsen, C.-C. Wu, J. M. Redwine et al., “Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 13, pp. 5161–5166, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Y. Hsia, E. Masliah, L. McConlogue et al., “Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 6, pp. 3228–3233, 1999. View at Publisher · View at Google Scholar · View at Scopus
  21. J. J. Palop, J. Chin, E. D. Roberson et al., “Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease,” Neuron, vol. 55, no. 5, pp. 697–711, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Larson, G. Lynch, D. Games, and P. Seubert, “Alterations in synaptic transmission and long-term potentiation in hippocampal slices from young and aged PDAPP mice,” Brain Research, vol. 840, no. 1-2, pp. 23–35, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Roder, L. Danober, M. F. Pozza, K. Lingenhoehl, K.-H. Wiederhold, and H.-R. Olpe, “Electrophysiological studies on the hippocampus and prefrontal cortex assessing the effects of amyloidosis in amyloid precursor protein 23 transgenic mice,” Neuroscience, vol. 120, no. 3, pp. 705–720, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Dewachter, L. Ris, S. Croes et al., “Modulation of synaptic plasticity and Tau phosphorylation by wild-type and mutant presenilin1,” Neurobiology of Aging, vol. 29, no. 5, pp. 639–652, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. I. Gureviciene, S. Ikonen, K. Gurevicius et al., “Normal induction but accelerated decay of LTP in APP + PS1 transgenic mice,” Neurobiology of Disease, vol. 15, no. 2, pp. 188–195, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. F. Trinchese, S. Liu, F. Battaglia, S. Walter, P. M. Mathews, and O. Arancio, “Progressive age-related development of Alzheimer-like pathology in APP/PS1 mice,” Annals of Neurology, vol. 55, no. 6, pp. 801–814, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Megill, T. Tran, K. Eldred et al., “Defective age-dependent metaplasticity in a mouse model of Alzheimer's disease,” The Journal of Neuroscience, vol. 35, no. 32, pp. 11346–11357, 2015. View at Publisher · View at Google Scholar
  28. D. Puzzo, L. Privitera, E. Leznik et al., “Picomolar amyloid-β positively modulates synaptic plasticity and memory in hippocampus,” The Journal of Neuroscience, vol. 28, no. 53, pp. 14537–14545, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Puzzo, L. Privitera, and A. Palmeri, “Hormetic effect of amyloid-beta peptide in synaptic plasticity and memory,” Neurobiology of Aging, vol. 33, no. 7, pp. 1484–e24, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Hsieh, J. Boehm, C. Sato et al., “AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss,” Neuron, vol. 52, no. 5, pp. 831–843, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. 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
  32. 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
  33. 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
  34. G. M. Shankar and D. M. Walsh, “Alzheimer's disease: synaptic dysfunction and Aβ,” Molecular Neurodegeneration, vol. 4, article 48, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. M. S. Parihar and G. J. Brewer, “Amyloid-β as a modulator of synaptic plasticity,” Journal of Alzheimer's Disease, vol. 22, no. 3, pp. 741–763, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. I. Klyubin, W. K. Cullen, N.-W. Hu, and M. J. Rowan, “Alzheimer's disease Aβ assemblies mediating rapid disruption of synaptic plasticity and memory,” Molecular Brain, vol. 5, no. 1, article 25, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. C. F. Zorumski and Y. Izumi, “NMDA receptors and metaplasticity: mechanisms and possible roles in neuropsychiatric disorders,” Neuroscience and Biobehavioral Reviews, vol. 36, no. 3, pp. 989–1000, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. W. C. Abraham, “Metaplasticity: tuning synapses and networks for plasticity,” Nature Reviews Neuroscience, vol. 9, no. 5, pp. 387–399, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. J. J. Palop and L. Mucke, “Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks,” Nature Neuroscience, vol. 13, no. 7, pp. 812–818, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. J. J. Palop and L. Mucke, “Synaptic depression and aberrant excitatory network activity in Alzheimer's disease: two faces of the same coin?” NeuroMolecular Medicine, vol. 12, no. 1, pp. 48–55, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. M. A. Busche, X. Chen, H. A. Henning et al., “Critical role of soluble amyloid-β for early hippocampal hyperactivity in a mouse model of Alzheimer's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 22, pp. 8740–8745, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Lalonde, K.-I. Fukuchi, and C. Strazielle, “Neurologic and motor dysfunctions in APP transgenic mice,” Reviews in the Neurosciences, vol. 23, no. 4, pp. 363–379, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. J. L. Jankowsky, H. H. Slunt, V. Gonzales et al., “Persistent amyloidosis following suppression of Aβ production in a transgenic model of Alzheimer disease,” PLoS Medicine, vol. 2, no. 12, article e355, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. D. L. Vogt, D. Thomas, V. Galvan, D. E. Bredesen, B. T. Lamb, and S. W. Pimplikar, “Abnormal neuronal networks and seizure susceptibility in mice overexpressing the APP intracellular domain,” Neurobiology of Aging, vol. 32, no. 9, pp. 1725–1729, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. J. C. Amatniek, W. A. Hauser, C. DelCastillo-Castaneda et al., “Incidence and predictors of seizures in patients with Alzheimer's disease,” Epilepsia, vol. 47, no. 5, pp. 867–872, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. J. R. Cirrito, K. A. Yamada, M. B. Finn et al., “Synaptic activity regulates interstitial fluid amyloid-β levels in vivo,” Neuron, vol. 48, no. 6, pp. 913–922, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. J. R. Cirrito, J.-E. Kang, J. Lee et al., “Endocytosis is required for synaptic activity-dependent release of amyloid-β in vivo,” Neuron, vol. 58, no. 1, pp. 42–51, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. 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
  49. R. S. Wilson, E. Segawa, P. A. Boyle, S. E. Anagnos, L. P. Hizel, and D. A. Bennett, “The natural history of cognitive decline in Alzheimer's disease,” Psychology and Aging, vol. 27, no. 4, pp. 1008–1017, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Blennow, M. J. de Leon, and H. Zetterberg, “Alzheimer's disease,” The Lancet, vol. 368, no. 9533, pp. 387–403, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Hardy and D. J. Selkoe, “The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics,” Science, vol. 297, no. 5580, pp. 353–356, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. R. E. Tanzi and L. Bertram, “Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective,” Cell, vol. 120, no. 4, pp. 545–555, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. E. D. Roberson, K. Scearce-Levie, J. J. Palop et al., “Reducing endogenous tau ameliorates amyloid β-induced deficits in an Alzheimer's disease mouse model,” Science, vol. 316, no. 5825, pp. 750–754, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. E. D. Roberson, B. Halabisky, J. W. Yoo et al., “Amyloid-β/fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease,” The Journal of Neuroscience, vol. 31, no. 2, pp. 700–711, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. L. M. Ittner, Y. D. Ke, F. Delerue et al., “Dendritic function of tau mediates amyloid-β 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
  56. J. P. Cleary, D. M. Walsh, J. J. Hofmeister et al., “Natural oligomers of the amyloid-β protein specifically disrupt cognitive function,” Nature Neuroscience, vol. 8, no. 1, pp. 79–84, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Nitta, A. Itoh, T. Hasegawa, and T. Nabeshima, “β-amyloid protein-induced Alzheimer's disease animal model,” Neuroscience Letters, vol. 170, no. 1, pp. 63–66, 1994. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Maurice, B. P. Lockhart, and A. Privat, “Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction,” Brain Research, vol. 706, no. 2, pp. 181–193, 1996. View at Publisher · View at Google Scholar · View at Scopus
  59. Y.-F. Cheng, C. Wang, H.-B. Lin et al., “Inhibition of phosphodiesterase-4 reverses memory deficits produced by Aβ25-35 or Aβ1-40 peptide in rats,” Psychopharmacology, vol. 212, no. 2, pp. 181–191, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. S. J. Webster, A. D. Bachstetter, P. T. Nelson, F. A. Schmitt, and L. J. Van Eldik, “Using mice to model Alzheimer's dementia: an overview of the clinical disease and the preclinical behavioral changes in 10 mouse models,” Frontiers in Genetics, vol. 5, artcile 88, Article ID Article 88, 2014. View at Publisher · View at Google Scholar · View at Scopus
  61. D. Puzzo, L. Lee, A. Palmeri, G. Calabrese, and O. Arancio, “Behavioral assays with mouse models of Alzheimer's disease: practical considerations and guidelines,” Biochemical Pharmacology, vol. 88, no. 4, pp. 450–467, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. B. De Strooper, P. Saftig, K. Craessaerts et al., “Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein,” Nature, vol. 391, no. 6665, pp. 387–390, 1998. View at Publisher · View at Google Scholar · View at Scopus
  63. R. Vassar, B. D. Bennett, S. Babu-Khan et al., “β-Secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE,” Science, vol. 286, no. 5440, pp. 735–741, 1999. View at Publisher · View at Google Scholar · View at Scopus
  64. D. Edbauer, E. Winkler, J. T. Regula, B. Pesold, H. Steiner, and C. Haass, “Reconstitution of γ-secretase activity,” Nature Cell Biology, vol. 5, no. 5, pp. 486–488, 2003. View at Publisher · View at Google Scholar · View at Scopus
  65. B. Passer, L. Pellegrini, C. Russo et al., “Generation of an apoptotic intracellular peptide by α-secretase cleavage of Alzheimer's amyloid β protein precursor,” Journal of Alzheimer's Disease, vol. 2, no. 3-4, pp. 289–301, 2000. View at Google Scholar · View at Scopus
  66. E. H. Corder, A. M. Saunders, W. J. Strittmatter et al., “Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families,” Science, vol. 261, no. 5123, pp. 921–923, 1993. View at Publisher · View at Google Scholar · View at Scopus
  67. A. J. C. Slooter, M. Cruts, S. Kalmijn et al., “Risk estimates of dementia by apolipoprotein E genotypes from a population-based incidence study: the Rotterdam study,” Archives of Neurology, vol. 55, no. 7, pp. 964–968, 1998. View at Publisher · View at Google Scholar · View at Scopus
  68. J. M. Castellano, J. Kim, F. R. Stewart et al., “Human apoE isoforms differentially regulate brain amyloid-β peptide clearance,” Science Translational Medicine, vol. 3, no. 89, Article ID 89ra57, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. 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
  70. N. Bastrikova, G. A. Gardner, J. M. Reece, A. Jeromin, and S. M. Dudek, “Synapse elimination accompanies functional plasticity in hippocampal neurons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 8, pp. 3123–3127, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. R. Lamprecht and J. LeDoux, “Structural plasticity and memory,” Nature Reviews Neuroscience, vol. 5, no. 1, pp. 45–54, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. E. Masliah, M. Mallory, M. Alford et al., “Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease,” Neurology, vol. 56, no. 1, pp. 127–129, 2001. View at Publisher · View at Google Scholar · View at Scopus
  73. S. W. Scheff, D. A. Price, F. A. Schmitt, S. T. Dekosky, and E. J. Mufson, “Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment,” Neurology, vol. 68, no. 18, pp. 1501–1508, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. S. W. Scheff and D. A. Price, “Alzheimer's disease-related alterations in synaptic density: neocortex and hippocampus,” Journal of Alzheimer's Disease, vol. 9, supplement 3, pp. 101–115, 2006. View at Google Scholar · View at Scopus
  75. 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
  76. H. L. Tan, B. N. Queenan, and R. L. Huganir, “GRIP1 is required for homeostatic regulation of AMPAR trafficking,” Proceedings of the National Academy of Sciences, vol. 112, no. 32, pp. 10026–10031, 2015. View at Publisher · View at Google Scholar
  77. M. A. Gainey, V. Tatavarty, M. Nahmani, H. Lin, and G. G. Turrigiano, “Activity-dependent synaptic GRIP1 accumulation drives synaptic scaling up in response to action potential blockade,” Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 27, pp. E3590–E3599, 2015. View at Publisher · View at Google Scholar
  78. V. Anggono, R. L. Clem, and R. L. Huganir, “PICK1 loss of function occludes homeostatic synaptic scaling,” The Journal of Neuroscience, vol. 31, no. 6, pp. 2188–2196, 2011. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Alfonso, H. W. Kessels, C. C. Banos et al., “Synapto-depressive effects of amyloid beta require PICK1,” The European Journal of Neuroscience, vol. 39, no. 7, pp. 1225–1233, 2014. View at Publisher · View at Google Scholar · View at Scopus
  80. J. D. Shepherd, G. Rumbaugh, J. Wu et al., “Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors,” Neuron, vol. 52, no. 3, pp. 475–484, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. K. Lee, S. E. Royston, M. O. Vest et al., “N-methyl-D-aspartate receptors mediate activity-dependent down-regulation of potassium channel genes during the expression of homeostatic intrinsic plasticity,” Molecular Brain, vol. 8, article 4, 2015. View at Publisher · View at Google Scholar
  82. J. Wu, R. S. Petralia, H. Kurushima et al., “Arc/Arg3.1 regulates an endosomal pathway essential for activity-dependent beta-amyloid generation,” Cell, vol. 147, no. 3, pp. 615–628, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. J.-H. Hu, J. M. Park, S. Park et al., “Homeostatic scaling requires group I mGluR activation mediated by Homer1a,” Neuron, vol. 68, no. 6, pp. 1128–1142, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. Q. Sun and G. G. Turrigiano, “PSD-95 and PSD-93 play critical but distinct roles in synaptic scaling up and down,” The Journal of Neuroscience, vol. 31, no. 18, pp. 6800–6808, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. M. J. Kim, K. Futai, J. Jo, Y. Hayashi, K. Cho, and M. Sheng, “Synaptic accumulation of PSD-95 and synaptic function regulated by phosphorylation of serine-295 of PSD-95,” Neuron, vol. 56, no. 3, pp. 488–502, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. J. Noritake, Y. Fukata, T. Iwanaga et al., “Mobile DHHC palmitoylating enzyme mediates activity-sensitive synaptic targeting of PSD-95,” The Journal of Cell Biology, vol. 186, no. 1, pp. 147–160, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. A.-M. Simon, L. Schiapparelli, P. Salazar-Colocho et al., “Overexpression of wild-type human APP in mice causes cognitive deficits and pathological features unrelated to Aβ levels,” Neurobiology of Disease, vol. 33, no. 3, pp. 369–378, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. F. Roselli, M. Tirard, J. Lu et al., “Soluble β-amyloid1-40 induces NMDA-dependent degradation of postsynaptic density-95 at glutamatergic synapses,” The Journal of Neuroscience, vol. 25, no. 48, pp. 11061–11070, 2005. View at Publisher · View at Google Scholar · View at Scopus
  89. F. Roselli, P. Hutzler, Y. Wegerich, P. Livrea, and O. F. X. Almeida, “Disassembly of shank and homer synaptic clusters is driven by soluble beta-amyloid1–40 through divergent NMDAR-dependent signalling pathways,” PLoS ONE, vol. 4, no. 6, Article ID e6011, 2009. View at Publisher · View at Google Scholar · View at Scopus
  90. S. M. Shin, N. Zhang, J. Hansen et al., “GKAP orchestrates activity-dependent postsynaptic protein remodeling and homeostatic scaling,” Nature Neuroscience, vol. 15, no. 12, pp. 1655–1666, 2012. View at Publisher · View at Google Scholar · View at Scopus
  91. F. Roselli, P. Livrea, and O. F. X. Almeida, “CDK5 is essential for soluble amyloid β-induced degradation of GKAP and remodeling of the synaptic actin cytoskeleton,” PLoS ONE, vol. 6, no. 7, Article ID e23097, 2011. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Kim and E. B. Ziff, “Calcineurin mediates synaptic scaling via synaptic trafficking of Ca2+-permeable AMPA receptors,” PLoS Biology, vol. 12, no. 7, Article ID e1001900, pp. 1–15, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. M. D'Amelio, V. Cavallucci, S. Middei et al., “Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease,” Nature Neuroscience, vol. 14, no. 1, pp. 69–76, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. S. S. Jang, S. E. Royston, J. Xu et al., “Regulation of STEP61 and tyrosine-phosphorylation of NMDA and AMPA receptors during homeostatic synaptic plasticity,” Molecular Brain, vol. 8, no. 1, article 55, 2015. View at Publisher · View at Google Scholar
  95. Y. Zhang, D. V. Venkitaramani, C. M. Gladding et al., “The tyrosine phosphatase STEP mediates AMPA receptor endocytosis after metabotropic glutamate receptor stimulation,” The Journal of Neuroscience, vol. 28, no. 42, pp. 10561–10566, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. P. Kurup, Y. Zhang, J. Xu et al., “Aβ-mediated NMDA receptor endocytosis in alzheimer's disease involves ubiquitination of the tyrosine phosphatase STEP61,” The Journal of Neuroscience, vol. 30, no. 17, pp. 5948–5957, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. Y. Zhang, P. Kurup, J. Xu et al., “Genetic reduction of striatal-enriched tyrosine phosphatase (STEP) reverses cognitive and cellular deficits in an Alzheimer's disease mouse model,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 44, pp. 19014–19019, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. J. Xu, M. Chatterjee, T. D. Baguley et al., “Inhibitor of the tyrosine phosphatase STEP reverses cognitive deficits in a mouse model of Alzheimer's disease,” PLoS Biology, vol. 12, no. 8, Article ID e1001923, 2014. View at Publisher · View at Google Scholar
  99. B. A. Siddoway, H. F. Altimimi, H. Hou et al., “An essential role for inhibitor-2 regulation of protein phosphatase-1 in synaptic scaling,” The Journal of Neuroscience, vol. 33, no. 27, pp. 11206–11211, 2013. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Knobloch, M. Farinelli, U. Konietzko, R. M. Nitsch, and I. M. Mansuy, “Aβ oligomer-mediated long-term potentiation impairment involves protein phosphatase 1-dependent mechanisms,” The Journal of Neuroscience, vol. 27, no. 29, pp. 7648–7653, 2007. View at Publisher · View at Google Scholar · View at Scopus
  101. S. L. Scudder, M. S. Goo, A. E. Cartier et al., “Synaptic strength is bidirectionally controlled by opposing activity-dependent regulation of Nedd4-1 and USP8,” The Journal of Neuroscience, vol. 34, no. 50, pp. 16637–16649, 2014. View at Publisher · View at Google Scholar · View at Scopus
  102. Y.-D. Kwak, B. Wang, J. J. Li et al., “Upregulation of the E3 ligase NEDD4-1 by oxidative stress degrades IGF-1 receptor protein in neurodegeneration,” The Journal of Neuroscience, vol. 32, no. 32, pp. 10971–10981, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. T. J. Craig, N. Jaafari, M. M. Petrovic, P. P. Rubin, J. R. Mellor, and J. M. Henley, “Homeostatic synaptic scaling is regulated by protein SUMOylation,” The Journal of Biological Chemistry, vol. 287, no. 27, pp. 22781–22788, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. L. Lee, E. Dale, A. Staniszewski et al., “Regulation of synaptic plasticity and cognition by SUMO in normal physiology and Alzheimer's disease,” Scientific Reports, vol. 4, article 7190, 2014. View at Publisher · View at Google Scholar
  105. M. A. Sutton, A. M. Taylor, H. T. Ito, A. Pham, and E. M. Schuman, “Postsynaptic decoding of neural activity: eEF2 as a biochemical sensor coupling miniature synaptic transmission to local protein synthesis,” Neuron, vol. 55, no. 4, pp. 648–661, 2007. View at Publisher · View at Google Scholar · View at Scopus
  106. M. Letellier, S. Elramah, M. Mondin et al., “MiR-92a regulates expression of synaptic GluA1-containing AMPA receptors during homeostatic scaling,” Nature Neuroscience, vol. 17, no. 8, pp. 1040–1042, 2014. View at Publisher · View at Google Scholar · View at Scopus
  107. J. Aoto, C. I. Nam, M. M. Poon, P. Ting, and L. Chen, “Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity,” Neuron, vol. 60, no. 2, pp. 308–320, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. M. M. Poon and L. Chen, “Retinoic acid-gated sequence-specific translational control by RARα,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 51, pp. 20303–20308, 2008. View at Publisher · View at Google Scholar · View at Scopus
  109. B. Maghsoodi, M. M. Poon, C. I. Nam, J. Aoto, P. Ting, and L. Chen, “Retinoic acid regulates RARα-mediated control of translation in dendritic RNA granules during homeostatic synaptic plasticity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 41, pp. 16015–16020, 2008. View at Publisher · View at Google Scholar · View at Scopus
  110. D. K. Lahiri and C. Nall, “Promoter activity of the gene encoding the beta-amyloid precursor protein is up-regulated by growth factors, phorbol ester, retinoic acid and interleukin-1,” Molecular Brain Research, vol. 32, no. 2, pp. 233–240, 1995. View at Publisher · View at Google Scholar · View at Scopus
  111. Y. Yang, W. W. Quitschke, and G. J. Brewer, “Upregulation of amyloid precursor protein gene promoter in rat primary hippocampal neurons by phorbol ester, IL-1 and retinoic acid, but not by reactive oxygen species,” Molecular Brain Research, vol. 60, no. 1, pp. 40–49, 1998. View at Publisher · View at Google Scholar · View at Scopus
  112. J. G. Culvenor, G. Evin, M. A. Cooney et al., “Presenilin 2 expression in neuronal cells: induction during differentiation of embryonic carcinoma cells,” Experimental Cell Research, vol. 255, no. 2, pp. 192–206, 2000. View at Publisher · View at Google Scholar · View at Scopus
  113. J.-I. Satoh and Y. Kuroda, “Amyloid precursor protein β-secretase (BACE) mRNA expression in human neural cell lines following induction of neuronal differentiation and exposure to cytokines and growth factors,” Neuropathology, vol. 20, no. 4, pp. 289–296, 2000. View at Publisher · View at Google Scholar · View at Scopus
  114. Y. Ding, A. Qiao, Z. Wang et al., “Retinoic acid attenuates β-amyloid deposition and rescues memory deficits in an Alzheimer's disease transgenic mouse model,” The Journal of Neuroscience, vol. 28, no. 45, pp. 11622–11634, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. L. C. Rutherford, S. B. Nelson, and G. G. Turrigiano, “BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses,” Neuron, vol. 21, no. 3, pp. 521–530, 1998. View at Publisher · View at Google Scholar · View at Scopus
  116. H. S. Phillips, J. M. Hains, M. Armanini, G. R. Laramee, S. A. Johnson, and J. W. Winslow, “BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease,” Neuron, vol. 7, no. 5, pp. 695–702, 1991. View at Publisher · View at Google Scholar · View at Scopus
  117. B. Connor, D. Young, Q. Yan, R. L. M. Faull, B. Synek, and M. Dragunow, “Brain-derived neurotrophic factor is reduced in Alzheimer's disease,” Molecular Brain Research, vol. 49, no. 1-2, pp. 71–81, 1997. View at Publisher · View at Google Scholar · View at Scopus
  118. A. Alvarez, R. Cacabelos, C. Sanpedro, M. Garcia-Fantini, and M. Aleixandre, “Serum TNF-alpha levels are increased and correlate negatively with free IGF-I in Alzheimer disease,” Neurobiology of Aging, vol. 28, no. 4, pp. 533–536, 2007. View at Publisher · View at Google Scholar · View at Scopus
  119. J. S. Collins, R. T. Perry, B. Watson Jr. et al., “Association of a haplotype for tumor necrosis factor in siblings with late-onset Alzheimer disease: the NIMH Alzheimer disease genetics initiative,” American Journal of Medical Genetics, vol. 96, no. 6, pp. 823–830, 2000. View at Publisher · View at Google Scholar · View at Scopus
  120. H. Fillit, W. Ding, L. Buee et al., “Elevated circulating tumor necrosis factor levels in Alzheimer's disease,” Neuroscience Letters, vol. 129, no. 2, pp. 318–320, 1991. View at Publisher · View at Google Scholar · View at Scopus
  121. S. L. Ma, N. L. S. Tang, L. C. W. Lam, and H. F. K. Chiu, “Association between tumor necrosis factor-α promoter polymorphism and Alzheimer's disease,” Neurology, vol. 62, no. 2, pp. 307–309, 2004. View at Publisher · View at Google Scholar · View at Scopus
  122. R. Paganelli, A. Di Iorio, L. Patricelli et al., “Proinflammatory cytokines in sera of elderly patients with dementia: levels in vascular injury are higher than those of mild-moderate Alzheimer's disease patients,” Experimental Gerontology, vol. 37, no. 2-3, pp. 257–263, 2002. View at Publisher · View at Google Scholar · View at Scopus
  123. Z. S. Tan, A. S. Beiser, R. S. Vasan et al., “Inflammatory markers and the risk of Alzheimer disease: the Framingham study,” Neurology, vol. 68, no. 22, pp. 1902–1908, 2007. View at Publisher · View at Google Scholar · View at Scopus
  124. E. Tobinick, H. Gross, A. Weinberger, and H. Cohen, “TNF-alpha modulation for treatment of Alzheimer's disease: a 6-month pilot study,” MedGenMed—Medscape General Medicine, vol. 8, no. 2, article 25, 2006. View at Google Scholar · View at Scopus
  125. D. Stellwagen and R. C. Malenka, “Synaptic scaling mediated by glial TNF-α,” Nature, vol. 440, no. 7087, pp. 1054–1059, 2006. View at Publisher · View at Google Scholar · View at Scopus
  126. C. C. Steinmetz and G. G. Turrigiano, “Tumor necrosis factor-α signaling maintains the ability of cortical synapses to express synaptic scaling,” The Journal of Neuroscience, vol. 30, no. 44, pp. 14685–14690, 2010. View at Publisher · View at Google Scholar · View at Scopus
  127. M. Kaneko, D. Stellwagen, R. C. Malenka, and M. P. Stryker, “Tumor necrosis factor-α mediates one component of competitive, experience-dependent plasticity in developing visual cortex,” Neuron, vol. 58, no. 5, pp. 673–680, 2008. View at Publisher · View at Google Scholar · View at Scopus
  128. L. A. Cingolani, A. Thalhammer, L. M. Y. Yu et al., “Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins,” Neuron, vol. 58, no. 5, pp. 749–762, 2008. View at Publisher · View at Google Scholar · View at Scopus
  129. L. A. Cingolani and Y. Goda, “Differential involvement of β3 integrin in pre- and postsynaptic forms of adaptation to chronic activity deprivation,” Neuron Glia Biology, vol. 4, no. 3, pp. 179–187, 2008. View at Publisher · View at Google Scholar · View at Scopus
  130. C. A. Goddard, D. A. Butts, and C. J. Shatz, “Regulation of CNS synapses by neuronal MHC class I,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 16, pp. 6828–6833, 2007. View at Publisher · View at Google Scholar · View at Scopus
  131. K. Uemura, C. M. Lill, M. Banks et al., “N-cadherin-based adhesion enhances Aβ release and decreases Aβ42/40 ratio,” Journal of Neurochemistry, vol. 108, no. 2, pp. 350–360, 2009. View at Publisher · View at Google Scholar · View at Scopus
  132. M. Asada-Utsugi, K. Uemura, Y. Noda et al., “N-cadherin enhances APP dimerization at the extracellular domain and modulates Aβ production,” Journal of Neurochemistry, vol. 119, no. 2, pp. 354–363, 2011. View at Publisher · View at Google Scholar · View at Scopus
  133. T. Okuda, L. M. Y. Yu, L. A. Cingolani, R. Kemler, and Y. Goda, “β-catenin regulates excitatory postsynaptic strength at hippocampal synapses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 33, pp. 13479–13484, 2007. View at Publisher · View at Google Scholar · View at Scopus
  134. N. Vitureira, M. Letellier, I. J. White, and Y. Goda, “Differential control of presynaptic efficacy by postsynaptic N-cadherin and β-catenin,” Nature Neuroscience, vol. 15, no. 1, pp. 81–89, 2012. View at Publisher · View at Google Scholar · View at Scopus
  135. A. Andreyeva, K. Nieweg, K. Horstmann et al., “C-terminal fragment of N-cadherin accelerates synapse destabilization by amyloid-β,” Brain, vol. 135, no. 7, pp. 2140–2154, 2012. View at Publisher · View at Google Scholar · View at Scopus
  136. A. K. Y. Fu, K.-W. Hung, W.-Y. Fu et al., “APC(Cdh1) mediates EphA4-dependent downregulation of AMPA receptors in homeostatic plasticity,” Nature Neuroscience, vol. 14, no. 2, pp. 181–191, 2011. View at Publisher · View at Google Scholar · View at Scopus
  137. A. K. Y. Fu, K.-W. Hung, H. Huang et al., “Blockade of EphA4 signaling ameliorates hippocampal synaptic dysfunctions in mouse models of Alzheimer's disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 27, pp. 9959–9964, 2014. View at Publisher · View at Google Scholar · View at Scopus
  138. K. Ibata, Q. Sun, and G. G. Turrigiano, “Rapid synaptic scaling induced by changes in postsynaptic firing,” Neuron, vol. 57, no. 6, pp. 819–826, 2008. View at Publisher · View at Google Scholar · View at Scopus
  139. C. P. Goold and R. A. Nicoll, “Single-cell optogenetic excitation drives homeostatic synaptic depression,” Neuron, vol. 68, no. 3, pp. 512–528, 2010. View at Publisher · View at Google Scholar · View at Scopus
  140. M. A. Gainey, J. R. Hurvitz-Wolff, M. E. Lambo, and G. G. Turrigiano, “Synaptic scaling requires the GluR2 subunit of the AMPA receptor,” The Journal of Neuroscience, vol. 29, no. 20, pp. 6479–6489, 2009. View at Publisher · View at Google Scholar · View at Scopus
  141. S. A. L. Corrêa, C. J. Hunter, O. Palygin et al., “MSK1 regulates homeostatic and experience-dependent synaptic plasticity,” The Journal of Neuroscience, vol. 32, no. 38, pp. 13039–13051, 2012. View at Publisher · View at Google Scholar · View at Scopus
  142. K. M. Webber, M. A. Smith, H.-G. Lee et al., “Mitogen- and stress-activated protein kinase 1: convergence of the ERK and p38 pathways in Alzheimer's disease,” Journal of Neuroscience Research, vol. 79, no. 4, pp. 554–560, 2005. View at Publisher · View at Google Scholar · View at Scopus
  143. M. P. Blackman, B. Djukic, S. B. Nelson, and G. G. Turrigiano, “A critical and cell-autonomous role for MeCP2 in synaptic scaling up,” The Journal of Neuroscience, vol. 32, no. 39, pp. 13529–13536, 2012. View at Publisher · View at Google Scholar · View at Scopus
  144. D. P. Seeburg, M. Feliu-Mojer, J. Gaiottino, D. T. S. Pak, and M. Sheng, “Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity,” Neuron, vol. 58, no. 4, pp. 571–583, 2008. View at Publisher · View at Google Scholar · View at Scopus
  145. D. P. Seeburg and M. Sheng, “Activity-induced polo-like kinase 2 is required for homeostatic plasticity of hippocampal neurons during epileptiform activity,” The Journal of Neuroscience, vol. 28, no. 26, pp. 6583–6591, 2008. View at Publisher · View at Google Scholar · View at Scopus
  146. A. Wilkaniec, G. A. Czapski, and A. Adamczyk, “Cdk5 at crossroads of protein oligomerization in neurodegenerative diseases: facts and hypotheses,” Journal of Neurochemistry, vol. 136, no. 2, pp. 222–233, 2016. View at Publisher · View at Google Scholar
  147. M. Marchetti and H. Marie, “Hippocampal synaptic plasticity in Alzheimer's disease: what have we learned so far from transgenic models?” Reviews in the Neurosciences, vol. 22, no. 4, pp. 373–402, 2011. View at Publisher · View at Google Scholar · View at Scopus
  148. E. L. Bienenstock, L. N. Cooper, and P. W. Munro, “Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex,” The Journal of Neuroscience, vol. 2, no. 1, pp. 32–48, 1982. View at Google Scholar · View at Scopus
  149. M. F. Bear, “Mechanism for a sliding synaptic modification threshold,” Neuron, vol. 15, no. 1, pp. 1–4, 1995. View at Publisher · View at Google Scholar · View at Scopus
  150. R. A. Sperling, B. C. Dickerson, M. Pihlajamaki et al., “Functional alterations in memory networks in early Alzheimer's disease,” NeuroMolecular Medicine, vol. 12, no. 1, pp. 27–43, 2010. View at Publisher · View at Google Scholar · View at Scopus
  151. M. A. Busche, G. Eichhoff, H. Adelsberger et al., “Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease,” Science, vol. 321, no. 5896, pp. 1686–1689, 2008. View at Publisher · View at Google Scholar · View at Scopus
  152. A. J. Larner and M. Doran, “Reply to Dr Raux et al.: molecular diagnosis of autosomal dominant early onset Alzheimer's disease: an update (J Med Genet 2005;42:793–5),” Journal of Medical Genetics, vol. 43, no. 8, article e44, 2006. View at Publisher · View at Google Scholar
  153. S. Jayadev, J. B. Leverenz, E. Steinbart et al., “Alzheimer's disease phenotypes and genotypes associated with mutations in presenilin 2,” Brain, vol. 133, no. 4, pp. 1143–1154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  154. C. J. Westmark, P. R. Westmark, A. M. Beard, S. M. Hildebrandt, and J. S. Malter, “Seizure susceptibility and mortality in mice that over-express amyloid precursor protein,” International Journal of Clinical and Experimental Pathology, vol. 1, no. 2, pp. 157–168, 2008. View at Google Scholar
  155. R. Lalonde, M. Dumont, M. Staufenbiel, and C. Strazielle, “Neurobehavioral characterization of APP23 transgenic mice with the SHIRPA primary screen,” Behavioural Brain Research, vol. 157, no. 1, pp. 91–98, 2005. View at Publisher · View at Google Scholar · View at Scopus
  156. P. E. Sanchez, L. Zhu, L. Verret et al., “Levetiracetam suppresses neuronal network dysfunction and reverses synaptic and cognitive deficits in an Alzheimer's disease model,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 42, pp. E2895–E2903, 2012. View at Publisher · View at Google Scholar · View at Scopus
  157. L. Verret, E. O. Mann, G. B. Hang et al., “Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model,” Cell, vol. 149, no. 3, pp. 708–721, 2012. View at Publisher · View at Google Scholar · View at Scopus
  158. B. F. Corbett, S. C. Leiser, H.-P. Ling et al., “Sodium channel cleavage is associated with aberrant neuronal activity and cognitive deficits in a mouse model of Alzheimer's disease,” The Journal of Neuroscience, vol. 33, no. 16, pp. 7020–7026, 2013. View at Publisher · View at Google Scholar · View at Scopus
  159. R. Minkeviciene, S. Rheims, M. B. Dobszay et al., “Amyloid β-induced neuronal hyperexcitability triggers progressive epilepsy,” The Journal of Neuroscience, vol. 29, no. 11, pp. 3453–3462, 2009. View at Publisher · View at Google Scholar · View at Scopus
  160. S. Ziyatdinova, K. Gurevicius, N. Kutchiashvili et al., “Spontaneous epileptiform discharges in a mouse model of Alzheimer's disease are suppressed by antiepileptic drugs that block sodium channels,” Epilepsy Research, vol. 94, no. 1-2, pp. 75–85, 2011. View at Publisher · View at Google Scholar · View at Scopus
  161. S. Li, M. Jin, T. Koeglsperger, N. E. Shepardson, G. M. Shankar, and D. J. Selkoe, “Soluble Aβ oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors,” The Journal of Neuroscience, vol. 31, no. 18, pp. 6627–6638, 2011. View at Publisher · View at Google Scholar · View at Scopus
  162. N.-W. Hu, I. Klyubin, R. Anwy, and M. J. Rowan, “GluN2B subunit-containing NMDA receptor antagonists prevent Aβ-mediated synaptic plasticity disruption in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 48, pp. 20504–20509, 2009. View at Publisher · View at Google Scholar · View at Scopus
  163. 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
  164. Q. Yang, Z.-H. Liao, Y.-X. Xiao, Q.-S. Lin, Y.-S. Zhu, and S.-T. Li, “Hippocampal synaptic metaplasticity requires the activation of NR2B-containing NMDA receptors,” Brain Research Bulletin, vol. 84, no. 2, pp. 137–143, 2011. View at Publisher · View at Google Scholar · View at Scopus
  165. T. Frankiewicz and C. G. Parsons, “Memantine restores long term potentiation impaired by tonic N-methyl-d-aspartate (NMDA) receptor activation following reduction of Mg2+ In hippocampal slices,” Neuropharmacology, vol. 38, no. 9, pp. 1253–1259, 1999. View at Publisher · View at Google Scholar · View at Scopus
  166. W. Zajaczkowski, T. Frankiewicz, C. G. Parsons, and W. Danysz, “Uncompetitive NMDA receptor antagoists attenuate NMDA-induced impairment of passive avoidance learning and LTP,” Neuropharmacology, vol. 36, no. 7, pp. 961–971, 1997. View at Publisher · View at Google Scholar · View at Scopus
  167. J. L. Jankowsky, H. H. Slunt, T. Ratovitski, N. A. Jenkins, N. G. Copeland, and D. R. Borchelt, “Co-expression of multiple transgenes in mouse CNS: a comparison of strategies,” Biomolecular Engineering, vol. 17, no. 6, pp. 157–165, 2001. View at Publisher · View at Google Scholar · View at Scopus
  168. J. L. Jankowsky, D. J. Fadale, J. Anderson et al., “Mutant presenilins specifically elevate the levels of the 42 residue β-amyloid peptide in vivo: evidence for augmentation of a 42-specific γ secretase,” Human Molecular Genetics, vol. 13, no. 2, pp. 159–170, 2004. View at Publisher · View at Google Scholar · View at Scopus
  169. A. Savonenko, G. M. Xu, T. Melnikova et al., “Episodic-like memory deficits in the APPswe/PS1dE9 mouse model of Alzheimer's disease: relationships to beta-amyloid deposition and neurotransmitter abnormalities,” Neurobiology of Disease, vol. 18, no. 3, pp. 602–617, 2005. View at Google Scholar
  170. A. Volianskis, R. Køstner, M. Mølgaard, S. Hass, and M. S. Jensen, “Episodic memory deficits are not related to altered glutamatergic synaptic transmission and plasticity in the CA1 hippocampus of the APPswe/PS1ΔE9-deleted transgenic mice model of β-amyloidosis,” Neurobiology of Aging, vol. 31, no. 7, pp. 1173–1187, 2010. View at Publisher · View at Google Scholar · View at Scopus
  171. E. M. Quinlan, D. H. Olstein, and M. F. Bear, “Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 22, pp. 12876–12880, 1999. View at Publisher · View at Google Scholar · View at Scopus
  172. E. M. Quinlan, D. Lebel, I. Brosh, and E. Barkai, “A molecular mechanism for stabilization of learning-induced synaptic modifications,” Neuron, vol. 41, no. 2, pp. 185–192, 2004. View at Publisher · View at Google Scholar · View at Scopus
  173. B. D. Philpot, A. K. Sekhar, H. Z. Shouval, and M. F. Bear, “Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptors in visual cortex,” Neuron, vol. 29, no. 1, pp. 157–169, 2001. View at Publisher · View at Google Scholar · View at Scopus
  174. B. D. Philpot, J. S. Espinosa, and M. F. Bear, “Evidence for altered NMDA receptor function as a basis for metaplasticity in visual cortex,” The Journal of Neuroscience, vol. 23, no. 13, pp. 5583–5588, 2003. View at Google Scholar · View at Scopus
  175. A. Citri and R. C. Malenka, “Synaptic plasticity: multiple forms, functions, and mechanisms,” Neuropsychopharmacology, vol. 33, no. 1, pp. 18–41, 2008. View at Publisher · View at Google Scholar · View at Scopus
  176. O. A. Shipton and O. Paulsen, “GluN2A and GluN2B subunit-containing NMDA receptors in hippocampal plasticity,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 369, no. 1633, Article ID 20130163, 2014. View at Publisher · View at Google Scholar · View at Scopus
  177. C. G. Lau and R. S. Zukin, “NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders,” Nature Reviews Neuroscience, vol. 8, no. 6, pp. 413–426, 2007. View at Publisher · View at Google Scholar · View at Scopus
  178. A. Barria and R. Malinow, “NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII,” Neuron, vol. 48, no. 2, pp. 289–301, 2005. View at Publisher · View at Google Scholar · View at Scopus
  179. E. M. Quinlan, B. D. Philpot, R. L. Huganir, and M. F. Bear, “Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo,” Nature Neuroscience, vol. 2, no. 4, pp. 352–357, 1999. View at Publisher · View at Google Scholar · View at Scopus
  180. M. Matos, E. Augusto, C. R. Oliveira, and P. Agostinho, “Amyloid-beta peptide decreases glutamate uptake in cultured astrocytes: involvement of oxidative stress and mitogen-activated protein kinase cascades,” Neuroscience, vol. 156, no. 4, pp. 898–910, 2008. View at Publisher · View at Google Scholar · View at Scopus
  181. S. Huang, M. Trevino, K. He et al., “Pull-push neuromodulation of LTP and LTD enables bidirectional experience-induced synaptic scaling in visual cortex,” Neuron, vol. 73, no. 3, pp. 497–510, 2012. View at Publisher · View at Google Scholar · View at Scopus
  182. V. Anggono and R. L. Huganir, “Regulation of AMPA receptor trafficking and synaptic plasticity,” Current Opinion in Neurobiology, vol. 22, no. 3, pp. 461–469, 2012. View at Publisher · View at Google Scholar · View at Scopus
  183. H.-K. Lee, K. Takamiya, J.-S. Han et al., “Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory,” Cell, vol. 112, no. 5, pp. 631–643, 2003. View at Publisher · View at Google Scholar · View at Scopus
  184. H.-K. Lee, M. Barbarosie, K. Kameyama, M. F. Bear, and R. L. Huganir, “Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity,” Nature, vol. 405, no. 6789, pp. 955–959, 2000. View at Publisher · View at Google Scholar · View at Scopus
  185. H.-K. Lee, K. Takamiya, K. He, L. Song, and R. L. Huganir, “Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus,” Journal of Neurophysiology, vol. 103, no. 1, pp. 479–489, 2010. View at Publisher · View at Google Scholar · View at Scopus
  186. J. A. Esteban, S.-H. Shi, C. Wilson, M. Nuriya, R. L. Huganir, and R. Malinow, “PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity,” Nature Neuroscience, vol. 6, no. 2, pp. 136–143, 2003. View at Publisher · View at Google Scholar · View at Scopus
  187. H.-Y. Man, Y. Sekine-Aizawa, and R. L. Huganir, “Regulation of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 9, pp. 3579–3584, 2007. View at Publisher · View at Google Scholar · View at Scopus
  188. D. Holman, M. Feligioni, and J. M. Henley, “Differential redistribution of native AMPA receptor complexes following LTD induction in acute hippocampal slices,” Neuropharmacology, vol. 52, no. 1, pp. 92–99, 2007. View at Publisher · View at Google Scholar · View at Scopus
  189. A. Goel, L. W. Xu, K. P. Snyder et al., “Phosphorylation of AMPA receptors is required for sensory deprivation-induced homeostatic synaptic plasticity,” PLoS ONE, vol. 6, no. 3, Article ID e18264, 2011. View at Publisher · View at Google Scholar · View at Scopus
  190. K. He, L. Song, L. W. Cummings, J. Goldman, R. L. Huganir, and H.-K. Lee, “Stabilization of Ca2+-permeable AMPA receptors at perisynaptic sites by GluR1-S845 phosphorylation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 47, pp. 20033–20038, 2009. View at Publisher · View at Google Scholar · View at Scopus
  191. K. W. Roche, R. J. O'Brien, A. L. Mammen, J. Bernhardt, and R. L. Huganir, “Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit,” Neuron, vol. 16, no. 6, pp. 1179–1188, 1996. View at Publisher · View at Google Scholar · View at Scopus
  192. A. Barria, V. Derkach, and T. Soderling, “Identification of the Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the α-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate-type glutamate receptor,” The Journal of Biological Chemistry, vol. 272, no. 52, pp. 32727–32730, 1997. View at Publisher · View at Google Scholar
  193. A. L. Mammen, K. Kameyama, K. W. Roche, and R. L. Huganir, “Phosphorylation of the alpha-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II,” The Journal of Biological Chemistry, vol. 272, no. 51, pp. 32528–32533, 1997. View at Publisher · View at Google Scholar
  194. A. Barria, D. Muller, V. Derkach, L. C. Griffith, and T. R. Soderling, “Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation,” Science, vol. 276, no. 5321, pp. 2042–2045, 1997. View at Publisher · View at Google Scholar · View at Scopus
  195. X.-D. Hu, Q. Huang, X. Yang, and H. Xia, “Differential regulation of AMPA receptor trafficking by neurabin-targeted synaptic protein phosphatase-1 in synaptic transmission and long-term depression in hippocampus,” The Journal of Neuroscience, vol. 27, no. 17, pp. 4674–4686, 2007. View at Publisher · View at Google Scholar · View at Scopus
  196. Y. Makino, R. C. Johnson, Y. Yu, K. Takamiya, and R. L. Huganir, “Enhanced synaptic plasticity in mice with phosphomimetic mutation of the GluA1 AMPA receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 20, pp. 8450–8455, 2011. View at Publisher · View at Google Scholar · View at Scopus
  197. M.-C. Lee, R. Yasuda, and M. D. Ehlers, “Metaplasticity at single glutamatergic synapses,” Neuron, vol. 66, no. 6, pp. 859–870, 2010. View at Publisher · View at Google Scholar · View at Scopus
  198. B. D. Philpot and R. S. Zukin, “Synapse-specific metaplasticity: to be silenced is not to silence 2B,” Neuron, vol. 66, no. 6, pp. 814–816, 2010. View at Publisher · View at Google Scholar · View at Scopus
  199. G. G. Turrigiano, K. R. Leslie, N. S. Desai, L. C. Rutherford, and S. B. Nelson, “Activity-dependent scaling of quantal amplitude in neocortical neurons,” Nature, vol. 391, no. 6670, pp. 892–896, 1998. View at Publisher · View at Google Scholar · View at Scopus
  200. A. J. Watt, M. C. W. Van Rossum, K. M. MacLeod, S. B. Nelson, and G. G. Turrigiano, “Activity coregulates quantal AMPA and NMDA currents at neocortical synapses,” Neuron, vol. 26, no. 3, pp. 659–670, 2000. View at Publisher · View at Google Scholar · View at Scopus
  201. T. C. Thiagarajan, M. Lindskog, and R. W. Tsien, “Adaptation to synaptic inactivity in hippocampal neurons,” Neuron, vol. 47, no. 5, pp. 725–737, 2005. View at Publisher · View at Google Scholar · View at Scopus
  202. D. V. Lissin, S. N. Gomperts, R. C. Carroll et al., “Activity differentially regulates the surface expression of synaptic AMPA and NMDA glutamate receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 12, pp. 7097–7102, 1998. View at Publisher · View at Google Scholar · View at Scopus
  203. Z. Qiu, E. L. Sylwestrak, D. N. Lieberman, Y. Zhang, X.-Y. Liu, and A. Ghosh, “The Rett syndrome protein MeCP2 regulates synaptic scaling,” The Journal of Neuroscience, vol. 32, no. 3, pp. 989–994, 2012. View at Publisher · View at Google Scholar · View at Scopus
  204. H. Dong, P. Zhang, I. Song, R. S. Petralia, D. Liao, and R. L. Huganir, “Characterization of the glutamate receptor-interacting proteins GRIP1 and GRIP2,” The Journal of Neuroscience, vol. 19, no. 16, pp. 6930–6941, 1999. View at Google Scholar · View at Scopus
  205. J. Xia, X. Zhang, J. Staudinger, and R. L. Huganir, “Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1,” Neuron, vol. 22, no. 1, pp. 179–187, 1999. View at Publisher · View at Google Scholar
  206. H. J. Chung, J. Xia, R. H. Scannevin, X. Zhang, and R. L. Huganir, “Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins,” The Journal of Neuroscience, vol. 20, no. 19, pp. 7258–7267, 2000. View at Google Scholar · View at Scopus
  207. J. L. Perez, L. Khatri, C. Chang, S. Srivastava, P. Osten, and E. B. Ziff, “PICK1 targets activated protein kinase Cα to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2,” The Journal of Neuroscience, vol. 21, no. 15, pp. 5417–5428, 2001. View at Google Scholar · View at Scopus
  208. A. Terashima, L. Cotton, K. K. Dev et al., “Regulation of synaptic strength and AMPA receptor subunit composition by PICK1,” The Journal of Neuroscience, vol. 24, no. 23, pp. 5381–5390, 2004. View at Publisher · View at Google Scholar · View at Scopus
  209. D.-T. Lin and R. L. Huganir, “PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptor-induced internalization,” The Journal of Neuroscience, vol. 27, no. 50, pp. 13903–13908, 2007. View at Publisher · View at Google Scholar · View at Scopus
  210. E. Kim and M. Sheng, “PDZ domain proteins of synapses,” Nature Reviews Neuroscience, vol. 5, no. 10, pp. 771–781, 2004. View at Publisher · View at Google Scholar · View at Scopus
  211. L. Chen, D. M. Chetkovich, R. S. Petralia et al., “Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms,” Nature, vol. 408, no. 6815, pp. 936–943, 2000. View at Publisher · View at Google Scholar · View at Scopus
  212. R. A. Nicoll, S. Tomita, and D. S. Bredt, “Auxiliary subunits assist AMPA-type glutamate receptors,” Science, vol. 311, no. 5765, pp. 1253–1256, 2006. View at Publisher · View at Google Scholar · View at Scopus
  213. Y.-H. Jiang and M. D. Ehlers, “Modeling autism by SHANK gene mutations in mice,” Neuron, vol. 78, no. 1, pp. 8–27, 2013. View at Publisher · View at Google Scholar · View at Scopus
  214. E. Kim, S. Naisbitt, Y.-P. Hsueh et al., “GKAP, a novel synaptic protein that interacts with the guanylate kinase- like domain of the PSD-95/SAP90 family of channel clustering molecules,” The Journal of Cell Biology, vol. 136, no. 3, pp. 669–678, 1997. View at Publisher · View at Google Scholar · View at Scopus
  215. S. Naisbitt, E. Kim, J. C. Tu et al., “Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin,” Neuron, vol. 23, no. 3, pp. 569–582, 1999. View at Publisher · View at Google Scholar · View at Scopus
  216. J. F. Guzowski, J. A. Timlin, B. Roysam, B. L. McNaughton, P. F. Worley, and C. A. Barnes, “Mapping behaviorally relevant neural circuits with immediate-early gene expression,” Current Opinion in Neurobiology, vol. 15, no. 5, pp. 599–606, 2005. View at Publisher · View at Google Scholar · View at Scopus
  217. O. Steward, C. S. Wallace, G. L. Lyford, and P. F. Worley, “Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites,” Neuron, vol. 21, no. 4, pp. 741–751, 1998. View at Publisher · View at Google Scholar · View at Scopus
  218. S. Chowdhury, J. D. Shepherd, H. Okuno et al., “Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking,” Neuron, vol. 52, no. 3, pp. 445–459, 2006. View at Publisher · View at Google Scholar · View at Scopus
  219. S. Park, J. M. Park, S. Kim et al., “Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD,” Neuron, vol. 59, no. 1, pp. 70–83, 2008. View at Publisher · View at Google Scholar · View at Scopus
  220. P. R. Brakeman, A. A. Lanahan, R. O'Brien et al., “Homer: a protein that selectively binds metabotropic glutamate receptors,” Nature, vol. 386, no. 6622, pp. 284–288, 1997. View at Publisher · View at Google Scholar · View at Scopus
  221. F. Ango, L. Prézeau, T. Muller et al., “Agonist-independent activation of metabotropic glutamate receptors by the intracellular protein Homer,” Nature, vol. 411, no. 6840, pp. 962–965, 2001. View at Publisher · View at Google Scholar · View at Scopus
  222. T. Hayashi and R. L. Huganir, “Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases,” The Journal of Neuroscience, vol. 24, no. 27, pp. 6152–6160, 2004. View at Publisher · View at Google Scholar · View at Scopus
  223. G. Ahmadian, W. Ju, L. Liu et al., “Tyrosine phosphorylation of GluR2 is required for insulin-stimulated AMPA receptor endocytosis and LTD,” The EMBO Journal, vol. 23, no. 5, pp. 1040–1050, 2004. View at Publisher · View at Google Scholar · View at Scopus
  224. K. A. Pelkey, R. Askalan, S. Paul et al., “Tyrosine phosphatase STEP is a tonic brake on induction of long-term potentiation,” Neuron, vol. 34, no. 1, pp. 127–138, 2002. View at Publisher · View at Google Scholar · View at Scopus
  225. R. M. Mulkey, S. Endo, S. Shenolikar, and R. C. Malenka, “Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression,” Nature, vol. 369, no. 6480, pp. 486–488, 1994. View at Publisher · View at Google Scholar · View at Scopus
  226. W. Morishita, J. H. Connor, H. Xia, E. M. Quinlan, S. Shenolikar, and R. C. Malenka, “Regulation of synaptic strength by protein phosphatase 1,” Neuron, vol. 32, no. 6, pp. 1133–1148, 2001. View at Publisher · View at Google Scholar · View at Scopus
  227. G. M. Thomas and R. L. Huganir, “Palmitoylation-dependent regulation of glutamate receptors and their PDZ domain-containing partners,” Biochemical Society Transactions, vol. 41, no. 1, pp. 72–78, 2013. View at Publisher · View at Google Scholar · View at Scopus
  228. G. Yang, W. Xiong, L. Kojic, and M. S. Cynader, “Subunit-selective palmitoylation regulates the intracellular trafficking of AMPA receptor,” The European Journal of Neuroscience, vol. 30, no. 1, pp. 35–46, 2009. View at Publisher · View at Google Scholar
  229. T. Hayashi, G. Rumbaugh, and R. L. Huganir, “Differential regulation of AMPA receptor subunit trafficking by palmitoylation of two distinct sites,” Neuron, vol. 47, no. 5, pp. 709–723, 2005. View at Publisher · View at Google Scholar · View at Scopus
  230. D.-T. Lin, Y. Makino, K. Sharma et al., “Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation,” Nature Neuroscience, vol. 12, no. 7, pp. 879–887, 2009. View at Publisher · View at Google Scholar · View at Scopus
  231. J. B. Hoppe, C. G. Salbego, and H. Cimarosti, “SUMOylation: novel neuroprotective approach for Alzheimer's disease?” Aging and Disease, vol. 6, no. 5, pp. 322–330, 2015. View at Publisher · View at Google Scholar
  232. S. Martin, A. Nishimune, J. R. Mellor, and J. M. Henley, “SUMOylation regulates kainate-receptor-mediated synaptic transmission,” Nature, vol. 447, no. 7142, pp. 321–325, 2007. View at Publisher · View at Google Scholar · View at Scopus
  233. L. A. Schwarz, B. J. Hall, and G. N. Patrick, “Activity-dependent ubiquitination of GluA1 mediates a distinct AMPA receptor endocytosis and sorting pathway,” The Journal of Neuroscience, vol. 30, no. 49, pp. 16718–16729, 2010. View at Publisher · View at Google Scholar · View at Scopus
  234. A. Lin, Q. Hou, L. Jarzylo et al., “Nedd4-mediated AMPA receptor ubiquitination regulates receptor turnover and trafficking,” Journal of Neurochemistry, vol. 119, no. 1, pp. 27–39, 2011. View at Publisher · View at Google Scholar · View at Scopus
  235. M. P. Lussier, Y. Nasu-Nishimura, and K. W. Roche, “Activity-dependent ubiquitination of the AMPA receptor subunit GluA2,” The Journal of Neuroscience, vol. 31, no. 8, pp. 3077–3081, 2011. View at Publisher · View at Google Scholar · View at Scopus
  236. J. P. Meadows, M. C. Guzman-Karlsson, S. Phillips et al., “DNA methylation regulates neuronal glutamatergic synaptic scaling,” Science Signaling, vol. 8, no. 382, p. ra61, 2015. View at Publisher · View at Google Scholar
  237. A. Balkowiec and D. M. Katz, “Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons,” The Journal of Neuroscience, vol. 22, no. 23, pp. 10399–10407, 2002. View at Google Scholar · View at Scopus
  238. J. Budni, T. Bellettini-Santos, F. Mina, M. Lima Garcez, and A. Ioppi Zugno, “The involvement of BDNF, NGF and GDNF in aging and Alzheimer's disease,” Aging and Disease, vol. 6, no. 5, pp. 331–341, 2015. View at Publisher · View at Google Scholar
  239. G. Leal, P. M. Afonso, I. L. Salazar, and C. B. Duarte, “Regulation of hippocampal synaptic plasticity by BDNF,” Brain Research, vol. 1621, pp. 82–101, 2015. View at Publisher · View at Google Scholar
  240. S. Peng, D. J. Garzon, M. Marchese et al., “Decreased brain-derived neurotrophic factor depends on amyloid aggregation state in transgenic mouse models of Alzheimer's disease,” The Journal of Neuroscience, vol. 29, no. 29, pp. 9321–9329, 2009. View at Publisher · View at Google Scholar · View at Scopus
  241. M. A. Sutton, H. T. Ito, P. Cressy, C. Kempf, J. C. Woo, and E. M. Schuman, “Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis,” Cell, vol. 125, no. 4, pp. 785–799, 2006. View at Publisher · View at Google Scholar · View at Scopus
  242. I. J. Cajigas, G. Tushev, T. J. Will, S. Tom Dieck, N. Fuerst, and E. M. Schuman, “The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging,” Neuron, vol. 74, no. 3, pp. 453–466, 2012. View at Publisher · View at Google Scholar · View at Scopus
  243. W. Ju, W. Morishita, J. Tsui et al., “Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors,” Nature Neuroscience, vol. 7, no. 3, pp. 244–253, 2004. View at Publisher · View at Google Scholar · View at Scopus
  244. A. B. McGeachie, L. A. Cingolani, and Y. Goda, “A stabilising influence: integrins in regulation of synaptic plasticity,” Neuroscience Research, vol. 70, no. 1, pp. 24–29, 2011. View at Publisher · View at Google Scholar · View at Scopus
  245. S. Mortillo, A. Elste, Y. Ge et al., “Compensatory redistribution of neuroligins and N-cadherin following deletion of synaptic β1-integrin,” Journal of Comparative Neurology, vol. 520, no. 9, pp. 2041–2052, 2012. View at Publisher · View at Google Scholar · View at Scopus
  246. D. T. S. Pak, S. Yang, S. Rudolph-Correia, E. Kim, and M. Sheng, “Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP,” Neuron, vol. 31, no. 2, pp. 289–303, 2001. View at Publisher · View at Google Scholar · View at Scopus
  247. K. Kubota, K. Inoue, R. Hashimoto et al., “Tumor necrosis factor receptor-associated protein 1 regulates cell adhesion and synaptic morphology via modulation of N-cadherin expression,” Journal of Neurochemistry, vol. 110, no. 2, pp. 496–508, 2009. View at Publisher · View at Google Scholar · View at Scopus
  248. P. D. Drew, M. Lonergan, M. E. Goldstein, L. A. Lampson, K. Ozato, and D. E. McFarlin, “Regulation of MHC class I and β2-microglobulin gene expression in human neuronal cells. Factor binding to conserved cis-acting regulatory sequences correlates with expression of the genes,” The Journal of Immunology, vol. 150, no. 8, part 1, pp. 3300–3310, 1993. View at Google Scholar · View at Scopus
  249. B. C. Albensi and M. P. Mattson, “Evidence for the involvement of TNF and NF-κB in hippocampal synaptic plasticity,” Synapse, vol. 35, no. 2, pp. 151–159, 2000. View at Google Scholar · View at Scopus
  250. M. P. Mattson, B. Cheng, D. Davis, K. Bryant, I. Lieberburg, and R. E. Rydel, “β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity,” The Journal of Neuroscience, vol. 12, no. 2, pp. 376–389, 1992. View at Google Scholar · View at Scopus
  251. M. Nuriya and R. L. Huganir, “Regulation of AMPA receptor trafficking by N-cadherin,” Journal of Neurochemistry, vol. 97, no. 3, pp. 652–661, 2006. View at Publisher · View at Google Scholar · View at Scopus
  252. L. Saglietti, C. Dequidt, K. Kamieniarz et al., “Extracellular interactions between GluR2 and N-cadherin in spine regulation,” Neuron, vol. 54, no. 3, pp. 461–477, 2007. View at Publisher · View at Google Scholar · View at Scopus
  253. H. Togashi, K. Abe, A. Mizoguchi, K. Takaoka, O. Chisaka, and M. Takeichi, “Cadherin regulates dendritic spine morphogenesis,” Neuron, vol. 35, no. 1, pp. 77–89, 2002. View at Publisher · View at Google Scholar · View at Scopus
  254. L. Tang, C. P. Hung, and E. M. Schuman, “A role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation,” Neuron, vol. 20, no. 6, pp. 1165–1175, 1998. View at Publisher · View at Google Scholar · View at Scopus
  255. O. Bozdagi, W. Shan, H. Tanaka, D. L. Benson, and G. W. Huntley, “Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation,” Neuron, vol. 28, no. 1, pp. 245–259, 2000. View at Publisher · View at Google Scholar · View at Scopus
  256. O. Bozdagi, X.-B. Wang, J. S. Nikitczuk et al., “Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin,” The Journal of Neuroscience, vol. 30, no. 30, pp. 9984–9989, 2010. View at Publisher · View at Google Scholar · View at Scopus
  257. P. Mendez, M. De Roo, L. Poglia, P. Klauser, and D. Muller, “N-cadherin mediates plasticity-induced long-term spine stabilization,” The Journal of Cell Biology, vol. 189, no. 3, pp. 589–600, 2010. View at Publisher · View at Google Scholar · View at Scopus