Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2014, Article ID 128631, 7 pages
http://dx.doi.org/10.1155/2014/128631
Research Article

BACE1 Is Necessary for Experience-Dependent Homeostatic Synaptic Plasticity in Visual Cortex

Zanvyl-Krieger Mind/Brain Institute, Solomon H. Snyder Department of Neuroscience, Johns Hopkins University, 3400 N. Charles Street, Dunning Hall 348, Baltimore, MD 21218, USA

Received 21 February 2014; Accepted 22 April 2014; Published 14 May 2014

Academic Editor: Clive Bramham

Copyright © 2014 Emily Petrus and Hey-Kyoung Lee. 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. J. Selkoe, “Resolving controversies on the path to Alzheimer's therapeutics,” Nature Medicine, vol. 17, no. 9, pp. 1060–1065, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. B. Katz and S. Rimmer, “Ophthalmologic manifestations of Alzheimer's disease,” Survey of Ophthalmology, vol. 34, no. 1, pp. 31–43, 1989. View at Google Scholar · View at Scopus
  3. M. Kiyosawa, T. M. Bosley, J. Chawluk et al., “Alzheimer's disease with prominent visual symptoms. Clinical and metabolic evaluation,” Ophthalmology, vol. 96, no. 7, pp. 1077–1086, 1989. View at Google Scholar · View at Scopus
  4. A. A. Sadun, M. Borchert, and E. DeVita, “Assessment of visual impairment in patients with Alzheimer's disease,” The American Journal of Ophthalmology, vol. 104, no. 2, pp. 113–120, 1987. View at Google Scholar · View at Scopus
  5. A. G. Lee and C. O. Martin, “Neuro-ophthalmic findings in the visual variant of Alzheimer's disease,” Ophthalmology, vol. 111, no. 2, pp. 376–380, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Bublak, P. Redel, C. Sorg et al., “Staged decline of visual processing capacity in mild cognitive impairment and Alzheimer's disease,” Neurobiology of Aging, vol. 32, no. 7, pp. 1219–1230, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. P. R. Hof, C. Bouras, J. Constantinidis, and J. H. Morrison, “Selective disconnection of specific visual association pathways in cases of Alzheimer's disease presenting with Balint's syndrome,” Journal of Neuropathology and Experimental Neurology, vol. 49, no. 2, pp. 168–184, 1990. View at Google Scholar · View at Scopus
  8. P. R. Hof, C. Bouras, J. Constantinidis, and J. H. Morrison, “Balint's syndrome in Alzheimer's disease: specific disruption of the occipito-parietal visual pathway,” Brain Research, vol. 493, no. 2, pp. 368–375, 1989. View at Google Scholar · View at Scopus
  9. J. H. Morrison, P. R. Hof, and C. Bouras, “An anatomic substrate for visual disconnection in Alzheimer's disease,” Annals of the New York Academy of Sciences, vol. 640, pp. 36–43, 1991. View at Google Scholar · View at Scopus
  10. R. C. Pearson, M. M. Esiri, and R. W. Hiorns, “Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 13, pp. 4531–4534, 1985. View at Google Scholar · View at Scopus
  11. D. A. Lewis, M. J. Campbell, R. D. Terry, and J. H. Morrison, “Laminar and regional distributions of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: a quantitative study of visual and auditory cortices,” Journal of Neuroscience, vol. 7, no. 6, pp. 1799–1808, 1987. View at Google Scholar · View at Scopus
  12. P. R. Hof and J. H. Morrison, “Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer's disease: II. Primary and secondary visual cortex,” Journal of Comparative Neurology, vol. 301, no. 1, pp. 55–64, 1990. View at Google Scholar · View at Scopus
  13. P. R. Hof, B. A. Vogt, C. Bouras et al., “Atypical form of Alzheimer's disease with prominent posterior cortical atrophy: a review of lesion distribution and circuit disconnection in cortical visual pathways,” Vision Research, vol. 37, no. 24, pp. 3609–3625, 1997. View at Google Scholar
  14. C. Grienberger, N. L. Rochefort, H. Adelsberger et al., “Staged decline of neuronal function in vivo in an animal model of Alzheimer's disease,” Nature Communications, vol. 3, article 1783, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Beker, V. Kellner, L. Kerti et al., “Interaction between amyloid-beta pathology and cortical functional columnar organization,” Journal of Neuroscience, vol. 32, no. 33, pp. 11241–11249, 2012. View at Google Scholar
  16. 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
  17. C. M. William, M. L. Andermann, G. J. Goldey et al., “Synaptic plasticity defect following visual deprivation in Alzheimer's disease model transgenic mice,” Journal of Neuroscience, vol. 32, no. 23, pp. 8004–8011, 2012. View at Google Scholar
  18. H. Wang, A. Megill, K. He et al., “Consequences of inhibiting amyloid precursor protein processing enzymes on synaptic function and plasticity,” Neural Plasticity, vol. 2012, Article ID 272374, 24 pages, 2012. View at Publisher · View at Google Scholar
  19. 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
  20. 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
  21. D. V. Venkitaramani, J. Chin, W. J. Netzer et al., “β-amyloid modulation of synaptic transmission and plasticity,” Journal of Neuroscience, vol. 27, no. 44, pp. 11832–11837, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. A. W. Bero, P. Yan, J. H. Roh et al., “Neuronal activity regulates the regional vulnerability to amyloid-β 2 deposition,” Nature Neuroscience, vol. 14, no. 6, pp. 750–756, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. J. R. Cirrito, J.-E. Kang, J. Lee et al., “Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo,” Neuron, vol. 58, no. 1, pp. 42–51, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. 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
  25. K. S. Vetrivel and G. Thinakaran, “Amyloidogenic processing of β-amyloid precursor protein in intracellular compartments,” Neurology, vol. 66, supplement 2, pp. S69–S73, 2006. View at Google Scholar · View at Scopus
  26. C. G. Almeida, D. Tampellini, R. H. Takahashi et al., “Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses,” Neurobiology of Disease, vol. 20, no. 2, pp. 187–198, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. 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
  28. 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
  29. M. Gao, K. Sossa, L. Song et al., “A specific requirement of Arc/Arg3.1 for visual experience-induced homeostatic synaptic plasticity in mouse primary visual cortex,” Journal of Neuroscience, vol. 30, no. 21, pp. 7168–7178, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Goel, B. Jiang, L. W. Xu, L. Song, A. Kirkwood, and H.-K. Lee, “Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience,” Nature Neuroscience, vol. 9, no. 8, pp. 1001–1003, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. N. S. Desai, R. H. Cudmore, S. B. Nelson, and G. G. Turrigiano, “Critical periods for experience-dependent synaptic scaling in visual cortex,” Nature Neuroscience, vol. 5, no. 8, pp. 783–789, 2002. View at Publisher · View at Google Scholar · View at Scopus
  32. K. He, E. Petrus, N. Gammon et al., “Distinct sensory requirements for unimodal and cross-modal homeostatic synaptic plasticity,” Journal of Neuroscience, vol. 32, no. 25, pp. 8469–8474, 2012. View at Google Scholar
  33. 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
  34. E. Petrus, T. T. Anguh, H. Pho, A. Lee, N. Gammon, and H.-K. Lee, “Developmental switch in the polarity of experience-dependent synaptic changes in layer 6 of mouse visual cortex,” Journal of Neurophysiology, vol. 106, no. 5, pp. 2499–2505, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Goel and H. K. Lee, “Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex,” Journal of Neuroscience, vol. 27, no. 25, pp. 6692–6700, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. J. L. Whitt, E. Petrus, and H. K. Lee, “Experience-dependent homeostatic synaptic plasticity in neocortex,” Neuropharmacology, vol. 78, pp. 45–54, 2014. View at Publisher · View at Google Scholar
  37. H. Cai, Y. Wang, D. McCarthy et al., “BACE1 is the major β-secretase for generation of Aβ peptides by neurons,” Nature Neuroscience, vol. 4, no. 3, pp. 233–234, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. F. M. Laird, H. Cai, A. V. Savonenko et al., “BACE1, a major determinant of selective vulnerability of the brain to amyloid-β amyloidogenesis, is essential for cognitive, emotional, and synaptic functions,” Journal of Neuroscience, vol. 25, no. 50, pp. 11693–11709, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Dominguez, J. Tournoy, D. Hartmann et al., “Phenotypic and biochemical analyses of BACE1- and BACE2-deficient mice,” Journal of Biological Chemistry, vol. 280, no. 35, pp. 30797–30806, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. X. Hu, X. Zhou, W. He et al., “BACE1 deficiency causes altered neuronal activity and neurodegeneration,” Journal of Neuroscience, vol. 30, no. 26, pp. 8819–8829, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. B. D. Hitt, T. C. Jaramillo, D. M. Chetkovich, and R. Vassar, “BACE1-/- mice exhibit seizure activity that does not correlate with sodium channel level or axonal localization,” Molecular Neurodegeneration, vol. 5, no. 1, article 31, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Y. Kim, B. W. Carey, H. Wang et al., “BACE1 regulates voltage-gated sodium channels and neuronal activity,” Nature Cell Biology, vol. 9, no. 7, pp. 755–764, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. P. H. Kuhn, K. Koroniak, S. Hogl et al., “Secretome protein enrichment identifies physiological BACE1 protease substrates in neurons,” The EMBO Journal, vol. 31, no. 14, pp. 3157–3168, 2012. View at Google Scholar
  44. L. Zhou, S. Barao, M. Laga et al., “The neural cell adhesion molecules L1 and CHL1 are cleaved by BACE1 protease in vivo,” Journal of Biological Chemistry, vol. 287, no. 31, pp. 25927–25940, 2012. View at Google Scholar
  45. Q. Li and T. C. Südhof, “Cleavage of Amyloid-β Precursor Protein and Amyloid-β Precursor-like Protein by BACE 1,” Journal of Biological Chemistry, vol. 279, no. 11, pp. 10542–10550, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. H. K. Wong, T. Sakurai, F. Oyama et al., “β subunits of voltage-gated sodium channels are novel substrates of β-site amyloid precursor protein-cleaving enzyme (BACE1) and γ-secretase,” Journal of Biological Chemistry, vol. 280, no. 24, pp. 23009–23017, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. X. Hu, C. W. Hicks, W. He et al., “Bace1 modulates myelination in the central and peripheral nervous system,” Nature Neuroscience, vol. 9, no. 12, pp. 1520–1525, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Willem, A. N. Garratt, B. Novak et al., “Control of peripheral nerve myelination by the β-secretase BACE1,” Science, vol. 314, no. 5799, pp. 664–666, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. B. De Strooper, “Aph-1, Pen-2, and Nicastrin with Presenilin generate an active γ-Secretase complex,” Neuron, vol. 38, no. 1, pp. 9–12, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. K. G. Pratt, E. C. Zimmerman, D. G. Cook, and J. M. Sullivan, “Presenilin 1 regulates homeostatic synaptic scaling through Akt signaling,” Nature Neuroscience, vol. 14, no. 9, pp. 1112–1114, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Ishida, K. Furukawa, J. N. Keller et al., “Secreted form of beta-amyloid precursor protein shifts the frequency dependency for induction of LTD, and enhances LTP in hippocampal slices,” NeuroReport, vol. 8, no. 9-10, pp. 2133–2137, 1997. View at Google Scholar
  52. C. J. Taylor, D. R. Ireland, I. Ballagh et al., “Endogenous secreted amyloid precursor protein-α regulates hippocampal NMDA receptor function, long-term potentiation and spatial memory,” Neurobiology of Disease, vol. 31, no. 2, pp. 250–260, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Cai, X. Qi, N. Kociok et al., “beta-Secretase (BACE1) inhibition causes retinal pathology by vascular dysregulation and accumulation of age pigment,” EMBO Molecular Medicine, vol. 4, no. 9, pp. 980–991, 2012. View at Google Scholar
  54. B. S. Blais, M. Y. Frenkel, S. R. Kuindersma et al., “Recovery from monocular deprivation using binocular deprivation,” Journal of Neurophysiology, vol. 100, no. 4, pp. 2217–2224, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. M. P. Mattson, “Pathways towards and away from Alzheimer's disease,” Nature, vol. 430, no. 7000, pp. 631–639, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. I. Bezprozvanny and M. P. Mattson, “Neuronal calcium mishandling and the pathogenesis of Alzheimer's disease,” Trends in Neurosciences, vol. 31, no. 9, pp. 454–463, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. 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