Synaptic depression and aberrant excitatory network activity in alzheimer's disease: Two faces of the same coin?

NeuroMolecular Medicine

Volumn 12, Issue 1, 2010, Pages 48-55

  Palop, J J ^a   Mucke, Lennart ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

A induced epileptiform activity; Alzheimer's disease; Amyloid ; Cognitive decline; Network dysfunction; Synaptic depression

Indexed keywords

AMYLOID BETA PROTEIN;

ABBERANT EXCITATORY NEURONAL ACTIVITY; ALZHEIMER DISEASE; BRAIN REGION; COGNITIVE DEFECT; CORTICAL SYNCHRONIZATION; DISEASE ASSOCIATION; EPILEPTIC DISCHARGE; GLUTAMATERGIC TRANSMISSION; HUMAN; LEARNING; LONG TERM DEPRESSION; MEMORY; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW; SEIZURE; SYNAPTIC TRANSMISSION; ANIMAL; CYTOLOGY; HOMEOSTASIS; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; HOMEOSTASIS; HUMANS; LONG-TERM SYNAPTIC DEPRESSION; NERVE NET; NEURONS; SYNAPTIC TRANSMISSION;

EID: 77952484484     PISSN: 15351084     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12017-009-8097-7     Document Type: Review

References (58)

1. Bezprozvanny, I., & Mattson, M. P. (2008). Neuronal calcium mishandling and the pathogenesis of Alzheimer's disease. Trends in Neurosciences, 31, 454-463.
2. Braak, H., & Braak, E. (1991). Neuropathology stageing of Alzheimer-related changes. Acta Neuropathologica, 82, 239-259.
3. Braak, H., Del Tredici, K., Rub, U., de Vos, R. A., Jansen Steur, E. N., & Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson's disease. Neurobiology of Aging, 24, 197-211. (Pubitemid 36007810)
4. Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain's default network: anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 1-38.
5. Buckner, R. L., Snyder, A. Z., Shannon, B. J., LaRossa, G., Sachs, R., Fotenos, A. F., et al. (2005). Molecular, structural, and functional characterization of Alzheimer's disease: Evidence for a relationship between default activity, amyloid, and memory. Journal of Neuroscience, 25, 7709-7717. (Pubitemid 41208641)
6. Busche, M. A., Eichhoff, G., Adelsberger, H., Abramowski, D., Wiederhold, K. H., Haass, C., et al. (2008). Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science, 321, 1686-1689.
7. Chang, S., Ma, T. R., Miranda, R. D., Balestra, M. E., Mahley, R. W., & Huang, Y. (2005). Lipid- and receptor-binding regions of apolipoprotein E4 fragments act in concert to cause mitochondrial dysfunction and neurotoxicity. Proceedings of the National Academy of Sciences of the United States of America, 102, 18694-18699. (Pubitemid 43011288)
8. Chapman, P. F., White, G. L., Jones, M. W., Cooper-Blacketer, D., Marshall, V. J., Irizarry, M., et al. (1999). Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nature Neuroscience, 2, 271-276. (Pubitemid 30491299)
9. Cho, D. H., Nakamura, T., Fang, J., Cieplak, P., Godzik, A., Gu, Z., et al. (2009). S-nitrosylation of Drp1 mediates beta-amyloidrelated mitochondrial fission and neuronal injury. Science, 324, 102-105.
10. Cirrito, J. R., Kang, J. E., Lee, J., Stewart, F. R., Verges, D. K., Silverio, L. M., et al. (2008). Endocytosis is required for synaptic activitydependent release of amyloid-beta in vivo. Neuron, 58, 42-51. (Pubitemid 351467029)
11. Cirrito, J. R., Yamada, K A., Finn, M. B., Sloviter, R. S., Bales, K. R., May, P. C., et al. (2005). Synaptic activity regulates interstitial fluid amyloid-b levels in vivo. Neuron, 48, 913-922.
12. Cleary, J. P., Walsh, D. M., Hofmeister, J. J., Shankar, G. M., Kuskowski, M. A., Selkoe, D. J., et al. (2005). Natural oligomers of the amyloid-/? protein specifically disrupt cognitive function. Nature Neuroscience, 8, 79-84.
13. Dineley, K. T., Westerman, M., Bui, D., Bell, K., Ashe, K. H., & Sweatt, J. D. (2001). b-Amyloid activates the mitogen-activated protein kinase cascade via hippocampal a7 nicotinic acetylcholine receptors: In vitro and in vivo mechanisms related to Alzheimer's disease. Journal of Neuroscience, 21, 4125-4133. (Pubitemid 32538537)
14. Du, H., Guo, L., Fang, F., Chen, D., Sosunov, A. A., McKhann, G. M., et al. (2008). Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nature Medicine, 14, 1097-1105.
15. Harris, M. E., Carney, J. M., Cole, P. S., Hensley, K., Howard, B. J., Martin, L., et al. (1995). b-Amyloid peptide-derived, oxygendependent free radicals inhibit glutamate uptake in cultured astrocytes: Implications for Alzheimer's disease. Neuroreport, 6, 1875-1879.
16. Hsia, A., Masliah, E., McConlogue, L., Yu, G., Tatsuno, G., Hu, K., et al. (1999). 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, 96, 3228-3233. (Pubitemid 29148873)
17. Hsieh, H., Boehm, J., Sato, C., Iwatsubo, T., Tomita, T., Sisodia, S., et al. (2006). AMPAR removal underlies Aβ-induced synaptic depression and dendritic spine loss. Neuron, 52, 831-843. (Pubitemid 44828454)
18. Kamenetz, F., Tomita, T., Hsieh, H., Seabrook, G., Borchelt, D., Iwatsubo, T., et al. (2003). APP processing and synaptic function. Neuron, 37, 925-937.
19. Keller, J. N., Pang, Z., Geddes, J. W., Begley, J. G., Germeyer, A., Waeg, G., et al. (1997). Impairment of glucose and glutamate transport, and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid b-peptide: Role of the lipid peroxidation product 4-hydroxynonenal. Journal of Neurochemistry, 69, 273-284. (Pubitemid 27274182)
20. 2+ imparts NMDA receptor subtype selectivity to the Alzheimer's drug memantine. Journal of Neuroscience, 29, 2774-2779.
21. Lauren, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W., & Strittmatter, S. M. (2009). Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature, 457, 1128-1132.
22. Li, S., Hong, S., Shepardson, N. E., Walsh, D. M., Shankar, G. M., & Selkoe, D. (2009a). Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron, 62, 788-801.
23. Li, C. Y., Poo, M. M., & Dan, Y. (2009b). Burst spiking of a single cortical neuron modifies global brain state. Science, 324, 643-646.
24. Lipton, S. A. (2005). The molecular basis of memantine action in Alzheimer's disease and other neurologic disorders: low-affinity, uncompetitive antagonism. Current Alzheimer Research, 2, 155-165.
25. Lustig, C., Snyder, A. Z., Bhakta, M., O'Brien, K. C., McAvoy, M., Raichle, M. E., et al. (2003). Functional deactivations: change with age and dementia of the Alzheimer type. Proceedings of the National Academy of Sciences of the United States of America, 100, 14504-14509. (Pubitemid 37499266)
26. Mackenzie, I. R., & Miller, L. A. (1994). Senile plaques in temporal lobe epilepsy. Acta Neuropathologica, 87, 504-510. (Pubitemid 24128978)
27. 2- homeostasis and cell death. Journal of Neuroscience, 15, 6239-6249.
28. Masliah, E., Alford, M., Mallory, M., Rockenstein, E., Moechars, D., & Van Leuven, F. (2000). Abnormal glutamate transport function in mutant amyloid precursor protein transgenic mice. Experimental Neurology, 163, 381-387. (Pubitemid 30399086)
29. Mattson, M. P., Cheng, B., Davis, D., Bryant, K., Lieberburg, I., & Rydel, R. E. (1992). b-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. Journal of Neuroscience, 12, 376-389.
30. Mattson, M. P., Gleichmann, M., & Cheng, A. (2008). Mitochondria in neuroplasticity and neurological disorders. Neuron, 60, 748-766.
31. Meilandt, W. J., Yu, G.-Q., Chin, J., Roberson, E. D., Palop, J. J., Wu, T., et al. (2008). Enkephalin elevations contribute to neuronal and behavioral impairments in a transgenic mouse model of Alzheimer's disease. Journal of Neuroscience, 28, 5007-5017.
32. Minkeviciene, R., Rheims, S., Dobszay, M. B., Zilberter, M., Hartikainen, J., Fulop, L., et al. (2009). Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. Journal of Neuroscience, 29, 3453-3462.
33. Mintun, M. A., Larossa, G. N., Sheline, Y. I., Dence, C. S., Lee, S. Y., Mach, R. H., et al. (2006). [11C]PIB in a nondemented population: Potential antecedent marker of Alzheimer disease. Neurology, 67, 446-452.
34. Origlia, N., Righi, M., Capsoni, S., Cattaneo, A., Fang, F., Stern, D. M., et al. (2008). Receptor for advanced glycation end productdependent activation of p38 mitogen-activated protein kinase contributes to amyloid-beta-mediated cortical synaptic dysfunction. Journal of Neuroscience, 28, 3521-3530. (Pubitemid 351469321)
35. Palop, J. J., Chin, J., Bien-Ly, N., Massaro, C., Yeung, B. Z., Yu, G.Q., et al. (2005). Vulnerability of dentate granule cells to disruption of Arc expression in human amyloid precursor protein transgenic mice. Journal of Neuroscience, 25, 9686-9693. (Pubitemid 41510909)
36. Palop, J. J., Chin, J., & Mucke, L. (2006). A network dysfunction perspective on neurodegenerative diseases. Nature, 443, 768-773. (Pubitemid 44622680)
37. Palop, J., Chin, J., Roberson, E., Wang, J., Thwin, M., Bien-Ly, N., et al. (2007). Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron, 55, 697-711. (Pubitemid 47321079)
38. Palop, J. J., Jones, B., Kekonius, L., Chin, J., Yu, G.-Q., Raber, J., et al. (2003). Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's diseaserelated cognitive deficits. Proceedings of the National Academy of Sciences of the United States of America, 100, 9572-9577. (Pubitemid 37033969)
39. Palop, J. J., & Mucke, L. (2009). Epilepsy and cognitive impairments in Alzheimer's disease. Archives of Neurology, 66, 435-440.
40. Petrella, J. R., Prince, S. E., Wang, L., Hellegers, C., & Doraiswamy, P. M. (2007). Prognostic value of posteromedial cortex deactivation in mild cognitive impairment. PLoS One, 2, e1104. (Pubitemid 351586850)
41. Pihlajamaki, M., DePeau, K. M., Blacker, D., & Sperling, R. A. (2008). Impaired medial temporal repetition suppression is related to failure of parietal deactivation in Alzheimer disease. American Journal of Geriatric Psychiatry, 16, 283-292.
42. Porsteinsson, A. P., Grossberg, G. T., Mintzer, J., & Olin, J. T. (2008). Memantine treatment in patients with mild to moderate Alzheimer's disease already receiving a Cholinesterase inhibitor: a randomized, double-blind, placebo-controlled trial. Current Alzheimer Research, 5, 83-89. (Pubitemid 351536358)
43. Roberson, E. D., Scearce-Levie, K., Palop, J. J., Yan, F., Cheng, I. H., Wu, T., et al. (2007). Reducing endogenous tau ameliorates amyloid β-induced deficits in an Alzheimer's disease mouse model. Science, 316, 750-754. (Pubitemid 46717684)
44. Rothman, S. M., & Olney, J. W. (1995). Excitotoxicity and the NMDA receptor -Still lethal after eight years. Trends in Neurosciences, 18, 57-58.
45. Sanchez-Mejia, R. O., Newman, J. W., Toh, S., Yu, G.-Q., Zhou, Y., Halabisky, B., et al. (2008). Phospholipase A2 reduction ameliorates cognitive deficits in mouse model of Alzheimer's disease. Nature Neuroscience, 11, 1311-1318.
46. Seeley, W. W., Crawford, R. K., Zhou, J., Miller, B. L., & Greicius, M. D. (2009). Neurodegenerative diseases target large-scale human brain networks. Neuron, 62, 42-52.
47. Shankar, G. M., Bloodgood, B. L., Townsend, M., Walsh, D. M., Selkoe, D. J., & Sabatini, B. L. (2007). Natural oligomers of the Alzheimer amyloid-β protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. Journal of Neuroscience, 27, 2866-2875. (Pubitemid 46438992)
48. Snyder, E. M., Nong, Y., Almeida, C. G., Paul, S., Moran, T., Choi, E. Y., et al. (2005). Regulation of NMDA receptor trafficking by amyloid-β. Nature Neuroscience, 8, 1051-1058. (Pubitemid 41061516)
49. Sperling, R. A., Laviolette, P. S., O'Keefe, K., O'Brien, J., Rentz, D. M., Pihlajamaki, M., et al. (2009). Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron, 63, 178-188.
50. Townsend, M., Shankar, G. M., Mehta, T., Walsh, D. M., & Selkoe, D. J. (2006). Effects of secreted oligomers of amyloid β-protein on hippocampal synaptic plasticity: A potent role for trimers. Journal of Physiology, 572, 477-492.
51. Turrigiano, G. G., Leslie, K. R., Desai, N. S., Rutherford, L. C., & Nelson, S. B. (1998). Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature, 391, 892-896.
52. Turrigiano, G. G., & Nelson, S. B. (2004). Homeostatic plasticity in the developing nervous system. Nature Reviews. Neuroscience, 5, 97-107. (Pubitemid 38160285)
53. Vicario-Abejon, C., Owens, D., McKay, R., & Segal, M. (2002). Role of neurotrophins in central synapse formation and stabilization. Nature Reviews. Neuroscience, 3, 965-974. (Pubitemid 135715882)
54. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., et al. (2002). Naturally secreted oligomers of amyloid /? protein potently inhibit hippocampal long-term potentiation in vivo. Nature, 416, 535-539. (Pubitemid 34288854)
55. Wang, X., Su, B., Siedlak, S. L., Moreira, P. I., Fujioka, H., Wang, Y., et al. (2008). Amyloid-beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proceedings of the National Academy of Sciences of the United States of America, 105, 19318-19823.
56. Wishart, H. A., Saykin, A. J., Rabin, L. A., Santulli, R. B., Flashman, L. A., Guerin, S. J., et al. (2006). Increased brain activation during working memory in cognitively intact adults with the APOE epsilon4 allele. American Journal of Psychiatry, 163, 1603-1610. (Pubitemid 44465762)
57. Wu, J., Anwyl, R., & Rowan, M. J. (1995). beta-Amyloid selectively augments NMDA receptor-mediated synaptic transmission in rat hippocampus. Neuroreport, 6, 2409-2413.
58. Yoshiike, Y., Kayed, R., Milton, S. C., Takashima, A., & Glabe, C. G. (2007). Pore-forming proteins share structural and functional homology with amyloid oligomers. Neuromuscular Medicine, 9, 270-275. (Pubitemid 350129702)