Progressive effect of beta amyloid peptides accumulation on CA1 pyramidal neurons: A model study suggesting possible treatments

Frontiers in Computational Neuroscience

Volumn 6, Issue JUL, 2012, Pages

  Culmone, Viviana ^a,b   Migliore, Michele ^a  

^a CNR   (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

Author keywords

A peptide; Hippocampal neuron; Ion channels modulation; Realistic model

Indexed keywords

CHEMICAL ACTIVATION; GLYCOPROTEINS; MODULATION; NEURODEGENERATIVE DISEASES; PEPTIDES; PROTEINS;

BETA AMYLOID PEPTIDES; CA1 PYRAMIDAL NEURON; HIPPOCAMPAL NEURONS; ION CHANNEL; PHARMACOLOGICAL MANIPULATION; REALISTIC MODEL; SYNAPTIC TRANSMISSION; THERAPEUTIC TREATMENTS;

NEURONS;

AMYLOID BETA PROTEIN;

ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; DISEASE COURSE; HIPPOCAMPAL CA1 REGION; MATHEMATICAL MODEL; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; POTASSIUM CURRENT; PYRAMIDAL NERVE CELL; SODIUM CURRENT; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 84872080503     PISSN: None     EISSN: 16625188     Source Type: Journal    
DOI: 10.3389/fncom.2012.00052     Document Type: Article

References (51)

1. Bentwich, J., Dobronevsky, E., Aichenbaum, S., Shorer, R., Peretz, R., Khaigrekht, M., Marton, R. G., and Rabey, J. M. (2011). Beneficial effect of repetitive transcranial magnetic stimulation combined with cognitive training for the treatment of Alzheimer's disease: a proof of concept study. J. Neural Transm. 118, 463-471.
2. Billings, L. M., Green, K. N., McGaugh, J. L., and LaFerla, F. M. (2007). Learning decreases Aβ*56 and tau pathology and ameliorates behavioral decline in 3xTg-AD mice. J. Neurosci. 27, 751-761.
3. Brookmeyer, R., Johnson, E., Ziegler-Graham, K., and Arrighi, K. M. (2007). Forecasting the global burden of Alzheimer's disease. Alzheimers Demen. 3, 186-191.
4. Csicsvari, J., Hirase, H., Czurko, A., Mamiya, A., and Buzsáki, G. (1999). Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci. 19, 274-287.
5. Eckert, A., Hauptmann, S., Scherping, I., Rhein, V., Müller-Spahn, F., Götz, J., and Müller, W. E. (2008). Soluble beta-amyloid leads to mitochondrial defects in amyloid precursor protein and tau transgenic mice. Neurodegener. Dis. 5, 157-159.
6. Ferrante, M., Blackwell, K. T., Migliore, M., and Ascoli, G. (2008). Computational models of neuronal biophysics and the characterization of potential neuropharmacological targets. Curr. Med. Chem. 15, 2456-2471.
7. Gasparini, S., Migliore, M., and Magee, J. C. (2004). On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci. 24, 11046-11056.
8. Goedert, M. (1987). Neuronal localization of amyloid beta protein precursor mRNA in normal human brain and in Alzheimer's disease. EMBO J. 6, 3627-3632.
9. Good, T. A., Smith, D. O., and Murphy, R. M. (1996). Beta-amyloid peptide blocks the fast-inactivating K+ current in rat hippocampal neurons. Biophys. J. 70, 296-304.
10. Hamos, J. E., DeGennaro, L. J., and Drachman, D. A. (1989). Synaptic loss in Alzheimer's disease and other dementias. Neurology 39, 355-361.
11. Hasselmo, M. E. (1997). A computational model of the progression of Alzheimer's disease. MD Comput. 14, 181-191.
12. Hines, M. L., and Carnevale, N. T. (1997). The NEURON simulation environment. Neural Comput. 9, 1179-1209.
13. Horn, D., Levy, N., and Ruppin, E. (1996). Neuronal-based synaptic compensation: a computational study in Alzheimer's disease. Neural Comput. 8, 1227-1243.
14. Iwatsubo, T., Odaka, A., Suzuki, N., Mizusawa, H., Nukina, N., and Ihara, Y. (1994). Visualization of A beta 42 and A beta 40 in senile plaques with end-specific A beta monoclonals: evidence that an initially deposited species is A beta 42. Neuron 13, 45-53.
15. Kamenetz, F., Tomita, T., Hsieh, H., Seabrook, G., Borchelt, D., Iwatsubo, T., Sisodia, S., and Malinow, R. (2003). APP processing and synaptic function. Neuron 37, 925-937.
16. Kerrigan, T. L., Atkinson, L., Peers, C., and Pearson, H. A. (2008). Modulation of “A”-type K+ current by rodent and human forms of amyloid b protein. Mol. Neurosci. 19, 839-843.
17. Kim, D. Y., Carey, B. W., Wang, H., Ingano, L. A. M., Binshtok, A. M., Wertz, M. H., Pettingell, W. H., He, P., Lee, V. M.-Y., Woolf, C. J., and Kovacs, D. M. (2007). BACE1 regulates voltage-gated sodium channels and neuronal activity. Nat. Cell Biol. 9, 755-764.
18. Kloskowska, E., Malkiewicza, K., Winblada, B., Benedikza, E., and Brutonb, J. D. (2008). APPswe mutation increases the frequency of spontaneous Ca2+-oscillations in rat hippocampal neurons. Neurosci. Lett. 436, 250-254.
19. Knobloch, M., and Mansuy, I. M. (2008). Dendritic spine loss and synaptic alterations in Alzheimer's disease. Mol. Neurobiol. 37, 73-82.
20. Kuchibhotla, K. V., Lattarulo, C. R., Hyman, B. T., and Bucskai, B. J. (2009). Synchronous hyperactivity and intracellular calcium waves in astrocytes in Alzheimer mice. Science 323, 1211-1215.
21. LaFerla, F. M., Green, K. N., and Oddo, S. (2007). Intracellular amyloid-β in Alzheimer's disease. Nat. Rev. Neurosci. 8, 499-509.
22. MacLean, J. N., Zhang, Y., Goeritz, M. L., Casey, R., Oliva, R., Guckenheimer, J., and Harris-Warrick, R. M. (2005). Activity-independent coregulation of IA and Ih in rhythmically active neurons. J. Neurophysiol. 94, 3601-3617.
23. Manczak, M., Anekonda, T. S., Henson, E., Park, B. S., Quinn, J., Reddy, P. H., and Genet, H. M. (2006). Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression. Hum. Mol. Genet. 15, 1437-49.
24. Mattson, M. P., and Chan, S. L. (2001). Dysregulation of cellular calcium homeostasis in Alzheimer's disease: bad genes and bad habits. J. Mol. Neurosci. 17, 205-224.
25. Megìas, M., Emri, Z. S., Freund, T. S., and Gulyàs, A. I. (2001). Total number and distribution of Synapses on hippocampal CA1 pyramidal cells. Neuroscience 102, 527-540.
26. Migliore, M. (2003). On the integration of subthreshold inputs from Perforant Path and Schaffer Collaterals in hippocampal CA1 pyramidal neurons. J. Comput. Neurosci. 14, 185-192.
27. Migliore, M., Novara, G., and Tegolo, D. (2008). Single neuron binding properties and the magical number 7. Hippocampus 18, 1122-1130.
28. Migliore, M., and Shepherd, G. M. (2002). Emerging rules for the distributions of active dendritic conductances. Nat. Rev. Neurosci. 3, 362-370.
29. Moreira, P. I., Santos, M. S., Moreno, A., and Oliveira, C. (2001). Amyloid β-peptide promotes permeability transition pore in brain mitochondria. Biosci. Rep. 21, 789-800.
30. Morse, T. M., Carnevale, N. T., Mutalik, P. G., Migliore, M., and Shepherd, G. M. (2010). Abnormal excitability of oblique dendrites implicated in early Alzheimer's: a computational study. Front. Neural Circuits 4:16. doi: 10.3389/fncir.2010.00016
31. Nagy, Z., Esiri, M. M., Jobst, K. A., Morris, J. H., King, E. M.-F., McDonald, B., Litchfield, S., Smith, A., Barnetson, L., and Smith, A. D. (1995). Relative roles of plaques and tangles in the dementia of Alzheimer's disease: correlations using three sets of neuropathological criteria. Dementia 6, 21-31.
32. Palop, J. J., and Mucke, L. (2010). Amyloid-β Induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat. Neurosci. 13, 812-818.
33. Parameshwaran, K., Sims, C., Kanju, P., Vaithianathan, T., Shonesy, B. C., Dhanasekaran, M., Bahr, B. A., and Suppiramanian, V. (2007). Amyloid Aβ1-42 but not Aβ-40 attenuates synaptic AMPA receptor function. Synapse61, 367-374.
34. Perez-Cruz, C., Nolte, M. W., van Gaalen, M. M., Rustay, N. R., Termpont, A., Tanghe, A., Kirchhoff, F., and Ebert, U. (2011). Reduced spine density in specific regions of CA1 pyramidal neurons in two transgenic mouse models of Alzheimer's disease. J. Neurosci. 31, 3926-3934.
35. Plant, L. D., Webster, N. J., Boyle, J. P., Ramsden, M., Freir, D. B., Peers, C., and Pearson, H. A. (2006). Amyloid- β peptide as a physiological modulator of neuronal “A”-type K+ current. Neurobiol. Aging 27, 1673-1683.
36. Ponomareva, N. V., Korovaitseva, G. I., and Rogaev, E. I. (2008). EEG alterations in non-demented individuals related to apolipoprotein E genotype and to risk of Alzheimer disease. Neurobiol. Aging 31, 819-827.
37. Reddy, P. H., and Beal, M. F. (2008). Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimer's disease. Trends Mol. Med. 14, 45-53.
38. Rensink, A. A. M., de Waal, R. M. W., Kremer, B., and Verbeek, M. M. (2003). Pathology of cerebral amyloid angiopathy. Brain Res. Rev. 43, 207-223.
39. Rowan, M. (2012). Information-selectivity of beta-amyloid pathology in an associative memory model. Front. Comput. Neurosci. 6:2. doi: 10.3389/fncom.2012.00002
40. Rui, Y., Li, R., Liu, Y., Zhu, S., Yu, X., Sheng, Z., and Xie, Z. (2006). Acute effect of β amyloid on synchronized spontaneous Ca2+ oscillations in cultured hippocampal networks. Cell Biol. Int. 30, 733-740.
41. Ruppin, E., and Reggia, J. A. (1995). A neural model of memory impairment in diffuse cerebral atrophy. Br. J. Psychiatry 166, 19-28.
42. Sato, S., Xu, J., Okuyama, S., Martinez, L. B., Walsh, S. M., Jacobsen, M. T., Swan, R. J., Schlautman, J. D., Ciborowski, P., and Ikezu, T. (2008). Spatial learning impairment, enhanced CDK5/p35 activity, and downregulation of NMDA receptor expression in transgenic mice expressing tau-tubulin kinase 1. J. Neurosci. 28, 14511-14521.
43. Schenk, D., Barbour, R., Dunn, W., Gordon, G., Grajeda, H., Guido, T., Hu, K., Huang, J., Johnson-Wood, K., Khan, K., Kholodenko, D., Lee, M., Liao, Z., Lieberburg, I., Motter, R., Mutter, L., Soriano, F., Shopp, G., Vasquez, N., Vandevert, C., Walker, S., Wogulis, M., Yednock, T., Games, D., and Seubert, P. (1999). Immunization with amyloid-β attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400, 173-177.
44. Selkoe, D. J. (1999). Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 399, A23-A31.
45. Shankar, G. M., Bloodgood, B. L., Townsend, M., Walsh, D. M., Selkoe, D. J., and Sabatini, B. L. (2007). Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA type glutamate receptor-dependent signaling pathway. J. Neurosci. 27, 2866-2875.
46. Snyder, E. M., Nong, Y., Almeida, C. G., Paul, S., Moran, T., Choi, E. Y., Nairn, A. C., Salter, M. W., Lombroso, P. J., Gouras, G. K., and Greengard, P. (2005). Regulation of NMDA receptor trafficking by amyloid-beta. Nat. Neurosci. 8, 1051-1058.
47. Terry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R., Hansen, L. A., and Katzman, R. (1991). Physical basis of cognitive alterations in alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580.
48. Terry, R. D. (2000). Cell death or synaptic loss in Alzheimer disease. J. Neuropathol. Exp. Neurol. 59, 1118-1119.
49. Texidó, L., Martín-Satué, M., Alberdi, E., Solsona, C., and Matute, C. (2011). Amyloid β peptide oligomers directly activate NMDA receptors. Cell Calcium 49, 184-190.
50. Wei, W., Nguyen, L. N., Kessels, H. W., Higiwara, H., Sisodia, S., and Malinow, R. (2010). Amyloid beta from axons and dendrites reduces local spine number and plasticity. Nat. Neurosci. 13, 190-196.
51. Zou, X., Coyle, D., Wong-Lin, K., and Maguire, L. (2011). Computational study of hippocampal-septal theta rhythm changes due to β-amyloid-altered ionic channels. PLoS ONE 6:e21579. doi: 10.1371/journal.pone.0021579