Altered intrinsic neuronal excitability and reduced Na+ currents in a mouse model of Alzheimer's disease

Neurobiology of Aging

Volumn 32, Issue 11, 2011, Pages 2109.e1-2109.e14

  Brown, Jon T ^a   Chin, Jeannie ^b   Leiser, Steven C ^b   Pangalos, Menelas N ^b   Randall, Andrew D ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b PFIZER INC   (United States)

Author keywords

Alzheimer's disease; Beta amyloid; Electrophysiology; Hippocampus; Sodium channels

Indexed keywords

AMYLOID BETA PROTEIN; VOLTAGE GATED SODIUM CHANNEL;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; CORRELATIONAL STUDY; GENE OVEREXPRESSION; GENOTYPE; HIPPOCAMPAL CA1 REGION; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE STIMULATION; NONHUMAN; PATCH CLAMP; POTASSIUM CURRENT; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SODIUM CURRENT; STIMULUS RESPONSE; TRANSGENIC MOUSE; VOLTAGE CLAMP; WAVEFORM;

EID: 80052619181     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.05.025     Document Type: Article

References (56)

1. Arendash G.W., King D.L., Gordon M.N., Morgan D., Hatcher J.M., Hope C.E., Diamond D.M. Progressive, age-related behavioral impairments in transgenic mice carrying both mutant amyloid precursor protein and presenilin-1 transgenes. Brain Res 2001, 891:42-53.
2. Ashe K.H. Learning and memory in transgenic mice modeling Alzheimer's disease. Learn. Mem 2001, 8:301-308.
3. Becker A.J., Pitsch J., Sochivko D., Opitz T., Staniek M., Chen C.C., Campbell K.P., Schoch S., Yaari Y., Beck H. Transcriptional upregulation of Cav32 mediates epileptogenesis in the pilocarpine model of epilepsy. J. Neurosci 2008, 28:13341-13353.
4. Brace H.M., Jefferys J.G., Mellanby J. Long-term changes in hippocampal physiology and learning ability of rats after intrahippocampal tetanus toxin. J. Physiol 1985, 368:343-357.
5. Brager D.H., Johnston D. Plasticity of intrinsic excitability during long-term depression is mediated through mGluR-dependent changes in I(h) in hippocampal CA1 pyramidal neurons. J. Neurosci 2007, 27:13926-13937.
6. Brown J.T., Booth C.A., Randall A.D. Synaptic activation of mGluR1 generates persistent depression of a fast after-depolarizing potential in CA3 pyramidal neurons. Eur. J. Neurosci 2011, 33:879-889.
7. Brown J.T., Randall A.D. Activity-dependent depression of the spike after-depolarization generates long-lasting intrinsic plasticity in hippocampal CA3 pyramidal neurons. J. Physiol 2009, 587:1265-1281.
8. Brown J.T., Richardson J.C., Collingridge G.L., Randall A.D., Davies C.H. Synaptic transmission and synchronous activity is disrupted in hippocampal slices taken from aged TAS10 mice. Hippocampus 2005, 15:110-117.
9. Busche M.A., Eichhoff G., Adelsberger H., Abramowski D., Wiederhold K.H., Haass C., Staufenbiel M., Konnerth A., Garaschuk O. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 2008, 321:1686-1689.
10. Chapman P.F., White G.L., Jones M.W., Cooper-Blacketer D., Marshall V.J., Irizarry M., Younkin L., Good M.A., Bliss T.V., Hyman B.T., Younkin S.G., Hsiao K.K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci 1999, 2:271-276.
11. Chen C. beta-Amyloid increases dendritic Ca2+ influx by inhibiting the A-type K+ current in hippocampal CA1 pyramidal neurons. Biochem. Biophys. Res. Commun 2005, 338:1913-1919.
12. Citron M. Strategies for disease modification in Alzheimer's disease. Nat. Rev 2004, 5:677-685.
13. Driver J.E., Racca C., Cunningham M.O., Towers S.K., Davies C.H., Whittington M.A., LeBeau F.E. Impairment of hippocampal gamma-frequency oscillations in vitro in mice overexpressing human amyloid precursor protein (APP). Eur. J. Neurosci 2007, 26:1280-1288.
14. Fan Y., Fricker D., Brager D.H., Chen X., Lu H.C., Chitwood R.A., Johnston D. Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat. Neurosci 2005, 8:1542-1551.
15. Fitzjohn S.M., Morton R.A., Kuenzi F., Rosahl T.W., Shearman M., Lewis H., Smith D., Reynolds D.S., Davies C.H., Collingridge G.L., Seabrook G.R. 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. J. Neurosci 2001, 21:4691-4698.
16. Fukumoto H., Cheung B.S., Hyman B.T., Irizarry M.C. Beta-secretase protein and activity are increased in the neocortex in Alzheimer disease. Arch. Neurol 2002, 59:1381-1389.
17. Fukumoto H., Rosene D.L., Moss M.B., Raju S., Hyman B.T., Irizarry M.C. Beta-secretase activity increases with aging in human, monkey, and mouse brain. Am. J. Pathol 2004, 164:719-725.
18. Good T.A., Smith D.O., Murphy R.M. Beta-amyloid peptide blocks the fast-inactivating K+ current in rat hippocampal neurons. Biophys. J 1996, 70:296-304.
19. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
20. Hodgkin A.L., Huxley A.F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol 1952, 117:500-544.
21. Holcomb L., Gordon M.N., McGowan E., Yu X., Benkovic S., Jantzen P., Wright K., Saad I., Mueller R., Morgan D., Sanders S., Zehr C., O'Campo K., Hardy J., Prada C.M., Eckman C., Younkin S., Hsiao K., Duff K. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat. Med 1998, 4:97-100.
22. Hsia A.Y., Masliah E., McConlogue L., Yu G.Q., Tatsuno G., Hu K., Kholodenko D., Malenka R.C., Nicoll R.A., Mucke L. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:3228-3233.
23. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
24. Huth T., Schmidt-Neuenfeldt K., Rittger A., Saftig P., Reiss K., Alzheimer C. Non-proteolytic effect of beta-site APP-cleaving enzyme 1 (BACE1) on sodium channel function. Neurobiol. Dis 2009, 33:282-289.
25. Jacobsen J.S., Reinhart P., Pangalos M.N. Current concepts in therapeutic strategies targeting cognitive decline and disease modification in Alzheimer's disease. Neurorx 2005, 2:612-626.
26. Kim D.Y., Carey B.W., Wang H., Ingano L.A., Binshtok A.M., Wertz M.H., Pettingell W.H., He P., Lee V.M., Woolf C.J., Kovacs D.M. BACE1 regulates voltage-gated sodium channels and neuronal activity. Nat. Cell Biol 2007, 9:755-764.
27. Kim D.Y., Ingano L.A., Carey B.W., Pettingell W.H., Kovacs D.M. Presenilin/gamma-secretase-mediated cleavage of the voltage-gated sodium channel beta2-subunit regulates cell adhesion and migration. J. Biol. Chem 2005, 280:23251-23261.
28. Larson J., Lynch G., Games D., Seubert P. Alterations in synaptic transmission and long-term potentiation in hippocampal slices from young and aged PDAPP mice. Brain Res 1999, 840:23-35.
29. McGowan E., Sanders S., Iwatsubo T., Takeuchi A., Saido T., Zehr C., Yu X., Uljon S., Wang R., Mann D., Dickson D., Duff K. Amyloid phenotype characterization of transgenic mice overexpressing both mutant amyloid precursor protein and mutant presenilin 1 transgenes. Neurobiol. Dis 1999, 6:231-244.
30. Metz A.E., Jarsky T., Martina M., Spruston N. R-type calcium channels contribute to afterdepolarization and bursting in hippocampal CA1 pyramidal neurons. J. Neurosci 2005, 25:5763-5773.
31. Metz A.E., Spruston N., Martina M. Dendritic D-type potassium currents inhibit the spike afterdepolarization in rat hippocampal CA1 pyramidal neurons. J. Physiol 2007, 581:175-187.
32. Minkeviciene R., Rheims S., Dobszay M.B., Zilberter M., Hartikainen J., Fülöp L., Penke B., Zilberter Y., Harkany T., Pitkänen A., Tanila H. Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. J. Neurosci 2009, 29:3453-3462.
33. Naundorf B., Wolf F., Volgushev M. Unique features of action potential initiation in cortical neurons. Nature 2006, 440:1060-1063.
34. Nowacki J., Osinga H.M., Brown J.T., Randall A.D., Tsaneva-Atanasova K. A unified model of CA1/3 pyramidal cells: An investigation into excitability. Prog. Biophys. Mol. Biol 2010, 105:35-48.
35. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003, 39:409-421.
36. Palop J.J., Chin J., Roberson E.D., Wang J., Thwin M.T., Bien-Ly N., Yoo J., Ho K.O., Yu G.Q., Kreitzer A., Finkbeiner S., Noebels J.L., Mucke L. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 2007, 55:697-711.
37. Palop J.J., Mucke L. Epilepsy and cognitive impairments in Alzheimer disease. Arch. Neurol 2009, 66:435-440.
38. Randall A.D., Witton J., Booth C., Hynes-Allen A., Brown J.T. The functional neurophysiology of the amyloid precursor protein (APP) processing pathway. Neuropharmacology 2010, 59:243-267.
39. Rocher A.B., Crimins J.L., Amatrudo J.M., Kinson M.S., Todd-Brown M.A., Lewis J., Luebke J.I. Structural and functional changes in tau mutant mice neurons are not linked to the presence of NFTs. Exp. Neurol 2010, 223:385-393.
40. Rocher A.B., Kinson M.S., Luebke J.I. Significant structural but not physiological changes in cortical neurons of 12-month-old Tg2576 mice. Neurobiol. Dis 2008, 32:309-318.
41. Roder S., Danober L., Pozza M.F., Lingenhoehl K., Wiederhold K.H., Olpe H.R. Electrophysiological studies on the hippocampus and prefrontal cortex assessing the effects of amyloidosis in amyloid precursor protein 23 transgenic mice. Neuroscience 2003, 120:705-720.
42. Sabatini B.L., Regehr W.G. Control of neurotransmitter release by presynaptic waveform at the granule cell to Purkinje cell synapse. J. Neurosci 1997, 17:3425-3435.
43. Schorge S., Walker M.C. A self-activating intrinsic brake on bursting in CA3 neurons. J. Physiol 2009, 587:1143-1144.
44. Spencer J.P., Weil A., Hill K., Hussain I., Richardson J.C., Cusdin F.S., Chen Y.H., Randall A.D. Transgenic mice over-expressing human beta-amyloid have functional nicotinic alpha 7 receptors. Neuroscience 2006, 137:795-805.
45. Su H., Sochivko D., Becker A., Chen J., Jiang Y., Yaari Y., Beck H. Upregulation of a T-type Ca2+ channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J. Neurosci 2002, 22:3645-3655.
46. Trinchese F., Liu S., Battaglia F., Walter S., Mathews P.M., Arancio O. Progressive age-related development of Alzheimer-like pathology in APP/PS1 mice. Ann. Neurol 2004, 55:801-814.
47. Vreugdenhil M., Hack S.P., Draguhn A., Jefferys J.G. Tetanus toxin induces long-term changes in excitation and inhibition in the rat hippocampal CA1 area. Neuroscience 2002, 114:983-994.
48. Wang Q., Rowan M.J., Anwyl R. Beta-amyloid-mediated inhibition of NMDA receptor-dependent long-term potentiation induction involves activation of microglia and stimulation of inducible nitric oxide synthase and superoxide. J. Neurosci 2004, 24:6049-6056.
49. Wheeler D.B., Randall A., Tsien R.W. Changes in action potential duration alter reliance of excitatory synaptic transmission on multiple types of Ca2+ channels in rat hippocampus. J. Neurosci 1996, 16:2226-2237.
50. Wittner L., Henze D.A., Zaborszky L., Buzsaki G. Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct. Funct 2007, 212:75-83.
51. Witton J., Brown J.T., Jones M.W., Randall A.D. Altered synaptic plasticity in the mossy fibre pathway of transgenic mice expressing mutant amyloid precursor protein. Mol. Brain 2010, 3:32.
52. Ye C.P., Selkoe D.J., Hartley D.M. Protofibrils of amyloid beta-protein inhibit specific K+ currents in neocortical cultures. Neurobiol. Dis 2003, 13:177-190.
53. Yue C., Remy S., Su H., Beck H., Yaari Y. Proximal persistent Na+ channels drive spike afterdepolarizations and associated bursting in adult CA1 pyramidal cells. J. Neurosci 2005, 25:9704-9720.
54. Yue C., Yaari Y. KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J. Neurosci 2004, 24:4614-4624.
55. Zhao J., Fu Y., Yasvoina M., Shao P., Hitt B., O'Connor T., Logan S., Maus E., Citron M., Berry R., Binder L., Vassar R. Beta-site amyloid precursor protein cleaving enzyme 1 levels become elevated in neurons around amyloid plaques: implications for Alzheimer's disease pathogenesis. J. Neurosci 2007, 27:3639-3649.
56. Ziyatdinova S., Gurevicius K., Kutchiashvili N., Bolkvadze T., Nissinen J., Tanila H., Pitkänen A. Spontaneous epileptiform discharges in a mouse model of Alzheimer's disease are suppressed by antiepileptic drugs that block sodium channels. Epilepsy Res 2011, 94:75-85.