Calcium Signaling, Excitability, and Synaptic Plasticity Defects in a Mouse Model of Alzheimer's Disease

Journal of Alzheimer's Disease

Volumn 45, Issue 2, 2015, Pages 561-580

  Zhang, Hua ^a   Liu, Jie ^a   Sun, Suya ^a,b   Pchitskaya, Ekaterina ^c   Popugaeva, Elena ^c   Bezprozvanny, Ilya ^a,c  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c PETER THE GREAT ST PETERSBURG POLYTECHNIC UNIVERSITY   (Russian Federation)

Author keywords

Alzheimer's disease; calcium signaling; excitability; synaptic plasticity

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; AMYLOID BETA PROTEIN[1-42]; ANISOMYCIN; APAMIN; CALCINEURIN; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL; CALCIUM CHANNEL L TYPE; CYTARABINE; DANTROLENE; GLIAL FIBRILLARY ACIDIC PROTEIN; NIFEDIPINE; PICROTOXIN; TACROLIMUS; VOLTAGE GATED CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CENTRAL STIMULANT AGENT; PRESENILIN 1;

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; DENDRITIC SPINE; ELECTRIC POTENTIAL; GLIA CELL; HIPPOCAMPAL NEURONAL CULTURE; IN VITRO STUDY; LONG TERM POTENTIATION; MEMORY CONSOLIDATION; MEMORY DISORDER; MENTAL DETERIORATION; MOUSE; MOUSE MODEL; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SYNAPSE; WHOLE CELL PATCH CLAMP; ANIMAL; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; GENETICS; HIPPOCAMPUS; HUMAN; METABOLISM; MUTATION; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPTIC POTENTIAL; TIME; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM SIGNALING; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM STIMULANTS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEURONAL PLASTICITY; NEURONS; PICROTOXIN; PRESENILIN-1; SYNAPTIC POTENTIALS; TIME FACTORS;

EID: 84925366380     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-142427     Document Type: Article

References (60)

1. Zhou Q, Poo MM (2004) Reversal and consolidation of activity-induced synaptic modifications. Trends Neurosci 27, 378-383.
2. Lisman J, Raghavachari S (2006) A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci STKE 2006, re11.
3. Lynch MA (2004) Long-term potentiation and memory. Physiol Rev 84, 87-136.
4. Raymond CR (2007) LTP forms 1, 2 and 3: Different mechanisms for the "long" in long-term potentiation. Trends Neurosci 30, 167-175.
5. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539.
6. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL (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.
7. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14, 837-842.
8. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2, 271-276.
9. Sun X, Beglopoulos V, Mattson MP, Shen J (2005) Hippocampal spatial memory impairments caused by the familial Alzheimer's disease-linked presenilin 1 M146V mutation. Neurodegener Dis 2, 6-15.
10. Wang R, Dineley KT, Sweatt JD, Zheng H (2004) Presenilin 1 familial Alzheimer's disease mutation leads to defective associative learning and impaired adult neurogenesis. Neuroscience 126, 305-312.
11. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM (2003) Triple-transgenic model of Alzheimer's disease with plaques and tangles: Intracellular Abeta and synaptic dysfunction. Neuron 39, 409-421.
12. Auffret A, Gautheron V, Mattson MP, Mariani J, Rovira C (2010) Progressive age-related impairment of the late long-term potentiation in Alzheimer's disease presenilin-1 mutant knock-in mice. J Alzheimers Dis 19, 1021-1033.
13. Chakroborty S, Goussakov I, Miller MB, Stutzmann GE (2009) Deviant ryanodine receptor-mediated calcium release resets synaptic homeostasis in presymptomatic 3xTg-AD mice. J Neurosci 29, 9458-9470.
14. Frey JU (2010) Continuous blockade of GABA-ergic inhibition induces novel forms of long-lasting plastic changes in apical dendrites of the hippocampal cornu ammonis 1 (CA1) in vitro. Neuroscience 165, 188-197.
15. Arnold FJ, Hofmann F, Bengtson CP, Wittmann M, Vanhoutte P, Bading H (2005) Microelectrode array recordings of cultured hippocampal networks reveal a simple model for transcription and protein synthesis-dependent plasticity. J Physiol 564, 3-19.
16. Wiegert JS, Hofmann F, Bading H, Bengtson CP (2009) A transcription-dependent increase in miniature EPSC frequency accompanies late-phase plasticity in cultured hippocampal neurons. BMC Neurosci 10, 124.
17. Hardingham GE, Arnold FJ, Bading H (2001) A calcium microdomain near NMDA receptors: On switch for ERK-dependent synapse-to-nucleus communication. Nat Neurosci 4, 565-566.
18. Hardingham GE, Arnold FJ, Bading H (2001) Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat Neurosci 4, 261-267.
19. Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5, 405-414.
20. Zhang H, Sun S, Herreman A, De Strooper B, Bezprozvanny I (2010) Role of presenilins in neuronal calcium homeostasis. J Neurosci 30, 8566-8580.
21. Sun S, Zhang H, Liu J, Popugaeva E, Xu N-J, Feske S, White CL, 3rd, Bezprozvanny I (2014) Reduced synaptic STIM2 expression and impaired store-operated calcium entry cause destabilization of mature spines in mutant presenilin mice. Neuron 82, 79-93.
22. Stutzmann GE, Caccamo A, LaFerla FM, Parker I (2004) Dysregulated IP3 signaling in cortical neurons of knock-in mice expressing an Alzheimer's-linked mutation in presenilin1 results in exaggerated Ca2+ signals and altered membrane excitability. J Neurosci 24, 508-513.
23. Stutzmann GE, Smith I, Caccamo A, Oddo S, Parker I, Laferla F (2007) Enhanced ryanodine-mediated calcium release in mutant PS1-expressing Alzheimer's mouse models. Ann N Y Acad Sci 1097, 265-277.
24. Goussakov I, Miller MB, Stutzmann GE (2010) NMDA-mediated Ca(2+) influx drives aberrant ryanodine receptor activation in dendrites of young Alzheimer's disease mice. J Neurosci 30, 12128-12137.
25. Stutzmann GE, Smith I, Caccamo A, Oddo S, Laferla FM, Parker I (2006) Enhanced ryanodine receptor recruitment contributes to Ca2+ disruptions in young, adult, and aged Alzheimer's disease mice. J Neurosci 26, 5180-5189.
26. Chakroborty S, Kim J, Schneider C, Jacobson C, Molgo J, Stutzmann GE (2012) Early presynaptic and postsynaptic calcium signaling abnormalities mask underlying synaptic depression in presymptomatic Alzheimer's disease mice. J Neurosci 32, 8341-8353.
27. Kumar A, Foster TC (2004) Enhanced long-term potentiation during aging is masked by processes involving intracellular calcium stores. J Neurophysiol 91, 2437-2444.
28. Gant JC, Sama MM, Landfield PW, Thibault O (2006) Early and simultaneous emergence of multiple hippocampal biomarkers of aging is mediated by Ca2+-induced Ca2+ release. J Neurosci 26, 3482-3490.
29. Bodhinathan K, Kumar A, Foster TC (2010) Redox sensitive calcium stores underlie enhanced after hyperpolarization of aged neurons: Role for ryanodine receptor mediated calcium signaling. J Neurophysiol 104, 2586-2593.
30. Bodhinathan K, Kumar A, Foster TC (2010) Intracellular redox state alters NMDA receptor response during aging through Ca2+/calmodulin-dependent protein kinase II. J Neurosci 30, 1914-1924.
31. Burke SN, Barnes CA (2006) Neural plasticity in the ageing brain. Nat Rev Neurosci 7, 30-40.
32. Rodriguez A, Ehlenberger DB, Dickstein DL, Hof PR, Wearne SL (2008) Automated three-dimensional detection and shape classification of dendritic spines from fluorescence microscopy images. PLoS One 3, e1997.
33. Kasumu AW, Hougaard C, Rode F, Jacobsen TA, Sabatier JM, Eriksen BL, Strobaek D, Liang X, Egorova P, Vorontsova D, Christophersen P, Ronn LC, Bezprozvanny I (2012) Selective positive modulator of calcium-activated potassium channels exerts beneficial effects in a mouse model of spinocerebellar ataxia type 2. Chem Biol 19, 1340-1353.
34. Kasumu AW, Liang X, Egorova P, Vorontsova D, Bezprozvanny I (2012) Chronic suppression of inositol 1,4,5-triphosphate receptor-mediated calcium signaling in cerebellar purkinje cells alleviates pathological phenotype in spinocerebellar ataxia 2 mice. J Neurosci 32, 12786-12796.
35. Murakoshi H, Yasuda R (2012) Postsynaptic signaling during plasticity of dendritic spines. Trends Neurosci 35, 135-143.
36. Matsuzaki M (2007) Factors critical for the plasticity of dendritic spines and memory storage. Neurosci Res 57, 1-9.
37. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749-757.
38. Bourne J, Harris KM (2007) Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol 17, 381-386.
39. Kasai H, Matsuzaki M, Noguchi J, Yasumatsu N, Nakahara H (2003) Structure-stability-function relationships of dendritic spines. Trends Neurosci 26, 360-368.
40. Bond CT, Herson PS, Strassmaier T, Hammond R, Stackman R, Maylie J, Adelman JP (2004) Small conductance Ca2+-activated K+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci 24, 5301-5306.
41. Pedarzani P, McCutcheon JE, Rogge G, Jensen BS, Christophersen P, Hougaard C, Strobaek D, Stocker M (2005) Specific enhancement of SK channel activity selectively potentiates the afterhyperpolarizing current I(AHP) and modulates the firing properties of hippocampal pyramidal neurons. J Biol Chem 280, 41404-41411.
42. Liu J, Supnet C, Sun S, Zhang H, Good L, Popugaeva E, Bezprozvanny I (2014) The role of ryanodine receptor type 3 in a mouse model of Alzheimer disease. Channels (Austin) 8, 230-242.
43. Krause T, Gerbershagen MU, Fiege M, Weisshorn R, Wappler F (2004) Dantrolene - a review of its pharmacology, therapeutic use and new developments. Anaesthesia 59, 364-373.
44. Obenaus A, Mody I, Baimbridge KG (1989) Dantrolene-Na (Dantrium) blocks induction of long-term potentiation in hippocampal slices. Neurosci Lett 98, 172-178.
45. Pratt KG, Zimmerman EC, Cook DG, Sullivan JM (2011) Presenilin 1 regulates homeostatic synaptic scaling through Akt signaling. Nat Neurosci 14, 1112-1114.
46. Redondo RL, Morris RG (2011) Making memories last: The synaptic tagging and capture hypothesis. Nat Rev Neurosci 12, 17-30.
47. Dudek SM, Fields RD (2002) Somatic action potentials are sufficient for late-phase LTP-related cell signaling. Proc Natl Acad Sci U S A 99, 3962-3967.
48. Raymond CR (2008) Different requirements for action potentials in the induction of different forms of long-term potentiation. J Physiol 586, 1859-1865.
49. McHugh TJ, Blum KI, Tsien JZ, Tonegawa S, Wilson MA (1996) Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87, 1339-1349.
50. Buzsaki G, Buhl DL, Harris KD, Csicsvari J, Czeh B, Morozov A (2003) Hippocampal network patterns of activity in the mouse. Neuroscience 116, 201-211.
51. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55, 697-711.
52. Palop JJ, Mucke L (2010) Synaptic depression and aberrant excitatory network activity in Alzheimer's disease: Two faces of the same coin? Neuromolecular Med 12, 48-55.
53. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, Staufenbiel M, Konnerth A, Garaschuk O (2008) Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 321, 1686-1689.
54. Minkeviciene R, Rheims S, Dobszay MB, Zilberter M, Hartikainen J, Fulop L, Penke B, Zilberter Y, Harkany T, Pitkanen A, Tanila H (2009) Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. J Neurosci 29, 3453-3462.
55. Palop JJ, Mucke L (2010) Amyloid-beta-induced neuronal dysfunction in Alzheimer's disease: From synapses toward neural networks. Nat Neurosci 13, 812-818.
56. Verret L, Mann EO, Hang GB, Barth AM, Cobos I, Ho K, Devidze N, Masliah E, Kreitzer AC, Mody I, Mucke L, Palop JJ (2012) Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149, 708-721.
57. Sanchez PE, Zhu L, Verret L, Vossel KA, Orr AG, Cirrito JR, Devidze N, Ho K, Yu GQ, Palop JJ, Mucke L (2012) Levetiracetam suppresses neuronal network dysfunction and reverses synaptic and cognitive deficits in an Alzheimer's disease model. Proc Natl Acad Sci U S A 109, E2895-E2903.
58. Bakker A, Krauss GL, Albert MS, Speck CL, Jones LR, Stark CE, Yassa MA, Bassett SS, Shelton AL, Gallagher M (2012) Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 74, 467-474.
59. Oh MM, Oliveira FA, Disterhoft JF (2010) Learning and aging related changes in intrinsic neuronal excitability. Front Aging Neurosci 2, 2.
60. Foster TC (2007) Calcium homeostasis and modulation of synaptic plasticity in the aged brain. Aging Cell 6, 319-325.