Suppression of InsP3 receptor-mediated Ca2+ signaling alleviates mutant presenilin-linked familial Alzheimer's disease pathogenesis

Journal of Neuroscience

Volumn 34, Issue 20, 2014, Pages 6910-6923

  Shilling, Dustin ^a   Müller, Marioly ^a   Takano, Hajime ^a,b   Mak, Don On Daniel ^a   Abel, Ted ^c   Coulter, Douglas A ^a,b   Foskett, J Kevin ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alzheimer's disease; Amyloid; Calcium; Ion channel; Memory; Mouse model

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; INOSITOL 1, 4, 5 TRISPHOSPHATE RECEPTOR; RYANODINE RECEPTOR; UNCLASSIFIED DRUG; AMYLOID; CALCIUM; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; ION CHANNEL; PRESENILIN 1;

ALZHEIMER DISEASE; AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENE EXPRESSION; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MOUSE; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WESTERN BLOTTING; ANIMAL; BRAIN CORTEX; CALCIUM SIGNALING; DISEASE MODEL; GENETICS; HIPPOCAMPUS; MEMORY; MEMORY DISORDER; METABOLISM; MOUSE MODEL; NERVE CELL;

ALZHEIMER'S DISEASE; AMYLOID; CALCIUM; ION CHANNEL; MEMORY; MOUSE MODEL;

ALZHEIMER DISEASE; ANIMALS; CALCIUM SIGNALING; CEREBRAL CORTEX; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; LONG-TERM POTENTIATION; MEMORY DISORDERS; MICE; NEURONS; PRESENILIN-1; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84900458562     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5441-13.2014     Document Type: Article

References (54)

1. 2+ transients and epileptiform potentials in hippocampal neurons. Neuroreport 14:471-475. Medline
2. 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. CrossRef Medline
3. 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. CrossRef Medline
4. Barco A, Alarcon JM, Kandel ER (2002) Expression of constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108:689-703. CrossRef Medline
5. Berridge MJ (1998) Neuronal calcium signaling. Neuron 21:13-26. CrossRef Medline
6. Bettens K, Sleegers K, Van Broeckhoven C (2013) Genetic insights in Alzheimer's disease. Lancet Neurol 12:92-104. CrossRef Medline
7. Bruno AM, Huang JY, Bennett DA, Marr RA, Hastings ML, Stutzmann GE (2012) Altered ryanodine receptor expression in mild cognitive impairment and Alzheimer's disease. Neurobiol Aging 33:1001. e1-6. CrossRef Medline
8. 2+ channel function as an early preventative strategy for Alzheimer's disease. PLoS One 7:e52056. CrossRef Medline
9. 2+ disruption in Alzheimer's disease by presenilin regulation of InsP3 receptor channel gating. Neuron 58:871-883. CrossRef Medline
10. Cheung KH, Mei L, Mak DO, Hayashi I, Iwatsubo T, Kang DE, Foskett JK (2010) Gain-of-function enhancement of IP3 receptor modal gating by familial Alzheimer's disease-linked presenilin mutants in human cells and mouse neurons. Sci Signal 3:ra22. CrossRef Medline
11. Cirrito JR, Yamada KA, Finn MB, Sloviter RS, Bales KR, May PC, Schoepp DD, Paul SM, Mennerick S, HoltzmanDM (2005) Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 48:913-922. CrossRef Medline
12. ClintonLK, BillingsLM, GreenKN, CaccamoA, NgoJ, OddoS, McGaughJL, La Ferla FM (2007) Age-dependentsexualdimorphismincognitionandstressresponse in the 3xTg-AD mice. Neurobiol Dis 28:76-82. CrossRef Medline
13. 2+release from the endoplasmic reticulum by stimulated production of inositol trisphosphate. J Neurosci 33:3824-3833. CrossRef Medline
14. Dickerson BC, Salat DH, Greve DN, Chua EF, Rand-Giovannetti E, RentzDM, Bertram L, Mullin K, Tanzi RE, Blacker D, Albert MS, Sperling RA (2005) Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 65:404-411. CrossRef Medline
15. Etcheberrigaray R, Hirashima N, Nee L, Prince J, Govoni S, Racchi M, Tanzi RE, Alkon DL (1998) Calcium responses in fibroblasts from asymptomatic members of Alzheimer's disease families. Neurobiol Dis 5:37-45. CrossRef Medline
16. Fukushima H, Maeda R, Suzuki R, Suzuki A, Nomoto M, Toyoda H, Wu LJ, Xu H, Zhao MG, Ueda K, Kitamoto A, Mamiya N, Yoshida T, HommaS, Masushige S, Zhuo M, Kida S (2008) Upregulation of calcium/calmodulindependent protein kinase IV improves memory formation and rescues memory loss with aging. J Neurosci 28:9910-9919. CrossRef Medline
17. Furuichi T, Simon-Chazottes D, Fujino I, Yamada N, Hasegawa M, Miyawaki A, Yoshikawa S, Guénet JL, Mikoshiba K (1993) Widespread expression of inositol 1,4,5-trisphosphate receptor type 1 gene (Insp3r1) in the mouse central nervous system. Receptors Channels 1:11-24. Medline
18. Gonzalez GA, Montminy MR (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59: 675-680. CrossRef Medline
19. Guo Q, Fu W, Sopher BL, Miller MW, Ware CB, Martin GM, Mattson MP (1999) Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knock-in mice. Nat Med 5:101-106. CrossRef Medline
20. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356. CrossRef Medline
21. Hartigan JA, Johnson GV (1999) Transient increases in intracellular calcium result in prolonged site-selective increases in Tau phosphorylation through a glycogen synthase kinase 3beta-dependent pathway. J Biol Chem 274:21395-21401. CrossRef Medline
22. Honarnejad K, Herms J (2012) Presenilins: role in calcium homeostasis. Int J Biochem Cell Biol 44:1983-1986. CrossRef Medline
23. Itkin A, Dupres V, Dufrêne YF, Bechinger B, Ruysschaert JM, Raussens V (2011) Calcium ions promote formation of amyloid beta-peptide (1-40) oligomers causally implicated in neuronal toxicity of Alzheimer's disease. PLoS One 6:e18250. CrossRef Medline
24. La Ferla FM (2002) Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nat Rev Neurosci 3:862-872. CrossRef Medline
25. Lu Y, Christian K, Lu B (2008) BDNF: a key regulator for protein synthesisdependent LTP and long-term memory? Neurobiol Learn Mem 89:312-323. CrossRef Medline
26. Matthews RP, Guthrie CR, Wailes LM, Zhao X, Means AR, McKnight GS (1994) Calcium/calmodulin-dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Mol Cell Biol 14:6107-6116. CrossRef Medline
27. Meberg PJ, Miller MW (2003) Culturing hippocampal and cortical neurons. Methods in Cell Biol 71:111-127. CrossRef Medline
28. Mullane K, WilliamsM (2013) Alzheimer's therapeutics: continued clinical failures question the validity of the amyloid hypothesis-but what lies beyond? Biochem Pharmacol 85:289-305. CrossRef Medline
29. 2+ signaling. Proc Natl Acad Sci U S A 108:13293-13298. CrossRef Medline
30. Nagase T, Ito KI, Kato K, Kaneko K, Kohda K, Matsumoto M, Hoshino A, Inoue T, Fujii S, Kato H, Mikoshiba K (2003) Long-term potentiation and long-term depression in hippocampal CA1 neurons of mice lacking the IP(3) type 1 receptor. Neuroscience 117:821-830. CrossRef Medline
31. Namiki S, Sasaki T, Matsuki N, Ikegaya Y (2009) Regional difference in stainability with calcium-sensitive acetoxymethyl-ester probes in mouse brain slices. Int J Neurosci 119:214-226. CrossRef Medline
32. Noble W, Olm V, Takata K, Casey E, Mary O, Meyerson J, Gaynor K, LaFrancois J, Wang L, Kondo T, Davies P, Burns M, Veeranna, Nixon R, Dickson D, Matsuoka Y, Ahlijanian M, Lau LF, DuffK (2003) Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38:555-565. CrossRef Medline
33. 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. CrossRef Medline
34. Oliveira AM, Hawk JD, Abel T, Havekes R (2010) Post-training reversible inactivation of the hippocampus enhances novel object recognition memory. Learn Mem 17:155-160. CrossRef Medline
35. Oulès B, Del Prete D, Greco B, Zhang X, Lauritzen I, Sevalle J, Moreno S, Paterlini-Bréchot P, Trebak M, Checler F, Benfenati F, Chami M (2012) Ryanodine receptor blockade reduces amyloid-beta load and memory impairments in Tg2576 mouse model of Alzheimer disease. J Neurosci 32:11820-11834. CrossRef Medline
36. Raymond CR, Redman SJ (2006) Spatial segregation of neuronal calcium signals encodes different forms of LTP in rat hippocampus. J Physiol 570:97-111. CrossRef Medline
37. Reiman EM, Quiroz YT, Fleisher AS, Chen K, Velez-Pardo C, Jimenez-Del-Rio M, Fagan AM, Shah AR, Alvarez S, Arbelaez A, Giraldo M, Acosta-Baena N, Sperling RA, Dickerson B, Stern CE, Tirado V, Munoz C, Reiman RA, Huentelman MJ, Alexander GE, Langbaum JB, Kosik KS, Tariot PN, Lopera F (2012) Brain imaging and fluid biomarker analysis in young adults at genetic risk for autosomal dominant Alzheimer's disease in the presenilin 1 E280A kindred: a case-control study. Lancet Neurol 11:1048-1056. CrossRef Medline
38. 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:E2895-2903. CrossRef Medline
39. Schneider I, Reverse D, Dewachter I, Ris L, Caluwaerts N, Kuiperi C, Gilis M, Geerts H, Kretzschmar H, Godaux E, Moechars D, Van Leuven F, Herms J (2001) Mutant presenilins disturb neuronal calcium homeostasis in the brain of transgenic mice, decreasing the threshold for excitotoxicity and facilitating long-term potentiation. J Biol Chem 276:11539-11544. CrossRef Medline
40. 2+-calmodulin-dependent protein kinase Ia kinase. Phosphorylation of threonine 196 is essential for activation. J Biol Chem 270:17616-17621. CrossRef Medline
41. 2+ release in the 3xTg-AD mouse model of Alzheimer's disease. J Neurochem 94:1711-1718. CrossRef Medline
42. Steinert JR, Chernova T, Forsythe ID (2010) Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist 16:435-452. CrossRef Medline
43. Street VA, Bosma MM, Demas VP, Regan MR, Lin DD, Robinson LC, Agnew WS, Tempel BL (1997) The type 1 inositol 1,4,5-trisphosphate receptor gene is altered in the opisthotonos mouse. J Neurosci 17:635-645. Medline
44. 2+ signals and altered membrane excitability. J Neurosci 24:508-513. CrossRef Medline
45. 2+ disruptions in young, adult, and aged Alzheimer's disease mice. J Neurosci 26: 5180-5189. CrossRef Medline
46. 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. AnnN Y Acad Sci 1097:265-277. CrossRef Medline
47. 3 receptors in LTP and LTD induction in guinea pig hippocampal CA1 neurons. LearnMem12:594-600. CrossRef Medline
48. Tseng BP, Green KN, Chan JL, Blurton-Jones M, LaFerla FM (2008) Abeta inhibits the proteasome and enhances amyloid and tau accumulation. Neurobiol Aging 29:1607-1618. CrossRef Medline
49. Turner BM (1998) Histone acetylation as an epigenetic determinant of long-term transcriptional competence. Cell Mol Life Sci 54:21-31. CrossRef Medline
50. 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. CrossRef Medline
51. Wimmer ME, Hernandez PJ, Blackwell J, Abel T (2012) Aging impairs hippocampus-dependent long-term memory for object location in mice. Neurobiol Aging 33:2220-2224. CrossRef Medline
52. Winton MJ, Lee EB, Sun E, Wong MM, Leight S, Zhang B, Trojanowski JQ, LeeVM (2011) Intraneuronal APP, not free Abeta peptides in 3xTg-AD mice: implications for tau versus Abeta-mediated Alzheimer neurodegeneration. J Neurosci 31:7691-7699. CrossRef Medline
53. Woods NK, Padmanabhan J (2012) Neuronal calcium signaling and Alzheimer's disease. Adv Exp Med Biol 740:1193-1217. CrossRef Medline
54. Yin JC, Tully T (1996) CREB and the formation of long-term memory. Curr Opin Neurobiol 6:264-268. CrossRef Medline