Calcium dysregulation in Alzheimer's disease: Recent advances gained from genetically modified animals

Cell Calcium

Volumn 38, Issue 3-4 SPEC. ISS., 2005, Pages 427-437

  Smith, Ian F ^a   Green, Kim N ^a   LaFerla, Frank M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's; Alzheimer's disease; Amyloid; Calcium dysregulation; Presenilin; Transgenic

Indexed keywords

AMYLOID BETA PROTEIN; CALCIUM ION; DNA; PRESENILIN 1; PRESENILIN 2;

ALZHEIMER DISEASE; BEHAVIOR DISORDER; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CELL LINE; CELL LOSS; CELL TYPE; COGNITIVE DEFECT; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; DISEASE COURSE; DNA MODIFICATION; EVIDENCE BASED MEDICINE; GENE MUTATION; HUMAN; MEDICAL RESEARCH; MEMORY DISORDER; MOUSE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SENILE PLAQUE; SYNAPTIC TRANSMISSION;

ANIMALIA; MUS MUSCULUS;

EID: 24644456470     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceca.2005.06.021     Document Type: Article

References (109)

1. Y.H. Suh F. Checler Amyloid precursor protein, presenilins, and alpha-synuclein: Molecular pathogenesis and pharmacological applications in Alzheimer's disease Pharmacol. Rev. 54 2002 469-525
2. A. Alzheimer, About a peculiar disease of the cerebral cortex. Translated 1987 by L. Jarvik and H. Greenson. Alzheimer Dis. Assoc. Disord., 1907, 3-8.
3. K. Ogomori T. Kitamoto J. Tateishi Y. Sato M. Suetsugu M. Abe Beta-protein amyloid is widely distributed in the central nervous system of patients with Alzheimer's disease Am. J. Pathol. 134 1989 243-251
4. J. Hardy D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353-356
5. S. Oddo L. Billings J.P. Kesslak D.H. Cribbs F.M. LaFerla Aβ immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome Neuron. 43 2004 321-332
6. D.L. Price R.E. Tanzi D.R. Borchelt S.S. Sisodia Alzheimer's disease: genetic studies and transgenic models Annu. Rev. Genet. 32 1998 461-493
7. L.M. Billings S. Oddo K.N. Green J.L. McGaugh F.M. LaFerla Intraneuronal Aβ causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice Neuron 45 2005 675-688
8. F.M. LaFerla Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease Nat. Rev. Neurosci. 3 2002 862-872
9. M. Shoji T.E. Golde J. Ghiso T.T. Cheung S. Estus L.M. Shaffer X.D. Cai D.M. McKay R. Tintner B. Frangione et al. Production of the Alzheimer amyloid beta protein by normal proteolytic processing Science 258 1992 126-129
10. J.D. Buxbaum K.N. Liu Y. Luo J.L. Slack K.L. Stocking J.J. Peschon R.S. Johnson B.J. Castner D.P. Cerretti R.A. Black Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor J. Biol. Chem. 273 1998 27765-27767
11. S. Lammich E. Kojro R. Postina S. Gilbert R. Pfeiffer M. Jasionowski C. Haass F. Fahrenholz Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease Proc. Natl. Acad. Sci. USA 96 1999 3922-3927
12. R. Vassar B.D. Bennett S. Babu-Khan S. Kahn E.A. Mendiaz P. Denis D.B. Teplow S. Ross P. Amarante R. Loeloff Y. Luo S. Fisher J. Fuller S. Edenson J. Lile M.A. Jarosinski A.L. Biere E. Curran T. Burgess J.C. Louis F. Collins J. Treanor G. Rogers M. Citron Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE Science 286 1999 735-741
13. I. Hussain D. Powell D.R. Howlett D.G. Tew T.D. Meek C. Chapman I.S. Gloger K.E. Murphy C.D. Southan D.M. Ryan T.S. Smith D.L. Simmons F.S. Walsh C. Dingwall G. Christie Identification of a novel aspartic protease (Asp 2) as beta-secretase Mol. Cell Neurosci. 14 1999 419-427
14. S. Sinha J.P. Anderson R. Barbour G.S. Basi R. Caccavello D. Davis M. Doan H.F. Dovey N. Frigon J. Hong K. Jacobson-Croak N. Jewett P. Keim J. Knops I. Lieberburg M. Power H. Tan G. Tatsuno J. Tung D. Schenk P. Seubert S.M. Suomensaari S. Wang D. Walker J. Zhao L. McConlogue V. John Purification and cloning of amyloid precursor protein beta-secretase from human brain Nature 402 1999 537-540
15. H. Steiner E. Winkler D. Edbauer S. Prokop G. Basset A. Yamasaki M. Kostka C. Haass PEN-2 is an integral component of the gamma-secretase complex required for coordinated expression of presenilin and nicastrin J. Biol. Chem. 277 2002 39062-39065
16. R. Francis G. McGrath J. Zhang D.A. Ruddy M. Sym J. Apfeld M. Nicoll M. Maxwell B. Hai M.C. Ellis A.L. Parks W. Xu J. Li M. Gurney R.L. Myers C.S. Himes R. Hiebsch C. Ruble J.S. Nye D. Curtis aph-1 and pen-2 are required for Notch pathway signaling, gamma-secretase cleavage of betaAPP, and presenilin protein accumulation Dev. Cell 3 2002 85-97
17. D. Levitan J. Lee L. Song R. Manning G. Wong E. Parker L. Zhang PS1 N- and C-terminal fragments form a complex that functions in APP processing and Notch signalling Proc. Natl. Acad. Sci. USA 98 2001 12186-12190
18. B. De Strooper P. Saftig K. Craessaerts H. Vanderstichele G. Guhde W. Annaert K. Von Figura F. Van Leuven Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein Nature 391 1998 387-390
19. C. Haass A.Y. Hung M.G. Schlossmacher D.B. Teplow D.J. Selkoe beta-Amyloid peptide and a 3-kDa fragment are derived by distinct cellular mechanisms J. Biol. Chem. 268 1993 3021-3024
20. J.T. Jarrett E.P. Berger P.T. Lansbury Jr. The carboxy terminus of the beta amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease Biochemistry 32 1993 4693-4697
21. C.C. Glabe Amyloid accumulation and pathogensis of Alzheimer's disease: significance of monomeric, oligomeric and fibrillar Abeta Subcell. Biochem. 38 2005 167-177
22. R. Sherrington E.I. Rogaev Y. Liang E.A. Rogaeva G. Levesque M. Ikeda H. Chi C. Lin G. Li K. Holman et al. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease Nature 375 1995 754-760
23. E. Levy-Lahad W. Wasco P. Poorkaj D.M. Romano J. Oshima W.H. Pettingell C.E. Yu P.D. Jondro S.D. Schmidt K. Wang et al. Candidate gene for the chromosome 1 familial Alzheimer's disease locus Science 269 1995 973-977
24. D.J. Selkoe M.B. Podlisny Deciphering the genetic basis of Alzheimer's disease Annu. Rev. Genomics Hum. Genet. 3 2002 67-99
25. D. Scheuner C. Eckman M. Jensen X. Song M. Citron N. Suzuki T.D. Bird J. Hardy M. Hutton W. Kukull E. Larson E. Levy-Lahad M. Viitanen E. Peskind P. Poorkaj G. Schellenberg R. Tanzi W. Wasco L. Lannfelt D. Selkoe S. Younkin Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease Nat. Med. 2 1996 864-870
26. Q. Guo K. Furukawa B.L. Sopher D.G. Pham J. Xie N. Robinson G.M. Martin M.P. Mattson Alzheimer's PS-1 mutation perturbs calcium homeostasis and sensitizes PC12 cells to death induced by amyloid beta-peptide Neuroreport 8 1996 379-383
27. Q. Guo S. Christakos N. Robinson M.P. Mattson Calbindin D28k blocks the proapoptotic actions of mutant presenilin 1: Reduced oxidative stress and preserved mitochondrial function Proc. Natl. Acad. Sci. USA 95 1998 3227-3232
28. M.A. Leissring Y. Akbari C.M. Fanger M.D. Cahalan M.P. Mattson F.M. LaFerla Capacitative calcium entry deficits and elevated luminal calcium content in mutant presenilin-1 knockin mice J. Cell Biol. 149 2000 793-798
29. M.A. Leissring B.A. Paul I. Parker C.W. Cotman F.M. LaFerla Alzheimer's presenilin-1 mutation potentiates inositol 1,4,5-trisphosphate-mediated calcium signaling in Xenopus oocytes J. Neurochem. 72 1999 1061-1068
30. M.A. Leissring I. Parker F.M. LaFerla Presenilin-2 mutations modulate amplitude and kinetics of inositol 1,4,5-trisphosphate-mediated calcium signals J. Biol. Chem. 274 1999 32535-32538
31. M.A. Leissring M.P. Murphy T.R. Mead Y. Akbari M.C. Sugarman M. Jannatipour B. Anliker U. Muller P. Saftig B. De Strooper M.S. Wolfe T.E. Golde F.M. LaFerla A physiologic signaling role for the gamma -secretase-derived intracellular fragment of APP Proc. Natl. Acad. Sci. USA 99 2002 4697-4702
32. Q. Guo W. Fu B.L. Sopher M.W. Miller C.B. Ware G.M. Martin M.P. Mattson Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knock-in mice Nat. Med. 5 1999 101-106
33. S.L. Chan M. Mayne C.P. Holden J.D. Geiger M.P. Mattson Presenilin-1 mutations increase levels of ryanodine receptors and calcium release in PC12 cells and cortical neurons J. Biol. Chem. 275 2000 18195-18200
34. G.E. Stutzmann A. Caccamo F.M. LaFerla I. Parker Dysregulated IP3 signaling in cortical neurons of knock-in mice expressing an Alzheimer's-linked mutation in presenilin1 results in exaggerated calcium signals and altered membrane excitability J. Neurosci. 24 2004 508-513
35. C.R. Rose A. Konnerth Stores not just for storage. intracellular calcium release and synaptic plasticity Neuron 31 2001 519-522
36. P.A. Barrow R.M. Empson S.J. Gladwell C.M. Anderson R. Killick X. Yu J.G. Jefferys K. Duff Functional phenotype in transgenic mice expressing mutant human presenilin-1 Neurobiol. Dis. 7 2000 119-126
37. A. Parent D.J. Linden S.S. Sisodia D.R. Borchelt Synaptic transmission and hippocampal long-term potentiation in transgenic mice expressing FAD-linked presenilin 1 Neurobiol. Dis. 6 1999 56-62
38. S. Oddo A. Caccamo J.D. Shepherd M.P. Murphy T.E. Golde R. Kayed R. Metherate M.P. Mattson Y. Akbari F.M. LaFerla Triple-transgenic model of Alzheimer's disease with plaques and tangles: Intracellular Aβ and synaptic dysfunction Neuron. 39 2003 409-421
39. I.F. Smith. B. Hitt, K.N. Green, S. Oddo, F.M. LaFerla, Enhanced caffeine-induced calcium release in the 3xTg-AD model of Alzheimer's disease. J. Neurochem. 2005, in press.
40. R. Etcheberrigaray N. Hirashima L. Nee J. Prince S. Govoni M. Racchi R.E. Tanzi D.L. Alkon Calcium responses in fibroblasts from asymptomatic members of Alzheimer's disease families Neurobiol. Dis. 5 1998 37-45
41. R.S. Zucker W.G. Regehr Short-term synaptic plasticity Annu. Rev. Physiol. 64 2002 355-405
42. A.M. Thomson Facilitation, augmentation and potentiation at central synapses Trends Neurosci. 23 2000 305-312
43. T.V. Bliss G.L. Collingridge A synaptic model of memory: Long-term potentiation in the hippocampus Nature 361 1993 31-39
44. F. Kamenetz T. Tomita H. Hsieh G. Seabrook D. Borchelt T. Iwatsubo S. Sisodia R. Malinow APP processing and synaptic function Neuron 37 2003 925-937
45. D.M. Walsh I. Klyubin J.V. Fadeeva W.K. Cullen R. Anwyl M.S. Wolfe M.J. Rowan D.J. Selkoe Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo Nature 416 2002 535-539
46. I. Klyubin D.M. Walsh C.A. Lemere W.K. Cullen G.M. Shankar V. Betts E.T. Spooner L. Jiang R. Anwyl D.J. Selkoe M.J. Rowan Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo Nat. Med. 2005
47. B. Passer L. Pellegrini C. Russo R.M. Siegel M.J. Lenardo G. Schettini M. Bachmann M. Tabaton L. D'Adamio Generation of an apoptotic intracellular peptide by gamma-secretase cleavage of Alzheimer's amyloid beta protein precursor J. Alzheimers Dis. 2 2000 289-301
48. J. Herms I. Schneider I. Dewachter N. Caluwaerts H. Kretzschmar F. Van Leuven Capacitive calcium entry is directly attenuated by mutant presenilin-1, independent of the expression of the amyloid precursor protein J. Biol. Chem. 278 2003 2484-2489
49. Y. Akbari B.D. Hitt M.P. Murphy N.N. Dagher B.P. Tseng K.N. Green T.E. Golde F.M. LaFerla Presenilin regulates capacitative calcium entry dependently and independently of gamma-secretase activity Biochem. Biophys. Res. Commun. 322 2004 1145-1152
50. M.P. Mattson Pathways towards and away from Alzheimer's disease Nature 430 2004 631-639
51. T.V. Bliss T. Lomo Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path J. Physiol. 232 1973 331-356
52. S.M. Fitzjohn G.L. Collingridge Calcium stores and synaptic plasticity Cell Calcium 32 2002 405-411
53. K. Ueda S. Shinohara T. Yagami K. Asakura K. Kawasaki Amyloid beta protein potentiates Calcium influx through L-type voltage-sensitive Calcium channels: A possible involvement of free radicals J. Neurochem. 68 1997 265-271
54. J. Wu R. Anwyl M.J. Rowan beta-Amyloid selectively augments NMDA receptor-mediated synaptic transmission in rat hippocampus Neuroreport 6 1995 2409-2413
55. J.J. Dougherty J. Wu R.A. Nichols Beta-amyloid regulation of presynaptic nicotinic receptors in rat hippocampus and neocortex J. Neurosci. 23 2003 6740-6747
56. (1-40)] in bilayer membranes Proc. Natl. Acad. Sci. USA 90 1993 10573-10577
57. I.F. Smith J.P. Boyle P.F. Vaughan H.A. Pearson C. Peers Effects of chronic hypoxia on calcium stores and capacitative calcium entry in human neuroblastoma (SH-SY5Y) cells J. Neurochem. 79 2001 877-884
58. R.J. Mark K. Hensley D.A. Butterfield M.P. Mattson Amyloid beta-peptide impairs ion-motive ATPase activities: Evidence for a role in loss of neuronal calcium homeostasis and cell death J. Neurosci. 15 1995 6239-6249
59. C.S. Casley J.M. Land M.A. Sharpe J.B. Clark M.R. Duchen L. Canevari Beta-amyloid fragment 25-35 causes mitochondrial dysfunction in primary cortical neurons Neurobiol. Dis. 10 2002 258-267
60. E. Boitier R. Rea M.R. Duchen Mitochondria exert a negative feedback on the propagation of intracellular calcium waves in rat cortical astrocytes J. Cell Biol. 145 1999 795-808
61. M.J. Berridge M.D. Bootman H.L. Roderick Calcium signalling: Dynamics, homeostasis and remodelling Nat. Rev. Mol. Cell Biol. 4 2003 517-529
62. Y.J. Zhu H. Lin R. Lal Fresh and nonfibrillar amyloid beta protein(1-40) induces rapid cellular degeneration in aged human fibroblasts: Evidence for AbetaP-channel-mediated cellular toxicity Faseb. J. 14 2000 1244-1254
63. J.R. Brorson V.P. Bindokas T. Iwama C.J. Marcuccilli J.C. Chisholm R.J. Miller The calcium influx induced by beta-amyloid peptide 25-35 in cultured hippocampal neurons results from network excitation J. Neurobiol. 26 1995 325-338
64. J.H. Weiss C.J. Pike C.W. Cotman Calcium channel blockers attenuate beta-amyloid peptide toxicity to cortical neurons in culture J. Neurochem. 62 1994 372-375
65. R.M. Davidson L. Shajenko T.S. Donta Amyloid beta-peptide Aβ potentiates a nimodipine-sensitive L-type barium conductance in N1E-115 neuroblastoma cells Brain Res. 643 1994 324-327
66. F.J. Ekinci K.U. Malik T.B. Shea Activation of the L voltage-sensitive calcium channel by mitogen-activated protein (MAP) kinase following exposure of neuronal cells to beta-amyloid. MAP kinase mediates beta-amyloid-induced neurodegeneration J. Biol. Chem. 274 1999 30322-30327
67. K.N. Green C. Peers Divergent pathways account for two distinct effects of amyloid beta peptides on exocytosis and calcium currents: Involvement of ROS and NF-kappaB J. Neurochem. 81 2002 1043-1051
68. S.T. Brown J.L. Scragg J.P. Boyle K. Hudasek C. Peers I.M. Fearon Hypoxic augmentation of calcium channel currents requires a functional electron transport chain J. Biol. Chem. 2005
69. W.R. Markesbery J.M. Carney Oxidative alterations in Alzheimer's disease Brain Pathol. 9 1999 133-146
70. R.J. Mark M.A. Lovell W.R. Markesbery K. Uchida M.P. Mattson A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide J. Neurochem. 68 1997 255-264
71. J.N. Keller Z. Pang J.W. Geddes J.G. Begley A. Germeyer G. Waeg M.P. Mattson Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid beta-peptide: Role of the lipid peroxidation product 4-hydroxynonenal J. Neurochem. 69 1997 273-284
72. C. Lu S.L. Chan W. Fu M.P. Mattson The lipid peroxidation product 4-hydroxynonenal facilitates opening of voltage-dependent calcium channels in neurons by increasing protein tyrosine phosphorylation J. Biol. Chem. 277 2002 24368-24375
73. J.L. Scragg I.M. Fearon J.P. Boyle S.G. Ball G. Varadi C. Peers Alzheimer's amyloid peptides mediate hypoxic up-regulation of L-type calcium channels Faseb. J. 19 2005 150-152
74. (45)calcium influx and voltage-dependent calcium channel activity by beta-amyloid-(1-40) in rat cortical synaptosomes and cultured cortical neurons. Modulation by the proinflammatory cytokine interleukin-1beta J. Biol. Chem. 275 2000 4713-4718
75. + channel currents in primary cultures of rat cerebellar granule and cortical neurones J. Neurochem. 79 2001 699-712
76. M. Kawahara Y. Kuroda N. Arispe E. Rojas Alzheimer's beta-amyloid, human islet amylin, and prion protein fragment evoke intracellular free calcium elevations by a common mechanism in a hypothalamic GnRH neuronal cell line J. Biol. Chem. 275 2000 14077-14083
77. 2+-sensitive, cation-selective channels across excised membrane patches from hypothalamic neurons Biophys. J. 73 1997 67-75
78. 2+ interaction with Alzheimer amyloid beta protein calcium channels Proc. Natl. Acad. Sci. USA 93 1996 1710-1715
79. N. Arispe E. Rojas H.B. Pollard Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: Blockade by tromethamine and aluminium Proc. Natl. Acad. Sci. USA 90 1993 567-571
80. 2+-sensitive channel J. Biol. Chem. 273 1998 13379-13382
81. H.B. Pollard N. Arispe E. Rojas Ion channel hypothesis for Alzheimer amyloid peptide neurotoxicity Cell Mol. Neurobiol. 15 1995 513-526
82. N. Arispe H.B. Pollard E. Rojas beta-Amyloid calcium-channel hypothesis for neuronal death in Alzheimer disease Mol. Cell Biochem. 140 1994 119-125
83. T. Nakagawa H. Zhu N. Morishima E. Li J. Xu B.A. Yankner J. Yuan Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta Nature 403 2000 98-103
84. S.C. Taylor T.F. Batten C. Peers Hypoxic enhancement of quantal catecholamine secretion. Evidence for the involvement of amyloid beta-peptides J. Biol. Chem. 274 1999 31217-31222
85. K.N. Green C. Peers Amyloid beta peptides mediate hypoxic augmentation of calcium channels J. Neurochem. 77 2001 953-956
86. A. Demuro E. Mina R. Kayed S.C. Milton I. Parker C.G. Glabe Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers J. Biol. Chem. 280 2005 17294-17300
87. J.G. Begley W. Duan S. Chan K. Duff M.P. Mattson Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice J. Neurochem. 72 1999 1030-1039
88. Q. Guo L. Sebastian B.L. Sopher M.W. Miller C.B. Ware G.M. Martin M.P. Mattson Increased vulnerability of hippocampal neurons from presenilin-1 mutant knock-in mice to amyloid beta-peptide toxicity: Central roles of superoxide production and caspase activation J. Neurochem. 72 1999 1019-1029
89. D.H. Chui H. Tanahashi K. Ozawa S. Ikeda F. Checler O. Ueda H. Suzuki W. Araki H. Inoue K. Shirotani K. Takahashi F. Gallyas T. Tabira Transgenic mice with Alzheimer presenilin 1 mutations show accelerated neurodegeneration without amyloid plaque formation Nat. Med. 5 1999 560-564
90. G.E. Gibson H. Zhang L. Toral-Barza S. Szolosi B. Tofel-Grehl Calcium stores in cultured fibroblasts and their changes with Alzheimer's disease Biochim. Biophys. Acta 1316 1996 71-77
91. G.E. Gibson P. Nielsen K.A. Sherman J.P. Blass Diminished mitogen-induced calcium uptake by lymphocytes from Alzheimer patients Biol. Psychiatry 22 1987 1079-1086
92. N. Hirashima R. Etcheberrigaray S. Bergamaschi M. Racchi F. Battaini G. Binetti S. Govoni D.L. Alkon Calcium responses in human fibroblasts: A diagnostic molecular profile for Alzheimer's disease Neurobiol. Aging 17 1996 549-555
93. C. Peterson R.R. Ratan M.L. Shelanski J.E. Goldman Cytosolic free calcium and cell spreading decrease in fibroblasts from aged and Alzheimer donors Proc. Natl. Acad. Sci. USA 83 1986 7999-8001
94. C. Peterson G.E. Gibson J.P. Blass Altered calcium uptake in cultured skin fibroblasts from patients with Alzheimer's disease N Engl J Med 312 1985 1063-1065
95. C. Peterson J.E. Goldman Alterations in calcium content and biochemical processes in cultured skin fibroblasts from aged and Alzheimer donors Proc. Natl. Acad. Sci. USA 83 1986 2758-2762
96. C. Peterson R.R. Ratan M.L. Shelanski J.E. Goldman Altered response of fibroblasts from aged and Alzheimer donors to drugs that elevate cytosolic free calcium Neurobiol. Aging 9 1988 261-266
97. C. Peterson R. Ratan M. Shelanski J. Goldman Changes in calcium homeostasis during aging and Alzheimer's disease Ann. N Y Acad. Sci. 568 1989 262-270
98. Y. Tatebayashi M. Takeda Y. Kashiwagi M. Okochi T. Kurumadani A. Sekiyama G. Kanayama S. Hariguchi T. Nishimura Cell-cycle-dependent abnormal calcium response in fibroblasts from patients with familial Alzheimer's disease Dementia 6 1995 9-16
99. Q. Guo B.L. Sopher K. Furukawa D.G. Pham N. Robinson G.M. Martin M.P. Mattson Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid beta-peptide: involvement of calcium and oxyradicals J. Neurosci. 17 1997 4212-4222
100. J.N. Keller Q. Guo F.W. Holtsberg A.J. Bruce-Keller M.P. Mattson Increased sensitivity to mitochondrial toxin-induced apoptosis in neural cells expressing mutant presenilin-1 is linked to perturbed calcium homeostasis and enhanced oxyradical production J. Neurosci. 18 1998 4439-4450
101. K. Furukawa Q. Guo G.D. Schellenberg M.P. Mattson Presenilin-1 mutation alters NGF-induced neurite outgrowth, calcium homeostasis, and transcription factor (AP-1) activation in PC12 cells J. Neurosci. Res. 52 1998 618-624
102. B.O. Popescu A. Cedazo-Minguez L.M. Popescu B. Winblad R.F. Cowburn M. Ankarcrona Caspase cleavage of exon 9 deleted presenilin-1 is an early event in apoptosis induced by calcium ionophore A 23187 in SH-SY5Y neuroblastoma cells J. Neurosci. Res. 66 2001 122-134
103. I.F. Smith, J.P. Boyle, P.F.T. Vaughan, H.A. Pearson, R.F. Cowburn, C.S. Peers, Calcium stores and capacitative calcium entry in human neuroblastoma (SH-SY5Y) cells expressing a familial Alzheimer's disease presenilin-1 mutation. Brain Res. 949 (2002) 105-111.
104. A. Cedazo-Minguez B.O. Popescu M. Ankarcrona T. Nishimura R.F. Cowburn The presenilin 1 {capital delta}E9 mutation gives enhanced basal phospholipase C activity and a resultant increase in intracellular calcium concentrations J. Biol. Chem. 2002
105. A.S. Yoo I. Cheng S. Chung T.Z. Grenfell H. Lee E. Pack-Chung M. Handler J. Shen W. Xia G. Tesco A.J. Saunders K. Ding M.P. Frosch R.E. Tanzi T.W. Kim Presenilin-mediated modulation of capacitative calcium entry Neuron 27 2000 561-572
106. M. Nakajima M. Miura T. Aosaki T. Shirasawa Deficiency of presenilin-1 increases calcium-dependent vulnerability of neurons to oxidative stress in vitro J. Neurochem. 78 2001 807-814
107. C.B. Lessard M.P. Lussier S. Cayouette G. Bourque G. Boulay The overexpression of presenilin2 and Alzheimer's-disease-linked presenilin2 variants influences TRPC6-enhanced calcium entry into HEK293 cells Cell Signal 17 2005 437-445
108. I. Schneider D. Reverse I. Dewachter L. Ris N. Caluwaerts C. Kuiperi M. Gilis H. Geerts H. Kretzschmar E. Godaux D. Moechars F. Van Leuven J. Herms 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 2001 11539-11544
109. G. Zatti R. Ghidoni L. Barbiero G. Binetti T. Pozzan C. Fasolato P. Pizzo The presenilin 2 M239I mutation associated with familial Alzheimer's disease reduces calcium release from intracellular stores Neurobiol. Dis. 15 2004 269-278