Intracellular Calcium Dysregulation: Implications for Alzheimer's Disease

BioMed Research International

Volumn 2016, Issue , 2016, Pages

  Magi, Simona ^a   Castaldo, Pasqualina ^a   MacRi, Maria Loredana ^a   Maiolino, Marta ^a   Matteucci, Alessandra ^a   Bastioli, Guendalina ^a   Gratteri, Santo ^b   Amoroso, Salvatore ^a   Lariccia, Vincenzo ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; SODIUM CALCIUM EXCHANGE PROTEIN; AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; CALCIUM BALANCE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CELL FUNCTION; CYTOSOL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; MITOCHONDRION; NONHUMAN; PATHOGENESIS; REVIEW; AMYLOID PLAQUE; CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; GENETICS; METABOLISM; NERVE CELL; OXIDATIVE STRESS; PATHOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; CALCIUM; CALCIUM SIGNALING; ENDOPLASMIC RETICULUM; HUMANS; MITOCHONDRIA; NEURONS; OXIDATIVE STRESS; PLAQUE, AMYLOID;

EID: 84975291015     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2016/6701324     Document Type: Review

References (145)

1. C. Ballard, S. Gauthier, A. Corbett, C. Brayne, D. Aarsland, E. Jones, "Alzheimer's disease,"TheLancet, vol. 377, no. 9770, pp. 1019-1031, 2011.
2. C. Reitz and R. Mayeux, "Alzheimer disease: epidemiology, diagnostic criteria, risk factors and biomarkers," Biochemical Pharmacology, vol. 88, no. 4, pp. 640-651, 2014.
3. Alzheimer's Association, "2013 Alzheimer's disease facts and figures," Alzheimer's&Dementia, vol. 9, no. 2,pp. 208-245, 2013.
4. S. M. Bonomo, A. E. Rigamonti, M. Giunta et al., "Menopausal transition: a possible risk factor for brain pathologic events," Neurobiology of Aging, vol. 30, no. 1, pp. 71-80, 2009.
5. C. J. Pike, J. C. Carroll, E. R. Rosario, A. M. Barron, "Protective actions of sex steroid hormones in Alzheimer's disease," Frontiers inNeuroendocrinology, vol. 30,no. 2, pp. 239-258, 2009.
6. D. P. Srivastava, K. M. Woolfrey, P. Penzes, "Insights into rapid modulation of neuroplasticity by brain estrogens," Pharmacological Reviews, vol. 65, no. 4, pp. 1318-1350, 2013.
7. F. M. LaFerla, "Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease," Nature Reviews Neuroscience, vol. 3, no. 11, pp. 862-872, 2002.
8. J. McInnes, "Insights on altered mitochondrial function and dynamics in the pathogenesis of neurodegeneration," Translational Neurodegeneration, vol. 2, no. 1, article 12, 2013.
9. D. Sepulveda-Falla, A. Barrera-Ocampo, C.Hagel et al., "Familial Alzheimer's disease-associated presenilin-1 alters cerebellar activity and calcium homeostasis," The Journal of Clinical Investigation, vol. 124, no. 4, pp. 1552-1567, 2014.
10. R. E. Tanzi, J. F. Gusella, P. C.Watkins et al., "Amyloid protein gene: cDNA, mRNA distribution, genetic linkage near the Alzheimer locus," Science, vol. 235, no. 4791, pp. 880-884, 1987.
11. R. Sherrington, E. I. Rogaev, Y. Liang et al., "Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease," Nature, vol. 375, no. 6534, pp. 754-760, 1995.
12. E. Levy-Lahad,W.Wasco, P. Poorkaj et al., "Candidate gene for the chromosome 1 familial Alzheimer's disease locus," Science, vol. 269, no. 5226, pp. 973-977, 1995.
13. A. Serrano-Pozo, M. P. Frosch, E. Masliah, B. T. Hyman, "Neuropathological alterations in Alzheimer disease," Cold Spring Harbor Perspectives in Medicine, vol. 1, no. 1, Article ID a006189, 2011.
14. X. Xu, "-Secretase catalyzes sequential cleavages of the APP transmembrane domain," Journal of Alzheimer's Disease, vol. 16, no. 2, pp. 211-224, 2009.
15. S. Gandy, G. Caporaso, J. Buxbaum, B. Frangione, P. Greengard, "APP processing, A-amyloidogenesis, the pathogenesis of Alzheimer's disease," Neurobiology of Aging, vol. 15, no. 2, pp. 253-256, 1994.
16. Y.-W. Zhang andH. Xu, "Molecular and cellularmechanisms for Alzheimer's disease: understanding APP metabolism," Current Molecular Medicine, vol. 7, no. 7, pp. 687-696, 2007.
17. M. Citron, "Alzheimer's disease: strategies for diseasemodification," Nature Reviews Drug Discovery, vol. 9, no. 5, pp. 387-398, 2010.
18. S. Barghorn, V. Nimmrich, A. Striebinger et al., "Globular amyloid-peptide1-42 oligomer-a homogenous and stable neuropathological protein in Alzheimer's disease," Journal of Neurochemistry, vol. 95, no. 3, pp. 834-847, 2005.
19. A.Hamilton, G.W. Zamponi, S. S.G. Ferguson, "Glutamate receptors function as scaffolds for the regulation of-amyloid and cellular prion protein signaling complexes," Molecular Brain, vol. 8, no. 1, article 18, 2015.
20. M. Renner, P. N. Lacor, P. T. Velasco et al., "Deleterious effects of amyloid oligomers acting as an extracellular scaffold for mGluR5," Neuron, vol. 66, no. 5, pp. 739-754, 2010.
21. D. Aydin, S. W. Weyer, U. C. Müller, "Functions of the APP gene family in the nervous system: insights from mouse models," Experimental Brain Research, vol. 217, no. 3-4, pp. 423-434, 2012.
22. D. Puzzo, L. Privitera, E. Leznik et al., "Picomolar amyloid-positively modulates synaptic plasticity and memory in hippocampus," The Journal of Neuroscience, vol. 28, no. 53, pp. 14537-14545, 2008.
23. M. J. Berridge, M. D. Bootman, H. L. Roderick, "Calcium signalling: dynamics, homeostasis and remodelling," Nature Reviews Molecular Cell Biology, vol. 4, no. 7, pp. 517-529, 2003.
24. M. P. Blaustein andW. J. Lederer, "Sodium/calciumexchange: its physiological implications," Physiological Reviews, vol. 79, no. 3, pp. 763-854, 1999.
25. J. Santo-Domingo and N. Demaurex, "Calcium uptake mechanisms of mitochondria," Biochimica et Biophysica Acta-Bioenergetics, vol. 1797, no. 6-7, pp. 907-912, 2010.
26. P. Castaldo, M. Cataldi, S. Magi, V. Lariccia, S. Arcangeli, S. Amoroso, "Role of the mitochondrial sodium/calcium exchanger in neuronal physiology and in the pathogenesis of neurological diseases," Progress in Neurobiology, vol. 87, no. 1, pp. 58-79, 2009.
27. P. Gobbi, P. Castaldo, A.Minelli et al., "Mitochondrial localization of Na+/Ca2+ exchangers NCX1-3 in neurons and astrocytes of adult rat brain in situ," Pharmacological Research, vol. 56, no. 6, pp. 556-565, 2007.
28. M. D. Weingarten, A. H. Lockwood, S. Y. Hwo, M. W. Kirschner, "Aprotein factor essential for microtubule assembly," Proceedings of the National Academy of Sciences of the United States of America, vol. 72, no. 5, pp. 1858-1862, 1975.
29. M. Goedert, M. G. Spillantini, M. C. Potier, J. Ulrich, R. A. Crowther, "Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain," The EMBO Journal, vol. 8, no. 2, pp. 393-399, 1989.
30. K. S. Kosik, L. D. Orecchio, S. Bakalis, R. L. Neve, "Developmentally regulated expression of specific tau sequences," Neuron, vol. 2, no. 4, pp. 1389-1397, 1989.
31. P. H. Reddy, "Abnormal tau, mitochondrial dysfunction, impaired axonal transport ofmitochondria, synaptic deprivation in Alzheimer's disease," Brain Research, vol. 1415,pp. 136-148, 2011.
32. S. S.KhanandG. S. Bloom, "Tau: the center of a signaling nexus in Alzheimer's disease," Frontiers in Neuroscience, vol. 10, article 31, 2016.
33. A. de Calignon, L.M. Fox, R. Pitstick et al., "Caspase activation precedes and leads to tangles," Nature, vol. 464, no. 7292, pp. 1201-1204, 2010.
34. A. de Calignon, T. L. Spires-Jones, R. Pitstick, G. A. Carlson, B. T. Hyman, "Tangle-bearing neurons survive despite disruption ofmembrane integrity in amouse model of tauopathy," Journal of Neuropathology and Experimental Neurology, vol. 68, no. 7, pp. 757-761, 2009.
35. T. Gomez-Isla, J. L. Price, D. W. McKeel Jr., J. C. Morris, J. H. Growdon, B. T. Hyman, "Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease," The Journal of Neuroscience, vol. 16, no. 14, pp. 4491-4500, 1996.
36. P. R. Hof, T. Bussière, G. Gold et al., "Stereologic evidence for persistence of viable neurons in layer II of the entorhinal cortex and the CA1 field in Alzheimer disease," Journal of Neuropathology and Experimental Neurology, vol. 62, no. 1, pp. 55-67, 2003.
37. K. Iqbal and I. Grundke-Iqbal, "Neurofibrillary pathology leads to synaptic loss and not the other way around in Alzheimer disease," Journal of Alzheimer's Disease, vol. 4, no. 3, pp. 235-238, 2002.
38. T. Kimura, T. Fukuda, N. Sahara et al., "Aggregation of detergent-insoluble tau is involved in neuronal loss but not in synaptic loss," The Journal of Biological Chemistry, vol. 285, no. 49, pp. 38692-38699, 2010.
39. T. L. Spires-Jones, A. De Calignon, T. Matsui et al., "In vivo imaging reveals dissociation between caspase activation and acute neuronal death in tangle-bearing neurons," The Journal of Neuroscience, vol. 28, no. 4, pp. 862-867, 2008.
40. Y. Yoshiyama, M. Higuchi, B. Zhang et al., "Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model," Neuron, vol. 53, no. 3, pp. 337-351, 2007.
41. H. Akiyama, S. Barger, S. Barnum et al., "Inflammation and Alzheimer's disease," Neurobiology of Aging, vol. 21, no. 3, pp. 383-421, 2000.
42. F. E. McAlpine, J.-K. Lee, A. S. Harms et al., "Inhibition of soluble TNF signaling in a mouse model of Alzheimer's disease prevents pre-plaque amyloid-associated neuropathology," Neurobiology of Disease, vol. 34, no. 1, pp. 163-177, 2009.
43. G. Cantarella, D. Uberti, T. Carsana, G. Lombardo, R. Bernardini, M. Memo, "Neutralization of TRAIL death pathway protects human neuronal cell line from-amyloid toxicity," Cell Death and Differentiation, vol. 10, no. 1, pp. 134-141, 2003.
44. N. Ronsisvalle, G. Di Benedetto, C. Parenti, S. Amoroso, R. Bernardini, G. Cantarella, "CHF5074 protects SH-SY5Y human neuronal-like cells from amyloid-beta 25-35 and tumor necrosis factor related apoptosis inducing ligand toxicity in vitro," Current Alzheimer Research, vol. 11, no. 7, pp. 714-724, 2014.
45. P. I. Moreira, S. M. Cardoso, M. S. Santos, C. R. Oliveira, "The key role of mitochondria in Alzheimer's disease," Journal of Alzheimer's Disease, vol. 9, no. 2, pp. 101-110, 2006.
46. P. I.Moreira, C. Carvalho, X. Zhu, M. A. Smith, G. Perry, "Mitochondrial dysfunction is a trigger of Alzheimer's disease pathophysiology," Biochimica et Biophysica Acta-Molecular Basis of Disease, vol. 1802, no. 1, pp. 2-10, 2010.
47. P. I. Moreira, X. Zhu, X. Wang et al., "Mitochondria: a therapeutic target in neurodegeneration," Biochimica et Biophysica Acta-Molecular Basis of Disease, vol. 1802, no. 1, pp. 212-220, 2010.
48. B. Su, X.Wang, A. Nunomura et al., "Oxidative stress signaling in Alzheimer's disease," Current Alzheimer Research, vol. 5, no. 6, pp. 525-532, 2008.
49. X. Gan, L. Wu, S. Huang et al., "Oxidative stress-mediated activation of extracellular signal-regulated kinase contributes to mild cognitive impairment-relatedmitochondrial dysfunction," Free Radical Biology and Medicine, vol. 75, pp. 230-240, 2014.
50. M. J. Berridge, "Dysregulation of neural calcium signaling in Alzheimer disease, bipolar disorder and schizophrenia," Prion, vol. 7, no. 1, pp. 2-13, 2013.
51. Z. S. Khachaturian, "Calcium, membranes, aging and Alzheimer's disease: introduction and overview," Annals of the New York Academy of Sciences, vol. 568, pp. 1-4, 1989.
52. J. Marx, "Alzheimer's disease. Fresh evidence points to an old suspect: calcium," Science, vol. 318, no. 5849, pp. 384-385, 2007.
53. I. Bezprozvanny, "Calcium signaling and neurodegenerative diseases," Trends in Molecular Medicine, vol. 15, no. 3, pp. 89-100, 2009.
54. I. Bezprozvanny and M. P. Mattson, "Neuronal calcium mishandling and the pathogenesis of Alzheimer's disease," Trends in Neurosciences, vol. 31, no. 9, pp. 454-463, 2008.
55. M. P. Mattson, "ER calcium and Alzheimer's disease: in a state of flux," Science Signaling, vol. 3, no. 114, article pe10, 2010.
56. A. Demuro, I. Parker, G. E. Stutzmann, "Calcium signaling and amyloid toxicity in Alzheimer disease," The Journal of Biological Chemistry, vol. 285, no. 17, pp. 12463-12468, 2010.
57. T. Kubo, S. Nishimura, Y. Kumagae, I. Kaneko, "In vivo conversion of racemized-amyloid ([D-Ser26]A25-35/40) and fragment presence in the brains ofAlzheimer's patients," Journal of Neuroscience Research, vol. 70, no. 3, pp. 474-483, 2002.
58. A. Rani, Neha, R. K. Sodhi, A. Kaur, "Protective effect of a calcium channel blocker 'diltiazem' on aluminum chlorideinduced dementia in mice," Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 388, no. 11, pp. 1151-1161, 2015.
59. X.Wang, L.Wang, R. Jiang, Y. Yuan, Q. Yu, Y. Li, "Exendin-4 antagonizes A1-42-induced suppression of long-termpotentiation by regulating intracellular calcium homeostasis in rat hippocampal neurons," Brain Research, vol. 1627, pp. 101-108, 2015.
60. Z. Zhang, R. Chen, W. An et al., "A novel acetylcholinesterase inhibitor and calcium channel blocker SCR-1693 improves A25-35-impaired mouse cognitive function," Psychopharmacology, vol. 233, no. 4, pp. 599-613, 2016.
61. C. J. Maxwell, D. B. Hogan, E. M. Ebly, "Calcium-channel blockers and cognitive function in elderly people: results from the Canadian Study of Health and Aging," Canadian Medical Association Journal, vol. 161, no. 5, pp. 501-506, 1999.
62. S. R. Heckbert, W. T. Longstreth Jr., B. M. Psaty et al., "The association of antihypertensive agents with MRI white matter findings and with modified mini-mental state examination in older adults," Journal of the American Geriatrics Society, vol. 45, no. 12, pp. 1423-1530, 1997.
63. G. Wagner, A. Icks, H.-H. Abholz, D. Schröder-Bernhardi, W. Rathmann, K. Kostev, "Antihypertensive treatment and risk of dementia: a retrospective database study," International Journal of Clinical Pharmacology andTherapeutics, vol. 50, no. 3, pp. 195-201, 2012.
64. G. E. Stutzmann, "The pathogenesis of Alzheimers disease-is it a lifelong 'calciumopathy'" Neuroscientist, vol. 13, no. 5, pp. 546-559, 2007.
65. O. Thibault, J. C. Gant, P. W. Landfield, "Expansion of the calcium hypothesis of brain aging and Alzheimer's disease: minding the store," Aging Cell, vol. 6, no. 3, pp. 307-317, 2007.
66. N. Arispe, H. B. Pollard, E. Rojas, "Giant multilevel cation channels formed by Alzheimer disease amyloid-protein [AP-(1-40)] in bilayer membranes," Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 22, pp. 10573-10577, 1993.
67. J.-C. Fernandez-Morales, J.-A. Arranz-Tagarro, E. Calvo-Gallardo, M. Maroto, J.-F. Padn, A. G. Garca, "Stabilizers of neuronal and mitochondrial calcium cycling as a strategy for developing a medicine for Alzheimer's disease," ACS Chemical Neuroscience, vol. 3, no. 11, pp. 873-883, 2012.
68. J. R. Lopez, A. Lyckman, S. Oddo, F. M. LaFerla, H. W. Querfurth, A. Shtifman, "Increased intraneuronal resting [Ca2+] in adult Alzheimer's disease mice," Journal of Neurochemistry, vol. 105, no. 1, pp. 262-271, 2008.
69. K. V. Kuchibhotla, S. T. Goldman, C. R. Lattarulo, H.-Y. Wu, B. T. Hyman, B. J. Bacskai, "A plaques lead to aberrant regulation of calciumhomeostasis in vivo resulting in structural and functional disruption of neuronal networks," Neuron, vol. 59, no. 2, pp. 214-225, 2008.
70. N. Patel, S. Ramachandran, R. Azimov, B. L. Kagan, R. Lal, "Ion channel formation by Tau protein: implications for Alzheimer's disease and tauopathies," Biochemistry, vol. 54, no. 50, pp. 7320-7325, 2015.
71. L. E. Jensen, G. Bultynck, T. Luyten, H. Amijee, M. D. Bootman, H. L. Roderick, "Alzheimer's disease-associated peptide A42 mobilizes ER Ca2+ via InsP3R-dependent and-independentmechanisms," Frontiers inMolecular Neuroscience, vol. 6, article 36, 2013.
72. A. Demuro and I. Parker, "Cytotoxicity of intracellular A42 amyloid oligomers involves Ca2+ release from the endoplasmic reticulum by stimulated production of inositol trisphosphate," The Journal of Neuroscience, vol. 33, no. 9, pp. 3824-3833, 2013.
73. E. Ferreiro, R. Resende, R. Costa, C. R. Oliveira, C. M. F. Pereira, "An endoplasmic-reticulum-specific apoptotic pathway is involved in prion and amyloid-beta peptides neurotoxicity," Neurobiology of Disease, vol. 23, no. 3, pp. 669-678, 2006.
74. E. Ferreiro, C. R. Oliveira, C. M. F. Pereira, "Involvement of endoplasmic reticulum Ca2+ release through ryanodine and inositol 1,4,5-triphosphate receptors in the neurotoxic effects induced by the amyloid-peptide," Journal of Neuroscience Research, vol. 76, no. 6, pp. 872-880, 2004.
75. K.N.Green, A.Demuro, Y. Akbari et al., "SERCApump activity is physiologically regulated by presenilin and regulates amyloid production," Journal of Cell Biology, vol. 181, no. 7, pp. 1107-1116, 2008.
76. M. Brini and E. Carafoli, "Calcium pumps in health and disease," Physiological Reviews, vol. 89, no. 4, pp. 1341-1378, 2009.
77. N. C. Danbolt, "Glutamate uptake," Progress in Neurobiology, vol. 65, no. 1, pp. 1-105, 2001.
78. L. Berliocchi, D. Bano, P. Nicotera, "Ca2+ signals and death programmes in neurons," Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 360, no. 1464, pp. 2255-2258, 2005.
79. D. W. Choi, "Glutamate neurotoxicity and diseases of the nervous system," Neuron, vol. 1, no. 8, pp. 623-634, 1988.
80. F. M. Ribeiro, M. Paquet, S. P. Cregan, S. S. G. Ferguson, "Group I metabotropic glutamate receptor signalling and its implication in neurological disease," CNS and Neurological Disorders-Drug Targets, vol. 9, no. 5, pp. 574-595, 2010.
81. E.Masliah, M. Alford, R. DeTeresa, M.Mallory, L. Hansen, "Deficient glutamate transport is associated with neurodegeneration in Alzheimer's disease," Annals of Neurology, vol. 40, no. 5, pp. 759-766, 1996.
82. S. Li, S. Hong, N. E. Shepardson, D. M. Walsh, G. M. Shankar,D. Selkoe, "Soluble oligomers of amyloid protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake," Neuron, vol. 62, no. 6, pp. 788-801, 2009.
83. C. P. Jacob, E. Koutsilieri, J. Bartl et al., "Alterations in expression of glutamatergic transporters and receptors in sporadic Alzheimer's disease," Journal of Alzheimer's Disease, vol. 11, no. 1, pp. 97-116, 2007.
84. S. Marenco and D. R. Weinberger, "Therapeutic potential of positive AMPA receptor modulators in the treatment of neuropsychiatric disorders," CNS Drugs, vol. 20, no. 3, pp. 173-185, 2006.
85. P. Riederer and S. Hoyer, "From benefit to damage. Glutamate and advanced glycation end products in Alzheimer brain," Journal of Neural Transmission, vol. 113, no. 11, pp. 1671-1677, 2006.
86. B. Brawek and O. Garaschuk, "Network-wide dysregulation of calcium homeostasis in Alzheimer's disease," Cell and Tissue Research, vol. 357, no. 2, pp. 427-438, 2014.
87. A. C. R. G. Fonseca, P. I.Moreira, C. R. Oliveira, S.M. Cardoso, P. Pinton, C. F. Pereira, "Amyloid-beta disrupts calcium and redox homeostasis in brain endothelial cells," Molecular Neurobiology, vol. 51, no. 2, pp. 610-622, 2015.
88. K. T. Oseki, P. T. Monteforte, G. J. S. Pereira et al., "Apoptosis induced by A25-35 peptide is Ca2+-IP3 signaling-dependent inmurine astrocytes," European Journal of Neuroscience, vol. 40, no. 3, pp. 2471-2478, 2014.
89. I. Dal Prà, U. Armato, F. Chioffi et al., "The A peptidesactivated calcium-sensing receptor stimulates the production and secretion of vascular endothelial growth factor-a by normoxic adult human cortical astrocytes," NeuroMolecular Medicine, vol. 16, no. 4, pp. 645-657, 2014.
90. I. Dal Prà, A. Chiarini, L. Gui et al., "Do astrocytes collaborate with neurons in spreading the 'infectious' A and Tau drivers of Alzheimer's disease" Neuroscientist, vol. 21, no. 1, pp. 9-29, 2015.
91. S. Yano, E.M. Brown, N. Chattopadhyay, "Calcium-sensing receptor in the brain," Cell Calcium, vol. 35, no. 3, pp. 257-264, 2004.
92. M. Ruat and E. Traiffort, "Roles of the calcium sensing receptor in the central nervous system," Best Practice and Research: Clinical Endocrinology and Metabolism, vol. 27, no. 3, pp. 429-442, 2013.
93. U. Armato, A. Chiarini, B. Chakravarthy et al., "Calciumsensing receptor antagonist (calcilytic) NPS 2143 specifically blocks the increased secretion of endogenous A42 prompted by exogenous fibrillary or soluble A25-35 in human cortical astrocytes and neurons-therapeutic relevance to Alzheimer's disease," Biochimica et Biophysica Acta-Molecular Basis of Disease, vol. 1832, no. 10, pp. 1634-1652, 2013.
94. C. Ruhrberg andV. L. Bautch, "Neurovascular development and links to disease," Cellular andMolecular Life Sciences, vol. 70,no. 10, pp. 1675-1684, 2013.
95. A. E. Davey, K. Leach, C. Valant, A. D. Conigrave, P. M. Sexton, A. Christopoulos, "Positive and negative allosteric modulators promote biased signaling at the calcium-sensing receptor," Endocrinology, vol. 153, no. 3, pp. 1232-1241, 2012.
96. A. Sanchez, D. Tripathy, J. Luo, X. Yin, J. Martinez, P. Grammas, "Neurovascular unit and the effects of dosage in VEGF toxicity: role for oxidative stress and thrombin," Journal of Alzheimer's Disease, vol. 34, no. 1, pp. 281-291, 2013.
97. A. Sanchez, S. Wadhwani, P. Grammas, "Multiple neurotrophic effects of VEGF on cultured neurons," Neuropeptides, vol. 44, no. 4, pp. 323-331, 2010.
98. B. D. Quednau, D. A. Nicoll, K. D. Philipson, "Tissue specificity and alternative splicing of the Na+/Ca2+ exchanger isoforms NCX1, NCX2, NCX3 in rat," American Journal of Physiology-Cell Physiology, vol. 272, no. 4, part 1, pp. C1250-C1261, 1997.
99. S. Magi, S. Arcangeli, P. Castaldo et al., "Glutamate-induced ATP synthesis: relationship between plasma membrane Na+/Ca2+ exchanger and excitatory amino acid transporters in brain and heart cell models," Molecular Pharmacology, vol. 84, no. 4, pp. 603-614, 2013.
100. S. Magi, V. Lariccia, P. Castaldo et al., "Physical and functional interaction of NCX1 and EAAC1 transporters leading to glutamate-enhanced ATP production in brain mitochondria," PLoS ONE, vol. 7, no. 3,Article ID e34015, 2012.
101. R. A. Colvin, J.W. Bennett, S. L. Colvin, R. A. Allen, J.Martinez, G. D. Miner, "Na+/Ca2+ exchange activity is increased in Alzheimer's disease brain tissues," Brain Research, vol. 543, no. 1, pp. 139-147, 1991.
102. H.-S. Kim, J.-H. Lee, Y.-H. Suh, "C-terminal fragment of Alzheimer's amyloid precursor protein inhibits sodium/calcium exchanger activity in SK-N-SH cell," NeuroReport, vol. 10, no. 1, pp. 113-116, 1999.
103. A.Wu, C. A. Derrico, L. Hatem, R. A. Colvin, "Alzheimer's amyloid-beta peptide inhibits sodium/calcium exchange measured in rat and human brain plasma membrane vesicles," Neuroscience, vol. 80, no. 3, pp. 675-684, 1997.
104. S. Sokolow, S. H. Luu, A. J. Headley et al., "High levels of synaptosomalNa+-Ca2+ exchangers (NCX1,NCX2,NCX3) colocalized with amyloid-beta in human cerebral cortex affected by Alzheimer's disease," Cell Calcium, vol. 49,no. 4, pp. 208-216, 2011.
105. D. Bano, E.Munarriz, H. L. Chen et al., "The plasmamembrane Na+/Ca2+ exchanger is cleaved by distinct protease families in neuronal cell death," Annals of the New York Academy of Sciences, vol. 1099, pp. 451-455, 2007.
106. D. Bano, K.W. Young, C. J.Guerin et al., "Cleavage of the plasma membrane Na+/Ca2+ exchanger in excitotoxicity," Cell, vol. 120, no. 2, pp. 275-285, 2005.
107. J. Atherton, K. Kurbatskaya, M. Bondulich et al., "Calpain cleavage and inactivation of the sodium calcium exchanger-3 occur downstreamofA in Alzheimer's disease," Aging Cell, vol. 13, no. 1, pp. 49-59, 2014.
108. A. Minelli, P. Castaldo, P. Gobbi, S. Salucci, S. Magi, S. Amoroso, "Cellular and subcellular localization of Na+-Ca2+ exchanger protein isoforms, NCX1, NCX2, NCX3 in cerebral cortex and hippocampus of adult rat," Cell Calcium, vol. 41, no. 3, pp. 221-234, 2007.
109. N. N. Danial and S. J. Korsmeyer, "Cell death: critical control points," Cell, vol. 116, no. 2, pp. 205-219, 2004.
110. D. R. Green and G. Kroemer, "The pathophysiology of mitochondrial cell death," Science, vol. 305, no. 5684, pp. 626-629, 2004.
111. R. Rizzuto, D. De Stefani, A. Raffaello, C. Mammucari, "Mitochondria as sensors and regulators of calcium signalling," Nature Reviews Molecular Cell Biology, vol. 13, no. 9, pp. 566-578, 2012.
112. S. Orrenius, B. Zhivotovsky, P. Nicotera, "Regulation of cell death: the calcium-apoptosis link," Nature Reviews Molecular Cell Biology, vol. 4, no. 7, pp. 552-565, 2003.
113. M. R. Duchen, "Mitochondria and calcium: fromcell signalling to cell death," The Journal of Physiology, vol. 529, part 1, pp. 57-68, 2000.
114. M. Ankarcrona, F. Mangialasche, B. Winblad, "Rethinking Alzheimer's disease therapy: aremitochondria the key" Journal of Alzheimer's Disease, vol. 20, supplement 2, pp. S579-S590, 2010.
115. P. H. Reddy, S. McWeeney, B. S. Park et al., "Gene expression profiles of transcripts in amyloid precursor protein transgenic mice: up-regulation of mitochondrial metabolism and apoptotic genes is an early cellular change in Alzheimer's disease," Human Molecular Genetics, vol. 13, no. 12, pp. 1225-1240, 2004.
116. M. Manczak, T. S. Anekonda, E. Henson, B. S. Park, J. Quinn, P. H. Reddy, "Mitochondria are a direct site of A accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression," HumanMolecular Genetics, vol. 15,no. 9, pp. 1437-1449, 2006.
117. S. B. Berman, Y.-B. Chen, B. Qi et al., "Bcl-x L increases mitochondrial fission, fusion, biomass in neurons," The Journal of Cell Biology, vol. 184, no. 5, pp. 707-719, 2009.
118. X.Wang, B. Su, H.-G. Lee et al., "Impaired balance ofmitochondrial fission and fusion in Alzheimer's disease," The Journal of Neuroscience, vol. 29, no. 28, pp. 9090-9103, 2009.
119. X.Wang, B. Su, S. L. Siedlak et al., "Amyloid-overproduction causes abnormal mitochondrial dynamics via differential modulation ofmitochondrial fission/fusion proteins," Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 49, pp. 19318-19323, 2008.
120. X. Gan, S. Huang, L. Wu et al., "Inhibition of ERK-DLP1 signaling and mitochondrial division alleviates mitochondrial dysfunction in Alzheimer's disease cybrid cell," Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, vol. 1842, no. 2, pp. 220-231, 2014.
121. K. L. Schulz, A. Eckert, V. Rhein et al., "A new link tomitochondrial impairment in tauopathies," Molecular Neurobiology, vol. 46, no. 1, pp. 205-216, 2012.
122. M. Manczak and P. H. Reddy, "Abnormal interaction between the mitochondrial fission protein Drp1 and hyperphosphorylated tau in Alzheimer's disease neurons: implications for mitochondrial dysfunction and neuronal damage," Human Molecular Genetics, vol. 21, no. 11, pp. 2538-2547, 2012.
123. R. A.Quintanilla,R. vonBernhardi, J. A.Godoy,N. C. Inestrosa, G. V. W. Johnson, "Phosphorylated tau potentiates A-induced mitochondrial damage in mature neurons," Neurobiology of Disease, vol. 71, pp. 260-269, 2014.
124. R. A. Rissman, W. W. Poon,M. Blurton-Jones et al., "Caspasecleavage of tau is an early event in Alzheimer disease tangle pathology," The Journal of Clinical Investigation, vol. 114, no. 1, pp. 121-130, 2004.
125. R. A. Quintanilla, P. J. Dolan, Y. N. Jin, G. V. W. Johnson, "Truncated tau and A cooperatively impair mitochondria in primary neurons," Neurobiology of Aging, vol. 33, no. 3, pp. 619.e25-619.e35, 2012.
126. V. Rhein, X. Song, A. Wiesner et al., "Amyloid-and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's disease mice," Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 47, pp. 20057-20062, 2009.
127. L. Hedskog, C. M. Pinho, R. Filadi et al., "Modulation of the endoplasmic reticulum-mitochondria interface in Alzheimer's disease and related models," Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 19, pp. 7916-7921, 2013.
128. G. Csordas, C. Renken, P. Varnai et al., "Structural and functional features and significance of the physical linkage between ER and mitochondria,"The Journal of Cell Biology, vol. 174, no. 7, pp. 915-921, 2006.
129. D. R.Voelker, "Bridging gaps in phospholipid transport," Trends in Biochemical Sciences, vol. 30, no. 7, pp. 396-404, 2005.
130. E.Area-Gomez, A. J. C. de Groof, I. Boldogh et al., "Presenilins are enriched in endoplasmic reticulum membranes associated with mitochondria,"TheAmericanJournal of Pathology, vol. 175, no. 5, pp. 1810-1816, 2009.
131. N. Takasugi, T. Tomita, I. Hayashi et al., "The role of presenilin cofactors in the-secratase complex," Nature, vol. 422, no. 6930, pp. 438-441, 2003.
132. T. Tomita, K. Maruyama, T. C. Saido et al., "The presenilin 2 mutation (N141I) linked to familial Alzheimer disease (Volga German families) increases the secretion of amyloid protein ending at the 42nd (or 43rd) residue," Proceedings of theNational Academy of Sciences of the United States of America, vol. 94, no. 5, pp. 2025-2030, 1997.
133. M. A. Fernandez, J. A. Klutkowski, T. Freret, M. S. Wolfe, "Alzheimer presenilin-1 mutations dramatically reduce trimming of long amyloid-peptides (A) by-secretase to increase 42-to-40-residue A,"The Journal of Biological Chemistry, vol. 289, no. 45, pp. 31043-31052, 2014.
134. E. Area-Gomez, M. Del Carmen Lara Castillo, M. D. Tambini et al., "Upregulated function of mitochondria-associated ER membranes in Alzheimer disease," The EMBO Journal, vol. 31, no. 21, pp. 4106-4123, 2012.
135. B. Schreiner, L. Hedskog, B. Wiehager, M. Ankarcrona, "Amyloid-peptides are generated in mitochondria-associated endoplasmic reticulum membranes," Journal of Alzheimer's Disease, vol. 43, no. 2, pp. 369-374, 2015.
136. S. L. Mironov and N. Symonchuk, "ER vesicles and mitochondria move and communicate at synapses," Journal of Cell Science, vol. 119, no. 23, pp. 4926-4934, 2006.
137. T. Simmen, J. E. Aslan, A.D. Blagoveshchenskaya et al., "PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis," The EMBO Journal, vol. 24, no. 4, pp. 717-729, 2005.
138. T. Hayashi and T.-P. Su, "Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca2+ signaling and cell survival," Cell, vol. 131, no. 3, pp. 596-610, 2007.
139. I. Smets, A. Caplanusi, S. Despa et al., "Ca2+ uptake in mitochondria occurs via the reverse action of the Na+/Ca2+ exchanger in metabolically inhibited MDCK cells," American Journal of Physiology-Renal Physiology, vol. 286, no. 4, pp. F784-F794, 2004.
140. J. G. McCormack, A. P. Halestrap, R.M. Denton, "Role of calcium ions in regulation of mammalian intramitochondrial metabolism," Physiological Reviews, vol. 70, no. 2, pp. 391-425, 1990.
141. C. Zhang, R. A. Rissman, J. Feng, "Characterization ofATP alternations in an Alzheimer's disease transgenicmousemodel," Journal of Alzheimer's Disease, vol. 44, no. 2, pp. 375-378, 2015.
142. S. Orrenius, V. Gogvadze, B. Zhivotovsky, "Calcium and mitochondria in the regulation of cell death," Biochemical and Biophysical Research Communications, vol. 460, no. 1, pp. 72-81, 2015.
143. C. Thiffault and J. P. Bennett Jr., "Cyclical mitochondrial M fluctuations linked to electron transport, F0F1 ATPsynthase and mitochondrial Na+/Ca+2 exchange are reduced in Alzheimer's disease cybrids," Mitochondrion, vol. 5, no. 2, pp. 109-119, 2005.
144. J.H.Chin, F.W. Tse, K.Harris, J.H. Jhamandas, "-Amyloid enhances intracellular calcium rises mediated by repeated activation of intracellular calciumstores and nicotinic receptors in acutely dissociated rat basal forebrain neurons," Brain Cell Biology, vol. 35, no. 2-3, pp. 173-186, 2006.
145. M. Chen and H. T. Nguyen, "Our 'energy-Ca2+ signaling deficits' hypothesis and its explanatory potential for key features of Alzheimer's disease," Frontiers in Aging Neuroscience, vol. 6, article 329, 2014.