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Current Alzheimer Research

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ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

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Mini-Review Article

Fine Tuning of Intracellular Ca2+ Content by Pharmacological Agents – A Strategy to Prevent Synapse Loss in Alzheimer Disease Hippocampal Neurons

Author(s): Elena Popugaeva*

Volume 17, Issue 12, 2020

Page: [1065 - 1071] Pages: 7

DOI: 10.2174/1567205018666210119145735

Price: $65

Abstract

Alzheimer disease is the dominant form of elderly dementia. Today all clinical trials that target β-amyloid have failed to indicate that β-amyloid may not be a causative agent in AD pathogenesis. Thus there is a need to search for alternative ways to treat AD patients.

Neuronal store-operated calcium entry is a fine-tuning mechanism that regulates intracellular Ca2+ content. Recent evidence suggests that store-operated calcium channels may be targeted with pharmacological agents in order to prevent synapse loss, recover long-term potentiation and change behavior.

Current mini-review discusses basic chemical structures that modulate intracellular calcium dysbalance via targeting store-operated calcium channels and their applicability as anti-AD pharmacological agents.

Keywords: Alzheimer's disease, calcium hypothesis, nSOCE, pharmacological agents, β-amyloid, pharmacological.

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[1]
Ferri CP, Prince M, Brayne C, et al. Global prevalence of dementia: A Delphi consensus study. Lancet 2005; 366(9503): 2112-7.
[http://dx.doi.org/10.1016/S0140-6736(05)67889-0] [PMID: 16360788]
[2]
Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer’s disease: Progress and problems on the road to therapeutics. Science 2002; 297(5580): 353-6.
[http://dx.doi.org/10.1126/science.1072994] [PMID: 12130773]
[3]
Hardy J. The amyloid hypothesis for Alzheimer’s disease: A critical reappraisal. J Neurochem 2009; 110(4): 1129-34.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06181.x] [PMID: 19457065]
[4]
Bergmans BA, De Strooper B. gamma-secretases: From cell biology to therapeutic strategies. Lancet Neurol 2010; 9(2): 215-26.
[http://dx.doi.org/10.1016/S1474-4422(09)70332-1] [PMID: 20129170]
[5]
Karch CM, Cruchaga C, Goate AM. Alzheimer’s disease genetics: From the bench to the clinic. Neuron 2014; 83(1): 11-26.
[http://dx.doi.org/10.1016/j.neuron.2014.05.041] [PMID: 24991952]
[6]
Jelic V, Kivipelto M, Winblad B. Clinical trials in mild cognitive impairment: Lessons for the future. J Neurol Neurosurg Psychiatry 2006; 77(4): 429-38.
[http://dx.doi.org/10.1136/jnnp.2005.072926] [PMID: 16306154]
[7]
Raschetti R, Albanese E, Vanacore N, Maggini M. Cholinesterase inhibitors in mild cognitive impairment: A systematic review of randomised trials. PLoS Med 2007; 4(11)e338
[http://dx.doi.org/10.1371/journal.pmed.0040338] [PMID: 18044984]
[8]
Marasco RA. Current and evolving treatment strategies for the Alzheimer disease continuum. Am J Manag Care 2020; 26(8): S167-76.
[PMID: 32840330]
[9]
Chen HS, Lipton SA. The chemical biology of clinically tolerated NMDA receptor antagonists. J Neurochem 2006; 97(6): 1611-26.
[http://dx.doi.org/10.1111/j.1471-4159.2006.03991.x] [PMID: 16805772]
[10]
Olney JW. Glutaate-induced retinal degeneration in neonatal mice. Electron microscopy of the acutely evolving lesion. J Neuropathol Exp Neurol 1969; 28(3): 455-74.
[http://dx.doi.org/10.1097/00005072-196907000-00007] [PMID: 5788942]
[11]
Olney JW, Ho OL. Brain damage in infant mice following oral intake of glutamate, aspartate or cysteine. Nature 1970; 227(5258): 609-11.
[http://dx.doi.org/10.1038/227609b0] [PMID: 5464249]
[12]
Peters O, Fuentes M, Joachim LK, et al. Combined treatment with memantine and galantamine-CR compared with galantamine-CR only in antidementia drug naïve patients with mild-to-moderate Alzheimer’s disease. Alzheimers Dement 2015; 1(3): 198-204.
[http://dx.doi.org/10.1016/j.trci.2015.10.001] [PMID: 29854939]
[13]
Selkoe DJ, Hardy J. The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol Med 2016; 8(6): 595-608.
[http://dx.doi.org/10.15252/emmm.201606210] [PMID: 27025652]
[14]
Cummings J, Aisen PS, DuBois B, et al. Drug development in Alzheimer’s disease: The path to 2025. Alzheimers Res Ther 2016; 8: 39.
[http://dx.doi.org/10.1186/s13195-016-0207-9] [PMID: 27646601]
[15]
Honig LS, Vellas B, Woodward M, et al. Trial of solanezumab for mild dementia due to Alzheimer’s disease. N Engl J Med 2018; 378(4): 321-30.
[http://dx.doi.org/10.1056/NEJMoa1705971] [PMID: 29365294]
[16]
Selkoe DJ. Alzheimer’s disease is a synaptic failure. Science 2002; 298(5594): 789-91.
[http://dx.doi.org/10.1126/science.1074069] [PMID: 12399581]
[17]
DeKosky ST, Scheff SW. Synapse loss in frontal cortex biopsies in Alzheimer’s disease: Correlation with cognitive severity. Ann Neurol 1990; 27(5): 457-64.
[http://dx.doi.org/10.1002/ana.410270502] [PMID: 2360787]
[18]
Terry RD, Masliah E, Salmon DP, et al. Physical basis of cognitive alterations in Alzheimer’s disease: Synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991; 30(4): 572-80.
[http://dx.doi.org/10.1002/ana.410300410] [PMID: 1789684]
[19]
Scheff SW, Price DA. Synaptic pathology in Alzheimer’s disease: A review of ultrastructural studies. Neurobiol Aging 2003; 24(8): 1029-46.
[http://dx.doi.org/10.1016/j.neurobiolaging.2003.08.002] [PMID: 14643375]
[20]
Khachaturian ZS. Hypothesis on the regulation of cytosol calcium concentration and the aging brain. Neurobiol Aging 1987; 8(4): 345-6.
[http://dx.doi.org/10.1016/0197-4580(87)90073-X] [PMID: 3627349]
[21]
Berridge MJ. Calcium hypothesis of Alzheimer’s disease. Pflugers Arch 2010; 459(3): 441-9.
[PMID: 19795132]
[22]
Demuro A, Parker I, Stutzmann GE. Calcium signaling and amyloid toxicity in Alzheimer disease. J Biol Chem 2010; 285(17): 12463-8.
[http://dx.doi.org/10.1074/jbc.R109.080895] [PMID: 20212036]
[23]
Mattson MP. ER calcium and Alzheimer’s disease: In a state of flux. Sci Signal 2010; 3(114): pe10.
[http://dx.doi.org/10.1126/scisignal.3114pe10] [PMID: 20332425]
[24]
Supnet C, Bezprozvanny I. The dysregulation of intracellular calcium in Alzheimer disease. Cell Calcium 2010; 47(2): 183-9.
[http://dx.doi.org/10.1016/j.ceca.2009.12.014] [PMID: 20080301]
[25]
Choi DW. Ionic dependence of glutamate neurotoxicity. J Neurosci 1987; 7(2): 369-79.
[http://dx.doi.org/10.1523/JNEUROSCI.07-02-00369.1987] [PMID: 2880938]
[26]
Tymianski M, Charlton MP, Carlen PL, Tator CH. Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J Neurosci 1993; 13(5): 2085-104.
[http://dx.doi.org/10.1523/JNEUROSCI.13-05-02085.1993] [PMID: 8097530]
[27]
Lipton SA. Paradigm shift in neuroprotection by NMDA receptor blockade: Memantine and beyond. Nat Rev Drug Discov 2006; 5(2): 160-70.
[http://dx.doi.org/10.1038/nrd1958] [PMID: 16424917]
[28]
Talantova M, Sanz-Blasco S, Zhang X, et al. Aβ induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. Proc Natl Acad Sci USA 2013; 110(27): E2518-27.
[http://dx.doi.org/10.1073/pnas.1306832110] [PMID: 23776240]
[29]
Berman RM, Cappiello A, Anand A, et al. Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 2000; 47(4): 351-4.
[http://dx.doi.org/10.1016/S0006-3223(99)00230-9] [PMID: 10686270]
[30]
Murrough JW, Perez AM, Pillemer S, et al. Rapid and longer-term antidepressant effects of repeated ketamine infusions in treatment-resistant major depression. Biol Psychiatry 2013; 74(4): 250-6.
[http://dx.doi.org/10.1016/j.biopsych.2012.06.022] [PMID: 22840761]
[31]
Duman RS, Aghajanian GK, Sanacora G, Krystal JH. Synaptic plasticity and depression: New insights from stress and rapid-acting antidepressants. Nat Med 2016; 22(3): 238-49.
[http://dx.doi.org/10.1038/nm.4050] [PMID: 26937618]
[32]
Smalheiser NR. Ketamine: A neglected therapy for Alzheimer disease. Front Aging Neurosci 2019; 11: 186.
[http://dx.doi.org/10.3389/fnagi.2019.00186] [PMID: 31396078]
[33]
Zanos P, Moaddel R, Morris PJ, et al. NMDAR inhibition-independent antidepressant actions of ketamine metabolites. Nature 2016; 533(7604): 481-6.
[http://dx.doi.org/10.1038/nature17998] [PMID: 27144355]
[34]
Forette F, Seux ML, Staessen JA, et al. The prevention of dementia with antihypertensive treatment: new evidence from the Systolic Hypertension in Europe (Syst-Eur) study. Arch Intern Med 2002; 162(18): 2046-52.
[http://dx.doi.org/10.1001/archinte.162.18.2046] [PMID: 12374512]
[35]
Nedergaard M, Verkhratsky A. Calcium dyshomeostasis and pathological calcium signalling in neurological diseases. Cell Calcium 2010; 47(2): 101-2.
[http://dx.doi.org/10.1016/j.ceca.2009.12.011] [PMID: 20079921]
[36]
Sun S, Zhang H, Liu J, et al. Reduced synaptic STIM2 expression and impaired store-operated calcium entry cause destabilization of mature spines in mutant presenilin mice. Neuron 2014; 82(1): 79-93.
[http://dx.doi.org/10.1016/j.neuron.2014.02.019] [PMID: 24698269]
[37]
Rogaev EI, Sherrington R, Wu C, et al. Analysis of the 5′ sequence, genomic structure, and alternative splicing of the presenilin-1 gene (PSEN1) associated with early onset Alzheimer disease. Genomics 1997; 40(3): 415-24.
[http://dx.doi.org/10.1006/geno.1996.4523] [PMID: 9073509]
[38]
Rogaev EI, Sherrington R, Rogaeva EA, et al. Familial Alzheimer’s disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer’s disease type 3 gene. Nature 1995; 376(6543): 775-8.
[http://dx.doi.org/10.1038/376775a0] [PMID: 7651536]
[39]
Lleó A, Blesa R, Gendre J, et al. A novel presenilin 2 gene mutation (D439A) in a patient with early-onset Alzheimer’s disease. Neurology 2001; 57(10): 1926-8.
[http://dx.doi.org/10.1212/WNL.57.10.1926] [PMID: 11723295]
[40]
Mullan M, Crawford F, Axelman K, et al. A pathogenic mutation for probable Alzheimer’s disease in the APP gene at the N-terminus of beta-amyloid. Nat Genet 1992; 1(5): 345-7.
[http://dx.doi.org/10.1038/ng0892-345] [PMID: 1302033]
[41]
Jansen WJ, Ossenkoppele R, Knol DL, et al. Prevalence of cerebral amyloid pathology in persons without dementia: a meta-analysis. JAMA 2015; 313(19): 1924-38.
[http://dx.doi.org/10.1001/jama.2015.4668] [PMID: 25988462]
[42]
Duara R, Lopez-Alberola RF, Barker WW, et al. A comparison of familial and sporadic Alzheimer’s disease. Neurology 1993; 43(7): 1377-84.
[http://dx.doi.org/10.1212/WNL.43.7.1377] [PMID: 8327141]
[43]
Lippa CF, Saunders AM, Smith TW, et al. Familial and sporadic Alzheimer’s disease: Neuropathology cannot exclude a final common pathway. Neurology 1996; 46(2): 406-12.
[http://dx.doi.org/10.1212/WNL.46.2.406] [PMID: 8614503]
[44]
Drummond E, Wisniewski T. Alzheimer’s disease: Experimental models and reality. Acta Neuropathol 2017; 133(2): 155-75.
[http://dx.doi.org/10.1007/s00401-016-1662-x] [PMID: 28025715]
[45]
Bezprozvanny I. Calcium signaling and neurodegenerative diseases. Trends Mol Med 2009; 15(3): 89-100.
[http://dx.doi.org/10.1016/j.molmed.2009.01.001] [PMID: 19230774]
[46]
Alzheimer’s Association Calcium Hypothesis W. Calcium Hypothesis of Alzheimer’s disease and brain aging: A framework for integrating new evidence into a comprehensive theory of pathogenesis. Alzheimer’s Dementia: J Alzheimer’s Assoc 2017; 13(2): 178-82.
[47]
Leissring MA, Paul BA, Parker I, Cotman CW, LaFerla FM. Alzheimer’s presenilin-1 mutation potentiates inositol 1,4,5-trisphosphate-mediated calcium signaling in Xenopus oocytes. J Neurochem 1999; 72(3): 1061-8.
[http://dx.doi.org/10.1046/j.1471-4159.1999.0721061.x] [PMID: 10037477]
[48]
Stutzmann GE, Caccamo A, LaFerla FM, Parker I. 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 2004; 24(2): 508-13.
[http://dx.doi.org/10.1523/JNEUROSCI.4386-03.2004] [PMID: 14724250]
[49]
Stutzmann GE, Smith I, Caccamo A, Oddo S, Laferla FM, Parker I. Enhanced ryanodine receptor recruitment contributes to Ca2+ disruptions in young, adult, and aged Alzheimer’s disease mice. J Neurosci 2006; 26(19): 5180-9.
[http://dx.doi.org/10.1523/JNEUROSCI.0739-06.2006] [PMID: 16687509]
[50]
Ito E, Oka K, Etcheberrigaray R, et al. Internal Ca2+ mobilization is altered in fibroblasts from patients with Alzheimer disease. Proc Natl Acad Sci USA 1994; 91(2): 534-8.
[http://dx.doi.org/10.1073/pnas.91.2.534] [PMID: 8290560]
[51]
Kuchibhotla KV, Goldman ST, Lattarulo CR, Wu HY, Hyman BT, Bacskai BJ. Abeta plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron 2008; 59(2): 214-25.
[http://dx.doi.org/10.1016/j.neuron.2008.06.008] [PMID: 18667150]
[52]
Vosler PS, Brennan CS, Chen J. Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration. Mol Neurobiol 2008; 38(1): 78-100.
[http://dx.doi.org/10.1007/s12035-008-8036-x] [PMID: 18686046]
[53]
Trinchese F, Fa’ M, Liu S, et al. Inhibition of calpains improves memory and synaptic transmission in a mouse model of Alzheimer disease. J Clin Invest 2008; 118(8): 2796-807.
[http://dx.doi.org/10.1172/JCI34254] [PMID: 18596919]
[54]
Palop JJ, Jones B, Kekonius L, et al. Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer’s disease-related cognitive deficits. Proc Natl Acad Sci USA 2003; 100(16): 9572-7.
[http://dx.doi.org/10.1073/pnas.1133381100] [PMID: 12881482]
[55]
Carreras-Sureda A, Pihán P, Hetz C. Calcium signaling at the endoplasmic reticulum: fine-tuning stress responses. Cell Calcium 2018; 70: 24-31.
[http://dx.doi.org/10.1016/j.ceca.2017.08.004] [PMID: 29054537]
[56]
Lopez JR, Lyckman A, Oddo S, Laferla FM, Querfurth HW, Shtifman A. Increased intraneuronal resting [Ca2+] in adult Alzheimer’s disease mice. J Neurochem 2008; 105(1): 262-71.
[http://dx.doi.org/10.1111/j.1471-4159.2007.05135.x] [PMID: 18021291]
[57]
Gafni J, Munsch JA, Lam TH, et al. Xestospongins: Potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor. Neuron 1997; 19(3): 723-33.
[http://dx.doi.org/10.1016/S0896-6273(00)80384-0] [PMID: 9331361]
[58]
Mattson MP, Zhu H, Yu J, Kindy MS. Presenilin-1 mutation increases neuronal vulnerability to focal ischemia in vivo and to hypoxia and glucose deprivation in cell culture: Involvement of perturbed calcium homeostasis. J Neurosci 2000; 20(4): 1358-64.
[http://dx.doi.org/10.1523/JNEUROSCI.20-04-01358.2000] [PMID: 10662826]
[59]
Bezprozvanny I. Role of inositol 1,4,5-trisphosphate receptors in pathogenesis of Huntington’s disease and spinocerebellar ataxias. Neurochem Res 2011; 36(7): 1186-97.
[http://dx.doi.org/10.1007/s11064-010-0393-y] [PMID: 21210219]
[60]
Chakroborty S, Briggs C, Miller MB, et al. Stabilizing ER Ca2+ channel function as an early preventative strategy for Alzheimer’s disease. PLoS One 2012; 7(12)e52056
[http://dx.doi.org/10.1371/journal.pone.0052056] [PMID: 23284867]
[61]
Oulès B, Del Prete D, Greco B, et al. Ryanodine receptor blockade reduces amyloid-β load and memory impairments in Tg2576 mouse model of Alzheimer disease. J Neurosci 2012; 32(34): 11820-34.
[http://dx.doi.org/10.1523/JNEUROSCI.0875-12.2012] [PMID: 22915123]
[62]
Peng J, Liang G, Inan S, et al. Dantrolene ameliorates cognitive decline and neuropathology in Alzheimer triple transgenic mice. Neurosci Lett 2012; 516(2): 274-9.
[http://dx.doi.org/10.1016/j.neulet.2012.04.008] [PMID: 22516463]
[63]
Zhang H, Sun S, Herreman A, De Strooper B, Bezprozvanny I. Role of presenilins in neuronal calcium homeostasis. J Neurosci 2010; 30(25): 8566-80.
[http://dx.doi.org/10.1523/JNEUROSCI.1554-10.2010] [PMID: 20573903]
[64]
Solovyova N, Fernyhough P, Glazner G, Verkhratsky A. Xestospongin C empties the ER calcium store but does not inhibit InsP3-induced Ca2+ release in cultured dorsal root ganglia neurones. Cell Calcium 2002; 32(1): 49-52.
[http://dx.doi.org/10.1016/S0143-4160(02)00094-5] [PMID: 12127062]
[65]
Diver JM, Sage SO, Rosado JA. The inositol trisphosphate receptor antagonist 2-aminoethoxydiphenylborate (2-APB) blocks Ca2+ entry channels in human platelets: Cautions for its use in studying Ca2+ influx. Cell Calcium 2001; 30(5): 323-9.
[http://dx.doi.org/10.1054/ceca.2001.0239] [PMID: 11733938]
[66]
Gregory RB, Rychkov G, Barritt GJ. Evidence that 2-aminoethyl diphenylborate is a novel inhibitor of store-operated Ca2+ channels in liver cells, and acts through a mechanism which does not involve inositol trisphosphate receptors. Biochem J 2001; 354(Pt 2): 285-90.
[http://dx.doi.org/10.1042/bj3540285] [PMID: 11171105]
[67]
Secondo A, Bagetta G, Amantea D. On the Role of store-operated calcium entry in acute and chronic neurodegenerative diseases. Front Mol Neurosci 2018; 11: 87.
[http://dx.doi.org/10.3389/fnmol.2018.00087] [PMID: 29623030]
[68]
Tu H, Nelson O, Bezprozvanny A, et al. Presenilins form ER calcium leak channels, a function disrupted by mutations linked to familial Alzheimer’s disease. Cell 2006; 126: 981-93.
[http://dx.doi.org/10.1016/j.cell.2006.06.059] [PMID: 16959576]
[69]
Putney JW Jr. Capacitative calcium entry in the nervous system. Cell Calcium 2003; 34(4-5): 339-44.
[http://dx.doi.org/10.1016/S0143-4160(03)00143-X] [PMID: 12909080]
[70]
Popugaeva E, Pchitskaya E, Bezprozvanny I. Dysregulation of intracellular calcium signaling in Alzheimer's disease Antioxidants Redox Signal 2018; 29(12): 1176-88.
[http://dx.doi.org/10.1089/ars.2018.7506]
[71]
Putney JW. Pharmacology of store-operated calcium channels. Mol Interv 2010; 10(4): 209-18.
[http://dx.doi.org/10.1124/mi.10.4.4] [PMID: 20729487]
[72]
Zhang H, Sun S, Wu L, et al. Store-operated calcium channel complex in postsynaptic spines: A new therapeutic target for Alzheimer’s disease treatment. J Neurosci 2016; 36(47): 11837-50.
[http://dx.doi.org/10.1523/JNEUROSCI.1188-16.2016] [PMID: 27881772]
[73]
Ryazantseva M, Goncharova A, Skobeleva K, et al. Presenilin-1 delta E9 mutant induces STIM1-driven store-operated calcium channel hyperactivation in hippocampal neurons. Mol Neurobiol 2018; 55(6): 4667-80.
[http://dx.doi.org/10.1007/s12035-017-0674-4] [PMID: 28707074]
[74]
Jaworska A, Dzbek J, Styczynska M, Kuznicki J. Analysis of calcium homeostasis in fresh lymphocytes from patients with sporadic Alzheimer’s disease or mild cognitive impairment. Biochim Biophys Acta 2013; 1833(7): 1692-9.
[http://dx.doi.org/10.1016/j.bbamcr.2013.01.012] [PMID: 23354174]
[75]
Lisman J, Yasuda R, Raghavachari S. Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 2012; 13(3): 169-82.
[http://dx.doi.org/10.1038/nrn3192] [PMID: 22334212]
[76]
Foster TC, Sharrow KM, Masse JR, Norris CM, Kumar A. Calcineurin links Ca2+ dysregulation with brain aging. J Neurosci 2001; 21(11): 4066-73.
[http://dx.doi.org/10.1523/JNEUROSCI.21-11-04066.2001] [PMID: 11356894]
[77]
Jouvenceau A, Dutar P. A role for the protein phosphatase 2B in altered hippocampal synaptic plasticity in the aged rat. J Physiol Paris 2006; 99(2-3): 154-61.
[http://dx.doi.org/10.1016/j.jphysparis.2005.12.009] [PMID: 16442785]
[78]
Ting CP, Maimone TJ. Total synthesis of hyperforin. J Am Chem Soc 2015; 137(33): 10516-9.
[http://dx.doi.org/10.1021/jacs.5b06939] [PMID: 26252484]
[79]
Di Carlo G, Borrelli F, Ernst E, Izzo AA. St John’s wort: Prozac from the plant kingdom. Trends Pharmacol Sci 2001; 22(6): 292-7.
[http://dx.doi.org/10.1016/S0165-6147(00)01716-8] [PMID: 11395157]
[80]
Woelk H, Burkard G, Grünwald J. Benefits and risks of the hypericum extract LI 160: drug monitoring study with 3250 patients. J Geriatr Psychiatry Neurol 1994; 7(1): S34-8.
[http://dx.doi.org/10.1177/089198879400701s10] [PMID: 7857506]
[81]
Sawamura S, Hatano M, Takada Y, et al. Screening of transient receptor potential canonical channel activators identifies novel neurotrophic piperazine compounds. Mol Pharmacol 2016; 89(3): 348-63.
[http://dx.doi.org/10.1124/mol.115.102863] [PMID: 26733543]
[82]
Popugaeva E, Chernyuk D, Zhang H, et al. Derivatives of piperazines as potential therapeutic agents for Alzheimer’s disease. Mol Pharmacol 2019; 95(4): 337-48.
[http://dx.doi.org/10.1124/mol.118.114348] [PMID: 30696719]
[83]
Häfner S, Urban N, Schaefer M. Discovery and characterization of a positive allosteric modulator of transient receptor potential canonical 6 (TRPC6) channels. Cell Calcium 2019; 78: 26-34.
[http://dx.doi.org/10.1016/j.ceca.2018.12.009] [PMID: 30594060]
[84]
Källestål C, Blandón Zelaya E, Peña R, et al. Predicting poverty. Data mining approaches to the health and demographic surveillance system in Cuatro Santos, Nicaragua. Int J Equity Health 2019; 18(1): 165.
[http://dx.doi.org/10.1186/s12939-019-1054-7] [PMID: 31665013]
[85]
Chernyuk D, Zernov N, Kabirova M, Bezprozvanny I, Popugaeva E. Antagonist of neuronal store-operated calcium entry exerts beneficial effects in neurons expressing PSEN1ΔE9 mutant linked to familial Alzheimer disease. Neuroscience 2019; 410: 118-27.
[http://dx.doi.org/10.1016/j.neuroscience.2019.04.043] [PMID: 31055008]
[86]
Wu J, Ryskamp DA, Liang X, et al. Enhanced Store-operated calcium entry leads to striatal synaptic loss in a Huntington’s disease mouse model. J Neurosci 2016; 36(1): 125-41.
[http://dx.doi.org/10.1523/JNEUROSCI.1038-15.2016] [PMID: 26740655]
[87]
Tang Q, Guo W, Zheng L, et al. Structure of the receptor-activated human TRPC6 and TRPC3 ion channels. Cell Res 2018; 28(7): 746-55.
[http://dx.doi.org/10.1038/s41422-018-0038-2] [PMID: 29700422]

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