Українська English

ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

(English title: Physiological Journal)

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2010; 56(1): 127-142


MOLECULAR AND CELLULAR MECHANISMS OF ALZHEIMER’S DISEASE DEVELOPMENT

E.P. Kostyuk, T.Y. Korol, P.G. Kostyuk

    Bogomoletz Institute of physiology NAS of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz56.01.127


Abstract

Neuropathological studies classified several neurodegenerative illnesses among which Alzheimer’s and Parkinson’s diseases are the most frequent. Alzheimer’s disease is characterized by the presence of cognitive syndromes and almost complete destruction of memory. It is suggested that the basis of these syndromes is formation of senile plaques the main component of which is β-amyloid-42 peptide (mainly in hippocampal neurons), changes in calcium homeostasis and synaptic plasticity. Recent data indicate that alterations of calcium homeostasis connected with changes in neuronal membrane and functioning of the endoplasmic reticulum and leads to changes in long-term potentiation and long-term depression. Therefore the task of this review was the analysis of alterations in the functioning of structures involved in calcium homeostasis (including mitochondria, endoplasmic reticulum, calcium channels) as well as processes leading to changes in synaptic plasticity. Beside this we intend to clarify (mainly from the data of literature) which process is the most ponderable in the development of Alzheimer’s disease.

Keywords: Alzheimer’s disease, amyloid, calcium homeostasis, synaptic plasticity, mitochondria, endoplasmic reticulum, calcium channels.

References

  1. Abramov A.Y., Canevari L., Duchen M.R. Beta-amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase . J.Neurosci. 2004.  24.  P. 565-575. CrossRef PubMed PubMedCentral
  2.  
  3. Arispe N., Pollard H.B., Rojas E. Giant multilevel cation channels formed by Alzheimer disease amyloid betaprotein [A beta P-(140)] in bilayer membranes . Proc.Nat.Acad.Sci.USA.  1993.  90.  P. 10573-10577. CrossRef PubMed PubMedCentral
  4.  
  5. Arispe N., Pollard H.B.,Rojas E. The ability of amyloid betaprotein [A beta P (140)] to form Ca2+ channels provides a mechanism for neuronal death in Alzheimer’s disease . Ann.N.Y.Acad.Sci.  1994.  747. P. 256-266. CrossRef PubMed
  6.  
  7. Arispe N., Rojas E., Pollard H.B. Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum . Proc.Nat.Acad.Sci.USA.  1993.  90. P. 567-571. CrossRef PubMed PubMedCentral
  8.  
  9. Athos J., Impey S., Pineda V.V. et al. Hippocampal CRE-mediated gene expression is required for contextual memory formation . Nat.Neurosci.  2002.  5. P. 1119-1120. CrossRef PubMed
  10.  
  11. Beal M.F. Oxidative damage as an early marker of Alzheimer’s disease and mild cognitive impairment . Neurobiol.Aging.  2005.  26.  P. 585-586. CrossRef PubMed
  12.  
  13. Becker N., Wierenga C.J., Fonseca R. et al. LTD induction causes morphological changes of presynaptic boutons and reduces their contacts with spines . Neuron.  2008.  60.  P. 590-597. CrossRef PubMed
  14.  
  15. Billups B., Forsythe I.D. Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses . J.Neurosci.  2002. 22.  P. 5840-5847. CrossRef PubMed PubMedCentral
  16.  
  17. Bosetti F., Brizzi F., Barogi S. et al. Cytochrome c oxidase and mitochondrial F1F0-ATPase (ATP synthase) activities in platelets and brain from patients with Alzheimer’s disease . Neurobiol.Aging.  2002. 23.  P. 371-376. CrossRef.1016/S0197-4580(01)00314-1
  18.  
  19. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes . Acta Neuropathol.  1991. 82.  P. 239-259. CrossRef PubMed
  20.  
  21. Brecht W.J., Harris F.M., Chang S. et al. Neuron-specific apolipoprotein e4 proteolysis is associated with increased tau phosphorylation in brains of transgenic mice . J.Neurosci.  2004.  24.  P. 2527-2534. CrossRef PubMed PubMedCentral
  22.  
  23. Brorson J.R., Bindokas V.P., Iwama T. et al. The Ca2+ influx induced by beta-amyloid peptide 2535 in cultured hippocampal neurons results from network excitation . J.Neurobiol.  1995.  26.  P. 325-338. CrossRef PubMed
  24.  
  25. Bruce-Keller A.J., Li Y.J., Lovell M.A. et al. 4- Hydroxynonenal, a product of lipid peroxidation, damages cholinergic neurons and impairs visuospatial memory in rats . J.Neuropathol.Exp.Neurol.  1998. 57.  P. 257-267. CrossRef PubMed
  26.  
  27. Butterfield D.A., Drake J., Pocernich C. et al. Evidence of oxidative damage in Alzheimer’s disease brain: central role for amyloid beta-peptide . Trends Mol.Med.  2001.  7.  P. 548-554. CrossRef.1016/S1471-4914(01)02173-6
  28.  
  29. Caruso A., Motolese M., Iacovelli L. et al. Inhibition of the canonical Wnt signaling pathway by apolipoprotein E4 in PC12 cells . J.Neurochem.  2006.  98. P. 364-371. CrossRef PubMed
  30.  
  31. Cedazo-Minguez A., Popescu B.O., Blanco-Millan J.M. et al. Apolipoprotein E and beta-amyloid (142) regulation of glycogen synthase kinase-3beta . J.Neurochem.  2003.  87.  P. 1152-1164. CrossRef PubMed
  32.  
  33. Chen Q.S., Kagan B.L., Hirakura Y. et al. Impairment of hippocampal longterm potentiation by Alzheimer amyloid beta-peptides . J.Neurosci.Res.  2000.  60. P. 65-72. CrossRef.1002/(SICI)1097-4547(20000401)60:1<65::AID-JNR7>3.0.CO;2-Q
  34.  
  35. Cheung K.H., Shineman D., Muller M. et al. Mechanism of Ca2+ disruption in Alzheimer’s disease by presenilin regulation of InsP3 receptor channel gating . Neuron.  2008.  58.  P. 871-883. CrossRef PubMed PubMedCentral
  36.  
  37. Cochilla A.J., Alford S. Metabotropic glutamate receptor-mediated control of neurotransmitter release . Ibid.  1998.  20.  P. 1007-1016. CrossRef.1016/S0896-6273(00)80481-X
  38.  
  39. De Mattos P.S., Del Lama M.A., Toppa R.H. et al. Populational genetic structure of free-living maned wolves (Chrysocyon brachyurus) determined by proteic markers . Braz.J.Biol.  2004.  64.  P. 639-644. CrossRef PubMed
  40.  
  41. De S.B., Saftig P., Craessaerts K. et al. Deficiency of presenilin1 inhibits the normal cleavage of amyloid precursor protein . Nature.  1998.  391.  P. 387-390. CrossRef PubMed
  42.  
  43. Dejda A., Sokolowska P., Nowak J.Z. Neuroprotective potential of three neuropeptides PACAP, VIP and PHI . Pharmacol.Rep.  2005.  57.  P. 307-320.
  44.  
  45. Dubinsky J.M., Levi Y. Calcium-induced activation of the mitochondrial permeability transition in hippocampal neurons . J.Neurosci.Res.  1998.  53. P. 728-741. CrossRef.1002/(SICI)1097-4547(19980915)53:6<728::AID-JNR10>3.3.CO;2-Z
  46.  
  47. Duchen M.R. Roles of mitochondria in health and disease . Diabetes.  2004.  53 Suppl 1.  P. S96-102. CrossRef PubMed
  48.  
  49. Dudek S.M., Bear M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade . Proc. Nat. Acad. Sci.USA.  1992.  89.  P. 4363-4367. CrossRef PubMed PubMedCentral
  50.  
  51. Fagan A.M., Watson M., Parsadanian M. et al. Human and murine ApoE markedly alters A beta metabolism before and after plaque formation in a mouse model of Alzheimer’s disease . Neurobiol.Dis.  2002.  9. P. 305-318. CrossRef PubMed
  52.  
  53. Gelinas J.N., Banko J.L., Peters M.M. et al. Activation of exchange protein activated by cyclic-AMP enhances long-lasting synaptic potentiation in the hippocampus . Learn.Mem.  2008.  15.  P. 403-411. CrossRef PubMed PubMedCentral
  54.  
  55. Gend ron T.F., Pet rucelli L. The role o f tau in neurodegeneration . Mol.Neurodegener.  2009.  4. P. 13. CrossRef PubMed PubMedCentral
  56.  
  57. Gibson G.E., Sheu K.F., Blass J.P. Abnormalities of mitochondrial enzymes in Alzheimer disease . J.Neural Transm.  1998.  105.  P. 855-870. CrossRef PubMed
  58.  
  59. Glodzik-Sobanska L., Pirraglia E., Brys M. et al. The effects of normal aging and ApoE genotype on the levels of CSF biomarkers for Alzheimer ’s disease . Neurobiol.Aging.  2009.  30.  P. 672-681. CrossRef PubMed PubMedCentral
  60.  
  61. Green K.N., Demuro A., Akbari Y. et al. SERCA pump activity is physiologically regulated by presenilin and regulates amyloid beta production . J.Cell Biol.  2008. 181.  P. 1107-1116. CrossRef PubMed PubMedCentral
  62.  
  63. Green K.N., LaFerla F.M. Linking calcium to Abeta and Alzheimer’s disease . Neuron.  2008.  59. P. 190-194. CrossRef PubMed
  64.  
  65. Hardy J. A hundred years of Alzheimer ’s disease research . Ibid.  2006.  52.  P. 313. CrossRef PubMed
  66.  
  67. Alzheimer’s disease: the amyloid cascade hypothesis: an update and reappraisal . J.Alzheimers.Dis.  2006. 9.  P. 151-153. CrossRef PubMed
  68.  
  69. Hardy J. Does Abeta 42 have a function related to blood homeostasis? . Neurochem.Res.  2007.  32. P. 833-835. CrossRef PubMed
  70.  
  71. Harris F.M., Tesseur I., Brecht W.J. et al. Astroglial regulation of apolipoprotein E expression in neuronal cells. Implications for Alzheimer’s disease . J.Biol. Chem.  2004.  279.  P. 3862-3868. CrossRef PubMed
  72.  
  73. He L.M., Chen L.Y., Lou X.L. et al. Evaluation of betaamyloid peptide 2535 on calcium homeostasis in cultured rat dorsal root ganglion neurons . Brain Res. 2002.  939.  P. 65-75. CrossRef.1016/S0006-8993(02)02549-0
  74.  
  75. Hiruma H., Katakura T., Takahashi S. et al. Glutamate and amyloid beta-protein rapidly inhibit fast axonal transport in cultured rat hippocampal neurons by different mechanisms . J.Neurosci.  2003.  23. P. 8967-8977. CrossRef PubMed PubMedCentral
  76.  
  77. Hollenbeck P.J., Saxton W.M. The axonal transport of mitochondria . J.Cell Sci.  2005.  118.  P. 5411-5419. CrossRef PubMed PubMedCentral
  78.  
  79. Holmes C., Boche D., Wilkinson D. et al. Long-term effects of Abeta42 immunisation in Alzheimer’s disease: follow-up of a randomised, placebocontrolled phase I trial . Lancet.  2008.  372.  P. 216-223. CrossRef.1016/S0140-6736(08)61075-2
  80.  
  81. Huang T.H., Yang D.S., Fraser P.E.,Chakrabartty A. Alternate aggregation pathways of the Alzheimer beta- amyloid peptide. An in vitro model of preamyloid . J.Biol.Chem.  2000.  275.  P. 36436-36440. CrossRef PubMed
  82.  
  83. Huang T.H., Yang D.S., Plaskos N.P. et al. Structural studies of soluble oligomers of the Alzheimer betaamyloid peptide . J.Mol.Biol.  2000.  297.  P. 73-87. CrossRef PubMed
  84.  
  85. Huang Y., Liu X.Q., Wyss-Coray T. et al. Apolipoprotein E fragments present in Alzheimer’s disease brains induce neurofibrillary tangle-like intracellular inclusions in neurons . Proc.Natl.Acad.Sci.USA. 2001.  98.  P. 8838-8843. CrossRef PubMed PubMedCentral
  86.  
  87. Huber K.M., Mauk M.D., Kelly P.T. LTP induced by activation of voltage-dependent Ca2+ channels requires protein kinase activity . Neuroreport.  1995.  6. P. 1281-1284. CrossRef PubMed
  88.  
  89. Irizarry M.C., Cheung B.S., Rebeck G.W. Apolipoprotein E affects the amount, form, and anatomical distribution of amyloid beta-peptide deposition in homozygous APP(V717F) transgenic mice . Acta Neuropathol.  2000.  100.  P. 451-458. CrossRef PubMed
  90.  
  91. Irizarry M.C., Rebeck G.W., Cheung B. et al. Modulation of A beta deposition in APP transgenic mice by an apolipoprotein E null background . Ann.N.Y.Acad.Sci. 2000.  920.  P. 171-178. CrossRef PubMed
  92.  
  93. Ito S., Ohta S., Nishimaki K., Kagawa Y. et al. Functional integrity of mitochondrial genomes in human platelets and autopsied brain tissues from elderly patients with Alzheimer’s disease . Proc. Nat. Acad. Sci.USA.  1999.  96.  P. 2099-2103. CrossRef PubMed PubMedCentral
  94.  
  95. Kang J.S., Tian J.H., Pan P.Y. et al. Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation . Cell.  2008. 132.  P. 137-148. CrossRef PubMed PubMedCentral
  96.  
  97. Katsuki H., Izumi Y.,Zorumski C.F. Removal of extracellular calcium after conditioning stimulation disrupts long-term potentiation in the CA1 region of rat hippocampal slices . Neuroscience.  1997.  76. P. 1113-1119. CrossRef.1016/S0306-4522(97)80003-6
  98.  
  99. Kawahara M., Arispe N., Kuroda Y. et al. Alzheimer’s disease amyloid beta-protein forms Zn(2+)-sensitive, cationselective channels across excised membrane patches from hypothalamic neurons . Biophys.J. 1997.  73.  P. 67-75. CrossRef.1016/S0006-3495(97)78048-2
  100.  
  101. Kawahara M., Kuroda Y. Molecular mechanism of neuronal death in Alzheimer’s disease: Ca(2+)-channel formation of beta amyloid protein molecules] . Tanpakushitsu Kakusan Koso.  1997.  42.  P. 2002-2010.
  102.  
  103. Keil U., Bonert A., Marques C.A. et al. Amyloid betainduced changes in nitric oxide production and mitochondrial activity lead to apoptosis . J.Biol.Chem. 2004.  279.  P. 50310-50320. CrossRef PubMed
  104.  
  105. Kelleher R.J., III, Govindarajan A., Jung H.Y. et al. Translational control by MAPK signaling in long-term synaptic plasticity and memory . Cell.  2004.  116. P. 467-479. CrossRef.1016/S0092-8674(04)00115-1
  106.  
  107. Klishin A., Lozovaya N., Krishtal O. Persistently enhanced ratio of NMDA and non-NMDA components of rat hippocampal EPSC after block of A1 adenosine receptors at increased [Ca2+]o. [Mg2+]o . Neurosci. Lett.  1994.  179.  P. 132-136. CrossRef.1016/0304-3940(94)90952-0
  108.  
  109. Kostyuk P.G., Verkhratsky A.N. Calcium signalling in the nervous system . Chichester, New-York, Brisbane, Toronto, Singapure: Clarendon press, John Wiley and Sons.  1995.  P. 206.
  110.  
  111. LaFerla F.M. Calcium dyshomeostasis and intracellular signalling in Alzheimer’s disease . Nat.Rev.Neurosci. 2002.  3.  P. 862-872. CrossRef PubMed
  112.  
  113. Laird F.M., Cai H., Savonenko A.V. et al. BACE1, a major determinant of selective vulnerability of the brain to amyloid-beta amyloidogenesis, is essential for cognitive, emotional, and synaptic functions . J.Neurosci.  2005.  25.  P. 11693-11709. CrossRef PubMed PubMedCentral
  114.  
  115. Leissring M.A., Parker I., LaFerla F.M. Presenilin-2 mutations modulate amplitude and kinetics of inositol 1, 4,5-trisphosphate-mediated calcium signals . J.Biol.Chem.  1999.  274.  P. 32535-32538. CrossRef PubMed
  116.  
  117. Leissring M.A., Paul B.A., Parker I. et al. F.M. Alzheimer’s presenilin-1 mutation potentiates inositol 1,4,5-trisphosphate-mediated calcium signaling in Xenopus oocytes . J.Neurochem.  1999.  72.  P. 1061-1068. CrossRef PubMed
  118.  
  119. Levy M., Faas G.C., Saggau P. et al. Mitochondrial regulation of synaptic plasticity in the hippocampus . . J.Biol.Chem.  2003.  278.  P. 17727-17734. CrossRef PubMed
  120.  
  121. Levy-Lahad E., Lahad A., Wijsman E.M. et al. Apolipoprotein E genotypes and age of onset in earlyonset familial Alzheimer’s disease . Ann.Neurol. 1995.  38.  P. 678-680. CrossRef PubMed
  122.  
  123. Lin M.S., Chen L.Y., Wang S.S. et al. Examining the levels of ganglioside and cholesterol in cell membrane on attenuation the cytotoxicity of beta-amyloid peptide . Colloids Surf.B Biointerfaces.  2008.  65. P. 172-177. CrossRef PubMed
  124.  
  125. Liu J., Head E., Gharib A.M. et al. Memory loss in old rats is associated with brain mitochondrial decay and RNA. DNA oxidation: partial reversal by feeding acetylL-carnitine and. or R-alpha-lipoic acid . Proc. Nat. Acad. Sci.USA.  2002.  99.  P. 2356-2361. CrossRef PubMed PubMedCentral
  126.  
  127. Liu Q., Kawai H.,Berg D.K. beta-Amyloid peptide blocks the response of alpha 7-containing nicotinic receptors on hippocampal neurons . Ibid.  2001. 98.  P. 4734-4739. CrossRef PubMed PubMedCentral
  128.  
  129. Magoori K., Kang M.J., Ito M.R. et al. Severe hypercholesterolemia, impaired fat tolerance, and advanced atherosclerosis in mice lacking both low density lipoprotein receptor-related protein 5 and apolipoprotein E . J.Biol.Chem.  2003.  278.  P. 11331- 11336. CrossRef PubMed
  130.  
  131. Markham A., Cameron I., Franklin P. BDNF increases rat brain mitochondrial respiratory coupling at complex I, but not complex II . Eur.J.Neurosci.  2004.  20. P. 1189-1196. CrossRef PubMed
  132.  
  133. Matos M., Augusto E., Oliveira C.R. et al. Amyloidbeta peptide decreases glutamate uptake in cultured astrocytes: involvement of oxidative stress and mitogen-activated protein kinase cascades . Neuroscience. 2008.  156.  P. 898-910. CrossRef PubMed
  134.  
  135. Mattson M.P., Gleichmann M.,Cheng A. Mitochondria in neuroplasticity and neurological disorders . Neuron.  2008.  60.  P. 748-766. CrossRef PubMed PubMedCentral
  136.  
  137. Mattson M.P., LaFerla F.M., Chan S.L. et al. Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders . Trends Neurosci.  2000. 23.  P. 222-229. CrossRef.1016/S0166-2236(00)01548-4
  138.  
  139. Maurer I., Zierz S., Moller H.J. A selective defect of cytochrome c oxidase is present in brain of Alzheimer disease patients . Neurobiol.Aging.  2000.  21. P. 455-462. CrossRef.1016/S0197-4580(00)00112-3
  140.  
  141. Nakajima M., Miura M., Aosaki T. et al. Deficiency of presenilin-1 increases calciumdependent vulnerability of neurons to oxidative stress in vitro . J.Neurochem.  2001.  78.  P. 807-814. CrossRef PubMed
  142.  
  143. Perroy J., Prezeau L., De W.M. et al. Selective blockade of P. Q-type calcium channels by the metabotropic glutamate receptor type 7 involves a phospholipase C pathway in neurons . J.Neurosci.  2000.  20. P. 7896-7904. CrossRef PubMed PubMedCentral
  144.  
  145. Pigino G., Morfini G., Pelsman A. et al. Alzheimer’s presenilin 1 mutations impair kinesin-based axonal transport . J.Neurosci.  2003.  23.  P. 4499-4508. CrossRef PubMed PubMedCentral
  146.  
  147. Pinhei ro P.S., Mulle C. P resynaptic glutamate receptors: physiological functions and mechanisms of action . Nat.Rev.Neurosci.  2008.  9.  P. 423-436. CrossRef PubMed
  148.  
  149. Querfurth H.W., Jiang J., Geiger J.D. et al. Caffeine stimulates amyloid beta-peptide release from betaamyloid precursor protein-transfected HEK293 cells . J.Neurochem.  1997.  69.  P. 1580-1591. CrossRef PubMed
  150.  
  151. Ramsden M., Plant L.D., Webster N.J. et al. Differential effects of unaggregated and aggregated amyloid beta protein (140) on K(+) channel currents in primary cultures of rat cerebellar granule and cortical neurones . J.Neurochem.  2001.  79.  P. 699-712. CrossRef PubMed
  152.  
  153. Reddy P.H., Mani G., Park B.S., Jacques J., Murdoch G., Whetsell W., Jr., Kaye J.,Manczak M. Differential loss of synaptic proteins in Alzheimer’s disease: implications for synaptic dysfunction . J.Alzheimers. Dis.  2005.  7.  P. 103-117. CrossRef PubMed
  154.  
  155. Roy S., Coffee P., Smith G. et al. Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport . J.Neurosci. 2000.  20.  P. 6849-6861. CrossRef PubMed PubMedCentral
  156.  
  157. Rusakov D.A., Saitow F., Lehre K.P. et al. Modulation of presynaptic Ca2+ entry by AMPA receptors at individual GABAergic synapses in the cerebellum . J.Neurosci.  2005.  25.  P. 4930-4940. CrossRef PubMed PubMedCentral
  158.  
  159. Saunders A.M., Roses A.D. Apolipoprotein E4 allele frequency, ischemic cerebrovascular disease, and Alzheimer’s disease . Stroke.  1993.  24.  P. 1416-1417. CrossRef PubMed
  160.  
  161. Scragg J.L., Fearon I.M., Boyle J.P. et al. Alzheimer’s amyloid peptides mediate hypoxic up-regulation of Ltype Ca2+ channels . FASEB J.  2005.  19.  P. 150-152. CrossRef PubMed
  162.  
  163. Sherrington R., Rogaev E.I., Liang Y. et al. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer’s disease . Nature.  1995.  375. P. 754-760. CrossRef PubMed
  164.  
  165. Shuttlewo rth C.W., B rennan A.M.,Conno r J.A. NAD(P)H fluorescence imaging of postsynaptic neuronal activation in murine hippocampal slices . J.Neurosci.  2003.  23.  P. 3196-3208. CrossRef PubMed PubMedCentral
  166.  
  167. Sindreu C.B., Scheiner Z.S.,Storm D.R. Ca2+-stimulated adenylyl cyclases regulate ERK-dependent activation of MSK1 during fear conditioning . Neuron. 2007.  53.  P. 79-89. CrossRef PubMed PubMedCentral
  168.  
  169. Sisodia S.S., Annaert W., Kim S.H. et al. Gammasecretase: never more enigmatic . Trends Neurosci. 2001.  24.  P. S2-S6. CrossRef.1016/S0166-2236(01)00002-9
  170.  
  171. Small S.A., Duff K. Linking Abeta and tau in late onset Alzheimer’s disease: a dual pathway hypothesis . Neuron.  2008.  60.  P. 534-542. CrossRef PubMed PubMedCentral
  172.  
  173. Smith I.F., Hitt B., Green K.N. et al. Enhanced caffeineinduced Ca2+ release in the 3xTg-AD mouse model of Alzheimer’s disease . J.Neurochem.  2005.  94. P. 1711-1718. CrossRef PubMed
  174.  
  175. Steele P.M., Mauk M.D. Inhibitory control of LTP and LTD: stability of synapse strength . J.Neurophysiol.  1999.  81.  P. 1559-1566. CrossRef PubMed
  176.  
  177. Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory . Curr.Opin.Neurobiol. 2004.  14.  P. 311-317. CrossRef PubMed
  178.  
  179. Tamagno E., Parola M., Guglielmotto M. et al. Multiple signaling events in amyloid beta-induced, oxidative stress-dependent neuronal apoptosis . Free Radic.Biol.Med.  2003.  35.  P. 45-58. CrossRef.1016/S0891-5849(03)00244-2
  180.  
  181. Trimmer P.A., Swerdlow R.H., Parks J.K. et al. Abnormal mitochondrial morphology in sporadic Parkinson’s and Alzheimer’s disease cybrid cell lines . . Exp.Neurol.  2000.  162.  P. 37-50. CrossRef PubMed
  182.  
  183. Tu H., Nelson O., Bezprozvanny A. et al. Presenilins form ER Ca2+ leak channels, a function disrupted by familial Alzheimer’s disease-linked mutations . Cell. 2006.  126.  P. 981-993. CrossRef PubMed PubMedCentral
  184.  
  185. Vaisid T., Barnoy S.,Kosower N.S. Calpastatin overexpression attenuates amyloid-beta-peptide toxicity in differentiated PC12 cells . Neuroscience. 2008.  156.  P. 921-931. CrossRef PubMed
  186.  
  187. Weiss J.H., Pike C.J.,Cotman C.W. Ca 2+ channel blockers attenuate beta-amyloid peptide toxicity to cortical neurons in culture . J.Neurochem.  1994. 62.  P. 372-375. CrossRef PubMed
  188.  
  189. White F., Nicoll J.A., Roses A.D. et al. Impaired neuronal plasticity in transgenic mice expressing human apolipoprotein E4 compared to E3 in a model of entorhinal cortex lesion . Neurobiol.Dis.  2001.  8. P. 611-625. CrossRef PubMed
  190.  
  191. Wong S.T., Athos J., Figueroa X.A. et al. Calciumstimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP . Neuron.  1999.  23.  P. 787-798. CrossRef.1016/S0896-6273(01)80036-2
  192.  
  193. Wu A., Derrico C.A., Hatem L. et al. Alzheimer’s amyloid-beta peptide inhibits sodium. calcium exchange measured in rat and human brain plasma membrane vesicles . Neuroscience.  1997.  80.  P. 675-684. CrossRef.1016/S0306-4522(97)00053-5
  194.  
  195. Wu Z.L., Thomas S.A., Villacres E.C. et al. Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice . Proc.Nat.Acad.Sci. USA.  1995. 92.  P. 220-224. CrossRef PubMed PubMedCentral
  196.  
  197. Yankner B.A., Duffy L.K.,Kirschner D.A. Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides . Science.  1990. 250.  P. 279-282. CrossRef PubMed
  198.  
  199. Yoo A.S., Cheng I., Chung S. et al. Presenilin-mediated modulation of capacitative calcium entry . Neuron. 2000.  27.  P. 561-572. CrossRef.1016/S0896-6273(00)00066-0
  200.  
  201. Yuan L.L., Adams J.P., Swank M. et al. Protein kinase modulation of dendritic K+  channels in hippocampus involves a mitogen-activated protein kinase pathway . . J.Neurosci.  2002.  22.  P. 4860-4868. CrossRef PubMed PubMedCentral
  202.  
  203. Zheng Z., Keifer J. Protein kinase C-dependent and independent signaling pathways regulate synaptic GluR1 and GluR4 AMPAR subunits during in vitro classical conditioning . Neuroscience.  2008.  156.  P. 872-884. CrossRef PubMed PubMedCentral

© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2025.