Українська Русский English

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

Fiziologichnyi Zhurnal

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  
  18. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes . Acta Neuropathol.  1991. 82.  P. 239-259. CrossRef PubMed
  19.  
  20. 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
  21.  
  22. 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
  23.  
  24. 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
  25.  
  26. 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  
  27. 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
  28.  
  29. 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
  30.  
  31. 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  
  32. 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
  33.  
  34. Cochilla A.J., Alford S. Metabotropic glutamate receptor-mediated control of neurotransmitter release . Ibid.  1998.  20.  P. 1007-1016. CrossRef  
  35. 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
  36.  
  37. 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
  38.  
  39. Dejda A., Sokolowska P., Nowak J.Z. Neuroprotective potential of three neuropeptides PACAP, VIP and PHI . Pharmacol.Rep.  2005.  57.  P. 307-320.
  40.  
  41. 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  
  42. Duchen M.R. Roles of mitochondria in health and disease . Diabetes.  2004.  53 Suppl 1.  P. S96-102. CrossRef PubMed
  43.  
  44. 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
  45.  
  46. 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
  47.  
  48. 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
  49.  
  50. Gend ron T.F., Pet rucelli L. The role o f tau in neurodegeneration . Mol.Neurodegener.  2009.  4. P. 13. CrossRef PubMed PubMedCentral
  51.  
  52. 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
  53.  
  54. 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
  55.  
  56. 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
  57.  
  58. Green K.N., LaFerla F.M. Linking calcium to Abeta and Alzheimer’s disease . Neuron.  2008.  59. P. 190-194. CrossRef PubMed
  59.  
  60. Hardy J. A hundred years of Alzheimer ’s disease research . Ibid.  2006.  52.  P. 313. CrossRef PubMed
  61.  
  62. Alzheimer’s disease: the amyloid cascade hypothesis: an update and reappraisal . J.Alzheimers.Dis.  2006. 9.  P. 151-153. CrossRef PubMed
  63.  
  64. Hardy J. Does Abeta 42 have a function related to blood homeostasis? . Neurochem.Res.  2007.  32. P. 833-835. CrossRef PubMed
  65.  
  66. 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
  67.  
  68. 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  
  69. 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
  70.  
  71. Hollenbeck P.J., Saxton W.M. The axonal transport of mitochondria . J.Cell Sci.  2005.  118.  P. 5411-5419. CrossRef PubMed PubMedCentral
  72.  
  73. 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  
  74. 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
  75.  
  76. 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
  77.  
  78. 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
  79.  
  80. 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
  81.  
  82. 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
  83.  
  84. 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
  85.  
  86. 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
  87.  
  88. 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
  89.  
  90. 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  
  91. 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  
  92. 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.
  93.  
  94. 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
  95.  
  96. 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  
  97. 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  
  98. 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.
  99.  
  100. LaFerla F.M. Calcium dyshomeostasis and intracellular signalling in Alzheimer’s disease . Nat.Rev.Neurosci. 2002.  3.  P. 862-872. CrossRef PubMed
  101.  
  102. 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
  103.  
  104. 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
  105.  
  106. 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
  107.  
  108. 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
  109.  
  110. 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
  111.  
  112. 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
  113.  
  114. 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
  115.  
  116. 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
  117.  
  118. 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
  119.  
  120. 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
  121.  
  122. 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
  123.  
  124. Mattson M.P., Gleichmann M.,Cheng A. Mitochondria in neuroplasticity and neurological disorders . Neuron.  2008.  60.  P. 748-766. CrossRef PubMed PubMedCentral
  125.  
  126. 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  
  127. 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  
  128. 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
  129.  
  130. 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
  131.  
  132. 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
  133.  
  134. 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
  135.  
  136. 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
  137.  
  138. 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
  139.  
  140. 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
  141.  
  142. 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
  143.  
  144. 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
  145.  
  146. 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
  147.  
  148. 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
  149.  
  150. 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
  151.  
  152. 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
  153.  
  154. 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
  155.  
  156. Sisodia S.S., Annaert W., Kim S.H. et al. Gammasecretase: never more enigmatic . Trends Neurosci. 2001.  24.  P. S2-S6. CrossRef  
  157. 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
  158.  
  159. 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
  160.  
  161. 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
  162.  
  163. Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory . Curr.Opin.Neurobiol. 2004.  14.  P. 311-317. CrossRef PubMed
  164.  
  165. 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  
  166. 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
  167.  
  168. 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
  169.  
  170. 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
  171.  
  172. 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
  173.  
  174. 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
  175.  
  176. 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  
  177. 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  
  178. 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
  179.  
  180. 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
  181.  
  182. Yoo A.S., Cheng I., Chung S. et al. Presenilin-mediated modulation of capacitative calcium entry . Neuron. 2000.  27.  P. 561-572. CrossRef  
  183. 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
  184.  
  185. 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, 2014-2019.