MOLECULAR AND CELLULAR MECHANISMS OF ALZHEIMERS 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 Alzheimers and Parkinsons diseases
are the most frequent. Alzheimers 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 Alzheimers disease.
Keywords:
Alzheimers disease, amyloid, calcium homeostasis, synaptic plasticity, mitochondria, endoplasmic reticulum, calcium channels.
References
- 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
- 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
- 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 Alzheimers disease . Ann.N.Y.Acad.Sci. 1994. 747. P. 256-266.
CrossRef
PubMed
- 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
- 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
- Beal M.F. Oxidative damage as an early marker of Alzheimers disease and mild cognitive impairment . Neurobiol.Aging. 2005. 26. P. 585-586.
CrossRef
PubMed
- 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
- 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
- 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 Alzheimers disease . Neurobiol.Aging. 2002. 23. P. 371-376.
CrossRef
- Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes . Acta Neuropathol. 1991. 82. P. 239-259.
CrossRef
PubMed
- 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
- 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
- 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
- Butterfield D.A., Drake J., Pocernich C. et al. Evidence of oxidative damage in Alzheimers disease brain: central role for amyloid beta-peptide . Trends Mol.Med. 2001. 7. P. 548-554.
CrossRef
- 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
- 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
- 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
- Cheung K.H., Shineman D., Muller M. et al. Mechanism of Ca2+ disruption in Alzheimers disease by presenilin regulation of InsP3 receptor channel gating . Neuron. 2008. 58. P. 871-883.
CrossRef
PubMed PubMedCentral
- Cochilla A.J., Alford S. Metabotropic glutamate receptor-mediated control of neurotransmitter release . Ibid. 1998. 20. P. 1007-1016.
CrossRef
- 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
- 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
- Dejda A., Sokolowska P., Nowak J.Z. Neuroprotective potential of three neuropeptides PACAP, VIP and PHI . Pharmacol.Rep. 2005. 57. P. 307-320.
- 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
- Duchen M.R. Roles of mitochondria in health and disease . Diabetes. 2004. 53 Suppl 1. P. S96-102.
CrossRef
PubMed
- 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
- 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 Alzheimers disease . Neurobiol.Dis. 2002. 9. P. 305-318.
CrossRef
PubMed
- 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
- Gend ron T.F., Pet rucelli L. The role o f tau in neurodegeneration . Mol.Neurodegener. 2009. 4. P. 13.
CrossRef
PubMed PubMedCentral
- 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
- 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
- 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
- Green K.N., LaFerla F.M. Linking calcium to Abeta and Alzheimers disease . Neuron. 2008. 59. P. 190-194.
CrossRef
PubMed
- Hardy J. A hundred years of Alzheimer s disease research . Ibid. 2006. 52. P. 313.
CrossRef
PubMed
- Alzheimers disease: the amyloid cascade hypothesis: an update and reappraisal . J.Alzheimers.Dis. 2006. 9. P. 151-153.
CrossRef
PubMed
- Hardy J. Does Abeta 42 have a function related to blood homeostasis? . Neurochem.Res. 2007. 32. P. 833-835.
CrossRef
PubMed
- Harris F.M., Tesseur I., Brecht W.J. et al. Astroglial regulation of apolipoprotein E expression in neuronal cells. Implications for Alzheimers disease . J.Biol. Chem. 2004. 279. P. 3862-3868.
CrossRef
PubMed
- 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
- 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
- Hollenbeck P.J., Saxton W.M. The axonal transport of mitochondria . J.Cell Sci. 2005. 118. P. 5411-5419.
CrossRef
PubMed PubMedCentral
- Holmes C., Boche D., Wilkinson D. et al. Long-term effects of Abeta42 immunisation in Alzheimers disease: follow-up of a randomised, placebocontrolled phase I trial . Lancet. 2008. 372. P. 216-223.
CrossRef
- 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
- 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
- Huang Y., Liu X.Q., Wyss-Coray T. et al. Apolipoprotein E fragments present in Alzheimers disease brains induce neurofibrillary tangle-like intracellular inclusions in neurons . Proc.Natl.Acad.Sci.USA. 2001. 98. P. 8838-8843.
CrossRef
PubMed PubMedCentral
- 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
- 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
- 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
- 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 Alzheimers disease . Proc. Nat. Acad. Sci.USA. 1999. 96. P. 2099-2103.
CrossRef
PubMed PubMedCentral
- 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
- 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
- Kawahara M., Arispe N., Kuroda Y. et al. Alzheimers 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
- Kawahara M., Kuroda Y. Molecular mechanism of neuronal death in Alzheimers disease: Ca(2+)-channel formation of beta amyloid protein molecules] . Tanpakushitsu Kakusan Koso. 1997. 42. P. 2002-2010.
- 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
- 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
- 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
- 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.
- LaFerla F.M. Calcium dyshomeostasis and intracellular signalling in Alzheimers disease . Nat.Rev.Neurosci. 2002. 3. P. 862-872.
CrossRef
PubMed
- 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
- 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
- Leissring M.A., Paul B.A., Parker I. et al. F.M. Alzheimers presenilin-1 mutation potentiates inositol 1,4,5-trisphosphate-mediated calcium signaling in Xenopus oocytes . J.Neurochem. 1999. 72. P. 1061-1068.
CrossRef
PubMed
- 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
- Levy-Lahad E., Lahad A., Wijsman E.M. et al. Apolipoprotein E genotypes and age of onset in earlyonset familial Alzheimers disease . Ann.Neurol. 1995. 38. P. 678-680.
CrossRef
PubMed
- 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
- 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
- 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
- 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
- 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
- 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
- Mattson M.P., Gleichmann M.,Cheng A. Mitochondria in neuroplasticity and neurological disorders . Neuron. 2008. 60. P. 748-766.
CrossRef
PubMed PubMedCentral
- 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
- 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
- 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
- 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
- Pigino G., Morfini G., Pelsman A. et al. Alzheimers presenilin 1 mutations impair kinesin-based axonal transport . J.Neurosci. 2003. 23. P. 4499-4508.
CrossRef
PubMed PubMedCentral
- 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
- 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
- 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
- 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 Alzheimers disease: implications for synaptic dysfunction . J.Alzheimers. Dis. 2005. 7. P. 103-117.
CrossRef
PubMed
- 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
- 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
- Saunders A.M., Roses A.D. Apolipoprotein E4 allele frequency, ischemic cerebrovascular disease, and Alzheimers disease . Stroke. 1993. 24. P. 1416-1417.
CrossRef
PubMed
- Scragg J.L., Fearon I.M., Boyle J.P. et al. Alzheimers amyloid peptides mediate hypoxic up-regulation of Ltype Ca2+ channels . FASEB J. 2005. 19. P. 150-152.
CrossRef
PubMed
- Sherrington R., Rogaev E.I., Liang Y. et al. Cloning of a gene bearing missense mutations in early-onset familial Alzheimers disease . Nature. 1995. 375. P. 754-760.
CrossRef
PubMed
- 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
- 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
- Sisodia S.S., Annaert W., Kim S.H. et al. Gammasecretase: never more enigmatic . Trends Neurosci. 2001. 24. P. S2-S6.
CrossRef
- Small S.A., Duff K. Linking Abeta and tau in late onset Alzheimers disease: a dual pathway hypothesis . Neuron. 2008. 60. P. 534-542.
CrossRef
PubMed PubMedCentral
- Smith I.F., Hitt B., Green K.N. et al. Enhanced caffeineinduced Ca2+ release in the 3xTg-AD mouse model of Alzheimers disease . J.Neurochem. 2005. 94. P. 1711-1718.
CrossRef
PubMed
- 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
- Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory . Curr.Opin.Neurobiol. 2004. 14. P. 311-317.
CrossRef
PubMed
- 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
- Trimmer P.A., Swerdlow R.H., Parks J.K. et al. Abnormal mitochondrial morphology in sporadic Parkinsons and Alzheimers disease cybrid cell lines . . Exp.Neurol. 2000. 162. P. 37-50.
CrossRef
PubMed
- Tu H., Nelson O., Bezprozvanny A. et al. Presenilins form ER Ca2+ leak channels, a function disrupted by familial Alzheimers disease-linked mutations . Cell. 2006. 126. P. 981-993.
CrossRef
PubMed PubMedCentral
- 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
- 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
- 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
- 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
- Wu A., Derrico C.A., Hatem L. et al. Alzheimers amyloid-beta peptide inhibits sodium. calcium exchange measured in rat and human brain plasma membrane vesicles . Neuroscience. 1997. 80. P. 675-684.
CrossRef
- 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
- 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
- Yoo A.S., Cheng I., Chung S. et al. Presenilin-mediated modulation of capacitative calcium entry . Neuron. 2000. 27. P. 561-572.
CrossRef
- 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
- 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
|