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Stress-induced alternative splicing of acetylcholinesterase results in enhanced fear memory and long-term potentiation
Open accessAbstract
Stress insults intensify fear memory; however, the mechanism(s) facilitating this physiological response is still unclear. Here, we report the molecular, neurophysiological and behavioral findings attributing much of this effect to alternative splicing of the acetylcholinesterase (AChE) gene in hippocampal neurons. As a case study, we explored immobilization-stressed mice with intensified fear memory and enhanced long-term potentiation (LTP), in which alternative splicing was found to induce overproduction of neuronal 'readthrough' AChE-R (AChE-R). Selective downregulation of AChE-R mRNA and protein by antisense oligonucleotides abolished the stress-associated increase in AChE-R, the elevation of contextual fear and LTP in the hippocampal CA1 region. Reciprocally, we intrahippocampally injected a synthetic peptide representing the C-terminal sequence unique to AChE-R. The injected peptide, which has been earlier found to exhibit no enzymatic activity, was incorporated into cortical, hippocampal and basal nuclei neurons by endocytosis and retrograde transport and enhanced contextual fear. Compatible with this hypothesis, inherited AChE-R overexpression in transgenic mice resulted in perikaryal clusters enriched with PKCbetaII, accompanied by PKC-augmented LTP enhancement. Our findings demonstrate a primary role for stress-induced alternative splicing of the AChE gene to elevated contextual fear and synaptic plasticity, and attribute to the AChE-R splice variant a major role in…
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“The ability of ACh to induce synaptic plasticity through actions on pre- and post-synaptic nAChRs and mAChRs is likely to modulate learning and memory, including memory of stressful events (Nijholt et al., 2004)”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Nijholt et al., 2004
In the citing paper
“Stress also induces alternative splicing of the AChE mRNA in the hippocampus leading to altered ACh signaling in this structure (Nijholt et al., 2004).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Nijholt et al., 2004
Citations
Cites
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859
The molecular biology of memory storage: a dialogue between genes and synapses
Kandel, E. R. (2001) · Science · doi:10.1126/science.1067020 · Cited by 3,917
Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.
Phillips, R. G., & LeDoux, J. E. (1992) · Behavioral Neuroscience · doi:10.1037/0735-7044.106.2.274 · Cited by 3,292
mouse brain in stereotaxic coordinates
Franklin, K. B. J., & Paxinos, G. (1997) · Cited by 3,258
Dynamics of the Hippocampal Ensemble Code for Space
Wilson, M. A., & McNaughton, B. L. (1993) · Science · doi:10.1126/science.8351520 · Cited by 2,350
The stressed hippocampus, synaptic plasticity and lost memories
Kim, J. J., & Diamond, D. M. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn849 · Cited by 1,543
Smith, M., Makino, S., Květňanský, R., & Post, R. M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-01768.1995 · Cited by 1,449
Acetylcholinesterase — new roles for an old actor
Soreq, H., & Seidman, S. (2001) · Nature reviews. Neuroscience · doi:10.1038/35067589 · Cited by 1,437
Self-citationStress and cognition: are corticosteroids good or bad guys?
de Kloet, E. R., Oitzl, M. S., & Joëls, M. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01438-1 · Cited by 1,258
Neuroligin Expressed in Nonneuronal Cells Triggers Presynaptic Development in Contacting Axons
Scheiffele, P., Fan, J., Choih, J., Fetter, R., & Serafini, T. (2000) · Cell · doi:10.1016/s0092-8674(00)80877-6 · Cited by 1,218
Cited by
Sorted by citations
Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.036 · Cited by 1,404
“Stress also induces alternative splicing of the AChE messenger RNA (mRNA) in the hippocampus, leading to altered ACh signaling in this structure (Nijholt et al., 2004).”
BackgroundStress effects in the hippocampus: Synaptic plasticity and memory
Kim, J. J., Song, E. Y., Kim, J. J., Song, E. Y., & Kosten, T. A. (2006) · Stress · doi:10.1080/10253890600678004 · Cited by 261
“Recent studies have reported that stress enhances hippocampal-dependent aversive tasks (i.e. trace eyeblink conditioning and contextual fear conditioning) (Beylin and Shors 1998; Nijholt et al. 2004).”
BackgroundChapter 8 Synaptic plasticity in learning and memory: Stress effects in the hippocampus
Howland, J. G., & Wang, Y. T. (2008) · Progress in brain research · doi:10.1016/s0079-6123(07)00008-8 · Cited by 243
“Interestingly, acute stress also enhances memory in aversive hippocampal-dependent tasks such as contextual fear conditioning and trace eye-blink conditioning (Beylin and Shors, 1998; Nijholt et al., 2004), thereby demonstrating that the effects of stress may differ in aversively motivated contexts.”
BackgroundCholinergic regulation of mood: from basic and clinical studies to emerging therapeutics
Dulawa, S. C., & Janowsky, D. S. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0219-x · Cited by 187
“Furthermore, stress induces alternative splicing of AChE mRNAs and modulation of AChE activity 82, 83 .”
BackgroundNeuromodulation by acetylcholine: examples from schizophrenia and depression
Higley, M. J., & Picciotto, M. R. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.06.004 · Cited by 184
“Exposure to an acute stress may lead to adaptive behavioral responses mediated through ACh release in the hippocampus, whereas chronic increases in ACh signaling can lead to mood disorders, perhaps by evoking synaptic plasticity in different neuronal subtypes throughout the hippocampus [88] and contributing to encodin…”
Aisa, B., Elizalde, N., Tordera, R. M., Lasheras, B., Rı́o, J. D., & Ramírez, M. J. (2009) · Hippocampus · doi:10.1002/hipo.20586 · Cited by 184
“…there is a substantial literature on the effects of stress on memory from behavioral and pharmacologic perspectives, there is still an insufficient understanding of the molecular mechanisms involved in the modulation of memory and brain plasticity by stress (McEwen, 1997; Nijholt et al., 2004).”
BackgroundVirtues and woes of AChE alternative splicing in stress-related neuropathologies
Meshorer, E., & Soreq, H. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.02.005 · Cited by 176
Self-citationShaltiel, G., Hanan, M., Wolf, Y., Barbash, S., Kovalev, E., Shoham, S., & Soreq, H. (2012) · Brain Structure and Function · doi:10.1007/s00429-011-0376-z · Cited by 173
Self-citationTermination and beyond: acetylcholinesterase as a modulator of synaptic transmission
Zimmerman, G., & Soreq, H. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0239-8 · Cited by 171
Self-citationWhich acetylcholinesterase functions as the main catalytic enzyme in the Class Insecta?
Kim, Y. H., & Lee, S. H. (2012) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2012.11.004 · Cited by 140
Acute and long‐term consequences of exposure to organophosphate nerve agents in humans
Figueiredo, T. H., Apland, J. P., Braga, M. F. M., & Marini, A. M. (2018) · Epilepsia · doi:10.1111/epi.14500 · Cited by 137
RACK1 has the nerve to act: Structure meets function in the nervous system
Sklan, E. H., Podoly, E., & Soreq, H. (2006) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2005.12.002 · Cited by 130
Self-citationSklan, E. H., Lowenthal, A., Korner, M., Ritov, Y., Landers, D. M., Rankinen, T., Bouchard, C., Leon, A. S., Rice, T., Rao, D. C., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307659101 · Cited by 130
Self-citationDiamond, D. M., Park, C. R., Campbell, A. M., & Woodson, J. C. (2005) · Hippocampus · doi:10.1002/hipo.20107 · Cited by 128
“…al., 1999; Izquierdo et al., 2001, 2003; Kim and Diamond, 2002; Woodson et al., 2003; Xiong et al., 2003; Conrad et al., 2004; El Hage et al., 2004; Nijholt et al., 2004; Kim et al., 2005; Park et al., 2005; Radecki et al., 2005) and people (Kirschbaum et al., 1996; Eichenbaum, 1999; Strange et…”
BackgroundSandi, C., Woodson, J. C., Haynes, V. F., Park, C. R., Touyarot, K., Lopez-Fernandez, M. A., Venero, C., & Diamond, D. M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.12.034 · Cited by 122
Iwamoto, Y., Morinobu, S., Takahashi, T., & Yamawaki, S. (2006) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2006.12.010 · Cited by 106
Whitehead, G., Jo, J., Hogg, E. L., Piers, T. M., Kim, D.-H., Seaton, G., Seok, H., Bru‐Mercier, G., Son, G. H., Regan, P. L., et al. (2013) · Brain · doi:10.1093/brain/awt293 · Cited by 110
“There is strong evidence to support the notion that acute stress can facilitate memory through enhanced synaptic plasticity (Conrad et al., 1999; Blank et al., 2002; Hui et al., 2004; Nijholt et al., 2004; Yuen et al., 2011), though the mechanism underlying this process is unknown.”
BackgroundChanges in readthrough acetylcholinesterase expression modulate amyloid-beta pathology
Berson, A., Knobloch, M., Hanan, M., Diamant, S., Sharoni, M. A., Schuppli, D., Geyer, B. C., Ravid, R., Mor, T. S., Nitsch, R. M., et al. (2007) · Brain · doi:10.1093/brain/awm276 · Cited by 106
“…of AChE-R protects neurons from both aging (Sternfeld et al., 2000) and Ab-induced neuropathologies, and that it elevates hippocampal longterm potentiation (Nijholt et al., 2004) supports the notion that the selective loss of AChE-R has a pivotal role in the Ab-induced toxicity in AD.”
BackgroundSelf-citationThe intracrine hypothesis: An update
Ré, R. N., & Cook, J. L. (2005) · Regulatory Peptides · doi:10.1016/j.regpep.2005.09.012 · Cited by 101
ACBD2/ECI2-Mediated Peroxisome-Mitochondria Interactions in Leydig Cell Steroid Biosynthesis
Fan, J., Li, X., Issop, L., Culty, M., & Papadopoulos, V. (2016) · Molecular Endocrinology · doi:10.1210/me.2016-1008 · Cited by 102
Rinwa, P., & Kumar, A. (2012) · Brain Research · doi:10.1016/j.brainres.2012.10.002 · Cited by 98
“Stress has been well documented to induce alterations in activity of acetylcholinesterase enzyme (Nijholt et al., 2004).”
BackgroundOmri, A. E., Han, J., Yamada, P., Kawada, K., Abderrabba, M., & Isoda, H. (2010) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2010.07.006 · Cited by 88
Gawali, N. B., Bulani, V. D., Gursahani, M., Deshpande, P. S., Kothavade, P. S., & Juvekar, A. R. (2017) · Brain Research · doi:10.1016/j.brainres.2017.03.004 · Cited by 92
Kroes, R. A., Burgdorf, J. S., Otto, N. J., Panksepp, J., & Moskal, J. R. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.03.022 · Cited by 81
Anxiety and panic: from human studies to animal research and back
Battaglia, M., & Ogliari, A. L. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.06.013 · Cited by 79
CREB Regulates AChE-R-Induced Proliferation of Human Glioblastoma Cells
Perry, C., Sklan, E. H., & Soreq, H. (2004) · Neoplasia · doi:10.1593/neo.03424 · Cited by 70
“There is also recent immunocytochemical evidence demonstrating the cytosolic localization of neuronal AChE-R [35].”
BackgroundSelf-citationGrisaru, D., Pick, M., Perry, C., Sklan, E. H., Almog, R., Goldberg, I., Naparstek, E., Lessing, J. B., Soreq, H., & Deutsch, V. R. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.1.27 · Cited by 64
“Our current findings attribute much of this effect to the cleavable, cellpenetrating C-terminal peptide of AChE-R (29), which accumulates in the human circulation under stress (24).”
BackgroundSelf-citationAChE and the amyloid precursor protein (APP) – Cross-talk in Alzheimer's disease
Nalivaeva, N. N., & Turner, A. J. (2016) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2016.04.009 · Cited by 60
Zimmermann, M. (2013) · British Journal of Pharmacology · doi:10.1111/bph.12359 · Cited by 60
“, 2008): as both in vitro and in vivo work shows, powerful inductors for AChE-R are stress, for example, forced swim stress, continuous use as well as toxic concentrations of AChE inhibitors or inflammation (Kaufer et al., 1998; Nijholt et al., 2004; Dori et al., 2007; Evron et al., 2007), with stress-inducible change…”
BackgroundZimmerman, G., Shaltiel, G., Barbash, S., Cohen, J., Gasho, C. J., Shenhar‐Tsarfaty, S., Shalev, H., Berliner, S. A., Shelef, I., Shoham, S., et al. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.4 · Cited by 55
“shock-stressed mice.(35) The current study’s aim was to test the long-term effects of ODN mEN101 and its human ortholog BL7040(36) on inflammation, anxiety and the inter-relationships”
BackgroundSelf-citationThe adaptive and maladaptive continuum of stress responses – a hippocampal perspective
Suri, D., & Vaidya, V. A. (2015) · Reviews in the Neurosciences · doi:10.1515/revneuro-2014-0083 · Cited by 66
Roca, C., Requena-Triguero, C., Sebastián-Pérez, V., Malhotra, S., Radoux, C. J., Pérez, C., Martı́nez, A., Paez, J. A., Blundell, T. L., & Campillo, N. E. (2018) · Journal of Enzyme Inhibition and Medicinal Chemistry · doi:10.1080/14756366.2018.1476502 · Cited by 54
“Acetylcholinesterase (AChE) is a well-known enzyme for the hydrolysis of the neurotransmitter acetylcholine (ACh) 1 – 4 , being the target of the main marketed pharmacological treatment of Alzheimer ’ s disease (AD).”
BackgroundOstroveanu, A., van der Zee, E. A., Eisel, U. L. M., Schmidt, M., & Nijholt, I. M. (2009) · Hippocampus · doi:10.1002/hipo.20700 · Cited by 52
“RT-PCR was performed using Superscript III One-Step RT-PCR with Platinum Taq DNA Polymerase (Invitrogen, 12574) as described before (Nijholt et al., 2004).”
MethodSelf-citationRinwa, P., & Kumar, A. (2013) · Archives of Pharmacal Research · doi:10.1007/s12272-013-0205-4 · Cited by 52
“ACh is degraded by the enzyme acetylcholinesterase, which gets modified on stress exposure (Nijholt et al. 2004).”
BackgroundCytokines and cholinergic signals co-modulate surgical stress-induced changes in mood and memory
Shapira‐Lichter, I., Beilin, B., Ofek, K., Bessler, H., Gruberger, M., Shavit, Y., Seror, D., Grinevich, G., Posner, E., Reichenberg, A., et al. (2007) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.09.006 · Cited by 47
Self-citationDong, H., Xiang, Y.-Y., Farchi, N., Ju, W., Wu, Y., Chen, L., Wang, Y., Hochner, B., Yang, B., Soreq, H., et al. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2106-04.2004 · Cited by 56
“Excess AChE emerges under conditions of stress (Meshorer et al., 2002; Nijholt et al., 2004) and exposure to AChE inhibitors (Kaufer et al., 1998).”
Self-citationVeena, J., Srikumar, B. N., Mahati, K., Raju, T. R., & Rao, B. S. S. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2279-3 · Cited by 46
“Acetylcholine (ACh) is among the neurotransmitters that influence neurogenesis.”
BackgroundInfluentialCrowding, an environmental stressor, blocks long-term memory formation in Lymnaea
Caigny, P. D., & Lukowiak, K. (2008) · Journal of Experimental Biology · doi:10.1242/jeb.020347 · Cited by 43
“Equally, LTM can be enhanced through fearful stressors (Blank et al., 2002; Nijholt et al., 2004; Orr and Lukowiak, 2008).”
BackgroundGilboa-Geffen, A., Hartmann, G., & Soreq, H. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00030 · Cited by 45
Self-citationLópez-Granero, C., Cañadas, F., Cardona, D., Yu, Y., Giménez, E., Lozano, R., Ávila, D. S., Aschner, M., & Sánchez-Santed, F. (2012) · Toxicological Sciences · doi:10.1093/toxsci/kfs280 · Cited by 42
“bound properties of AChE (Meshorer and Soreq, 2006; Nijholt et al., 2004) as well as the”
BackgroundChauhan, N. B., & Siegel, G. J. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.01.008 · Cited by 40
Cocaine‐ or stress‐induced metaplasticity of LTP in the dorsal and ventral hippocampus
Keralapurath, M. M., Clark, J. K., Hammond, S., & Wagner, J. J. (2014) · Hippocampus · doi:10.1002/hipo.22250 · Cited by 37
“…assessing the effects of stress on hippocampal dependent tasks, where performance is influenced by stress either positively (Luine et al., 1993; Nijholt et al., 2004) in the vH (where LTP is increased) or negatively (Beylin and Shors, 1998; Diamond et al., 1996) in the dH (where LTP is…”
BackgroundAntunes‐Martins, A., Keiko, M., Irvine, E. E., Lepicard, E. M., & Giese, K.-P. (2007) · Learning & Memory · doi:10.1101/lm.640307 · Cited by 38
“…suggests that alternative splicing is an important, but not well understood mechanism of brain plasticity (Bottai et al. 2002; Lee and Irizarry 2003; Nijholt et al. 2004; O’Connor et al. 2004; Rattiner et al. 2004; Beffert et al. 2005), we studied the expression of Srp20 and Psf in more detail.”
BackgroundThe thymic theme of acetylcholinesterase splice variants in myasthenia gravis
Gilboa-Geffen, A., Lacoste, P. P., Soreq, L., Cizeron-Clairac, G., Panse, R. L., Truffault, F., Shaked, I., Soreq, H., & Berrih‐Aknin, S. (2007) · Blood · doi:10.1182/blood-2006-07-033373 · Cited by 37
Self-citationNon‐hydrolytic functions of acetylcholinesterase
Greenfield, S. A., Zimmermann, M., & Bond, C. E. (2008) · FEBS Journal · doi:10.1111/j.1742-4658.2007.06235.x · Cited by 35
Kim, S., Kim, K., Lee, J. H., Han, S. H., & Lee, S. H. (2019) · Scientific Reports · doi:10.1038/s41598-019-46842-0 · Cited by 35
Evron, T., Geyer, B. C., Cherni, I., Muralidharan, M., Kilbourne, J. A., Fletcher, S. P., Soreq, H., & Mor, T. S. (2007) · The FASEB Journal · doi:10.1096/fj.07-8112com · Cited by 35
“AChE-R overproduction quickly restores the cholinergic balance by increasing ACh hydrolysis potential throughout the circulation; however, persistent overproduction of AChE-R associates with overproduction of proinflammatory cytokines (46), behavioral impairments (29), declarative memory loss (47), muscle malfunctioni…”
BackgroundSelf-citationLópez-Granero, C., Cardona, D., Giménez, E., Lozano, R., Barril, J., Sánchez-Santed, F., & Cañadas, F. (2013) · Toxicology · doi:10.1016/j.tox.2013.03.009 · Cited by 33
Mechanisms of Disease: intracrine physiology in the cardiovascular system
Ré, R. N., & Cook, J. L. (2007) · Nature Clinical Practice Cardiovascular Medicine · doi:10.1038/ncpcardio0985 · Cited by 32
Chen, G., & Miller, G. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062217 · Cited by 32
“Indeed, AS is modulated by the circadian clock, psychological stress, and numerous hormones and chemicals [8–10], while an estimated 15–60% of human genetic diseases, ranging from neurological to tumorigenic and metabolic disorders, involve splicing mutations [2,11–14].”
BackgroundPresenilin 1 Interacts with Acetylcholinesterase and Alters Its Enzymatic Activity and Glycosylation
Silveyra, M. X., Evin, G. M., Montenegro, M. F., Vidal, C. J., Martı́nez, S., Culvenor, J. G., & Sáez‐Valero, J. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.02065-07 · Cited by 32
“Multiple lines of evidence point to the participation and/or modulation of these processes by AChE (48, 62, 73, 81).”
BackgroundDori, A., & Soreq, H. (2006) · Journal of Molecular Neuroscience · doi:10.1385/jmn:28:3:247 · Cited by 31
“from AChE-R is a key element in the induction of contextual fear conditioning, we tested its capacity to induce or imitate stress reactions (Nijholt et al., 2004).”
Self-citationLópez-Granero, C., Cardona, D., Giménez, E., Lozano, R., Barril, J., Aschner, M., Sánchez-Santed, F., & Cañadas, F. (2013) · NeuroToxicology · doi:10.1016/j.neuro.2013.11.004 · Cited by 30
Evron, T., Greenberg, D., Mor, T. S., & Soreq, H. (2006) · Toxicology · doi:10.1016/j.tox.2006.08.018 · Cited by 29
Self-citationKye, M. J., Spiess, J., & Blank, T. (2007) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-006-9320-6 · Cited by 27
“Thus far, little is known about the downstream effectors for the neuroendocrine response to stressful events [3–6].”
BackgroundSelf-citationDarreh‐Shori, T., Rezaeianyazdi, S., Lana, E., Mitra, S., Gellerbring, A., Karami, A., Bogdanović, N., Lithner, C. U., Winblad, B. G., & Behbahani, H. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1383-3 · Cited by 28
Cholinergic neurotransmission in the basolateral amygdala during cued fear extinction
Kellis, D. M., Kaigler, K. F., Witherspoon, E., Fadel, J. R., & Wilson, M. A. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100279 · Cited by 29
“Various stressors can alter ACHE enzyme activity and alter the expression of ACHE splice variants in multiple brain regions including amygdala (Kaufer et al., 1998; Birikh et al., 2003; Nijholt et al., 2004; Sklan et al., 2004; Das et al., 2005; Meshorer et al., 2005; Perrier et al., 2005; Salmon et al., 2005; Dori et…”
BackgroundAdamec, R. E., HEAD, D. W., Soreq, H., & Blundell, J. J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.12.023 · Cited by 28
Self-citationCohen, J. E., Zimmerman, G., Melamed‐Book, N., Friedman, A., Dori, A., & Soreq, H. (2007) · Hippocampus · doi:10.1002/hipo.20381 · Cited by 27
“Both loss (e.g., Wallenstein and Vago, 2001) and gain (e.g., Nijholt et al., 2004) of cholinergic balance impair cognitive performance attesting to the importance of cholinergic homeostasis in hippocampal dependent learning.”
BackgroundSelf-citationA Novel Isoform of Acetylcholinesterase Exacerbates Photoreceptors Death after Photic Stress
Kehat, R., Zemel, E., Cuenca, N., Evron, T., Toiber, D., Loewenstein, A., Soreq, H., & Perlman, I. (2007) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.06-0847 · Cited by 26
“Qualitative ISH analysis indicated that the Monarsen treatment reduced the expression of mRNA AChE-R more efficiently than it did for mRNA AChE-S (data not shown), supporting previous observations of particular vulnerability of nascent mRNA transcripts to the antisense effect.(27,35,36) These results further suggest t…”
MethodResultSelf-citationNkpaa, K. W., Owoeye, O., Amadi, B. A., Adedara, I. A., Abolaji, A. O., Wegwu, M. O., & Farombi, E. O. (2020) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.22681 · Cited by 26
Rinwa, P., & Kumar, A. (2013) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-013-0925-5 · Cited by 26
Nijholt, I. M., Ostroveanu, A., Scheper, W. A., Penke, B., Luiten, P. G. M., van der Zee, E. A., & Eisel, U. L. M. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.03.008 · Cited by 27
Self-citationFarchi, N., Shoham, S., Hochner, B., & Soreq, H. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05249.x · Cited by 26
“1A, modified from Nijholt et al., 2004).”
BackgroundMethodInfluentialSelf-citationModerate stress enhances memory persistence: Are adrenergic mechanisms involved?
Parfitt, G. M., Barbosa, Â. K., Campos, R. C., Koth, A. P., & Barros, D. M. (2012) · Behavioral Neuroscience · doi:10.1037/a0029861 · Cited by 25
Blank, T., Nijholt, I. M., & Spiess, J. (2004) · Molecular Neurobiology · doi:10.1385/mn:29:2:131 · Cited by 25
“Whereas the impact of CRF diminishes within hours (14), the elevated levels of AChE-R can be detected even weeks after the stress experience (48).”
BackgroundInfluentialSelf-citationReadthrough Acetylcholinesterase: A Multifaceted Inducer of Stress Reactions
Zimmerman, G., & Soreq, H. (2006) · Journal of Molecular Neuroscience · doi:10.1385/jmn:30:1:197 · Cited by 25
“…level, an increase of AChE-R mRNA is observed, with a corresponding increase in AChE-R staining at hippocampal CA1 neurons, up to 3 h after confined swim (Kaufer et al., 1998), following 1 h immobilization stress (Nijholt et al., 2004) or 45 min after exposure to AChE-I (Meshorer et al., 2002).”
BackgroundInfluentialSelf-citationBen‐Ari, S., Toiber, D., Sas‐Chen, A., Soreq, H., & Ben‐Shaul, Y. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03725.x · Cited by 25
“Abbreviations used: AChE, acetylcholinesterase; AChE-E, erythrocytic AChE; AChE-R, stress-induced soluble readthrough AChE; AChE-S, synaptic AChE; BS, bluescript; CDF, cumulative distribution functions; CMV, cytomegalovirus; Gad1, glutamic acid decarboxylase 1; LR, log2 transformed Cy3/Cy5 ratio; LTP, long-term potent…”
BackgroundInfluentialSelf-citationRNA-Targeted Suppression of Stress-Induced Allostasis in Primate Spinal Cord Neurons
Evron, T., BenMoyal‐Segal, L., Lamm, N., Gilboa-Geffen, A., & Soreq, H. (2005) · Neurodegenerative Diseases · doi:10.1159/000086427 · Cited by 24
Self-citationStress‐induced Alternative Splicing Modulations in Brain and Periphery
Shaked, I., Zimmerman, G., & Soreq, H. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1410.001 · Cited by 24
“Acknowledgments This work was supported by the European Community’s Grants LSHG-CT2006-037277, LSHM-CT-2006-037378, The German Israel Project (DIP-G 3.2), and the Israel Ministry of Science (3-2589).”
BackgroundInfluentialSelf-citationWhy is stress so deadly? An evolutionary perspective
Hadany, L., Beker, T., Eshel, I., & Feldman, M. W. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2005.3384 · Cited by 24
Sun, L., Liu, T., Liu, J., Gao, C., & Zhang, X. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.929781 · Cited by 27
“Another type of neural plasticity besides neurogenesis is synaptic plasticity, which includes synaptogenesis as well as synaptic functions like long-term potentiation (LTP) and pre-synaptic plasticity.”
BackgroundUcán-Marín, F., Ernst, W., O'Dor, R. K., & Sherry, J. P. (2012) · Aquaculture · doi:10.1016/j.aquaculture.2011.12.036 · Cited by 23
“Excess AChE activity can be a response to stress (Nijholt et al., 2004), however, stress was unlikely to have been an explanatory factor in the present experiment since both control and treated fish were held under identical low stress conditions.”
Wang, M., Ramasamy, V. S., Samidurai, M., & Jo, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-47452-6 · Cited by 22
Ben‐Shaul, Y., BenMoyal‐Segal, L., Ben‐Ari, S., Bergman, H., & Soreq, H. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04812.x · Cited by 23
“a maintained extreme excess of AChE-R also results in undesired consequences (Brenner et al., 2003; Nijholt et al., 2004), possibly explaining why this splice variant is only induced when a need arises.”
BackgroundInfluentialSelf-citationBasolateral amygdala GABA-A receptors mediate stress-induced memory retrieval impairment in rats
Sardari, M., Rezayof, A., Khodagholi, F., & Zarrindast, M. (2013) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713001363 · Cited by 20
“Although the general outcome of stress is memory impairment (Segev et al., 2012), there are some studies that have reported the neutral (Nijholt et al., 2004; Joëls et al., 2006) or even the facilitative role of stress on memory formation (Beylin and Shors, 1998).”
The physiological basis of intracrine stem cell regulation
Ré, R. N., & Cook, J. L. (2008) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00461.2008 · Cited by 20
“In addition, ARP is internalized by neurons through endocytosis and retrograde transport and, thereafter, enhances fear conditioning in an AChE antisense-sensitive manner (34).”
BackgroundCoimbra, B., Soares‐Cunha, C., Borges, S., de Vasconcelos, N. A. P., Sousa, N., & Rodrigues, A. J. (2017) · eLife · doi:10.7554/elife.25843 · Cited by 19
“In fact, it has been shown that stress changes cholinergic enzymes expression (Finkelstein et al., 1985; Kaufer et al., 1998), either by inducing an alternative splicing of AChE gene (Nijholt et al., 2004), or by modulating the epigenetic status of its promoter regions (Sailaja et al., 2012).”
Therapeutic potential of some stress mediators in early Alzheimer's disease
Pardon, M. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.09.006 · Cited by 17
“This may constitute a mechanism whereby positive lifestyle factors delay the progression of cognitive deterioration in AD since AChE-R is also known to facilitate hippocampal LTP and contextual (episodic) fear memory (Nijholt et al., 2004).”
BackgroundAntistress Effects of the Ethanolic Extract fromCymbopogon schoenanthusGrowing Wild in Tunisia
Othman, M. B., Han, J., Omri, A. E., Ksouri, R., Neffati, M., & Isoda, H. (2013) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2013/737401 · Cited by 17
“It was demonstrated that different stress paradigms [2, 3] significantly affected learning and memory function and intensified fear memory in mice.”
BackgroundPeripheral Site Acetylcholinesterase Blockade Induces RACK1-Associated Neuronal Remodeling
Farchi, N., Ofek, K., Podoly, E., Dong, H., Xiang, Y., Diamant, S., Livnah, O., Li, J., Hochner, B., Lu, W.-Y., et al. (2007) · Neurodegenerative Diseases · doi:10.1159/000101842 · Cited by 17
Self-citationSklan, E. H., Berson, A., Birikh, K. R., Gutnick, A., Shahar, O. D., Shoham, S., & Soreq, H. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.080 · Cited by 16
Self-citationWaiskopf, N., & Soreq, H. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800159-2.00052-x · Cited by 15
Self-citationBenito-Murcia, M., Botías, C., Martín‐Hernández, R., Higes, M., Rodríguez, F. S., Pérez‐López, M., Míguez‐Santiyán, M. P., & Martinez-Morcillo, S. (2022) · Environmental Toxicology and Pharmacology · doi:10.1016/j.etap.2022.103920 · Cited by 15
Park, E., Lee, M. S., Baik, S. M., Cho, E. B., Son, G. H., Seong, J. Y., Lee, K. H., & Kim, K. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m807386200 · Cited by 15
Lutz, P., Wiaderna, D., Gralewicz, S., & Kur, B. (2006) · International Journal of Occupational Medicine and Environmental Health · doi:10.2478/v10001-006-0017-6 · Cited by 15
“It has recently been shown that exposure to cholinesterase inhibitors is followed weeks later by an increase in excitability of cholinergically innervated limbic structures and an exaggerated conditioned fear response [11,12].”
BackgroundRegulation of Gene Expression in Plants
Bassett, C. L. (2007) · Springer eBooks · doi:10.1007/978-0-387-35640-2 · Cited by 15
Readthrough acetylcholinesterase in inflammation-associated neuropathies
Dori, A., Ifergane, G., Saar-Levy, T., Bersudsky, M., Mor, I., Soreq, H., & Wirguin, I. (2007) · Life Sciences · doi:10.1016/j.lfs.2007.02.011 · Cited by 14
Self-citationOriel, S., & Kofman, O. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00110 · Cited by 15
Molecular mechanisms underlying activity-dependent AMPA receptor cycling in retinal ganglion cells
Casimiro, T. M., Nawy, S., & Carroll, R. C. (2013) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2013.07.010 · Cited by 13
“Arc has been indirectly linked to the regulation of GluA1 AMPARs as Arc's down-regulation or genetic knockout results in elevated levels of GluA2-lacking receptors at the membrane surface (Chowdhury et al., 2006; Nijholt et al., 2004; Shepherd et al., 2006; Zhao et al., 2004).”
BackgroundLivneh, U., Dori, A., Katzav, A., & Kofman, O. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.02.029 · Cited by 12
Dori, A., Oriel, S., Livneh, U., Duek, O. A., Lin, T., & Kofman, O. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.044 · Cited by 12
Thirty years of intracrinology.
Ré, R. N. (2014) · PubMed Central · Cited by 11
Tillman, G. D., Calley, C. S., Green, T. A., Buhl, V. I., Biggs, M. M., Spence, J. S., Briggs, R. W., Haley, R. W., Kraut, M. A., & Hart, J. (2012) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2012.08.004 · Cited by 10
“(2008) found evidence of the read-through variant of acetylcholinesterase (AChE-R), which had been found to be overexpressed in mice that had been stressed with immobilization (Nijholt et al., 2004), playing a role in the hyperarousal resulting from predator stress in mice.”
Alternative Processing as a Mechanism for Regulating Gene Expression
Louzada, E. S. (2007) · Springer eBooks · doi:10.1007/978-0-387-35640-2_3 · Cited by 9
The roles of RACK1 in the pathogenesis of Alzheimer's disease
He, W., Shi, X., & Dong, Z. (2023) · Journal of Biomedical Research · doi:10.7555/jbr.37.20220259 · Cited by 11
Long-Term Effects of Maternal Deprivation on Cholinergic System in Rat Brain
Marković, B., Radonjić, N. V., Aksić, M., Filipović, B., & Petronijević, N. (2014) · BioMed Research International · doi:10.1155/2014/636574 · Cited by 9
Neuromuscular Therapeutics by RNA‐Targeted Suppression of ACHE Gene Expression
Dori, A., & Soreq, H. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1348.004 · Cited by 9
Self-citationTochigi, M., Otani, T., Yamasue, H., Kasai, K., Kato, T., Iwanami, A., Kato, N., & Sasaki, T. (2005) · Neuroscience Research · doi:10.1016/j.neures.2005.03.012 · Cited by 9
Geyer, B. C., Evron, T., Soreq, H., & Mor, T. S. (2009) · Elsevier eBooks · doi:10.1016/b978-012374484-5.00046-8 · Cited by 7
Self-citation
Metadata
- Authors
- Nijholt, I., Farchi, N., Kye, M., Sklan, E. H., Shoham, S., Verbeure, B., Owen, D., Hochner, B., Spiess, J., Soreq, H., & Blank, T.
- Affiliations
- Max Planck Institute of Experimental Medicine (DE)
- Hebrew University of Jerusalem (IL)
- Herzog Hospital (IL)
- MRC Laboratory of Molecular Biology (GB)
- Corresponding author
- Blank, T
- Venue
- Molecular Psychiatry
- Published
- 2003-10-28
- Volume
- 9
- Issue
- 2
- Pages
- 174-183
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- OpenAlex
- W2165828523
- Cited by
- 126
- References
- 43
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 3 · 2020: 6 · 2019: 3 · 2018: 6 · 2017: 3 · 2016: 2 · 2015: 4 · 2014: 7 · 2013: 10 · 2012: 10
- FWCI
- 4.20
- Type
- journal article
- Language
- en
- Open access
- Locations
- Molecular Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Max-Planck-Gesellschaft
- Medical Research and Materiel Command
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Keywords
- acetylcholinesterase, alternative splicing, stress, fear memory, long-term potentiation, hippocampus, CA1, antisense oligonucleotides, contextual fear, PKCβII, synaptic plasticity, restraint stress, transgenic mice
- MeSH terms
- Acetylcholinesterase, Animals, Fear, Hippocampus, Memory, Neuronal Plasticity, Protein Kinase C, RNA, Messenger, Stress, Physiological, Gene Expression Regulation, Enzymologic, Alternative Splicing, Long-Term Potentiation, Mice, Protein Kinase C beta
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