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.
“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
Stress induces alternative splicing of the AChE mRNA in the hippocampus leading to altered ACh signaling in this structure.
“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
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“bound properties of AChE (Meshorer and Soreq, 2006; Nijholt et al., 2004) as well as the”
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Cocaine‐ or stress‐induced metaplasticity of LTP in the dorsal and ventral hippocampus
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“…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 · see citing works
“…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 · see citing works
Self-citationNon‐hydrolytic functions of acetylcholinesterase
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“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 · see citing works
Mechanisms of Disease: intracrine physiology in the cardiovascular system
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“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 31 · see citing works
“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 · see citing works
“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 · see citing works
Evron, T., Greenberg, D., Mor, T. S., & Soreq, H. (2006) · Toxicology · doi:10.1016/j.tox.2006.08.018 · Cited by 29 · see citing works
Self-citationKye, M. J., Spiess, J., & Blank, T. (2007) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-006-9320-6 · Cited by 27 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
“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…”
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Rinwa, P., & Kumar, A. (2013) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-013-0925-5 · Cited by 26 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
Blank, T., Nijholt, I. M., & Spiess, J. (2004) · Molecular Neurobiology · doi:10.1385/mn:29:2:131 · Cited by 25 · see citing works
“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 · see citing works
“…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 · see citing works
“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 · see citing works
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 · see citing works
“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
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Sun, L., Liu, T., Liu, J., Gao, C., & Zhang, X. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.929781 · Cited by 26 · see citing works
“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.”
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“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 · see citing works
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“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 · see citing works
“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
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“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 · see citing works
“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
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“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 · see citing works
“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 · see citing works
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“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
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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 · see citing works
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Molecular mechanisms underlying activity-dependent AMPA receptor cycling in retinal ganglion cells
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“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).”
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Thirty years of intracrinology.
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“(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
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The roles of RACK1 in the pathogenesis of Alzheimer's disease
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Long-Term Effects of Maternal Deprivation on Cholinergic System in Rat Brain
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Neuromuscular Therapeutics by RNA‐Targeted Suppression of ACHE Gene Expression
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Self-citation
- 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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