The participation of DNA methylation processes in the mechanisms of anterograde and retrograde amnesia caused by impaired reconsolidation of conditioned food aversion memory by NMDA glutamate receptor antagonists or serotonin receptor antagonists, respectively, were studied on grape snails. Anterograde amnesia was characterized by impaired formation of long-term memory during repeated learning. Administration of a DNA methyltransferase (DNMT) inhibitor to amnestic animals resulted in accelerated formation of long-term memory during 1 day of repetitive training vs 3 days during initial training. In serotonin-dependent retrograde amnesia, repeated learning without DNMT inhibitor administration or after inhibitor injections led to the formation of long-term memory. The dynamics of memory formation was similar in both cases and did not differ from that during the initial training: the memory was formed within 3 days of training. Thus, epigenetic processes of DNA methylation are selectively involved in the mechanisms of anterograde amnesia, but do not participate in the mechanisms of retrograde amnesia.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Kopelman MD. Disorders of memory. Brain. 2002; 125(10):2152-2190. doi: https://doi.org/10.1093/brain/awf229
Nikitin VP, Solntseva SV, Kozyrev SA, Nikitin PV, Shevelkin AV. NMDA or 5-HT receptor antagonists impair memory reconsolidation and induce various types of amnesia. Behav. Brain Res. 2018;345:72-82. doi: https://doi.org/10.1016/j.bbr.2018.02.036
Nikitin VP, Solntseva SV, Nikitin PV, Kozyrev SA. The role of DNA methylation in the mechanisms of memory reconsolidation and development of amnesia. Behav. Brain Res. 2015;279:148-154. doi: https://doi.org/10.1016/j.bbr.2014.11.025
Bayraktar G, Kreutz MR. Neuronal DNA methyltransferases: epigenetic mediators between synaptic activity and gene expression? Neuroscientist. 2018;24(2):171-185. doi: https://doi.org/10.1177/1073858417707457
Denis H, Ndlovu MN, Fuks F. Regulation of mammalian DNA methyltransferases: a route to new mechanisms. EMBO Rep. 2011;12(7):647-656. doi: https://doi.org/10.1038/embor.2011.110
Jarome TJ, Lubin FD. Epigenetic mechanisms of memory formation and reconsolidation. Neurobiol. Learn. Mem. 2014;115:116-127. doi: https://doi.org/10.1016/j.nlm.2014.08.002
Lukowiak K, Heckler B, Bennett TE, Schriner EK, Wyrick K, Jewett C, Todd RP, Sorg BA. Enhanced memory persistence is blocked by a DNA methyltransferase inhibitor in the snail Lymnaea stagnalis. J. Exp. Biol. 2014;217(16):2920-2929. doi: https://doi.org/10.1242/jeb.106765
Morris MJ, Monteggia LM. Role of DNA methylation and the DNA methyltransferases in learning and memory. Dialogues Clin. Neurosci. 2014;16(3):359-371. doi: https://doi.org/10.31887/DCNS.2014.16.3/mmorris
Oliveira AM. DNA methylation: a permissive mark in memory formation and maintenance. Learn. Mem. 2016;23(10):587-593. doi: https://doi.org/10.1101/lm.042739.116
Pearce K, Cai D, Roberts AC, Glanzman DL. Role of protein synthesis and DNA methylation in the consolidation and maintenance of long-term memory in Aplysia. Elife. 2017;6:e18299. doi: https://doi.org/10.7554/eLife.18299
Rajasethupathy P, Antonov I, Sheridan R, Frey S, Sander C, Tuschl T, Kandel ER. A role for neuronal piRNAs in the epigenetic control of memory-related synaptic plasticity. Cell. 2012;149(3):693-707. doi: https://doi.org/10.1016/j.cell.2012.02.057
Haubrich J, Bernabo M, Baker AG, Nader K. Impairments to consolidation, reconsolidation, and long-term memory maintenance lead to memory erasure. Annu. Rev. Neurosci. 2020;43:297-314. doi: https://doi.org/10.1146/annurev-neuro-091319-024636
Nader K. New approaches to amnesia. Learn. Mem. 2009;16(11):672-675. doi: https://doi.org/10.1101/lm.1598209
Ryan TJ, Frankland PW. Forgetting as a form of adaptive engram cell plasticity. Nat. Rev. Neurosci. 2022;23(3):173-186. doi: https://doi.org/10.1038/s41583-021-00548-3
Solntseva SV, Nikitin PV, Kozyrev SA, Nikitin VP. Learning against the background of DNA methyltransferase inhibition leads to the formation of memory that is resistant to reactivation and impairment. Bull. Exp. Biol. Med. 2021;170(3):288-293. doi: https://doi.org/10.1007/s10517-021-05053-2
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated from Byulleten’ Eksperimental’noi Biologii i Meditsiny, Vol. 175, No. 4, pp. 419-425, April, 2023
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Kozyrev, S.A., Solntseva, S.V., Storozheva, Z.I. et al. Epigenetic Processes of DNA Methylation Are Selectively Involved in the Mechanisms of Retrograde and Anteograde Amnesia. Bull Exp Biol Med 175, 427–432 (2023). https://doi.org/10.1007/s10517-023-05879-y
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10517-023-05879-y