Abstract
The role of histone acetylation in memory reinstatement after its disruption by antimnemonic drugs has been shown recently. It is known that a normally functioning serotonergic system is required for successful reconsolidation of context memory in terrestrial snails Helix lucorum. In the present study, using the nonselective antagonist of serotonergic receptors methiothepin and the histone deacetylase (HDAC) inhibitor sodium butyrate, we studied the role of histone acetylation in the maintenance and restoration of context memory after its impairment with methiothepin. The results obtained clearly demonstrate that memory impaired by methiothepin during reconsolidation is not restored later under conditions of an increased level of histone acetylation due to administration of sodium butyrate, both with weak memory reactivation (reminder of context) and with strong memory reactivation (electric shock). However, simultaneous administration of HDAC inhibitor sodium butyrate and a blocker of serotonin receptors methiothepin under conditions of memory reactivation prevented the impairment of context memory. The data obtained demonstrated that histone acetylation is a regulatory component for memory maintenance and reconsolidation.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- 5-HT:
-
Serotonin
- HDAC:
-
Histone deacetylase
- MET:
-
Methiothepin
- NaB:
-
Sodium butyrate
- PKMζ:
-
Protein-kinase Mζ
- ZIP:
-
Zeta Inhibitory Peptide
References
Alberini, C.M., Kandel, E.R.: The regulation of transcription in memory consolidation. Cold Spring Harb. Perspect. Biol. 7, a021741 (2014). https://doi.org/10.1101/cshperspect.a021741
Balaban, P.M., Vehovszky, A., Maximova, O.A., Zakharov, I.S.: Effect of 5,7-dihydroxytryptamine on the food-aversive conditioning in the snail Helix Lucorum L. Brain Res. 404, 201–210 (1987). https://doi.org/10.1016/0006-8993(87)91371-0
Balaban, P., Bravarenko, N.: Long-term sensitization and environmental conditioning in terrestrial snails. Exp. Brain Res. 96, 487–493 (1993). https://doi.org/10.1007/BF00234116
Balaban, P.M.: Cellular mechanisms of behavioral plasticity in terrestrial snail. Neurosci. Biobehav. Rev. 26, 597–630 (2002). https://doi.org/10.1016/s0149-7634(02)00022-2
Kandel, E.R., Schwartz, J.H.: Molecular biology of an elementary form of learning: modulation of transmitter release by cuclic AMP. Science 218, 433–443 (1982). https://doi.org/10.1126/science.6289442
Balaban, P.M., Vinarskaya, A.K., Zuzina, A.B., Ierusalimsky, V.N., Malyshev, A.Y.: Impairment of the serotonergic neurons underlying reinforcement elicits extinction of the repeatedly reactivated context memory. Sci. Rep. 6, 36933 (2016). https://doi.org/10.1038/srep36933
Deryabina, I.B., Muranova, L.N., Andrianov, V.V., Gainutdinov, K.L.: Impairing of serotonin synthesis by P-chlorphenylanine prevents the forgetting of contextual memory after reminder and the protein synthesis inhibition. Front. Pharmacol. 9, 607 (2018). https://doi.org/10.3389/fphar.2018.00607
Alarcón, J.M., Malleret, G., Touzani, K., Vronskaya, S., Ishii, S., Kandel, E.R., Barco, A.: Chromatin acetylation, memory, and LTP are impaired in CBP+/− mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42, 947–959 (2004). https://doi.org/10.1016/j.neuron.2004.05.021
Bredy, T.W., Wu, H., Crego, C., Zellhoefer, J., Sun, Y.E., Barad, M.: Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learn. Mem. 14, 268–276 (2007). https://doi.org/10.1101/lm.500907
Bredy, T.W., Barad, M.: The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. Learn. Mem. 15, 39–45 (2008). https://doi.org/10.1101/lm.801108
Hemstedt, T.J., Lattal, K.M., Wood, M.A.: Reconsolidation and extinction: Using epigenetic signatures to challenge conventional wisdom. Neurobiol. Learn. Mem. 142, 55–65 (2017). https://doi.org/10.1016/j.nlm.2017.01.007
Itzhak, Y., Anderson, K.L., Kelley, J.B., Petkov, M.: Histone acetylation rescues contextual fear conditioning in nNOS KO mice and accelerates extinction of cued fear conditioning in wild type mice. Neurobiol. Learn. Mem. 97, 409–417 (2012). https://doi.org/10.1016/j.nlm.2012.03.005
Korzus, E., Rosenfeld, M.G., Mayford, M.: CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42, 961–972 (2004). https://doi.org/10.1016/j.neuron.2004.06.002
Lattal, K.M., Barrett, R.M., Wood, M.A.: Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction. Behav. Neurosci. 121, 1125–1131 (2007). https://doi.org/10.1037/0735-7044.121.5.1125
Levenson, J.M., O’Riordan, K.J., Brown, K.D., Trinh, M.A., Molfese, D.L., Sweatt, J.D.: Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 279, 40545–40559 (2004). https://doi.org/10.1074/jbc.M402229200
Si, J., Yang, J., Xue, L., Yang, C., Luo, Y., Shi, H., Lu, L.: Activation of NF-κB in basolateral amygdala is required for memory reconsolidation in auditory fear conditioning. PLoS ONE 7, e43973 (2012). https://doi.org/10.1371/journal.pone.0043973
Vecsey, C.G., Hawk, J.D., Lattal, K.M., Stein, J.M., Fabian, S.A., Attner, M.A., Cabrera, S.M., McDonough, C.B., Brindle, P.K., Abel, T., Wood, M.A.: Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J. Neurosci. 27, 6128–6140 (2007). https://doi.org/10.1523/JNEUROSCI.0296-07.2007
Villain, H., Florian, C., Roullet, P.: HDAC inhibition promotes both initial consolidation and reconsolidation of spatial memory in mice. Sci. Rep. 6, 27015 (2016). https://doi.org/10.1038/srep27015
Barichello, T., Generoso, J.S., Simões, L.R., Faller, C.J., Ceretta, R.A., Petronilho, F., Lopes-Borges, J., Valvassori, S.S., Quevedo, J.: Sodium butyrate prevents memory impairment by re-establishing BDNF and GDNF expression in experimental pneumococcal meningitis. Mol. Neurobiol. 52, 734–740 (2015). https://doi.org/10.1007/s12035-014-8914-3
Hu, Y.T., Tang, C.K., Wu, C.P., Wu, P.C., Yang, E.C., Tai, C.C., Wu, Y.L.: Histone deacetylase inhibitor treatment restores memory-related gene expression and learning ability in neonicotinoid-treated Apis Mellifera. Insect Mol. Boil. 27, 512–521 (2018). https://doi.org/10.1111/imb.12390
Chen, S., Cai, D., Pearce, K., Sun, P.Y., Roberts, A.C., Glanzman, D.L.: Reinstatement of long-term memory following erasure of its behavioral and synaptic expression in Aplysia. ELife. 3, e03896 (2014). https://doi.org/10.7554/eLife.03896
Ko, H.G., Kim, J.I., Sim, S.E., Kim, T., Yoo, J., Choi, S.L., Baek, S.H., Yu, W.J., Yoon, J.B., Sacktor, T.C., Kaang, B.K.: The role of nuclear PKMζ in memory maintenance. Neurobiol. Learn. Mem. 135, 50–56 (2016). https://doi.org/10.1016/j.nlm.2016.06.010
Zuzina, A.B., Vinarskaya, A.K., Balaban, P.M.: Histone deacetylase inhibitors rescue the impaired memory in terrestrial snails. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 206, 639–649 (2020). doi: https://doi.org/10.1007/s00359-020-01422-w
Zuzina, A.B., Vinarskaya, A.K., Balaban, P.M.: Increase in serotonin precursor levels reinstates the context memory during reconsolidation. Invert. Neurosci. 19, 8 (2019). https://doi.org/10.1007/s10158-019-0227-9
Asaoka, N., Nagayasu, K., Nishitani, N., Yamashiro, M., Shirakawa, H., Nakagawa, T., Kaneko, S.: Inhibition of histone deacetylases enhances the function of serotoninergic neurons in organotypic raphe slice cultures. Neurosci. Lett. 593, 72–77 (2015). https://doi.org/10.1016/j.neulet.2015.03.028
Holloway, T., González-Maeso, J.: Epigenetic mechanisms of serotonin signaling. ACS Chem. Neurosci. 6, 1099–1109 (2015). https://doi.org/10.1021/acschemneuro.5b00033
Guan, Z., Giustetto, M., Lomvardas, S., Kim, J.H., Miniaci, M.C., Schwartz, J.H., Thanos, D., Kandel, E.R.: Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111, 483–493 (2002). https://doi.org/10.1016/s0092-8674(02)01074-7
Walther, D.J., Peter, J.U., Winter, S., Holtje, M., Paulmann, N., Grohmann, M., Vowinckel, J., Alamo-Bethencourt, V., Wilhelm, C.S., Ahnert-Hilger, G., Bader, M.: Serotonylation of small GTPases is a signal transduction pathway that triggers platelet α-granule release. Cell 115, 851–862 (2003). https://doi.org/10.1016/s0092-8674(03)01014-6
Dai, Y., Dudek, N.L., Patel, T.B., Muma, N.A.: Transglutaminase-catalyzed transamidation: a novel mechanism for Rac1 activation by 5-hydroxytryptamine 2A receptor stimulation. J. Pharmacol. Exp. Ther. 326, 153–162 (2008). https://doi.org/10.1124/jpet.107.135046
Dai, Y., Dudek, N.L., Li, Q., Muma, N.A.: Phospholipase C, Ca2+, and calmodulin signaling are required for 5-HT2A receptor-mediated transamidation of Rac1by transglutaminase. Psychopharmacology 213, 403–412 (2011). https://doi.org/10.1007/s00213-010-1984-7
Farrelly, L.A., Thompson, R.E., Zhao, S., Lepack, A.E., Lyu, Y., Bhanu, N.V., Zhang, B., Loh, Y.-H.E., Ramakrishnan, A., Vadodaria, K.C., Heard, K.J., Erikson, G., Nakadai, T., Bastle, R.M., Lukasak, B.J., Zebroski, H., 3rd., Alenina, N., Bader, M., Berton, O., Roeder, R.G., Molina, H., Gage, F.H., Shen, L., Garcia, B.A., Li, H., Muir, T.W., Maze, I.: Histone serotonylation is a permissive modification that enhances TFIID binding to H3K4me. Nature 567, 535–539 (2019). https://doi.org/10.1038/s41586-019-1024-7
Balaban, P.M., Roshchin, M., Timoshenko, A., Zuzina, A.B., Lemak, M., Ierusalimsky, V.N., Aseyev, N.A., Malyshev, A.Y.: Homolog of protein kinase Mzeta maintains context aversive memory and underlying long-term facilitation in terrestrial snail Helix. Front. Cell. Neurosci. 9, 222 (2015). https://doi.org/10.3389/fncel.2015.00222
Abramova, M.S., Nistratova, V.L., Moskvitin, A.A., Pivovarov, A.S.: Methiothepin-sensitive serotonin receptors are involved in the postsynaptic mechanism of sensitization of the defensive response in the common snail. Neurosci. Behav. Physiol. 36, 589–596 (2006). https://doi.org/10.1007/s11055-006-0062-4
Solntseva, S.V., Nikitin, V.P.: Neurochemical mechanisms of food aversion conditioning consolidation in snail Helix lucorum. Ross. Fiziol. Zh. Im. I. M. Sechenova. 94, 1259–1269 (2008)
Kwapis, J.L., Jarome, T.J., Lonergan, M.E., Helmstetter, F.J.: Protein kinase Mzeta maintains fear memory in the amygdala but not in the hippocampus. Behav. Neurosci. 123, 844–850 (2009). https://doi.org/10.1037/a0016343
Kwapis, J.L., Jarome, T.J., Gilmartin, M.R., Helmstetter, F.J.: Intra-amygdala infusion of the protein kinase Mzeta inhibitor ZIP disrupts foreground context fear memory. Neurobiol. Learn. Mem. 98, 148–153 (2012). https://doi.org/10.1016/j.nlm.2012.05.003
Migues, P.V., Hardt, O., Wu, D.C., Gamache, K., Sacktor, T.C., Wang, Y.T., Nader, K.: PKMzeta maintains memories by regulating GluR2-dependent AMPA receptor trafficking. Nat. Neurosci. 13, 630–634 (2010). https://doi.org/10.1038/nn.2531
Pastalkova, E., Serrano, P., Pinkhasova, D., Wallace, E., Fenton, A.A., Sacktor, T.C.: Storage of spatial information by the maintenance mechanism of LTP. Science 313, 1141–1144 (2006). https://doi.org/10.1126/science.1128657
Serrano, P., Friedman, E.L., Kenney, J., Taubenfeld, S.M., Zimmerman, J.M., Hanna, J., Alberini, C., Kelley, A.E., Maren, S., Rudy, J.W., Yin, J.C., Sacktor, T.C., Fenton, A.A.: PKMzeta maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biol. 6, 2698–2706 (2008). https://doi.org/10.1371/journal.pbio.0060318
Shema, R., Sacktor, T.C., Dudai, Y.: Rapid erasure of long-term memory associations in the cortex by an inhibitor of PKM. Science 317, 951–953 (2007). https://doi.org/10.1126/science.1144334
Yao, Y., Kelly, M.T., Sajikumar, S., Serrano, P., Tian, D., Bergold, P.J., Frey, J.U., Sacktor, T.C.: PKM zeta maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J. Neurosci. 28, 7820–7827 (2008). https://doi.org/10.1523/JNEUROSCI.0223-08.2008
Yeh, S.H., Lin, C.H., Gean, P.W.: Acetylation of nuclear factor-kappaB in rat amygdala improves long-term but not short-term retention of fear memory. Mol. Pharmacol. 65, 1286–1292 (2004). https://doi.org/10.1124/mol.65.5.1286
Bousiges, O., Vasconcelos, A.P., Neidl, R., Cosquer, B., Herbeaux, K., Panteleeva, I., Loeffler, J.P., Cassel, J.C., Boutillier, A.L.: Spatial memory consolidation is associated with induction of several lysine-acetyltransferase (histone acetyltransferase) expression levels and H2B/H4 acetylation-dependent transcriptional events in the rat hippocampus. Neuropsychopharmacology 35, 2521–2537 (2010). https://doi.org/10.1038/npp.2010.117
Mahan, A.L., Mou, L., Shah, N., Hu, J.-H., Worley, P.F., Ressler, K.J.: Epigenetic modulation of Homer1a transcription regulation in amygdala and hippocampus with Pavlovian fear conditioning. J. Neurosci. 32, 4651–4659 (2012). https://doi.org/10.1523/JNEUROSCI.3308-11.2012
Peleg, S., Sananbenesi, F., Zovoilis, A., Burkhardt, S., Bahari-Javan, S., Agis-Balboa, R.C., Cota, P., Wittnam, J.L., Gogol-Doering, A., Opitz, L., Salinas-Riester, G., Dettenhofer, M., Kang, H., Farinelli, L., Chen, W., Fischer, A.: Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328, 753–756 (2010). https://doi.org/10.1126/science.1186088
Hebbes, T.R., Thorne, A.W., Crane-Robinson, C.: A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J. 7, 1395–1402 (1988)
Brownell, J.E., Allis, C.D.: Special HATs for special occasions: Linking histone acetylation to chromatin assembly and gene activation. Curr. Opin. Genet. Dev. 6, 176–184 (1996). https://doi.org/10.1016/s0959-437x(96)80048-7
Gräff, J., Joseph, N.F., Horn, M.E., Samiei, A., Meng, J., Seo, J., Rei, D., Bero, A.W., Phan, T.X., Wagner, F., Holson, E., Xu, J., Sun, J., Neve, R.L., Mach, R.H., Haggarty, S.J., Tsai, L.H.: Epigenetic priming of memory updating during reconsolidation to attenuate remote fear memories. Cell 156, 261–276 (2014). https://doi.org/10.1016/j.cell.2013.12.020
Levenson, J.M., Sweatt, J.D.: Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 6, 108–118 (2005). https://doi.org/10.1038/nrn1604
Pearce, K., Cai, D., Roberts, A.C., Glanzman, D.L.: Role of protein synthesis and DNA methylation in the consolidation and maintenance of long-term memory in Aplysia. Elife. 6, e18299 (2017). https://doi.org/10.7554/eLife.18299
Aknowledgments
This study was supported by grant of Russian Science Foundation 19–75-10067 (behavioral experiments), grant of Russian Science Foundation 20–75-00090 (experiments with methiothepin).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Ethics declarations
The authors declare that they have no conflict of interest.
Author Contributions. The authors contributed equally. All authors read and approved the final manuscript.
Ethical Approval: All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving snails were in accordance with the ethical standards and approved (#011 from 10.10.2019) by Ethical Committee of the Institute of Higher Nervous Activity and Neurophysiology of Russian Academy of Sciences.
Rights and permissions
Copyright information
© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this paper
Cite this paper
Zuzina, A.B., Vinarskaya, A.K., Balaban, P.M., Roshchin, M.V. (2021). Histone Deacetylase Inhibitor Prevents Memory Impairment by Methiothepin. In: Velichkovsky, B.M., Balaban, P.M., Ushakov, V.L. (eds) Advances in Cognitive Research, Artificial Intelligence and Neuroinformatics. Intercognsci 2020. Advances in Intelligent Systems and Computing, vol 1358. Springer, Cham. https://doi.org/10.1007/978-3-030-71637-0_71
Download citation
DOI: https://doi.org/10.1007/978-3-030-71637-0_71
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-71636-3
Online ISBN: 978-3-030-71637-0
eBook Packages: Intelligent Technologies and RoboticsIntelligent Technologies and Robotics (R0)