Skip to main content

Advertisement

Log in

Epigenetics and the Formation of Long-Term Memory

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

The most urgent problem in neurobiology is the search for the mechanisms underlying long-term memory. Gene expression has been shown to be needed for long-term memory to form. Which genes are expressed and how their expression is regulated are subject to intense investigation. The task is complicated by the multicomponent nature of the systems regulating the genome. A number of DNA-binding transcription factors involved in regulating gene expression in learning have now been identified. However, activation of these factors alone is insufficient to induce expression; modification (remodeling) of chromatin is also required. Chromatin remodeling processes are epigenetic. The most important roles in chromatin remodeling are played by the processes of phosphorylation, acetylation, and methylation of histones and methylation of DNA. Impairments to these processes lead to the inability to form long-term memory. This review addresses the role of transcription factors and chromatin modifications in the formation of long-term memory in invertebrates and vertebrates and assesses the potential for improving memory by modifying epigenetic mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. K. V. Anokhin, “Molecular scenarios for the consolidation of longterm memory,” Zh. Vyssh. Nerv. Deyat., 47, No. 2, 261–279 (1997).

    CAS  Google Scholar 

  2. V. L. Bianki and E. B. Filippova, Evolution of Functional Asymmetry of the Brain [in Russian], Nauka, Leningrad (1987), pp. 304–352.

    Google Scholar 

  3. L. N. Grinkevich, P. D. Lisachev, and T. I. Merkulova, “Formation of AP-1 transcription factors during learning in Helix,” Ros. Fiziol. Zh., 87, No. 6, 762–773 (2001).

    CAS  Google Scholar 

  4. L. N. Grinkevich and G. V. Vasil’ev, “Possible molecular-cellular mechanisms for the regulation of gene expression during learning,” Ros. Fiziol. Zh., 85, No. 1, 48–66 (1999).

    CAS  Google Scholar 

  5. L. N. Grinkevich, P. D. Lisachev, K. A. Baranova, and O. A. Kharchenko, “Comparative analysis of the activation of MAPK/ERK kinases in the CNS of animals with different learning abilities,” Ros. Fiziol. Zh., 92, No. 6, 536–545 (2006).

    CAS  Google Scholar 

  6. A. B. Danilova, P. D. Lisachev, and L. N. Grinkevich, “Comparative studies of protein acetylation in the CNS of adult and juvenile Helix during the formation of long-term memory,” Info. Vestn. VOGiS, 14, No. 2, 312–319 (2010).

    Google Scholar 

  7. V. A. Dyatlov, “The role of calcium ions in the processes of modulation of neuron responses to application of acetylcholine by serotonin in the common snail,” Neirofiziologiya, 20, No. 5, 666–671 (1988).

    CAS  Google Scholar 

  8. V. L. Karpov, “What determines the fate of a gene?” Priroda, No. 3, 34–43 (2005).

    Google Scholar 

  9. A. A. Pendina, V. V. Grinkevich, T. V. Kuznetsova, and V. S. Baranov, “DNA methylation – a universal mechanism regulating gene activity,” Ekol. Genet., 2, No. 3, 27–36 (2004).

    Google Scholar 

  10. N. B. Salimova, I. Miloshevich, and R. M. Salimov, “The actions of 5,6-hydroxytryptamine on behavior in the snail labyrinth,” Zh. Vyssh. Nerv. Deyat., 34, No. 5, 941–947 (1984).

    CAS  Google Scholar 

  11. K. G. Shevchenko, A. B. Danilova, and L. N. Grinkevich, “Posttranslational modification of histone H3 on memory consolidation and reconsolidation in the mollusk Helix,” Info. Vestn. VOGiS, 13, No. 4, 723–730 (2009).

    Google Scholar 

  12. T. Abel and R. S. Zukin, “Epigenetic targets of HDAC inhibition in neurodegenerative and psychiatric disorders,” Curr. Opin. Pharmacol., 8, No. 1, 57–64 (2008).

    CAS  PubMed Central  PubMed  Google Scholar 

  13. S. Akbarian and H. S. Huang, “Epigenetic regulation in human brain – focus on histone lysine methylation,” Biol. Psychiatry, 65, No. 3, 198–203 (2009).

    CAS  PubMed Central  PubMed  Google Scholar 

  14. J. M. Alarcon, G. Malleret, K. Touzani, et al., “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, No. 6, 947–959 (2004).

    CAS  PubMed  Google Scholar 

  15. C. M. Alberini, “Transcription factors in long-term memory and synaptic plasticity,” Physiol. Rev., 89, No. 1, 121–145 (2009).

    CAS  PubMed  Google Scholar 

  16. C. M. Alberini, M. Ghirardi, R. Metz, and E. R. Kandel, “C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia,” Cell, 76, 1099–1114 (1994).

    CAS  PubMed  Google Scholar 

  17. C. M. Atkins, J. S. Selcher, J. J. Petraitis, et al., “The MAPK cascade is required for mammalian associative learning,” Nat. Neurosci., 1, No. 7, 602–609 (1998).

    CAS  PubMed  Google Scholar 

  18. P. M. Balaban, “Cellular mechanisms of behavioral plasticity in terrestrial snail,” Neurosci. Biobehav. Rev., 26, 597–630 (2002).

    CAS  PubMed  Google Scholar 

  19. A. Barco and H. Marie, “Genetic approaches to investigate the role of CREB in neuronal plasticity and memory,” Mol. Neurobiol., 44, No. 3, 330–349 (2011).

    CAS  PubMed  Google Scholar 

  20. D. Bartsch, M. Ghirardi, P. Skehal, et al., “Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change,” Cell, 83, No. 2, 979–992 (1995).

    CAS  PubMed  Google Scholar 

  21. S. L. Berger, “The complex language of chromatin regulation during transcription,” Nature, 447, 407–412 (2007).

    CAS  PubMed  Google Scholar 

  22. D. E. Berman, S. Hazvi, K. Rosenblum, et al., “Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat,” J. Neurosci., 18, 10037–10044 (1998).

    CAS  PubMed  Google Scholar 

  23. S. Blum, A. N. Moore, F. R. Adams, and P. K. Dash, “A mitogen-activated protein kinase cascade in CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory,” J. Neurosci., 19, 3535–3544 (1999).

    CAS  PubMed  Google Scholar 

  24. T. W. Bredy, H. Wu, C. Crego, et al., “Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear,” Learn. Mem., 14, No. 4, 268–276 (2007).

    CAS  PubMed  Google Scholar 

  25. T. J. Carew, “Molecular enhancement of memory formation,” Neuron, 16, 5–8 (1996).

    CAS  PubMed  Google Scholar 

  26. D. Chakravarti, V. J. La Monte, M. C. Nelson, et al., “Role of CBP/p300 in nuclear receptor signaling,” Nature, 383, 99–103 (1996).

    CAS  PubMed  Google Scholar 

  27. Y. Chandramohan, S. K. Droste, J. S. Arthur, and J. M. Reul, “The forced swimming-induced behavioral immobility response involves histone H3 phospho-acetylation and c-Fos induction in dentate gyrus granule neurons via activation of the N-methyl-D-aspartate/extracellular signal-regulated kinase/mitogen- and stress-activated kinase signaling pathway,” Eur. J. Neurosci., 27, No. 10, 2701–2713 (2008).

    PubMed  Google Scholar 

  28. P. Cheung, C. D. Allis, and P. Sassone-Corsi, “Signaling to chromatin through histone modifications,” Cell, 103, 263–271 (2000).

    CAS  PubMed  Google Scholar 

  29. P. Cheung, K. G. Tanner,W. L. Cheung, et al., “Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation,” Mol. Cell., 5, No. 6, 905–915 (2000).

    CAS  PubMed  Google Scholar 

  30. J. C. Chrivia, R. P. S. Kwok, N. Lamb, et al., “Phosphorylated CREB binds specifically to the nuclear protein CBP,” Nature, 365, 855–859 (1993).

    CAS  PubMed  Google Scholar 

  31. W. B. Chwang, K. J. O’Riordan, J. M. Levenson, and J. D. Sweatt, “ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning,” Learn. Mem., 13, 322–328 (2006).

    CAS  PubMed  Google Scholar 

  32. W. B. Chwang, J. S. Arthur, A. Schumacher, and J. S. Sweatt, “The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation,” J. Neurosci., 27, No. 46, 12732–12742 (2007).

    CAS  PubMed  Google Scholar 

  33. T. Crow, J.-J. Xue-Bian, V. Siddiqi, and J. T. Neary, “Serotonin activation of ERK pathway in Hermissenda: contribution of calciumdependent protein kinase C,” J. Neurochem., 78, 358–364 (2001).

    CAS  PubMed  Google Scholar 

  34. A. B. Danilova, O. A. Kharchenko, K. G. Shevchenko, and L. N. Grinkevich, “Histone H3 acetylation is asymmetrically induced upon learning in identified neurons of the food aversion network in the mollusk Helix lucorum,” Front. Behav. Neurosci., 4, 180, 1–7 (2010).

    Google Scholar 

  35. P. K. Dash, S. A. Orsi, and A. N. Moore, “Sequestration of serum response factor in the hippocampus impairs long-term spatial memory,” J. Neurochem., 93, 268–278 (2005).

    Google Scholar 

  36. A. J. de Ruijter, A. H. van Gennip, H. N. Caron, et al., “Histone deacetylase (HDACs): characterization of the classical HDAC family,” Biochem. J., 370, 737–749 (2003).

    PubMed  Google Scholar 

  37. G. P. Delcuve, M. Rastegar, and J. R. Davie, “Epigenetic control,” J. Cell. Physiol., 219, No. 2, 243–250 (2009).

    CAS  PubMed  Google Scholar 

  38. S. Duvarci, K. Nader, and J. E. LeDoux, “Activation of extracellular signal-regulated kinase-mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning,” Eur. J. Neurosci., 21, No. 1, 283–289 (2005).

    PubMed  Google Scholar 

  39. H. Einat, P. Yuan, T. D. Gould, et al., “The role of the extracellular signal-regulated kinase signaling pathway in mood modulation,” J. Neurosci., 23, No. 19, 7311–7316 (2003).

    CAS  PubMed  Google Scholar 

  40. G. Faraco, T. Pancani, L. Formentini, et al., “Pharmacological inhibition of histone deacetylase by suberoylanilide hydroxamic acid specifically alters gene expression and reduces ischemic injury in the mouse brain,” Mol. Pharmacol., 70, No. 6, 1876–1884 (2006).

    CAS  PubMed  Google Scholar 

  41. V. Feld, B. Dimant, A. Delorenzi, et al., “Phosphorylation of extranuclear ERK/MAPK is required for long-term memory consolidation in the crab Chasmognathus,” Behav. Brain Res., 158, 251–261 (2005).

    CAS  PubMed  Google Scholar 

  42. R. J. Ferrante, J. K. Kubilus, J. Lee, et al., “Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington’s disease mice,” J. Neurosci., 23, No. 28, 9418–9427 (2003).

    CAS  PubMed  Google Scholar 

  43. R. D. Fields, F. Eshete, B. Stevens, and K. Itoh, “Action potentialdependent regulation of gene expression: temporal specificity in Ca2+, cAMP-responsive element binding proteins, and mitogen-activated protein kinase signaling,” J. Neurosci., 17, No. 19, 7252–7266 (1997).

    CAS  PubMed  Google Scholar 

  44. A. Fischer, F. Sananbenesi, X. Wang, et al., “Recovery of learning and memory is associated with chromatin remodeling,” Nature, 447, No. 7141, 178–182 (2007).

    CAS  PubMed  Google Scholar 

  45. L. Formisano, K. M. Noh, T. Miyawaki, et al., “Ischemic insults promote epigenetic reprogramming of mu opioid receptor expression in hippocampal neurons,” Proc. Natl. Acad. Sci. USA, 104, No. 10, 4170–4175 (2007).

    CAS  PubMed  Google Scholar 

  46. G. Gardian, S. E. Browne, D. K. Choi, et al., “Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington’s disease,” J. Biol. Chem., 280, No. 1, 556–563 (2005).

    CAS  PubMed  Google Scholar 

  47. L. N. Grinkevich, “Formation of C/EBP transcription factors and possible pathways for controlling their activity during learning in Helix,” Neurosci. Behav. Physiol., 32, No. 1, 33–39 (2002).

    CAS  PubMed  Google Scholar 

  48. L. N. Grinkevich, P. D. Lisachev, O. A. Kharchenko, et al., “Expression of MAP/ERK kinase cascade corresponds to the ability to develop food aversion in terrestrial snail at different stages of ontogenesis,” Brain Res., 1187, 12–19 (2008).

    CAS  PubMed  Google Scholar 

  49. Z. Guan, M. Giustetto, S. Lomvardas, et al., “Integration of longterm memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure,” Cell, 111, No. 4, 483–493 (2002).

    CAS  PubMed  Google Scholar 

  50. S. Gupta, S. Y. Kim, S. Artis, et al., “Histone methylation regulates memory formation,” J. Neurosci., 30, No. 10, 3589–3599 (2010).

    CAS  PubMed Central  PubMed  Google Scholar 

  51. T. Herdegen and J. D. Leah, “Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos, and Krox, and CREB/ARF proteins,” Brain Res. Rev., 28, No. 3, 370–490 (1998).

    CAS  PubMed  Google Scholar 

  52. O. Hobert, R. J. Johnston, Jr., and S. Chang, “Left-right asymmetry in the nervous system: the Caenorhabditis elegans model,” Nat. Rev. Neurosci., 3, No. 8, 629–640 (2002).

    CAS  PubMed  Google Scholar 

  53. S. C. Hu, J. Chrivia, and A. Ghosh, “Regulation of CBP-mediated transcription by neuronal calcium signaling,” Neuron, 22, No. 4, 799–808 (1999).

    CAS  PubMed  Google Scholar 

  54. R. Janknecht and T. Hunter, “A growing coactivator network,” Nature, 383, No. 6595, 22–23 (1996).

    CAS  PubMed  Google Scholar 

  55. L. Kaczmarek and A. Chandhuri, “Sensory regulation of immediate early gene expression in mammalian visual cortex: implications for functional mapping and neural plasticity,” Brain Res. Rev., 23, 237–256 (1997).

    CAS  PubMed  Google Scholar 

  56. B. Kaminska, L. Kaczmarek, S. Zangenehpour, and A. Chandhuri, “Rapid phosphorylation of Elk-1 transcription factor and activation of MAP kinase signal transduction pathways in response to visual stimulation,” Mol. Cell. Neurosci., 13, 405–414 (1999).

    CAS  PubMed  Google Scholar 

  57. E. R. Kandel, “The molecular biology of memory storage: a dialogue between genes and synapses,” Science, 294, No. 5544, 1030–1038 (2001).

    CAS  PubMed  Google Scholar 

  58. D. R. Kaplan and F. D. Miller, “Neurotrophin signal transduction in the nervous system,” Curr. Opin. Neurobiol., 10, No. 3, 381–391 (2000).

    CAS  PubMed  Google Scholar 

  59. M. Karin, Z. Liu, and E. Zandi, “AP-1 function and regulation,” Curr. Opin. Cell. Biol., 9, No. 2, 240–246 (1997).

    CAS  PubMed  Google Scholar 

  60. A. Kelly, S. Laroche, and S. Davis, “Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation memory,” J. Neurosci., 23, No. 12, 5354–5360 (2003).

    CAS  PubMed  Google Scholar 

  61. O. A. Kharchenko,V. V. Grinkevich, O. V. Vorobiova, and L. N. Grinkevich, “Learning-induced lateralized activation of the MAPK/ERK cascade in identified neurons of the food-aversion network in the mollusk Helix lucorum,” Neurobiol. Learn. Mem., 94, No. 2, 158–166 (2010).

    PubMed  Google Scholar 

  62. J. M. Kornhauser and M. E. Greenberg, “A kinase to remember: dual roles for MAP kinase in long-term memory,” Neuron, 18, No. 6, 839–842 (1997).

    CAS  PubMed  Google Scholar 

  63. E. Korzus, M. G. Rosenfeld, and M. Mayford, “CBP histone acetyltransferase activity is a critical component of memory consolidation,” Neuron, 42, No. 6, 961–972 (2004).

    CAS  PubMed  Google Scholar 

  64. S. V. Kyosseva, “Mitogen-activated protein kinase signaling,” Int. Rev. Neurobiol., 59, 201–220 (2004).

    CAS  PubMed  Google Scholar 

  65. J. L. Lee, P. De Ciano, B. J. Everitt, and K. L. Thomas, “Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior,” Neuron, 47, No. 6, 795–801 (2005).

    CAS  PubMed  Google Scholar 

  66. E. Lesburgueres, O. L. Gobbo, S. Alaux-Cantin, et al., “Early tagging of cortical networks is required for the formation of enduring associative memory,” Science, 331, No. 6019, 924–928 (2011).

    CAS  PubMed  Google Scholar 

  67. P. Letzkus, N. Boeddeker, J. T. Wood, et al., “Lateralization of visual learning in the honeybee,” Biol. Lett., 4, No. 1, 16–18 (2008).

    PubMed Central  PubMed  Google Scholar 

  68. J. M. Levenson, K. J. O’Riordan, K. D. Brown, et al., “Regulation of histone acetylation during memory formation in the hippocampus,” J. Biol. Chem., 279, 40545–40559 (2004).

    CAS  PubMed  Google Scholar 

  69. J. M. Levenson and J. D. Sweatt, “Epigenetic mechanisms: a common theme in vertebrate and invertebrate memory formation,” Cell. Mol. Life Sci., 63, 1009–1016 (2006).

    CAS  PubMed  Google Scholar 

  70. Q. Lu, A. E. Hutchins, C. M. Doyle, et al., “Acetylation of cAMPresponsive element-binding protein (CREB) by CREB-binding protein enhances CREB-dependent transcription,” J. Biol. Chem., 278, No. 18, 15727–15734 (2003).

    CAS  PubMed  Google Scholar 

  71. F. D. Lubin and J. D. Sweatt, “The IkB kinase regulates chromatin structure during reconsolidation of conditioned fear memories,” Neuron, 55, No. 6, 942–957 (2007).

    CAS  PubMed Central  PubMed  Google Scholar 

  72. F. D. Lubin, “Epigenetic gene regulation in the adult mammalian brain: multiple roles in memory formation,” Neurobiol. Learn. Mem., 96, No. 1, 68–78 (2011).

    CAS  PubMed Central  PubMed  Google Scholar 

  73. H. Martin, M. Flandez, C. Nombela, and M. Molina, “Protein phosphatases in MAPK signalling: we keep learning from yeast,” Mol. Microbiol., 58, No. 1, 6–16 (2005).

    CAS  PubMed  Google Scholar 

  74. K. C. Martin, D. Michael, J. C. Rose, et al., “MAP kinase translocates into the nucleus of the presynaptic cell and is required for longterm facilitation in Aplysia,” Neuron, 18, 899–912 (1997).

    CAS  PubMed  Google Scholar 

  75. K. J. McManus and M. J. Hendzel, “CBP, a transcriptional coactivator and acetyltransferase,” Biochem. Cell. Biol., 79, No. 3, 253–266 (2001).

    CAS  PubMed  Google Scholar 

  76. B. Mellstrom, J. R. Naranjo, N. S. Folkes, et al., “Transcriptional response to cAMP in brain: specific distribution and induction of CREM antagonists,” Neuron, 10, 655–665 (1993).

    CAS  PubMed  Google Scholar 

  77. K. Merienne, S. Pannetier, A. Harel-Bellan, and P. Sassone-Corsi, “Mitogen-regulated RSK2-CBP interaction controls their kinase and acetylase activities,” Mol. Cell. Biol., 21, No. 20, 7089–7096 (2001).

    CAS  PubMed Central  PubMed  Google Scholar 

  78. C. A. Miller, S. L. Campbell and J. D. Sweatt, “DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity,” Neurobiol. Learn. Mem., 89, 599–603 (2008).

    CAS  PubMed Central  PubMed  Google Scholar 

  79. M. S. Monsey, K. T. Ota, I. F. Akingbade, et al., “Epigenetic alterations are critical for fear memory consolidation and synaptic plasticity in the lateral amygdala,” PLoS One, 6, No. 5, 1–13 (2011).

    Google Scholar 

  80. K. Nader and O. Hardt, “A single standard for memory: the case for reconsolidation,” Nature Rev. Neurosci., 10, No. 3, 224–234 (2009).

    CAS  Google Scholar 

  81. P. C. Orban, P. F. Chapman, and R. Brambilla, “Is the Ras-MAPK signalling pathway necessary for long-term memory formation?” Trends Neurosci., 22, No. 1, 38–44 (1999).

    CAS  PubMed  Google Scholar 

  82. L. C. Ou and P. W. Gean, “Transcriptional regulation of brain-derived neurotrophic factor in the amygdala during consolidation of fear memory,” Mol. Pharmacol., 72, No. 2, 350–358 (2007).

    CAS  PubMed  Google Scholar 

  83. A. Pascual, K. L. Huang, J. Neveu, and T. Preat, “Neuroanatomy: brain asymmetry and long-term memory,” Nature, 427, No. 6975, 605–606 (2004).

    CAS  PubMed  Google Scholar 

  84. N. D. Perkins, L. K. Felzien, J. C. Betts, et al., “Regulation of NF-κB by cyclin-dependent kinases associated with the p300 coactivator,” Science, 275, No. 5299, 523–527 (1997).

    CAS  PubMed  Google Scholar 

  85. C. L. Peterson and M. A. Laniel, “Histones and histone modifications,” Curr. Biol., 14, No. 14, 546–551 (2004).

    Google Scholar 

  86. F. Petrij, R. H. Giles, H. G. Dauwerse, et al., “Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP,” Nature, 376, No. 6538, 348–351 (1995).

    CAS  PubMed  Google Scholar 

  87. L. J. Rogers and G. Vallortigara, “From antenna to antenna: Lateral shift of olfactory memory recall by honeybees,” PLoS One, 3, No. 6, e2340 (2008).

    PubMed Central  PubMed  Google Scholar 

  88. F. Sananbenesi, A. Fischer, C. Schrick, et al., “Mitogen-activated protein kinase signaling in the hippocampus and its modulation by corticotropin-releasing factor receptor2: a possible link between stress and fear memory,” J. Neurosci., 23, No. 36, 11436–11443 (2003).

    CAS  PubMed  Google Scholar 

  89. P. Sassone-Corsi, C. A. Mizzen, P. Cheung, et al., “Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3,” Science, 285, No. 5429, 886–891 (1999).

    CAS  PubMed  Google Scholar 

  90. F. A. Schroeder, C. L. Lin, W. E. Crusio, and S. Akbarian, “Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse,” Biol. Psychiatry, 62, No. 1, 55–64 (2007).

    CAS  PubMed  Google Scholar 

  91. V. Sgambato, P. Vanhoutte, C. Pages, et al., “In vivo expression and regulation of Elk-1, a target of the extracellular-regulated kinase signaling pathway, in the adult rat brain,” J. Neurosci., 18, No. 1, 214–226 (1998).

    CAS  PubMed  Google Scholar 

  92. S. Shen and P. Casaccia-Bonnefil, “Post-translational modifications of nucleosomal histones in oligodendrocyte lineage cells in development and disease,” J. Mol. Neurosci., 35, No. 1, 13–22 (2008).

    CAS  PubMed Central  PubMed  Google Scholar 

  93. A. Soloaga, S. Thomson, G. R. Wiggin, et al., “MSK2 and MSK1 mediate the mitogen- and stress-induced phosphorylation of histone H3 and HMG-14,” EMBO J., 22, No. 11, 2788–2797 (2003).

    CAS  PubMed  Google Scholar 

  94. S. Spange, T. Wagner, T. Heinzel, and O. H. Kramer, “Acetylation of non-histone proteins modulates cellular signaling at multiple levels,” Int. J. Biochem. Cell. Biol., 41, 185–198 (2009).

    CAS  PubMed  Google Scholar 

  95. A. Stipanovich, E. Valjent, M. Matamales, et al., “A phosphatase cascade by which rewarding stimuli control nucleosomal response,” Nature, 453, 879–885 (2008).

    CAS  PubMed Central  PubMed  Google Scholar 

  96. B. D. Strahl and C. D. Allis, “The language of covalent histone modifications,” Nature, 403, No. 6765, 41–45 (2000).

    CAS  PubMed  Google Scholar 

  97. H. Suzuki, T. R. Thiele, S. Faumont, et al., “Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis,” Nature, 454, No. 7200, 114–117 (2008).

    CAS  PubMed Central  PubMed  Google Scholar 

  98. M. W. Swank and J. D. Sweatt, “Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning,” J. Neurosci., 21, 3383–3391 (2001).

    CAS  PubMed  Google Scholar 

  99. J. D. Sweatt, “Experience-dependent epigenetic modifications in the central nervous system,” Biol. Psychiatry, 65, 191–197 (2009).

    PubMed Central  PubMed  Google Scholar 

  100. G. M. Thomas and R. L. Huganir, “MAPK cascade signaling and synaptic plasticity,” Nat. Rev. Neurosci., 5, No. 3, 173–183 (2004).

    CAS  PubMed  Google Scholar 

  101. R. Treisman, “Journey to the surface of the cell: fos regulation and the SRE,” EMBO J., 14, 4905–4913 (1995).

    CAS  PubMed  Google Scholar 

  102. N. C. Tronson and J. C. Taylor, “Molecular mechanisms of memory reconsolidation,” Nature Rev. Neurosci., 8, 262–275 (2007).

    CAS  Google Scholar 

  103. N. M. Tsankova, O. Berton, W. Renthal, et al., “Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action,” Nat. Neurosci., 9, No. 4, 519–525 (2006).

    CAS  PubMed  Google Scholar 

  104. M. A. Wood, J. D. Hawk, and T. Abel, “Combinatorial chromatin modifications and memory storage: A code for memory,” Learn. Mem., 13, 241–244 (2006).

    CAS  PubMed Central  PubMed  Google Scholar 

  105. J. Xing, D. D. Ginty, and M. E. Greenberg, “Coupling of the RASMAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase,” Science, 273, No. 5277, 959–963 (1996).

    CAS  PubMed  Google Scholar 

  106. W. Xu, H. Chen, K. Du, et al., “A transcriptional switch mediated by cofactor methylation,” Science, 294, No. 5551, 2507–2511 (2001).

    CAS  PubMed  Google Scholar 

  107. I. S. Zakharov and P. M. Balaban, “Neural mechanisms of agedependent changes in avoidance behaviour of the snail Helix lucorum,” Neuroscience, 23, No. 2, 721–729 (1987).

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. N. Grinkevich.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 98, No. 5, pp. 553–574, May, 2012.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Grinkevich, L.N. Epigenetics and the Formation of Long-Term Memory. Neurosci Behav Physi 44, 200–213 (2014). https://doi.org/10.1007/s11055-014-9897-2

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-014-9897-2

Keywords

Navigation