Neuroscience and Behavioral Physiology

, Volume 44, Issue 9, pp 1008–1013

Gender-Dependent Actions of the Histone Deacetylase Blocker Sodium Valproate on Olfactory Learning in 129Sv Mice during the Early Postnatal Period

  • O. V. Burenkova
  • E. A. Aleksandrova
  • I. Yu. Zaraiskaya
Article
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The processes of histone acetylation in the brain underlie both the mechanisms supporting the long-term stable effects of early experience, transmitted to offspring generations by epigenetic inheritance, and learning. However, the role of acetylation in learning has previously been studied only in adult animals: high levels of learning can be linked with high levels of histone H3 acetylation in the brain. The role of acetylation processes in the mechanisms of early learning has not been addressed. We report here our studies of the effects of blockade of histone deacetylation with sodium valproate, which increases the level of acetylation of histone H3, on the outcome of training to olfactory discrimination in 8-day-old mice of strain 129Sv, which have low levels of learning with simulation of maternal grooming. Four doses of sodium valproate, given from day 3 to day 6 of postnatal development, were found to have gender-dependent actions: there were selective improvements in learning in males but not females, though females showed this seen after repeated administration of physiological saline. The possible epigenetic mechanisms underlying these gender-related differences are discussed.

Keywords

olfactory learning ontogeny histone H3 acetylation blockade of histone deacetylases sodium valproate gender-related differences epigenetics 

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References

  1. 1.
    E. A. Aleksandrova, I. Yu. Zaraiskaya, and K. V. Anokhin, “Comparative analysis of the formation of behavior in mice of two inbred strains,” in: Behavior and Behavioral Ecology of Mammals, KMK, Moscow (2005), pp. 349–351.Google Scholar
  2. 2.
    O. V. Burenkova, E. A. Aleksandrova, and I. Yu. Zaraiskaya, “Deprivation of 129Sv mouse offspring of their mothers in early ontogeny improves olfactory learning with simulation of maternal grooming,” Byull. Eksperim. Biol. Med., 153, No. 5, 724–726 (2012).Google Scholar
  3. 3.
    A. V. Lobanov, O. N. Khokhlova, L. A. Zakharova, et al., “A model for analysis of neurotoxic actions on embryonic development in terms of assessment of somatosensory maturation in mice,” Toksikol. Vestn., No. 2, 22–25 (2008).Google Scholar
  4. 4.
    T. W. Bredy, R. A. Humpartzoomian, D. P. Campaign, and M. J. Meaney, “Partial reversal of the effect of maternal care on cognitive function through environmental enrichment,” Neuroscience, 118, 571–576 (2003).CrossRefPubMedGoogle Scholar
  5. 5.
    T. W. Bredy and M. Barad, “The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear,” Learn. Mem., 15, No. 1, 39–45 (2008).CrossRefPubMedCentralPubMedGoogle Scholar
  6. 6.
    I. Brouette-Lahlou, E. Vernet-Maury, and M. Vigouroux, “Role of pups’ ultrasonic calls in a particular maternal behavior in Wistar rat: pups’ anogenital licking,” Behav. Brain Res., 50, No. 1–2, 147–154 (1992).CrossRefPubMedGoogle Scholar
  7. 7.
    F. A. Champagne, J. P. Curley, E. B. Keverne, and P. P. Bateson, “Natural variations in postpartum maternal care in inbred and outbred mice,” Physiol. Behav., 91, No. 2–3, 325–334 (2007).CrossRefPubMedGoogle Scholar
  8. 8.
    W. Fischle, Y. Wang, and C. D. Allis, “Histone and chromatin cross-talk,” Curr. Opin. Cell Biol., 15, No. 2, 172–183 (2003).CrossRefPubMedGoogle Scholar
  9. 9.
    R. A. Hodgson, D. H. Guthrie, and G. B. Varty, “Duration of ultrasonic vocalization in the isolated rat pup as a behavioral measure: sensitivity to anxiolytic and antidepressant drugs,” Pharmacol. Biochem. Behav., 88, No. 3, 341–348 (2008).CrossRefPubMedGoogle Scholar
  10. 10.
    C. U. Johannessen and S. I. Johannessen, “Valproate: past, present, and future,” CNS Drug Rev., 9, No. 2, 199–216 (2003).CrossRefPubMedGoogle Scholar
  11. 11.
    J. M. Levenson, K. J. O’Riordan, K. D. Brown, et al., “Regulation of histone deacetylation during memory formation in the hippocampus,” J. Biol. Chem., 2790, No. 39, 40,545–40,559 (2004).CrossRefGoogle Scholar
  12. 12.
    K. I. Matsuda, H. Mori, and M. Kawata, “Epigenetic mechanisms are involved in sexual differentiation of the brain,” Rev. Endocr. Metab. Disord., 13, No. 3, 163–171 (2012).CrossRefPubMedGoogle Scholar
  13. 13.
    M. J. Meaney, “Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations,” Annu. Rev. Neurosci., 24, 1161–1192 (2001).CrossRefPubMedGoogle Scholar
  14. 14.
    E. K. Murray, A. Hien, G. J. de Vries, and N. G. Forger, “Epigenetic control of sexual differentiation of the bed nucleus of the stria terminalis,” Endocrinology, 150, No. 9, 4241–4247 (2009).CrossRefPubMedCentralPubMedGoogle Scholar
  15. 15.
    B. D. Strahl and C. D. Allis, “The language of covalent histone modifications,” Nature, 403, No. 6765, 41–45 (2000).CrossRefPubMedGoogle Scholar
  16. 16.
    R. M. Sullivan, J. L. McGaugh, and M. Lon, “Norepinephrine-induced plasticity and one-trial olfactory learning in neonatal rats,” Brain Res. Dev. Brain Res., 60, No. 2, 219–228 (1991).CrossRefPubMedGoogle Scholar
  17. 17.
    H. W. Tsai, P. A. Grant, and E. F. Rissman, “Sex differences in histone modifications in the neonatal mouse brain,” Epigenetics, 4, No. 1, 47–53 (2009).CrossRefPubMedCentralPubMedGoogle Scholar
  18. 18.
    C. G. Vecsey, J. D. Hawk, K. M. Lattal, et al., “Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB: CBP-dependent transcriptional activation,” J. Neurosci., 27, 6128–6140 (2007).CrossRefPubMedCentralPubMedGoogle Scholar
  19. 19.
    C. D. Walker, K. Kudreikis, A. Sherrerd, and C. C. Johnston, “Repeated neonatal pain influences maternal behavior, but not stress responsiveness in rat offspring,” Brain Res. Dev. Brain Res., 140, No. 2, 253–261 (2003).CrossRefPubMedGoogle Scholar
  20. 20.
    I. C. Weaver, N. Cervoni, F. A. Champagne, et al., “Epigenetic programming by maternal behavior,” Nat. Neurosci., 7, No. 8, 847–854 (2004).CrossRefPubMedGoogle Scholar
  21. 21.
    I. C. Weaver, F. A. Champagne, S. E. Brown, et al., “Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life,” J. Neurosci., 25, No. 47, 11,045–11,054 (2005).CrossRefGoogle Scholar
  22. 22.
    S. H. Yeh, C. H. Lin, and P. W. Gean, “Acetylation of nuclear factor-kB in rat amygdala improves long-term but not short-term retention of fear memory,“ Mol. Pharmacol., 65, 1286–1292 (2004).CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • O. V. Burenkova
    • 1
  • E. A. Aleksandrova
    • 1
  • I. Yu. Zaraiskaya
    • 1
  1. 1.Research Institute of Normal PhysiologyRussian Academy of Medical SciencesMoscowRussia

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