Abstract—We studied the capability to learn in a passive avoidance task and the rate of its extinction in male rats whose fathers were subjected to stress during the period of spermatogenesis using the “stress–restress” paradigm (a model of post-traumatic stress disorder). In the brain of trained and untrained rats, we studied the expression of genes encoding insulin-like growth factor II and H19, the expression of which is imprinted at the early stages of ontogeny. Experimental males exhibited impaired memory consolidation and accelerated extinction of a passive avoidance response. The expression of Igf2 was decreased in the hippocampus and neocortex of untrained male offspring of stressed fathers. The increased expression of the Igf2 and H19 genes was revealed in the hippocampus of male offspring of control fathers 20 h after training, whereas in the experimental rats, the expression of these genes did not alter. Our data show that the impairment of memory in male offspring of stressed fathers may be mediated by decreased expression of the Igf2 gene.
Similar content being viewed by others
REFERENCES
Yehuda, R., Halligan, S.L., and Bierer, L.M., J. Psychiatr. Res., 2001, vol. 35, pp. 261–270.
Scharf, M., Dev. Psychopathol., 2007, vol. 19, pp. 603–622.
Yehuda, R., Daskalakis, N.P., Lehrner, A., Desarnaud, F., Bader, H.N., Makotkine, I., Flory, J.D., Bierer, L.M., and Meaney, M.J., Am. J. Psychiatry, 2014, vol. 171, pp. 872–880.
Rodgers, A.B., Morgan, C.P., Bronson, S.L., Revello, S., and Bale, T.L., J. Neurosci., 2013, vol. 33, pp. 9003–9012.
Dietz, D.M., Lapiant, Q., Watts, E.L., Hodes, G.E., Russo, S.J., Feng, J., Oosting, R.S., Vialou, V., and Nestler, E.J., Biol. Psychiatry, 2011, vol. 70, pp. 408–414.
Harker, A., Carroll, C., Raza, S., Kolba, B., and Gibb, R., Neuroscience, 2018, vol. 388, pp. 474–485.
Short, A.K., Fennell, K.A., Perreau, V.M., Fox, A., O’Bryan, M.K., Kim, J.H., Bredy, T.W., Pang, T.Y., and Hannan, A.J., Transl. Psychiatry, 2016, vol. 6, e837.
Chen, D.Y., Stern, S.A., Garcia-Osta, A., Saunier-Rebori, B., Pollonini, G., Bambah-Mukku, D., Blitzer, R.D., and Alberini, C.M., Nature, 2011, vol. 469, no. 7331, pp. 491–497.
Sasaki, H., Ishihara, K., and Kato, R.J., Biochemistry, 2000, vol. 127, pp. 711–715.
Tycko, B. and Morison, I.M., J. Cell Physiol., 2002, vol. 192, pp. 245–258.
Kohtz, A., Pollonini, G., Riccio, A., and Alberini, C.M., PLoS One, 2015, vol. 10, e0141078.
Yehuda, R., Ann. N.Y. Acad. Sci., 2009, vol. 1179, pp. 56–59.
Ordyan, N.E., Smolenskiy, I.V., Pivina, S.G., Akulova, V.K., and Rakitskaya, V.V., Neurosci. Behav. Physiol., 2014, vol. 44, pp. 657–663.
Livak, K.J. and Schmittgen, T.D., Methods, 2001, vol. 25, pp. 402–408.
Bergman, D., Halje, M., Nordin, M., and Engstrom, W., Gerontology, 2013, vol. 59, pp. 240–249.
Ho-Shing, O. and Dulac, C., Curr. Opin. Behav. Sci., 2019, vol. 25, pp. 66–76.
Russo, V.C., Goldin, A., Feldman, E.L., and Werther, G.A., Endocr. Rev., 2005, vol. 26, pp. 916–943.
Stern, S.A., Chen, D.Y., and Alberini, C.M., Learn. Memory, 2014, vol. 21, pp. 556–563.
Steinmetz, A.B., Johnson, S.A., Iannitelli, D.E., Pollonini, G., and Alberini, C.M., Neurobiol. Aging, 2016, vol. 44, pp. 9–21.
Pascual-Lucas, M., Viana da Silva, S., Di Scala, M., Garcia-Barroso, C., González-Aseguinolaza, G., Mulle, C., Alberini, C.M., Cuadrado-Tejedor, M., and Garcia-Osta, A., EMBO Mol. Med., 2014, vol. 6, pp. 1246–1262.
Nordin, M., Bergman, D., Halje, M., Ehgstrom, W., and Ward, A., Cell Prolifer., 2014, vol. 47, pp. 189–199.
Gabory, A., Jammes, H., and Dandolo, L., BioEssays, 2010, vol. 32, pp. 473–480.
Ratajczak, M.Z., Folia Histochem. Cytobiol., 2012, vol. 50, pp. 171–179.
Smith, G., Mungall, A.J., Griffiths-Jones, S., Smith, P., Buery, D., Matthews, L., Rogers, J., Pask, A.J., Shaw, G., Vandeberg, J.L., McCarrey, J.R., the SAVOIR Consortium, Renfree, M.B., Reik, W., and Dunhan, I., Nat. Genet., 2008, vol. 40, pp. 971–996.
Farzi-Molan, A., Babashah, S., Bakhshinejad, B., Atashi, A., and Fakhr Taha, M., Cell Biol. Int., 2018, vol. 42, pp. 940–948.
Chan, J.C., Nugent, B.M., and Bale, Y.L., Biol. Psychiatry, 2018, vol. 83, pp. 886–894.
Okada, Y. and Yamaguchi, K., Cell. Mol. Life Sci., 2017, vol. 74, pp. 1957–1967.
Chen, Q., Yan, W., and Duan, E., Nature Rev., 2016, vol. 17, pp. 733–743.
Yuan, S., Schuster, A., Tang, C., Yu, T., Ortogero, N., Bao, J., Zheng, H., and Yan, W., Development, 2016, vol. 143, pp. 635–647.
Mychasiuk, R., Harker, A., Ilnytskyy, S., and Gibb, R., Neuroscience, 2013, vol. 241, pp. 100–105.
Pedone, H.V., Pikaart, M.J., Cerrato, F., Vernucci, M., Undagro, P., Bruni, C.B., and Riccio, A., FEBS Lett., 1999, vol. 458, pp. 45–50.
Funding
This study was supported by the Russian Foundation for Basic Research, project no. 18–015–00186 (PI, Ordyan N.E.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest. The authors declare no conflict of interest.
Ethical approval. All experiments with animals were performed in accordance with the EU Directive 2010/63/EU for the care and use of animals for experimental procedures and the rules of “Guide for the Care and Use of Laboratory Animals”.
Rights and permissions
About this article
Cite this article
Ordyan, N.E., Malysheva, O.V., Akulova, V.K. et al. The Capability to Learn and Expression of the Insulin-Like Growth Factor II Gene in the Brain of Male Rats Whose Fathers Were Subjected to Stress Factors in the “Stress–Restress” Paradigm. Neurochem. J. 14, 191–196 (2020). https://doi.org/10.1134/S1819712420020075
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1819712420020075