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Transgenerational Sequelae of Acute Antenatal Stress in Pregnant Rats

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We report here the first studies of the effects of acute hypobaric hypoxia (AHH)during the period of early organogenesis on three sequential generations: the generation including pregnant females exposed to AHH (F0) and the two subsequent generations – F1 and F2. All three generations showed significant abnormalities in behavioral measures of motor and orientational-investigative activity, reflecting the state of anxiety, while generations F1 and F2 also showed changes in the ability of offspring to learn with positive reinforcement. These changes persisted to the pubertal period of life. In addition, females of generations F0 and F1 showed influences of AHH on maternal behavior, these influences being in different directions. The possible mechanisms of the effects of gestational stress during early organogenesis on subsequent generations are discussed.

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References

  1. Ya. Buresh, O. Bureshova, and J. P. Houston, Methods and Basic Experiments in Studies of the Brain and Behavior [in Russian], Vysshaya Shkola, Moscow (1991).

    Google Scholar 

  2. A. V. Graf, M. V. Maslova, A. S. Maklakova, et al., “Hypoxia during organogenesis has irreversible effects on heart activity and the noradrenalinergic component of regulation during the postnatal period,” Patogenez, No. 4, 1–3 (2005).

  3. A. V. Graf, M. V. Maslova, A. S. Maklakova, et al., “Antenatal acute hypoxia at different stages of embryogenesis alters behavioral patterns and bioamine levels in offspring,” Ros. Fiziol., 92, No. 2, 152–157 (2005).

    Google Scholar 

  4. A. V. Graf, M. V. Maslova, L. K. Trofimova, et al., “Effects of antenatal hypoxia on the developmental dynamics of ECG measures and biogenic amine contents in the central nervous system,” Byull. Eksperim. Biol. Med., 144, No. 8, 155–158 (2007).

    Google Scholar 

  5. V. A. Dubynin and A. A. Kamenskii, Beta-Casomorphines and Their Role in the Regulation of Behavior [in Russian], KMK Scientific Press, Moscow (2010).

    Google Scholar 

  6. T. Yu. Dunaeva, L. K. Trofimova, A. V. Graf, et al., “Transgenerational effects of antenatal acute hypoxia in early organogenesis,” Byull. Eksperim. Biol. Med., 146, No. 10, 364–366 (2008).

    Google Scholar 

  7. A. P. Dyban, V. F. Puchkov, V. S. Baranov, et al., “Laboratory mammals: the mouse (Mus musculus), rat (Rattus norvegicus), rabbit (Orictolagus cuniculus), and hamster (Cricetus griseolus),” in: Models for Developmental Biology [in Russian], Nauka, Moscow (1975).

  8. T. Cox, Stress [Russian translation], Meditsina, Moscow (1981).

    Google Scholar 

  9. V. A. Kosolanov, O. V. Ostrovskii, and A. A. Spasov, “Antioxidant defense and lipid peroxidation in rat tissues after hypobaric hypoxia,” Byull. Eksperim. Biol. Med., 126, No. 11, 519–521 (1998).

    Google Scholar 

  10. L. D. Luk’yanova, Methodological Recommendations for the Study of Agents Proposed for Clinical Study as Antioxidants [in Russian], Moscow (1990).

  11. L. D. Luk’yanova and I. D. Ushakov, The Problem of Hypoxia: Molecular, Physiological, and Medical Aspects [in Russian], Istoki, Voronezh (2004).

    Google Scholar 

  12. V. F. Puchkov and P. G. Svetlova, “Studies on the critical period of development and its significance for contemporary embryology,” Morfologiya, 105, No. 11, 147–158 (1993).

    CAS  Google Scholar 

  13. H. Selye, Stress without Distress [Russian translation], Progress, Moscow (1979).

    Google Scholar 

  14. L. K. Trofimova, A. A. Baizhumanov, E. N. Goncharenko, et al., “Changes in adrenal and plasma glucocorticoid contents in pregnant females and their offspring affected by antenatal stresses of different etiologies,” Izv. Ros. Akad. Nauk. Ser. Biol., No. 1, 101–106 (2011).

    Google Scholar 

  15. L. K. Trofimova, M. V. Maslova, A. V. Graf, et al., “Effects of antenatal hypoxic stress of different etiologies on males: correlation of behavioral patterns with changes in antioxidant defense activity and GABA metabolism,” Neirokhimiya, 25, No. 1–2, 86–89 (2008).

    CAS  Google Scholar 

  16. C. Bertram, O. Khan, S. Ohiri, et al., “Transgenerational effects of prenatal nutrient restriction on cardiovascular and hypothalamicpituitary-adrenal function,” J. Physiol., 586, No. 8, 2217–2229 (2008).

    Article  PubMed  CAS  Google Scholar 

  17. M. M. Brouwers, W. F. Feitz, L. A. Roelofs, et al., “Hypospadias: a transgenerational effect of diethylstilbestrol,” Hum. Reprod., 21, No. 3, 666–669 (2006).

    Article  PubMed  CAS  Google Scholar 

  18. A. J. Drake, B. R. Walker, and J. R. Seckl, “Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats,” Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, No. 1, 34–38 (2005).

    Article  Google Scholar 

  19. T. U. Dunaeva, A. V. Graf, L. K. Trofimova, et al., “Transgenerational effects of acute hypobaric hypoxia of early organogenesis on white rats posterity behavior and cognition function,” Acta Physiol., 196, 671 (2009).

    Google Scholar 

  20. E. W. Fish, D. Shahrokh, R. Bagot, et al., “Epigenetic programming of stress responses through variations in maternal care,” Ann. N.Y. Acad. Sci., 1036, 167–180 (2004).

    Article  PubMed  Google Scholar 

  21. D. Francis, J. Diorio, D. Liu, and M. J. Meaney, “Nongenomic transmission across generations of maternal behavior and stress responses in the rat,” Science, 286, No. 5442, 1155–1158 (1999).

    Article  PubMed  CAS  Google Scholar 

  22. A. V. Graf, A. V. Maslova, Y. V. Krushinskaya, et al., “The role of gestational acute stress in the development of prenatal pathologies,” Acta Physiol., 198, 677 (2010).

    Google Scholar 

  23. A. Kapoor, E. Dunn, A. Kostaki, et al., “Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids,” J. Physiol., 572, No. 1, 31–44 (2006).

    PubMed  CAS  Google Scholar 

  24. A. E. Kelley and C. G. Lang, “Effect of GBR 12909, a selective dopamine uptake inhibitor, on motor activity and operant behavior in the rat,” Eur. J. Pharmacol., 167, No. 3, 385–395 (1989).

    Article  PubMed  CAS  Google Scholar 

  25. A. Kostaki, D. Owen, D. Li, and S. G. Matthews, “Transgenerational effects of prenatal glucocorticoid exposure on growth, endocrine function, and behavior in the guinea pig,” Pediatr. Res., 58, 1–52 (2005).

    Article  Google Scholar 

  26. S. G. Matthews and D. I. Phillips, “Minireview: transgenerational inheritance of the stress response: a new frontier in stress research,” Endocrinol., 151, No. 1, 7–13 (2010).

    Article  CAS  Google Scholar 

  27. M. M. Myers, S. A. Brunelli, J. M. Squire, et al., “Maternal behavior of SHR rats and its relationship to offspring blood pressures,” Dev. Psychobiol., 22, No. 1, 29–53 (1989).

    Article  PubMed  CAS  Google Scholar 

  28. R. C. Painter, C. Osmond, P. Gluckman, et al., “Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life,” BJOG, 115, No. 10, 1243–1249 (2008).

    Article  PubMed  CAS  Google Scholar 

  29. L. K. Trofimova, A. V. Graf, T. Yu. Dunaeva, et al., “Influence of acute hypoxia on antioxidant system of non-pregnant and pregnant rats,” Acta Physiol., 193, No. 664, 138–139 (2008).

    Google Scholar 

  30. N. A. Youngson and E. Whitelaw, “Transgenerational epigenetic effects,” Annu. Rev. Genomics Hum. Genet., 9, 233–257 (2008).

    Article  PubMed  CAS  Google Scholar 

  31. E. Zambrano, P. M. Martinez-Samayoa, C. J. Bautista, et al., “Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation,” J. Physiol., 566, No. 1, 225–236 (2005).

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Faculty of Biology, M. V. Lomonosov Moscow State University, 1/12 Vorob’evy Gory, GSP-1, 119992, Moscow, Russia

    A. V. Graf, T. Yu. Dunaeva, A. S. Maklakova, M. V. Maslova, N. A. Sokolova & L. K. Trofimova

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  1. A. V. Graf
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  2. T. Yu. Dunaeva
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  3. A. S. Maklakova
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  4. M. V. Maslova
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  5. N. A. Sokolova
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  6. L. K. Trofimova
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Corresponding author

Correspondence to M. V. Maslova.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 98, No. 3, pp. 331–341, March, 2012.

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Graf, A.V., Dunaeva, T.Y., Maklakova, A.S. et al. Transgenerational Sequelae of Acute Antenatal Stress in Pregnant Rats. Neurosci Behav Physi 43, 1032–1038 (2013). https://doi.org/10.1007/s11055-013-9847-4

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  • DOI: https://doi.org/10.1007/s11055-013-9847-4

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