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Neuroscience and Behavioral Physiology

, Volume 40, Issue 6, pp 693–700 | Cite as

Effects of Hypoxic Preconditioning on Expression of Transcription Factor NGFI-A in the Rat Brain after Unavoidable Stress in the “Learned Helplessness” Model

  • K. A. Baranova
  • E. A. Rybnikova
  • V. I. Mironova
  • M. O. Samoilov
Article

We report here our immunocytochemical studies establishing that the development of a depression-like state in rats following unavoidable stress in a “learned helplessness” model is accompanied by stable activation of the expression of transcription factor NGFI-A in the dorsal hippocampus (field CA1) and the magnocellular paraventricular nucleus of the hypothalamus, along with an early wave of post-stress expression, which died down rapidly, in the ventral hippocampus (the dentate gyrus) and a long period of up to five days of high-level expression in the neocortex. In rats subjected to three sessions of preconditioning consisting of moderate hypobaric hypoxia (360 mmHg, 2 h, with intervals of 24 h), which did not form depression in these circumstances, there were significant changes in the dynamics of immunoreactive protein content in the hippocampus, with a stable increase in expression in the ventral hippocampus and only transient and delayed (by five days) expression in field CA1. In the neocortex (layer II), preconditioning eliminated the effects of stress, preventing prolongation of the first wave of NGFI-A expression to five days, while in the magnocellular hypothalamus, conversely, preconditioning stimulated a second (delayed) wave of the expression of this transcription factor. The pattern of NGFI-A expression in the hippocampus, neocortex, and hypothalamus seen in non-preconditioned rats appears to reflect the pathological reaction to aversive stress, which, rather than adaptation, produced depressive disorders. Post-stress modification of the expression of the product of the early gene NGFI-A in the brain induced by hypoxic preconditioning probably plays an important role in increased tolerance to severe psychoemotional stresses and is an important component of antidepressant mechanisms.

Key words

NGFI-A hypoxic preconditioning psychoemotional stress depressive states neuroprotection “learned helplessness” 

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References

  1. 1.
    K. V. Beltikova and Ya. A. Kochetkov, “Characteristics of clinicalhormonal interactions in depressive disorders,” in: Current Problems in Psychiatric Endocrinology. Collection of Studies [in Russian], Moscow (2004), pp. 77–91.Google Scholar
  2. 2.
    E. A. Rybnikova, V. I. Mironova, E. I. Tyulkova, and M. O. Samoilov, “Anxiolytic effects of moderate hypobaric hypoxia in rats in a model of post-traumatic stress disorder,” Zh. Vyssh. Nerv. Deyat., 4, 475–482 (2008).Google Scholar
  3. 3.
    E. A. Rybnikova, L. I. Khozhai, E. I. Tyulkova, T. S. Glushchenko, N. A. Sitnik, M. Pelto-Huikko, V. A. Otellin, and M. V. Samoilov, “Expression of early gene proteins, structural changes in brain neurons in hypobaric hypoxia, and the correcting effect of preconditioning,” Morfologiya, 125, No. 2, 10–15 (2004).Google Scholar
  4. 4.
    M. O. Samoilov, E. A. Rybnikova, E. I. Tyulkova, L. A. Vataeva, V. A. Otellin, and L. I. Khozhai, “Effects of hypobaric hypoxia on behavioral responses and early gene expression in the rat brain: the correcting effect of preconditioning,” Dokl. Ros. Akad. Nauk., 381, 513–515 (2001).Google Scholar
  5. 5.
    E. Belaidi, P. C. Beguin, C. Ribuot, and D. Godin-Ribuot, “Hypoxic preconditioning: role of transcription factor HIF-1alpha,” Ann. Cardiol. Angiol., 55, No. 2, 70–73 (2006).CrossRefGoogle Scholar
  6. 6.
    L. Bjartmar, I. M. Johansson, J. Marcusson, S. B. Ross, J. R. Seckl, and T. Olsson, “Selective effects on NGFI-A, MR, GR and NGFI-B hippocampal mRNA expression after chronic treatment with different subclasses of antidepressants in the rat,” Psychopharmacology (Berlin), 151, No. 1, 7–12 (2000).Google Scholar
  7. 7.
    B. Bozon, S. Davis, and S. Laroche, “Regulated transcription of the immediate-early gene Zif268: mechanisms and gene dosage-dependent function in synaptic plasticity and memory formation,” Hippocampus, 12, No. 5, 570–577 (2002).CrossRefPubMedGoogle Scholar
  8. 8.
    X. Cao, R. A. Koski, A. Gashler, M. McKiernan, C. F. Morris, R. Gaffney, R. V. Hay, and V. P. Sikhatme, “Identification and characterization of the EGR-1 gene product, a DNA-binding zinc finger protein induced by differentiation and growth signals,” Mol. Cell. Biol., 10, 1931–1939 (1990).PubMedGoogle Scholar
  9. 9.
    Y. Dai, M. Xu,Y. Wang, Z. Pasha, T. Li, and M. Ashraf, “HIF-1alpha induced-VEGF overexpression in bone marrow stem cells protects cardiomyocytes against ischemia,” J. Mol. Cell. Cardiol., 42, No. 6, 1036–1044, (2007).CrossRefPubMedGoogle Scholar
  10. 10.
    S. Davis, B. Bozon, and S. Laroche, “How necessary is the activation of the immediate early gene zif 268 in synaptic plasticity and learning?” Brain Res., 142, No. 1, 17–30 (2003).Google Scholar
  11. 11.
    S. Fulda and K. M. Debatin, “HIF-1-regulated glucose metabolism: a key to apoptosis resistance?” Cell Cycle, 6, No. 7, 790–792 (2007).PubMedGoogle Scholar
  12. 12.
    M. T. Ghorbel, I. Seugnet, N. Hadj-Sahraoui, P. Topilko, G. Levi, and B. Demeneix, “Thyroid hormone effects on Krox-24 transcription in the post-natal mouse brain are developmentally regulated but are not correlated with mitosis,” Oncogene, 18, No. 4, 917–924 (1999).CrossRefPubMedGoogle Scholar
  13. 13.
    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/ATF proteins,” Brain Res. Rev., 28, No. 3, 370–490 (1998).CrossRefPubMedGoogle Scholar
  14. 14.
    D. M. Holtzman, R. A. Sheldon,W. Jaffe,Y. Cheng, and D. M. Ferriero, “Nerve growth factor protects the neonatal brain against hypoxic-ischemic injury,” Ann. Neurol., 39, No. 1, 114–122 (1996).CrossRefPubMedGoogle Scholar
  15. 15.
    J. Honkaniemi and F. R. Sharp, “Global ischemia induces immediate-early genes encoding zinc finger transcription factors,” J. Cereb. Blood Flow Metab., 16, No. 4, 557–565 (1996).CrossRefPubMedGoogle Scholar
  16. 16.
    M. W. Jones, M. L. Errington, P. J. French, A. Fine, T. V. Bliss, S. Garel, P. Charnay, B. Bozon, S. Laroche, and S. Davis, “A requirement for the immediate early gene Zif268 in the expression of late LTP and longterm memories,” Nat. Neurosci., 4, No. 3, 289–296 (2001).CrossRefPubMedGoogle Scholar
  17. 17.
    E. Knapska and L. Kaczmarek, “A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK?” Prog. Neurobiol., 74, No. 4, 183–211 (2004).CrossRefPubMedGoogle Scholar
  18. 18.
    T. W. Lovenberg, M. G. Erlander, B. M. Baron, and J. G. Sutcliffe, “Cloning of new 5-HT receptors,” Int. Clin. Psychopharmacol., 8, Supplement 2, 19–23 (1993).CrossRefPubMedGoogle Scholar
  19. 19.
    S. Morinobu, H. Strausbaugh, R. Terwilliger, and R. S. Duman, “Regulation of c-Fos and NGFI-A by antidepressant treatments,” Synapse, 25, No. 4, 313–320 (1997).CrossRefPubMedGoogle Scholar
  20. 20.
    T. Olsson, A. Hakansson, and J. R. Seckl, “Ketanserin selectively blocks acute stress-induced changes in NGFI-A and mineralocorticoid receptor gene expression in hippocampal neurons,” Neurosci., 76, No. 2, 441–448 (1997).CrossRefGoogle Scholar
  21. 21.
    G. Paxinos and G. Watson, The Rat Brain in Stereotaxic Coordinates, Academic Press, San Diego (1986).Google Scholar
  22. 22.
    C. Pipaon, A. Santos, and A. Perez-Castillo, Thyroid hormone upregulates NGFI-A gene expression in rat brain during development,” J. Biol. Chem., 267, No. 1, 21–23 (1992).PubMedGoogle Scholar
  23. 23.
    J. L. Plassat, N. Amlaiky, and R. Hen, “Molecular cloning of a mammalian serotonin receptor that activates adenylate cyclase,” Mol. Pharmacol., 44, No. 2, 229–236 (1993).PubMedGoogle Scholar
  24. 24.
    J. B. Rosen, M. S. Fanselow, S. L. Young, M. Sitcoske, and S. Maren, “Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning,” Brain Res., 796, No. 1–2, 132–142 (1998).CrossRefPubMedGoogle Scholar
  25. 25.
    E. Rybnikova, V. Mironova, S. Pivina, R. Tulkova, N. Ordyan, L. Vataeva, E. Vershinina, E. Abritalin, A. Kolchev, N. Nalivaeva, A. J. Turner, and M. Samoilov, “Antidepressant-like effects of mild hypoxia preconditioning in the learned helplessness model in rats,” Neurosci. Lett., 417, No. 3, 234–239 (2007).CrossRefPubMedGoogle Scholar
  26. 26.
    E. Rybnikova, E. Tulkova, M. Pelto-Huikko, and M. Samoilov, “Mild preconditioning hypoxia modifies nerve growth factorinduced gene A messenger RNA expression in the rat brain induced by severe hypoxia,” Neurosci. Lett., 329, No. 1, 49–52, (2002).CrossRefPubMedGoogle Scholar
  27. 27.
    E. Rybnikova, L. Vataeva, E. Tyulkova, T. Gluschenko, V. Otellin, M. Pelto-Huikko, and M. O. Samoilov, “Mild hypoxia preconditioning prevents impairment of passive avoidance learning and suppression of brain NGFI-A expression induced by severe hypoxia,” Behav. Brain Res., 160, No. 1, 107–114 (2005).CrossRefPubMedGoogle Scholar
  28. 28.
    E. A. Rybnikova,V. I. Mironova, S. G. Pivina, N. E. Ordyan, E. I. Tyulkova, and M. O. Samoilov, “Hypoxic preconditioning prevents development of post-stress depressions in rats,” Dokl. Biol. Sci., 411, 431–433 (2006).CrossRefPubMedGoogle Scholar
  29. 29.
    R. M. Sapolsky, “Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders,” Arch. Gen. Psychiatry, 57, 925–935 (2000).CrossRefPubMedGoogle Scholar
  30. 30.
    M. E. Seligman and G. Beagley, “Learned helplessness in the rat,” J. Comp. Physiol. Psychol., 88, 534–541 (1975).CrossRefPubMedGoogle Scholar
  31. 31.
    E. Senba and T. Ueyama, “Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat,” Neurosci. Res., 29, No. 3, 183–207 (1997).CrossRefPubMedGoogle Scholar
  32. 32.
    F. R. Sharp, R. Ran, A. Lu,Y. Tang, K. I. Strauss, T. Glass, T. Ardizzone, and M. Bernaudin, “Hypoxic preconditioning protects against ischemic brain injury,” NeuroRx, 1, No. 1, 26–35 (2004).CrossRefPubMedGoogle Scholar
  33. 33.
    M. Sheng and M. E. Greenberg, “The regulation and function of c-fos and other immediate early genes in the nervous system,” Neuron, 44, No. 4, 477–485 (1990).CrossRefGoogle Scholar
  34. 34.
    V. P. Sukhatme, X. Cao, L. C. Chang, C. Tsai-Morris, D. Stamenkovich, P. C. P. Ferreira, D. R. Cohen, S. A. Edwards, T. B. Shows, T. Curran, M. M. Le Beau, and E. D. Adamson, “A zinc fingerencoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization,” Cell, 53, 37–43 (1988).CrossRefPubMedGoogle Scholar
  35. 35.
    A. P. Tsou, A, Kosaka, C. Bach, P. Zuppan, C. Yee, L. Tom, R. Alvarez, D. Ramsey, D. W. Bonnhaus, E. Stefanich, et al., “Cloning and expression of a 5-hydroxytryptamine7 receptor positively coupled to adenylyl cyclase,” J. Neurochem., 63, No. 2, 456–464 (1994).PubMedGoogle Scholar
  36. 36.
    R. Tupler, G. Perini, and M. R. Green, “Expressing the human genome,” Nature, 409, 832–833 (2001).CrossRefPubMedGoogle Scholar
  37. 37.
    T. Ueyama, H. Ohya, R. Yoshimura, and E. Senba, “Effects of ethanol on the stress-induced expression of NGFI-A mRNA in the rat brain,” Alcohol, 18, No. 2–3, 171–176 (1999).CrossRefPubMedGoogle Scholar
  38. 38.
    S. Umemoto,Y. Kawai, and E. Senba, “Differential regulation of IEGs in the rat PVH in single and repeated stress models,” Neuroreport, 6, No. 1, 201–204 (1994).CrossRefPubMedGoogle Scholar
  39. 39.
    J. Q. Wang, “Regulation of immediate early gene c-fos and zif/268 mRNA expression in rat striatum by metabotropic glutamate receptor,” Mol. Brain Res., 57, No. 1, 46–53 (1998).CrossRefPubMedGoogle Scholar
  40. 40.
    I. C. Weaver, A. C. D’Alessio, S. E. Brown, I. C. Hellstrom, S. Dymov, S. Sharma, M. Szyf, and M. J. Meaney, “The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes,” J. Neurosci., 27, No. 7, 1756–1768 (2007).CrossRefPubMedGoogle Scholar
  41. 41.
    V. L. Woodburn, N. J. Hayward, J. A. Poat, G. N. Woodruff, and J. Hughes, “The effect of dizocilpine and enadoline on immediate early gene expression in the gerbil global ischaemia model,” Neuropharmacology, 32, No. 10, 1047–1059 (1993).CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2010

Authors and Affiliations

  • K. A. Baranova
    • 1
  • E. A. Rybnikova
    • 1
  • V. I. Mironova
    • 1
  • M. O. Samoilov
    • 1
  1. 1.Pavlov Institute of PhysiologyRussian Academy of SciencesSt. PetersburgRussia

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