Skip to main content
SpringerLink
Log in

The Effect of a Single Heating Treatment on Laboratory Mice Behavior, Adult Neurogenesis, and the Expression of Heatshock Protein HSP-70

  • RESEARCH ARTICLE
  • Published:
Moscow University Biological Sciences Bulletin Aims and scope Submit manuscript

Abstract

Male hybrid mice (F1 CBA × C57BL/6J) were kept for 1.5 h at 39.5°С. In cognitive tests (extrapolation and puzzle-box elementary logic task solution), mice of the experimental groups (after exposure to an elevated temperature) solved the tasks more quickly and more successfully, while their activity in the “small open field” (in which no stress-inducing stimuli were present) and in the Porsolt test (unescapable swimming) was higher than in control mice. In separate experiments, the temporary impairment in the adult neurogenesis (the decrease of new cell numbers detected immunо-histochemically by the marker Ki67) after elevated temperature exposure was demonstrated in both the subgranular area of dentate fascia and in the subventricular proliferative zone of the forebrain. The heating treatment was accompanied by the increase of HSP-70 expression at the time point 3 h after the treatment, while no differences from control were found after 24 h.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Pastukhov, Yu.F. and Ekimova, I.V., Molecular, cellular and protective functions of the heat shock protein 70 kDa, Neironauki, 2005, vol. 2, no. 2, pp. 3–25.

    Google Scholar 

  2. De Maio, A., Extracellular HSP70: Export and function, Curr. Protein Pept. Sci., 2014, vol. 15, no. 3, pp. 225–231.

    Article  CAS  PubMed  Google Scholar 

  3. Bozaykut, P., Ozer, N.K., and Karademir, B., Regulation of protein turnover by heat shock proteins, Free Radic. Biol. Med., 2014, vol. 77, pp. 195–209.

    Article  CAS  PubMed  Google Scholar 

  4. Ren, M., Leng, Y., Jeong, M., Leeds, P.R., and Chuang, D.M., Valproic acid reduces brain damage induced by transient focal cerebral ischemia in rats: Potential roles of histone deacetylase inhibition and heat shock protein induction, J. Neurochem., 2004, vol. 89, no. 6, pp. 1358–1367.

    Article  CAS  PubMed  Google Scholar 

  5. Santoro, M.G., Heat shock factors and the control of the stress response, Biochem. Pharmacol., 2000, vol. 59, no. 1, pp. 55–63.

    Article  CAS  PubMed  Google Scholar 

  6. Zlatković, J., Bernardi, R.E., and Filipović, D., Protective effect of Hsp70i against chronic social isolation stress in the rat hippocampus, J. Neural Transm. (Vienna), 2014, vol. 121, no. 1, pp. 3–14.

    Article  CAS  PubMed  Google Scholar 

  7. Duhan, V., Joshi, N., Nagarajan, P., and Upadhyay, P., Protocol for long duration whole body hyperthermia in mice, J. Vis. Exp., 2012, vol. 25, no. 66.

  8. Bobkova, N., Guzhova, I., Margulis, B., Nesterova, I., Medvedinskaya, N., Samokhin, A., Alexandrova, I., Garbuz, D., Nudler, E., and Evgen’ev, M., Dynamics of endogenous HSP70 synthesis in the brain of olfactory bulbectomized mice, Cell Stress Chaperon, 2013, vol. 18, no. 1, pp. 109–118.

    Article  CAS  Google Scholar 

  9. Evgen’ev, M.B., Krasnov, G.S., Nesterova, I.V., Garbuz, D.G., Karpov, V.L., Morozov, A.V., Snezhkina, A.V., Samokhin, A.N., Sergeev, A., Kulikov, A.M., and Bobkova, N.V., Molecular mechanisms underlying neuroprotective effect of intranasal administration of human hsp70 in mouse model of Alzheimer’s disease, J. Alzheimers. Dis., 2017, vol. 59, no. 4, pp. 1415–1426.

    Article  CAS  PubMed  Google Scholar 

  10. Chen, S. and Brown, I.R., Neuronal expression of constitutive heat shock proteins: Implications for neurodegenerative diseases, Cell Stress Chaperon, 2007, vol. 12, no. 1, pp. 51–58.

    Article  CAS  Google Scholar 

  11. Zhu, C., Wu, Y., Chen, S., Yu, M., Zeng, Y., You, X., Xiao, J., and Wang, S., Protective immune responses in mice induced by intramuscular and intranasal immunization with a Mycoplasma pneumoniae P1C DNA vaccine, Can. J. Microbiol., 2012, vol. 58, no. 5, pp. 644–652.

    Article  CAS  PubMed  Google Scholar 

  12. Wang, Y.S., Liu, S.J., Huang, S.C., Chang, C.C., Huang, Y.C., Fong, W.L., Chi, M.S., and Chi, K.H., Recombinant heat shock protein 70 in combination with radiotherapy as a source of tumor antigens to improve dendritic cell immunotherapy, Front. Oncol., 2012, vol. 2, p. 149.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Ohnishi, K., Matsumoto, H., Takahashi, A., Wang, X., and Ohnishi, T., Heat shock transcription factor, HSF, is activated by ultraviolet irradiation, Photochem. Photobiol., 1996, vol. 64, no. 6, pp. 949–952.

    CAS  PubMed  Google Scholar 

  14. Liu, F.F., Miller, N., Levin, W., Zanke, B., Cooper, B., Henry, M., Sherar, M.D., Pintilie, M., Hunt, J.W., and Hill, R.P., The potential role of HSP70 as an indicator of response to radiation and hyperthermia treatments for recurrent breast cancer, Int. J. Hyperthermia, 1996, vol. 12, no. 2, pp. 197–208.

    Article  CAS  PubMed  Google Scholar 

  15. Lee, H.J., Lee, Y.J., Kwon, H.C., Bae, S., Kim, S.H., Min, J.J., Cho, C.K., and Lee, Y.S., Radioprotective effect of heat shock protein 25 on submandibular glands of rats, Am. J. Pathol., 2006, vol. 169, no. 5, pp. 1601–1607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Schildkopf, P., Frey, B., Ott, O.J., Rubner, Y., Multhoff, G., Sauer, R., Fietkau, R., and Gaipl, U.S., Radiation combined with hyperthermia induces HSP70-dependent maturation of dendritic cells and release of pro-inflammatory cytokines by dendritic cells and macrophages, Radiother. Oncol., 2011, vol. 101, no. 1, pp. 109–115.

    Article  CAS  PubMed  Google Scholar 

  17. Fedotova, I.B., Nikolaev, G.M., Kostyna, Z.A., and Poletaeva, I.I., Remote effects of short-term neonatal hyperthermia in Krushinsky-Molodkina rats prone to audiogenic seizures strain, Dokl. Biol. Sci., 2017, vol. 472, no. 1, pp. 1–3.

    Article  CAS  PubMed  Google Scholar 

  18. Krushinskii, L.V., Biologicheskie osnovy rassudochnoi deyatel’nosti (Biological Elements of Rational Activity), Moscow: Mosk. Gos. Univ., 1977.

  19. Poletaeva, I.I., Popova, N.V., and Romanova, L.G., Genetic aspects of animal reasoning, Behav. Genet., 1993, vol. 23, no. 5, pp. 467–475.

    Article  CAS  PubMed  Google Scholar 

  20. Perepelkina, O.V., Golibrodo, V.A., Lilp, I.G., and Poletaeva, I.I., Selection of mice for high scores of elementary logical task solution, Dokl. Biol. Sci., 2015, vol. 460, no. 1, pp. 52–56.

    Article  CAS  PubMed  Google Scholar 

  21. Galsworthy, M.J., Paya-Cano, J.L., Liu, L., Monleón, S., Gregoryan, G., Fernandes, C., Schalkwyk, L.C., and Plomin, R., Assessing reliability, heritability and general cognitive ability in a battery of cognitive tasks for laboratory mice, Behav. Genet., 2005, vol. 35, no. 5, pp. 675–692.

    Article  PubMed  Google Scholar 

  22. Ben Abdallah, N.M.-B., Fuss, J., Trusel, M., Galsworthy, M.J., Bobsin, K., Colacicco, G., Deacon, R.M., Riva, M.A., Kellendonk, C., Sprengel, R., Lipp, H.P., and Gass, P., The puzzle box as a simple and efficient behavioral test for exploring impairments of general cognition and executive functions in mouse models of schizophrenia, Exp. Neurol., 2011, vol. 227, no. 1, pp. 42–52.

    Article  PubMed  Google Scholar 

  23. Porsolt, R.D., Animal model of depression, Biomedicine, 1979, vol. 30, no. 3, pp. 139–140.

    CAS  PubMed  Google Scholar 

  24. Zucca, P., Milos, N., and Vallortigara, G., Piagetian object permanence and its development in Eurasian jays (Garrulus glandarius), Anim. Cognit., 2007, vol. 10, no. 2, pp. 243–258.

    Article  Google Scholar 

  25. Timoshenko, T.V., Perepelkina, O.V., Markina, N.V., Revischin, A.V., Pavlova, G.V., Poletaeva, I.I., and Sukhih, G.T., Audiogenic epilepsy in mice with different genotypes after neonatal treatments enhancing neurogenesis in dentate gyrus, Bull. Exp. Biol. Med., 2009, vol. 147, no. 4, pp. 458–461.

    Article  CAS  PubMed  Google Scholar 

  26. Cleveland, D.W., Fischer, S.G., Kirschner, M.W., and Laemmli, U.K., Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis, J. Biol. Chem., 1977, vol. 252, no. 3, pp. 1102–1106.

    CAS  PubMed  Google Scholar 

  27. Schneider, C.A., Rasband, W.S., and Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis, Nat. Methods, 2012, vol. 9, no. 7, pp. 671–675.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Lipp, H.-P., Evolutionary shaping of adult hippocampal neurogenesis in mammals–cognitive gain or developmental priming of personality traits?, Front. Neurosci., 2017, vol. 11, p. 420.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Vilar, M. and Mira, H., Regulation of neurogenesis by neurotrophins during adulthood: Expected and unexpected roles, Front Neurosci., 2016, vol. 10, p. 26.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Rossi, C., Angelucci, A., Costantin, L., Braschi, C., Mazzantini, M., Babbini, F., Fabbri, M.E., Tessarollo, L., Maffei, L., Berardi, N., and Caleo, M., Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment, Eur. J. Neurosci., 2006, vol. 24, no. 7, pp. 1850–1856.

    Article  PubMed  Google Scholar 

  31. Hashimoto, K., Tomitaka, S., Bi, Y., Narita, N., Minabe, Y., and Iyo, M., Rolipram, a selective phosphodiesterase type-IV inhibitor, prevents induction of heat shock protein HSP-70 and hsp-70 mRNA in rat retrosplenial cortex by the NMDA receptor antagonist dizocilpine, Eur. J. Neurosci., 1997, vol. 9, no. 9, pp. 1891–1901.

    Article  CAS  PubMed  Google Scholar 

  32. Wetsel, W.C., Hyperthermic effects on behavior, Int. J. Hyperthermia, 2011, vol. 7, no. 4, pp. 353–373.

    Article  Google Scholar 

Download references

Funding

The work was supported by the Russian Foundation for Basic Researches (grant no. 17-29-01001 and state registration project AAAA-A16-116021660055-1.

Author information

Authors and Affiliations

  1. Department of Biology, Moscow State University, 119234, Moscow, Russia

    O. V. Perepelkina, N. A. Ogienko, I. G. Lilp & I. I. Poletaeva

  2. Institute of Molecular Biology, Russian Academy of Sciences, 119991, Moscow, Russia

    D. G. Garbuz

  3. Institute of Gene Biology, Russian Academy of Sciences, 119334, Moscow, Russia

    A. V. Revishchin & G. V. Pavlova

Authors
  1. O. V. Perepelkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. A. Ogienko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. G. Lilp
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. G. Garbuz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. V. Revishchin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. G. V. Pavlova
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. I. I. Poletaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. I. Poletaeva.

Ethics declarations

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. Experiments were performed according to the Directive 2010/63/EU of European Parliament and European Union Council on welfare of animals used for scientific goals.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Perepelkina, O.V., Ogienko, N.A., Lilp, I.G. et al. The Effect of a Single Heating Treatment on Laboratory Mice Behavior, Adult Neurogenesis, and the Expression of Heatshock Protein HSP-70. Moscow Univ. Biol.Sci. Bull. 74, 86–91 (2019). https://doi.org/10.3103/S0096392519020093

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0096392519020093

Keywords:

Search

Navigation