Skip to main content
SpringerLink
Log in

Change in the State of Neurons in the Medulla Oblongata of Fish Perccottus glehni during Wintering (Ultrastructural and Biochemical Studies)

  • Published:
Cell and Tissue Biology Aims and scope Submit manuscript

Abstract

The aim of this study was to conduct a comparative analysis of the ultrastructure of neurons of the medulla oblongata (MO) in fish during wintering and to identify the role of components of the synthesis and degradation systems in adapting to unfavorable conditions (hypoxia, hypothermia, starvation). Mautner neurons (MNs) localized in the MO have a wide set of metabolic and functional capabilities. They were shown to be able to accumulate glycogen, having their own system of glycogenesis, glycogenolysis, and deposition of glycogen, which is an alternative source of energy during wintering. The study of MO neurons located near the somatic part of the MN showed that some of these cells, like the MNs, are able to induce a similar additional energy source—glycogen—as indicated by the appearance of glycogen fields in their cytoplasm during wintering. In such cells, as in MNs, during this period, the components of the ultrastructure remain in an active state. The rough endoplasmic reticulum and polyribosomes retain an intact structure in them. At the same time, the Golgi apparatus is reorganized significantly and the catabolic system is activated. In other cells adjacent to MNs, in which there is no accumulation of glycogen, structural degradation is observed. Thus, the features of the ultrastructure of the studied MO neurons indicate the important role of glycogen in their functioning during the wintering period. It can be suggested that, in the medulla oblongata, MNs and some other neurons retain their activity, forming specific centers that are involved in the adaptation of fish to adverse wintering conditions.

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.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

REFERENCES

  1. Altan-Bonnet, N. and Lippincott, J., The golgi apparatus: structure, function and cellular dynamics, in Biogenesis of Cellular Organelles, New York: Academic/Plenum, 2005, pp. 96–110. https://doi.org/10.1007/b138220

  2. Barthet, V.J.A. and Ryan, K.M., Autophagy in neurodegeneration: can’t digest it spit it out, Trends Cell Biol., 2018, vol. 28, pp. 171–173. https://doi.org/10.1016/j.tcb.2018.01.001

    Article  PubMed  Google Scholar 

  3. Bocharova, L.S., Gordon, R.Ya., Rogaschevsky, V.V., Ignatyev, D.A., and Khutzian, S.S., Cyclic structural changes in endoplasmic reticulum and Golgi complex in the hippocampal neurons of ground squirrels during hibernation, Cell Tissue Biol., 2011, vol. 5, pp. 243–254. https://doi., 2011, vol. 101134/S1990519X11030023

  4. Caspenter, K.L.H., Jalloh, I., and Hutchinson, P.J., Glycolysis and the significance of lactate in traumatic brain injury, Front. Neurosci., 2015, vol. 9, pp. 1–16. https://dx.doi.org/10.3389%2Ffnins.2015.00112

    Google Scholar 

  5. Cataldo, A.M. and Broadwell, R.D., Cytochemical staining of the endoplasmic reticulum and glycogen in mouse anterior pituitary cells, J. Histochem. Cytochem., 1984, vol. 32, pp. 1285–1291.

    Article  CAS  Google Scholar 

  6. Cataldo, A.M. and Broadwell, R.D., Cytochemical identification of cerebral glycogen and glucose-6-phosphatase activity under normal and experimental conditions: I. Neurons and glia, J. Electron Microsc. Tech., 1986, vol. 3, pp. 413–437.

    Article  CAS  Google Scholar 

  7. Eaton, R.C., Farley, R.D., Kimmel, C.B., and Schabtach, E., Functional development in the Mauthner cell system of embryos and larvae of the zebra fish, J. Neurobiol., 1977, vol. 8, pp. 151–172. https://doi.org/10.1002/neu.480080207

    Article  CAS  PubMed  Google Scholar 

  8. Falkowska, A., Gutowska, I., Goschorska, M., Nowacki, P., Chlubek, D., and Baranowska-Bosiacka, I., Energy metabolism of the brain, including the cooperation between astrocytes and neurons, especially in the context of glycogen metabolism, Int. J. Mol. Sci., 2015, vol. 16, pp. 25959–25981. https://doi.org/10.3390/ijms1611259397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Fernandez-Fernandez, M.R., Ruiz-Garcia, D., Martin-Solana, E., Chichon, F.Ja., Carrascosa, J.L., and Fernandez, J.-J., 3D electron tomography of brain tissue unveils distinct golgi structures that sequester cytoplasmic contents in neurons, J. Cell Sci., 2017, vol. 130, pp. 83–89. https://doi.org/10.1242/jcs.188060

    Article  CAS  PubMed  Google Scholar 

  10. Gordon, R.Ya., Bocharova, L.S., Kruman, I.I., Popov, V.I., Kazantsev, A.P., Khutzian, S.S., and Karnaukhov, V.N., Acridine orange as an indicator of the cytometric ribosome state, Cytometry, 1997, vol. 29, pp. 215–221.

    Article  CAS  Google Scholar 

  11. Ivanov, K.P., Osnovy energetiki organizma, teoreticheskie i prakticheskie aspekty (Fundamentals of the Energy of the Organism: Theoretical and Practical Aspects), vol. 4: Energoresursy organizma i fiziologiya vyzhivaniya (Energy Resources of the Body and Survival Physiology). St. Petersburg: Nauka, 2004.

  12. Jin, Y., Lin, Y., Feng, J.F., Feng, J., Gao, G.Y., and Jiang, J.Y., Moderate hypothermia significantly decreases hippocampal cell death involving autophagy pathway after moderate traumatic brain injury, J. Neurotrauma, 2015, vol. 32, pp. 1090–1100. https://doi.org/10.1089/neu.2014.3649

  13. Karanova, M., Influence of low temperature on the evolution of amino acids pools adaptive modifications in poikilothermic animals (review), Int. J. Biochem. Biophys., 2013, vol. 1, pp. 33–40. https://doi.org/10.13189/ijbb.2013.010202

    Article  CAS  Google Scholar 

  14. Kimmel, C.B., Sessions, S.K, and Kimmel, R.J., Morphogenesis and synaptogenesis of the zebrafish Mauthner neuron, J. Comp. Neurol., 1981, vol. 198, pp. 101–120.

    Article  CAS  Google Scholar 

  15. Lim, Y., Cho, H., and Kim, E.-K., Brain metabolism as a model of autophagy in neurodegeneration, Brain Res., 2016, vol. 1649, pp. 158–165. https://doi.org/10.1016/j.brainres.2016.02.049

    Article  CAS  PubMed  Google Scholar 

  16. Maday, S., Mechanisms of neuronal homeostasis autophagy in the axon, Brain Res., 2017, vol. 1649, pp. 143–150. https://doi.org/10.1016/j.brainres.2016.03.047

    Article  CAS  Google Scholar 

  17. Moshkov, D.A., Adaptatsiya i ul’trastruktura neirona (Adaptation and Neuron Ultrastructure), Moscow: Nauka, 1985.

  18. Nixon, R.A., Wegiel, J., Kumar, A., Yu, W.H., Peterhoff, C., and Cataldo, A., Extensive involvement of autophagy in Alzheimer disease: an immunoelectron microscopy study, J. Neurophatol. Exp. Neurol., 2005, vol. 64, pp. 113–122.

    Article  Google Scholar 

  19. Persico, A., Cervigni, R.I., Borretta, M.L., and Colanzi, A., Mitotic inheritance of the Golgi complex, FEBS Lett., 2009, vol. 583, pp. 3857–3862. https://doi.org/10.1016/j.febslet.2009.10.077

    Article  CAS  PubMed  Google Scholar 

  20. Saez, I., Duran, J., Sinadinos, C., Beltran, A., Yanes, O., Tevy, M.F., Martınez-Pons, C., Milan, M., and Guinovar, J.J., Neurons have an active glycogen metabolism that contributes to tolerance to hypoxia, J. Cereb. Blood Flow Metab., 2014, vol. 34, pp. 945–955. https://doi.org/10.1038/jcbfm.2014.33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Santalova, I.M. and Moshkov, D.A., Smooth endoplasmic reticulum in fish Mauthner cells at different functional states, Neurosience, 1999, vol. 89, pp. 593–602. https://doi.org/10.1016/S0306-4522(98)00305-4

    Article  CAS  Google Scholar 

  22. Santalova, I.M., Penkova, N.A., Mikheeva, I.B., and Moshkov, D.A., Effect of winter dormancy on three-dimensional structure of the Mauthner neurons in Perccottus glehni fish, Probl. Kriobiol. Kriomed., 2015, vol. 25, pp. 114–121.

    Google Scholar 

  23. Santalova, I.M., Gordon, R.Ya., Mikheeva, I.B., Khutsian, S.S., and Maevsky, E.I., Peculiarities of the structure of glycogen as indicator of the functional state of Mauthner neurons in fish Perccottus glehni during wintering, Neurosci. Lett., 2018, vol. 664, pp. 133–138. https://doi.org/10.1016/j.neulet.2017.11.024

    Article  CAS  PubMed  Google Scholar 

  24. Tang, D., Wang, Ch., Gao, Y., Pua, J., Long, J., and Xu, W., Deep hypothermia-enhanced autophagy protects PC12 cells against oxygen glucose deprivation via a mitochondrial pathway, Neurosci. Lett., 2016, vol. 632, pp. 79–85. https://doi.org/10.1038/srep27642

    Article  CAS  PubMed  Google Scholar 

  25. Vaughn, J.E. and Grieshaber, J.A., An electron microscopic investigation of glycogen and mitochondria in developing and adult rat spinal motor neuropil, J. Neurucytol., 1972, vol. 1, pp. 397–594.

    Article  CAS  Google Scholar 

  26. Velickovska, V. and van Breukelen, F., Ubiquitylation of proteins in livers of hibernating golden-mantled ground squirrels, Spermophilus lateralis,Cryobiology, 2007, vol. 55, pp. 230–235. https://doi.org/10.1016/j.cryobiol.2007.08.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Weis, S.A., Zottoli, S.J., Do, S.C., Faber, D.S., and Preuss, T., Correlation of C-start behaviors with neural activity recorded from the hindbrain of free-swimming goldfish (Carassius auratus), J. Exp. Biol., 209, pp. 4788–4801. https://doi.org/10.1242/jeb.02582

Download references

Funding

The study was carried out under a state order to the Institute of Cell Biophysics of the Russian Academy of Sciences, topic no. 0116-2016-0005.

Author information

Authors and Affiliations

  1. Institute of Cell Biophysics, Russian Academy of Sciences, 142290, Pushchino, Moscow oblast, Russia

    R. Ya. Gordon, M. V. Karanova & S. S. Khutsian

  2. Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, 142290, Pushchino, Moscow oblast, Russia

    I. M. Santalova, I. B. Mikheeva & S. S. Khutsian

Authors
  1. R. Ya. Gordon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. M. Santalova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. B. Mikheeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. V. Karanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. S. Khutsian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Ya. Gordon.

Ethics declarations

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

Statement on the welfare of animals. All experimental procedures were carried out in accordance with the guidelines for the care and use of experimental animals approved by the Animal Ethics Committee in Institute of Theoretical and Experimental Biophysics of the Russian Academy of Sciences.

Additional information

Accepted abbreviations: GA—Golgi apparatus, MN—Mautner neurons, MO—medulla oblongata, ER—endoplasmic reticulum.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gordon, R.Y., Santalova, I.M., Mikheeva, I.B. et al. Change in the State of Neurons in the Medulla Oblongata of Fish Perccottus glehni during Wintering (Ultrastructural and Biochemical Studies). Cell Tiss. Biol. 14, 209–217 (2020). https://doi.org/10.1134/S1990519X20030037

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990519X20030037

Keywords:

Search

Navigation