Skip to main content
SpringerLink
Log in

Cystathionine β-Synthase in the Brain of the Trout Oncorhynchus mykiss after Unilateral Eye Damage and in Conditions of in vitro Cultivation

  • MECHANISMS OF CELL PROLIFERATION AND DIFFERENTIATION
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

Expression of cystathionine β-synthase (CBS) in the brain of adult trout under normal conditions and 1 week after an eye injury was assessed using Western blot analysis. The study of CBS distribution in the brain of intact trout and after a mechanical eye injury in the telencephalon, tectum, cerebellum, and brainstem was carried out by the method of immunoperoxidase labeling on free-floating sections. The results of the study showed an increase in CBS expression in different brain divisions after an eye injury. In the visual projection center of the brain (tectum), radial glia cells expressing CBS were revealed after the injury. The emergence of CBS+ heterogeneous radial glia in the trout tectum after eye injury indicates the ability of the reactive neural stem cells (NSC) to synthesize hydrogen sulfide. CBS+ fibers and cells were found in the proliferative zones of cerebellum (valvula) and telencephalon (ventral region). In the intact trout tegmentum, CBS expression was observed in large neurons of the dorsal region and in the proliferative zones. After the eye injury, reactive neurogenic niches appeared in the brainstem, and no CBS-immunopositivity was detected in the periventricular zone. The increased expression of H2S-producing CBS enzyme after a traumatic impact can probably be explained by the neuroprotective functions of hydrogen sulfide, which are implemented in the matrix zones of the brain associated with reparative neurogenesis. A cultivation of trout brain cells showed the formation of neurosphere-like complexes, a part of which exhibited CBS-immunopositivity in the monolayer.

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.
Fig. 8.

Similar content being viewed by others

REFERENCES

  1. Braun, K., Scheich, H., Schachner, M., and Heizmann, C.W., Distribution of parvalbumin, cytochrome oxidase activity and 14C-2-deoxyglucose uptake in the brain of the zebra finch. I. Auditory and vocal motor systems, Cell Tissue Res., 1985, vol. 240, pp. 101–115.

    Article  CAS  Google Scholar 

  2. Doe, C.Q., Fuerstenberg, S., and Peng, C.Y., Neural stem cells: from fly to vertebrates, J. Neurobiol., 1998, vol. 36, pp. 111–127.

    Article  CAS  PubMed  Google Scholar 

  3. Hinsch, K. and Zupanc, G.K., Generation and long-term persistence of new neurons in the adult zebrafish brain: a quantitative analysis, Neuroscience, 2007, vol. 146, pp. 679–696.

    Article  CAS  PubMed  Google Scholar 

  4. Kizil, C., Kaslin, J., Kroehne, V., and Brand, M., Adult neurogenesis and brain regeneration in zebrafish, Dev. Neurobiol., 2012, vol. 72, pp. 429–461.

    Article  PubMed  Google Scholar 

  5. Kyritsis, N., Kizil, C., Zocher, S., Kroehne, V., Kaslin, J., Freudenreich, D., Iltzsche, A., and Brand, M., Acute inflammation initiates the regenerative response in the adult zebrafish brain, Science, 2012, vol. 338, pp. 1353–1356.

    Article  CAS  PubMed  Google Scholar 

  6. Nagpure, B.V. and Bian, J.S., Brain, learning, and memory: role of H2S in neurodegenerative diseases, Handb. Exp. Pharmacol., 2015, vol. 230, pp. 193–215.

    Article  CAS  PubMed  Google Scholar 

  7. Ogino, T., Sawada, M., Takase, H., Nakai, C., Herranz-Pérez, V., Cebrián-Silla, A., Kaneko, N., García-Verdugo, J.M., and Sawamoto, K., Characterization of multiciliated ependymal cells that emerge in the neurogenic niche of the aged zebrafish brain, J. Comp. Neurol., 2016, vol. 524, pp. 2982–2992.

    Article  CAS  PubMed  Google Scholar 

  8. Palencia, G., Medrano, J.A., Ortiz-Plata, A., Farfan, D.J., Sotelo, J., Sanchez, A., and Trejo-Solis, C., Anti-poptotic, anti-oxidant, and anti-inflammatory effects of thalidomide on cerebral ischemia/reperfusion injury in rats, J. Neurol. Sci., 2015, vol. 351, pp. 78–87.

    Article  CAS  PubMed  Google Scholar 

  9. Puschina, E.V., Neurochemical organization and connections of the cerebral preglomerular complex of the masu salmon, Neurophysiology, 2012, vol. 43, no. 6, pp. 437–451.

    Article  Google Scholar 

  10. Pushchina, E.V. and Varaksin, A.A., Hydrogen sulfide-, parvalbumin-, and GABA-producing system in the masu salmon brain, Neurophysiology, 2011, vol. 43, no. 2, pp. 109–122.

    Google Scholar 

  11. Pushchina, E.V. and Varaksin, A.A., Neurolin expression in the optic nerve and immunoreactivity of Pax6-positive niches in the brain of rainbow trout (Oncorhynchus mykiss) after unilateral eye injury, Neural Regen. Res., [serial online]. 2019 [cited 2018 Nov 21]; vol. 14, pp. 156–171. Available from: http://www.nrronline. org/text.asp?2019/14/1/156/243721.

  12. Pushchina, E.V., Varaksin, A.A., and Obukhov, D.K., Cystathionine β-synthase in the CNS of masu salmon Oncorhynchus masou (Salmonidae) and carp Cyprinus carpio (Cyprinidae), Neurochem. J., 2011, vol. 5, no. 1, pp. 24–34.

    Article  CAS  Google Scholar 

  13. Pushchina, Ye.V., Obukhov, D.K., and Varaksin, A.A., Neurochemical markers of cells of the periventricular brain area in the masu salmon Oncorhynchus masou (Salmonidae), Russ. J. Dev. Biol., 2012a, vol. 43, no. 1, pp. 35–48.

    Article  CAS  Google Scholar 

  14. Pushchina, E.V., Varaksin, A.A., and Obukhov, D.K., Gaseous mediators in the brain of masu salmon Oncorhynchus masou (Salmoniformes, Salmonidae), Zh. Evol. Biokhim. Fiziol., 2012b, vol. 48, no. 1, pp. 85–95.

    CAS  PubMed  Google Scholar 

  15. Pushchina, E.V., Varaksin, A.A., Shukla, S., and Bulygyn, D.A., Multiphoton confocal microscopy (in vivo imaging) in the study of early response of macrophages/microglia in damaged midbrain of juvenile chum salmon Oncorhynchus keta, Am. J. BioSci. Spec. Iss.: Adult Repar. Neurog: Actual Quest., 2015a, vol. 3, nos. 2–3, pp. 12–18.

    CAS  Google Scholar 

  16. Pushchina, E.V., Shukla, S., and Varaksin, A.A., Hydrogen sulfide in proliferating and differentiated cells in primary cultures of juvenile brain of masu salmon Oncorhynchus masou, Adv. Biosci. Biotechnol., 2015b, vol. 6, pp. 539–545.

    Article  CAS  Google Scholar 

  17. Pushchina, E.V., Shukla, S., and Varaksin, A.A., Cell proliferation and differentiation in primary cultures of the juvenile brain of the masu salmon Oncorhynchus masou, Russ. J. Mar. Biol., 2015c, vol. 41, no. 6, pp. 499–502.

    Article  CAS  Google Scholar 

  18. Pushchina, E.V., Varaksin, A.A., and Obukhov, D.K., Reparative neurogenesis in the brain and changes in the optic nerve of adult trout Oncorhynchus mykiss after mechanical damage of the eye, Russ. J. Dev. Biol., 2016a, vol. 47, no. 1, pp. 11–32.

    Article  Google Scholar 

  19. Pushchina, E.V., Shukla, S., Varaksin, A.A., and Obu-khov, D.K., Cell proliferation and apoptosis in optic nerve and brain integration centers of adult trout Oncorhynchus mykiss after optic nerve injury, Neural Regen. Res., 2016b, vol. 11, pp. 578–590.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Pushchina, E.V., Varaksin, A.A., Obukhov, D.K., and Shukla, S., The Neurochemical Organization and Adult Neurogenesis in the Masu Salmon Oncorhynchus masou Brain, New York: Nova Science Publ., Inc., 2017a.

  21. Pushchina, E.V., Zharikova, E.I., and Varaksin, A.A., Persistent and reparative neurogenesis in the juvenile masu salmon Oncorhynchus masou telencephalon after mecha-nical injury, Russ. J. Dev. Biol., 2017b, vol. 48, no. 5, pp. 307–320.

    Article  Google Scholar 

  22. Pushchina, E.V., Varaksin, A.A., and Obukhov, D.K., The Pax2 and Pax6 transcription factors in the optic nerve and brain of trout Oncorhynchus mykiss after a mechanical eye injury, Russ. J. Dev. Biol., 2018, vol. 49, no. 5, pp. 264–290.

    Article  CAS  Google Scholar 

  23. Sodha, N.R. and Sellke, F.W., Attenuation of inflammatory responses by hydrogen sulfide (H2S) in ischemia/reperfusion injury, Methods Enzymol., 2015, vol. 555, pp. 127–144.

    Article  CAS  PubMed  Google Scholar 

  24. Ugrumov, M.V., Non-dopaminergic neurons partly expressing dopaminergic phenotype: distribution in the brain, development and functional significance, J. Chem. Neuroanat., 2009, vol. 38, pp. 241–256.

    Article  CAS  PubMed  Google Scholar 

  25. Ugrumov, M.V., Developing brain as an endocrine organ: a paradoxical reality, Neurochem. Res., 2010, vol. 35, pp. 837–850.

    Article  CAS  PubMed  Google Scholar 

  26. Wang, R., Physiological implication of hydrogen sulfide: a whiff exploration that blossomed, Physiol. Rev., 2012, vol. 92, pp. 791–896.

    Article  CAS  PubMed  Google Scholar 

  27. Wang, J.F., Li, Y., Song, J.N., and Pang, H.G., Role of hydrogen sulfide in secondary neuronal injury, Neurochem. Int., 2014, vol. 64, pp. 37–47.

    Article  CAS  PubMed  Google Scholar 

  28. Wu, D., Wang, J., Li, H., Xue, M., Ji, A., and Li, Y., Role of hydrogen sulfide in ischemia-reperfusion injury, Oxid. Med. Cell. Longev., 2015. https://doi.org/10.1155/2015/186908

  29. Zhang, X. and Bian, J.S., Hydrogen sulfide: a neuromodulator and neuroprotectant in the central nervous system, ACS Chem. Neurosci., 2014, vol. 5, pp. 876–883.

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

The work was financially supported by the president of the Russian Federation (grant no. MD-4318.2015.4) and the Far East Program for Basic Research for 2015–2017, Far East Branch, Russian Academy of Sciences (project no. 15-I-6-116, section III).

Author information

Authors and Affiliations

  1. National Scientific Center of Marine Biology, Far East Branch, Russian Academy of Sciences, 690041, Vladivostok, Russia

    E. V. Pushchina & A. A. Varaksin

  2. Bogomoletz Institute of Physiology, National Academy of Sciences of Ukraine, 01024, Kyiv, Ukraine

    E. V. Pushchina

  3. St. Petersburg University, 199034, St. Petersburg, Russia

    D. K. Obukhov

Authors
  1. E. V. Pushchina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. Varaksin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. K. Obukhov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. V. Pushchina.

Additional information

Translated by E. Shvetsov

Abbreviations: CBS–, cystathionine β-synthase-negative; CBS+, cystathionine β-synthase-positive; KATP, ATP-sensitive potassium channels; Vd, dorsal zone of the telencephalon ventral region; GABA+, gamma-aminobutyric acid-immunopositive cells; DTN, dorsal tegmentum nuclei; Dc, central zone of the telencephalon dorsal region; ODU, optical density units; IHC, immunohistochemistry; MRF, mesencephalic reticular formation; SM, stratum marginale (marginal layer); NSC, neural stem cells; ON, optic nerve; OD, optical density; OL, layer of optic fibers; OT, optic tectum; PA, parvalbumin; PA+, parvalbumin-immunopositive cells; PVZ, periventricular zone; PVL, periventricular layer; RG, radial glia; RF, reticular formation; SVZ, subventricular zone; SGAC, stratum griseum et album centrale (central gray and white layer); SGC, stratum griseum centrale (central gray layer).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pushchina, E.V., Varaksin, A.A. & Obukhov, D.K. Cystathionine β-Synthase in the Brain of the Trout Oncorhynchus mykiss after Unilateral Eye Damage and in Conditions of in vitro Cultivation. Russ J Dev Biol 50, 39–58 (2019). https://doi.org/10.1134/S1062360419020048

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360419020048

Keywords:

Search

Navigation