Skip to main content
Log in

Proliferation and Neuro- and Gliogenesis in Normal and Mechanically Damaged Mesencephalic Tegmentum in Juvenile Chum Salmon, Oncorhynchus keta

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

Abstract

Processes of proliferation and constitutive neuro- and gliogenesis in the mesencephalic tegmentum of intact juvenile chum salmon, Oncorhynchus keta, and at 3 days after a traumatic injury were studied by immunohistochemistry (IHC) labeling of PCNA, HuCD, and GFAP. In the chum tegmentum, the proliferative activity was revealed both in separate cells and in small cell clusters of the periventricular zone (PVZ). The presence of constitutive neurogenic zones provides the processes of persistent brain growth. After damage to the tegmentum, proliferation in PVZ is activated, the constitutive neurogenic zones reactivate, reactive neurogenic niches form in the parenchyma, and the proliferative activity is also initiated in the centers of secondary proliferation (basal tegmentum). It was first found that traumatic damage to the tegmentum leads to accelerated differentiation of neurons in the subventricular zone (SVZ) and dorsomedial tegmentum as well as to the appearance of HuCD+ cells with the ependymo- and radioglial phenotype in SVZ, which are absent in intact animals. It was first shown that the local foci of posttraumatic neurogenesis, located in the reticular formation parenchyma, and the zones of posttraumatic gliosis, which contribute to a more efficient process of cell migration to the injury area, are formed as a result of tegmentum damage. The data obtained provide new information on the constitutive biology of neural stem cells and their involvement in brain regeneration.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.

Similar content being viewed by others

REFERENCES

  1. Adolf, B., Chapouton, P., Lam, C.S., Topp, S., Tannhäuser, B., Strahle, U., Götz, M., and Bally-Cuif, L., Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon, Dev. Biol., 2006, vol. 295, pp. 278–293.

    Article  CAS  PubMed  Google Scholar 

  2. Ahmed, S., Gan, H.T., Lam, C.S., Poonepalli, A., Ramasamy, S., Tay, Y., Tham, M., and Yu, Y.H., Transcription factors and neural stem cell self-renewal, growth and differentiation, Cell Adh. Migr., 2009, vol. 3, pp. 412–424.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Alunni, A., Vaccari, S., Torcia, S., Meomartini, M.E., Nicotra, A., and Alfei, L., Characterization of glial fibrillary acidic protein and astroglial architecture in the brain of a continuously growing fish, the rainbow trout, Eur. J. Histochem., 2005, vol. 49, pp. 157–166.

    CAS  PubMed  Google Scholar 

  4. Alunni, A., Hermel, J.M., Heuzé, A., Bourrat, F., Jamen, F., and Joly, J.S., Evidence for neural stem cells in the medaka optic tectum proliferation zones, Dev. Neurobiol., 2010, vol. 70, pp. 693–713.

    Article  CAS  PubMed  Google Scholar 

  5. Alvarez-Buylla, A., García-Verdugo, J.M., and Tramontin, A.D., A unified hypothesis on the lineage of neural stem cells, Nat. Rev. Neurosci., 2001, vol. 2, pp. 287–293.

    Article  CAS  PubMed  Google Scholar 

  6. Bayer, S.A., Yackel, J.W., and Puri, P.S., Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life, Science, 1982, vol. 216, pp. 890–892.

    Article  CAS  PubMed  Google Scholar 

  7. Beckervorders, R., Deshpande, A., Schaffner, I., Huttner, H.B., Lepier, A., Lie, D.C., and Götz, M., In vivo targeting of adult neural stem cells in the dentate gyrus by a split-cre approach, Stem Cell Rep., 2014, vol. 2, no. 2, pp. 153–162.

    Article  CAS  Google Scholar 

  8. Bodega, G., Suarez, I., Rubio, M., Villalba, R.M., and Fernandez, B., Astroglial pattern in the spinal cord of the adult barbel (Barbus comiza), Anat. Embryol., 1993, vol. 187, pp. 385–395.

    Article  CAS  Google Scholar 

  9. Bravo, R. and Macdonald-Bravo, H., Existence of two populations of cyclin/proliferating cell nuclear antigen during the cell cycle: association with DNA replication sites, J. Cell Biol., 1987, vol. 105, pp. 1549–1554.

    Article  CAS  PubMed  Google Scholar 

  10. Butler, A.B. and Hodos, W., Comparative Vertebrate Neuroanatomy: Evolution and Adaptation, John Wiley and Sons, Inc., 2005. 2nd ed.

    Book  Google Scholar 

  11. Candal, E., Anadon, R., DeGrip, W.J., and Rodriguez-Moldes, I., Patterns of cell proliferation and cell death in the developing retina and optic tectum of the brown trout, Dev. Brain Res., 2005, vol. 154, pp. 101–119.

    Article  CAS  Google Scholar 

  12. Chapouton, P., Skupien, P., Hesl, B., Coolen, M., Moore, J.C., Madelaine, R., Kremmer, E., Faus-Kessler, T., Blader, P., Lawson, N.D., and Bally-Cuif, L., Notch activity levels control the balance between quiescence and recruitment of adult neural stem cells, J. Neurosci., 2010, vol. 30, pp. 7961–7974.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Christie, K.J. and Turnley, A.M., Regulation of endogenous neural stem/progenitor cells for neural repair—factors that promote neurogenesis and gliogenesis in the normal and damaged brain, Front. Cell. Neurosci., 2013, vol. 6, p. 70. https://doi.org/10.3389/fncel.2012.00070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Codega, P., Silva-Vargas, V., Paul, A., Maldonado-Soto, A.R., Deleo, A.M., Pastrana, E., and Doetsch, F., Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche, Neuron, 2014, vol. 82, pp. 545–559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Coskun, V., Wu, H., Blanchi, B., Tsao, S., Kim, K., Zhao, J., Biancotti, J.C., Hutnick, L., Krueger, R.C., Jr., Fan, G., de Vellis, J., and Sun, Y.E., CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain, Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, pp. 1026–1031.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Dirian, L., Galant, S., Coolen, M., Chen, W., Bedu, S., Houart, C., Bally-Cuif, L., and Foucher, I., Spatial regionalization and heterochrony in the formation of adult pallial neural stem cells, Dev. Cell, 2014, vol. 30, pp. 123–136.

    Article  CAS  PubMed  Google Scholar 

  17. Ekström, P., Johnsson, C.M., and Ohlin, L.M., Ventricular proliferation zones in the brain of an adult teleost fish and their relation to neuromeres and migration (secondary matrix) zones, J. Comp. Neurol., 2001, vol. 436, pp. 92–110.

    Article  PubMed  Google Scholar 

  18. Ferretti, P., Is there a relationship between adult neurogenesis and neuron generation following injury across evolution?, Eur. J. Neurosci., 2011, vol. 34, pp. 951–962.

    Article  PubMed  Google Scholar 

  19. Fishell, G. and Kriegstein, A.R., Neurons from radial glia: the consequences of asymmetric inheritance, Curr. Opin. Neurobiol., 2003, vol. 13, pp. 34–41.

    Article  CAS  PubMed  Google Scholar 

  20. Fröidö, E.M., Westerlund, J., and Isomaa, B., Culturing and characterization of astrocytes isolated from juvenile rainbow trout (Oncorhynchus mykiss), Comp. Biochem. Physiol., 2002, vol. 133, pp. 17–28.

    Article  Google Scholar 

  21. Ganz, J., Kaslin, J., Hochmann, S., Freudenreich, D., and Brand, M., Heterogeneity and Fgf dependence of adult neural progenitors in the zebrafish telencephalon, Glia, 2010, vol. 58, pp. 1345–1363.

    Article  PubMed  Google Scholar 

  22. Giachino, C., Basak, O., Lugert, S., Knuckles, P., Obernier, K., Fiorelli, R., Frank, S., Raineteau, O., Alvarez-Buylla, A., and Taylor, V., Molecular diversity subdivides the adult forebrain neural stem cell population, Stem Cells, 2014, vol. 32, pp. 70–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Götz, M. and Huttner, W.B., The cell biology of neurogenesis, Nat. Rev. Mol. Cell Biol., 2005, vol. 6, pp. 777–788.

    Article  CAS  PubMed  Google Scholar 

  24. Grandel, H., Kaslin, J., Ganz, J., Wenzel, I., and Brand, M., Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate, Dev. Biol., 2006, vol. 295, pp. 263–277.

    Article  CAS  PubMed  Google Scholar 

  25. Grandel, H. and Brand, M., Comparative aspects of adult neural stem cell activity in vertebrates, Dev. Genes Evol., 2013, vol. 223, pp. 131–147.

    Article  PubMed  Google Scholar 

  26. Ito, Y., Tanaka, H., Okamoto, H., and Ohshima, T., Characterization of neural stem cells and their progeny in the adult zebrafish optic tectum, Dev. Biol., 2010, vol. 342, pp. 26–38.

    Article  CAS  PubMed  Google Scholar 

  27. Kálmán, M., Astroglial architecture of the carp (Cyprinus carpio) brain as revealed by immunohistochemical staining against glial fibrillary acidic protein (GFAP), Anat. Embryol. (Berl.), 1998, vol. 198, pp. 409–433.

    Article  Google Scholar 

  28. Kálmán, M. and Gould, R.M., GFAP-immunopositive structures in spiny dogfish, Squalus acanthias, and little skate, Raia erinacea, brains: differences have evolutionary implications, Anat. Embryol. (Berl.), 2001, vol. 204, pp. 59–80.

    Article  Google Scholar 

  29. Kaslin, J., Ganz, J., Geffarth, M., Grandel, H., Hans, S., and Brand, M., Stem cells in the adult zebrafish cerebellum: initiation and maintenance of a novel stem cell niche, J. Neurosci., 2009, vol. 29, pp. 6142–6153.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kawai, H., Arata, N., and Nakayasu, H., Three-dimensional distribution of astrocytes in zebrafish spinal cord, Glia, 2001, vol. 36, pp. 406–413.

    Article  CAS  PubMed  Google Scholar 

  31. Kishimoto, N., Shimizu, K., and Sawamoto, K., Neuronal regeneration in a zebrafish model of adult brain injury, Dis. Models Mech., 2012, vol. 5, pp. 200–209.

    Article  CAS  Google Scholar 

  32. Kriegstein, A. and Alvarez-Buylla, A., The glial nature of embryonic and adult neural stem cells, Annu. Rev. Neurosci., 2009, vol. 32, pp. 149–184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lam, S.H., Mathavan, S., and Gong, Z., Zebrafish spotted-microarray for genome-wide expression profiling experiments. Part I: array printing and hybridization, Methods Mol. Biol., 2009, vol. 546, pp. 175–195.

    Article  CAS  PubMed  Google Scholar 

  34. Luo, Y., Coskun, V., Liang, A., Yu, J., Cheng, L., Ge, W., Shi, Z., Zhang, K., Li, C., Cui, Y., Lin, H., Luo, D., Wang, J., Lin, C., Dai, Z., Zhu, H., Zhang, J., Liu, J., Liu, H., Horvath, S., Sun, Y.E., and Li, S., Single-cell transcriptome analyses reveal signals to activate dormant neural stem cells, Cell, 2015, vol. 161, pp. 1175–1186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Margotta, V., Morelli, A., Gelosi, E., and Alfei, L., PCNA positivity in the mesencephalic matrix areas in the adult of a teleost Carassius carassius L., Ital. J. Anat. Embryol., 2002, vol. 107, pp. 185–198.

    PubMed  Google Scholar 

  36. März, M., Chapouton, P., Diotel, N., Vaillant, C., Hesl, B., Takamiya, M., Lam, C.S., Kah, O., Bally-Cuif, L., and Strähle, U., Heterogeneity in progenitor cell subtypes in the ventricular zone of the zebrafish adult telencephalon, Glia, 2010, vol. 58, pp. 870–888.

    PubMed  Google Scholar 

  37. Merkle, F.T., Tramontin, A.D., García-Verdugo, J.M., and Alvarez-Buylla, A., Radial glia give rise to adult neural stem cells in the subventricular zone, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, pp. 17528–17532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Merkle, F.T., Mirzadeh, Z., and Alvarez-Buylla, A., Mosaic organization of neural stem cells in the adult brain, Science, 2007, vol. 317, pp. 381–384.

    Article  CAS  PubMed  Google Scholar 

  39. Merkulov, G.A., Kurs patologogistologicheskoi tekhniki (A Course in Pathohistological Techniques), Leningrad: Meditsina, 1969.

  40. Mueller, T. and Wullimann, M.F., BrdU-, neuroD (nrd)- and Hu-studies reveal unusual non-ventricular neurogenesis in the postembryonic zebrafish forebrain, Mech. Dev., 2002, vol. 117, pp. 123–135.

    Article  CAS  PubMed  Google Scholar 

  41. Mueller, T. and Wullimann, M.F., Anatomy of neurogenesis in the early zebrafish brain, Dev. Brain Res., 2003, vol. 140, pp. 137–155.

    Article  CAS  Google Scholar 

  42. Nakamura, H., Midbrain Patterning. Isthmus organizer, tectum regionalization, and polarity formation, in Patterning and Cell Type Specification in the Developing CNS and PNS, Rubenstein, J. and Rakic, P., Eds., San Diego: Academic Press, 2013, pp. 45–60.

    Google Scholar 

  43. Noctor, S.C., Martinez-Cerdeño, V., Ivic, L., and Kriegstein, A.R., Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases, Nat. Neurosci., 2004, vol. 7, pp. 136–144.

    Article  CAS  PubMed  Google Scholar 

  44. Olivera-Pasilio, V., Peterson, D.A., and Castelló, M.E., Spatial distribution and cellular composition of adult brain proliferative zones in the teleost, Gymnotus omarorum, Front. Neuroanat., 2014, vol. 8, p. 83. https://doi.org/10.3389/fnana.2014.00088

    Article  Google Scholar 

  45. Onteniente, B., Kimura, H., and Maeda, T., Comparative study of the glial fibrillary acidic protein in vertebrates by PAP immunohistochemistry, J. Comp. Neurol., 1983, vol. 141, pp. 283–312.

    Google Scholar 

  46. Parish, C.L., Beljajeva, A., Arenas, E., and Simon, A., Midbrain dopaminergic neurogenesis and behavioural recovery in a salamander lesion-induced regeneration model, Development, 2007, vol. 134, pp. 2881–2887.

    Article  CAS  PubMed  Google Scholar 

  47. Pellegrini, E., Mouriec, K., Anglade, I., Menuet, A., Le Page, Y., Gueguen, M.M., Marmignon, M.H., Brion, F., Pakdel, F., and Kah, O., Identification of aromatase-positive radial glial cells as progenitor cells in the ventricular layer of the forebrain in zebrafish, J. Comp. Neurol., 2007, vol. 501, pp. 150–167.

    Article  CAS  PubMed  Google Scholar 

  48. Pushchina, E.V., Fleishman, M.Yu., and Timoshin, S.S., Proliferative zones in the brain of the Amur sturgeon fry. Interactions with neuromeres and migration of secondary matrix zones, Russ. J. Dev. Biol., 2007, vol. 38, no. 5, pp. 286–293.

    Article  Google Scholar 

  49. 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., 2016, vol. 47, no. 1, pp. 11–32.

    Article  Google Scholar 

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

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

    Article  Google Scholar 

  52. Rapacioli, M., Duarte, S., Rodríguez Celín, A., Fiore, L., Teruel, L., Scicolone, G., Sánchez, V., and Flores, V., Optic tectum morphogenesis: a step-by-step model based on the temporal-spatial organization of the cell proliferation. Significance of deterministic and stochastic components subsumed in the spatial organization, Dev. Dyn., 2012, vol. 241, pp. 1043–1061.

    Article  PubMed  Google Scholar 

  53. Rink, E. and Wullimann, M.F., The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum), Brain Res., 2001, vol. 889, pp. 316–330.

    Article  CAS  PubMed  Google Scholar 

  54. Rothenaigner, I., Krecsmarik, M., Hayes, J.A., Bahn, B., Lepier, A., Fortin, G., Götz, M., Jagasia, R., and Bally-Cuif, L., Clonal analysis by distinct viral vectors identifies bona fide neural stem cells in the adult zebrafish telencephalon and characterizes their division properties and fate, Development, 2011, vol. 138, pp. 1459–1469.

    Article  CAS  PubMed  Google Scholar 

  55. Rubio, M., Suarez, I., Bodega, G., and Fernandez, B., Glial fibrillary acidic protein and vimentin immunohistochemistry in the posterior rhombencephalon of the Iberian barb (Barbus comiza), Neurosci. Lett., 1992, vol. 134, pp. 203–206.

    Article  CAS  PubMed  Google Scholar 

  56. Stukaneva, M.E., Pushchina, E.V., and Varaksin, A.A., GFAP and PCNA marking in the cerebellum of masu salmon’s (Oncorhynchus masou) juvenile after mechanical injury, Russ. J. Dev. Biol., 2017, vol. 48, no. 5, pp. 321–329.

    Article  CAS  Google Scholar 

  57. Suh, H., Consiglio, A., Ray, J., Sawai, T., D’Amour, K.A., and Gage, F.H., In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus, Cell Stem Cell, 2007, vol. 1, pp. 515–528.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Teles, M.C., Sîrbulescu, R.F., Wellbrock, U.M., Oliveira, R.F., and Zupanc, G.K., Adult neurogenesis in the brain of the Mozambique tilapia, Oreochromis mossambicus, J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol., 2012, vol. 198, pp. 427–449.

    Article  CAS  PubMed  Google Scholar 

  59. Than-Trong, E. and Bally-Cuif, L., Radial glia and neural progenitors in the adult zebrafish central nervous system, Glia, 2015, vol. 63, pp. 1406–1428.

    Article  PubMed  Google Scholar 

  60. Wasowicz, M., Ward, R., and Reperant, J., An investigation of astroglial morphology in torpedo and scyliorhinus, J. Neurocytol., 1999, vol. 28, pp. 639–653.

    Article  CAS  PubMed  Google Scholar 

  61. Wullimann, M.F. and Puelles, L., Postembryonic neural proliferation in the zebrafish forebrain and its relationship to prosomeric domains, Anat. Embryol. (Berl.), 1999, vol. 199, pp. 329–348.

    Article  CAS  Google Scholar 

  62. Wullimann, M.F. and Mueller, T., Teleostean and mammalian forebrains contrasted: evidence from genes to behavior, J. Comp. Neurol., 2004, vol. 475, pp. 143–162.

    Article  CAS  PubMed  Google Scholar 

  63. Xu, L., Tang, X., Wang, Y., Xu, H., and Fan, X., Radial glia, the keystone of the development of the hippocampal dentate gyrus, Mol. Neurobiol., 2015, vol. 51, pp. 131–141.

    Article  CAS  PubMed  Google Scholar 

  64. Zupanc, G.K., Neurogenesis, cell death and regeneration in the adult gymnotiform brain, J. Exp. Biol., 1999, vol. 202, pt. 10, pp. 1435–1446.

    CAS  PubMed  Google Scholar 

  65. Zupanc, G.K., Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish, Brain Behav. Evol., 2001, vol. 58, pp. 250–275.

    Article  CAS  PubMed  Google Scholar 

  66. Zupanc, G.K. and Sîrbulescu, R.F., Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish, Eur. J. Neurosci., 2011, vol. 34, pp. 917–929.

    Article  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

Authors

Corresponding author

Correspondence to E. V. Pushchina.

Additional information

Translated by E. Shvetsov

Abbreviations: BrdU, bromodeoxyuridine; GFAP, glial fibrillary acidic protein; GFAP+, GFAP-immunopositive; GFAP–, GFAP-immunonegative; HuCD, neuronal protein; HuCD+, HuCD-immunopositive; HuCD–, HuCD-immunonegative; PCNA, proliferating cell nuclear antigen; PCNA+, PCNA-immunopositive; PCNA–, PCNA-immunonegative; aNSC, neural stem cell of adult animal; DLT, dorsolateral tegmentum; DMT, dorsomedial tegmentum; DMTN, dorsomedial tegmentum nucleus; ODU, optical density units; CNN, constitutive neurogenic niches; FLL, fasciculus longitudinalis lateralis; MRF, mesencephalic reticular formation; NSC, neural stem cell; OD, optical density; TS, torus semicircularis; PVZ, periventricular zone; RG, radial glia; RNN, reactive neurogenic niches; RF, reticular formation; SVZ, subventricular zone; NI, nucleus isthmi (isthmic nucleus).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pushchina, E.V., Kapustyanov, I.A. & Varaksin, A.A. Proliferation and Neuro- and Gliogenesis in Normal and Mechanically Damaged Mesencephalic Tegmentum in Juvenile Chum Salmon, Oncorhynchus keta. Russ J Dev Biol 50, 59–76 (2019). https://doi.org/10.1134/S106236041902005X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S106236041902005X

Keywords:

Navigation