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Structural Organization of Astrocytes in the Subgranular Zone of the Rabbit Hippocampal Dentate Fascia

  • Morphological Basics for Evolution of Functions
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Abstract

Neurogenesis in the subgranular zone (SGZ) of the mammalian hippocampus is well known to occur throughout the life span. Astrocytes in this specialized proliferative zone are supposed to have properties of progenitor cells. Structural features of these cells and their interspecies differences remain understudied, while data on the structural organization of the SGZ in the rabbit (order Lagomorpha, superorder Glires), which is widely used in medical and biological studies, are lacking at all. The present work was focused on the structural and cytochemical organization of astrocytes in the SGZ of the rabbit hippocampal dentate fascia as studied by laser confocal microscopy. The study was carried out on the brain of adult Chinchilla rabbits compared to that of adult Wistar rats. Two morphological astrocyte types were identified in the rabbit SGZ: radial gliocyte-like (type I) and atypical fibrous astrocyte-like (type II) cells. By contrast, the rat SGZ exhibited a predominance of type II astrocytes which lacked long unramified processes penetrating through the granular layer and reaching the molecular layer. SGZ astrocytes, both in the rabbit and rat, were characterized by intense immunoreactivity for glutamine synthetase, most pronounced in the processes that formed the perivascular glia limitans. Importantly, the peculiarities of the astrocyte organization in the dentate fascia of the rabbit hippocampus allowed SGZ delimitation, whereas astrocytes in the rat SGZ exhibited no local morphological distinctions. The latter finding indicates a more complex organization of the neurogenic zone in the hippocampus of lagomorphs in contrast to the same zone in rodents.

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References

  1. McEwen, B.S., Plasticity of the hippocampus: adaptation to chronic stress and allostatic load, Ann. N.Y. Acad. Sci., 2001, vol. 933, pp. 265–277.

    Article  CAS  PubMed  Google Scholar 

  2. Clark, R.E., Broadbent, N.J., and Larry, R., Squire hippocampus and remote spatial memory in rats, Hippocampus, 2005, vol. 15, no. 2, pp. 260–272.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bartsch, T., Döhring, J., Rohr, A., Jansen, O., and Deuschl, G., CA1 neurons in the human hippocampus are critical for autobiographical memory, mental time travel, and autonoetic consciousness, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, no. 42, pp. 17562–17567.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Encinas, J.M., Sierra, A., Valcárcel-Martín, R., and Martín-Suárez, S., A developmental perspective on adult hippocampal neurogenesis, Int. J. Dev. Neurosci., 2013, vol. 31, no. 7, pp. 640–645.

    Article  PubMed  Google Scholar 

  5. Aleksandrova, M.A. and Marey, M.V., Stem cells in the brain of mammals and humans: fundamental and applied aspects, Zh. Vyssh. Nervn. Deyat. im. I.P. Pavlova, 2015, vol. 65, no. 3, pp. 1–35.

    Google Scholar 

  6. Gage, F.H., Neurogenesis in the adult brain, J. Neurosci., 2002, vol. 22, vol. 3, pp. 612–613.

    Article  Google Scholar 

  7. Steinler, D.A. and Laywell, E.D., Astrocytes as stem cells: nomenclature, phenotype, and translation, Glia, 2003, vol. 43, no. 1, pp. 62–69.

    Article  Google Scholar 

  8. 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 

  9. Chavushyan, V.A., Meliksetyan, I.B., Sarkisyan, D.S., Stepanyan, A.Yu., Avetisyan, Z.A., Simonyan, K.V., Danielyan, M.A., and Kamenetskyi, V.S., An electrophysiological and morpho- histochemical study of the effect of adrenalectomy on hippocampal neurons, Zh. Evol. Biokhim. Fiziol., 2013, vol. 49, no. 2, pp. 153–161.

    Google Scholar 

  10. Korzhevskii, D.E., Sukhorukova, E.G., Kirik, O.V., and Alekseeva, O.S., Astrocytes in the subventricular zone of the telencephalon, Morfol., 2011, vol. 139, no. 3, pp. 77–79.

    CAS  Google Scholar 

  11. Khozhai, L.I. and Otellin, V.A., Distribution of GAD67-expressing neurons and morphological changes in hippocampal structures during pubertal period after acute perinatal hypoxia in rats, J. Evol. Biochem. Physiol., 2017, vol. 53, no. 6, pp. 448–452.

    Google Scholar 

  12. Oikonomidis, N., Kavantzas, N., Korou, L.M., Konstantopoulos, P., Pergialiotis, V., Misiakos, E., Rizos, I., Verikokos, C., and Perrea, D.N., Pretreatment with simvastatin prevents the induction of diet-induced atherosclerosis in a rabbit model, Biomed. Rep., 2016, vol. 5, no. 6, pp. 667–674.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Yershov, A.L., Jordan, B.S., Guymon, C.H., and Dubick, M.A., Relationship between the inoculum dose of Streptococcus pneumoniae and pneumonia onset in a rabbit model, Eur. Respir. J., 2005, vol. 25, no. 4, pp. 693–700.

    Article  CAS  PubMed  Google Scholar 

  14. Ionicheva, L.V., Smirnov, L.D., Kustikova, I.N., Mikulyak, N.I., and Zinovyev, A.I., Antioxidant correction of postradiation distubances of hemopoiesis and cell composition in rabbits in experiment, Vestn. Nov. Med. Tekhnol., 2008, vol. 15, no. 1, pp. 8–11.

    Google Scholar 

  15. Korzhevskii, D.E., Sukhorukova, E.G., Kirik, O.V., and Grigorev, I.P., Immunohistochemical demonstration of specific antigens in the human brain fixed in zinc-ethanol-formaldehyde, Europ. J. Histochem., 2015, vol. 59, no. 3, p. 2530.

    Article  CAS  Google Scholar 

  16. Sukhorukova, E.G., Korzhevskii, D.E., and Alekseseva, O.S., Gilal fibrillary acidic protein, the component of intermediate filaments in vertebrate brain astrocytes, J. Evol. Biochem. Physiol., 2015, vol. 51, no. 1, pp. 1–10.

    Article  CAS  Google Scholar 

  17. Doetsch, F., Caillé, I., Lim, D.A., García-Verdugo, J.M., and Alvarez-Buylla, A., Subventricular zone astrocytes are neural stem cells in the adult mammalian brain, Cell, 1999, vol. 97, no. 6, pp. 703–716.

    Article  CAS  PubMed  Google Scholar 

  18. Sukhorukova, E.G., Alekseeva, O.S., Kirik, O.V., Grudinina, N.A., Korzhevskii, D.E., Comparative aspects of structural organization of astrocytes of the first layer of the human and rat cerebral cortex, Zh. Evol. Biokhim. Fiziol., 2012, vol. 48, no. 3, pp. 280–286.

    CAS  PubMed  Google Scholar 

  19. Verkhratsky, A., Zorec, R., Rodriguez, J.J., and Parpura, V., Pathobiology of neurodegeneration: the role for astroglia, Opera Med. Physiol., 2016, no. 1, pp. 13–22.

    Google Scholar 

  20. Barry, D.S., Pakan, J.M., and McDermott, K.W., Radial glial cells: key organisers in CNS development, Int. J. Biochem. Cell Biol., 2014, vol. 46, pp. 76–79.

    Article  CAS  PubMed  Google Scholar 

  21. Yarygin, K.N., and Yarygin, V.N., Neurogenesis in the central nervous system and prospects of regenerative neurology, Zh. Nevrol. Psikhiatr. im. S.S. Korskaova, 2012, no. 1, pp. 1–13.

    Google Scholar 

  22. Cameron, H.A. and McKay, R.D., Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus, J. Comp. Neurol., 2001, vol. 435, no. 4, pp. 406–417.

    Article  CAS  PubMed  Google Scholar 

  23. Amador-Arjona, A., Elliott, J., Miller, A., Ginbey, A., Pazour, G.J., Enikolopov, G., Roberts, A.J., and Terskikh, A.V., Primary cilia regulate proliferation of amplifying progenitors in adult hippocampus: implications for learning and memory, J. Neurosci., 2011, vol. 31, no. 27, pp. 9933–9944.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Coulthard, L.G., Hawksworth, O.A., Li, R., Bala chandran, A., Lee, J.D., Sepehrband, F., Kurnia wan, N., Jeanes, A., Simmons, D.G., Wolvetang, E., and Woodruff, T.M., Complement C5aR1 signaling promotes polarization and proliferation of embryonic neural progenitor cells through PKCξ, J. Neurosci., 2017, vol. 37, no. 22, pp. 5395–5407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chen, J.J., Wang, T., An, C.D., Jiang, C.Y., Zhao, J., and Li, S., Brain-derived neurotrophic factor: a mediator of inflammation-associated neurogenesis in Alzheimer’s disease, Rev. Neurosci., 2016, vol. 27, no. 8, pp. 793–811.

    Article  PubMed  Google Scholar 

  26. Nakamichi, N., Takarada, T., and Yoneda, Y., Neurogenesis mediated by gamma-aminobutyric acid and glutamatesignaling, J. Pharmacol. Sci., 2009, vol. 110, no. 2, pp. 133–149.

    Article  CAS  PubMed  Google Scholar 

  27. Anlauf, E. and Derouiche, A., Glutamine synthetase as an astrocytic marker: its cell type and vesicle localization, Front. Endocrinol., 2013, vol. 4, pp. 1–5.

    Article  Google Scholar 

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Authors and Affiliations

  1. Institute of Experimental Medicine, St. Petersburg, Russia

    E. G. Sukhorukova, O. V. Kirik, D. A. Sufieva & D. E. Korzhevskii

  2. Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences, St. Petersburg, Russia

    O. S. Alekseeva

Authors
  1. E. G. Sukhorukova
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  2. O. V. Kirik
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  3. D. A. Sufieva
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  4. O. S. Alekseeva
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  5. D. E. Korzhevskii
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Correspondence to O. S. Alekseeva.

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Russian Text © The Author(s), 2019, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2019, Vol. 55, No. 2, pp. 138–144.

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Sukhorukova, E.G., Kirik, O.V., Sufieva, D.A. et al. Structural Organization of Astrocytes in the Subgranular Zone of the Rabbit Hippocampal Dentate Fascia. J Evol Biochem Phys 55, 148–154 (2019). https://doi.org/10.1134/S002209301902008X

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  • DOI: https://doi.org/10.1134/S002209301902008X

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