Advertisement

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

  • E. G. Sukhorukova
  • O. V. Kirik
  • D. A. Sufieva
  • O. S. AlekseevaEmail author
  • D. E. Korzhevskii
Morphological Basics for Evolution of Functions
  • 3 Downloads

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.

Keywords

hippocampus astrocytes neural stem cells rabbit 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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. 6.
    Gage, F.H., Neurogenesis in the adult brain, J. Neurosci., 2002, vol. 22, vol. 3, pp. 612–613.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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. 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.Google Scholar
  11. 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. 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.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.Google Scholar
  19. 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. 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.CrossRefGoogle Scholar
  21. 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. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  • E. G. Sukhorukova
    • 1
  • O. V. Kirik
    • 1
  • D. A. Sufieva
    • 1
  • O. S. Alekseeva
    • 2
    Email author
  • D. E. Korzhevskii
    • 1
  1. 1.Institute of Experimental MedicineSt. PetersburgRussia
  2. 2.Sechenov Institute of Evolutionary Physiology and BiochemistryRussian Academy of SciencesSt. PetersburgRussia

Personalised recommendations