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Cell and Tissue Biology

, Volume 12, Issue 6, pp 477–483 | Cite as

Gap Junctions in the Composition of Neurogliovascular Ensembles in Rat Cortical Barrel Columns

  • E. Yu. KirichenkoEmail author
  • P. E. Povilaytite
  • A. K. Logvinov
  • Yu. G. Kirichenko
  • S. Yu. Filippova
Article
  • 11 Downloads

Abstract

Complex morphological study of gap junctions (GJs) in the blood–brain barrier in the rat cortical barrel columns using light and transmission electron microscopy and immunohistochemistry showed that astrocytes united by GJs in a single network can act as the main mediator between neurons and the vascular bed, forming a complex of neurogliovascular ensembles. The possibility of using such complexes to determine the functional organization of cortical columns is discussed.

Keywords:

barrel cortex gap junction astrocyte blood–brain barrier 

Notes

ACKNOWLEDGMENTS

This work was carried out with support from the program of governmental assignment of the Ministry of Education and Science of the Russian Federation no. 6.6047.2017/8.9 (basic part).

COMPLIANCE WITH ETHICAL STANDARDS

Сonflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. The accommodation of animals and experimental studies were carried out in accordance with the protocol approved by the Bioethics Commission of Southern Federal University in April 18, 2012.

REFERENCES

  1. 1.
    Ambrosi, C., Ren, C., Spagnol, G., Cavin, G., Cone, A., Grintsevich, E.E., Sosinsky, G.E., and Sorgen, P.L., Connexin 43 forms supramolecular complexes through non-overlapping binding sites for drebrin, tubulin, and ZO-1, PLoS One, 2016, vol. 11. e0157073.CrossRefGoogle Scholar
  2. 2.
    Bernardinelli, Y., Magistretti, P.J., and Chatton, J.Y., Astrocytes generate Na+-mediated metabolic waves, Proc. Natl. Acad. Sci. U. S. A., 2004, vol. 101, pp. 14937–14942.CrossRefGoogle Scholar
  3. 3.
    Blinder, P., Tsai, P.S., Kaufhold, J.P., Knutsen, P.M., Suhl, H., and Kleinfeld, D., The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow, Nat. Neurosci., 2013, vol. 16, pp. 889–897.CrossRefGoogle Scholar
  4. 4.
    Bozzola, J.J. and Russel, L.D., Electron Microscopy: Principles and Techniques for Biologists, Boston: Jones and Bastlett Publishers, 1992.Google Scholar
  5. 5.
    Chernorizov, A.M., Glia: morphology, physiology and functions, in Fundamental’noe rukovodstvo. Neiron. Obrabotka signalov, plastichnost’, modelirovanie (Fundamental Handbook. Neuron: Signal Processing, Plasticity, and Modeling), Tumen: Kompaniya Mir Ltd., 2008, pp. 33–100.Google Scholar
  6. 6.
    De Felipe, J., The evolution of the brain, the human nature of cortical circuits, and intellectual creativity, Front. Neuroanat., 2011, vol. 5, p. 29.Google Scholar
  7. 7.
    Eilam, R., Aharoni, R., Arnon, R., and Malach, R., Astrocyte morphology is confined by cortical functional boundaries in mammals ranging from mice to human, Elife, 2016, vol. 5. e15915.CrossRefGoogle Scholar
  8. 8.
    Giaume, C., Koulakoff, A., Roux, L., Holcman, D., and Rouach, N., Astroglial networks: a step further in neuroglial and gliovascular interactions, Nat. Rev. Neurosci., 2010, vol. 11, pp. 87–99.CrossRefGoogle Scholar
  9. 9.
    Gordon, G.R., Choi, H.B., Rungta, R.L., Ellis-Davies, G.C., and MacVicar, B.A., Brain metabolism dictates the polarity of astrocyte control over arterioles, Nature, 2008, vol. 456, pp. 745–749.CrossRefGoogle Scholar
  10. 10.
    Halassa, M.M., Fellin, T., Takano, H., Dong, J.H., and Haydon, P.G., Synaptic islands defined by the territory of a single astrocyte, J. Neurosci., 2007, vol. 27, pp. 6473–6477.CrossRefGoogle Scholar
  11. 11.
    Kamasawa, N., Sik, A., Morita, M., Yasumura, T., Davidson, K.G.V., Nagy, J.I., and Rash, J.E., Connexin-47 and connexin-32 in gap junctions of oligodendrocyte somata, myelin sheaths, paranodal loops and Schmidt–Lanterman incisures: implications for ionic homeostasis and potassium siphoning, Neuroscience, 2005, vol. 136, pp. 65–86.CrossRefGoogle Scholar
  12. 12.
    Kettenmann, H. and Ransom, B.R., Neuroglia, Oxford: Oxford University Press, 2005.Google Scholar
  13. 13.
    Kirichenko, E.Y., Churyumova, G.A., and Logvinov, A.K., Ultrastructural study of glial gap junctions in the thalamic nuclei of rat, Biochemistry (Moscow) Suppl. Series A: Membrane Cell Biol., 2016, vol. 3, pp. 207–217.Google Scholar
  14. 14.
    Kogan, A.B., Elektrofiziologiya (Electrophysiology), Moscow: Vyschaya Shkola, 1969.Google Scholar
  15. 15.
    Kunze, A., Congreso, M.R., Hartmann, C., Wallraff-Beck, A., Hüttmann, K., Bedner, P., Requardt, R., Seifert, G., Redecker, C., Willecke, K., Hofmann, A., Pfeifer, A., Theis, M., and Steinhäuser, C., Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus, Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, pp. 11336–11341.CrossRefGoogle Scholar
  16. 16.
    Lutz, S.E., Zhao, Y., Gulinello, M., Lee, S.C., Raine, C.S., and Brosnan, C.F., Deletion of astrocyte connexins 43 and 30 leads to a dysmyelinating phenotype and hippocampal CA1 vacuolation, J. Neurosci., 2009, vol. 29, pp. 7743–7752.CrossRefGoogle Scholar
  17. 17.
    Mathiisen, T.M., Lehre, K.P., Danbolt, N.C., and Ottersen, O.P., The perivascular astroglial sheath provides a complete covering of the brain microvessels: an electron microscopic 3D reconstruction, Glia, 2010, vol. 58, pp. 1094–1103.CrossRefGoogle Scholar
  18. 18.
    Meshulam, L., Galron, R., Kanner, S., De, Pittà, M., Bonifazi, P., Goldin, M., Frenkel, D., Ben-Jacob, E., and Barzilai, A., The role of the neuro-astro-vascular unit in the etiology of ataxia telangiectasia, Front. Pharmacol., 2012, vol. 3, p. 157.CrossRefGoogle Scholar
  19. 19.
    Mountcastle, V.B., Perceptual Neuroscience. The Cerebral Cortex, Cambridge: Harvard University Press, 1998.Google Scholar
  20. 20.
    Mulligan, S.J. and MacVicar, B.A., Calcium transients in astrocyte endfeet cause cerebrovascular constrictions, Nature, 2004, vol. 431, pp. 195–199.CrossRefGoogle Scholar
  21. 21.
    Nagy, J.I., Ionescu, A.V., Lynn, B.D., and Rash, J.E., Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: implications from normal and connexin32 knockout mice, Glia, 2003, vol. 44, pp. 205–218.CrossRefGoogle Scholar
  22. 22.
    Nicholls, J.G., Martin, A.R., Fuchs, P.A., and Wallace, B.G., From Neuron to Brain, Sinauer Associates Inc., 1999.Google Scholar
  23. 23.
    Nuriya, M., Shinotsuka, T., and Yasui, M., Diffusion properties of molecules at the blood–brain interface: potential contributions of astrocyte endfeet to diffusion barrier functions, Cerebral Cortex, 2013, vol. 23, pp. 2118–2126.CrossRefGoogle Scholar
  24. 24.
    Odermatt, B., Wellershaus, K., Wallraff, A., Seifert, G., Degen, G., Euwens, C., Fuss, B., Bussow, H., Schilling, K., Stenhauser, C., and Willecke, K., Connexin 47 (Cx47)-deficient mice with enhanced green fluorescent protein reporter gene reveal predominant oligodendrocytic expression of Cx47 and display vacuolized myelin in the CNS, J. Neurosci., 2003, vol. 23, pp. 4549–4559.CrossRefGoogle Scholar
  25. 25.
    Orthmann-Murphy, J.L., Freidin, M., Fischer, E., Scherer, S.S., and Abrams, C.K., Two distinct heterotypic channels mediate gap junction coupling between astrocyte and oligodendrocyte connexins, J. Neurosci., 2007, vol. 27, pp. 13949–13957.CrossRefGoogle Scholar
  26. 26.
    Pannasch, U., Vargová, L., Reingruber, J., Ezan, P., Holcman, D., Giaume, C., Syková, E., and Rouach, N., Astroglial networks scale synaptic activity and plasticity, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, pp. 8467–8472.CrossRefGoogle Scholar
  27. 27.
    Paxinos, G. and Watson, C., The Rat Brain in Stereotaxic Coordinates, San Diego: Acad. Press, 1998.Google Scholar
  28. 28.
    Rouach, N., Koulakoff, A., Abudara, V., Willecke, K., and Giaume, C., Astroglial metabolic networks sustain hippocampal synaptic transmission, Science, 2008, vol. 322, pp. 1551–1555.CrossRefGoogle Scholar
  29. 29.
    Roux, L., Benchenane, K., Rothstein, J.D., Bonvento, G., and Giaume, C., Plasticity of astroglial networks in olfactory glomeruli, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, pp. 18 442–18 446.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • E. Yu. Kirichenko
    • 1
    Email author
  • P. E. Povilaytite
    • 2
  • A. K. Logvinov
    • 1
  • Yu. G. Kirichenko
    • 2
  • S. Yu. Filippova
    • 1
  1. 1.Laboratory of Functional Genomics and Morphology, Ivanovsky Academy of Biology and Biotechnology of the Southern Federal UniversityRostov-on-DonRussia
  2. 2.Department of Experimental Pathomorphology and Electron Microscopy of the Rostov Regional Pathologo-Anatomical BureauRostov-on-DonRussia

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