Panglial gap junctions between astrocytes and olfactory ensheathing cells mediate transmission of Ca2+ transients and neurovascular coupling

Glia. 2019 Jul;67(7):1385-1400. doi: 10.1002/glia.23613. Epub 2019 Mar 18.

Abstract

Astrocytes are arranged in highly organized gap junction-coupled networks, communicating via the propagation of Ca2+ waves. Astrocytes are gap junction-coupled not only to neighboring astrocytes, but also to oligodendrocytes, forming so-called panglial syncytia. It is not known, however, whether glial cells in panglial syncytia transmit information using Ca2+ signaling. We used confocal Ca2+ imaging to study intercellular communication between astrocytes and olfactory ensheathing glial cells (OECs) in in-toto preparations of the mouse olfactory bulb. Our results demonstrate that Ca2+ transients in juxtaglomerular astrocytes, evoked by local photolysis of "caged" ATP and "caged" tACPD, led to subsequent Ca2+ responses in OECs. This transmission of Ca2+ responses from astrocytes to OECs persisted in the presence of neuronal inhibition, but was absent when gap junctional coupling was suppressed with carbenoxolone. When Ca2+ transients were directly evoked in OECs by puff application of DHPG, they resulted in delayed Ca2+ responses in juxtaglomerular astrocytes, indicating that panglial transmission of Ca2+ signals occurred in a bidirectional manner. In addition, panglial transmission of Ca2+ signals from astrocytes to OECs resulted in vasoconstriction of OEC-associated blood vessels in the olfactory nerve layer. Our results demonstrate functional transmission of Ca2+ signals between different classes of glial cells within gap junction-coupled panglial networks and the resulting regulation of blood vessel diameter in the olfactory bulb.

Keywords: astrocyte; calcium signaling; gap junction; neurovascular coupling; olfactory ensheathing cell; panglial network; syncytium.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Animals, Newborn
  • Astrocytes / physiology*
  • Calcium Signaling / physiology*
  • Cell Communication / physiology
  • Gap Junctions / physiology*
  • Mice
  • Mice, Transgenic
  • Neuroglia / physiology*
  • Neurovascular Coupling / physiology*
  • Olfactory Bulb / cytology
  • Olfactory Bulb / physiology
  • Olfactory Mucosa / physiology*
  • Organ Culture Techniques