Introduction
Connexins are a multigenic family of proteins that can be
distinguished on the basis of their molecular weight. Six
oligomerized connexins form a hemichannel (or connexon)
that can bind to another hemichannel present in the membrane
of an adjacent cell, resulting in a complete intercellular
channel. These channels, which accumulate at specific
membrane areas defined as gap junctions, allow cells to share
small molecules (<1 kDa) such as metabolites and ions. Such
an exchange of signals (or intercellular coupling) has been
implicated in various cellular mechanisms, including ionic
homeostasis, electrical synchronization, proliferation and
migration (Bruzzone et al., 1996; Kumar and Gilula, 1996).
Connexins are expressed in the three main cell types of
the central nervous system (CNS), that is, astrocytes,
oligodendrocytes and neurons. Increasing evidence suggests
that connexins regulate different aspects of neuronal networks
and neuron-glia interactions, in both the developing and
mature brain (for a review, see Dermietzel and Spray, 1998).
This would require the establishment of communication
compartments that isolate groups of coupled cells engaged in
a coordinated activity from other populations that participate
in distinct processes. Such a dynamic regulation of cell-cell
communication seems particularly well suited to respond to the
instructive cues operating during CNS development (Kandler
and Katz, 1995; Nadarajah et al., 1997; Naus and Bani-
Yaghoub, 1998). Thus, in vivo studies have shown that, in the
developing neocortex, neuroblasts and proliferating cells
located in the ventricular zone are coupled, whereas
differentiating or migrating neurons are not (LoTurco and
Kriegstein, 1991; Bittman et al., 1997). Evidence for coupling
territories has also been obtained in other areas of
neurogenesis, such as the subventricular zone and rostral
migratory stream (Miragall et al., 1997; Menezes et al., 2000).
Furthermore, there is an inverse correlation between the
expression of connexin43 (Cx43) and Cx26, and cell
proliferation (Miragall et al., 1997; Bittman and LoTurco,
1999), suggesting that coupling and cell cycle of neural
progenitors may be interdependent.
Studies in vitro have shown that Cx43 expression and
coupling are downregulated as differentiation proceeds in
either immortalized rodent neuroblasts (Rozental et al., 1998)
or cell lines derived from rat peripheral neurotumoral cells
(Donahue at al., 1998). In a human teratocarcinoma cell line
consisting of precursors able to differentiate into post-mitotic
neurons, Cx43 protein expression is decreased after neuronal
3241
Embryonic neural progenitors isolated from the mouse
striatal germinal zone grow in vitro as floating cell
aggregates called neurospheres, which, upon adhesion, can
be induced to differentiate into the three main cell types of
the central nervous system (CNS), that is, astrocytes,
neurons and oligodendrocytes. To study the possible role
of connexins and junctional communication during
differentiation of neural progenitors, we assessed cell-to-
cell communication by microinjecting Lucifer Yellow into
neurospheres at various times after adhesion. Cells located
in neurospheres were strongly coupled, regardless of the
differentiation time. Microinjections performed on the cell
layers formed by differentiated cells migrating out of the
neurosphere established that only astrocytes were coupled.
These observations suggest the existence of at least
three distinct communication compartments: coupled
proliferating cells located in the sphere, uncoupled cells
undergoing neuronal or oligodendrocytic differentiation
and coupled differentiating astrocytes. A blockade of
junctional communication by 18-β-glycyrrhetinic acid
(βGA) reduced, in a concentration-dependent manner, the
viability of undifferentiated neural progenitor cells. This
effect appeared to be specific, inasmuch as it was reversible
and that cell survival was not affected in the presence of
the inactive analog glycyrrhyzic acid. Addition of βGA to
adherent neurospheres also decreased cell density and
altered the morphology of differentiated cells. Cx43
was strongly expressed in either undifferentiated or
differentiated neurospheres, where it was found both
within the sphere and in astrocytes, the two cell populations
that were dye coupled. Western blot analysis further
showed that Cx43 phosphorylation was strongly increased
in adherent neurospheres, suggesting a post-translational
regulation during differentiation. These results point to a
major role of cell-to-cell communication and Cx43 during
the differentiation of neural progenitor cells in vitro.
Key words: Astrocyte, CNS, Connexin, Gap junction, Neuron,
Oligodendrocyte
Summary
Cell coupling and Cx43 expression in embryonic
mouse neural progenitor cells
Nathalie Duval
1
, Danielle Gomès
1
, Viviane Calaora
1
, Alessandra Calabrese
2
, Paolo Meda
2
and
Roberto Bruzzone
1,
*
1
Institut Pasteur, Unité de Neurovirologie et Régénération du Système Nerveux, 75015 Paris, France
2
Département de Morphologie, Centre Médical Universitaire, 1211 Geneva, Switzerland
*Author for correspondence (e-mail: bruzzone@pasteur.fr)
Accepted 11 June 2002
Journal of Cell Science 115, 3241-3251 (2002) © The Company of Biologists Ltd
Research Article