INTRODUCTION
Glia play diverse supportive roles in the adult nervous system,
including wrapping and insulating neurons, providing them
with nourishment, maintaining their ionic homeostasis, and
helping to establish and maintain the blood-brain and blood-
nerve barrier. During development, glia help control the
patterning of neuronal differentiation and, in particular, guide
axons to their targets (Klaes et al., 1994; Klämbt et al., 1996).
The specific role that glia play in the formation of axon
pathways appears to depend on the context. In Drosophila, the
glia along the midline of the central nervous system (CNS)
provide complex guidance cues for commissural axons
(Klämbt et al., 1991; Tear et al., 1993). Midline glia bear not
only attractive cues, such as the Netrins, which attract
commissural fibers to the midline, but also repulsive cues, such
as Slit, which prevent commissural fibers from recrossing the
midline (Seeger et al., 1993; Mitchell et al., 1996; Tear et al.,
1996; Kidd et al., 1999). However, the role of glia in the
formation of other axonal pathways is less clear. On the one
hand, studies of mutants such as glial cells missing (gcm),
pointed (pnt) and reversed polarity (repo) in Drosophila
suggest an ancillary role (Klaes et al., 1994; Halter et al., 1995;
Hosoya et al., 1995; Jones et al., 1995). The analysis of gcm
mutants, which lack all glia except for those in the midline,
demonstrates that most axon pathways in the embryo, and
specifically the longitudinal axon tracts, can develop without
glia, albeit with greater variability, and suggests a merely
facilitory role for glia in the formation of non-commissural
pathways (Hosoya et al., 1995; Jones et al., 1995). By contrast,
toxin-induced ablation of longitudinal glia early in
development leads to a complete loss of the longitudinal axon
tracts, suggesting that longitudinal glia are strictly required for
growth cone guidance in the formation of these axon tracts
(Hidalgo et al., 1995). Genetic and toxin ablation studies agree
that glia have an essential role in the maintenance of
established axon pathways.
In order for glial cells to fulfill their role in axon guidance
or even maintenance, they have to be positioned correctly with
respect to the neurons. For many glial cell populations, this
means migration over many cell diameters within a restricted
period of time during development. Examples of migrating
glial cells include the midline glia in the Drosophila CNS and
the oligodendrocytes of the optic nerve in vertebrates (Small
et al., 1987; Klämbt et al., 1991). The mechanisms involved in
glial migration are not well understood, and only a few cellular
and molecular components have so far been identified. In
vertebrates, the fibroblast growth factor (FGF) receptor as well
as several components involved in cell adhesion have been
implicated in oligodendrocyte motility (Milner et al., 1996;
Payne et al., 1996; Osterhout et al., 1997). Similarly, in
Drosophila, the FGF receptor Breathless (Btl) has been
implicated in the migration of a subset of midline glia in the
embryo, suggesting that activation of the Ras signaling
pathway is involved in the migration process (Klämbt et al.,
1992; Fried-Reichman et al., 1994).
In this study, we report on the migration and function of glial
cells in the developing adult eye of Drosophila. A previous
3285 Development 126, 3285-3292 (1999)
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DEV8599
Although glial cells have been implicated widely in the
formation of axon tracts in both insects and vertebrates,
their specific function appears to be context-dependent,
ranging from providing essential guidance cues to playing
a merely facilitory role. Here we examine the role of the
retinal basal glia (RBG) in photoreceptor axon guidance in
Drosophila. The RBG originate in the optic stalk and have
been thought to migrate into the eye disc along
photoreceptor axons, thus precluding any role in axon
guidance. Here we show the following. (1) The RBG can, in
fact, migrate into the eye disc even in the absence of
photoreceptor axons in the optic stalk; they also migrate to
ectopic patches of differentiating photoreceptors without
axons providing a continuous physical substratum. This
suggests that glial cells are attracted into the eye disc not
through haptotaxis along established axons, but through
another mechanism, possibly chemotaxis. (2) If no glial
cells are present in the eye disc, photoreceptor axons are
able to grow and direct their growth posteriorly as in wild
type, but are unable to enter the optic stalk. This indicates
that the RBG have a crucial role in axon guidance, but not
in axonal outgrowth per se. (3) A few glia close to the entry
of the optic stalk suffice to guide the axons into the stalk,
suggesting that glia instruct axons by local interaction.
Key words: Drosophila, Visual system development, Glia,
Migration, Axon guidance
SUMMARY
Migration and function of glia in the developing Drosophila eye
Radha Rangarajan, Qizhi Gong and Ulrike Gaul*
Laboratory of Developmental Neurogenetics, Rockefeller University, 1230 York Avenue, New York, NY 10021, USA
*Author for correspondence (e-mail: gaul@rockvax.rockefeller.edu)
Accepted 12 May; published on WWW 5 July 1999