INTRODUCTION
During embryonic development of the vertebrate nervous
system a variety of neurons, with characteristic morphol-
ogy, axonal projections and connectivity, arise at pre-
dictable times and locations. For many neuronal types a
wealth of information is available on the processes of
axonal pathfinding and synapse formation, but less is known
about the regulatory processes and molecules that are
involved in the generation of different neurons. To under-
stand the molecular mechanisms participating in the gener-
ation of specific neuronal cell types we need to identify reg-
ulatory proteins that are expressed at the initial stages of
differentiation in these various neurons.
One such class of proteins are the homeodomain proteins
and a number of homeobox genes are expressed during the
formation of the vertebrate central nervous system (CNS;
Kessel and Gruss, 1990). The Hox genes are expressed at
high levels in the mouse spinal cord and hindbrain and the
temporal and spatial patterns of expression of these genes
are consistent with a role in the definition of spatial domains
in the CNS (Kessel and Gruss, 1991; Hunt et al., 1991). In
contrast to the broad expression patterns of the Hox genes,
a few homeobox genes show a much more restricted pat-
tern of expression in the adult brain including the mid- and
forebrain. These include members of the Dlx (Price et al.,
1991), Pax (Krauss et al., 1991), Nkx (Price et al., 1992),
Otx (Simeone et al., 1992a), and Emx families of genes
(Simeone et al., 1992b).
Islet-1 (Isl-1) is one of the three original members of the
LIM homeodomain protein family (Way and Chalfie, 1988;
Freyd et al., 1990; Karlsson et al., 1990). This family of
proteins has now expanded and includes an increasing
number of new members from many different species
(Bourgouin et al., 1992, Cohen et al., 1992, Taira et al.,
1992, Xu et al., 1993). A variety of proteins containing one
or two LIM motifs but which lack a homeodomain have
also been described (Greenberg et al., 1990). Isl-1 was orig-
inally isolated as a protein that could bind to the insulin
gene enhancer. We have previously analyzed the pattern of
expression of Isl-1 in the adult rat using anti-Isl-1 antiserum
(Thor et al., 1991). Isl-1 was found to be expressed in a
subset of endocrine cells and neurons. In the central ner-
vous system (CNS), Isl-1 expression is restricted to the parts
of the brain involved in autonomic and endocrine control.
Isl-1 is not expressed in regions involved in processing of
sensory information and neocortical areas. Thus, Isl-1
appears to be selectively expressed in the phylogenetically
old parts of the brain.
In the chicken spinal cord Isl-1 has been identified as the
earliest known marker of developing motor neurons and the
onset of Isl-1 expression in the motor neurons can be
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Development 118, 417-425 (1993)
Printed in Great Britain © The Company of Biologists Limited 1993
Isl-1 has previously been established as the earliest
marker of developing chicken spinal motor neurons
where it is regulated by inductive signals from the floor-
plate and notochord. We now report that, in zebrafish,
the expression of Isl-1 is initiated in Rohon-Beard cells,
primary motor neurons, interneurons and cranial gan-
glia, hours before the neural tube itself is formed. The
expression is initiated simultaneously in the Rohon-
Beard cells and the primary motor neurons, at the axial
level of the presumptive first somite. The Isl-1-express-
ing motor neurons appear on either side of the ventral
midline whereas the interneurons and Rohon-Beard
cells initiate expression while located at the edge of the
germinal shield. Isl-1 expression is initiated in these cells
before the formation of a differentiated notochord.
Isl-1 is expressed in the various functional classes of
primary neurons at 24 hours postfertilization. This
selective expression of a homeodomain protein in the
primary neurons implies that these neurons share a
common program of early development and that they
have evolved and been selected for as a coordinated
system. One of the functions of the primary neurons is
to send long axons which pioneer the major axon tracts
in the zebrafish embryo. An evolutionary conserved
functional role for Isl-1 in the expression of the pio-
neering phenotype of the primary neurons is suggested.
Key words: LIM homeodomain, Islet-1, zebrafish, pioneering
neurons, primary neurons
SUMMARY
Zebrafish primary neurons initiate expression of the LIM homeodomain
protein Isl-1 at the end of gastrulation
V. Korzh, T. Edlund* and S. Thor
Department of Microbiology, University of Umeå, S-90187 Umeå, Sweden
*Author for correspondence