INTRODUCTION
The trigeminal ganglion, which provides sensation for much of
the face, has served as a good experimental system for inves-
tigating the development of peripheral ganglia because of its
size and accessibility (reviewed in Davies, 1988). Trigeminal
sensory neurons originate from two distinct embryonic cell
populations: the neural crest and the ectodermal placodes
(Yntema, 1942; Hamburger, 1961; Noden, 1978; Narayanan
and Narayanan, 1980; Ayer-LeLièvre and Le Douarin, 1982;
D’Amico-Martel and Noden, 1980, 1983; reviewed by Noden,
1993). The cranial neural crest population exits from the dorsal
neural tube and migrates under the head ectoderm. In addition
to contributing neurons and glia to cranial ganglia, neural crest
cells form connective tissue and bones of the face and skull
(reviewed in Le Douarin, 1982). The cranial sensory placode
population undergoes an epithelial-mesenchymal transition
from a thickened ectodermal epithelium; these cells then
invaginate, migrate, condense and differentiate into neurons,
receptors and some support cells of the peripheral nervous
system (reviewed by Webb and Noden, 1993).
Unlike most placodes, the trigeminal placode is not mor-
phologically distinct from the surrounding ectoderm. As a con-
sequence, most information about its development comes from
observations of placode cells during their migration and gan-
gliogenesis. The trigeminal ganglion comprises two lobes: the
ophthalmic lobe and the maxillomandibular lobe. Both receive
contributions from ectodermal placodes and neural crest cells.
In amphibians, the two lobes remain separate or fuse secon-
darily during development, suggesting that they are embryo-
logically and evolutionarily distinct (Hamburger, 1961;
Northcutt and Brandle, 1995). Histological analyses in the
mouse and chick indicate that placode cells leave the ectoder-
mal layer by breaking through the basal lamina as individuals
or small clusters of cells (Hamburger, 1961; D’Amico-Martel
and Noden, 1983; Nichols, 1986; reviewed by Webb and
Noden, 1993). They then migrate to the distal regions of the
trigeminal ganglion. Trigeminal placode cells become
immunoreactive for neuronal markers and exit the cell cycle
early in their development (Moody et al., 1989; D’Amico-
Martel and Noden, 1980). In contrast, the neural crest
component of the trigeminal ganglion only expresses neuronal
markers after condensation. If placode cells fail to invaginate,
they can form ectopic ganglia in the surface ectoderm
(Kuratani and Hirano, 1990), suggesting that migration and
interaction with neural crest cells are not necessary for their
neuronal differentiation.
Molecular markers of undifferentiated placodal epithelia
have not previously been described (Webb and Noden, 1993),
making it difficult to characterize the induction and cell speci-
fication of this cranial placode. In this study, we have used the
transcription factor Pax-3 and the FGF receptor FREK as
4287 Development 124, 4287-4295 (1997)
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DEV4919
Cranial sensory ganglia in vertebrates develop from the
ectodermal placodes, the neural crest, or both. Although
much is known about the neural crest contribution to
cranial ganglia, relatively little is known about how placode
cells form, invaginate and migrate to their targets. Here, we
identify Pax-3 as a molecular marker for placode cells that
contribute to the ophthalmic branch of the trigeminal
ganglion and use it, in conjunction with DiI labeling of the
surface ectoderm, to analyze some of the mechanisms
underlying placode development. Pax-3 expression in the
ophthalmic placode is observed as early as the 4-somite
stage in a narrow band of ectoderm contiguous to the
midbrain neural folds. Its expression broadens to a patch
of ectoderm adjacent to the midbrain and the rostral
hindbrain at the 8- to 10-somite stage. Invagination of the
first Pax-3-positive cells begins at the 13-somite stage.
Placodal invagination continues through the 35-somite
stage, by which time condensation of the trigeminal
ganglion has begun. To challenge the normal tissue inter-
actions leading to placode formation, we ablated the cranial
neural crest cells or implanted barriers between the neural
tube and the ectoderm. Our results demonstrate that,
although the presence of neural crest cells is not mandatory
for Pax-3 expression in the forming placode, a diffusible
signal from the neuroectoderm is required for induction
and/or maintenance of the ophthalmic placode.
Key words: placode, cranial ganglion, neural crest, Pax-3, FREK,
chick
SUMMARY
Neural tube-ectoderm interactions are required for trigeminal placode
formation
Michael R. Stark
1,2
, John Sechrist
1
, Marianne Bronner-Fraser
1,
* and Christophe Marcelle
1
1
Division of Biology 139-74, California Institute of Technology, Pasadena, CA 91125, USA
2
Department of Developmental and Cell Biology, University of California, Irvine, CA 92697, USA
*Author for correspondence