INTRODUCTION
The neural crest, a transitory population of cells that is
characteristic of vertebrate embryos, forms at the border of the
neural plate, posteriorly to the diencephalon. After induction,
neural crest cells undergo an epithelial-to-mesenchymal
transition and migrate into several locations to give rise to a
large variety of derivatives (for a review, see Le Douarin and
Kalcheim, 1999). Experimental manipulations in chick, fish
and amphibian embryos have shown that both the ectoderm and
the neural plate can give rise to neural crest cells when they
are juxtaposed (Moury and Jacobson, 1989; Moury and
Jacobson, 1990; Selleck and Bronner-Fraser, 1995; Mancilla
and Mayor, 1996; Woo and Fraser, 1998). However, in vivo,
the neural crest forms adjacent to three different tissues, the
non neural ectoderm, the neural plate and the underlying
paraxial mesoderm, all of which thus constitute potential
sources of neural crest inducers (Schroeder, 1970). Although
many studies have focused on neural crest induction by the
ectoderm in the chick embryo (Dickinson et al., 1995; Basch
et al., 2000; Knecht and Bronner-Fraser, 2002), a pioneering
study by Raven and Kloos (Raven and Kloos, 1945) showed
that the paraxial mesoderm can induce neural crest formation
in the ectoderm of amphibians. More recent studies also show
that recombining the paraxial mesoderm with naive ectoderm
in Xenopus laevis embryos results in potent neural crest
induction in the ectodermal part of the explant and that excising
the paraxial mesoderm results in lack of neural crest formation
in vivo (Mancilla and Mayor, 1996; Bonstein et al., 1998;
Marchant et al., 1998). In chick embryos, some data also
indicate that the melanocytes, which are neural crest
derivatives, are induced after neural plate-paraxial mesoderm
recombination (Selleck and Bronner-Fraser, 1995). Although
tested separately in these experimental assays, the possibility
that the inducing activities from the ectoderm and the
mesoderm might act in concert during normal development
remains to be explored.
In the amphibian embryo, the current analysis of the
molecular basis of ectoderm-neural tissue interactions results
in a two-step model of neural crest induction detailed below
(reviewed by Aybar and Mayor, 2002; Knecht and Bronner-
Fraser, 2002). Slug was generally used in these studies as a
3111 Development 130, 3111-3124
© 2003 The Company of Biologists Ltd
doi:10.1242/dev.00531
At the border of the neural plate, the induction of the
neural crest can be achieved by interactions with the
epidermis, or with the underlying mesoderm. Wnt signals
are required for the inducing activity of the epidermis in
chick and amphibian embryos. Here, we analyze the
molecular mechanisms of neural crest induction by the
mesoderm in Xenopus embryos. Using a recombination
assay, we show that prospective paraxial mesoderm induces
a panel of neural crest markers (Slug, FoxD3, Zic5 and
Sox9), whereas the future axial mesoderm only induces a
subset of these genes. This induction is blocked by a
dominant negative (dn) form of FGFR1. However, neither
dnFGFR4a nor inhibition of Wnt signaling prevents neural
crest induction in this system. Among the FGFs, FGF8 is
strongly expressed by the paraxial mesoderm. FGF8 is
sufficient to induce the neural crest markers FoxD3, Sox9
and Zic5 transiently in the animal cap assay. In vivo, FGF8
injections also expand the Slug expression domain. This
suggests that FGF8 can initiate neural crest formation and
cooperates with other DLMZ-derived factors to maintain
and complete neural crest induction. In contrast to Wnts,
eFGF or bFGF, FGF8 elicits neural crest induction in the
absence of mesoderm induction and without a requirement
for BMP antagonists. In vivo, it is difficult to dissociate the
roles of FGF and WNT factors in mesoderm induction and
neural patterning. We show that, in most cases, effects on
neural crest formation were parallel to altered mesoderm
or neural development. However, neural and neural crest
patterning can be dissociated experimentally using
different dominant-negative manipulations: while Nfz8
blocks both posterior neural plate formation and neural
crest formation, dnFGFR4a blocks neural patterning
without blocking neural crest formation. These results
suggest that different signal transduction mechanisms may
be used in neural crest induction, and anteroposterior
neural patterning.
Key words: FGF, WNT, FGF8, Paraxial mesoderm, Xenopus embryo,
Neural crest, Neural patterning
SUMMARY
Neural crest induction by paraxial mesoderm in Xenopus embryos requires
FGF signals
Anne-Hélène Monsoro-Burq*, Russell B. Fletcher and Richard M. Harland
Department of Molecular and Cellular Biology, University of California at Berkeley, CA 94720, USA
*Author for correspondence (e-mail: monsoro@uclink.berkeley.edu)
Accepted 30 March 2003