INTRODUCTION
Neurulation is the process by which progenitors of the central
nervous system are shaped, separated from and brought
beneath the epidermis. The cellular basis of these movements
have been investigated in amphibians (Jacobson, 1981;
Jacobson and Gordon, 1976; Keller et al., 1992b), chicken
(Schoenwolf and Smith, 1990b; Smith and Schoenwolf, 1997)
and mice (Bush et al., 1990; Sausedo and Schoenwolf, 1994;
Smith et al., 1994) but remains poorly understood. In the chick,
which has been used extensively as a paradigm for vertebrate
neurulation, a broad neural plate folds and the margins of the
plate are raised and brought into apposition at the neural folds
as cells take on stereotypical shapes. Analysis of serial sections
and electron microscopy have identified cell movements and
shape changes accompanying neural tube formation in chick
(Schoenwolf and Alvarez, 1989; Schoenwolf and Smith,
1990a) where these cell behaviors (apical contraction and
interkinetic nuclear migration) result in the formation of a
‘medial hinge’ overlying the notochord and a ‘dorsal lateral
hinge’ near the prospective sulcus limitans, that together bring
the neural folds into opposition. The epidermis then fuses, the
neural ectoderm fuses and the neural crest is released from
neural epithelium of the newly formed neural tube. In this
manner, it is thought that the flat neural plate rolls into a tube
with the lumenal face of the neural tube forming from the
apical face of the neural plate.
However, additional processes appear to be involved in chick
neurulation. By following the rapid events at the start of
neurulation, van Straaten and coworkers (1996) found that the
lateral face of the two neural folds ‘zip’ into apposition,
starting near the floorplate and proceeding dorsally. They
found that the lumen of the neural tube nearly disappears after
apposition and then re-opens to form the lumen after the neural
4547 Development 126, 4547-4556 (1999)
Printed in Great Britain © The Company of Biologists Limited 1999
DEV6419
We have characterized the cell movements and prospective
cell identities as neural folds fuse during neural tube
formation in Xenopus laevis. A newly developed whole-
mount, two-color fluorescent RNA in situ hybridization
method, visualized with confocal microscopy, shows that
the dorsal neural tube gene xpax3 and the neural-crest-
specific gene xslug are expressed far lateral to the medial
site of neural fold fusion and that expression moves
medially after fusion. To determine whether cell
movements or dynamic changes in gene expression are
responsible, we used low-light videomicroscopy followed by
fluorescent in situ and confocal microscopy. These methods
revealed that populations of prospective neural crest and
dorsal neural tube cells near the lateral margin of the
neural plate at the start of neurulation move to the dorsal
midline using distinctive forms of motility. Before fold
fusion, superficial neural cells apically contract, roll the
neural plate into a trough and appear to pull the superficial
epidermal cell sheet medially. After neural fold fusion,
lateral deep neural cells move medially by radially
intercalating between other neural cells using two types of
motility. The neural crest cells migrate as individual cells
toward the dorsal midline using medially directed
monopolar protrusions. These movements combine the two
lateral populations of neural crest into a single medial
population that form the roof of the neural tube. The
remaining cells of the dorsal neural tube extend
protrusions both medially and laterally bringing about
radial intercalation of deep and superficial cells to form a
single-cell-layered, pseudostratified neural tube. While
ours is the first description of medially directed cell
migration during neural fold fusion and re-establishment
of the neural tube, these complex cell behaviors may be
involved during cavitation of the zebrafish neural keel and
secondary neurulation in the posterior axis of chicken and
mouse.
Time-lapse sequences online:
http://www.people.virginia.edu/~lad4x/tubeclosure.html and
http://www.biologists.com/Development/movies/dev6419.html
Key words: Tyramide, Fluorescent in situ hybridization, Whole-
mount confocal microscopy, xk81, Epidermal cytokeratin, xslug,
Neural crest, xpax3, n-tubulin, neuron, xash3, Mediolateral
intercalation, Radial intercalation, Directed protrusive activity,
Convergent extension
SUMMARY
Neural tube closure in Xenopus laevis involves medial migration, directed
protrusive activity, cell intercalation and convergent extension
L. A. Davidson* and R. E. Keller
Department of Biology, Gilmer Hall, University of Virginia, Charlottesville, VA 22903, USA
*Author for correspondence (e-mail: lance_davidson@virginia.edu)
Accepted 21 July; published on WWW 27 September 1999