INTRODUCTION
The paraxial mesoderm of vertebrate embryos segments into
metameric units, the somites, which develop stepwise to give
rise initially to the ventral mesenchymal sclerotome and the
dorsal epithelial dermomyotome (DM). Sclerotomal cells then
undergo further morphogenetic changes and form the vertebrae
and ribs (Brand-Saberi and Christ, 2000; Huang et al., 2000b)
(see Kato and Aoyama, 1998). DM precursors give rise to the
epaxial muscles of the back, the hypaxial muscles of the body
wall and limbs, and the dorsal dermis (Christ et al., 1983;
Kalcheim et al., 1999; Huang and Christ, 2000), yet the
mechanism by which these derivatives form from the DM is
not fully resolved. In the past few years, the existence of an
additional cellular domain in the medial epithelial somite has
been described. It consists of a specialized subset of early post-
mitotic progenitors which in avian embryos, express both
MyoD and Myf5. During the process of somite dissociation,
these cells bend underneath the forming DM and upon
delamination and polarized caudorostral migration,
differentiate into the first unit-length myofibers that span the
entire mediolateral extent of each segment (Kahane et al.,
1998a; Kahane et al., 2002). Notably, these early fibers were
suggested to provide a scaffold for further addition of
myogenic cells that arise in the overlying DM. These pioneer
myoblasts, together with DM-derived myofibers, constitute the
myotome from which vertebral muscles of the back and the
body wall (intercostal and abdominal) will form (Kalcheim et
al., 1999). At variance, limb muscles derive exclusively from
the ventrolateral lip (VLL) of the DM (Chevallier et al., 1977)
and bear no contribution of pioneer myofibers (N.K. and C.K.,
unpublished).
A wealth of information is available on early patterning
of somite derivatives that involves opposite and mutually
inhibitory gradients of factor activity (reviewed by Brent and
Tabin, 2002). Yet, the mechanisms by which these basic
gradients are translated into morphogenetic processes remain
incompletely understood. Ordahl and colleagues (Denetclaw et
al., 1997; Denetclaw and Ordahl, 2000) have proposed that
growth of both the myotome and DM is driven by two stem
cell systems restricted to the dorsomedial and ventrolateral lips
(DML and VLL, respectively) of the DM. The DML was
suggested to drive medial growth of the myotome and the VLL
to be responsible for expansion in a ventral direction
(Denetclaw et al., 1997; Denetclaw and Ordahl, 2000; Ordahl
et al., 2001). Consequently, both myotome and DM expand
incrementally in opposite medial and lateral directions, with
the youngest cells approaching the medial and lateral extremes
4325 Development 130, 4325-4336
© 2003 The Company of Biologists Ltd
doi:10.1242/dev.00667
We have previously shown that overall growth of the
myotome in the mediolateral direction occurs in a coherent
and uniform pattern. We asked whether development of the
dermomyotome and resultant dermis follow a similar
pattern or are, alternatively, controlled by restricted pools
of stem cells driving directional growth. To this end, we
studied cellular events that govern dermomyotome
development and the regional origin of dermis.
Measurements of cell proliferation, nuclear density and
cellular rearrangements revealed that the developing
dermomyotome can be subdivided in the transverse plane
into three distinct and dynamic regions: medial, central
and lateral, rather than simply into epaxial and hypaxial
domains. To understand how these temporally and
spatially restricted changes affect overall dermomyotome
growth, lineage tracing with CM-DiI was performed. A
proportional pattern of growth was measured along the
entire epithelium, suggesting that mediolateral growth of
the dermomyotome is coherent. Hence, they contrast with
a stem cell view suggesting focal and inversely oriented
sources of growth restricted to the medial and lateral edges.
Consistent with this uniform mediolateral growth, lineage
tracing experiments showed that the dermomyotome-
derived dermis originates from progenitors that reside
along the medial as well as the lateral halves of somites, and
whose contribution to dermis is regionally restricted. Taken
together, our results support the view that all derivatives of
the dorsal somite (dermomyotome, myotome and dermis)
keep a direct topographical relationship with their
epithelial ascendants.
Key words: Avian embryo, Cell delamination, Dermis,
Dermomyotome, Desmin, Epithelial-mesenchymal conversion,
Myotome, Somite
SUMMARY
Coherent development of dermomyotome and dermis from the entire
mediolateral extent of the dorsal somite
Raz Ben-Yair, Nitza Kahane and Chaya Kalcheim*
Department of Anatomy and Cell Biology, Hebrew University-Hadassah Medical School, Jerusalem 91120, PO Box 12272, Israel
*Author for correspondence (e-mail: kalcheim@nn-shum.cc.huji.ac.il
Accepted 9 June 2003