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In this review we focus on the development of verte-
brate limbs. Studying limb development has a number
of advantages. In particular, developing limbs can be
readily manipulated (both surgically and genetically)
without influencing the viability of the embryo, yet many
of the emerging principles can be applied to under-
standing earlier developmental events, such as specify-
ing the main body axes.
To set the scene we start with a brief overview of limb
development as it was understood before the use of the
tools of molecular biology. Then we follow with an assess-
ment of where we stand today and conclude with a dis-
cussion of what we might hope to learn in the near future.
The past: limb organizer centres
Limb specification begins very early during develop-
ment with the establishment of a special group of cells
termed the ‘limb field’
1
. As development proceeds, pre-
cisely positioned limb buds appear, opposite each other,
as a result of the coordinated proliferation of cells
derived from the somites and the lateral plate meso-
derm (Fig. 1a–c)
2,3
. Although the mechanisms that ini-
tially establish and position the limb field are still
unknown, nearly five decades of transplantation experi-
ments have provided extraordinary insights into the
subsequent development of the limb bud.
It is now clear that very early interactions between
cells ensure that the limb develops with predetermined
anteroposterior and dorsoventral asymmetry.
These signals are (Fig. 1d, e): (1) the ectodermal
cells
4,5
covering the limb bud that, at early stages, con-
trol the dorsoventral asymmetry of the future limb; (2) a
specialized epithelium, located at the tip of the growing
limb bud, termed the apical ectodermal ridge (AER)
6–8
that, in conjunction with the cells directly underneath,
(3) the so-called progress zone (PZ)
9
, directs the out-
growth of the limb along the proximodistal axis; and (4)
a group of mesodermal cells located at the posterior
margin of the limb bud, termed the zone of polarizing
activity (ZPA)
10
or polarizing region, that controls the
outgrowth of the limb along the anteroposterior axis.
The present: the molecular basis of limb development
The advent of molecular and genetic techniques has
not only allowed us to begin to unravel how these organ-
izer centres interact with each other, but has also led to
the identification of some of the molecules directly
responsible for providing the initial positional cues that
establish these signalling centres. These molecules have
been identified through a variety of means: differential
screening; chance; purely biochemical approaches; or
by homology to developmental genes in Drosophila
where they were identified in mutation screens. A brief
examination of the character of these genes reveals that
they encode two types of protein: transcriptional regu-
lators and signalling proteins.
Limbs are moving:
where are they going?
JOHN W.R. SCHWABE (jws2@mrc-lmb.cam.ac.uk)
CONCEPCIÓN RODRIGUEZ- ESTEBAN (crodriguez@aim.salk.edu)
JUAN CARLOS IZPISÚA BELMONTE (belmonte@salk.edu)
The past decade has witnessed many changes in the way in
which biologists study vertebrate development. Like
curious children, we have progressed from merely
watching and playing with our toys to the more exciting
activity of taking them apart. This progression is mainly
due to the application of a number of new techniques that
allow us not only to ablate gene function, but also to induce
gene activity inappropriately in time and space. Through
the use of these techniques we can now disassemble our
‘toys’ and begin to understand how the pieces fit together
and, thus, we are beginning to understand how the
vertebrate embryo develops. Additionally, the analysis and
comparison of limb development in diverse species has
provided much insight into the evolutionary mechanisms
through which changes in developmental pathways have
led to the extraordinary diversity of limbs.