INTRODUCTION
The migrations of neurons and their growth cones shape the
structure and connectivity of developing nervous systems.
Notable examples include the migrations of neural crest cells
to generate the peripheral nervous system of vertebrates (Le
Douarin, 1980) and the radial migrations of neurons that form
the layers of the mammalian cortex (O’Rourke et al., 1992;
Walsh and Cepko, 1993). In addition, extensive migrations of
growth cones generate the axonal patterns of connectivity
required for nervous system function (Goodman and Shatz,
1993).
Growth cones and migrating cells navigate through
complex environments to reach their destinations by respond-
ing to guidance cues provided by other cells and the extra-
cellular matrix. These cues include cell-associated molecules,
immobilized matrix components and diffusible molecules. In
vivo and in vitro studies have defined activities that stimulate
or inhibit axon outgrowth nondirectionally, and directional
activities that attract or repel migrating cells and growth
cones (Reichardt and Tomaselli, 1991; Keynes and Cook,
1995). A major goal of developmental neurobiology is to
understand how these cues are provided and interpreted as
well as how individual cells integrate information from
multiple cues.
Genetic analysis of the nematode Caenorhabditis elegans
has identified a guidance mechanism that provides directional
information along the dorsoventral axis to migrating cells and
growth cones. The product of the C. elegans gene unc-6 acts
as a directional cue for both dorsally and ventrally directed
migrations (Hedgecock et al., 1990; McIntire, et al., 1992).
unc-6 encodes a secreted, laminin-related protein that has been
proposed to be distributed in a gradient along the dorsoventral
axis (Hedgecock et al., 1990; Ishii et al., 1992). The unc-5 gene
is specifically required for dorsally directed migrations and
appears to encode an UNC-6 receptor (Leung-Hagesteijn et al.,
1992; Hamelin et al., 1993).
UNC-6 is closely related to the netrins, vertebrate proteins
that act in vitro as chemotropic molecules for commissural
growth cones in the developing spinal cord (Tessier-Lavigne
et al., 1988; Kennedy et al., 1994; Serafini et al., 1994). netrin-
1 is secreted by the ventral floor plate cells, suggesting that a
gradient of netrin activity might direct commissural growth
cones ventrally to the floor plate. Therefore, one cue that
functions in guiding circumferential migrations appears to be
functionally conserved between species (Goodman, 1994).
Although components involved in directing circumferential
(dorsoventral) migrations have been identified, relatively little
is known about the molecules involved in directing longitudi-
nal (anteroposterior) migrations. Longitudinal axon outgrowth
and cell migration is a prominent feature of the development
of the C. elegans nervous system. Most neuronal cell bodies
in C. elegans are located in ganglia of the head and tail or
ventrally along the length of the animal (Fig. 1; Albertson and
Thomson, 1976; White et al., 1976, 1986). Many of these
neurons extend axons along the main longitudinal nerve
bundles, the ventral and dorsal nerve cords, while others extend
longitudinal axons along several smaller lateral nerve bundles.
671
Development 122, 671-682 (1996)
Printed in Great Britain © The Company of Biologists Limited 1996
DEV9455
The assembly of the nervous system in the nematode C.
elegans requires the directed migrations of cells and growth
cones along the anteroposterior and dorsoventral body
axis. We show here that the gene vab-8 is essential for most
posteriorly directed migrations of cells and growth cones.
Mutations in vab-8 disrupt fourteen of seventeen posteri-
orly directed migrations, but only two of seventeen anteri-
orly directed and dorsoventral migrations. For two types
of neurons that extend axons both anteriorly and posteri-
orly, vab-8 mutations disrupt only the growth of the poste-
riorly directed axon. vab-8 encodes two genetic activities
that function in the guidance of different migrations. Our
results suggest that most posteriorly directed cell and
growth cone migrations are guided by a common
mechanism involving the vab-8 gene.
Key words: anterior-posterior axis, axon guidance, cell migration,
pathfinding, C. elegans, vab-8 gene
SUMMARY
The C. elegans gene vab-8 guides posteriorly directed axon outgrowth and
cell migration
Bruce Wightman
1,
*, Scott G. Clark
3
, Anna M. Taskar
1
, Wayne C. Forrester
1
, Andres V. Maricq
3
,
Cornelia I. Bargmann
2,3
and Gian Garriga
1
1
Department of Molecular and Cell Biology, University of California, Berkeley, CA, 94720-3204, USA
2
Howard Hughes Medical Institute and
3
Programs in Developmental Biology, Neuroscience, and Genetics, Department of
Anatomy, University of California, San Francisco, CA 94143-0452, USA
*Author for correspondence (e-mail: wightman@mendel.berkeley.edu)