The Semaphorins are a family of secreted and transmembrane proteins known to elicit growth cone repulsion and collapse. We made and characterized a putative null mutant of the C. elegans gene semaphorin-2a (Ce-sema-2a). This mutant failed to complement mutants of mab-20 (Baird, S. E., Fitch, D. H., Kassem, I. A. A. and Emmons, S. W. (1991) Development 113, 515–526). In addition to low-frequency axon guidance errors, mab-20 mutants have unexpected defects in epidermal morphogenesis. Errant epidermal cell migrations affect epidermal enclosure of the embryo, body shape and sensory rays of the male tail. These phenotypic traits are explained by the formation of inappropriate contacts between cells of similar type and suggest that Ce-Sema-2a may normally prevent formation or stabilization of ectopic adhesive contacts between these cells.

Altschul
S. F.
,
Gish
W.
,
Miller
W.
,
Myers
E. W.
,
Lipman
D. J.
(
1990
)
Basic local alignment search tool.
J. Mol. Biol
215
,
403
410
Bagnard
D.
,
Lohrum
M.
,
Uziel
D.
,
Puschel
A. W.
,
Boiz
J.
(
1998
)
Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections.
Development
125
,
5043
5053
Baird
S. E.
,
Fitch
D. H.
,
Kassem
I. A. A.
,
Emmons
S. W.
(
1991
)
Pattern formation in the nematode epidermis: determination of the peripheral sense organs in the C. elegans male tail.
Development
113
,
515
526
Behar
O.
,
Golden
J. A.
,
Mashima
H.
,
Schoen
F. J.
,
Fishman
M. C.
(
1996
)
Semaphorin III is needed for normal patterning and growth of nerves, bones and heart.
Nature
383
,
525
528
Carlier
M. F.
(
1998
)
Control of actin dynamics.
Curr. Opin. Cell Biol
10
,
45
51
Chan
S. S.-Y.
,
Zheng
H.
,
Su
M.-W.
,
Wilk
R.
,
Killeen
M. T.
,
Hedgecock
E. M.
,
Culotti
J. G.
(
1996
)
UNC-40, a C. elegans homolog of DCC(deleted in colorectal cancer), is required in motile cells responding to UNC-6 netrin cues.
Cell
87
,
187
195
Chow
K. L.
,
Emmons
S. W.
(
1994
)
Hom-C/Hox genes and four interacting loci determine the morphogenetic properties of single cells in the nematode male tail.
Development
120
,
2579
2593
Colavita
A.
,
Culotti
J. G.
(
1998
)
Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans.
Dev. Biol
194
,
72
85
Colavita
A.
,
Krishna
S.
,
Zheng
H.
,
Padgett
R. W.
,
Culotii
J. G.
(
1998
)
Pioneer axon guidance by UNC-129, a C. elegans TGB-.
Science
281
,
706
709
Costa
M.
,
Raich
W.
,
Agbunag
C.
,
Leung
B.
,
Hardin
J.
,
Priess
J. R.
(
1998
)
A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo.
J. Cell Biol
141
,
297
308
de la Torre
J. R.
,
Hopker
V. H.
,
Ming
G.-L.
,
Poo
M.-m.
,
Tessier-Lavigne
M.
,
Hemmati-Brivanlou
A.
,
Holt
C. E.
(
1997
)
Turning of retinal growth cones in a Netrin-1 gradient mediated by the Netrin receptor DCC.
Neuron
19
,
1211
1224
Eickholt
B. J.
,
Mackenzie
S. L.
,
Graham
A.
,
Walsh
F. S.
,
Doherty
P.
(
1999
)
Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions.
Development
126
,
2181
2189
Fan
J.
,
Raper
J. A.
(
1995
)
Localized collapsing cues can steer growth cones without inducing their full collapse.
Neuron
14
,
263
274
Finney
M.
,
Ruvkun
G.
(
1990
)
The unc-86 gene product couples cell lineage and cell identity in C. elegans.
Cell
63
,
895
905
Francis
R.
,
Waterston
R. H.
(
1991
)
Muscle cell attachment in Caenorhabditis elegans.
J. Cell Biol
114
,
465
479
Frohman
M. A.
,
Dush
M. K.
,
Martin
G. R.
(
1988
)
Rapid production of full-length cDNAs from rare transcripts:amplification using a single gene-specific oligonucleotide primer.
Proc. Natl. Acad. Sci. USA
85
,
8998
9002
He
Z.
,
Tessier-Lavigne
M.
(
1997
)
Neuropilin is a receptor for the axonal chemorepellent Semaphorin III.
Cell
90
,
739
751
Hedgecock
E. M.
,
Culotti
J. G.
,
Hall
D. H.
(
1990
)
The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans.
Neuron
2
,
61
85
Kitsukawa
T.
,
Shimono
A.
,
Kawakami
A.
,
Kondoh
H.
,
Fujisawa
H.
(
1995
)
Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs.
Development
121
,
4309
4318
Kolodkin
A. L.
,
Matthes
D. J.
,
Goodman
C. S.
(
1993
)
The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules.
Cell
75
,
1389
1399
Kolodkin
A. L.
,
Matthes
D. J.
,
O'Connor
T. P.
,
Patel
N. H.
,
Admon
A.
,
Bentley
D.
,
Goodman
C. S.
(
1992
)
Fasciclin IV: Sequence, expression and function during growth cone guidance in the grasshopper embryo.
Neuron
9
,
831
845
Krause
M.
,
Hirsh
D.
(
1987
)
A trans-spliced leader sequence on actin mRNA in C. elegans.
Cell
49
,
753
761
Labouesse
M.
,
Hartwieg
E.
,
Horvitz
H. R.
(
1996
)
The Caenorhabditis elegans LIN-26 protein is required to specify and/or maintain all non-neuronal ectodermal cell fates.
Development
122
,
2579
2588
Leung-Hagesteijn
C.
,
Spence
A. M.
,
Stern
B. D.
,
Zhou
Y.
,
Su
M.-W.
,
Hedgecock
E. M.
,
Culotti
J. G.
(
1992
)
UNC-5, a transmembrane protein with immunoglobulin and thrombospodin type 1 domains, guides cell and pioneer axon migrations in C. elegans.
Cell
71
,
289
299
Mello
C. C.
,
Fire
A.
(
1995
)
DNA transformation in Caenorhabditiselegans; modern biological analysis of an organism. (ed. H. F. Epstein and D. C. Shakes).
Methods in Cell Biology
48
,
452
482
Podbilewicz
B.
,
White
J. G.
(
1994
)
Cell fusions in the developing epithelia of C. elegans.
Dev. Biol
161
,
408
424
Priess
J. R.
,
Hirsh
D. I.
(
1986
)
Caenorhabditis elegans morphogenesis: The role of the cytoskeleton in elongation of the embryo.
Dev. Biol
117
,
156
173
Riesgo-Escovar
J. R.
,
Hafen
E.
(
1997
)
Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure.
Genes Dev
11
,
1717
1727
Schnabel
R.
,
Hutter
H.
,
Moerman
D.
,
Schnabel
H.
(
1997
)
Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: Variability of development and regional specification.
Dev. Biol
184
,
234
265
Semaphorin Nomenclature Committee
(
1999
)
Unified nomenclature for the semaphorins/collapsins.
Cell
28
,
551
552
Soker
S.
,
Takashima
S.
,
Miao
H. Q.
,
Neufeld
G.
,
Kladsbrun
M.
(
1998
)
Neuropilin-1 is expressed by endothelial and tumour cells as an isoform-specific receptor for vascular endothelial growth factor.
Cell
92
,
735
745
Song
H.-j.
,
Ming
G.-l.
,
He
Z.
,
Lehmann
M.
,
McKerracher
L.
,
Tessier-Lavigne
M.
,
Poo
M.-m.
(
1998
)
Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides.
Science
281
,
1515
1518
Sulston
J. E.
,
Horvitz
H. R.
(
1977
)
Postembryonic cell lineages of the nematode Caenorhabditis elegans.
Dev. Biol
56
,
110
156
Sulston
J. E.
,
Albertson
D. G.
,
Thomson
J. N.
(
1980
)
The Caenorhabditis elegans male: Postembryonic development of nongonadal structures.
Dev. Biol
78
,
542
576
Sulston
J. E.
,
Schierenberg
E.
,
White
J. G.
,
Thomson
J. N.
(
1983
)
The embryonic cell lineage of the nematode Caenorhabditis elegans.
Dev. Biol
100
,
64
119
Tanaka
E.
,
Sabry
J.
(
1995
)
Making the connection: Cytoskeletal rearrangements during growth cone guidance.
Cell
83
,
171
176
Williams-Masson
E. M.
,
Malik
A. N.
,
Hardin
J.
(
1997
)
An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis.
Development
124
,
2889
2901
Williams-Masson
E. M.
,
Hied
P. J.
,
Lavin
C. A.
,
Hardin
J.
(
1998
)
The cellular mechanism of epithelial rearrangement during morphogenesis of the Caenorhabditis elegans dorsal hypodermis.
Dev. Biol
204
,
263
276
Winberg
M. L.
,
Mitchell
K. J.
,
Goodman
C. S.
(
1998
)
Genetic analysis of the mechanisms controlling target selection: Complementary and combinatorial functions of Netrins, Semaphorins and IgCAMs.
Cell
93
,
581
591
Wong
J. T.
,
Yu
W. T.
,
O'Connor
T. P.
(
1997
)
Transmembrane grasshopper Semaphorin I promotes axon outgrowth in vivo.
Development
124
,
3597
3607
Yu
H.-H.
,
Araj
H. H.
,
Rallis
S. A.
,
Kolodkin
A. L.
(
1998
)
The transmembrane Semaphorin Sema I is required in Drosophila for embryonic motor and CNS axon guidance.
Neuron
20
,
207
220
Zwaal
R. R.
,
Broeks
A.
,
van Meurs
J.
,
Groenen
T. M.
,
Plasterk
R. H.
(
1993
)
Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank.
Proc. Natl. Acad. Sci. U.S.A
90
,
7431
7435
This content is only available via PDF.