We identified two cadherins, c-cad6B and c-cad7, expressed by neural crest cells at their premigratory and migratory stages, respectively, in chicken embryos. cDNA transfection experiments showed that both were homophilic adhesion molecules, endowing cells with specific adhesiveness. During development, c-cad6B appeared in the neural fold, localizing at the future neural crest area. This expression was maintained during neural tube closure, but disappeared after neural crest cells had left the neural tube, suggesting its role in neural fold fusion and/or in the formation and maintenance of the presumptive neural crest domain in the neural plate/tube. Crest cells emerging from the neural tube lost c-cad6B, and a subpopulation of them began to express c-cad7. This subpopulation-specific expression of c-cad7 persisted during their migration. The migrating c-cad7-positive cells clustered together, and eventually populated restricted regions including the dorsal and ventral roots but very little ganglia. The latter was populated with N-cadherin-positive crest cells. Migrating neural crest cells expressed alpha- and beta-catenin at cell-cell contacts, indicating that their cadherins are functioning. These results suggest that the migrating crest cells are grouped into subpopulations expressing different cadherins. The cadherin-mediated specific interaction between crest cells likely plays a role in intercellular signaling between homotypic cells as well as in sorting of heterotypic cells.

Reference

Akitaya
T.
,
Bronner-Fraser
M.
(
1992
)
Expression of cell adhesion molecules during initiation and cessation of neural crest cell migration.
Dev. Dynamics
194
,
12
20
Aoyama
H.
,
Delouvee
A.
,
Thiery
J. P.
(
1985
)
Cell adhesion mechanisms in gangliogenesis studied in avian embryo and in a model system.
Cell Differ
17
,
247
260
Bhattacharyya
A.
,
Frank
E.
,
Ranter
N.
,
Brackenbury
R.
(
1991
)
Po is an early marker of the Schwann cell lineage in chickens.
Neuron
7
,
831
844
Bronner-Fraser
M.
(
1985
)
Alterations in neural crest migration by a monoclonal antibody that affects cell adhesion.
J. Cell Biol
101
,
610
617
Bronner-Fraser
M.
(
1986
)
Analysis of the early stages of trunk neural crest migration in avian embryos using monoclonal antibody HNK-1.
Dev. Biol
115
,
44
55
Bronner-Fraser
M.
,
Wolf
J. J.
,
Murray
B. A.
(
1992
)
Effects of antibodies against N-cadherin and N-CAM on the cranial neural crest and neural tube.
Dev. Biol
153
,
291
301
Delannet
M.
,
Martin
F.
,
Bossy
B.
,
Cheresh
D. A.
,
Reichardt
L. F.
,
Duband
J. L.
(
1994
)
Specific roles of the V 1V 3 and V 5 integrins in avian neural crest cell adhesion and migration on vitronectin.
Development
120
,
2687
2702
Duband
J. L.
,
Volberg
T.
,
Sabanay
I.
,
Thiery
J. P.
,
Geiger
B.
(
1988
)
Spatial and temporal distribution of the adherens-junction-associatedadhesion molecule A-CAM during avian embryogenesis.
Development
103
,
325
344
Duband
J. L.
,
Dofour
S.
,
Yamada
S. S.
,
Yamada
K. M.
,
Thiery
J. P.
(
1991
)
Neural crest cell locomotion induced by antibodies to1 integrins: a tool for studying the roles of substratum molecular avidity and density in migration.
J. Cell Sci
98
,
517
532
Erickson
C. A.
,
Perris
R.
(
1993
)
The role of cell-cell and cell-matrix interactions in the morphogenesis of the neural crest.
Dev. Biol
159
,
60
74
Friedlander
D. R.
,
Mege
R.
,
Cunningham
B. A.
,
Edelman
G. M.
(
1989
)
Cell-sorting out is modulated by both the specificity and amount of different cell adhesion molecules (CAMs) expressed on cell surfaces.
Proc. Natl. Acad. Sci. USA
86
,
7043
7047
Fujimori
T.
,
Miyatani
S.
,
Takeichi
M.
(
1990
)
Ectopic expression of N-cadherin perturbs histogenesis in Xenopus embryos.
Development
110
,
97
104
Gomperts
M.
,
Garcia-Castro
M.
,
Wylie
C.
,
Heasman
J.
(
1994
)
Interactions between primordial germ cells play a role in their migration in mouse embryos.
Development
120
,
135
141
Goulding
M.
,
Lumsden
A.
,
Paquette
A. J.
(
1994
)
Regulation of Pax-3 expression in the dermomyotome and its role in muscle development.
Development
120
,
957
971
Hamburger
V.
,
Hamilton
H.
(
1951
)
A series of normal stages in the development of the chicken embryo.
J. Morphol
88
,
49
92
Hatta
K.
,
Takeichi
M.
(
1986
)
Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chicken embryos.
Nature
320
,
447
449
Hatta
K.
,
Takagi
S.
,
Fujisawa
H.
,
Takeichi
M.
(
1987
)
Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos.
Dev. Biol
120
,
215
227
Herrencknecht
K.
,
Ozawa
M.
,
Eckerskorn
C.
,
Lottspeich
F.
,
Lenter
M.
,
Kemler
R.
(
1991
)
The uvomorulin-anchorage protein-catenin is a vinculin homologue.
Proc. Natl. Acad. Sci. USA
88
,
9156
9160
Hirano
S.
,
Kimoto
N.
,
Shimoyama
Y.
,
Hirohashi
S.
,
Takeichi
M.
(
1992
)
Identification of a neural-catenin as a key regulator of cadherin function and multicellular organization.
Cell
70
,
1
20
Inuzuka
H.
,
Miyatani
S.
,
Takeichi
M.
(
1991
)
R-cadherin: A novel Ca2+-dependent cell-cell adhesion molecule expressed in the retina.
Neuron
7
,
69
79
Kato
K.
,
Takahashi
Y.
,
Hayashi
S.
,
Kondoh
H.
(
1988
)
Improved mammalian vectors for high expression of G418 resistance.
Cell. Struct. Funct
12
,
575
580
Kemler
R.
(
1993
)
From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion.
Trends Genet
9
,
317
321
Lallier
T. E.
,
Bronner-Fraser
M.
(
1993
)
Inhibition of neural crest cell attachment by integrin antisense oligonucleotides.
Science
259
,
692
695
Marusich
M.
,
Weston
J.
(
1991
)
Development of the neural crest.
Curr. Opin. Gen. Dev
1
,
221
229
Matsunaga
M.
,
Hatta
K.
,
Takeichi
M.
(
1988
)
Role of N-cadherin cell adhesion molecules in the histogenesis of neural retina.
Neuron
1
,
289
295
Matsunami
H.
,
Miyatani
S.
,
Inoue
T.
,
Copeland
N. G.
,
Gilbert
D. J.
,
Jenkins
N. A.
,
Takeichi
M.
(
1993
)
Cell binding specificity of mouse R-cadherin and chromosomal mapping of the gene.
J. Cell Sci
106
,
401
409
McCrea
P. D.
,
Turck
C. W.
,
Gumbiner
B.
(
1991
)
A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin.
Science
254
,
1359
1361
Miyatani
S.
,
Shimamura
K.
,
Hatta
M.
,
Nagafuchi
A.
,
Nose
A.
,
Matsunaga
M.
,
Hatta
K.
,
Takeichi
M.
(
1989
)
Neural cadherin: Role in selective cell-cell adhesion.
Science
245
,
631
635
Nagafuchi
A.
,
Shirayoshi
Y.
,
Okazaki
K.
,
Yasuda
K.
,
Takeichi
M.
(
1987
)
Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA.
Nature
329
,
341
343
Nagafuchi
A.
,
Takeichi
M.
(
1989
)
Transmembrane control of cadherin-mediated cell adhesion: A 94kd protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin.
Cell Regul
1
,
37
44
Nagafuchi
A.
,
Takeichi
M.
,
Tsukita
S.
(
1991
)
The 102kd cadherin-associated protein: similarity to vinculin and posttranscriptional regulation of expression.
Cell
65
,
849
857
Nagafuchi
A.
,
Ishihara
S.
,
Tsukita
S.
(
1994
)
The role of catenins in the cadherin-mediated cell adhesion: functional analysis of E-cadherin-catenin fusion molecules.
J. Cell Biol
127
,
235
246
Nose
A.
,
Takeichi
M.
(
1986
)
A novel cadherin adhesion molecule: Its expression patterns associated with implantation and organogenesis of mouse embryos.
J. Cell Biol
103
,
2649
2658
Nose
A.
,
Nagafuchi
A.
,
Takeichi
M.
(
1988
)
Expressed recombinant cadherins mediate cell sorting in model system.
Cell
54
,
993
1001
Ozawa
M.
,
Baribault
H.
,
Kemler
R.
(
1989
)
The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species.
EMBO J
8
,
1711
1717
Sano
K.
,
Tanihara
H.
,
Heimark
R. L.
,
Obata
S.
,
Davidson
M.
,
John
T. S.
,
Taketani
S.
,
Suzuki
S.
(
1993
)
Protocadherins: a large family of cadherin-related molecules in central nervous system.
EMBO J
12
,
2249
2256
Selleck
M. A. J.
,
Scherson
T. Y.
,
Bronner-Fraser
M.
(
1993
)
Origins of neural crest cell diversity.
Dev. Biol
159
,
1
11
Shimamura
K.
,
Takahashi
T.
,
Takeichi
M.
(
1992
)
E-cadherin expression in a particular subset of sensory neurons.
Dev. Biol
152
,
242
254
Shimamura
K. S. H.
,
McMahon
A. P.
,
Takeichi
M.
(
1994
)
Wnt-1-dependent regulation of local E-cadherin and N-catenin expression in the embryonic mouse brain.
Development
120
,
2225
2234
Stemple
D. L.
,
Anderson
D. J.
(
1992
)
Isolation of a stem cell for neurons and glia from the mammalian neural crest.
Cell
71
,
973
985
Suzuki
S.
,
Sano
K.
,
Tanihara
H.
(
1991
)
Diversity of the cadherinfamily: Evidence for eight new cadherins in nervous tissue.
Cell Regul
2
,
261
270
Takeichi
M.
(
1977
)
Functional correlation between cell adhesive properties and some cell surface proteins.
J. Cell Biol
75
,
464
474
Takeichi
M.
(
1987
)
Cadherins: a molecular family essential for selective cell-cell adhesion and animal morphogenesis.
Trends Genet
3
,
213
217
Takeichi
M.
(
1988
)
The cadherins: cell-cell adhesion molecules controlling animal morphogenesis.
Development
102
,
639
655
Takeichi
M.
(
1991
)
Cadherin cell adhesion receptors as a morphogenetic regulator.
Science
251
,
1451
1455
Thiery
J. P.
,
Duband
J. L.
,
Rutishauser
U.
,
Edelman
G. M.
(
1982
)
Cell adhesion molecules in early chicken embryogenesis.
Proc. Natl. Acad. Sci. USA
79
,
6737
6741
Thiery
J. P.
,
Delouvee
A.
,
Gallin
W. J.
,
Cunningham
B. A.
,
Edelman
G. M.
(
1984
)
Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers.
Dev. Biol
102
,
61
78
Vincent
M.
,
Duband
J.-L.
,
Thiery
J.-P.
(
1983
)
A cell surface determinant expressed early on migrating neural crest cells.
Dev. Brain Res
9
,
235
238
Watabe
M.
,
Nagafuchi
A.
,
Tsukita
S.
,
Takeichi
M.
(
1994
)
Induction of polarized cell-cell association and retardation of growth by activation of the E-cadherin-catenin adhesion system in a dispersed carcinoma line.
J. Cell. Biol
127
,
247
256
Winklbauer
R.
,
Selchow
A.
,
Nagel
M.
,
Angres
B.
(
1992
)
Cell interaction and its role in mesoderm cell migration during Xenopus gastrulation.
Dev. Dynamics
195
,
290
302
Williams
B. A.
,
Ordahl
C. P.
(
1994
)
Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification.
Development
120
,
785
796
This content is only available via PDF.