After unilateral ablation of the avian cranial neural folds, the remaining neuroepithelial cells are able to replace the missing neural crest population (Scherson et al., 1993). Here, we characterize the cellular and molecular nature of this regulative response by defining: (1) the time and location of neural crest cell production by the neuroepithelium; (2) rostrocaudal axial differences in the regulative response; and (3) the onset of expression of Slug, a transcription factor present in premigratory and migrating neural crest cells. Using DiI and HNK-1 antibody labeling techniques, we find that neural crest regeneration occurs only after apposition of the remaining neuroepithelium with the epidermis, suggesting that the developmental mechanism underlying regeneration of the neural crest may recapitulate initial generation of the neural crest. The regulative response occurs maximally at the 3–5 somite stage, and slowly declines thereafter. Surprisingly, there are profound regional differences in the regenerative ability. Whereas a robust regulation occurs in the caudal midbrain/hindbrain, the caudal forebrain/rostral midbrain regenerates neural crest to a much lesser extent. After neural fold removal in the hindbrain, regenerated neural crest cells migrate in a segmental pattern analogous to that seen in unablated embryos; a decrease in regulative response appears to occur with increasing depth of the ablation. Up-regulation of Slug appears to be an early response after ablation, with Slug transcripts detectable proximal to the ablated region 5–8 hours after surgery and prior to emergence of neural crest cells. Both bilateral and unilateral ablations yield substantial numbers of neural crest cells, though the former recover less rapidly and have greater deficits in neural crest-derived structures than the latter. These experiments demonstrate that the regulative ability of the cranial neuroepithelium to form neural crest depends on the time, location and extent of neural fold ablation.

Reference

Birgbauer
E.
,
Sechrist
J.
,
Bronner-Fraser
M.
,
Fraser
S.
(
1995
)
Rhombomeric origin and rostrocaudal reassortment of neural crest cells revealed by intravital microscopy.
Development
121
,
935
945
Bronner-Fraser
M.
,
Fraser
S. E.
(
1988
)
Cell lineage analysis shows multipotentiality of some avian neural crest cells.
Nature
355
,
161
164
Bronner-Fraser
M.
,
Fraser
S. E.
(
1989
)
Developmental potential of avian trunk neural crest cells in situ.
Neuron
3
,
755
766
Dickinson
M.
,
Selleck
M.
,
McMahon
A.
,
Bronner-Fraser
M.
(
1995
)
Dorsalization of the neural tube by the non-neural ectoderm.
Development
121
,
2099
2106
Frank
E.
,
Sanes
J. R.
(
1991
)
Lineage of neurons and glia in chick dorsal root ganglia: analysis in vivo with a recombinant retrovirus.
Development
111
,
895
908
Hammond
W. S.
,
Yntema
C. L.
(
1958
)
Origin of ciliary ganglia in the chick.
J. Exp. Zool
111
,
457
502
Hamburger
V.
(
1961
)
Experimental analysis of the dual origin of the trigeminal ganglion in the chick embryo.
J. Exp. Zool
148
,
91
123
Hamburger
V.
,
Hamilton
H. L.
(
1951
)
A series of normal stages in the development of the chick embryo.
J. Morphol
88
,
49
92
Hunt
P.
,
Ferretti
P.
,
Krumlauf
R.
,
Thorogood
P.
(
1995
)
Restoration of the normal Hox code and branchial arch morphogenesis after extensive deletion of the hindbrain neural crest.
Dev. Biol
168
,
584
597
Lee
V.
,
Carden
M.
,
Schlaepfer
W.
,
Trojanowski
J.
(
1987
)
Monoclonal antibodies distinguish several differentially phosphorylated states of the two largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous system of adult rats.
J. Neurosci
7
,
3474
3489
Lumsden
A.
,
Sprawson
N.
,
Graham
A.
(
1991
)
Segmental origin and migration of neural crest cells in the hindbrain region of the chick embryo.
Development
113
,
1281
1291
Nieto
M. A.
,
Sargent
M. G.
,
Wilkinson
D. G.
,
Cooke
J.
(
1994
)
Control of cell behavior during vertebrate development by Slug, a zinc finger gene.
Science
264
,
835
839
Rosenquist
G. C.
(
1981
)
Epiblast origin and early migration of neural crest cells in the chick embryo.
Dev. Biol
87
,
201
211
Scherson
T.
,
Serbedzija
G.
,
Fraser
S.
,
Bronner-Fraser
M.
(
1993
)
Regulative capacity of the cranial neural tube to form neural crest.
Development
118
,
1049
1061
Sechrist
J.
,
Serbedzija
G.
,
Scherson
T.
,
Fraser
S. E.
,
Bronner-Fraser
M.
(
1993
)
Segmental migration of the hindbrain neural crest does not arise from its segmental generation.
Development
118
,
691
703
Selleck
M. A. J.
,
Bronner-Fraser
M.
(
1995
)
Origins of the avian neural crest: the role of neural plate-epidermal interactions.
Development
121
,
525
538
Fraser
M.
,
Fraser
S. E.
(
1989
)
Vital dye analysis of the timing and pathways of avian trunk neural crest cell migration.
Development
106
,
806
816
Serbedzija
G.
,
Bronner-Fraser
M.
,
Fraser
S. E.
(
1992
)
Vital dye analysis of cranial neural crest cell migration in the mouse embryo.
Development
116
,
297
307
Sharma
K.
,
Korade
Z.
,
Frank
E.
(
1995
)
Late-migrating neuroepithelial cells from the spinal cord differentiate into sensory ganglion cells and melanocytes.
Neuron
14
,
143
52
Smith
J.
,
Fauquet
M.
,
Ziller
C.
,
LeDouarin
N. M.
(
1979
)
Acetylcholine synthesis by mesencephalic neural crest cells in the process of migration in viv o.
Nature
282
,
853
855
Storey
K. G.
,
Crossley
J. M.
,
DeRobertis
E. M.
,
Norris
W. E.
,
Stern
C. D.
(
1992
)
Neural induction and regionalisation in the chick embryo.
Development
114
,
729
741
Tucker
G. C.
,
Aoyama
H.
,
Lipinski
M.
,
Tursz
T.
,
Thiery
J. P.
(
1984
)
Identical reactivity of monoclonal antibodies HNK-1 and NC-1: Conservation in vertebrates on cells derived from the neural primordium and on some leukocytes.
Cell Differ
14
,
223
230
Vincent
M.
,
Duband
J. L.
,
Thiery
J. P.
(
1983
)
A cell surface determinant expressed early on migrating avian neural crest cells.
Dev. Brain Res
9
,
235
238
Wilkinson
D. G.
,
Nieto
A. M.
(
1993
)
Analysis of gene expression by in situ hybridisation to tissue sections and in whole mounts.
Methods Enzymol
225
,
361
373
This content is only available via PDF.