Somites, like all axial structures, display dorsoventral polarity. The dorsal portion of the somite forms the dermamyotome, which gives rise to the dermis and axial musculature, whereas the ventromedial somite disperses to generate the sclerotome, which later comprises the vertebrae and intervertebral discs. Although the neural tube and notochord are known to regulate some aspects of this dorsoventral pattern, the precise tissues that initially specify the dermamyotome, and later the myotome from it, have been controversial. Indeed, dorsal and ventral neural tube, notochord, ectoderm and neural crest cells have all been proposed to influence dermamyotome formation or to regulate myocyte differentiation. In this report we describe a series of experimental manipulations in the chick embryo to show that dermamyotome formation is regulated by interactions with the dorsal neural tube. First, we demonstrate that when a neural tube is rotated 180 degrees around its dorsoventral axis, a secondary dermamyotome is induced from what would normally have developed as sclerotome. Second, if we ablate the dorsal neural tube, dermamyotomes are absent in the majority of embryos. Third, if we graft pieces of dorsal neural tube into a ventral position between the notochord and ventral somite, a dermamyotome develops from the sclerotome that is proximate to the graft, and myocytes differentiate. In addition, we also show that myogenesis can be regulated by the dorsal neural tube because when pieces of dorsal neural tube and unsegmented paraxial mesoderm are combined in tissue culture, myocytes differentiate, whereas mesoderm cultures alone do not produce myocytes autonomously. In all of the experimental perturbations in vivo, the dorsal neural tube induced dorsal structures from the mesoderm in the presence of notochord and floorplate, which have been reported previously to induce sclerotome. Thus, we have demonstrated that in the context of the embryonic environment, a dorsalizing signal from the dorsal neural tube can compete with the diffusible ventralizing signal from the notochord. In contrast to dorsal neural tube, pieces of ventral neural tube, dorsal ectoderm or neural crest cells, all of which have been postulated to control dermamyotome formation or to induce myogenesis, either fail to do so or provoke only minimal inductive responses in any of our assays. However, complicating the issue, we find consistent with previous studies that following ablation of the entire neural tube, dermamyotome formation still proceeds adjacent to the dorsal ectoderm. Together these results suggest that, although dorsal ectoderm may be less potent than the dorsal neural tube in inducing dermamyotome, it does nonetheless possess some dermamyotomal-inducing activity. Based on our data and that of others, we propose a model for somite dorsoventral patterning in which competing diffusible signals from the dorsal neural tube and from the notochord/floorplate specify dermamyotome and sclerotome, respectively. In our model, the positioning of the dermamyotome dorsally is due to the absence or reduced levels of the notochord-derived ventralizing signals, as well as to the presence of dominant dorsalizing signals. These dorsal signals are possibly localized and amplified by binding to the basal lamina of the ectoderm, where they can signal the underlying somite, and may also be produced by the ectoderm as well.

Reference

Aoyama
H.
,
Asamoto
K.
(
1988
)
Determination of somite cells:independence of cell differentiation and morphogenesis.
Development
104
,
15
28
Basler
K.
,
Edlund
E.
,
Jessell
T. M.
,
Yamada
T.
(
1993
)
Control of cell pattern in the neural tube: Regulation of cell differentiation by dorsalin-1, a novel TGFβ family member.
Cell
73
,
687
702
Bellairs
R.
(
1963
)
The development of the somites in the chick embryo.
J. Embryol. Exp. Morph
11
,
697
714
Bober
E.
,
Brand-Saberi
B.
,
Ebensperger
C.
,
Wilting
J.
,
Balling
R.
,
Paterson
B. M.
,
Arnold
H.-H.
,
Christ
B.
(
1994
)
Initial steps of myogenesis in somites are independent of influence from axial structures.
Development
120
,
3073
3082
Borman
W. H.
,
Yorde
D. E.
(
1994
)
Barrier inhibition of a temporal neuraxial influence on early chick somitic myogenesis.
Dev. Dynamics
200
,
68
78
Buffinger
N.
,
Stockdale
F. E.
(
1994
)
Myogenic specification in somites: induction by axial structures.
Development
120
,
1443
1452
Christ
B.
,
Brand-Saberi
B.
,
Grim
M.
,
Wilting
J.
(
1992
)
Local signaling in dermomyotomal cell type specification.
Anat. Embryol
186
,
505
510
Erickson
C. A.
,
Goins
T. L.
(
1995
)
Avian neural crest cells can migrate in the dorsolateral path only if they are specified as melanocytes.
Development
121
,
915
924
Erickson
C. A.
,
Duong
T. D.
,
Tosney
K. W.
(
1992
)
Descriptive and experimental analysis of the dispersion of neural crest cells along the dorsolateral path and their entry into ectoderm in the chick embryo.
Dev. Biol
151
,
251
272
Erickson
C. A.
,
Tucker
R. P.
,
Edwards
B. F.
(
1987
)
Changes in the distribution of intermediate-filament types in Japanese quail during morphogenesis.
Differentiation
34
,
88
97
Fan
C.-M.
,
Tessier-Lavigne
M.
(
1994
)
Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog.
Cell
79
,
1175
1186
Goulding
M. D.
,
Lumsden
A.
,
Gruss
P.
(
1993
)
Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord.
Development
117
,
1001
1016
Goulding
M.
,
Lumsden
A.
,
Paquette
A. J.
(
1994
)
Regulation of Pax-3 expression in the dermamyotome and its role in muscle development.
Development
120
,
957
971
Johnson
R. L.
,
Laufer
E.
,
Riddle
R. D.
,
Tabin
C.
(
1994
)
Ectopic expression of Sonic hedgehog alters dorsal-ventral patterning of somites.
Cell
79
,
1165
1173
Kaehn
K.
,
Jacob
H. J.
,
Christ
B.
,
Hinrichsen
K.
,
Poelmann
R. E.
(
1988
)
The onset of myotome formation in the chick.
Anat. Embryol
177
,
191
201
Kenny-Mobbs
T.
,
Thorogood
P.
(
1987
)
Autonomy of differentiation in avian brachial somites and the influence of adjacent tissues.
Development
100
,
449
462
Kosher
R. A.
,
Lash
J. W.
(
1975
)
Notochordal stimulation of in vitro somite chondrogenesis before and after enzymatic removal of perinotochordal materials.
Dev. Biol
42
,
362
378
Kuratani
S.
,
Martin
J. F.
,
Wawersik
S.
,
Lilly
B.
,
Eichele
G.
,
Olson
E. N.
(
1994
)
The expression pattern of the chick homeobox gene gMHox suggests a role in patterning of the limbs and face and in compartmentalization of somites.
Dev. Biol
161
,
357
369
Lash
J.
,
Holtzer
S.
,
Holtzer
H.
(
1957
)
An experimental analysis of the development of the spinal column.
Exp. Cell Res
13
,
292
203
Loring
J. F.
,
Erickson
C. A.
(
1987
)
Neural crest cell migratory pathways in the trunk of the chick embryo.
Dev. Biol
121
,
220
236
Loring
J.
,
Glimelius
R.
,
Erickson
C.
,
Weston
J. A.
(
1981
)
Analysis of developmentally homogeneous neural crest cell populations in vitro. I. Formation, morphology and differentiative behavior.
Dev. Biol
82
,
86
94
Mestres
P.
,
von Hinrichsen
K.
(
1976
)
Zur Histogenese des Somiten beim Huhnchen.
J. Embryol. Exp. Morph
36
,
669
683
Munsterberg
A.E.
,
Lassar
A.B.
(
1995
)
Combinatorial signals from the neural tube, floor plate and notochord induce myogenic bHLH gene expression in the somite.
Development
121
,
651
660
Ordahl
C. P.
,
Le Douarin
N. M.
(
1992
)
Two myogenic lineages within the developing somite.
Development
114
,
339
353
Parr
B. A.
,
Shea
M. J.
,
Vassileva
G.
,
McMahon
A. P.
(
1993
)
Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds.
Development
119
,
247
261
Pourquie
O.
,
Coltey
M.
,
Teillet
M.-A.
,
Ordahl
C.
,
Le Douarin
N. M.
(
1993
)
Control of dorsoventral patterning of somitic derivatives by notochord and floor plate.
Proc. Natl. Acad. Sci.USA
90
,
5242
5246
Pourquie
O.
,
Coltey
M.
,
Breant
C.
,
Le Douarin
N. M.
(
1995
)
Control of somite patterning by signals from the lateral plate.
Proc. Natl. Acad. Sci. USA
92
,
3219
3223
Rong
P.-M.
,
Teillet
M.-A.
,
Ziller
C.
,
Le Douarin
N. M.
(
1992
)
The neural tube/notochord complex is necessary for vertebral but not limb and body wall striated muscle differentiation.
Development
115
,
657
672
Rong
P.-M.
,
Ziller
C.
,
Pena-Melion
A.
,
Le Douarin
N. M.
(
1987
)
A monoclonal antibody specific for avian early myogenic cells and differentiated muscle.
Dev. Biol
122
,
338
353
Stern
C. D.
,
Fraser
S. E.
,
Keynes
R. J.
,
Primmett
D. R. N.
(
1988
)
A cell lineage analysis of segmentation in the chick embryo.
Development
104
,
231
244
Stern
H. M.
,
Hauschka
S. D.
(
1995
)
Neural tube and notochord promote in vitro myogenesis in single somite explants.
Dev. Biol
167
,
87
103
Tosney
K. W.
,
Dehnbostel
D. B.
,
Erickson
C. A.
(
1994
)
Neural crest cells prefer the myotome's basal lamina over the sclerotome as a substratum.
Dev. Biol
163
,
389
406
Tucker
R. P.
,
Erickson
C. A.
(
1984
)
Morphology and behavior of quail neural crest cells in artificial three-dimensional extracellular matrices.
Dev. Biol
104
,
390
405
van Straaten
H. W. M.
,
Hekking
J. W. M.
(
1991
)
Development of floor plate, neurons and axonal outgrowth pattern in the early spinal cord of the notochord-deficient chick embryo.
Anat. Embryol
184
,
55
63
Vivarelli
E.
,
Cossu
G.
(
1986
)
Neural control of early myogenic differentiation in cultures of mouse somites.
Dev. Biol
117
,
319
325
Watterson
R. L.
,
Fowler
I.
,
Fowler
B. J.
(
1954
)
The role of the neural tube and notochord in development of the axial skeleton of the chick embryo.
Am. J. Anat
95
,
337
397
Yip
J. W.
(
1990
)
Identification of location and timing of guidance cues in sympathetic preganglionic axons of the chick.
J. Neurosci
10
,
2476
2484
This content is only available via PDF.