Chimeras were prepared by transplanting somites from 9-day post-coitum mouse embryos or somitic dermomyotomes from 10-day post-coitum mouse embryos into 2-day-old chick embryos at different axial levels. Mouse somitic cells then differentiated in ovo in dermis, cartilage and skeletal muscle as they normally do in the course of development and were able to migrate into chick host limb. To trace the behavior of somitic myogenic stem cells more closely, somites arising from mice bearing a transgene of the desmin gene linked to a reporter gene coding for Escherichia coli beta-galactosidase (lacZ) were grafted in ovo. Interestingly, the transgene was rapidly expressed in myotomal muscles derived from implants. In the limb muscle mass, positive cells were found several days after implantation. Activation of desmin nls lacZ also occurred in in vitro cultures of somite-derived cells. Our experimental method facilitates investigation of the mechanisms of mammalian development, allowing the normal fate of implanted mouse cells to be studied and providing suitable conditions for identification of descendants of genetically modified cells.
Reference
Aoyama
H.
, Asamoto
K.
(1988
) Determination of somite cells: independence of cell differentiation and morphogenesis.
Development
104
, 15
–28
Auda-Boucher
G.
, Fontaine-Perus
J.
(1994
) Differentiation potentialities of distinct myogenic cell precursors in avian embryos.
Dev. Dyn
201
, 95
–107
Babai
F.
, Musevi-Aghdam
J.
, Schurch
W.
, Royal
A.
, Gabbiani
G.
(1990
) Coexpression of-sarcomeric actin, -smooth muscle actin and desmin during myogenesis in rat and mouse embryos.
I. Skeletal muscle. Differentiation
44
, 1382
–142
Beddington
R. S. P.
, Martin
P.
(1989
) An in situ transgenic enzyme marker to monitor migration of cells in the mid-gestation mouse embryo: somite contribution to the limb.
Mol. Biol. Med
6
, 263
–274
Beresford
B.
(1983
) Brachial muscles in the chick embryo: the fate of individual somites.
J. Embryol. Exp. Morph
77
, 99
–116
Bober
E.
, Lyons
G. E.
, Braun
T.
, Cossu
G.
, Buckingham
M.
, Arnold
H. H.
(1991
) The muscle regulatory gene, myf-6 has a biphasic pattern of expression during early mouse development.
J. Cell Biol
133
, 1255
–1265
Bober
E.
, Franz
T.
, Arnold
H. H.
, Gruss
P.
, Tremblay
J. P.
(1994
) Pax3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells.
Development
120
, 603
–612
Borman
W. H.
, Yorde
D. E.
(1994
) Analysis of chick somite myogenesis by in situ confocal microscopy of desmin expression.
J. Histochem. Cytochem
42
, 265
–272
Borman
W. H.
, Urlakis
K. J.
, Yorde
D. E.
(1994
) Analysis of the in vivo myogenesis status of chick somites by desmin expression in vitro.
Dev. Dyn
199
, 268
–279
Braun
T.
, Rudnicki
M.
, Arnold
H.
, Jaenisch
R.
(1992
) Targeted inactivation of the muscle regulatory gene myf-5 results in abnormal rib development and perinatal death.
Cell
71
, 369
–382
Cheng
T. S.
, Hanley
T. A.
, Mudd
J.
, Merlie
J. P.
, Olson
E. N.
(1992
) Mapping of myogenin transcription during embryogenesis using transgenes linked to the myogenin control region.
J. Cell Biol
119
, 1649
–1656
Chevallier
A.
(1977
) Origine des ceintures scapulaires et pelviennes chez l'embryon d'oiseau.
J. Embryol. Exp. Morph
42
, 275
–292
Chevallier
A.
, Kieny
M.
, Mauger
A.
(1977
) Limb-somite relationship: origin of the limb musculature.
J. Embryol. Exp. Morph
41
, 245
–258
Chevallier
A.
, Kieny
M.
, Mauger
A.
(1978
) Limb-somite relationship: effect of removal of somitic mesoderm on the wing musculature.
J. Embryol. Exp. Morph
43
, 263
–278
Christ
B.
, Jacob
H.
, Jacob
M.
(1977
) Experimental analysis of the origin of the wing musculature in avian embryos.
Anat. Embryol
150
, 171
–186
Christ
B.
, Jacob
H.
, Jacob
M.
(1978
) On the formation of the myotomes in avian embryos. An experimental and scanning electron microscope study.
Experientia
34
, 514
–516
Emerson
C. P.
(1990
) Myogenesis and developmental control genes.
Curr. Op. Gen. Dev
2
, 1065
–1075
Emerson
C. P.
(1993
) Skeletal myogenesis: genetics and embryology to the fore.
Curr. Op. Gen. Dev
3
, 265
–274
Fontaine-Perus
J.
, Chanconie
M.
, Le Douarin
N. M.
(1985
) Embryonic origin of substance P-containing neurons in cranial and spinal sensory ganglia.
Dev. Biol
107
, 227
–238
Franz
T.
(1993
) The Splotch (Sp1H) and Splotch-delayed (Spd) alleles: differential phenotypic effects on neural crest and limb musculature.
Anat. Embryol
187
, 371
–377
Franz
T.
, Kothary
R.
, Surani
M. A.
, Halata
Z.
, Grim
M.
(1993
) The Splotch mutation interferes with muscle development in the limbs.
Anat. Embryol
187
, 153
–160
Geisler
N.
, Weber
K.
(1982
) The amino acid sequence of chicken muscle desmin provides a common structural model for intermediate filament proteins.
EMBO J
1
, 1649
–1656
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. L.
(1951
) A series of normal stages in the development of the chick embryo.
J. Morph
88
, 49
–92
Hasty
P.
, Bradley
A.
, Morris
J. H.
, Edmonson
D. G.
, Venuti
J. M.
, Olson
E. N.
, Klein
W. H.
(1993
) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene.
Nature
364
, 501
–506
Hinterberger
J. T.
, Sassoon
D. A.
, Rhodes
S. J.
, Konieczny
S. F.
(1991
) Expression of the muscle regulatory factor MRF4 during somite and skeletal myofiber development.
Dev. Biol
147
, 144
–156
Laframboise
W. A.
, Daood
M. J.
, Guthrie
R. D.
, Schiaffino
S.
, Moretti
L.
, Brozanski
B.
, Ontell
M. P.
, Butler-Browne
G. S.
, Whalen
R. G.
, Ontell
M.
(1991
) Emergence of a mature myosin phenotype in the rat diaphragm muscle.
Dev. Biol
144
, 1
–15
Lazarides
E.
, Hubbard
B. D.
(1976
) Immunological characterization of the subunit of the 1OO A filaments from muscle cells.
Proc. Natl. Acad. Sci. USA
73
, 4344
–4348
Lee
K. H.
, Sze
L. Y.
(1993
) Role of the brachial somites in the development of appendicular musculature in rat embryos.
Dev. Dyn
198
, 86
–93
Li
Z.
, Marchand
P.
, Babinet
C.
, Paulin
D.
(1993
) Desmin sequence elements regulating skeletal muscle-specific expression in transgenic mice.
Development
117
, 947
–959
Lyons
G. E.
, Ontell
M.
, Cox
R.
, Sassoon
D.
, Buckingham
M.
(1990
) The expression of myosin genes in developing skeletal muscle in the mouse embryo.
J. Cell Biol
111
, 1465
–1476
Mayo
M.
, Brinbas
M.
, Santos
V.
, Shum
L.
, Slavkin
H. C.
(1992
) Desmin expression during early mouse tongue morphogenesis.
J. Dev. Biol
36
, 255
–263
Moscona
A.
(1957
) The development in vitro of chimeric aggregates of dissociated embryonic chick and mouse cells.
Proc. Natl. Acad. Sci. USA
43
, 184
–194
Nabeshima
Y.
, Hanaoka
K.
, Hayasaka
M.
, Esumi
E.
, Li
S.
, Nonaka
I.
, Nabeshima
Y.
(1993
) Myogenein gene disruption results in perinatal lethality because of severe defect.
Nature
364
, 532
–535
Olson
E. N.
(1992
) Interplay between proliferation and differentiation within the myogenic lineage.
Dev. Biol
154
, 261
–272
Ordahl
C. P.
, Le Douarin
N.M.
(1992
) Two myogenic lineages within the developing somite.
Development
114
, 339
–353
Ott
M.
, Bober
E.
, Lyons
G.
, Arnold
H.
, Buckingham
M.
(1991
) Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo.
Development
111
, 1097
–1107
Rudnicki
M. A.
, Braun
T.
, Hinuma
S.
, Jaenisch
R.
(1992
) Inactivation of MyoD in mice leads to up-regulation of the myogenic HLHgene myogenin and results in apparently normal muscle development.
Cell
71
, 383
–390
Rudnicki
M. A.
, Schnegelsberg
P. N.
, Stead
R. H.
, Braun
T.
, Arnold
H. H.
, Jaenish
R.
(1993
) MyoD or Myf5 is required for the formation of skeletal muscle.
Cell
15
, 1531
–1539
Sassoon
D.
, Lyons
G.
, Wright
W. E.
, Lin
V.
, Lassar
A.
, Weintraub
H.
, Buckingham
M.
(1989
) Expression of two myogenic regulatory factors myogenin and MyoD during mouse embryogenesis.
Nature
341
, 303
–307
Small
J. V.
, Sobieszek
A.
(1977
) Studies on the function and composition of the 10-nm (100-A) filaments of vertebrate smooth muscle.
J. Cell Sci
23
, 243
–268
Tajbakhsh
S.
, Buckingham
M.
(1994
) Mouse limb muscle is determined in the absence of the earliest myogenic factor Myf5.
Proc. Natl. Acad. Sci. USA
91
, 747
–751
Tam
P. P. L.
(1981
) The control of somitogenesis in mouse embryos.
J. Embryol. Exp. Morph
65
, 103
–128
Williams
B. A.
, Ordahl
C.
(1994
) Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification.
Development
120
, 785
–796
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