© The Rockefeller University Press,
0021-9525/1999//869 $5.00
The Journal of Cell Biology, Volume 147, Number 4,
, 1999 869-878
Skeletal Myogenic Progenitors Originating from Embryonic Dorsal Aorta Coexpress Endothelial and Myogenic Markers and Contribute to Postnatal Muscle Growth and Regeneration
Luciana De Angelisa,
Libera Berghellaa,
Marcello Colettaa,
Laura Lattanzia,
Malvina Zanchib,
M. Gabriellac,
Carola Ponzettod, and
Giulio Cossua
a Istituto Pasteur-Fondazione Cenci Bolognetti, Dipartimento di Istologia ed Embriologia, Università di Roma, La Sapienza, 00161 Rome, Italy
b Clinica Dermosifilopatica, Policlinico S. Orsola, 40100 Bologna, Italy
c Istituto di Anatomia Umana, Università di Pavia, 27100 Pavia, Italy
d Dipartimento Scienze Mediche, Università del Piemonte Orientale Amedeo Avogadro, 28100 Novara, Italy
Dipartimento di Istologia ed Embriologia, Università di Roma, La Sapienza, Medica Via A, Scarpa 14, 00161 Rome, Italy.3906 446 28543906 4976 6757
cossu{at}axrma.uniroma1.it
Skeletal muscle in vertebrates is derived from somites, epithelial structures of the paraxial mesoderm, yet many unrelated reports describe the occasional appearance of myogenic cells from tissues of nonsomite origin, suggesting either transdifferentiation or the persistence of a multipotent progenitor. Here, we show that clonable skeletal myogenic cells are present in the embryonic dorsal aorta of mouse embryos. This finding is based on a detailed clonal analysis of different tissue anlagen at various developmental stages. In vitro, these myogenic cells show the same morphology as satellite cells derived from adult skeletal muscle, and express a number of myogenic and endothelial markers. Surprisingly, the latter are also expressed by adult satellite cells. Furthermore, it is possible to clone myogenic cells from limbs of mutant c-Met–/– embryos, which lack appendicular muscles, but have a normal vascular system. Upon transplantation, aorta-derived myogenic cells participate in postnatal muscle growth and regeneration, and fuse with resident satellite cells.
The potential of the vascular system to generate skeletal muscle cells may explain observations of nonsomite skeletal myogenesis and raises the possibility that a subset of satellite cells may derive from the vascular system.
Key Words: myogenesis satellite cells endothelial cells multipotent progenitors vascular–endothelial cadherin
© 1999 The Rockefeller University Press
1.used in this paper: β-gal+, β-galactosidase positive; MetD, Met receptor unable to transduce the HGF signal; RT, reverse transcriptase; TA, Tibialis anterior; VE, vascular–endothelial; wt, wild-type
Dr. Berghella's present address is Department of Biology, California Institute of Technology, Pasadena, CA 91125.

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-
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[Full Text]
-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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[Full Text]
-
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54: 1177-1191
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[Full Text]
-
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-
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(2006). Melanoma cell adhesion molecule is a novel marker for human fetal myogenic cells and affects myoblast fusion. J. Cell Sci.
119: 3117-3127
[Abstract]
[Full Text]
-
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(2006). Muscle stem cells in development, regeneration, and disease.. Genes Dev.
20: 1692-1708
[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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[Full Text]
-
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19: 1787-1798
[Abstract]
[Full Text]
-
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186: 21-31
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-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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(2004). Fusion-independent expression of functional ACh receptors in mouse mesoangioblast stem cells contacting muscle cells. J. Physiol.
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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166: 347-357
[Abstract]
[Full Text]
-
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(2004). Msx2 and Necdin Combined Activities Are Required for Smooth Muscle Differentiation in Mesoangioblast Stem Cells. Circ. Res.
94: 1571-1578
[Abstract]
[Full Text]
-
Trounson, A.
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[Abstract]
[Full Text]
-
Gargioli, C., Slack, J. M. W.
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131: 2669-2679
[Abstract]
[Full Text]
-
CHARGE, S. B. P., RUDNICKI, M. A.
(2004). Cellular and Molecular Regulation of Muscle Regeneration. Physiol. Rev.
84: 209-238
[Abstract]
[Full Text]
-
Auda-Boucher, G., Rouaud, T., Fontaine-Perus, J., Le Grand, F., Gardahaut, M.-F.
(2003). Developmental Behavior of Embryonic Myogenic Progenitors Transplanted into Adult Muscle as Revealed by Desmin LacZ Recombinant Gene. J. Histochem. Cytochem.
51: 1255-1267
[Abstract]
[Full Text]
-
Germani, A., Di Carlo, A., Mangoni, A., Straino, S., Giacinti, C., Turrini, P., Biglioli, P., Capogrossi, M. C.
(2003). Vascular Endothelial Growth Factor Modulates Skeletal Myoblast Function. Am. J. Pathol.
163: 1417-1428
[Abstract]
[Full Text]
-
Pesce, M., Orlandi, A., Iachininoto, M. G., Straino, S., Torella, A. R., Rizzuti, V., Pompilio, G., Bonanno, G., Scambia, G., Capogrossi, M. C.
(2003). Myoendothelial Differentiation of Human Umbilical Cord Blood-Derived Stem Cells in Ischemic Limb Tissues. Circ. Res.
93
: e51-e62
[Abstract]
[Full Text]
-
Allen, D. L., Teitelbaum, D. H., Kurachi, K.
(2003). Growth factor stimulation of matrix metalloproteinase expression and myoblast migration and invasion in vitro. Am. J. Physiol. Cell Physiol.
284: C805-C815
[Abstract]
[Full Text]
-
Asakura, A., Seale, P., Girgis-Gabardo, A., Rudnicki, M. A.
(2002). Myogenic specification of side population cells in skeletal muscle. JCB
159: 123-134
[Abstract]
[Full Text]
-
Qu-Petersen, Z., Deasy, B., Jankowski, R., Ikezawa, M., Cummins, J., Pruchnic, R., Mytinger, J., Cao, B., Gates, C., Wernig, A., Huard, J.
(2002). Identification of a novel population of muscle stem cells in mice: potential for muscle regeneration. JCB
157: 851-864
[Abstract]
[Full Text]
-
Tamaki, T., Akatsuka, A., Ando, K., Nakamura, Y., Matsuzawa, H., Hotta, T., R Roy, R., Edgerton, V. R.
(2002). Identification of myogenic-endothelial progenitor cells in the interstitial spaces of skeletal muscle. JCB
157: 571-577
[Abstract]
[Full Text]
-
Grounds, M. D., White, J. D., Rosenthal, N., Bogoyevitch, M. A.
(2002). The Role of Stem Cells in Skeletal and Cardiac Muscle Repair. J. Histochem. Cytochem.
50: 589-610
[Abstract]
[Full Text]
-
Fukada, S.-i., Miyagoe-Suzuki, Y., Tsukihara, H., Yuasa, K., Higuchi, S., Ono, S., Tsujikawa, K., Takeda, S.'i., Yamamoto, H.
(2002). Muscle regeneration by reconstitution with bone marrow or fetal liver cells from green fluorescent protein-gene transgenic mice. J. Cell Sci.
115: 1285-1293
[Abstract]
[Full Text]
-
Minasi, M. G., Riminucci, M., De Angelis, L., Borello, U., Berarducci, B., Innocenzi, A., Caprioli, A., Sirabella, D., Baiocchi, M., De Maria, R., Boratto, R., Jaffredo, T., Broccoli, V., Bianco, P., Cossu, G.
(2002). The meso-angioblast: a multipotent, self-renewing cell that originates from the dorsal aorta and differentiates into most mesodermal tissues. Development
129: 2773-2783
[Abstract]
[Full Text]
-
Gerhart, J., Bast, B., Neely, C., Iem, S., Amegbe, P., Niewenhuis, R., Miklasz, S., Cheng, P. F., George-Weinstein, M.
(2001). MyoD-positive myoblasts are present in mature fetal organs lacking skeletal muscle. JCB
155: 381-392
[Abstract]
[Full Text]
-
Condorelli, G., Borello, U., De Angelis, L., Latronico, M., Sirabella, D., Coletta, M., Galli, R., Balconi, G., Follenzi, A., Frati, G., Cusella De Angelis, M. G., Gioglio, L., Amuchastegui, S., Adorini, L., Naldini, L., Vescovi, A., Dejana, E., Cossu, G.
(2001). Cardiomyocytes induce endothelial cells to trans-differentiate into cardiac muscle: Implications for myocardium regeneration. Proc. Natl. Acad. Sci. USA
10.1073/pnas.191217898v1
[Abstract]
[Full Text]
-
Hawke, T. J., Garry, D. J.
(2001). Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol.
91: 534-551
[Abstract]
[Full Text]
-
Beauchamp, J. R., Heslop, L., Yu, D. S.W., Tajbakhsh, S., Kelly, R. G., Wernig, A., Buckingham, M. E., Partridge, T. A., Zammit, P. S.
(2000). Expression of Cd34 and Myf5 Defines the Majority of Quiescent Adult Skeletal Muscle Satellite Cells. JCB
151: 1221-1234
[Abstract]
[Full Text]
-
Lee, J. Y., Qu-Petersen, Z., Cao, B., Kimura, S., Jankowski, R., Cummins, J., Usas, A., Gates, C., Robbins, P., Wernig, A., Huard, J.
(2000). Clonal Isolation of Muscle-Derived Cells Capable of Enhancing Muscle Regeneration and Bone Healing. JCB
150: 1085-1100
[Abstract]
[Full Text]
-
Graves, D. C., YablonkaReuveni, Z.
(2000). Vascular Smooth Muscle Cells Spontaneously Adopt a Skeletal Muscle Phenotype: A Unique Myf5-/MyoD+ Myogenic Program. J. Histochem. Cytochem.
48: 1173-1194
[Abstract]
[Full Text]
-
Gerhart, J., Baytion, M., DeLuca, S., Getts, R., Lopez, C., Niewenhuis, R., Nilsen, T., Olex, S., Weintraub, H., George-Weinstein, M.
(2000). DNA Dendrimers Localize Myod mRNA in Presomitic Tissues of the Chick Embryo. JCB
149: 825-834
[Abstract]
[Full Text]
-
Ordahl, C. P.
(1999). Myogenic Shape-Shifters. JCB
147: 695-698
[Full Text]
-
Condorelli, G., Borello, U., De Angelis, L., Latronico, M., Sirabella, D., Coletta, M., Galli, R., Balconi, G., Follenzi, A., Frati, G., Cusella De Angelis, M. G., Gioglio, L., Amuchastegui, S., Adorini, L., Naldini, L., Vescovi, A., Dejana, E., Cossu, G.
(2001). From the Cover: Cardiomyocytes induce endothelial cells to trans-differentiate into cardiac muscle: Implications for myocardium regeneration. Proc. Natl. Acad. Sci. USA
98: 10733-10738
[Abstract]
[Full Text]