Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration

Journal of Cell Biology

Volumn 147, Issue 4, 1999, Pages 869-877

  De Angelis, Luciana ^a   Berghella, Libera ^a,e   Coletta, Marcello ^a   Lattanzi, Laura ^a   Zanchi, Malvina ^b   Cusella De Angelis, M Gabriella ^c   Ponzetto, Carola ^d   Cossu, Giulio ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

^d UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^e CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Endothelial cells; Multipotent progenitors; Myogenesis; Satellite cells; Vascular endothelial cadherin

Indexed keywords

CELL MARKER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; DIFFERENTIATION; ENDOTHELIUM CELL; GENE EXPRESSION; MOUSE; MUSCLE DEVELOPMENT; MUSCLE GROWTH; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; SATELLITE CELL; SKELETAL MUSCLE; SOMITE; VERTEBRATE;

AGING; ANIMALS; ANIMALS, NEWBORN; AORTA; BETA-GALACTOSIDASE; EMBRYO; EMBRYONIC AND FETAL DEVELOPMENT; ENDOTHELIUM, VASCULAR; EXTREMITIES; FETAL TISSUE TRANSPLANTATION; GENES, REPORTER; MESODERM; MICE; MICE, SCID; MICE, TRANSGENIC; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; ORGAN CULTURE TECHNIQUES; REGENERATION; STEM CELLS;

ANIMALIA; VERTEBRATA;

EID: 0033571046     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.4.869     Document Type: Article

References (44)

1. Armand, O., A.M. Boutineau, A. Mauger, M.P. Pautou, and M. Kieny. 1983. Origin of satellite cells in avian skeletal muscles. Arch. Anal. Microsc. Morphol. Exp. 72:163-181.
2. Asahara, T., T. Murohara, A. Sullivan, M. Silver, R. van der Zee, T. Li, B. Witzenbichler, G. Schatteman, and J.M. Isner. 1997. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 275:964-967.
3. Bader, D., T. Masaki, and D.A. Fischman. 1982. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 95:763-770.
4. Bianco, P., and G. Cossu. 1999. Uno, nessuno e centomila: searching for the identity of mesodermal progenitors. Exp. Cell Res. 251:257-263.
5. Bischoff, R. 1994. The satellite cell and muscle regeneration. In Myology, 2nd ed. Engel, A.G., and C. Franzini-Armstrong, editors. McGraw-Hill, NY. 97-133.
6. Bladt, F., D. Rethmacher, S. Isenmann, A. Aguzzi, and C. Birchmaier. 1995. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature. 376:768-771.
7. Bober, E., T. Franz, H.H. Arnold, P. Gruss, and P. Tremblay. 1994. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development. 120:603-612.
8. Caplan, A. 1991. Mesenchymal stem cells. J. Orthopaed. Res. 169:641-650.
9. Christ, B., and C.P. Ordhal. 1995. Early stages of chick somite development. Anal. Embryol. 191:381-396.
10. Cooper, R.N., S. Tajbakhsh, V. Mouly, G. Cossu, M. Buckingham, and G.L. Butler-Browne. 1999. Two distinct pathways of satellite cell activation in regenerating mouse skeletal muscle. J. Cell Sci. 112:2895-2901.
11. Cornelison, D.D.W., and B.J. Wold. 1997. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 191:270-283.
12. Cossu, G. 1997. Unorthodox myogenesis: possible developmental significance and implications for tissue histogenesis and regeneration. Histol. Histopathol. 12:755-760.
13. Cossu, G., and M. Molinaro. 1987. Cell heterogeneity in the myogenic lineage. Curr. Topics Dev. Biol. 23:185-208.
14. Cossu, G., F. Eusebi, F. Grassi, and E. Wanke. 1987. Acetylcholine receptor channels are present in undifferentiated satellite cells but not in embryonic myoblasts in culture. Dev. Biol. 123:43-50.
15. Cossu, G., S. Tajbakhsh, and M. Buckingham. 1996a. How is myogenesis initiated in the embryo? Trends Genet. 12:218-223.
16. Cossu, G., R. Kelly, S. Tajbakhsh, S. Di Donna, E. Vivarelli, and M. Buckingham. 1996b. Activation of different myogenic pathways: Myf-5 is induced by the neural tube and MyoD by the dorsal ectoderm in mouse paraxial mesoderm. Development. 122:429-437.
17. Cusella-De Angelis, M.G., S. Molinari, A. Ledonne, M. Coletta, E. Vivarelli, M. Bouche, M. Molinaro, S. Ferrari, and G. Cossu. 1994. Differential response of embryonic and fetal myoblasts to TGFβ: a possible regulatory mechanism of skeletal muscle histogenesis. Development. 120:925-933.
18. Denetclaw, W.F., B. Christ, and C.P. Ordhal. 1997. Location and growth of epaxial myotome precursor cells. Development. 124:1601-1610.
19. Ferrari, G., M.G. Cusella-De Angelis, M. Coletta, A. Stornaioulo, E. Paolucci, G. Cossu, and F. Mavilio. 1998. Muscle regeneration by bone marrow-derived myogenic progenitors. Science. 279:1528-1530.
20. Ferrari, S., S. Molinari, R. Melchionna, M.G. Cusella-De Angelis, R. Battini, R. Kelly, and G. Cossu. 1997. Absence of MEF2 binding to the A/T-rich element in the muscle creatine kinase (MCK) enhancer correlates with lack of early expression of the MCK gene in embryonic mammalian muscle. Cell Growth Differ. 8:23-34.
21. Flamme, I., and W. Risau. 1992. Induction of vasculogenesis and hematopoiesis in vitro. Development. 116:435-439.
22. Garry, D.J., Q. Yang, R. Bassel-Duby, and R.S. Williams. 1997. Persistent expression of MNF identifies myogenic stem cells in postnatal muscle. Dev. Biol. 188:280-294.
23. Gibson, A.J., J. Karasinski, J. Relvas, J. Moss, T.G. Sherratt, P.N. Strong, and D.J. Watt. 1995. Dermal fibroblasts convert to a myogenic lineage in mdx mouse muscle. J. Cell Sci. 108:207-214.
24. Goulding, M., A. Lumsden, and A.J. Paquette. 1994. Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development. 120:957-971.
25. Grigoriadis, A.E., J. Heersche, and J.E. Aubin. 1988. Differentiation of muscle, fat, cartilage, and bone from progenitor cells present in a bone-derived clonal cell population: effect of dexamethasone. J. Cell Biol. 196:2139-2151.
26. Hatzopoulos, A.K., J. Folkman, E. Vasile, G.K. Eiselen, and R.D. Rosenberg. 1998. Isolation and characterization of endothelial progenitor cells from mouse embryos. Development. 125:1457-1468.
27. Irintchev, A., M. Zeschnigk, A. Starzinski-Powitz, and A Wernig. 1994. Expression pattern of M-cadherin in normal, denervated, and regenerating mouse muscles. Dev. Dyn. 199:326-337.
28. Kahane, N., Y. Cinnamon, and C. Kalcheim. 1998. The origin and fate of pioneer myotomal cells in the avian embryo. Mech. Dev. 74:59-73.
29. Katagiri, T., A. Yamaguchi, M. Komaki, E. Abe, N. Takahashi, T. Ikeda, V. Rosen, J.M. Wozney, A. Fujisawa-Sehara, and T. Suda. 1994. Bone morphogenetic protein-2 coverts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell Biol. 127:1755-1766.
30. Kelly, R., S. Alonso, S. Tajbakhsh, G. Cossu, and M. Buckingham. 1995. Myosin light chain 3F regulatory sequences confer regionalised cardiac and skeletal muscle expression in transgenic mice. J. Cell Biol. 129:383-396.
31. Koishi, K., M. Zhang, I.S. McLennan, and A.J. Harris. 1995. MyoD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Dev. Dyn. 202:244-254.
32. Lagrand, F., I. Khazaal, M. Peuchmaur, O. Fenneteau, H. Cave, P. Rohrlich, E. Vilmer, and B. Peault. 1997. Long-term malignant hematopoiesis in human acute leukemia bone marrow biopsies implanted in severe combined immunodeficiency mice. Blood. 90:2001-2009.
33. Maina, F., F. Casagrande, E. Audero, A. Simeone, P.M. Comoglio, R. Klein, and C. Ponzetto. 1996. Uncoupling of Grb2 from the Met receptor in vivo reveals complex roles in muscle development. Cell. 87:531-542.
34. Mayer, D.C., and L.A. Leinwand. 1997. Sarcomeric gene expression and contractility in myofibroblasts. J. Cell Boil. 139:1477-1484.
35. Megeney, L.A., B. Kabkar, K. Garrett, J. Anderson, and M.A. Rudnicki. 1996. MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev. 10:1173-1183.
36. Pardanaud, L., D. Luton, M. Prigent, L.M. Bourcheix, M. Catala, and F. Dieterlen-Lievre. 1996. Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development. 122:1363-1371.
37. Patapoutian, A., B.J. Wold, and R. Wagner. 1995. Evidence for developmentally programmed transdifferentiation in mouse esophageal muscle. Science. 270:1818-1821.
38. Prockop, DJ. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 276:71-74.
39. Salvatori, G., L. Lattanzi, M. Coletta, S. Aguanno, E. Vivarelli, R. Kelly, G. Ferrari, A.J. Harris, F. Mavilio, M. Molinaro, and G. Cossu. 1995. Myogenic conversion of mammalian fibroblasts induced by differentiating muscle cells. J. Cell Sci. 108:2733-2739.
40. Solursh, M., C. Drake, and S. Meier. 1987. The migration of myogenic cells from the somites at the wing level in avian embryos. Dev. Biol. 121:389-396.
41. Sugi, Y., and R.R. Markwald. 1996. Formation and early morphogenesis of endocardial endothelial precursor cells and the role of endoderm. Dev. Biol. 175:66-83.
42. Tajbakhsh, S., E. Vivarelli, M.G. Cusella-De Angelis, D. Rocancourt, M. Buckingham, and G. Cossu. 1994. A population of myogenic cells derived from the mouse neural tube. Neuron. 13:813-821.
43. Tajbakhsh, S., D. Rocancourt, and M. Buckingham. 1996. Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in Myf-5 null mice. Nature. 384:266-270.
44. Tajbakhsh, S., D. Rocancourt, G. Cossu, and M. Buckingham. 1997. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell. 89:127-138.