Pax3 regulation of FGF signaling affects the progression of embryonic progenitor cells into the myogenic program

Genes and Development

Volumn 22, Issue 13, 2008, Pages 1828-1837

  Lagha, Mounia ^a   Kormish, Jay D ^a,c   Rocancourt, Didier ^a   Manceau, Marie ^a,d   Epstein, Jonathan A ^a,e   Zaret, Kenneth S ^a,c   Relaix, Frédéric ^a,b   Buckingham, Margaret E ^a  

^a INSTITUT PASTEUR   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c FOX CHASE CANCER CENTER   (United States)

^d AIX MARSEILLE UNIVERSITÉ   (France)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Embryonic ChIP on chip; Fgfr4; Myogenesis; Pax3; Skeletal muscle progenitor cells; Somite; Sprouty1

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 4; SPROUTY PROTEIN; TRANSCRIPTION FACTOR PAX3;

ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; E BOX ELEMENT; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; GENE; GENE LOCUS; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SOMITE; TRANSGENIC MOUSE;

3' FLANKING REGION; AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; FIBROBLAST GROWTH FACTORS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; MYOBLASTS; PAIRED BOX TRANSCRIPTION FACTORS; PHOSPHOPROTEINS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 4; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION;

MUS MUSCULUS;

EID: 46249087227     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.477908     Document Type: Article

References (36)

1. Bajard, L., Relaix, F., Lagha, M., Rocancourt, D., Daubas, P., and Buckingham, M.E. 2006. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes & Dev. 20: 2450-2464.
2. Basson, M.A., Echevarria, D., Petersen Ahn, C., Sudarov, A., Joyner, A.L., Mason, I.J., Martinez, S., and Martin, G.R. 2008. Specific regions within the embryonic midbrain and cerebellum require different levels of FGF signaling during development. Development 135: 889-898.
3. Ben-Yair, R. and Kalcheim, C. 2005. Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development 132: 689-701.
4. Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A., and Birchmeier, C. 1995. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376: 768-771.
5. Buckingham, M. 2006. Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr. Opin. Genet. Dev. 16: 525-532.
6. Buckingham, M. and Relaix, F. 2007. The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu. Rev. Cell Dev. Biol. 23: 645-673.
7. Calmont, A., Wandzioch, E., Tremblay, K.D., Minowada, G., Kaestner, K.H., Martin, G.R., and Zaret, K.S. 2006. An FGF response pathway that mediates hepatic gene induction in embryonic endoderm cells. Dev. Cell 11: 339-348.
8. Edom-Vovard, F., Bonnin, M.A., and Duprez, D. 2001. Misexpression of Fgf-4 in the chick limb inhibits myogenesis by down-regulating Frek expression. Dev. Biol. 233: 56-71.
9. Engleka, K.A., Gitler, A.D., Zhang, M., Zhou, D.D., High, F.A., and Epstein, J.A. 2005. Insertion of Cre into the Pax3 locus creates a new allele of Splotch and identifies unexpected Pax3 derivatives. Dev. Biol. 280: 396-406.
10. Epstein, J.A., Shapiro, D.N., Cheng, J., Lam, P.Y., and Maas, R.L. 1996. Pax3 modulates expression of the c-Met receptor during limb muscle development. Proc. Natl. Acad. Sci. 93: 4213-4218.
11. Fukada, S., Uezumi, A., Ikemoto, M., Masuda, S., Segawa, M., Tanimura, N., Yamamoto, H., Miyagoe-Suzuki, Y., and Takeda, S. 2007. Molecular signature of quiescent satellite cells in adult skeletal muscle. Stem Cells 25: 2448-2459.
12. Gayraud-Morel, B., Chretien, F., Flamant, P., Gomes, D., Zammit, P.S., and Tajbakhsh, S. 2007. A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. Dev. Biol. 312: 13-28.
13. Giordani, J., Bajard, L., Demignon, J., Daubas, P., Buckingham, M., and Maire, P. 2007. Six proteins regulate the activation of Myf5 expression in embryonic mouse limbs. Proc. Natl. Acad. Sci. 104: 11310-11315.
14. Hacohen, N., Kramer, S., Sutherland, D., Hiromi, Y., and Krasnow, M.A. 1998. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92: 253-263.
15. Hadchouel, J., Tajbakhsh, S., Primig, M., Chang, T.H., Daubas, P., Rocancourt, D., and Buckingham, M. 2000. Modular long-range regulation of Myf5 reveals unexpected heterogeneity between skeletal muscles in the mouse embryo. Development 127: 4455-4467.
16. Hammond, C.L., Hinits, Y., Osborn, D.P., Minchin, J.E., Tettamanti, G., and Hughes, S.M. 2007. Signals and myogenic regulatory factors restrict pax3 and pax7 expression to dermomyotome-like tissue in zebrafish. Dev. Biol. 302: 504-521.
17. Hanafusa, H., Torii, S., Yasunaga, T., and Nishida, E. 2002. Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 4: 850-858.
18. Kastner, S., Elias, M.C., Rivera, A.J., and Yablonka-Reuveni, Z. 2000. Gene expression patterns of the fibroblast growth factors and their receptors during myogenesis of rat satellite cells. J. Histochem. Cytochem. 48: 1079-1096.
19. Kim, H.J. and Bar-Sagi, D. 2004. Modulation of signalling by Sprouty: A developing story. Nat. Rev. Mol. Cell Biol. 5: 441-450.
20. Klein, O.D., Lyons, D.B., Balooch, G., Marshall, G.W., Basson, M.A., Peterka, M., Boran, T., Peterkova, R., and Martin, G.R. 2008. An FGF signaling loop sustains the generation of differentiated progeny from stem cells in mouse incisors. Development 135: 377-385.
21. Lindon, C., Albagli, O., Domeyne, P., Montarras, D., and Pinset, C. 2000. Constitutive instability of muscle regulatory factor Myf5 is distinct from its mitosis-specific disappearance, which requires a D-box-like motif overlapping the basic domain. Mol. Cell. Biol. 20: 8923-8932.
22. MacArthur, C.A., Lawshe, A., Xu, J., Santos-Ocampo, S., Heikinheimo, M., Chellaiah, A.T., and Ornitz, D.M. 1995. FGF-8 isoforms activate receptor splice forms that are expressed in mesenchymal regions of mouse development. Development 121: 3603-3613.
23. Marcelle, C., Wolf, J., and Bronner-Fraser, M. 1995. The in vivo expression of the FGF receptor FREK mRNA in avian myoblasts suggests a role in muscle growth and differentiation. Dev. Biol. 172: 100-114.
24. Marics, I., Padilla, F., Guillemot, J.F., Scaal, M., and Marcelle, C. 2002. FGFR4 signaling is a necessary step in limb muscle differentiation. Development 129: 4559-4569.
25. Relaix, F., Polimeni, M., Rocancourt, D., Ponzetto, C., Schafer, B.W., and Buckingham, M. 2003. The transcriptional activator PAX3-FKHR rescues the defects of Pax3 mutant mice but induces a myogenic gain-of-function phenotype with ligand-independent activation of Met signaling in vivo. Genes & Dev. 17: 2950-2965.
26. Relaix, F., Rocancourt, D., Mansouri, A., and Buckingham, M. 2004. Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes & Dev. 18: 1088-1105.
27. Relaix, F., Rocancourt, D., Mansouri, A., and Buckingham, M. 2005. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435: 948-953.
28. Shim, K., Minowada, G., Coling, D.E., and Martin, G.R. 2005. Sprouty2, a mouse deafness gene, regulates cell fate decisions in the auditory sensory epithelium by antagonizing FGF signaling. Dev. Cell 8: 553-564.
29. Stark, K.L., McMahon, J.A., and McMahon, A.P. 1991. FGFR-4, a new member of the fibroblast growth factor receptor family, expressed in the definitive endoderm and skeletal muscle lineages of the mouse. Development 113: 641-651.
30. Tajbakhsh, S. and Cossu, G. 1997. Establishing myogenic identity during somitogenesis. Curr. Opin. Genet. Dev. 7: 634-641.
31. Taketomi, T., Yoshiga, D., Taniguchi, K., Kobayashi, T., Nonami, A., Kato, R., Sasaki, M., Sasaki, A., Ishibashi, H., Moriyama, M., et al. 2005. Loss of mammalian Sprouty2 leads to enteric neuronal hyperplasia and esophageal achalasia. Nat. Neurosci. 8: 855-857.
32. von Scheven, G., Alvares, L.E., Mootoosamy, R.C., and Dietrich, S. 2006. Neural tube derived signals and Fgf8 act antagonistically to specify eye versus mandibular arch muscles. Development 133: 2731-2745.
33. Weinstein, M., Xu, X., Ohyama, K., and Deng, C.X. 1998. FGFR-3 and FGFR-4 function cooperatively to direct alveogenesis in the murine lung. Development 125: 3615-3623.
34. Wiebe, P.O., Kormish, J.D., Roper, V.T., Fujitani, Y., Alston, N.I., Zaret, K.S., Wright, C.V., Stein, R.W., and Gannon, M. 2007. Ptf1a binds to and activates area III, a highly conserved region of the Pdx1 promoter that mediates early pancreas-wide Pdx1 expression. Mol. Cell. Biol. 27: 4093-4104.
35. Zhao, P. and Hoffman, E.P. 2004. Embryonic myogenesis pathways in muscle regeneration. Dev. Dyn. 229: 380-392.
36. Zhao, P., Caretti, G., Mitchell, S., McKeehan, W.L., Boskey, A.L., Pachman, L.M., Sartorelli, V., and Hoffman, E.P. 2006. Fgfr4 is required for effective muscle regeneration in vivo. Delineation of a MyoD-Tead2-Fgfr4 transcriptional pathway. J. Biol. Chem. 281: 429-438.