|
|
|
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
Development, Vol 126, Issue 18 4053-4063, Copyright © 1999 by Company of Biologists
JOURNAL ARTICLES |
AG Borycki, B Brunk, S Tajbakhsh, M Buckingham, C Chiang and CP Emerson
Department of Cell Biology, University of Pennsylvania School of Medicine, Philadelphia, PA 19104-6058, USA.
Sonic hedgehog (Shh), produced by the notochord and floor plate, is proposed to function as an inductive and trophic signal that controls somite and neural tube patterning and differentiation. To investigate Shh functions during somite myogenesis in the mouse embryo, we have analyzed the expression of the myogenic determination genes, Myf5 and MyoD, and other regulatory genes in somites of Shh null embryos and in explants of presomitic mesoderm from wild-type and Myf5 null embryos. Our findings establish that Shh has an essential inductive function in the early activation of the myogenic determination genes, Myf5 and MyoD, in the epaxial somite cells that give rise to the progenitors of the deep back muscles. Shh is not required for the activation of Myf5 and MyoD at any of the other sites of myogenesis in the mouse embryo, including the hypaxial dermomyotomal cells that give rise to the abdominal and body wall muscles, or the myogenic progenitor cells that form the limb and head muscles. Shh also functions in somites to establish and maintain the medio-lateral boundaries of epaxial and hypaxial gene expression. Myf5, and not MyoD, is the target of Shh signaling in the epaxial dermomyotome, as MyoD activation by recombinant Shh protein in presomitic mesoderm explants is defective in Myf5 null embryos. In further support of the inductive function of Shh in epaxial myogenesis, we show that Shh is not essential for the survival or the proliferation of epaxial myogenic progenitors. However, Shh is required specifically for the survival of sclerotomal cells in the ventral somite as well as for the survival of ventral and dorsal neural tube cells. We conclude, therefore, that Shh has multiple functions in the somite, including inductive functions in the activation of Myf5, leading to the determination of epaxial dermomyotomal cells to myogenesis, as well as trophic functions in the maintenance of cell survival in the sclerotome and adjacent neural tube.
This article has been cited by other articles:
|
|
 |
|
  H. Ochi, S. Hans, and M. Westerfield Smarcd3 Regulates the Timing of Zebrafish Myogenesis Onset J. Biol. Chem., February 8, 2008; 283(6): 3529 - 3536. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Buchberger, D. Freitag, and H.-H. Arnold A homeo-paired domain-binding motif directs Myf5 expression in progenitor cells of limb muscle Development, March 15, 2007; 134(6): 1171 - 1180. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Gerhart, J. Elder, C. Neely, J. Schure, T. Kvist, K. Knudsen, and M. George-Weinstein MyoD-positive epiblast cells regulate skeletal muscle differentiation in the embryo J. Cell Biol., October 23, 2006; 175(2): 283 - 292. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Borello, B. Berarducci, P. Murphy, L. Bajard, V. Buffa, S. Piccolo, M. Buckingham, and G. Cossu The Wnt/{beta}-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis Development, September 15, 2006; 133(18): 3723 - 3732. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. G. Davey, I. R. Paton, Y. Yin, M. Schmidt, F. K. Bangs, D. R. Morrice, T. G. Smith, P. Buxton, D. Stamataki, M. Tanaka, et al. The chicken talpid3 gene encodesa novel protein essentialfor Hedgehog signaling. Genes & Dev., May 15, 2006; 20(10): 1365 - 1377. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. M. Riccomagno, S. Takada, and D. J. Epstein Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh Genes & Dev., July 1, 2005; 19(13): 1612 - 1623. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. McDermott, M. Gustafsson, T. Elsam, C.-C. Hui, C. P. Emerson Jr, and A.-G. Borycki Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation Development, January 15, 2005; 132(2): 345 - 357. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Miura, H. Kato, Y. Kusakabe, M. Tagami, J. Miura-Ohnuma, Y. Ninomiya, and A. Hino A Strong Nerve Dependence of Sonic hedgehog Expression in Basal Cells in Mouse Taste Bud and an Autonomous Transcriptional Control of Genes in Differentiated Taste Cells Chem Senses, November 1, 2004; 29(9): 823 - 831. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Grimaldi, G. Tettamanti, B. L. Martin, W. Gaffield, M. E. Pownall, and S. M. Hughes Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis Development, July 15, 2004; 131(14): 3249 - 3262. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Komaki, A. Asakura, M. A. Rudnicki, J. Sodek, and S. Cheifetz MyoD enhances BMP7-induced osteogenic differentiation of myogenic cell cultures J. Cell Sci., March 15, 2004; 117(8): 1457 - 1468. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Teboul, D. Summerbell, and P. W.J. Rigby The initial somitic phase of Myf5 expression requires neither Shh signaling nor Gli regulation Genes & Dev., December 1, 2003; 17(23): 2870 - 2874. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Auda-Boucher, T. Rouaud, J. Fontaine-Perus, F. Le Grand, and M.-F. Gardahaut Developmental Behavior of Embryonic Myogenic Progenitors Transplanted into Adult Muscle as Revealed by Desmin LacZ Recombinant Gene J. Histochem. Cytochem., October 1, 2003; 51(10): 1255 - 1267. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. D. Sacks, G. M. Cann, W. Nikovits Jr, S. Conlon, N. R. Espinoza, and F. E. Stockdale Regulation of myosin expression during myotome formation Development, August 1, 2003; 130(15): 3391 - 3402. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Hadchouel, J. J. Carvajal, P. Daubas, L. Bajard, T. Chang, D. Rocancourt, D. Cox, D. Summerbell, S. Tajbakhsh, P. W. J. Rigby, et al. Analysis of a key regulatory region upstream of the Myf5 gene reveals multiple phases of myogenesis, orchestrated at each site by a combination of elements dispersed throughout the locus Development, August 1, 2003; 130(15): 3415 - 3426. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Buchberger, N. Nomokonova, and H.-H. Arnold Myf5 expression in somites and limb buds of mouse embryos is controlled by two distinct distal enhancer activities Development, July 15, 2003; 130(14): 3297 - 3307. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Ishibashi and A. P. McMahon A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mesencephalic primordia in the early mouse embryo Development, March 12, 2003; 129(20): 4807 - 4819. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. J. Venters and C. P. Ordahl Persistent myogenic capacity of the dermomyotome dorsomedial lip and restriction of myogenic competence Development, March 10, 2003; 129(16): 3873 - 3885. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y.-S. Kim, M. Lewandoski, A. O. Perantoni, S. Kurebayashi, G. Nakanishi, and A. M. Jetten Identification of Glis1, a Novel Gli-related, Kruppel-like Zinc Finger Protein Containing Transactivation and Repressor Functions J. Biol. Chem., August 16, 2002; 277(34): 30901 - 30913. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Zeng, H. Kempf, L. C. Murtaugh, M. E. Sato, and A. B. Lassar Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is maintained by BMP signals to induce somitic chondrogenesis Genes & Dev., August 1, 2002; 16(15): 1990 - 2005. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Teboul, J. Hadchouel, P. Daubas, D. Summerbell, M. Buckingham, and P. W. J. Rigby The early epaxial enhancer is essential for the initial expression of the skeletal muscle determination gene Myf5 but not for subsequent, multiple phases of somitic myogenesis Development, January 10, 2002; 129(19): 4571 - 4580. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. K. Gustafsson, H. Pan, D. F. Pinney, Y. Liu, A. Lewandowski, D. J. Epstein, and C. P. Emerson Jr. Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification Genes & Dev., January 1, 2002; 16(1): 114 - 126. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-B. Charrier, F. Lapointe, N. M. L. Douarin, and M.-A. Teillet Anti-apoptotic role of Sonic hedgehog protein at the early stages of nervous system organogenesis Development, October 15, 2001; 128(20): 4011 - 4020. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. E. Lewis and J. S. Eisen Hedgehog signaling is required for primary motoneuron induction in zebrafish Development, September 15, 2001; 128(18): 3485 - 3495. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. K. Dhoot, M. K. Gustafsson, X. Ai, W. Sun, D. M. Standiford, and C. P. Emerson Jr. Regulation of Wnt Signaling and Embryo Patterning by an Extracellular Sulfatase Science, August 31, 2001; 293(5535): 1663 - 1666. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Kahane, Y. Cinnamon, I. Bachelet, and C. Kalcheim The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development Development, June 15, 2001; 128(12): 2187 - 2198. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Ordahl, E Berdougo, S. Venters, and W. Denetclaw The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium Development, January 5, 2001; 128(10): 1731 - 1744. [Abstract] [PDF]
|
|
|
|
|
|
M Kruger, D Mennerich, S Fees, R Schafer, S Mundlos, and T Braun Sonic hedgehog is a survival factor for hypaxial muscles during mouse development Development, January 3, 2001; 128(5): 743 - 752. [Abstract] [PDF]
|
|
|
|
|
|
A. Borycki, A. M. Brown, and C. P. Emerson Shh and Wnt signaling pathways converge to control Gli gene activation in avian somites Development, May 15, 2000; 127(10): 2075 - 2087. [Abstract] [PDF]
|
|
|
|
|
|
J Hadchouel, S Tajbakhsh, M Primig, T. Chang, P Daubas, D Rocancourt, and M Buckingham Modular long-range regulation of Myf5 reveals unexpected heterogeneity between skeletal muscles in the mouse embryo Development, January 10, 2000; 127(20): 4455 - 4467. [Abstract] [PDF]
|
|
|
|
|
|
D Summerbell, P. Ashby, O Coutelle, D Cox, S Yee, and P. Rigby The expression of Myf5 in the developing mouse embryo is controlled by discrete and dispersed enhancers specific for particular populations of skeletal muscle precursors Development, January 9, 2000; 127(17): 3745 - 3757. [Abstract] [PDF]
|
|
|
|
|
|
H. Park, C Bai, K. Platt, M. Matise, A Beeghly, C. Hui, M Nakashima, and A. Joyner Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation Development, January 4, 2000; 127(8): 1593 - 1605. [Abstract] [PDF]
|
|
|
|
|
|
P Daubas, S Tajbakhsh, J Hadchouel, M Primig, and M Buckingham Myf5 is a novel early axonal marker in the mouse brain and is subjected to post-transcriptional regulation in neurons Development, January 1, 2000; 127(2): 319 - 331. [Abstract] [PDF]
|
|
|
|
|
|
U Borello, M Coletta, S Tajbakhsh, L Leyns, E. De Robertis, M Buckingham, and G Cossu Transplacental delivery of the Wnt antagonist Frzb1 inhibits development of caudal paraxial mesoderm and skeletal myogenesis in mouse embryos Development, January 10, 1999; 126(19): 4247 - 4255. [Abstract] [PDF]
|
|
|
|
|
|
A. G. Ridgeway, H. Petropoulos, S. Wilton, and I. S. Skerjanc Wnt Signaling Regulates the Function of MyoD and Myogenin J. Biol. Chem., October 13, 2000; 275(42): 32398 - 32405. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. G. Ridgeway and I. S. Skerjanc Pax3 Is Essential for Skeletal Myogenesis and the Expression of Six1 and Eya2 J. Biol. Chem., May 25, 2001; 276(22): 19033 - 19039. [Abstract] [Full Text] [PDF]
|
|
