The transition from differentiation to growth during dermomyotome-derived myogenesis depends on temporally restricted hedgehog signaling

Development (Cambridge)

Volumn 140, Issue 8, 2013, Pages 1740-1750

  Kahane, Nitza ^a   Ribes, Vanessa ^b,c   Kicheva, Anna ^b   Briscoe, James ^b   Kalcheim, Chaya ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

Avian embryo; Gli; Mouse; Myf5; Myotome; Somite

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR PAX7;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; COTURNIX; DERMOMYOTOME; EMBRYO; GALLUS GALLUS; IN VIVO STUDY; MOUSE; MUSCLE DEVELOPMENT; MYOTOME; NONHUMAN; NOTOCHORD; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHICK EMBRYO; DNA PRIMERS; ELECTROPORATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HEDGEHOG PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MUSCLE DEVELOPMENT; NOTOCHORD; PAX7 TRANSCRIPTION FACTOR; QUAIL; SIGNAL TRANSDUCTION; STEM CELLS; TIME FACTORS;

AVES; ERINACEIDAE; MUS;

EID: 84875430938     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.092726     Document Type: Article

References (81)

1. Ahn, S. and Joyner, A. L. (2004). Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118, 505-516.
2. Allen, B. L., Song, J. Y., Izzi, L., Althaus, I. W., Kang, J. S., Charron, F., Krauss, R. S. and McMahon, A. P. (2011). Overlapping roles and collective requirement for the coreceptors GAS1, CDO, and BOC in SHH pathway function. Dev. Cell 20, 775-787.
3. Amthor, H., Christ, B. and Patel, K. (1999). A molecular mechanism enabling continuous embryonic muscle growth - a balance between proliferation and differentiation. Development 126, 1041-1053.
4. Anderson, C., Williams, V. C., Moyon, B., Daubas, P., Tajbakhsh, S., Buckingham, M. E., Shiroishi, T., Hughes, S. M. and Borycki, A. G. (2012). Sonic hedgehog acts cell-autonomously on muscle precursor cells to generate limb muscle diversity. Genes Dev. 26, 2103-2117.
5. Balaskas, N., Ribeiro, A., Panovska, J., Dessaud, E., Sasai, N., Page, K. M., Briscoe, J. and Ribes, V. (2012). Gene regulatory logic for reading the Sonic Hedgehog signaling gradient in the vertebrate neural tube. Cell 148, 273-284.
6. 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.
7. Ben-Yair, R. and Kalcheim, C. (2008). Notch and bone morphogenetic protein differentially act on dermomyotome cells to generate endothelium, smooth, and striated muscle. J. Cell Biol. 180, 607-618.
8. Ben-Yair, R., Kahane, N. and Kalcheim, C. (2011). LGN-dependent orientation of cell divisions in the dermomyotome controls lineage segregation into muscle and dermis. Development 138, 4155-4166.
9. Biressi, S., Messina, G., Collombat, P., Tagliafico, E., Monteverde, S., Benedetti, L., Cusella De Angelis, M. G., Mansouri, A., Ferrari, S., Tajbakhsh, S. et al. (2008). The homeobox gene Arx is a novel positive regulator of embryonic myogenesis. Cell Death Differ. 15, 94-104.
10. Blagden, C. S. and Hughes, S. M. (1999). Extrinsic influences on limb muscle organisation. Cell Tissue Res. 296, 141-150.
11. Boardman, P. E., Sanz-Ezquerro, J., Overton, I. M., Burt, D. W., Bosch, E., Fong, W. T., Tickle, C., Brown, W. R., Wilson, S. A. and Hubbard, S. J. (2002). A comprehensive collection of chicken cDNAs. Curr. Biol. 12, 1965-1969.
12. Borycki, A. G., Mendham, L. and Emerson, C. P., Jr (1998). Control of somite patterning by Sonic hedgehog and its downstream signal response genes. Development 125, 777-790.
13. Borycki, A. G., Brunk, B., Tajbakhsh, S., Buckingham, M., Chiang, C. and Emerson, C. P., Jr (1999). Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development 126, 4053-4063.
14. Briscoe, J., Chen, Y., Jessell, T. M. and Struhl, G. (2001). A hedgehog-insensitive form of patched provides evidence for direct long-range morphogen activity of sonic hedgehog in the neural tube. Mol. Cell 7, 1279-1291.
15. Buckingham, M. (2001). Skeletal muscle formation in vertebrates. Curr. Opin. Genet. Dev. 11, 440-448.
16. Buckingham, M. and Montarras, D. (2008). Skeletal muscle stem cells. Curr. Opin. Genet. Dev. 18, 330-336.
17. Buckingham, M. and Vincent, S. D. (2009). Distinct and dynamic myogenic populations in the vertebrate embryo. Curr. Opin. Genet. Dev. 19, 444-453.
18. Büscher, D., Grotewold, L. and Rüther, U. (1998). The XtJ allele generates a Gli3 fusion transcript. Mamm. Genome 9, 676-678.
19. Buttitta, L., Mo, R., Hui, C. C. and Fan, C. M. (2003). Interplays of Gli2 and Gli3 and their requirement in mediating Shh-dependent sclerotome induction. Development 130, 6233-6243.
20. Cairns, D. M., Sato, M. E., Lee, P. G., Lassar, A. B. and Zeng, L. (2008). A gradient of Shh establishes mutually repressing somitic cell fates induced by Nkx3.2 and Pax3. Dev. Biol. 323, 152-165.
21. Chamberlain, C. E., Jeong, J., Guo, C., Allen, B. L. and McMahon, A. P. (2008). Notochord-derived Shh concentrates in close association with the apically positioned basal body in neural target cells and forms a dynamic gradient during neural patterning. Development 135, 1097-1106.
22. Charrier, J. B., Lapointe, F., Le Douarin, N. M. and Teillet, M. A. (2001). Anti-apoptotic role of Sonic hedgehog protein at the early stages of nervous system organogenesis. Development 128, 4011-4020.
23. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413.
24. Christ, B. and Scaal, M. (2008). Formation and differentiation of avian somite derivatives. Adv. Exp. Med. Biol. 638, 1-41.
25. Chuang, P. T. and McMahon, A. P. (1999). Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature 397, 617-621.
26. Cinnamon, Y., Kahane, N. and Kalcheim, C. (1999). Characterization of the early development of specific hypaxial muscles from the ventrolateral myotome. Development 126, 4305-4315.
27. Cinnamon, Y., Kahane, N., Bachelet, I. and Kalcheim, C. (2001). The sub-lip domain - a distinct pathway for myotome precursors that demonstrate rostral-caudal migration. Development 128, 341-351.
28. Cinnamon, Y., Ben-Yair, R. and Kalcheim, C. (2006). Differential effects of N-cadherin-mediated adhesion on the development of myotomal waves. Development 133, 1101-1112.
29. Cruz, C., Ribes, V., Kutejova, E., Cayuso, J., Lawson, V., Norris, D., Stevens, J., Davey, M., Blight, K., Bangs, F. et al. (2010). Foxj1 regulates floor plate cilia architecture and modifies the response of cells to sonic hedgehog signalling. Development 137, 4271-4282.
30. Danesin, C., Agius, E., Escalas, N., Ai, X., Emerson, C., Cochard, P. and Soula, C. (2006). Ventral neural progenitors switch toward an oligodendroglial fate in response to increased Sonic hedgehog (Shh) activity: involvement of Sulfatase 1 in modulating Shh signaling in the ventral spinal cord. J. Neurosci. 26, 5037-5048.
31. Delfini, M. C. and Duprez, D. (2004). Ectopic Myf5 or MyoD prevents the neuronal differentiation program in addition to inducing skeletal muscle differentiation, in the chick neural tube. Development 131, 713-723.
32. Delfini, M. C., De La Celle, M., Gros, J., Serralbo, O., Marics, I., Seux, M., Scaal, M. and Marcelle, C. (2009). The timing of emergence of muscle progenitors is controlled by an FGF/ERK/SNAIL1 pathway. Dev. Biol. 333, 229-237.
33. Dessaud, E., Yang, L. L., Hill, K., Cox, B., Ulloa, F., Ribeiro, A., Mynett, A., Novitch, B. G. and Briscoe, J. (2007). Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 450, 717-720.
34. Devoto, S. H., Stoiber, W., Hammond, C. L., Steinbacher, P., Haslett, J. R., Barresi, M. J., Patterson, S. E., Adiarte, E. G. and Hughes, S. M. (2006). Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish. Evol. Dev. 8, 101-110.
35. Dhoot, G. K., Gustafsson, M. K., Ai, X., Sun, W., Standiford, D. M. and Emerson, C. P., Jr (2001). Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293, 1663-1666.
36. Du, S. J., Devoto, S. H., Westerfield, M. and Moon, R. T. (1997). Positive and negative regulation of muscle cell identity by members of the hedgehog and TGF-beta gene families. J. Cell Biol. 139, 145-156.
37. Eggenschwiler, J. T. and Anderson, K. V. (2007). Cilia and developmental signaling. Annu. Rev. Cell Dev. Biol. 23, 345-373.
38. Feng, X., Adiarte, E. G. and Devoto, S. H. (2006). Hedgehog acts directly on the zebrafish dermomyotome to promote myogenic differentiation. Dev. Biol. 300, 736-746.
39. Gros, J., Scaal, M. and Marcelle, C. (2004). A two-step mechanism for myotome formation in chick. Dev. Cell 6, 875-882.
40. Gros, J., Manceau, M., Thomé, V. and Marcelle, C. (2005). A common somatic origin for embryonic muscle progenitors and satellite cells. Nature 435, 954-958.
41. Groysman, M., Shoval, I. and Kalcheim, C. (2008). A negative modulatory role for rho and rho-associated kinase signaling in delamination of neural crest cells. Neural Dev. 3, 27.
42. Gustafsson, M. K., Pan, H., Pinney, D. F., Liu, Y. L., Lewandowski, A., Epstein, D. J. and Emerson, C. P., Jr (2002). Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes Dev. 16, 114-126.
43. Halperin-Barlev, O. and Kalcheim, C. (2011). Sclerotome-derived Slit1 drives directional migration and differentiation of Robo2-expressing pioneer myoblasts. Development 138, 2935-2945.
44. 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.
45. Harfe, B. D., Scherz, P. J., Nissim, S., Tian, H., McMahon, A. P. and Tabin, C. J. (2004). Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 118, 517-528.
46. Hu, J. K., McGlinn, E., Harfe, B. D., Kardon, G. and Tabin, C. J. (2012). Autonomous and nonautonomous roles of Hedgehog signaling in regulating limb muscle formation. Genes Dev. 26, 2088-2102.
47. Huang, R. and Christ, B. (2000). Origin of the epaxial and hypaxial myotome in avian embryos. Anat. Embryol. (Berl.) 202, 369-374.
48. Hui, C. C. and Joyner, A. L. (1993). A mouse model of greig cephalopolysyndactyly syndrome: the extra-toesJ mutation contains an intragenic deletion of the Gli3 gene. Nat. Genet. 3, 241-246.
49. Hynes, M., Ye, W., Wang, K., Stone, D., Murone, M., Sauvage, F. and Rosenthal, A. (2000). The seven-transmembrane receptor smoothened cell-autonomously induces multiple ventral cell types. Nat. Neurosci. 3, 41-46.
50. Incardona, J. P., Gaffield, W., Kapur, R. P. and Roelink, H. (1998). The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development 125, 3553-3562.
51. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
52. Izzi, L., Lévesque, M., Morin, S., Laniel, D., Wilkes, B. C., Mille, F., Krauss, R. S., McMahon, A. P., Allen, B. L. and Charron, F. (2011). Boc and Gas1 each form distinct Shh receptor complexes with Ptch1 and are required for Shh-mediated cell proliferation. Dev. Cell 20, 788-801.
53. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
54. Kahane, N., Cinnamon, Y. and Kalcheim, C. (1998a). The origin and fate of pioneer myotomal cells in the avian embryo. Mech. Dev. 74, 59-73.
55. Kahane, N., Cinnamon, Y. and Kalcheim, C. (1998b). The cellular mechanism by which the dermomyotome contributes to the second wave of myotome development. Development 125, 4259-4271.
56. Kahane, N., Cinnamon, Y., Bachelet, I. and Kalcheim, C. (2001). The third wave of myotome colonization by mitotically competent progenitors: regulating the balance between differentiation and proliferation during muscle development. Development 128, 2187-2198.
57. Kahane, N., Cinnamon, Y. and Kalcheim, C. (2002). The roles of cell migration and myofiber intercalation in patterning formation of the postmitotic myotome. Development 129, 2675-2687.
58. Kahane, N., Ben-Yair, R. and Kalcheim, C. (2007). Medial pioneer fibers pattern the morphogenesis of early myoblasts derived from the lateral somite. Dev. Biol. 305, 439-450.
59. Kalcheim, C. and Ben-Yair, R. (2005). Cell rearrangements during development of the somite and its derivatives. Curr. Opin. Genet. Dev. 15, 371-380.
60. Kassar-Duchossoy, L., Giacone, E., Gayraud-Morel, B., Jory, A., Gomès, D. and Tajbakhsh, S. (2005). Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 19, 1426-1431.
61. Krüger, M., Mennerich, D., Fees, S., Schäfer, R., Mundlos, S. and Braun, T. (2001). Sonic hedgehog is a survival factor for hypaxial muscles during mouse development. Development 128, 743-752.
62. Lewis, K. E., Concordet, J. P. and Ingham, P. W. (1999). Characterisation of a second patched gene in the zebrafish Danio rerio and the differential response of patched genes to Hedgehog signalling. Dev. Biol. 208, 14-29.
63. Lewis, P. M., Dunn, M. P., McMahon, J. A., Logan, M., Martin, J. F., St-Jacques, B. and McMahon, A. P. (2001). Cholesterol modification of sonic hedgehog is required for long-range signaling activity and effective modulation of signaling by Ptc1. Cell 105, 599-612.
64. Martin, B. L., Peyrot, S. M. and Harland, R. M. (2007). Hedgehog signaling regulates the amount of hypaxial muscle development during Xenopus myogenesis. Dev. Biol. 304, 722-734.
65. Maurya, A. K., Tan, H., Souren, M., Wang, X., Wittbrodt, J. and Ingham, P. W. (2011). Integration of Hedgehog and BMP signalling by the engrailed2a gene in the zebrafish myotome. Development 138, 755-765.
66. McDermott, A., Gustafsson, M., Elsam, T., Hui, C. C., Emerson, C. P., Jr and Borycki, A. G. (2005). Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation. Development 132, 345-357.
67. Momose, T., Tonegawa, A., Takeuchi, J., Ogawa, H., Umesono, K. and Yasuda, K. (1999). Efficient targeting of gene expression in chick embryos by microelectroporation. Dev. Growth Differ. 41, 335-344.
68. Nitzan, E. and Kalcheim, C. (2013). Neural crest and somitic mesoderm as paradigms to investigate cell fate decisions during development. Dev. Growth Differ. 55, 60-78.
69. Polizio, A. H., Chinchilla, P., Chen, X., Manning, D. R. and Riobo, N. A. (2011). Sonic Hedgehog activates the GTPases Rac1 and RhoA in a Gli-independent manner through coupling of smoothened to Gi proteins. Sci. Signal. 4, pt7.
70. Pownall, M. E. and Emerson, C. P., Jr (1992). Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev. Biol. 151, 67-79.
71. Relaix, F., Rocancourt, D., Mansouri, A. and Buckingham, M. (2005). A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435, 948-953.
72. Ribes, V. and Briscoe, J. (2009). Establishing and interpreting graded Sonic Hedgehog signaling during vertebrate neural tube patterning: the role of negative feedback. Cold Spring Harb. Perspect. Biol. 1, a002014.
73. Ribes, V., Balaskas, N., Sasai, N., Cruz, C., Dessaud, E., Cayuso, J., Tozer, S., Yang, L. L., Novitch, B., Marti, E. et al. (2010). Distinct Sonic Hedgehog signaling dynamics specify floor plate and ventral neuronal progenitors in the vertebrate neural tube. Genes Dev. 24, 1186-1200.
74. Sasaki, H., Hui, C., Nakafuku, M. and Kondoh, H. (1997). A binding site for Gli proteins is essential for HNF-3beta floor plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124, 1313-1322.
75. Scaal, M. and Christ, B. (2004). Formation and differentiation of the avian dermomyotome. Anat. Embryol. (Berl.) 208, 411-424.
76. Stamataki, D., Ulloa, F., Tsoni, S. V., Mynett, A. and Briscoe, J. (2005). A gradient of Gli activity mediates graded Sonic Hedgehog signaling in the neural tube. Genes Dev. 19, 626-641.
77. Stellabotte, F. and Devoto, S. H. (2007). The teleost dermomyotome. Dev. Dyn. 236, 2432-2443.
78. Teboul, L., Summerbell, D. and Rigby, P. W. (2003). The initial somitic phase of Myf5 expression requires neither Shh signaling nor Gli regulation. Genes Dev. 17, 2870-2874.
79. Teillet, M. A., Lapointe, F. and Le Douarin, N. M. (1998). The relationships between notochord and floor plate in vertebrate development revisited. Proc. Natl. Acad. Sci. USA 95, 11733-11738.
80. Watanabe, T., Saito, D., Tanabe, K., Suetsugu, R., Nakaya, Y., Nakagawa, S. and Takahashi, Y. (2007). Tet-on inducible system combined with in ovo electroporation dissects multiple roles of genes in somitogenesis of chicken embryos. Dev. Biol. 305, 625-636.
81. Wolff, C., Roy, S. and Ingham, P. W. (2003). Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo. Curr. Biol. 13, 1169-1181.