Six1 regulates proliferation of Pax7-positive muscle progenitors in zebrafish

Journal of Cell Science

Volumn 126, Issue 8, 2013, Pages 1868-1880

  Nord, Hanna ^a   Skalman, Lars Nygård ^a   Von Hofsten, Jonas ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

Dermomyotome; Myogenesis; Pax7; pSMAD1 5 8; Six1; Six1a; Six1b

Indexed keywords

TRANSCRIPTION FACTOR PAX7; TRANSCRIPTION FACTOR SIX1;

ANIMAL CELL; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ZEBRA FISH;

DERMOMYOTOME; MYOGENESIS; PAX7; PSMAD1/5/8; SIX1; SIX1A; SIX1B;

ANIMALS; CELL PROLIFERATION; HOMEODOMAIN PROTEINS; MUSCLE DEVELOPMENT; MUSCLES; PAX7 TRANSCRIPTION FACTOR; STEM CELLS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84877964164     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.119917     Document Type: Article

References (48)

1. Amthor, H., Christ, B., Weil, M. and Patel, K. (1998). The importance of timing differentiation during limb muscle development. Curr. Biol. 8, 642-652.
2. Bajoghli, B., Aghaallaei, N., Heimbucher, T. and Czerny, T. (2004). An artificial promoter construct for heat-inducible misexpression during fish embryogenesis. Dev. Biol. 271, 416-430.
3. Bessarab, D. A., Chong, S. W. and Korzh, V. (2004). Expression of zebrafish six1 during sensory organ development and myogenesis. Dev. Dyn. 230, 781-786.
4. Bessarab, D. A., Chong, S. W., Srinivas, B. P. and Korzh, V. (2008). Six 1a is required for the onset of fast muscle differentiation in zebrafish. Dev. Biol. 323, 216-228.
5. Blagden, C. S., Currie, P. D., Ingham, P. W. and Hughes, S. M. (1997). Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev. 11, 2163-2175.
6. Bryson-Richardson, R. J. and Currie, P. D. (2008). The genetics of vertebrate myogenesis. Nat. Rev. Genet. 9, 632-646.
7. Burguiere, A. C., Nord, H. and von Hofsten, J. (2011). Alkali-like myosin light chain- 1 (myl1) is an early marker for differentiating fast muscle cells in zebrafish. Dev. Dyn. 240, 1856-1863.
8. Chen, B., Kim, E. H. and Xu, P. X. (2009). Initiation of olfactory placode development and neurogenesis is blocked in mice lacking both Six1 and Six4. Dev. Biol. 326, 75- 85.
9. Coletta, R. D., Christensen, K., Reichenberger, K. J., Lamb, J., Micomonaco, D., Huang, L., Wolf, D. M., Müller-Tidow, C., Golub, T. R., Kawakami, K. et al. (2004). The Six1 homeoprotein stimulates tumorigenesis by reactivation of cyclin A1. Proc. Natl. Acad. Sci. USA 101, 6478-6483.
10. Coletta, R. D., Christensen, K. L., Micalizzi, D. S., Jedlicka, P., Varella-Garcia, M. and Ford, H. L. (2008). Six1 overexpression in mammary cells induces genomic instability and is sufficient for malignant transformation. Cancer Res. 68, 2204-2213.
11. Dahlqvist, C., Blokzijl, A., Chapman, G., Falk, A., Dannaeus, K., Ibanez, C. F. and Lendahl, U. (2003). Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 130, 6089-6099.
12. Devoto, S. H., Melançon, E., Eisen, J. S. and Westerfield, M. (1996). Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122, 3371-3380.
13. 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.
14. Dolez, M., Nicolas, J. F. and Hirsinger, E. (2011). Laminins, via heparan sulfate proteoglycans, participate in zebrafish myotome morphogenesis by modulating the pattern of Bmp responsiveness. Development 138, 97-106.
15. 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.
16. 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.
17. Frank, N. Y., Kho, A. T., Schatton, T., Murphy, G. F., Molloy, M. J., Zhan, Q., Ramoni, M. F., Frank, M. H., Kohane, I. S. and Gussoni, E. (2006). Regulation of myogenic progenitor proliferation in human fetal skeletal muscle by BMP4 and its antagonist Gremlin. J. Cell Biol. 175, 99-110.
18. Grifone, R., Demignon, J., Houbron, C., Souil, E., Niro, C., Seller, M. J., Hamard, G. and Maire, P. (2005). Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo. Development 132, 2235-2249.
19. 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.
20. Hinits, Y., Osborn, D. P. and Hughes, S. M. (2009). Differential requirements for myogenic regulatory factors distinguish medial and lateral somitic, cranial and fin muscle fibre populations. Development 136, 403-414.
21. Hollway, G. E., Bryson-Richardson, R. J., Berger, S., Cole, N. J., Hall, T. E. and Currie, P. D. (2007). Whole-somite rotation generates muscle progenitor cell compartments in the developing zebrafish embryo. Dev. Cell 12, 207-219.
22. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
23. Laclef, C., Hamard, G., Demignon, J., Souil, E., Houbron, C. and Maire, P. (2003). Altered myogenesis in Six1-deficient mice. Development 130, 2239-2252.
24. Le Grand, F., Grifone, R., Mourikis, P., Houbron, C., Gigaud, C., Pujol, J., Maillet, M., Pages, G., Rudnicki, M., Tajbakhsh, S. et al. (2012). Six1 regulates stem cell repair potential and self-renewal during skeletal muscle regeneration. J. Cell Biol. 198, 815-832.
25. Lin, C. Y., Chen, W. T., Lee, H. C., Yang, P. H., Yang, H. J. and Tsai, H. J. (2009). The transcription factor Six1a plays an essential role in the craniofacial myogenesis of zebrafish. Dev. Biol. 331, 152-166.
26. Little, S. C. and Mullins, M. (2009). Bone morphogenetic protein heterodimers assemble heteromeric type I receptor complexes to pattern the dorsoventral axis. Nat. Cell Biol. 11, 637-643.
27. Massagué, J., Seoane, J. and Wotton, D. (2005). Smad transcription factors. Genes Dev. 19, 2783-2810.
28. 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.
29. Ono, Y., Calhabeu, F., Morgan, J. E., Katagiri, T., Amthor, H. and Zammit, P. S. (2011). BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ. 18, 222-234.
30. Pandur, P. D. and Moody, S. A. (2000). Xenopus Six1 gene is expressed in neurogenic cranial placodes and maintained in the differentiating lateral lines. Mech. Dev. 96, 253-257.
31. Pardali, K. and Moustakas, A. (2007). Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim. Biophys. Acta 1775, 21-62.
32. Patterson, S. E., Bird, N. C. and Devoto, S. H. (2010). BMP regulation of myogenesis in zebrafish. Dev. Dyn. 239, 806-817.
33. Relaix, F., Rocancourt, D., Mansouri, A. and Buckingham, M. (2005). A Pax3/Pax7- dependent population of skeletal muscle progenitor cells. Nature 435, 948-953.
34. Relaix, F., Montarras, D., Zaffran, S., Gayraud-Morel, B., Rocancourt, D., Tajbakhsh, S., Mansouri, A., Cumano, A. and Buckingham, M. (2006). Pax3 and Pax7 have distinct and overlapping functions in adult muscle progenitor cells. J. Cell Biol. 172, 91-102.
35. Spitz, F., Demignon, J., Porteu, A., Kahn, A., Concordet, J. P., Daegelen, D. and Maire, P. (1998). Expression of myogenin during embryogenesis is controlled by Six/ sine oculis homeoproteins through a conserved MEF3 binding site. Proc. Natl. Acad. Sci. USA 95, 14220-14225.
36. Stellabotte, F., Dobbs-McAuliffe, B., Fernández, D. A., Feng, X. and Devoto, S. H. (2007). Dynamic somite cell rearrangements lead to distinct waves of myotome growth. Development 134, 1253-1257.
37. Tapscott, S. J. (2005). The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development 132, 2685-2695.
38. Tapscott, S. J., Davis, R. L., Thayer, M. J., Cheng, P. F., Weintraub, H. and Lassar, A. B. (1988). MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science 242, 405-411.
39. Thisse, C., Thisse, B., Schilling, T. F. and Postlethwait, J. H. (1993). Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119, 1203-1215.
40. Von Hofsten, J., Elworthy, S., Gilchrist, M. J., Smith, J. C., Wardle, F. C. and Ingham, P. W. (2008). Prdm1- and Sox6-mediated transcriptional repression specifies muscle fibre type in the zebrafish embryo. EMBO Rep. 9, 683-689.
41. Wang, H., Noulet, F., Edom-Vovard, F., Tozer, S., Le Grand, F. and Duprez, D. (2010). Bmp signaling at the tips of skeletal muscles regulates the number of fetal muscle progenitors and satellite cells during development. Dev. Cell 18, 643-654.
42. Westerfield, M. (2000) The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press.
43. Windner, S. E., Bird, N. C., Patterson, S. E., Doris, R. A. and Devoto, S. H. (2012). Fss/ Tbx6 is required for central dermomyotome cell fate in zebrafish. Biol. Open 1, 806-814.
44. Yajima, H., Motohashi, N., Ono, Y., Sato, S., Ikeda, K., Masuda, S., Yada, E., Kanesaki, H., Miyagoe-Suzuki, Y., Takeda, S. et al. (2010). Six family genes control the proliferation and differentiation of muscle satellite cells. Exp. Cell Res. 316, 2932-2944.
45. Yamamoto, N., Akiyama, S., Katagiri, T., Namiki, M., Kurokawa, T. and Suda, T. (1997). Smad1 and smad5 act downstream of intracellular signalings of BMP-2 that inhibits myogenic differentiation and induces osteoblast differentiation in C2C12 myoblasts. Biochem. Biophys. Res. Commun. 238, 574-580.
46. Yanagisawa, M., Mukai, A., Shiomi, K., Song, S. Y. and Hashimoto, N. (2011). Community effect triggers terminal differentiation of myogenic cells derived from muscle satellite cells by quenching Smad signaling. Exp. Cell Res. 317, 221-233.
47. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., Lin,H. Y., Bloch, K. D. and Peterson, R. T. (2008). Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4, 33-41.
48. Zheng, W., Huang, L., Wei, Z. B., Silvius, D., Tang, B. and Xu, P. X. (2003). The role of Six1 in mammalian auditory system development. Development 130, 3989-4000.