Induced early expression of mrf4 but not myog rescues myogenesis in the myod/myf5 double-morphant zebrafish embryo

Journal of Cell Science

Volumn 122, Issue 4, 2009, Pages 481-488

  Schnapp, Esther ^a   Pistocchi, Anna Silvia ^b   Karampetsou, Evangelia ^b   Foglia, Efrem ^b   Lamia, Carla Lora ^b   Cotelli, Franco ^b   Cossu, Giulio ^a,b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

MRF; mrf4; myf5; Myod; Myogenin; Myotome; Skeletal myogenesis; Zebrafish

Indexed keywords

MYOD PROTEIN; MYOGENIC FACTOR 5; MYOGENIN; PROTEIN MRF4; UNCLASSIFIED DRUG; MYOGENIC FACTOR; MYOGENIC FACTOR 6; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; ENZYME ACTIVATION; GENETIC IDENTIFICATION; IN VITRO STUDY; MUSCLE DEVELOPMENT; MYOTOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; CYTOLOGY; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PRENATAL DEVELOPMENT; TIME; TRANSCRIPTION INITIATION;

DANIO RERIO; VERTEBRATA;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; EMBRYO, NONMAMMALIAN; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MUSCLE DEVELOPMENT; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; MYOGENIC REGULATORY FACTORS; MYOGENIN; TIME FACTORS; TRANSCRIPTIONAL ACTIVATION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 64849114391     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.038356     Document Type: Article

References (37)

1. Bergstrom, D. A. and Tapscott, S. J. (2001). Molecular distinction between specification and differentiation in the myogenic basic helix-loop-helix transcription factor family. Mol. Cell. Biol. 21, 2404-2412.
2. Bober, E., Lyons, G., Braun, T., Cossu, G., Buckingham, M. and Arnold, H. H. (1991). The muscle regulatory gene, Myf-6, has a biphasic pattern of expression during early mouse development. J. Cell Biol. 113, 1255-1265.
3. Braun, T. and Arnold, H. H. (1995). Inactivation of Myf-6 and Myf-5 genes in mice leads to alterations in skeletal muscle development. EMBO J. 14, 1176-1186.
4. Braun, T., Rudnicki, M. A., Arnold, H. H. and Jaenisch, R. (1992). Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71, 369-382.
5. Chen, Y. H. and Tsai, H. J. (2002). Treatment with Myf5-morpholino results in somite patterning and brain formation defects in zebrafish. Differentiation 70, 447-456.
6. Coutelle, O., Blagden, C. S., Hampson, R., Halai, C., Rigby, P. W. and Hughes, S. M. (2001). Hedgehog signalling is required for maintenance of myf5 and myoD expression and timely terminal differentiation in zebrafish adaxial myogenesis. Dev. Biol. 236, 136-150.
7. Della Gaspera, B., Sequeira, I., Charbonnier, F., Becker, C., Shi, D. L. and Chanoine, C. (2006). Spatio-temporal expression of MRF4 transcripts and protein during Xenopus laevis embryogenesis. Dev. Dyn. 235, 524-529.
8. Groves, J. A., Hammond, C. L. and Hughes, S. M. (2005). Fgf8 drives myogenic progression of a novel lateral fast muscle fibre population in zebrafish. Development 132, 4211-4222.
9. Haffter, P. and Nüsslein-Volhard, C. (1996). Large scale genetics in a small vertebrate, the zebrafish.. Int. J. Dev. Biol. 40, 221-227.
10. 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.
11. Hasty, P., Bradley, A., Morris, J. H., Edmondson, D. G., Venuti, J. M., Olson, E. N. and Klein, W. H. (1993). Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364, 501-506.
12. Higashijima, S., Okamoto, H., Ueno, N., Hotta, Y. and Eguchi, G. (1997). High-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Dev. Biol. 192, 289-299.
13. Hinits, Y., Osborn, D. P., Carvajal, J. J., Rigby, P. W. and Hughes, S. M. (2007). Mrf4 (myf6) is dynamically expressed in differentiated zebrafish skeletal muscle. Gene Expr. Patterns 7, 738-745.
14. Hinterberger, T. J., Sassoon, D. A., Rhodes, S. J. and Konieczny, S. F. (1991). Expression of the muscle regulatory factor MRF4 during somite and skeletal myofiber development. Dev. Biol. 147, 144-156.
15. Hopwood, N. D., Pluck, A. and Gurdon, J. B. (1989). MyoD expression in the forming somites is an early response to mesoderm induction in Xenopus embryos. EMBO J. 8, 3409-3417.
16. Hopwood, N. D., Pluck, A. and Gurdon, J. B. (1991). Xenopus Myf-5 marks early muscle cells and can activate muscle genes ectopically in early embryos. Development 111, 551-560.
17. Jennings, C. G. (1992). Expression of the myogenic gene MRF4 during Xenopus development. Dev. Biol. 151, 319-332.
18. Jowett, T. and Lettice, L. (1994). Whole-mount in situ hybridizations on zebrafish embryos using a mixture of digoxigenin- and fluorescein-labelled probes. Trends Genet. 10, 73-74.
19. Kablar, B., Krastel, K., Ying, C., Asakura, A., Tapscott, S. J. and Rudnicki, M. A. (1997). MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development 124, 4729-4738.
20. Kassar-Duchossoy, L., Gayraud-Morel, B., Gomes, D., Rocancourt, D., Buckingham, M., Shinin, V. and Tajbakhsh, S. (2004). Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 431, 466-471.
21. 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.
22. Lin, C. Y., Yung, R. F., Lee, H. C., Chen, W. T., Chen, Y. H. and Tsai, H. J. (2006). Myogenic regulatory factors Myf5 and Myod function distinctly during craniofacial myogenesis of zebrafish. Dev. Biol. 299, 594-608.
23. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
24. Maves, L., Waskiewicz, A. J., Paul, B., Cao, Y., Tyler, A., Moens, C. B. and Tapscott, S. J. (2007). Pbx homeodomain proteins direct Myod activity to promote fast-muscle differentiation. Development 134, 3371-3382.
25. Nabeshima, Y., Hanaoka, K., Hayasaka, M., Esumi, E., Li, S., Nonaka, I. and Nabeshima, Y. (1993). Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364, 532-535.
26. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220.
27. Nicolas, N., Gallien, C. L. and Chanoine, C. (1998). Expression of myogenic regulatory factors during muscle development of Xenopus: myogenin mRNA accumulation is limited strictly to secondary myogenesis. Dev. Dyn. 213, 309-321.
28. Patapoutian, A., Yoon, J. K., Miner, J. H., Wang, S., Stark, K. and Wold, B. (1995). Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome. Development 121, 3347-3358.
29. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
30. Rawls, A., Valdez, M. R., Zhang, W., Richardson, J., Klein, W. H. and Olson, E. N. (1998). Overlapping functions of the myogenic bHLH genes MRF4 and MyoD revealed in double mutant mice. Development 125, 2349-2358.
31. Roy, K., de la Serna, I. L. and Imbalzano, A. N. (2002). The myogenic basic helix-loop-helix family of transcription factors shows similar requirements for SWI/SNF chromatin remodeling enzymes during muscle differentiation in culture. J. Biol. Chem. 277, 33818-33824.
32. Rudnicki, M. A., Braun, T., Hinuma, S. and Jaenisch, R. (1992). Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383-390.
33. Rudnicki, M. A., Schnegelsberg, P. N., Stead, R. H., Braun, T., Arnold, H. H. and Jaenisch, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359.
34. 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.
35. Wang, Y. H., Li, C. K., Lee, G. H., Tsay, H. J., Tsai, H. J. and Chen, Y. H. (2008). Inactivation of zebrafish mrf4 leads to myofibril misalignment and motor axon growth disorganization. Dev. Dyn. 237, 1043-1050.
36. Weinberg, E. S., Allende, M. L., Kelly, C. S., Abdelhamid, A., Murakami, T., Andermann, P., Doerre, O. G., Grunwald, D. J. and Riggleman, B. (1996). Developmental regulation of zebrafish Myod in wild-type, no tail and spadetail embryos. Development 122, 271-280.
37. Zhang, W., Behringer, R. R. and Olson, E. N. (1995). Inactivation of the myogenic bHLH gene MRF4 results in up-regulation of myogenin and rib anomalies. Genes Dev. 9, 1388-1399.