A new role for the calcineurin/NFAT pathway in neonatal myosin heavy chain expression via the NFATc2/MyoD complex during mouse myogenesis

Development (Cambridge)

Volumn 140, Issue 24, 2013, Pages 4914-4925

  Daou, Nissrine ^a   Lecolle, Sylvie ^a   Lefebvre, Suzie ^a   della Gaspera, Bruno ^a   Charbonnier, Frédéric ^a   Chanoine, Christophe ^a   Armand, Anne Sophie ^a  

^a CNRS   (France)

Author keywords

Calcineurin; MyoD; Myogenesis; Myogenic regulatory factors; Myosin heavy chain; NFAT; Skeletal muscle

Indexed keywords

CALCINEURIN; ISOPROTEIN; MYOD PROTEIN; MYOSIN HEAVY CHAIN; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC1; TRANSCRIPTION FACTOR NFATC2; TRANSCRIPTION FACTOR NFATC3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIRTH; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE MUTATION; INTERCOSTAL MUSCLE; LIMB; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MUTANT; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

CALCINEURIN; MYOD; MYOGENESIS; MYOGENIC REGULATORY FACTORS; MYOSIN HEAVY CHAIN; NFAT; SKELETAL MUSCLE;

ANIMALS; CALCINEURIN; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; MICE; MICE, KNOCKOUT; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOD PROTEIN; MYOSIN HEAVY CHAINS; NFATC TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION;

EID: 84888868699     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.097428     Document Type: Article

References (30)

1. Allen, D. L. and Leinwand, L. A. (2001). Postnatal myosin heavy chain isoform expression in normal mice and mice null for IIb or IId myosin heavy chains. Dev. Biol. 229, 383-395.
2. Armand, A.-S., Lécolle, S., Launay, T., Pariset, C., Fiore, F., Della Gaspera, B., Birnbaum, D., Chanoine, C. and Charbonnier, F. (2004). IGF-II is up-regulated and myofibres are hypertrophied in regenerating soleus of mice lacking FGF6. Exp. Cell Res. 297, 27-38.
3. Armand, A.-S., Bourajjaj, M., Martínez-Martínez, S., El Azzouzi, H., da Costa Martins, P. A., Hatzis, P., Seidler, T., Redondo, J. M. and De Windt, L. J. (2008). Cooperative synergy between NFAT and MyoD regulates myogenin expression and myogenesis. J. Biol. Chem. 283, 29004-29010.
4. Armand, A.-S., Laziz, I., Djeghloul, D., Lécolle, S., Bertrand, A. T., Biondi, O., De Windt, L. J. and Chanoine, C. (2011). Apoptosis-inducing factor regulates skeletal muscle progenitor cell number and muscle phenotype. PLoS ONE 6, e27283.
5. Beylkin, D. H., Allen, D. L. and Leinwand, L. A. (2006). MyoD, Myf5, and the calcineurin pathway activate the developmental myosin heavy chain genes. Dev. Biol. 294, 541-553.
6. Brooke, M. H. and Kaiser, K. K. (1970). Muscle fiber types: how many and what kind? Arch. Neurol. 23, 369-379.
7. Buckingham, M. (1996). Skeletal muscle development and the role of the myogenic regulatory factors. Biochem. Soc. Trans. 24, 506-509.
8. Calabria, E., Ciciliot, S., Moretti, I., Garcia, M., Picard, A., Dyar, K. A., Pallafacchina, G., Tothova, J., Schiaffino, S. and Murgia, M. (2009). NFAT isoforms control activity-dependent muscle fiber type specification. Proc. Natl. Acad. Sci. USA 106, 13335-13340.
9. Chin, E. R., Olson, E. N., Richardson, J. A., Yang, Q., Humphries, C., Shelton, J. M., Wu, H., Zhu, W., Bassel-Duby, R. and Williams, R. S. (1998). A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev. 12, 2499-2509.
10. Condon, K., Silberstein, L., Blau, H. M. and Thompson, W. J. (1990a). Differentiation of fiber types in aneural musculature of the prenatal rat hindlimb. Dev. Biol. 138, 275-295.
11. Condon, K., Silberstein, L., Blau, H. M. and Thompson, W. J. (1990b). Development of muscle fiber types in the prenatal rat hindlimb. Dev. Biol. 138, 256-274.
12. DeNardi, C., Ausoni, S., Moretti, P., Gorza, L., Velleca, M., Buckingham, M. and Schiaffino, S. (1993). Type 2X-myosin heavy chain is coded by a muscle fiber type-specific and developmentally regulated gene. J. Cell Biol. 123, 823-835.
13. Hodge, M. R., Ranger, A. M., Charles de la Brousse, F., Hoey, T., Grusby, M. J. and Glimcher, L. H. (1996). Hyperproliferation and dysregulation of IL-4 expression in NF-ATp-deficient mice. Immunity 4, 397-405.
14. Horsley, V., Friday, B. B., Matteson, S., Kegley, K. M., Gephart, J. and Pavlath, G. K. (2001). Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J. Cell Biol. 153, 329-338.
15. Horsley, V., Jansen, K. M., Mills, S. T. and Pavlath, G. K. (2003). IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 113, 483-494.
16. Kegley, K. M., Gephart, J., Warren, G. L. and Pavlath, G. K. (2001). Altered primary myogenesis in NFATC3(-/-) mice leads to decreased muscle size in the adult. Dev. Biol. 232, 115-126.
17. Lyons, G. E., Ontell, M., Cox, R., Sassoon, D. and Buckingham, M. (1990). The expression of myosin genes in developing skeletal muscle in the mouse embryo. J. Cell Biol. 111, 1465-1476.
18. Martínez-Martínez, S., Gómez del Arco, P., Armesilla, A. L., Aramburu, J., Luo, C., Rao, A. and Redondo, J. M. (1997). Blockade of T-cell activation by dithiocarbamates involves novel mechanisms of inhibition of nuclear factor of activated T cells. Mol. Cell. Biol. 17, 6437-6447.
19. Molkentin, J. D., Lu, J. R., Antos, C. L., Markham, B., Richardson, J., Robbins, J., Grant, S. R. and Olson, E. N. (1998). A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93, 215-228.
20. Naya, F. J., Mercer, B., Shelton, J., Richardson, J. A., Williams, R. S. and Olson, E. N. (2000). Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. J. Biol. Chem. 275, 4545-4548.
21. Oh, M., Rybkin, I. I., Copeland, V., Czubryt, M. P., Shelton, J. M., van Rooij, E., Richardson, J. A., Hill, J. A., De Windt, L. J., Bassel-Duby, R. et al. (2005). Calcineurin is necessary for the maintenance but not embryonic development of slow muscle fibers. Mol. Cell. Biol. 25, 6629-6638.
22. Ontell, M., Ontell, M. P., Sopper, M. M., Mallonga, R., Lyons, G. and Buckingham, M. (1993). Contractile protein gene expression in primary myotubes of embryonic mouse hindlimb muscles. Development 117, 1435-1444.
23. Rao, A., Luo, C. and Hogan, P. G. (1997). Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15, 707-747.
24. Richard, A.F., Demignon, J., Sakakibara, I., Pujol, J., Favier, M., Strochlic, L., Le Grand, F., Sgarioto, N., Guernec, A., Schmitt, A. et al. (2011). Genesis of muscle fiber-type diversity during mouse embryogenesis relies on Six1 and Six4 gene expression. Dev. Biol. 359, 303-320.
25. 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.
26. Schiaffino, S. (2010). Fibre types in skeletal muscle: a personal account. Acta Physiol. (Oxf.) 199, 451-463.
27. Schiaffino, S. and Reggiani, C. (2011). Fiber types in mammalian skeletal muscles. Physiol. Rev. 91, 1447-1531.
28. van Oort, R. J., van Rooij, E., Bourajjaj, M., Schimmel, J., Jansen, M. A., van der Nagel, R., Doevendans, P. A., Schneider, M. D., van Echteld, C. J. A. and De Windt, L. J. (2006). MEF2 activates a genetic program promoting chamber dilation and contractile dysfunction in calcineurin-induced heart failure. Circulation 114, 298-308.
29. Whalen, R. G., Sell, S. M., Butler-Browne, G. S., Schwartz, K., Bouveret, P. and Pinset-Härstöm, I. (1981). Three myosin heavy-chain isozymes appear sequentially in rat muscle development. Nature 292, 805-809.
30. Wheeler, M. T., Snyder, E. C., Patterson, M. N. and Swoap, S. J. (1999). An E-box within the MHC IIB gene is bound by MyoD and is required for gene expression in fast muscle. Am. J. Physiol. 276, C1069-C1078.