Skip to main content
Log in

Differential muscle regulatory factor gene expression between larval and adult myogenesis in the frog Xenopus laevis: adult myogenic cell-specific myf5 upregulation and its relation to the notochord suppression of adult muscle differentiation

  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

Abstract

During Xenopus laevis metamorphosis, larval-to-adult muscle conversion depends on the differential responses of adult and larval myogenic cells to thyroid hormone. Essential differences in cell growth, differentiation, and hormone-dependent life-or-death fate have been reported between cultured larval (tail) and adult (hindlimb) myogenic cells. A previous study revealed that tail notochord cells suppress terminal differentiation in adult (but not larval) myogenic cells. However, little is known about the differences in expression patterns of myogenic regulatory factors (MRF) and the satellite cell marker Pax7 between adult and larval myogenic cells. In the present study, we compared mRNA expression of these factors between the two types. At first, reverse transcription polymerase chain reaction analysis of hindlimb buds showed sequential upregulation of myf5, myogenin, myod, and mrf4 during stages 50–54, when limb buds elongate and muscles begin to form. By contrast, in the tail, there was no such increase during the same period. Secondary, these results were duplicated in vitro: adult myogenic cells upregulated myf5, myod, and pax7 in the early culture period, followed by myogenin upregulation and myotube differentiation, while larval myogenic cells did not upregulate these genes and precociously started myotube differentiation. Thirdly, myf5 upregulation and early-phase proliferation in adult myogenic cells were potently inhibited by the presence of notochord cells, suggesting that notochord cells suppress adult myogenesis through inhibiting the transition from Myf5- stem cells to Myf5+ committed myoblasts. All of the data presented here suggest that myf5 upregulation can be a good criterion for the activation of adult myogenesis during X. laevis metamorphosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.

Similar content being viewed by others

References

  • Adaniya C.; Nishikawa A. Supernumerary limbs are generated by grafting whole limb buds onto tail of Xenopus laevis tadpoles. The 79th Annual Meeting of the Zoological Society of Japan, Abstracts (in Japanese). p125: 3P065; 2009.

  • Alley K. E. Myofiber turnover is used to retrofit frog jaw muscles during metamorphosis. Am J Anat 184: 1–12; 1989.

    Article  PubMed  CAS  Google Scholar 

  • Buckingham M. Myogenic progenitor cells and skeletal myogenesis in vertebrates. Curr Opin Genet Dev 16: 525–532; 2006.

    Article  PubMed  CAS  Google Scholar 

  • Buckingham M. Skeletal muscle progenitor cells and the role of Pax genes. C. R. Biologies 330: 530–533; 2007.

    Article  PubMed  CAS  Google Scholar 

  • Buckingham M.; Bajard L.; Chang T.; Daubas P.; Hadchouel J.; Meilhac S.; Montarras D.; Rocancourt D.; Relaix F. The formation of skeletal muscle: from somite to limb. J Anat 202: 59–68; 2003.

    Article  PubMed  Google Scholar 

  • Cerletti M.; Jurga S.; Witczak C. A.; Hirshman M. F.; Shadrach J. L.; Goodyear L. J.; Wagers A. J. Highly efficient, functional engraftment of skeletal muscle stem cells in dystrophic muscles. Cell 134: 37–47; 2008.

    Article  PubMed  CAS  Google Scholar 

  • Chanoine C.; d'Albis A.; Lenfant-Guyot M.; Janmot C.; Gallien C. L. Regulation by thyroid hormones of terminal differentiation in the skeletal dorsal muscle. II. Urodelan amphibians. Dev Biol 123: 33–42; 1987.

    Article  PubMed  CAS  Google Scholar 

  • Chen Y.; Lin G.; Slack J. M. Control of muscle regeneration in the Xenopus tadpole tail by Pax7. Development 133: 2303–2313; 2006.

    Article  PubMed  CAS  Google Scholar 

  • Daughters R. S.; Chen Y.; Slack J. M. Origin of muscle satellite cells in the Xenopus embryo. Development 138: 821–830; 2011.

    Article  PubMed  CAS  Google Scholar 

  • De Angelis L.; Berghella L.; Coletta M.; Lattanzi L.; Zanchi M.; Cusella-De Angelis M. G.; Ponzetto C.; Cossu G. Skeletal myogenic progenitors originating from embryonic dorsal aorta coexpress endothelial and myogenic markers and contribute to postnatal muscle growth and regeneration. J Cell Biol 147: 869–878; 1999.

    Article  PubMed  Google Scholar 

  • Gargioli C.; Slack J. M. Cell lineage tracing during Xenopus tail regeneration. Development 131: 2669–2679; 2004.

    Article  PubMed  CAS  Google Scholar 

  • Hasty P.; Bradley A.; Morris J. H.; Edmondson D. G.; Venuti J. M.; Olson E. N.; Klein W. H. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364: 501–506; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Hinterberger T. J.; Sassoon D. A.; Rhodes S. J.; Konieczny S. F. Expression of the muscle regulatory factor MRF4 during somite and skeletal myofiber development. Dev Biol 147: 144–156; 1991.

    Article  PubMed  CAS  Google Scholar 

  • Ishibashi J.; Perry R. L.; Asakura A.; Rudnicki M. A. MyoD induces myogenic differentiation through cooperation of its NH2− and COOH−terminal regions. J Cell Biol 171: 471–482; 2005.

    Google Scholar 

  • Jones G. E.; Murphy S. J.; Watt D. J. Segregation of the myogenic cell lineage in mouse muscle development. J Cell Sci 97: 659–67; 1990.

    PubMed  Google Scholar 

  • Kawakami K.; Kuroda M.; Nishikawa A. Regulation of desmin expression in adult-type myogenesis and muscle maturation during Xenopus laevis metamorphosis. Zoolog Sci 26: 389–397; 2009.

    Article  PubMed  CAS  Google Scholar 

  • Kerr J. F.; Harmon B.; Searle J. An electron-microscope study of cell deletion in the anuran tadpole tail during spontaneous metamorphosis with special reference to apoptosis of striated muscle fibers. J Cell Sci 14: 571–585; 1974.

    PubMed  CAS  Google Scholar 

  • Kuang S.; Kuroda K.; Le Grand F.; Rudnicki M. A. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129: 999–1010; 2007.

    Article  PubMed  CAS  Google Scholar 

  • Le Grand F.; Rudnicki M. A. Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 19: 628–633; 2007.

    Article  PubMed  Google Scholar 

  • Lepper C.; Conway S. J.; Fan C. M. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature 460: 627–631; 2009.

    Article  PubMed  CAS  Google Scholar 

  • Liu S. J. Characterization of functional capacity of adult ventricular myocytes in long-term culture. Int J Cardiol; 2013. doi:10.1016/j.ijcard.2012.12.100.

    Google Scholar 

  • Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493–495; 1961.

    Article  PubMed  CAS  Google Scholar 

  • Miller L. Hormone induced changes in keratin gene expression during amphibian metamorphosis. In: Gilbert L. I.; Atkinson B. G.; Tata J. R. (eds) Metamorphosis: post-embryonic reprogramming of gene expression in amphibian and insect cells. Academic, New York, pp 599–624; 1996.

    Google Scholar 

  • Muntz L. Myogenesis in the trunk and leg during development of the tadpole of Xenopus laevis (Daudin 1802). J Embryol Exp Morphol 33: 757–774; 1975.

    PubMed  CAS  Google Scholar 

  • Nabeshima Y.; Hanaoka K.; Hayasaka M.; Esumi E.; Li S.; Nonaka I.; Nabeshima Y. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364: 532–535; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Nicolas N.; Gallien C. L.; Chanoine C. Expression of myogenic regulatory factors during muscle development of Xenopus: myogenin mRNA accumulation is limited strictly to secondary myogenesis. Dev Dyn 213: 309–321; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Nieuwkoop P. D.; Faber J. Normal table of Xenopus laevis (Daudin). North-Holland, Amsterdam; 1967.

    Google Scholar 

  • Nishikawa A.; Hayashi H. Isoform transition of contractile proteins related to muscle remodeling with an axial gradient during metamorphosis in Xenopus laevis. Dev Biol 165: 86–94; 1994.

    Article  PubMed  CAS  Google Scholar 

  • Nishikawa A.; Hayashi H. Spatial, temporal and hormonal regulation of programmed muscle cell death during metamorphosis of the frog Xenopus laevis. Differentiation 59: 207–214; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Nishikawa A.; Yoshizato K. Hormonal regulation of growth and life span of bullfrog tadpole tail epidermal cells cultured in vitro. J Exp Zool 237: 221–230; 1986.

    Article  PubMed  CAS  Google Scholar 

  • Oustanina S.; Hause G.; Braun T. Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J 23: 3430–3439; 2004.

    Article  PubMed  CAS  Google Scholar 

  • Patapoutian A.; Yoon J. K.; Miner J. H.; Wang S.; Stark K.; Wold B. Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome. Development 121: 3347–3358; 1995.

    PubMed  CAS  Google Scholar 

  • Relaix F.; Rocancourt D.; Mansouri A.; Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435: 948–953; 2005.

    Article  PubMed  CAS  Google Scholar 

  • Rudnicki M. A.; Braun T.; Hinuma S.; Jaenisch R. 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; 1992.

    Article  PubMed  CAS  Google Scholar 

  • Rudnicki M. A.; Schnegelsberg P. N.; Stead R. H.; Braun T.; Arnold H. H.; Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75: 1351–1359; 1993.

    Article  PubMed  CAS  Google Scholar 

  • Satoh A.; Sakamaki K.; Ide H.; Tamura K. Characteristics of initiation and early events for muscle development in the Xenopus limb bud. Dev Dyn 234: 846–857; 2005.

    Article  PubMed  CAS  Google Scholar 

  • Schlosser G.; Koyano-Nakagawa N.; Kintner C. Thyroid hormone promotes neurogenesis in the Xenopus spinal cord. Dev Dyn 225: 485–498; 2002.

    Article  PubMed  CAS  Google Scholar 

  • Shibota Y.; Kaneko Y.; Kuroda M.; Nishikawa A. Larval-to-adult conversion of a myogenic system in the frog, Xenopus laevis, by larval-type myoblast-specific control of cell division, cell differentiation, and programmed cell death by triiodo-l-thyronine. Differentiation 66: 227–238; 2000.

    PubMed  CAS  Google Scholar 

  • Shimizu-Nishikawa K.; Shibota Y.; Takei A.; Kuroda M.; Nishikawa A. Regulation of specific developmental fates of larval- and adult-type muscles during metamorphosis of the frog Xenopus. Dev Biol 251: 91–104; 2002.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi S.; Esumi E.; Nabeshima Y.; Asashima M. Regulation of the Xmyf-5 and XmyoD expression pattern during early Xenopus development. Zool Sci 15: 231–238; 1998.

    Article  CAS  Google Scholar 

  • Tremblay P.; Dietrich S.; Mericskay M.; Schubert F. R.; Li Z.; Paulin D. A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors. Dev Biol 203: 49–61; 1998.

    Article  PubMed  CAS  Google Scholar 

  • Ustanina S.; Carvajal J.; Rigby P.; Braun T. The myogenic factor Myf5 supports efficient skeletal muscle regeneration by enabling transient myoblast amplification. Stem Cells 25: 2006–2016; 2007.

    Article  PubMed  CAS  Google Scholar 

  • Venuti J. M.; Morris J. H.; Vivian J. L.; Olson E. N.; Klein W. H. Myogenin is required for late but not early aspects of myogenesis during mouse development. J Cell Biol 128: 563–576; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Yamane H.; Ihara S.; Kuroda M.; Nishikawa A. Adult-type myogenesis of the frog Xenopus laevis specifically suppressed by notochord cells but promoted by spinal cord cells in vitro. In Vitro Cell Dev Biol Anim 47: 470–483; 2011.

    Article  PubMed  CAS  Google Scholar 

  • Zhang W.; Behringer R. R.; Olson E. N. Inactivation of the myogenic bHLH gene MRF4 results in up-regulation of myogenin and rib anomalies. Genes Dev 9: 1388–1399; 1995.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported in part by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akio Nishikawa.

Additional information

Editor: T. Okamoto

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamane, H., Nishikawa, A. Differential muscle regulatory factor gene expression between larval and adult myogenesis in the frog Xenopus laevis: adult myogenic cell-specific myf5 upregulation and its relation to the notochord suppression of adult muscle differentiation. In Vitro Cell.Dev.Biol.-Animal 49, 524–536 (2013). https://doi.org/10.1007/s11626-013-9635-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11626-013-9635-z

Keywords

Navigation