Skip to main content
Log in

Gene Orthologs of Myogenic Regulatory Factors (MRF) Family and their Possible Functions in Echinoderms

  • ORIGINAL PAPERS
  • Published:
Russian Journal of Marine Biology Aims and scope Submit manuscript

Abstract

MRF family genes are found in all animals and play an important role in the development of the muscular system. The study of the available transcriptomes and genomes of different members of Echinodermata showed that they have orthologs of the vertebrate MyoD gene. Crinoids and echinoids have three genes: MyoD1, MyoD2, and MyoD3. Asteroids apparently lost the MyoD3 gene, while holothurians lost MyoD2. In the holothurian Eupentacta fraudatrix, the expression of MyoD3 was significantly increased during muscle regeneration, while the number of MyoD1 transcripts did not change. This may indicate the involvement of MyoD3 in the regulation of myogenesis in holothurians.

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.

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Dolmatov, I.Yu. and Mashanov, V.S., Regeneratsiya u goloturii (Regeneration in Holothurians), Vladivostok: Dal’nauka, 2007.

  2. Dolmatov, I.Yu., Bobrovskaya, N.V., and Girich, A.S., Echinoderms as model objects for studying the mechanisms of regeneration, Vestn. S.-Peterb. Univ., Ser. 3, 2014, vol. 3, pp. 96–112.

    Google Scholar 

  3. Adams, M., Celniker, S., Holt R., et al., The genome sequence of Drosophila melanogaster, Science, 2000, vol. 287, no. 5461, pp. 2185–2195.

    Article  PubMed  Google Scholar 

  4. Andrikou, C., Iovene, E., Rizzo, F., et al., Myogenesis in the sea urchin embryo: The molecular fingerprint of the myoblast precursors, EvoDevo, 2013, vol. 4, 33.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Araki, S., Saiga, H., Makabe, K., and Satoh, N., Expression of AMD 1, a gene for a MyoD 1-related factor in the ascidian Halocynthia roretzi, Roux’s Arch. Dev. Biol., 1994, vol. 203, no. 3, pp. 320–327.

    Article  CAS  Google Scholar 

  6. Atchley, W., Fitch, W., and Bronner-Fraser, M., Molecular evolution of the MyoD family of transcription factors, Proc. Natl. Acad. Sci. U. S. A., 1994, vol. 91, no. 24, pp. 11522–11526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Balagopalan, L., Keller, C., and Abmayr, S., Loss-of-function mutations reveal that the Drosophila nautilus gene is not essential for embryonic myogenesis or viability, Dev. Biol., 2001, vol. 231, no. 2, pp. 374–382.

    Article  CAS  PubMed  Google Scholar 

  8. Baugh, L. and Hunter, C., MyoD, modularity, and myogenesis: Conservation of regulators and redundancy in C. elegans, Genes Dev., 2006, vol. 20, pp. 3342–3346.

    Article  CAS  PubMed  Google Scholar 

  9. Bergstrom, D. and Tapscott, S., Molecular distinction between specification and differentiation in the myogenic basic helix-loop-helix transcription factor family, Mol. Cell. Biol., 2001, vol. 21, no. 7, pp. 2404–2412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Boyko, A., Girich, A., Tkacheva, E., and Dolmatov, I., The Eupentacta fraudatrix transcriptome provides insights into regulation of cell transdifferentiation, Sci. Rep., 2020, vol. 10, 1522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Buckingham, M. and Rigby, P., Gene regulatory networks and transcriptional mechanisms that control myogenesis, Dev. Cell, 2014, vol. 28, no. 3, pp. 225–238.

    Article  CAS  PubMed  Google Scholar 

  12. Candia Carnevali, M.D., Regeneration in Echinoderms: Repair, regrowth, cloning, Invertebr. Survival J., 2006, vol. 3, no. 1, pp. 64–76.

    Google Scholar 

  13. Conerly, M., Yao, Z., Zhong, J., et al., Distinct activities of Myf5 and MyoD indicate separate roles in skeletal muscle lineage specification and differentiation, Dev. Cell, 2016, vol. 36, no. 4, pp. 375–385.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Dehal, P., Satou, Y., Campbell, R., et al., The draft genome of Ciona intestinalis: Insights into chordate and vertebrate origins, Science, 2003, vol. 298, no. 5601, pp. 2157–2167.

    Article  CAS  Google Scholar 

  15. Dolmatov, I., Development and evolution of the muscle system in the Echinodermata, in Echinoderms: Proc. 12th Int. Echinoderm Conf., Durham, U. S. A., 2010, pp. 163–166.

  16. Dolmatov, I., Afanasyev, S., and Boyko, A., Molecular mechanisms of fission in echinoderms: Transcriptome analysis, PLoS One, 2018, vol. 13, no. 4, e0195836.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Dolmatov, I., Eliseikina, M., Bulgakov, T., et al., Muscle regeneration in the holothurian Stichopus japonicus, Roux’s Arch. Dev. Biol., 1996, vol. 205, pp. 486–493.

    Article  CAS  Google Scholar 

  18. Dolmatov, I. and Ginanova, T., Muscle regeneration in holothurians, Microsc. Res., 2001, vol. 55, no. 6, pp. 452–463.

    Article  CAS  Google Scholar 

  19. Dolmatov, I. and Ivantey, V., Histogenesis of longitudinal muscle bands in holothurians, RJDB, 1993, vol. 24, pp. 67–72.

    Google Scholar 

  20. Fukushige, T., Brodigan, T., Schriefer, L., et al., Defining the transcriptional redundancy of early bodywall muscle development in C. elegans: Evidence for a unified theory of animal muscle development, Genes Dev., 2007, vol. 20, pp. 3395–3406.

    Article  CAS  Google Scholar 

  21. Garcia-Arraras, J. and Dolmatov, I., Echinoderms: Potential model systems for studies on muscle regeneration, Curr. Pharm. Des., 2010, vol. 16, no. 8, pp. 942–955.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Garcia-Arraras, J., Estrada-Rodgers, L., Santiago, R., et al., Cellular mechanisms of intestine regeneration in the sea cucumber, Holothuria glaberrima Selenka (Holothuroidea: Echinodermata), J. Exp. Zool., 1998, vol. 281, pp. 288–304.

    Article  CAS  PubMed  Google Scholar 

  23. Ginanova, T., DNA synthesis during muscle regeneration in sea cucumber, Biol. Bull., 1998, vol. 25, pp. 9–13.

    Google Scholar 

  24. Grounds, M., Garrett, K., Lai, M., et al., Identification of skeletal muscle precursor cells in vivo by use of MyoD1 and myogenin probes, Cell Tissue Res., 1992, vol. 267, pp. 99–104.

    Article  CAS  PubMed  Google Scholar 

  25. Guindon, S., Dufayard, J., Lefort, V., et al., New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0, Syst. Biol., 2010, vol. 59, no. 3, pp. 307–321.

    Article  CAS  PubMed  Google Scholar 

  26. Howard-Ashby, M., Materna, S., Brown, C., et al., Gene families encoding transcription factors expressed in early development of Strongylocentrotus purpuratus, Dev. Biol., 2006, vol. 300, no. 1, pp. 90–107.

    Article  CAS  PubMed  Google Scholar 

  27. Ishibashi, J., Perry, R., Asakura, A., and Rudnicki, M., MyoD induces myogenic differentiation through cooperation of its NH2- and COOH-terminal regions, J. Cell Biol., 2005, vol. 171, no. 3, pp. 471–482.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Karalaki, M., Fili, S., Philippou, A., and Kontsilieris, M., Muscle regeneration: Cellular and molecular events, In Vivo, 2009, vol. 23, pp. 779–796.

    CAS  PubMed  Google Scholar 

  29. Lanfear, R., Frandsen, P., Wright, A., et al., PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses, Mol. Biol. Evol., 2016, vol. 34, no. 3, pp. 772–773.

    Google Scholar 

  30. Lassar, A., Davis, R., Wright, W., et al., Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo, Cell, 1991, vol. 66, no. 2, pp. 305–315.

    Article  CAS  PubMed  Google Scholar 

  31. Mashanov, V., Dolmatov, I., and Heinzeller, T., Transdifferentiation in holothurian gut regeneration, Biol. Bull., 2005, vol. 209, no. 3, pp. 184–193.

    Article  PubMed  Google Scholar 

  32. Mashanov, V., Zueva, O., and Heinzeller, T., Regeneration of the radial nerve cord in a holothurian: A promising new model system for studying post-traumatic recovery in the adult nervous system, Tissue Cell, 2008, vol. 40, no. 5, pp. 351–372.

    Article  PubMed  Google Scholar 

  33. Michelson, A., Abmayr, S., Bate, M., et al., Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos, Genes Dev., 1990, vol. 4, pp. 2086–2097.

    Article  CAS  PubMed  Google Scholar 

  34. Mladenov, P., Igdoura, S., Asotra, S., et al., Purification and partial characterization of an autotomy-promoting factor from the sea star Pycnopodia helianthoides, Biol. Bull., 1989, vol. 176, no. 2, pp. 169–175.

    Article  CAS  Google Scholar 

  35. Pavlath, G., Dominov, J., Kegley, K., et al., Regeneration of transgenic skeletal muscles with altered timing of expression of the basic helix-loop-helix muscle regulatory factor MRF4, Am. J. Pathol., 2003, vol. 162, no. 5, pp. 1685–1691.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Ronquist, F., Teslenko, M., van der Mark, P., et al., MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space, Syst. Biol., 2012, vol. 61, no. 3, pp. 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Rudnicki, M., Braun, T., Hinuma, S., and 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, 1992, vol. 71, no. 3, pp. 383–390.

    Article  CAS  PubMed  Google Scholar 

  38. Rudnicki, M., Schnegelsberg, P., Stead, R., et al., MyoD or Myf-5 is required for the formation of skeletal muscle, Cell, 1993, vol. 75, no. 7, pp. 1351–1359.

    Article  CAS  PubMed  Google Scholar 

  39. Singh, K. and Dilworth, F., Differential modulation of cell cycle progression distinguishes members of the myogenic regulatory factor family of transcription factors, FEBS J., 2013, vol. 280, no. 17, pp. 3991–4003.

    Article  CAS  PubMed  Google Scholar 

  40. Van Doren, M., Ellis, H., and Posakony, J., The Drosophila extramacrochaetae protein antagonizes sequence-specific DNA binding by daughterless achaete-scute protein complexes, Development, 1991, vol. 113, no. 1, pp. 245–255.

    Article  CAS  PubMed  Google Scholar 

  41. Van Doren, M., Powell, P., Pasternak, D., et al., Spatial regulation of proneural gene activity: Auto- and cross-activation of achaete is antagonized by extramacrochaetae, Genes Dev., 1992, vol. 6, pp. 2592–2605.

    Article  CAS  PubMed  Google Scholar 

  42. Venuti, J., Goldberg, L., Chakraborty, T., et al., A myogenic factor from sea urchin embryos capable of programming muscle differentiation in mammalian cells, Proc. Natl. Acad. Sci. U. S. A., 1991, vol. 88, no. 14, pp. 6219–6223.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Weintraub, H., Dwarki, V., Verma, I., et al., Muscle-specific transcriptional activation by MyoD, Genes Dev., 1991, vol. 5, no. 8, pp. 1377–1386.

    Article  CAS  PubMed  Google Scholar 

  44. White, J., Scaffidi, A., Davies, M., et al., Myotube formation is delayed but not prevented in myoD-deficient skeletal muscle: Studies in regenerating whole muscle grafts of adult mice, J. Histochem. Cytochem., 2016, vol. 48, no. 11, pp. 1531–1544.

    Article  Google Scholar 

  45. Zhou, Z. and Bornemann, A., MRF4 protein expression in regenerating rat muscle, J. Muscle Res. Cell Motil., 2001, vol. 22, pp. 311–316.

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to A.S. Girich and A.V. Boyko for help in research.

Funding

This work was supported by the Russian Science Foundation (grant no. 21-74-30004).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. A. Nizhnichenko.

Ethics declarations

Conflict of interest. The authors declare that they have no conflicts of interest.

Statement on the welfare of animals. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Translated by T. Koznova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nizhnichenko, V.A., Dolmatov, I.Y. Gene Orthologs of Myogenic Regulatory Factors (MRF) Family and their Possible Functions in Echinoderms. Russ J Mar Biol 48, 185–194 (2022). https://doi.org/10.1134/S1063074022030063

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1063074022030063

Keywords:

Navigation