Skip to main content

Spatiotemporal expression of a twist homolog in the leech Helobdella austinensis

Abstract

Genes of the twist family encode bHLH transcription factors known to be involved in the regulation and differentiation of early mesoderm. Here, we report our characterization of Hau-twist, a twist homolog from the leech Helobdella austinensis, a tractable lophotrochozoan representative. Hau-twist was expressed in segmental founder cells of the mesodermal lineage, in subsets of cells within the mesodermal lineage of the germinal plate, in circumferential muscle fibers of a provisional integument during segmentation and organogenesis stages and on the ventral side of the developing proboscis. Thus, consistent with other systems, our results suggest that twist gene of the leech Helobdella might function in mesoderm differentiation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Astrow S, Holton B, Weisblat D (1987) Centrifugation redistributes factors determining cleavage patterns in leech embryos. Dev Biol 120(1):270–283

    CAS  Article  PubMed  Google Scholar 

  • Baylies MK, Bate M (1996) twist: a myogenic switch in Drosophila. Science 272:1481

    CAS  Article  PubMed  Google Scholar 

  • Cho SJ, Vallès Y, Giani VC Jr, Seaver EC, Weisblat DA (2010) Evolutionary dynamics of the wnt gene family: a lophotrochozoan perspective. Mol Biol Evol 27(7):1645–1658

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Dill KK, Thamm K, Seaver EC (2007) Characterization of twist and snail gene expression during mesoderm and nervous system development in the polychaete annelid Capitella sp. I. Dev Genes Evol 217:435–447

    Article  PubMed  Google Scholar 

  • Farooq M, Choi J, Seoane AI, Lleras RA, Tran HV, Mandal SA, Nelson CL, Soto JG (2012) Identification of 3'UTR sequence elements and a teloplasm localization motif sufficient for the localization of Hro-twist mRNA to the zygotic animal and vegetal poles. Develop Growth Differ 54(4):519–534

    CAS  Article  Google Scholar 

  • Gline SE, Nakamoto A, Cho SJ, Chi C, Weisblat DA (2011) Lineage analysis of micromere 4d, a super-phylotypic cell for Lophotrochozoa, in the leech Helobdella and the sludgeworm Tubifex. Dev Biol 353:120–133

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hamamori Y, Wu HY, Sartorelli V, Kedes L (1997) The basic domain of myogenic basic helix-loop-helix (bHLH) proteins is the novel target for direct inhibition by another bHLH protein, twist. Mol Cell Biol 17:6563–6573

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kang Y, Massagué J (2004) Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118(3):277–279

    CAS  Article  PubMed  Google Scholar 

  • Kang D, Huang F, Li D, Shankland M, Gaffield W, Weisblat DA (2003) A hedgehog homolog regulates gut formation in leech (Helobdella). Development 130:1645–1657

    CAS  Article  PubMed  Google Scholar 

  • Kuo DH, Weisblat DA (2011) Intermediate filament genes as differentiation markers in the leech Helobdella. Dev Genes Evol 221(4):225–240

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kutschera U, Langguth H, Kuo DH, Weisblat DA, Shankland M (2013) Description of a new leech species from North America, Helobdella austinensis n. sp. (Hirudinea: Glossiphoniidae), with observations on its feeding behaviour. Zoosyst Evol 89:239–246

    Article  Google Scholar 

  • Leptin M (1991) twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev 5:1568–1576

    CAS  Article  PubMed  Google Scholar 

  • Nederbragt AJ, Lespinet O, Van Wageningen S, Van Loon AE, Adoutte A, Dictus WJ (2002) A lophotrochozoan twist gene is expressed in the ectomesoderm of the gastropod mollusk Patella vulgata. Evol Dev 4:334–343

    CAS  Article  PubMed  Google Scholar 

  • Nelson BH, Weisblat DA (1991) Conversion of ectoderm to mesoderm by cytoplasmic extrusion in leech embryos. Science 253(5018):435–438

    CAS  Article  PubMed  Google Scholar 

  • Nelson BH, Weisblat DA (1992) Cytoplasmic and cortical determinants interact to specify ectoderm and mesoderm in the leech embryo. Development 115(1):103–115

    CAS  PubMed  Google Scholar 

  • O’Rourke MP, Soo K, Behringer RR, Hui CC, Tam PP (2002) Twist plays an essential role in FGF and SHH signal transduction during mouse limb development. Dev Biol 248(1):143–156

    Article  PubMed  Google Scholar 

  • Price AL, Patel NH (2008) Investigating divergent mechanisms of mesoderm development in arthropods: the expression of Ph-twist and Ph-mef2 in Parhyale hawaiensis. J Exp Zool B Mol Dev Evol 310:24–40

    Article  PubMed  Google Scholar 

  • Sablitzky F (2005) Proteins motifs: the helix motif. eLS

  • Simpson P (1983) Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics 105:615–632

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soto JG, Nelson BH, Weisblat DA (1997) A leech homolog of twist: evidence for its inheritance as maternal mRNA. Gene 199(1–2):31–37

    CAS  Article  PubMed  Google Scholar 

  • Thisse B, Stoetzel C, Gorostiza-Thisse C, Perrin-Schmitt F (1988) Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 7(7):2175–2183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weisblat DA, Huang FZ (2001) An overview of glossiphoniid leech development. Can J Zool 79:218–232

    Article  Google Scholar 

  • Weisblat DA, Kuo DH (2014) Developmental biology of the leech Helobdella. J Dev Biol 58:429–443

    CAS  Article  Google Scholar 

  • Weisblat DA, Shankland M (1985) Cell lineage and segmentation in the leech. Philos Trans R Soc Lond Ser B Biol Sci 312:39–56

    CAS  Article  Google Scholar 

  • Weisblat DA, Kim SY, Stent GS (1984) Embryonic origins of cells in the leech Helobdella triserialis. Dev Biol 104:65–85

    CAS  Article  PubMed  Google Scholar 

  • Woodruff JB, Mitchell BJ, Shankland M (2007) Hau-Pax3/7A is an early marker of leech mesoderm involved in segmental morphogenesis, nephridial development, and body cavity formation. Dev Biol 306(2):824–837

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank members of the Weisblat Lab for advice and support. This work was supported by the National Institute of Health [NIH R01 grant GM 074619 to DAW], “Cooperative Research Program for Agriculture Science and Technology Development [Project No. PJ011661]” Rural Development Administration, and by a grant from the Collaborative Genome Program (20140428) funded by the Ministry of Oceans and Fisheries, Republic of Korea. This work was supported by the research grant of the Chungbuk National University in 2014.

Author information

Affiliations

Authors

Corresponding authors

Correspondence to David A. Weisblat or Sung-Jin Cho.

Additional information

Communicated by Mark Q. Martindale

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kim, JS., Jiménez, B.I.M., Kwak, HJ. et al. Spatiotemporal expression of a twist homolog in the leech Helobdella austinensis . Dev Genes Evol 227, 245–252 (2017). https://doi.org/10.1007/s00427-017-0585-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-017-0585-4

Keywords

  • Mesoderm
  • Lophotrochozoa
  • twist gene
  • Leech