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A thymosin beta15-like peptide promotes intersegmental myotome extension in the chicken embryo

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Abstract

Beta-thymosins constitute a group of small actin-sequestering peptides. These highly conserved peptides are involved in cytoskeleton dynamics and can influence different cell properties such as motility, substrate adhesion, shape and chemotaxis. As a marker for tumour metastasis, the mammalian thymosin beta15 is believed to have an important diagnostic relevance in cancer prognosis, although little is known about its physiological function. In order to study the role of thymosin beta15 avian in embryogenesis, we cloned the chicken and quail orthologues of thymosin beta15 and used the chicken as a model for vertebrate development. Avian thymosin beta15, the first known non-mammalian thymosin beta15-like gene, encodes a peptide that possesses a cysteine at position one after the methionine which is a significant difference compared to its mammalian counterparts. Thymosin beta15 avian expression starts at an early stage of development. The expression pattern changes rapidly with development and differs from that of the related thymosin beta4 gene. The most prominent expression domain is seen in developing muscles of limbs and trunk. Gain-of-function experiments revealed that thymosin beta15avian has a function in normal myotome development. Ectopic over-expression of thymosin beta15 avian leads to premature elongation of myotome cells trespassing segment borders. We conclude that thymosin beta15 avian has a still undescribed function in promoting myocyte elongation.

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Acknowledgments

The authors want to thank Meike Ast-Dumbach, Günter Frank, Ellen Gimbel, Rana Houmany, Susanna Konradi, Lydia Koschny, Marion Otto, Ulrike Pein and Swantje Wulf for their excellent technical assistance, Kewal Krishan for fibroblast preparation and Alexander Bonafede, Fangping Dai, Rizwan Rehimi and Daniel Bemmerl for helpful support. The project was kindly supported by the EU’s 6th framework programme MYORES (511978) and by the DFG (BR 957/5-3 and GRK 1104 to B.B.-S.).

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Author notes

  1. Beate Brand-Saberi

    Present address: Institute of Anatomy and Molecular Embryology, Ruhr-University Bochum, Universitätsstrasse 150, 44780, Bochum, Germany

Authors and Affiliations

  1. Institute of Anatomy and Molecular Embryology, Ruhr-University Bochum, Universitätsstrasse 150, 44780, Bochum, Germany

    Verena Chankiewitz, Gabriela Morosan-Puopolo & Faisal Yusuf

  2. Department of Molecular Embryology, Institute of Anatomy and Cell Biology, University of Freiburg, Albertstrasse 17, 79104, Freiburg, Germany

    Stefan Rudloff, Felicitas Pröls & Beate Brand-Saberi

  3. Institute of Anatomy, University Hospital Essen, Essen, Germany

    Veronika Kleff

  4. Department of General Zoology and Neurobiology, Ruhr-University Bochum, Bochum, Germany

    Dietrich Kurt Hofmann

Authors
  1. Verena Chankiewitz
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  2. Gabriela Morosan-Puopolo
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  3. Faisal Yusuf
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  4. Stefan Rudloff
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  5. Felicitas Pröls
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  6. Veronika Kleff
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  7. Dietrich Kurt Hofmann
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  8. Beate Brand-Saberi
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Corresponding author

Correspondence to Beate Brand-Saberi.

Additional information

GenBank accession numbers: DQ 867000 and FJ 185173.

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418_2013_1156_MOESM1_ESM.tif

Supplementary Figure 1: Immunohistochemical detection of thymosin beta15. The photographs show transversal paraffin sections of a HH stage 22 chicken embryo, stained with first antibody against. Thymosin beta15 (a) and unstained negative control after omission of first antibody (b). The myotome (my), neural tube (nt), and limb bud mesenchyme (lb) are specifically and strongly stained for thymosin beta15 in (a). Bar: 200 μm (TIFF 45762 kb)

418_2013_1156_MOESM2_ESM.doc

Supplementary Table 1 Synopsis of thymosin beta15 avian expression in comparison with thymosin beta4 during avian development. The main difference is the mutually exclusive expression of thymosin beta15 avian in skeletal muscle and of thymosin beta4 in endothelia of blood vessels (DOC 30 kb)

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Chankiewitz, V., Morosan-Puopolo, G., Yusuf, F. et al. A thymosin beta15-like peptide promotes intersegmental myotome extension in the chicken embryo. Histochem Cell Biol 141, 275–287 (2014). https://doi.org/10.1007/s00418-013-1156-z

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