Skip to main content

Advertisement

SpringerLink
Log in

Developmental mechanisms of migratory muscle precursors in medaka pectoral fin formation

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

Limb muscles are formed from migratory muscle precursor cells (MMPs) that delaminate from the ventral region of dermomyotomes and migrate into the limb bud. MMPs remain undifferentiated during migration, commencing differentiation into skeletal muscle after arrival in the limb. However, it is still unclear whether the developmental mechanisms of MMPs are conserved in teleost fishes. Here, we investigate the development of pectoral fin muscles in the teleost medaka Oryzias latipes. Expression of the MMP marker lbx1 is first observed in several somites prior to the appearance of fin buds. lbx1-positive cells subsequently move anteriorly and localize in the prospective fin bud region to differentiate into skeletal muscle cells. To address the developmental mechanisms underlying fin muscle formation, we knocked down tbx5, a gene that is required for fin bud formation. tbx5 morphants showed loss of fin buds, whereas lbx1 expression initiated normally in anterior somites. Unlike in normal embryos, expression of lbx1 was not maintained in migrating fin MMPs or within the fin buds. We suggest that fin MMPs appear to undergo two phases in their development, with an initial specification of MMPs occurring independent of fin buds and a second fin bud-dependent phase of MMP migration and proliferation. Our results showed that medaka fin muscle is composed of MMPs. It is suggested that the developmental mechanism of fin muscle formation is conserved in teleost fishes including medaka. Through this study, we also propose new insights into the developmental mechanisms of MMPs in fin bud formation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Ahn D, Kourakis MJ, Rohde LA, Silver LM, Ho RK (2002) T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature 417:754–758

    Article  PubMed  CAS  Google Scholar 

  • Alvares E, Schubert FR, Thorpe C et al (2003) Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors. Dev Cell 5:379–390

    Article  PubMed  CAS  Google Scholar 

  • Birchmeier C, Brohmann H (2000) Genes that control the development of migrating muscle precursor cells. Curr Opin Cell Biol 12:725–730

    Article  PubMed  CAS  Google Scholar 

  • Bladt F, Riethmacher D, Isenmann S, Aguzzi A, Birchmeier C (1995) Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376:768–771

    Article  PubMed  CAS  Google Scholar 

  • Bober E, Franz T, Arnold H et al (1994) Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120:603–612

    PubMed  CAS  Google Scholar 

  • Bryson-Richardson RJ, Currie PD (2008) The genetics of vertebrate myogenesis. Nat Rev Genet 9:632–646

    Article  PubMed  CAS  Google Scholar 

  • Chevallier BA, Kieny M, Mauger A (1977) Limb-somite relationship: origin of the limb musculature. J Embryol Exp Morphol 41:245–258

    PubMed  CAS  Google Scholar 

  • Christ B, Jacob HJ, Jacob M (1977) Experimental analysis of the origin of the wing musculature in avian embryos. Anat Embryol 150:171–186

    Article  PubMed  CAS  Google Scholar 

  • Cohn MJ, Izpisúa-Belmonte JC, Abud H, Heath JK, Tickle C (1995) Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 80:739–746

    Article  PubMed  CAS  Google Scholar 

  • Cole NJ, Hall TE, Don EK et al (2011) Development and evolution of the muscles of the pelvic fin. PLoS Biol 9:e1001168

  • Dietrich S, Schubert FR, Healy C et al (1998) Specification of the hypaxial musculature. Development 125:2235–2249

  • Dietrich S, Abou-Rebyeh F, Brohmann H, Bladt F, Sonnenberg-Riethmacher E, Yamaai T, Lumsden A, Brand-Saberi B, Birchmeier C (1999) The role of SF/HGF and c-Met in the development of skeletal muscle. Development 126:1621–1629

    PubMed  CAS  Google Scholar 

  • Grandel H, Draper BW, Schulte-Merker S (2000) Dackel acts in the ectoderm of the zebrafish pectoral fin bud to maintain AER signaling. Development 127:4169–4178

    PubMed  CAS  Google Scholar 

  • Haines L, Neyt C, Gautier P, Keenan DG, Bryson-Richardson RJ, Hollway GE, Cole NJ, Currie PD (2004) Met and Hgf signaling controls hypaxial muscle and lateral line development in the zebrafish. Development 131:4857–4869

    Article  PubMed  CAS  Google Scholar 

  • Heymann S, Koudrova M, Arnold H-H, Köster M, Braun T (1996) Regulation and function of SF/HGF during migration of limb muscle precursor cells in chicken. Dev Biol 180:566–578

    Article  PubMed  CAS  Google Scholar 

  • Itoh N, Mima T, Mikawa T (1996) Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122:291–300

  • Iwamatsu T (2004) Stages of normal development in the medaka Oryzias latipes. Mech Dev 121:605–618

    Article  PubMed  CAS  Google Scholar 

  • Jagla K, Dolle P, Mattei M-G et al (1995) Mouse Lbxl and human LBXI define a novel mammalian homeobox gene family related to the Drosophila lady bird genes. Mech Dev 53:345–356

    Article  PubMed  CAS  Google Scholar 

  • Kusakabe R, Kusakabe T, Suzuki N (1999) In vivo analysis of two striated muscle actin promoters reveals combinations of multiple regulatory modules required for skeletal and cardiac muscle-specific gene expression. Int J Dev Biol 43:541–554

    PubMed  CAS  Google Scholar 

  • Kusakabe R, Kuraku S, Kuratani S (2011) Expression and interaction of muscle-related genes in the lamprey imply the evolutionary scenario for vertebrate skeletal muscle, in association with the acquisition of the neck and fins. Dev Biol 350:217–227

    Article  PubMed  CAS  Google Scholar 

  • Li S, Muneoka K (1999) Cell migration and chick limb development: chemotactic action of FGF-4 and the AER. Dev Biol 211:335–347

  • Lukowski CM, Drummond DL, Waskiewicz AJ (2011) Pbx-dependent regulation of lbx gene expression in developing zebrafish embryos. Genome 54:973–985

    Article  PubMed  CAS  Google Scholar 

  • Martin BL, Harland RM (2006) A novel role for lbx1 in Xenopus hypaxial myogenesis. Development 133:195–208

    Article  PubMed  CAS  Google Scholar 

  • Mennerich D, Schäfer K, Braun T (1998) Pax-3 is necessary but not sufficient for lbx1 expression in myogenic precursor cells of the limb. Mech Dev 73:147–158

    Article  PubMed  CAS  Google Scholar 

  • Neyt C, Jagla K, Thisse C, Thisse B, Haines L, Currie PD (2000) Evolutionary origins of vertebrate appendicular muscle. Nature 408:82–86

    Article  PubMed  CAS  Google Scholar 

  • Ochi H, Westerfield M (2009) Lbx2 regulates formation of myofibrils. BMC Dev Biol 9:13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Okamoto E, Kusakabe R, Kuraku S et al (2017) Migratory appendicular muscles precursor cells in the common ancestor to all vertebrates. Nat Ecol Evol 1:1731–1736

  • Robson LG, Hughes SM (1996) The distal limb environment regulates MyoD accumulation and muscle differentiation in mouse-chick chimæric limbs. Development 122:3899–3910

  • Ruvinsky I, Oates a C, Silver LM, Ho RK (2000) The evolution of paired appendages in vertebrates: T-box genes in the zebrafish. Dev Genes Evol 210:82–91

    Article  PubMed  CAS  Google Scholar 

  • Sabo MC, Nath K, Elinson RP (2009) Lbx1 expression and frog limb development. Dev Genes Evol 219:609–612

    Article  PubMed  CAS  Google Scholar 

  • Schäfer K, Braun T (1999) Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nat Genet 23:213–216

    Article  PubMed  Google Scholar 

  • Seimiya M, Kusakabe T, Suzuki N (1997) Primary structure and differential gene expression of three membrane forms of guanylyl cyclase found in the eye of the teleost Oryzias latipes. J Biol Chem 272:23407–23417

  • Tani S, Kusakabe R, Naruse K, Sakamoto H, Inoue K (2010) Genomic organization and embryonic expression of miR-430 in medaka (Oryzias latipes): insights into the post-transcriptional gene regulation in early development. Gene 449:41–49

    Article  PubMed  CAS  Google Scholar 

  • Tani S, Kuraku S, Sakamoto H, Inoue K, Kusakabe R (2013) Developmental expression and evolution of muscle-specific microRNAs conserved in vertebrates. Evol Dev 15:293–304

    Article  PubMed  CAS  Google Scholar 

  • Webb SE, Lee KK, Tang MK, Ede DA (1997) Fibroblast growth factors 2 and 4 stimulate migration of mouse embryonic limb myogenic cells. Dev Dyn 209:206–216

  • Windner SE, Steinbacher P, Obermayer A, Kasiba B, Zweimueller-Mayer J, Stoiber W (2011) Distinct modes of vertebrate hypaxial muscle formation contribute to the teleost body wall musculature. Dev Genes Evol 221:167–178

    Article  PubMed  PubMed Central  Google Scholar 

  • Wotton KR, Weierud FK, Dietrich S, Lewis KE (2008) Comparative genomics of Lbx loci reveals conservation of identical Lbx ohnologs in bony vertebrates. BMC Evol Biol 8:171

  • Yang X, Vogan K, Gros P et al (1996) Expression of the met receptor tyrosine kinase in muscle progenitor cells in somites and limbs is absent in Splotch mice. Development 122:2163–2171

  • Yusuf F, Rehimi R, Moroşan-Puopolo G, Dai F, Zhang X, Brand-Saberi B (2006) Inhibitors of CXCR4 affect the migration and fate of CXCR4+ progenitors in the developing limb of chick embryos. Dev Dyn 235:3007–3015

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank National Bio Resource Project Medaka (NBRP Medaka) for providing hatching enzyme. We also thank Dr. Marianne Bronner for valuable comments on the manuscript.

Funding

This study was supported by Grant-in-Aid for JSPS Research Fellow (24-2096), JSPS KAKENHI (16K18551) to STM, and also in part by a research grant from the Takeda Science Foundation to RK.

Author information

Authors and Affiliations

  1. Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodaicho, Nada-ku, Kobe, 657-8501, Japan

    Saori Tani-Matsuhana & Kunio Inoue

  2. Laboratory for Evolutionary Morphology, RIKEN Center for Biosystems Dynamics Research, 2-2-3 Minatojima-minami, Chuo-Ku, Kobe, 650-0047, Japan

    Rie Kusakabe

Authors
  1. Saori Tani-Matsuhana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rie Kusakabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kunio Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Saori Tani-Matsuhana.

Additional information

Communicated by Caroline Brennan

Electronic supplementary material

Fig. S1

Immunostaining with MF20 to detect skeletal muscle in medaka embryos. (a) In stage 33, MF20 signal is observed in trunk muscle and fin bud muscle. (b) In stage 35, MF20 can mark another signal positive band between post fin bud and somites, which seems to be PHM, in addition to trunk and fin bud muscle. (c) In stage 35, lbx1 is expressed in pectoral fin muscle, but not in PHM which is marked with MF20. Dorsal is to the top. Arrows and arrowheads in (a, b) show MF20 signals in pectoral fin buds and PHM, respectively. Arrows in (c) show lbx1-positive cells in pectoral fin buds. (PPTX 1669 kb)

Fig. S2

Expression patterns of tbx5a, tbx5b and dlx2 in medaka embryos. (a) tbx5a, (c) tbx5b and (e) dlx2 around stage 31. tbx5a and tbx5b are expressed in mesenchymal cells of fin buds, and dlx2 is expressed at the AER. (b), (d) and (f) are vertical sections of (a), (c) and (e) at the pectoral fin bud level, respectively. (a, c, e) Dorsal view, anterior is to the top. (b, d, f) Dorsal is to the top. Arrows show the expression signals in pectoral fin buds. Scale bars: 100 μm (a, c, e) or 50 μm (b, d, f) (PPTX 1655 kb)

Fig. S3

tbx5 MOs affect formation of pectoral fin buds in medaka embryos. (a) tbx5a MO was designed to be complementary to the junction of exon2 and intron2. The MO caused exon2 skipping and a frame shift. tbx5b MO was designed to be complementary to the junction of intron2 and exon3. The MO caused a premature stop codon in intron2. Arrows show primers for RT-PCR to check for the transcripts, tbx5a or tbx5b. (b) RT-PCR was performed to detect tbx5a or tbx5b transcripts in tbx5 MOs-injected embryos or uninjected embryos. Black asterisks and white asterisks show normal transcripts and abnormal transcripts, respectively. (c) Embryos injected with tbx5 MOs were inhibited from forming pectoral fin buds whereas uninjected embryos formed normal pectoral fin buds at stage 35 (shown in arrows). (d) dlx2 expression was not observed in prospective fin bud area of stage 31 embryos lacking visible fin bud by tbx5 MOs. (PPTX 1422 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tani-Matsuhana, S., Kusakabe, R. & Inoue, K. Developmental mechanisms of migratory muscle precursors in medaka pectoral fin formation. Dev Genes Evol 228, 189–196 (2018). https://doi.org/10.1007/s00427-018-0616-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-018-0616-9

Keywords

Search

Navigation