Developmental mechanisms of migratory muscle precursors in medaka pectoral fin formation
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.
KeywordsFish fin muscle Myogenesis lbx1 Migratory muscle precursors Medaka
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.
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.
- Cole NJ, Hall TE, Don EK et al (2011) Development and evolution of the muscles of the pelvic fin. PLoS Biol 9:e1001168Google Scholar
- Dietrich S, Schubert FR, Healy C et al (1998) Specification of the hypaxial musculature. Development 125:2235–2249Google Scholar
- Itoh N, Mima T, Mikawa T (1996) Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122:291–300Google Scholar
- Li S, Muneoka K (1999) Cell migration and chick limb development: chemotactic action of FGF-4 and the AER. Dev Biol 211:335–347Google 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 1:1731–1736Google Scholar
- Robson LG, Hughes SM (1996) The distal limb environment regulates MyoD accumulation and muscle differentiation in mouse-chick chimæric limbs. Development 122:3899–3910Google 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 272:23407–23417Google 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 209:206–216Google 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 8:171Google Scholar
- 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 122:2163–2171Google Scholar