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Int J Dev Biol
2017 Jan 01;611-2:17-27. doi: 10.1387/ijdb.160370mm.
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Models of amphibian myogenesis - the case of Bombina variegata.
Kiełbwna L
,
Migocka-Patrzałek M
.
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Several different models of myogenesis describing early stages of amphibian paraxial myotomal myogenesis are known. Myoblasts of Xenopus laevis and Hymenochirus boettgeri change their position from perpendicular to parallel, in relation to axial organs, and differentiate into mononucleate myotubes. In Bombina variegate the myotomal myoblasts change their shape from round to elongate and then differentiate into mononuclear, morphologically mature myotubes. In Pelobates fuscus and Triturus vulgaris, myoblasts fuse into multinuclear myotubes. Mono- and multinucleate myotubes achieve morphological maturity during the differentiation process. During myogenesis of B. variegata, the nuclei of mononucleate, differentiating myotubes contain a tetraploid quantity of DNA (4C DNA). The stable quantity of DNA is confirmed by lack of 3 H-thimidine incorporation into myotube nuclei. This outcome is a proof that myoblasts withdraw from the cell cycle in the G2 phase. The further development of myotomal myotubes involves myoblasts of mesenchymal origin. These myoblasts fuse with myotubes in X. laevis and B. variegate in the G1 phase. Secondary muscle fibres in amphibian myotomes have only mesenchymal origin. Mesenchymal myoblasts fuse into multinucleated myotubes. Myofibril development in the differentiating myotube and lack of DNA replication confirm the classical paradigm of myogenesis. Mesenchymal myoblasts are taking part in the myogenesis of musculus rectus abdominis and limb muscles. The mesenchymal cells in the myogenesis process show one model of myogenesis, which is a classical model of myogenesis. The mesenchymal cells probably come from dermatome.
Fig. 1. Different models of myotomal myogenesis. Consecutive stages of muscle fibre differentiation from left to right. (A) Xenopus laevis. Cell rotation. Differentiation of mononucleate myotubes, in myotube several mature myofibrils. On myotube surface elongated mesenchymal cells. In myotube one primary large nucleus and smaller secondary, mesenchymal nuclei. (B) Bombina variegata. In somite compact groups of rounded cells. Myoblasts change shape, elongate to occupy the whole myotome length. Near myotubes mesenchymal cells present. Nuclei in myotube differ in size: primary nucleus is larger, secondary, mesenchymal nuclei are smaller. Transversely striated myofibrils. (C) Pelobates fuscus. In somite compact group of polymorphic rounded cells. Linearly arranged myoblasts fuse into myotubes of several nuclei. Myotubes differentiate, a few mature myofibrils. After mesenchymal cells have immigrated into myotomes, the number of nuclei in myotubes increases. More numerous mature myofibrils (Kiełbówna, 1981). (D) Triturus vulgaris. Rosette-shaped somites. Fusing myoblasts most often form binucleate myotubes. Myotubes grow and differentiate, several striated myofibrils. Elongated mesenchymal cells appear on myotube surface. Number of nuclei in myotubes increases; length of differentiating myotubes increases as well, more numerous mature myofibrils (Daczewska & Kiełbówna, 2000).
Fig. 2. Histograms of DNA content in nuclei at various stages of myotomal myogenesis Bombina variegate. (A) diploid DNA content in erythrocyte nuclei (control). (B) DNA in cells of non-segmented mesoderm. Two classes of nuclei: diploid and tetraploid. (C) tetraploid DNA content in youngest myotomal myoblasts at stage 28. (D) tetraploid DNA content in paracephalic myotomal myotubes at stage 28. (E) DNA in mononucleate myotubes of swimming tadpoles, stage 41. (F) DNA in polykaryocytes. Primary nuclei in tetraploid class, secondary nuclei of mesenchymal origin in diploid class (Kiełbówna and Kościelski, 1979).
Fig. 3. Histograms of DNA content in nuclei of differentiating cells of limb muscle of Xenopus laevis. (A) diploid DNA content in nuclei of elongated myoblasts prior to fusion. (B) diploid class of nuclei in myotubes. (C) DNA in dividing mesenchymal cells. Diploid class of nuclei in post-mitotic phase, tetraploid class pre-mitotic (Kiełbówna, 1980).
