Lamprey contractile protein genes mark different populations of skeletal muscles during development

Kusakabe, Rie; Takechi, Masaki; Tochinai, Shin; Kuratani, Shigeru

doi:10.1002/jez.b.20009

Cited by 25 publications

(40 citation statements)

References 42 publications

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“…To address this problem, sequences from the proline residue of coding exon 20 to coding exon 29 in MYH M86-1 and from coding exon 30 to the end in MYH M86-2 were combined for MYHs of cluster A (MYH M86-1ϩ2 ), and the Tetraodon ortholog of torafugu M1876 (GSTENG00021733001 in SCAF14694) was used for the phylogenetic analysis. In addition, the two skeletal MYH sequences of Japanese lamprey (Lethenteron japonicum) reported recently (30) were aligned to consider the evolutionary relationship of MYHs, since it is well known that agnathan lampreys are derived from a common ancestor of gnathostome teleost and tetrapod. The topology obtained from the NJ tree is completely identical to that obtained from the ML tree (Fig.…”

Section: Resultsmentioning

confidence: 99%

Divergent evolution of the myosin heavy chain gene family in fish and tetrapods: evidence from comparative genomic analysis

Ikeda

Ono

Snell

et al. 2007

Physiological Genomics

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Myosin heavy chain genes ( MYHs) are the most important functional domains of myosins, which are highly conserved throughout evolution. The human genome contains 15 MYHs, whereas the corresponding number in teleost appears to be much higher. Although teleosts comprise more than one-half of all vertebrate species, our knowledge of MYHs in teleosts is rather limited. A comprehensive analysis of the torafugu ( Takifugu rubripes) genome database enabled us to detect at least 28 MYHs, almost twice as many as in humans. RT-PCR revealed that at least 16 torafugu MYH representatives (5 fast skeletal, 3 cardiac, 2 slow skeletal, 1 superfast, 2 smooth, and 3 nonmuscle types) are actually transcribed. Among these, MYH M743-2 and MYH M5 of fast and slow skeletal types, respectively, are expressed during development of torafugu embryos. Syntenic analysis reveals that torafugu fast skeletal MYHs are distributed across five genomic regions, three of which form clusters. Interestingly, while human fast skeletal MYHs form one cluster, its syntenic region in torafugu is duplicated, although each locus contains just a single MYH in torafugu. The results of the syntenic analysis were further confirmed by corresponding analysis of MYHs based on databases from Tetraodon, zebrafish, and medaka genomes. Phylogenetic analysis suggests that fast skeletal MYHs evolved independently in teleosts and tetrapods after fast skeletal MYHs had diverged from four ancestral MYHs.

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Section: Resultsmentioning

confidence: 99%

Divergent evolution of the myosin heavy chain gene family in fish and tetrapods: evidence from comparative genomic analysis

Ikeda

Ono

Snell

et al. 2007

Physiological Genomics

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“…4A-C; a full description of the genes and their expression was published in Kusakabe et al, 2004). This gene is first expressed in the myotomes at stage 22, and its initial expression in the cranial muscles was observed at stage 24, when a low level of transcript was identified in the mesenchyme of the cheek process, in the shape of the early upper lip muscle, and the rest of the trigeminal-nerve-innervated muscle group (Fig.…”

Section: Expression Patterns Of Genes Encoding Muscle Actinmentioning

confidence: 98%

“…According to a previous study, this gene is regarded as a marker for upper lip muscle (Fig. 4D), and in the cheek process of a stage 21 embryo, where no differentiation of the upper lip is visible, LjMA1 expression is upregulated only in the dorsal part of the mandibular mesoderm (Kusakabe et al, 2004). Therefore, the upper lip muscle might be specified even before the morphological differentiation of the cheek process into the upper lip and the mandibular-arch subdivisions in the early mandibular mesoderm, by the specific upregulation of LjMA1.…”

Section: Expression Patterns Of Genes Encoding Muscle Actinmentioning

confidence: 99%

Developmental fate of the mandibular mesoderm in the lamprey, Lethenteron japonicum: Comparative morphology and development of the gnathostome jaw with special reference to the nature of the trabecula cranii

et al. 2004

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The vertebrate jaw is a mandibular-arch derivative, and is regarded as the synapomorphy that defines the gnathostomes. Previous studies (Kuratani et al., Phil. Trans. Roy. Soc. 356:15, 2001; Shigetani et al., Science 296:1319, 2002) have suggested that the oral apparatus of the lamprey is derived from both the mandibular and premandibular regions, and that the jaw has arisen as a secondary narrowing of the oral patterning mechanism into the mandibular-arch domain. The heterotopy theory of jaw evolution states that the lamprey upper lip is a premandibular element, leaving further questions unanswered as to the homology of the trabecula in the lamprey and gnathostomes, and to the morphological nature of the muscles in the upper lip. Using focal injection of vital dyes into the cheek process core of lamprey embryos, we found that the upper lip muscle and trabecula are both derived from mandibular mesoderm. Secondary movement of the muscle primordium is also evident when the expression of the early muscle marker gene, LjMA2, is visualized. A nerve-fiber labeling study revealed that the upper lip muscle-innervating neurons are located in the rostral part of the brain stem, where the trigeminal motor nuclei are not found in gnathostomes. We conclude that the lamprey upper lip is composed of premandibular ectomesenchyme and a lamprey-specific muscle component derived from the mandibular mesoderm innervated by lamprey-specific motoneurons. Furthermore, the lamprey trabecula is most likely equivalent to a mesodermally derived neurocranial element, similar to the parachordal element in gnathostomes, rather than to the neural-crest-derived prechordal element.

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“…As OSM and SHM occur in chondrichthyes, but not agnathans (Kusakabe et al, 2004;Chatchavalvanich et al, 2006), it seems that in early bony fish the Pax3/7 and MRF gene families retained substantial evolutionary flexibility, which may have allowed migratory hypaxial muscle to co-evolve with the vertebrate jaw. We speculate that evolution of the jaw occurred concomitant with somite production of OSM/SHM, facilitating voluntary control of swallowing.…”

Section: Genetic Regulation Of Osmmentioning

confidence: 99%

Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion

et al. 2013

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Striated muscles that enable mouth opening and swallowing during feeding are essential for efficient energy acquisition, and are likely to have played a fundamental role in the success of early jawed vertebrates. The developmental origins and genetic requirements of these muscles are uncertain. Here, we determine by indelible lineage tracing in mouse that fibres of sternohyoid muscle (SHM), which is essential for mouth opening during feeding, and oesophageal striated muscle (OSM), which is crucial for voluntary swallowing, arise from Pax3-expressing somite cells. In vivo Kaede lineage tracing in zebrafish reveals the migratory route of cells from the anteriormost somites to OSM and SHM destinations. Expression of pax3b, a zebrafish duplicate of Pax3, is restricted to the hypaxial region of anterior somites that generate migratory muscle precursors (MMPs), suggesting that Pax3b plays a role in generating OSM and SHM. Indeed, loss of pax3b function led to defective MMP migration and OSM formation, disorganised SHM differentiation, and inefficient ingestion and swallowing of microspheres. Together, our data demonstrate Pax3-expressing somite cells as a source of OSM and SHM fibres, and highlight a conserved role of Pax3 genes in the genesis of these feeding muscles of vertebrates.

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Lamprey contractile protein genes mark different populations of skeletal muscles during development

Cited by 25 publications

References 42 publications

Divergent evolution of the myosin heavy chain gene family in fish and tetrapods: evidence from comparative genomic analysis

Divergent evolution of the myosin heavy chain gene family in fish and tetrapods: evidence from comparative genomic analysis

Developmental fate of the mandibular mesoderm in the lamprey, Lethenteron japonicum: Comparative morphology and development of the gnathostome jaw with special reference to the nature of the trabecula cranii

Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion

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