The Ontogenetic Development of the Somatic Musculature of the Trunk of the Aglossal Anuran Xenopus Laevis (Daudin)

Ryke, P.A.J.

doi:10.1111/j.1463-6395.1953.tb00367.x

Cited by 34 publications

(43 citation statements)

References 18 publications

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“…Although remodeling of the hypaxial musculature occurs during metamorphosis in biphasic anurans (23,24), there is no direct evidence in the literature for the role of TH in this event in any frog. In our investigation of E. coqui, methimazole prevented ventral convergence of the rectus abdominis, posterior extension of the pectoral muscles, and extension of the lateral muscle bands.…”

Section: Discussionmentioning

confidence: 99%

“…This is coincident with the repositioning of the rectus abdominis muscle bands from their initial lateral position to a more ventral one and also with the growth of the body musculature (22). Because in tadpoles this ventral convergence of the rectus abdominis occurs during metamorphosis (23,24), the axial musculature was examined to determine whether this event is TH dependent in E. coqui (Fig. 3 K-M).…”

Section: Establishment Of Assay Conditionsmentioning

confidence: 99%

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Thyroid hormone-dependent metamorphosis in a direct developing frog

Callery

Elinson

2000

Proc. Natl. Acad. Sci. U.S.A.

111

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The direct developing anuran, Eleutherodactylus coqui, lacks a tadpole, hatching as a tiny frog. We investigated the role of the metamorphic trigger, thyroid hormone (TH), in this unusual ontogeny. Expression patterns of the thyroid hormone receptors, TR␣ and TR␤, were similar to those of indirect developers. TR␤ mRNA levels increased dramatically around the time of thyroid maturation, when remodeling events reminiscent of metamorphosis occur. Treatment with the goitrogen methimazole inhibited this remodeling, which was reinitiated on cotreatment with TH. Despite their radically altered ontogeny, direct developers still undergo a TH-dependent metamorphosis, which occurs before hatching. We propose a new model for the evolution of anuran direct development.T he term ''amphibian'' conveys the image of a dual life history, split between water and land. However, 29 different anuran reproductive modes have been defined, on the basis of the site of egg development (1). Included in this developmental smorgasbord are species in which the larvae develop inside a foam nest (Chiromantis), those that brood live embryos in their stomach (Rheobatrachus), ''marsupial frogs'' in which the tadpoles develop within a parental pouch (Gastrotheca), and the most extreme modification, direct development, where the freeliving larva has been deleted from the life history (Eleutherodactylus).Direct development in Eleutherodactylus is a derived characteristic (2), yet embryogenesis in these frogs is so radically modified that little hint of their biphasic metamorphic ancestry is visible. Development is entirely terrestrial, with tiny froglets hatching from their jelly capsules 3 wk after fertilization. Many larval characteristics are lacking, including cement gland, lateral line organs, coiled gut, larval mouth parts, and some cranial cartilages (3). The only obviously larval feature is the tail, which shrinks before hatching.The ontogenetic modifications responsible for direct development are unknown. Because direct developers are thought to have evolved from biphasic frogs (1, 2), the role of thyroid hormone (TH) in direct development is of particular interest. TH, shown in other systems to signal through thyroid hormone receptors (TRs), controls the larval-to-adult transition in biphasic frogs (4). TR␤ expression in both Xenopus laevis and Rana catesbeiana is temporally correlated with the onset of metamorphosis, implicating this gene as a likely metamorphic mediator (5-7). The role of TH in direct development is unclear. Both chemical and surgical ablation of the thyroid axis in Eleutherodactylus martinicensis inhibited tail regression and pronephric degeneration (8, 9). These events were precociously induced by 3,3Ј,5-triiodothyronine (T 3 ) treatment, but other organ systems appeared unaffected (8). Although the similarity between such degenerative changes in Eleutherodactylus and those occurring in metamorphosis was noted, the specificity of effects caused by drug treatment was questioned. It was thought likely by these authors tha...

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Section: Discussionmentioning

confidence: 99%

Section: Establishment Of Assay Conditionsmentioning

confidence: 99%

Thyroid hormone-dependent metamorphosis in a direct developing frog

Callery

Elinson

2000

Proc. Natl. Acad. Sci. U.S.A.

111

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“…The first fate corresponds to early embryonic death and occurs in the cranial-most myotomal muscles. Fibers from these myotomes are the first in the embryo to differentiate and in Xenopus they even become innervated and functional (Ryke, 1938;Smit, 1953;Regel and Epstein, 1972;Blackshaw and Warner, 1976a; Review in . They also undergo autonomous, programmed cell death in a cranial/ caudal sequence beginning at approximately stage 26 and ending by stage 52 (Ryke, 1938;Smit, 1953;Chung et al, 1989).…”

Section: Existence Of Different Skeletal Muscle Fatesmentioning

confidence: 99%

“…Fibers from these myotomes are the first in the embryo to differentiate and in Xenopus they even become innervated and functional (Ryke, 1938;Smit, 1953;Regel and Epstein, 1972;Blackshaw and Warner, 1976a; Review in . They also undergo autonomous, programmed cell death in a cranial/ caudal sequence beginning at approximately stage 26 and ending by stage 52 (Ryke, 1938;Smit, 1953;Chung et al, 1989). For a long time, it has been postulated that trunk myotome muscles display a second fate, that is persistent through adulthood (Ryke, 1938).…”

Section: Existence Of Different Skeletal Muscle Fatesmentioning

confidence: 99%

“…They also undergo autonomous, programmed cell death in a cranial/ caudal sequence beginning at approximately stage 26 and ending by stage 52 (Ryke, 1938;Smit, 1953;Chung et al, 1989). For a long time, it has been postulated that trunk myotome muscles display a second fate, that is persistent through adulthood (Ryke, 1938). However, it has been shown recently that trunk myotome muscles as well as adductor jaw muscles die during metamorphosis and are progressively replaced by new adult muscles (Alley, 1989;Nishikawa andHayashi, 1994, 1995).…”

Section: Existence Of Different Skeletal Muscle Fatesmentioning

confidence: 99%

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Xenopusmuscle development: From primary to secondary myogenesis

Chanoine

Hardy

2002

Developmental Dynamics

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Xenopus myogenesis is characterized by specific features, different from those of mammalian and avian systems both at the cellular level and in gene expression patterns. During early embryogenesis, after the initial molecular signals inducing mesoderm, the myogenic determination factors XMyoD and XMyf-5 are activated in presomitic mesoderm in response to mesoderm-inducing factors. After these first inductions of the myogenic program, forming muscles in Xenopus can have different destinies, some of these resulting in cell death before adulthood. In particular, it is quite characteristic of this species that, during metamorphosis, the primary myotomal myofibers completely die and are progressively replaced by secondary "adult" multinucleated myofibers. This feature offers the unique opportunity to totally separate the molecular analysis of these two distinct types of myogenesis. The aim of this review is to summarize our knowledge on the cellular and molecular events as well as the epigenetic regulations involved in the construction of Xenopus muscles during development. Developmental Dynamics 226:12-23, 2003.

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Development and innervation of the abdominal muscle in embryonic Xenopus laevis

Lynch

1990

Am. J. Anat.

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The morphogenesis and innervation of the ventral abdominal musculature in Xenopus embryos was examined using microscopic techniques. Muscle development begins at Nieuwkoop and Faber Stage 31, when aggregates of undifferentiated cells form on the ventrolateral margins of rostral trunk myotomes. During subsequent stages, aggregates form and detach from progressively more caudal myotomes to form a series of seven discrete cell clusters (anlagen). The anlagen migrate ventrally in a cell-free space between the epidermis and a subepidermal layer of pigment cells. Extracellular aggregates of 30-nm granules are evident transiently between the migrating anlagen and the epidermis. During stages 39 and 40, each anlage transforms into a sheet of myotubes which attaches rostrally and caudally to adjacent sheets to form a seven-segmented muscle. The series of broad segments, approximately one fiber thick, extends from the pericardium to the level of the proctodeum. The embryonic muscle is innervated by the ventral rami of spinal nerves 2 to 9. The major nerve trunks to the muscle develop between stages 35/36 and 40. Axons initially grow ventrally along the paths taken by the muscle anlagen. When the anlagen become muscle segments, the nerves are deep to the narrow boundaries between the segments. Spinal nerve 2 ramifies in the first muscle segment and sends fibers rostrally to the geniohyoid muscle. The findings represent the first description of the development of this muscle in Xenopus and the first account of the development of the abdominal motor nerves in an amphibian embryo.

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The Ontogenetic Development of the Somatic Musculature of the Trunk of the Aglossal Anuran Xenopus Laevis (Daudin)

Cited by 34 publications

References 18 publications

Thyroid hormone-dependent metamorphosis in a direct developing frog

Thyroid hormone-dependent metamorphosis in a direct developing frog

Xenopusmuscle development: From primary to secondary myogenesis

Development and innervation of the abdominal muscle in embryonic Xenopus laevis

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