Stages in the normal development of Rana pipiens larvae

Taylor, Alan C.; Kollros, Jerry J.

doi:10.1002/ar.1090940103

Cited by 1,414 publications

(354 citation statements)

References 8 publications

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“…T 3 treatment rescued these suturing events (Fig. 3F), which have an intriguing parallel in biphasic frogs, where ventral suturing occurs in the corresponding region after the limbs burst through the operculum during metamorphic climax (25,26).…”

Section: Establishment Of Assay Conditionsmentioning

confidence: 81%

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: Establishment Of Assay Conditionsmentioning

confidence: 81%

Thyroid hormone-dependent metamorphosis in a direct developing frog

Callery

Elinson

2000

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

111

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“…Tadpoles and adults of the bullfrog Rana catesbeiana were collected from ponds in Ibaraki Prefecture, Japan. The developmental stages of the tadpoles were estimated according to the criteria of Taylor and Kollros [21]. Body masses of tadpoles (stages XϪXXV) and adult frogs ranged from 10 g to 20 g and from 400 g to 500 g, respectively.…”

Section: Methodsmentioning

confidence: 99%

Structural characteristics of bullfrog (Rana catesbeiana) transthyretin and its cDNA

Yamauchi

Takeuchi

Overall

et al. 1998

European Journal of Biochemistry

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Transthyretin, an extracellular thyroid-hormone-binding protein (THBP) in higher vertebrates, is synthesized and secreted by the choroid plexus of all classes of vertebrates, except fish and amphibians, and synthesized in the liver of endothermic animals. Here, we report the nucleotide sequence of the cDNA for a THBP found in plasma of bullfrog (Rana catesbeiana) tadpoles before the climax of metamorphosis.The amino acid sequence clearly shows this protein to be an amphibian transthyretin. The three-dimensional structure of bullfrog transthyretin was derived using homology modeling. Compared with transthyretins from other vertebrate species, bullfrog transthyretin is highly conserved at the thyroid hormonebinding sites and other important structural regions of the subunits. Bullfrog transthyretin mRNA was found in tadpole liver, but not in tadpole choroid plexus. Thus, during evolution, synthesis of transthyretin in the liver of metamorphosing amphibians preceded that in the choroid plexus of reptiles, birds and mammals. It was previously observed that the protein most abundantly synthesized and secreted by the choroid plexus in adult amphibians is a lipocalin [Achen, M. G., Harms, P. J., Thomas, T., Richardson, S. J., Wettenhall, R. E. H. & Schreiber, G. (1992) J. Biol. Chem. 267, 23170Ϫ23 174], in contrast to transthyretin being the most abundantly synthesized and secreted protein in the choroid plexus of mammals, birds and reptiles. Lipocalin mRNA was found in large amounts in tadpole choroid plexus, but not livers. Keywords : transthyretin; lipocalin ; metamorphosis; bullfrog (Rana catesbeiana).Amphibian metamorphosis can be induced by both thyroxine and 3,3′,5-triiodothyronine [1], and is regulated via the hypothalamus-pituitary-thyroid gland axis, which is established just before the onset of metamorphosis [2]. The concentration of thyroid hormones in the blood increases gradually during prometamorphosis, reaches a maximum level at the beginning of metamorphic climax, and then decreases and ceases to be detectable at the end of metamorphosis [3,4]. Thyroid hormone receptors, the genes of which are thought to be among the earliest genes responding to the elevation of thyroid hormone concentration in blood plasma, are upregulated in several tissues during both spontaneous and induced metamorphosis [5,6], and in cell-culture systems [7,8]. Thus, amphibian metamorphosis has provided a good model for analyzing the control of gene expression by thyroid hormones [9Ϫ11]. However, it is still unclear how thyroid hormones are delivered to target cells. Previously, the presence of a thyroid hormone-binding protein (THBP) in blood plasma from metamorphosing Rana catesbeiana (bullfrog) tadpoles had been described [12]. This THBP had a higher affinity Correspondence to K. Yamauchi,

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“…The developmental stage of each animal was identified according to the criteria of TAYLOR and KOLLROS (13). Tadpoles which developed too quickly or too slowly were not used for the experiments.…”

Section: Methodsmentioning

confidence: 99%

Hormones Controlling Collagen Synthesis During Metamorphosis in the Thigh Bone of the Tadpole of Rana Catesbeiana

Yamaguchi¹,

Yasumasu²

1977

Dev Growth Differ

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The rate of ''C-proline incorporation into collagen in the thigh bone of the Runa catesbeiana tadpole was determined in vitro. Intraperitoneal injection of bovine prolactin caused an increase in the rgte of collagen synthesis during the premetamorphic stages (stages 12-16) and the early metamorphic stage (stage 18), but it exerted no effect on collagen synthesis in the metamorphic stages (stages 20-25). On the other hand, injection of growth hormone stimulated the rate of collagen synthesis in the metamorphic stages and caused a slight increase in the premetamorphic stages. When a tadpole in the early premetamorphic stages (stages 12-14) was kept in 5 X lo-* M thyroxine solution for several days, the rate of collagen synthesis became higher than that in the bone of the control animal. The rate of collagen synthesis was not enhanced by prolactin in the thyroxine-treated tadpole, but was stimulated by growth hormone, even when the thyroxinetreated animal remained in the premetamorphic stages. With the treatment of the tadpole by thyroxine, prolactin-sensitivity seems to be reduced, and growth hormone-sensitivity becomes apparent.

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Stages in the normal development of Rana pipiens larvae

Cited by 1,414 publications

References 8 publications

Thyroid hormone-dependent metamorphosis in a direct developing frog

Thyroid hormone-dependent metamorphosis in a direct developing frog

Structural characteristics of bullfrog (Rana catesbeiana) transthyretin and its cDNA

Hormones Controlling Collagen Synthesis During Metamorphosis in the Thigh Bone of the Tadpole of Rana Catesbeiana

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