Metamorphosis: Model systems for studying gene expression in postembryonic development

Atkinson, Burr G.

doi:10.1002/dvg.1020150402

Cited by 46 publications

(29 citation statements)

References 84 publications

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“…Given the similarity between postembryonic development in mammals and frog metamorphosis (2,45,50), our results here suggest that the effects of T3 during mammalian postembryonic development are also mediated by TR and that the nongenomic action of T3 is not likely to have a major impact during this period of mammalian development. On the other hand, it is unclear whether the various developmental pheno- FIG.…”

Section: Figmentioning

confidence: 64%

Transgenic Analysis Reveals that Thyroid Hormone Receptor Is Sufficient To Mediate the Thyroid Hormone Signal in Frog Metamorphosis

Buchholz

Tomita

et al. 2004

Molecular and Cellular Biology

120

108

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Thyroid hormone (T3) has long been known to be important for vertebrate development and adult organ function. Whereas thyroid hormone receptor (TR) knockout and transgenic studies of mice have implicated TR involvement in mammalian development, the underlying molecular bases for the resulting phenotypes remain to be determined in vivo, especially considering that T3 is known to have both genomic, i.e., through TRs, and nongenomic effects on cells. Amphibian metamorphosis is an excellent model for studying the role of TR in vertebrate development because of its total dependence on T3. Here we investigated the role of TR in metamorphosis by developing a dominant positive mutant thyroid hormone receptor (dpTR). In the frog oocyte transcription system, dpTR bound a T3-responsive promoter and activated the promoter independently of T3. Transgenic expression of dpTR under the control of a heat shock-inducible promoter in premetamorphic tadpoles led to precocious metamorphic transformations. Molecular analyses showed that dpTR induced metamorphosis by specifically binding to known T3 target genes, leading to increased local histone acetylation and gene activation, similar to T3-bound TR during natural metamorphosis. Our experiments indicated that the metamorphic role of T3 is through genomic action of the hormone, at least on the developmental parameters tested. They further provide the first example where TR is shown to mediate directly and sufficiently these developmental effects of T3 in individual organs by regulating target gene expression in these organs.

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Section: Figmentioning

confidence: 64%

Transgenic Analysis Reveals that Thyroid Hormone Receptor Is Sufficient To Mediate the Thyroid Hormone Signal in Frog Metamorphosis

Buchholz

Tomita

et al. 2004

Molecular and Cellular Biology

120

108

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“…Amphibian metamorphosis is thought to mimic, by using TH, the evolutionary process of transition from the aquatic to the terrestrial life and may be compared with that of mammalian birth (Tata, 1993;Atkinson, 1994;Shi, 1999;Yoshizato, 2007). In fact, like that during amphibian metamorphosis, the level of TH in the human fetal plasma becomes transiently high around birth (Tata, 1993).…”

Section: Perspectivesmentioning

confidence: 99%

Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis

Ishizuya‐Oka

Shi

2007

Developmental Dynamics

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During amphibian metamorphosis, most or all of the larval intestinal epithelial cells undergo apoptosis. In contrast, stem cells of yet-unknown origin actively proliferate and, under the influence of the connective tissue, differentiate into the adult epithelium analogous to the mammalian counterpart. Thus, amphibian intestinal remodeling is useful for studying the stem cell niche, the clarification of which is urgently needed for regenerative therapies. This review highlights the molecular aspects of the niche using the Xenopus laevis intestine as a model. Because amphibian metamorphosis is completely controlled by thyroid hormone (TH), the analysis of TH response genes serves as a powerful means for clarifying its molecular mechanisms. Although functional analysis of the genes is still on the way, recent progresses in organ culture and transgenic studies have gradually uncovered important roles of cell-cell and cell-extracellular matrix interactions through stromelysin-3 and sonic hedgehog/bone morphogenetic protein-4 signaling pathway in the epithelial stem cell development. Developmental Dynamics 236:3358 -3368, 2007.

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“…1 affects diverse organ functions and metabolism in vertebrates (1-3) and plays critical roles in postembryonic organogenesis and tissue remodeling in vertebrates (1)(2)(3)(4)(5)(6). The effects of T 3 are mediated by T 3 receptors (TRs), which are transcription factors belonging to the nuclear receptor superfamily (3,(7)(8)(9)(10)(11).…”

Section: Thyroid Hormone (T 3 )mentioning

confidence: 99%

“…Amphibian metamorphosis bears strong similarities to postembryonic development in mammals (2,4,5) and offers a unique opportunity to study the role of cofactors in nuclear receptor function in vertebrate development. A major advantage of this model is that all tissues/organs require T 3 despite undergoing vastly different transformations during metamorphosis (2,43).…”

Section: Thyroid Hormone (T 3 )mentioning

confidence: 99%

Tissue- and Gene-specific Recruitment of Steroid Receptor Coactivator-3 by Thyroid Hormone Receptor during Development

Paul

Buchholz

et al. 2005

Journal of Biological Chemistry

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Numerous coactivators that bind nuclear hormone receptors have been isolated and characterized in vitro.Relatively few studies have addressed the developmental roles of these cofactors in vivo. By using the total dependence of amphibian metamorphosis on thyroid hormone (T 3 ) as a model, we have investigated the role of steroid receptor coactivator 3 (SRC3) in gene activation by thyroid hormone receptor (TR) in vivo. First, expression analysis showed that SRC3 was expressed in all tadpole organs analyzed. In addition, during natural as well as T 3 -induced metamorphosis, SRC3 was up-regulated in both the tail and intestine, two organs that undergo extensive transformations during metamorphosis and the focus of the current study. We then performed chromatin immunoprecipitation assays to investigate whether SRC3 is recruited to endogenous T 3 target genes in vivo in developing tadpoles. Surprisingly, we found that SRC3 was recruited in a gene-and tissue-dependent manner to target genes by TR, both upon T 3 treatment of premetamorphic tadpoles and during natural metamorphosis. In particular, in the tail, SRC3 was not recruited in a T 3 -dependent manner to the target TR␤A promoter, suggesting either no recruitment or constitutive association. Finally, by using transgenic tadpoles expressing a dominant negative SRC3 (FdnSRC3), we demonstrated that F-dnSRC3 was recruited in a T 3 -dependent manner in both the intestine and tail, blocking the recruitment of endogenous coactivators and histone acetylation. These results suggest that SRC3 is utilized in a gene-and tissue-specific manner by TR during development. Thyroid hormone (T 3 )1 affects diverse organ functions and metabolism in vertebrates (1-3) and plays critical roles in postembryonic organogenesis and tissue remodeling in vertebrates (1-6). The effects of T 3 are mediated by T 3 receptors (TRs), which are transcription factors belonging to the nuclear receptor superfamily (3, 7-11). TR forms a heterodimer with 9-cis-retinoic acid receptor (RXR) and binds to thyroid hormone response elements (TREs) of T 3 -responsive promoters to modulate transcription. TR/RXR heterodimers function to repress or activate target gene transcription in the absence or presence of T 3 , respectively, by recruiting corepressors or coactivators (3,(12)(13)(14)(15)(16)(17).The best characterized coactivators for TR belong to the SRC or p160 family, comprising three homologous members, SRC1/ NCoA-1, SRC2/TIF2/GRIP1, and SRC3/pCIP/ACTR/AIB-1/ RAC-3/TRAM-1 (18 -26). These proteins share considerable structural homology and are evolutionarily related, being about 40% identical among each other, with extensive similarity at the N-terminal basic helix-loop-helix and PAS dimerization domain (27-29). The central region of SRC proteins contain three leucine rich, LXXLL (L, leucine; X, any amino acid) motifs, forming short amphipathic ␣-helices (19, 26, 30 -32) and constitute the receptor interaction domain. SRC proteins interact with nuclear receptors directly in a ligand-dependent manner and...

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Metamorphosis: Model systems for studying gene expression in postembryonic development

Cited by 46 publications

References 84 publications

Transgenic Analysis Reveals that Thyroid Hormone Receptor Is Sufficient To Mediate the Thyroid Hormone Signal in Frog Metamorphosis

Transgenic Analysis Reveals that Thyroid Hormone Receptor Is Sufficient To Mediate the Thyroid Hormone Signal in Frog Metamorphosis

Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis

Tissue- and Gene-specific Recruitment of Steroid Receptor Coactivator-3 by Thyroid Hormone Receptor during Development

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