Thyroid Hormones and Postembryonic Development in Amniotes

Holzer, Guillaume; Laudet, Vincent

doi:10.1016/b978-0-12-385979-2.00014-9

Cited by 37 publications

(31 citation statements)

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“…45−47 Therefore, it is necessary to investigate further the effects of TBBPA at lower and more environmentally relevant concentrations. Given that TH signaling is conserved across all vertebrate species, in particular, there are many similarities between amphibian metamorphosis and development in higher vertebrates, 19,20 our findings from X. laevis highlight potential adverse influences of TBBPA on THdependent development in higher vertebrates, including humans. 48 Pages S3−S4: details of these methods: RNA extraction and quantitative RT-PCR, histological examination, TUNEL assay, and data analysis.…”

Section: ■ Discussionmentioning

confidence: 86%

Tetrabromobisphenol A Disrupts Vertebrate Development via Thyroid Hormone Signaling Pathway in a Developmental Stage-Dependent Manner

Zhang¹,

Lou³

et al. 2014

Environ. Sci. Technol.

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Data concerning effects of tetrabromobisphenol A (TBBPA) on thyroid hormone (TH)-dependent vertebrate development have been limited, although TBBPA has been demonstrated in vitro to disrupt the TH signaling pathway at the transcriptional level. In this study, we investigated the effects of TBBPA on T3-induced and spontaneous Xenopus laevis metamorphosis, which share many similarities with TH-dependent development in higher vertebrates. In a 6-day T3-induced metamorphosis assay using premetamorphic tadpoles, 10-1000 nM TBBPA exhibited inhibitory effects on T3-induced expression of TH-response genes and morphological changes in a concentration-dependent manner, with a weak stimulatory action on tadpole development and TH-response gene expression in the absence of T3 induction. In a spontaneous metamorphosis assay, we further found that TBBPA promoted tadpole development from stage 51 to 56 (pre- and prometamorphic stages) but inhibited metamorphic development from stage 57 to 66 (metamorphic climax). These results strongly show that TBBPA, even at low concentrations, disrupts TH-dependent development in a developmental stage-dependent manner, i.e., TBBPA exhibits an antagonistic activity at the developmental stages when animals have high endogenous TH levels, whereas it acts as an agonist at the developmental stages when animals have low endogenous TH levels. Our study highlights the adverse influences of TBBPA on TH-dependent development in vertebrates.

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Section: ■ Discussionmentioning

confidence: 86%

Tetrabromobisphenol A Disrupts Vertebrate Development via Thyroid Hormone Signaling Pathway in a Developmental Stage-Dependent Manner

Zhang¹,

Lou³

et al. 2014

Environ. Sci. Technol.

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“…The mammalian perinatal period is suggested to correspond to anuran metamorphosis, which is supported by the following observations: (a) transition from amniotic or aquatic to terrestrial life, (b) surge of THs in blood, (c) limb elongation (bone development), (d) skin keratinization, (e) hemoglobin switch from fetal or larval to adult type, (f) production of albumin and urea cycle enzymes in the liver and (g) developmental progression and restructuring of the nervous system (Tata, ). Although this concept is supported in several reviews (Holzer & Laudet, ; Nakajima, Fujimoto, & Yaoita, ), this similarity has not been experimentally verified.…”

Section: Introductionmentioning

confidence: 95%

Developmental gene expression patterns in the brain and liver of Xenopus tropicalis during metamorphosis climax

Yaoita

Nakajima

2018

Genes to Cells

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Thyroid hormones (THs) induce metamorphosis in amphibians, causing dynamic changes, whereas mammalian newborns undergo environmental transition from placenta to open air at birth. The similarity between amphibian metamorphosis and the mammalian perinatal periods has been repeatedly discussed. However, a corresponding developmental gene expression analysis has not yet been reported. In this study, we examined the developmental gene expression profiles in the brain and liver of Xenopus tropicalis during metamorphosis climax and compared them to the respective gene expression profiles of newborn rodents. Many upregulated genes identified in the tadpole brain during metamorphosis are also upregulated in the rodent brain during the first three postnatal weeks when the TH surge occurs. The upregulation of some genes in the brain was inhibited in thyroid hormone receptor α (TRα) knockout tadpoles but not in TRβ–knockout tadpoles, implying that brain metamorphosis is mainly mediated by TRα. The expression of some genes was also increased in the liver during metamorphosis climax. Our data suggest that the rodent brain undergoes TH‐dependent remodeling during the first three postnatal weeks as observed in X. tropicalis during the larva‐to‐adult metamorphosis.

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“…In contrast to most invertebrates, all chordates and some derived echinoderms and molluscs have evolved the capacity for internal thyroid hormone synthesis using exogenous sources of iodine (Heyland and Moroz, 2005;Heyland et al, 2006;Holzer and Laudet, 2013). This process occurs in the endostyle of nonvertebrate chordates, which is homologous to the thyroid gland in vertebrates (Eales, 1997).…”

Section: Commentarymentioning

confidence: 99%

“…However, the precarious supply of thyroid hormone from dietary sources would preclude it from assuming the essential functions it has in vertebrates. For example, the regulation of mammalian thermogenesis by thyroid hormone could not continually maintain body temperature if its availability were tied to the availability of particular food sources.In contrast to most invertebrates, all chordates and some derived echinoderms and molluscs have evolved the capacity for internal thyroid hormone synthesis using exogenous sources of iodine (Heyland and Moroz, 2005;Heyland et al, 2006;Holzer and Laudet, 2013). This process occurs in the endostyle of nonvertebrate chordates, which is homologous to the thyroid gland in vertebrates (Eales, 1997).…”

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confidence: 99%

The evolution of endothermy is explained by thyroid hormone-mediated responses to cold in early vertebrates

Little

Seebacher

2014

Journal of Experimental Biology

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The evolution of endothermy is one of the most intriguing and consistently debated topics in vertebrate biology, but the proximate mechanisms that mediated its evolution are unknown. Here, we suggest that the function of thyroid hormone in regulating physiological processes in response to cold is key to understanding the evolution of endothermy. We argue that the capacity of early chordates to produce thyroid hormone internally was the first step in this evolutionary process. Selection could then act on the capacity of thyroid hormone to regulate metabolism, muscle force production and cardiac performance to maintain their function against the negative thermodynamic effects of decreasing temperature. Thyroid-mediated cold acclimation would have been the principal selective advantage. The actions of thyroid hormone during cold acclimation in zebrafish are very similar to its role during endothermic thermogenesis. The thyroid-mediated increases in metabolism and locomotor performance in ectotherms eventually resulted in sufficient heat production to affect body temperature. From this point onwards, increased body temperature per se could be of selective advantage and reinforce thyroid-induced increases in physiological rates. Selection for increased body temperature would promote those mechanisms that maximise heat production, such as increased Na + /K + -ATPase activity, futile cycling by SERCA, and mitochondrial uncoupling, all of which are regulated by thyroid hormone. The specific end point of this broader evolutionary process would be endothermic thermoregulation. However, considering the evolution of endothermy in isolation is misleading because the selective advantages that drove the evolutionary process were independent from endothermy. In other words, without the selective advantages of thyroid-mediated cold acclimation in fish, there would be no endotherms. KEY WORDS: Thermoregulation, Locomotion, Metabolism, Heat production, Aerobic capacity IntroductionThe advantages that have led to the evolution of an endothermic physiology are still under debate. A widely accepted model is that directional selection for incremental increases in aerobic capacity and sustained activity led to the evolution of endothermy (the 'aerobic capacity' model) (Bennett and Ruben, 1979;Nespolo et al., 2011). The greater scope for physical activity means that endotherms tire less quickly and are therefore better able to forage, escape predators and migrate (Clarke and Pörtner, 2010). Increased physical activity requires a greater capacity for energy (ATP) production, and oxidative metabolic capacities of endotherms are consequently an order of magnitude greater than those of ectotherms COMMENTARY School of Biological Sciences A08, University of Sydney, NSW 2006, Australia.*Author for correspondence (frank.seebacher@sydney.edu.au) (Bennett and Ruben, 1979). In contrast, the 'parental care' model suggests that increased non-shivering thermogenesis permitted parents to control incubation temperatures and thereby provided the...

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Thyroid Hormones and Postembryonic Development in Amniotes

Cited by 37 publications

References 85 publications

Tetrabromobisphenol A Disrupts Vertebrate Development via Thyroid Hormone Signaling Pathway in a Developmental Stage-Dependent Manner

Tetrabromobisphenol A Disrupts Vertebrate Development via Thyroid Hormone Signaling Pathway in a Developmental Stage-Dependent Manner

Developmental gene expression patterns in the brain and liver of Xenopus tropicalis during metamorphosis climax

The evolution of endothermy is explained by thyroid hormone-mediated responses to cold in early vertebrates

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