Gene transcription ontogeny of hypothalamic-pituitary-thyroid axis development in early-life stage fathead minnow and zebrafish

Vergauwen, Lucia; Cavallin, Jenna E.; Ankley, Gerald T.; Bars, Chloé; Gabriëls, Isabelle J.; Michiels, Ellen D. G.; Fitzpatrick, Krysta R.; Periz-Stanaćev, Jelena; Randolph, Eric C.; Robinson, Serina L.; Saari, Travis; Schroeder, Anthony; Stinckens, Evelyn; Swintek, Joe; Cruchten, Steven Van; Verbueken, Evy; Villeneuve, Daniel L.; Knapen, Dries

doi:10.1016/j.ygcen.2018.05.001

Cited by 52 publications

(44 citation statements)

References 59 publications

(80 reference statements)

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“…A previous analysis identified a similar shift in T3/T4 ratio at 10-14 dpf, attributed to higher deiodinase activity (Chang, Wang et al 2012). Indeed, while expression of thyroglobulin remains relatively stable from 10-20 dpf, deiodinase 2 expression increases twofold (Vergauwen, Cavallin et al 2018). However, these patterns are difficult to perfectly correlate with our measurements, as dpf (used in these previous analyses) is a poor proxy for size and developmental stage (Parichy, Elizondo et al 2009, McMenamin, Chandless et al 2016.…”

Section: Bioavailability Of Th Shifts During Mid-larval Developmentsupporting

confidence: 53%

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in Danionins

Mauri

Donahue

et al. 2019

Preprint

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BackgroundChanges in post-embryonic developmental trajectories can profoundly alter adult phenotypes and life history transitions. In vertebrate clades with complex, biphasic life cycles, thyroid hormone (TH) regulates metamorphosis, and alterations to TH metabolism underlie famous cases of paedomorphosis. We tested the requirement for TH in multiple post-embryonic developmental processes in the zebrafish, and asked if TH loss was associated with paedomorphosis in miniaturized Danionellas.ResultsWe found that TH regulates the relative growth of different body parts in zebrafish, inhibiting head growth at juvenile stages. The lateral line also showed sensitivity to the hormone: head neuromasts were inhibited by TH, while trunk neuromasts required TH for their proliferation. While several aspects of Danionella morphology resembled that of larval zebrafish, these species did not resemble hypothyroid zebrafish in their shape or lateral line, and these fish showed functional thyroid follicles.ConclusionsAlthough zebrafish do not undergo a discrete ecological transformation, we found that multiple tissues go through a protracted metamorphosis, and that TH ushers in growth patterns and processes typical of juveniles. We found no evidence that compromised TH metabolism is responsible for paedomorphosis in Danionellas. Nonetheless, modulations to TH-sensitive pathways affect evolutionarily-relevant traits, and are likely important targets for adaptation.Bullet PointsThyroid hormone regulates shifts in relative growth trajectories in different zebrafish tissuesThyroid hormone inhibits head growth in juvenile zebrafish, and regulates juvenile growth patternsThyroid hormone stimulates formation of neuromast canals in the head and ‘stitches’ on the trunk of zebrafishDanionella, the miniaturized sister group to Danio morphologically resemble larval zebrafish and do not form neuromast canalsHypothyroidism is not the cause of paedomorphosis in DanionellaGrant SponsorsNIH R00GM105874NIH R03HD091634Burroughs Wellcome Collaborative Research Travel Grant 1017439

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Section: Bioavailability Of Th Shifts During Mid-larval Developmentsupporting

confidence: 53%

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in Danionins

Mauri

Donahue

et al. 2019

Preprint

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“…A previous analysis identified a similar shift in T3/T4 ratio at 10 to 14 days post fertilization (dpf), attributed to higher deiodinase activity . Indeed, while expression of thyroglobulin remains relatively stable from 10 to 20 dpf, deiodinase 2 expression increases 2‐fold . However, these patterns are difficult to perfectly correlate with our measurements, as dpf (used in these previous analyses) is an unreliable proxy for development …”

Section: Resultssupporting

confidence: 57%

“…53 Indeed, while expression of thyroglobulin remains relatively stable from 10 to 20 dpf, deiodinase 2 expression increases 2-fold. 54 However, these patterns are difficult to perfectly correlate with our measurements, as dpf (used in these previous analyses) is an unreliable proxy for development. 21,55 Shifts in allometric trajectories of WT fish occur at 8 to 10 mm SL (Figures 2A,B and 3C,D).…”

Section: Bioavailability Of Th Shifts During Midlarval Developmentmentioning

confidence: 76%

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in danionins

Mauri

Donahue

et al. 2019

Developmental Dynamics

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Background Differences in postembryonic developmental trajectories can profoundly alter adult phenotypes and life histories. Thyroid hormone (TH) regulates metamorphosis in many vertebrate taxa with multiphasic ecologies, and alterations to TH metabolism underlie notable cases of paedomorphosis in amphibians. We tested the requirement for TH in multiple postembryonic developmental processes in zebrafish, which has a monophasic ecology, and asked if TH production was compromised in paedomorphic Danionella. Results We showed that TH regulates allometric growth in juvenile zebrafish, and inhibits relative head growth. The lateral line system showed differential requirements for TH: the hormone promotes canal neuromast formation and inhibits neuromast proliferation in the head, but causes expansion of the neuromast population in the trunk. While Danionella morphology resembled that of larval zebrafish, the two Danionella species analyzed were not similar to hypothyroid zebrafish in their shape or neuromast distribution, and both possessed functional thyroid follicles. Conclusions Although zebrafish do not undergo a discrete ecological transformation, we found that multiple tissues undergo transitions in developmental trajectories that are dependent on TH, suggesting the TH axis and its downstream pathways as likely targets for adaptation. Nonetheless, we found no evidence that evolutionary paedomorphosis in Danionella is the result of compromised TH production.

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“…In a previous study we showed a peak of dio1 as well as dio2 mRNA in 5 day old normally developing zebrafish (Vergauwen et al, 2018), which does not suggest dominance of either isoform at that time point. However, it has been previously suggested that Dio2 is the major contributor to TH activation in developing zebrafish embryos (Darras et al, 2015;Walpita et al, 2010).…”

Section: Linking In Chemico Data To In Vivo Datamentioning

confidence: 58%

An AOP-based alternative testing strategy to predict the impact of thyroid hormone disruption on swim bladder inflation in zebrafish

Stinckens

Vergauwen²,

Ankley

et al. 2018

Aquatic Toxicology

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The adverse outcome pathway (AOP) framework can be used to help support the development of alternative testing strategies aimed at predicting adverse outcomes caused by triggering specific toxicity pathways. In this paper, we present a case-study demonstrating the selection of alternative in chemico assays targeting the molecular initiating events of established AOPs, and evaluate use of the resulting data to predict higher level biological endpoints. Based on two AOPs linking inhibition of the deiodinase (DIO) enzymes to impaired posterior swim bladder inflation in fish, we used in chemico enzyme inhibition assays to measure the molecular initiating events for an array of 51 chemicals. Zebrafish embryos were then exposed to 14 compounds with different measured inhibition potentials. Effects on posterior swim bladder inflation, predicted based on the information captured by the AOPs, were evaluated. By linking the two datasets and setting thresholds, we were able to demonstrate that the in chemico dataset can be used to predict biological effects on posterior chamber inflation, with only two outliers out of the 14 tested compounds. Our results show how information organized using the AOP framework can be employed to develop or select alternative assays, and successfully forecast downstream key events along the AOP. In general, such in chemico assays could serve as a first-tier high-throughput system to screen and prioritize chemicals for subsequent acute and chronic fish testing, potentially reducing the need for long-term and costly toxicity tests requiring large numbers of animals.

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Gene transcription ontogeny of hypothalamic-pituitary-thyroid axis development in early-life stage fathead minnow and zebrafish

Cited by 52 publications

References 59 publications

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in Danionins

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in Danionins

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in danionins

An AOP-based alternative testing strategy to predict the impact of thyroid hormone disruption on swim bladder inflation in zebrafish

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