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Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics.

ABSTRACT: Protrusile jaws are a highly useful innovation that has been linked to extensive diversification in fish feeding ecology. Jaw protrusion can enhance the performance of multiple functions, such as suction production and capturing elusive prey. Identifying the developmental factors that alter protrusion ability will improve our understanding of fish diversification. In the zebrafish protrusion arises postmetamorphosis. Fish metamorphosis typically includes significant changes in trophic morphology, accompanies a shift in feeding niche and coincides with increased thyroid hormone production. We tested whether thyroid hormone affects the development of zebrafish feeding mechanics. We found that it affected all developmental stages examined, but that effects were most pronounced after metamorphosis. Thyroid hormone levels affected the development of jaw morphology, feeding mechanics, shape variation, and cranial ossification. Adult zebrafish utilize protrusile jaws, but an absence of thyroid hormone impaired development of the premaxillary bone, which is critical to jaw protrusion. Premaxillae from early juvenile zebrafish and hypothyroid adult zebrafish resemble those from adults in the genera Danionella, Devario, and Microdevario that show little to no jaw protrusion. Our findings suggest that evolutionary changes in how the developing skulls of danionin minnows respond to thyroid hormone may have promoted diversification into different feeding niches.

SUBMITTER: Galindo D

PROVIDER: S-EPMC6815664 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics.

Galindo Demi D Sweet Elly E DeLeon Zoey Z Wagner Mitchel M DeLeon Adrian A Carter Casey C McMenamin Sarah K SK Cooper W James WJ

Evolution & development 20190802 5

Protrusile jaws are a highly useful innovation that has been linked to extensive diversification in fish feeding ecology. Jaw protrusion can enhance the performance of multiple functions, such as suction production and capturing elusive prey. Identifying the developmental factors that alter protrusion ability will improve our understanding of fish diversification. In the zebrafish protrusion arises postmetamorphosis. Fish metamorphosis typically includes significant changes in trophic morphology ...[more]

PMID: 31374588

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Project description:Background: Mutations of thyroid hormone receptor α1 (TRα1) cause resistance to thyroid hormone (RTHα). Patients exhibit growth retardation, delayed bone development, anemia, and bradycardia. By using mouse models of RTHα, much has been learned about the molecular actions of TRα1 mutants that underlie these abnormalities in adults. Using zebrafish models of RTHα that we have recently created, we aimed to understand how TRα1 mutants affect the heart function during this period. Methods: In contrast to human and mice, the thra gene is duplicated, thraa and thrab, in zebrafish. Using CRISPR/Cas9-mediated targeted mutagenesis, we created C-terminal mutations in each of two duplicated thra genes in zebrafish (thraa 8-bp insertion or thrab 1-bp insertion mutations). We recently showed that these mutant fish faithfully recapitulated growth retardation as found in patients and thra mutant mice. In the present study, we used histological analysis, gene expression profiles, confocal fluorescence, and transmission electron microscopy (TEM) to comprehensively analyze the phenotypic characteristics of mutant fish heart during development. Results: We found both a dilated atrium and an abnormally shaped ventricle in adult mutant fish. The retention of red blood cells in the two abnormal heart chambers, and the decreased circulating blood speed and reduced expression of contractile genes indicated weakened contractility in the heart of mutant fish. These abnormalities were detected in mutant fish as early as 35 days postfertilization (juveniles). Furthermore, the expression of genes associated with the sarcomere assembly was suppressed in the heart of mutant fish, resulting in abnormalities of sarcomere organization as revealed by TEM, suggesting that the abnormal sarcomere organization could underlie the bradycardia exhibited in mutant fish. Conclusions: Using a zebrafish model of RTHα, the present study demonstrated for the first time that TRα1 mutants could act to cause abnormal heart structure, weaken contractility, and disrupt sarcomere organization that affect heart functions. These findings provide new insights into the bradycardia found in RTHα patients.

Project description:Caecilians (Lissamphibia: Gymnophiona) are unique among vertebrates in having two sets of jaw-closing muscles, one on either side of the jaw joint. Using data from high-resolution X-ray radiation computed tomography scans, we modelled the effect of these two muscle groups (mm. levatores mandibulae and m. interhyoideus posterior) on bite force over a range of gape angles, employing a simplified lever arm mechanism that takes into account muscle cross-sectional area and fibre angle. Measurements of lever arm lengths, muscle fibre orientations and physiological cross-sectional area of cranial muscles were available from three caecilian species: Ichthyophis cf. kohtaoensis; Siphonops annulatus; and Typhlonectes natans. The maximal gape of caecilians is restricted by a critical gape angle above which the mm. levatores mandibulae will open the jaw and destabilize the mandibular joint. The presence of destabilizing forces in the caecilian jaw mechanism may be compensated for by a mandibular joint in that the fossa is wrapped around the condyle to resist dislocation. The caecilian skull is streptostylic; the quadrate-squamosal complex moves with respect to the rest of the skull. This increases the leverage of the jaw-closing muscles. We also demonstrate that the unusual jaw joint requires streptostyly because there is a dorsolateral movement of the quadrate-squamosal complex when the jaw closes. The combination of the two jaw-closing systems results in high bite forces over a wide range of gape angles, an important advantage for generalist feeders such as caecilians. The relative sizes and leverage mechanics of the two closing systems allow one to exert more force when the other has a poor mechanical advantage. This effect is seen in all three species we examined. In the aquatic T. natans, with its less well-roofed skull, there is a larger contribution of the mm. levatores mandibulae to total bite force than in the terrestrial I. cf. kohtaoensis and S. annulatus.

Project description:High throughput in vitro, in silico, and computational approaches have identified numerous environmental chemicals that interfere with thyroid hormone (TH) activity, and it is posited that human exposures to such chemicals are a contributing factor to neurodevelopmental disorders. However, whether hits in screens of TH activity are predictive of developmental neurotoxicity (DNT) has yet to be systematically addressed. The zebrafish has been proposed as a second tier model for assessing the in vivo DNT potential of TH active chemicals. As an initial evaluation of the feasibility of this proposal, we determined whether an endpoint often used to assess DNT in larval zebrafish, specifically photomotor behavior, is altered by experimentally induced hyper- and hypothyroidism. Developmental hyperthyroidism was simulated by static waterborne exposure of zebrafish to varying concentrations (3-300 nM) of thyroxine (T4) or triiodothyronine (T3) beginning at 6 h post-fertilization (hpf) and continuing through 5 days post-fertilization (dpf). Teratogenic effects and lethality were observed at 4 and 5 dpf in fish exposed to T4 or T3 at concentrations >30 nM. However, as early as 3 dpf, T4 (> 3 nM) and T3 (> 10 nM) significantly increased swimming activity triggered by sudden changes from light to dark, particularly during the second dark period (Dark 2). Conversely, developmental hypothyroidism, which was induced by treatment with 6-propyl-2-thiouracil (PTU), morpholino knockdown of the TH transporter mct8, or ablation of thyroid follicles in adult females prior to spawning, generally decreased swimming activity during dark periods, although effects did vary across test days. All effects of developmental hypothyroidism on photomotor behavior occurred independent of teratogenic effects and were most robust during Dark 2. Treatment with the T4 analog, Tetrac, restored photomotor response in mct8 morphants to control levels. Collectively, these findings suggest that while the sensitivity of photomotor behavior in larval zebrafish to detect TH disruption is influenced by test parameters, this test can distinguish between TH promoting and TH blocking activity and may be useful for assessing the DNT potential of TH-active chemicals.

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Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics.

Publications

Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics.

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