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Teleost Metamorphosis: The Role of Thyroid Hormone


Teleost Metamorphosis: The Role of Thyroid Hormone

Marco António Campinho. Front Endocrinol (Lausanne).


In most teleosts, metamorphosis encompasses a dramatic post-natal developmental process where the free-swimming larvae undergo a series of morphological, cellular and physiological changes that enable the larvae to become a fully formed, albeit sexually immature, juvenile fish. In all teleosts studied to date thyroid hormones (TH) drive metamorphosis, being the necessary and sufficient factors behind this developmental transition. During metamorphosis, negative regulation of thyrotropin by thyroxine (T4) is relaxed allowing higher whole-body levels of T4 that enable specific responses at the tissue/cellular level. Higher local thyroid cellular signaling leads to cell-specific responses that bring about localized developmental events. TH orchestrate in a spatial-temporal manner all local developmental changes so that in the end a fully functional organism arises. In bilateral teleost species, the most evident metamorphic morphological change underlies a transition to a more streamlined body. In the pleuronectiform lineage (flatfishes), these metamorphic morphological changes are more dramatic. The most evident is the migration of one eye to the opposite side of the head and the symmetric pelagic larva development into an asymmetric benthic juvenile. This transition encompasses a dramatic loss of the embryonic derived dorsal-ventral and left-right axis. The embryonic dorsal-ventral axis becomes the left-right axis, whereas the embryonic left-right axis becomes, irrespectively, the dorsal-ventral axis of the juvenile animal. This event is an unparalleled morphological change in vertebrate development and a remarkable display of the capacity of TH-signaling in shaping adaptation and evolution in teleosts. Notwithstanding all this knowledge, there are still fundamental questions in teleost metamorphosis left unanswered: how the central regulation of metamorphosis is achieved and the neuroendocrine network involved is unclear; the detailed cellular and molecular events that give rise to the developmental processes occurring during teleost metamorphosis are still mostly unknown. Also in flatfish, comparatively little is still known about the developmental processes behind asymmetric development. This review summarizes the current knowledge on teleost metamorphosis and explores the gaps that still need to be challenged.

Keywords: asymmetry; metamorphosis; morphogenesis; teleost; thyroid hormones.


Figure 1
Figure 1
Archetypal profile of T4 and T3 and expression of tshb, tg, dio2, dio3, thra, and thrb genes during teleost metamorphosis. The general observation in teleost species so far indicates that a surge of TH is accompanied by a rise in tshb and tg expression and the increased expression of TH signaling genes dio2 and thyroid hormone receptors together with a decrease of dio3. As soon as metamorphosis terminates TH levels decrease concomitantly with decreased levels of expression of tshb and tg and dio2 and thyroid hormone receptors, whereas dio3 levels increase to pre-metamorphic levels. Figure adapted from (15) with permission from Elsevier.
Figure 2
Figure 2
Diagram depicting HPT-axis regulation in anurans and teleosts. In anurans, hypothalamic derived CRH and/or TRH are involved in regulating pituitary TSHb expression and secretion that in turn regulates T4 production in the thyroid gland and consequently serum levels. Inversely, serum T4 then negatively regulates CRH/TRH and TSHb expression and secretion. In teleosts, HPT-axis regulation is more diverse and likely reflects species specificity. In salmonids, CRH seems to regulate pituitary TSHb expression and secretion, whereas in carp leptin and β-endorphin seem to assume that role. Notably, in carp, Galanin, and NPY seem to repress TSHb expression and secretion. Remarkably, in sole metamorphosis, neither TRH nor CRH seems to be involved in regulating pituitary TSHb raising questions about the role of the hypothalamus in HPT-axis regulation in these teleosts. Despite this, in all teleosts studied so far, the negative feedback loop between thyroid gland T4 and pituitary TSHb is present and conserved.

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