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Measurement and regulation of thyroidal status in teleost fish

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Summary

We have reviewed the stages in teleost thyroid function and its regulation, from the initial biosynthesis of the TH to their eventual interaction with putative receptors.

TH biosynthesis depends on an adequate plasma iodide level, determined partly by dietary iodide and partly by active branchial iodide uptake from the water, Pulse-injected radioiodide can be used to evaluate thyroidal iodide uptake, aspects of TH biosynthesis and TH thyroidal secretion. However, owing to variable plasma iodide levels, care is required in interpretating these parameters. TH biosynthesis, thyroglobulin properties and intrathyroidal secretion mechanisms have received limited recent attention. Histological indices of thyroid tissue changes, while useful in many situations, do not always correlate with more direct estimates of thyroidal secretion and can be misleading.

Thyroid function is regulated by the hypothalamo-pituitary-thyroid axis, but neither the identities of the hypothalamic factors nor a reliable immunoassay for TSH have been established. Currently, activity of the hypothalamic-pituitary axis is usually determined by pituitary thyrotrope histological appearance or bioassay of pituitary TSH. Plasma free T4 feeds back at both the pituitary and hypothalamic levels and inhibits TSH release. Thyroidal T4 secretory activity is presumably adjusted to maintain a constant plasma T4level according to physiologic state.

Plasma T4 is probably the most commonly used index of thyroidal status. However, (1) T4 is probably not the active form of TH, (2) the T4 plasma level may be influenced by the binding properties of plasma proteins, and (3) the T4 concentration alone makes no provision for the rate of T4 turnover in plasma. The most practical way to measure thyroidal T4SR is to determine plasma T4DR, and assuming steady-state conditions, equate it to T4SR. The T4DR is determined from kinetic studies employing*T4, which also enable estimates of sizes of vascular and extravascular T4 pools and their rates of exchange. Excretion of T4 or its derivatives in urine or bile can be determined also. A high proportion of T4 is enzymatically monodeiodinated in liver and other tissues, generating T3 for local (intracellular) and vascular systemic compartments.

Bothin vivo andin vitro methods have been used to quantify T4 deiodinase activity, which is highly responsive to physiologic state and environmental variables. T3 production is inhibited by a moderate T3 excess indicating an autoregulatory system, whereby tissue T3 levels are maintained at a set-point appropriate for a particular physiologic state. The rate of T3 production provides an informative measure of thyroidal status in a given tissue. However, other pathways also contribute to the maintenance of T3 homeostasis at a particular set-point. These include the rate of T3 degradation to 3,3′-T2, the rate of T4 substrate diversion to rT3 (an inactive isomer) and by the excretion of parent compounds or conjugates in bile and urine. Potential losses across branchial or integumentary surfaces have yet to be evaluated.

The most fundamental measure of thyroidal status is represented by the amount of T3 saturably bound to receptors/nucleus for the cell type of interest. This is estimated most accurately in double isotope studies in which T3 contributions from both vascular and intracellular compartments are evaluated. Less satisfactory but meaningful indices of T3 availability to receptor sites may be obtained from the plasma T3 (or free T3) level and from the tissue T3 level. The former is appropriate if the cell type in question obtains its T3 primarily from plasma; the latter should be measured if the cell type derives its T3 mainly through intracellular deiodinase activity. If the proportion of vascular T3/intracellular T3 bound to receptors is known, it may indicate the degree of receptor activation. However, even cytosolic T3 levels may not vary in proportion to nuclear T3 levels.

Differences in thyroidal function between teleosts and homeotherms can be attributed to distinctive strategies in iodide economy and to fundamental differences in control of thyroidal status. Owing to more certain iodide availability (branchial iodide pump and plasma iodide-binding proteins), teleosts are probably more liberal in their iodide use and have less efficient mechanisms for recovery and retention of hormonal iodide than homeotherms. Also, primary control of teleost thyroidal function appears peripheral. It is the finely regulated conversion of T4 to T3 in tissues which may largely determine the T4 secretion rate. Thus, T4, as a prohormone, may be produced more to satisfy the substrate needs for T4 conversion rather than to drive T3 production. Because TH are mainly implicated in tissue- or cell-specific processes involved in development, growth and reproduction in teleosts, it may be advantageous for their thyroidal status to be determined locally through T4-to-T3 deiodination. In homeotherms, primary control is mainly central through the hypothalamic-pituitary axis, which regulates thyroidal secretion of T4 and significant amounts of T3. The level of T4 (free T4) is believed to drive the production of T3 in most peripheral tissues. Because TH are extensively involved in the systemically integrated adjustment of basal metabolic rate in homeotherms, it may have been advantageous to evolve a system leaning towards central control by the hypothalamus, the brain centre associated with thermoregulation.

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  1. Department of Zoology, University of Manitoba, R3T 2N2, Winnipeg, MB, Canada

    J. G. Eales

  2. Department of Fisheries and Oceans, Freshwater Institute, 501 University Crescent, R3T 2N6, Winnipeg, MB, Canada

    S. B. Brown

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Eales, J.G., Brown, S.B. Measurement and regulation of thyroidal status in teleost fish. Rev Fish Biol Fisheries 3, 299–347 (1993). https://doi.org/10.1007/BF00043383

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