Iodine Metabolism and Thyroid-Related Functions in Organisms Lacking Thyroid Follicles: Are Thyroid Hormones also Vitamins?

Abstract

Thyroid-related functions in organisms devoid of follicular thyroid tissue have been reviewed. In the lamprey, a primitive vertebrate, the larva concentrates iodide and synthesizes thyroid hormones (TH) by iodoperoxidase (IP)-mediated iodination of a thyroglobulin (TG)-like molecule in a subpharyngeal afollicular endostyle. The endostyle is the thyroid homolog, and it reorganizes into a follicular thyroid at metamorphosis to the adult. Ascidians and amphloxus, invertebrate protochordate relatives of vertebrates, also concentrate iodide and synthesize TH in a subpharyngeal afollicular endostyle, but the endostyle never transforms to follicles. Ascidian plasma contains L-thyroxine and its more biologically active derivative 3,5,3'-triiodo-L-thyronine, and TH receptors exist, but TH effects are poorly understood. No other invertebrates possess an endostyle. Several invertebrates concentrate iodide at other sites and form protein-incorporated iodohistidines and iodotyrosines; however, de novo iodothyronine biosynthesis through IP-mediated TG iodination has not been established. Nevertheless, TH occur in invertebrates, and exogenous iodothyrosines or iodothyronines have effects on jellyfish, insects, and sea urchins. Furthermore, gut bacteria metabolize TH, and plants may synthesize TH by nonenzymatic oxidative iodination. Thus, TH occur in many organisms and, after ingestion and enteric absorption, can enter the food chain. Indeed, sea urchin larvae obtain TH required to induce metamorphosis from plant diatoms. Thyroid hormones can therefore have vitamin-like effects and, in conjunction with vitamin D, and possibly with other steroids, may be more aptly termed vitamones. Availability of exogenous TH has implications for models of invertebrate and vertebrate TH metabolism and iodine salvaging, and it may explain the prominent and probable ancestral role of peripheral mechanisms in regulating thyroidal status.

The history of a developmental stage: Metamorphosis in chordates

“…One study reported that THs accelerated metamorphosis in the mollusk abalone (Fukazawa et al, 2001) and another one in a crustacean [a prawn (Roustaian and Gaik, 2006)]. In contrast, THs did not seem to have any effect on the crustacean Daphnia (Kashian and Dodson, 2004) in accordance with the observation that no endogenous TH is present in this species (Eales, 1997). Consequently, hypotheses on the roles of THs or other derivatives and TR in protostomes can only be tentative: a potential responsiveness to THs would imply a very ancient function of TR as the TH receptor or, on the other hand, the establishment of an alternative function would imply an evolutionary shift.…”

Iodothyronine deiodinases: a functional and evolutionary perspective

“…of the complementary enzymatic dyad of halogenation/ dehalogenation (for review Eales (1997) and Valverde-R et al (2004)). Indeed, current information supports the notion that the vertebrate thyroid gland, as well as the endostyle and subpharyngeal gland in invertebrate chordates, may have evolved from a common ancestor (for review Kluge et al (2005) and Paris et al (2008)).…”

“…In vertebrates, iodine is critical for the synthesis of iodothyronines or thyroid hormones (THs), which, according to the ontogenetic stage of the organism, regulate early and postembryonic developmental processes and metabolic balance (Eales 1997, Valverde-R et al 2004, Yun et al 2005, Tata 2006). The major TH in circulation is thyroxine (T 4 ) whose synthesis is restricted to the thyroid gland.…”

Ciona intestinalis: Chordate development made simple

“…The outer regions of the U-shaped ascidian endostyle traditionally have been considered to share a common evolutionary origin with the vertebrate thyroid gland, based on the finding that both organs sequester iodine and display thyroid peroxidase activity (reviewed by Eales, 1997).…”

“…The feeding basket of the adult contains gill slits that appear to share a common origin with the gill slits of other chordates (Aros and Viragh, 1969). Likewise, the endostyle of the adult ascidian is a homolog of the vertebrate thyroid gland, sequestering iodine and producing thyroid hormone (Eales, 1997).…”