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• W2023422445 abstract "A new study shows that iodothyronines induce metamorphosis in the cephalochordate amphioxus by binding to a receptor homologous to vertebrate thyroid hormone receptors. Iodothyronine-induced metamorphosis may be an ancestral feature of the chordates. A new study shows that iodothyronines induce metamorphosis in the cephalochordate amphioxus by binding to a receptor homologous to vertebrate thyroid hormone receptors. Iodothyronine-induced metamorphosis may be an ancestral feature of the chordates. A complex life cycle, where an animal begins life as a larva then undergoes a metamorphosis to the juvenile adult form, is a widespread and ancient life history strategy [1Hall B.K. Wake M.H. Introduction: Larval development, evolution and ecology.in: Hall B.K. Wake M.H. The Origin and Evolution of Larval Forms. Academic Press, London, UK1999: 1-19Crossref Google Scholar]. Larvae generally exploit different ecological niches from adults, thus avoiding competition for resources. There is considerable morphological diversity among larvae and the transformations that they undergo during metamorphosis [1Hall B.K. Wake M.H. Introduction: Larval development, evolution and ecology.in: Hall B.K. Wake M.H. The Origin and Evolution of Larval Forms. Academic Press, London, UK1999: 1-19Crossref Google Scholar], which raises the question whether the complex life cycles of extant species reflect an ancestral or a derived state. Among chordates with complex life cycles, the best studied are the anuran amphibians (frogs and toads). Anuran larvae (tadpoles) are aquatic, and undergo morphological, biochemical and physiological transformation into the terrestrial juvenile adult. Gudernatch [2Gudernatsch J.F. Feeding experiments on tadpoles. I. The influence of specific organs given as food on growth and differentiation. A contribution to the knowledge of organs with internal secretion.Wilhelm Roux Arch. Entwicklungsmech. Org. 1912; 35: 457-483Crossref Scopus (190) Google Scholar] first showed that vertebrate thyroid glands contain an active component that induces precocious metamorphosis when fed to tadpoles. Thyroid hormone is now known to orchestrate the diverse morphological and physiological changes that occur during amphibian metamorphosis [3Brown D.D. Cai L.Q. Amphibian metamorphosis.Dev. Biol. 2007; 306: 20-33Crossref PubMed Scopus (265) Google Scholar]. Thyroid hormone has also been shown to control flatfish metamorphosis [4Dejesus E. Hirano T. Inui Y. Flounder metamorphosis - its regulation by various hormones.Fish Physiol. Biochem. 1993; 11: 323-328Crossref PubMed Scopus (43) Google Scholar], and exogenous thyroid hormone can induce metamorphosis in echinoderm larvae [5Chino Y. Saito M. Yamasu K. Suyemitsu T. Ishihara K. Formation of the adult rudiment of sea urchins is influenced by thyroid hormones.Dev. Biol. 1994; 161: 1-11Crossref PubMed Scopus (57) Google Scholar, 6Johnson L.G. Cartwright C.M. Thyroxine-accelerated larval development in the crown-of-thorns starfish, Acanthaster planci.Biological Bulletin. 1996; 190: 299-301Crossref Scopus (30) Google Scholar, 7Heyland A. Reitzel A.M. Hodin J. Thyroid hormones determine developmental mode in sand dollars (Echinodermata: Echinoidea).Evol. Dev. 2004; 6: 382-392Crossref PubMed Scopus (27) Google Scholar]. Now Paris et al. [8Paris M. Escriva H. Schubert M. Brunet F. Brtko J. Ciesielski F. Roecklin D. Vivat-Hannah V. Jamin E. Cravedi J.P. et al.Amphioxus post-embryonic development reveals the homology of chordate metamorphosis.Curr. Biol. 2008; 18: 825-830Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar] have reported in Current Biology that metamorphosis of the cephalochordate amphioxus can be induced by iodothyronines. The active component in vertebrate thyroid glands is 3,5,3′5′-tetraiodothyronine (thyroxine; T4) , a member of a class of compounds known as iodothyronines, which are derived from two tyrosine residues of a precursor protein which have iodine atoms attached to the aromatic rings [3Brown D.D. Cai L.Q. Amphibian metamorphosis.Dev. Biol. 2007; 306: 20-33Crossref PubMed Scopus (265) Google Scholar]. Thyroxine is generally considered to be a secondary precursor that must be converted to the biologically active form of the hormone, 3,5,3′-triiodothyronine (T3) [9St. Germain D.L. Galton V.A. The deiodinase family of selenoproteins.Thyroid. 1997; 7: 655-668Crossref PubMed Scopus (281) Google Scholar]. The actions of thyroid hormone are mediated by thyroid hormone receptors, which are ligand-activated transcription factors belonging to the steroid hormone receptor superfamily [10Germain P. Staels B. Dacquet C. Spedding M. Laudet V. Overview of nomenclature of nuclear receptors.Pharmacol. Rev. 2006; 58: 685-704Crossref PubMed Scopus (420) Google Scholar]. All jawed vertebrates that have been studied possess two thyroid hormone receptors, TRα and TRβ, which bind to DNA as dimers, with the preferred configuration being a heterodimer with retinoid X receptor (RXR) [11Yen P.M. Physiological and molecular basis of thyroid hormone action.Phys. Rev. 2001; 81: 1097-1142PubMed Google Scholar]. The thyroid hormone receptors have been shown to be essential for metamorphosis of the clawed toad Xenopus laevis [12Buchholz D.R. Paul B.D. Fu L.Z. Shi Y.B. Molecular and developmental analyses of thyroid hormone receptor function in Xenopus laevis, the African clawed frog.General Comparative Endocrinol. 2006; 145: 1-19Crossref PubMed Scopus (159) Google Scholar]. Thyroid hormone controls metamorphosis in vertebrate species, but the evolutionary origin of this developmental signaling in chordates is unknown. Most extant urochordates and cephalocordates have a complex life cycle [13Just J.J. Kraus-Just J. Check D.A. Survey of chordate metamorphosis.in: Frieden L.I.G.a.E. Metamorphosis. Second Edition. Plenum Press, New York, NY1981: 265-326Crossref Google Scholar]. The cephalochordate amphioxus, now considered to be among the most basal members of the phylum Chordata [14Delsuc F. Brinkmann H. Chourrout D. Philippe H. Tunicates and not cephalochordates are the closest living relatives of vertebrates.Nature. 2006; 439: 965-968Crossref PubMed Scopus (1142) Google Scholar], have larvae that are asymmetric, with the mouth on the left side, and gill slits on the right side of the body (Figure 1; reviewed in [13Just J.J. Kraus-Just J. Check D.A. Survey of chordate metamorphosis.in: Frieden L.I.G.a.E. Metamorphosis. Second Edition. Plenum Press, New York, NY1981: 265-326Crossref Google Scholar]). At metamorphosis the pelagic larva transforms into a benthic adult. The mouth moves medially from its left lateral position, and the primary gill slits move from right to left. A secondary set of gill slits develop simultaneously on the right side of the animal. Iodothyronines are produced by the endostyle of amphioxus, a structure considered the precursor of vertebrate thyroid follicles [13Just J.J. Kraus-Just J. Check D.A. Survey of chordate metamorphosis.in: Frieden L.I.G.a.E. Metamorphosis. Second Edition. Plenum Press, New York, NY1981: 265-326Crossref Google Scholar, 15Ogasawara M. Overlapping expression of amphioxus homologs of the thyroid transcription factor-1 gene and thyroid peroxidase gene in the endostyle: insight into evolution of the thyroid gland.Dev. Genes Evol. 2000; 210: 231-242Crossref PubMed Scopus (78) Google Scholar]. Over 40 years ago, it was hypothesized that amphioxus metamorphosis is controlled by iodothyronines; however, only one attempt was hitherto made to address this hypothesis, with results complicated by an incomplete experimental design [16Wickstea J.H. Branchiostoma lanceolatum larvae - some experiments on effect of thiouracil on metamorphosis.J. Mar. Biol. Assoc. UK. 1967; 47: 49-61Crossref Scopus (10) Google Scholar]. In their new work, Paris et al. [8Paris M. Escriva H. Schubert M. Brunet F. Brtko J. Ciesielski F. Roecklin D. Vivat-Hannah V. Jamin E. Cravedi J.P. et al.Amphioxus post-embryonic development reveals the homology of chordate metamorphosis.Curr. Biol. 2008; 18: 825-830Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar] found that precocious metamorphosis in larval amphioxus is induced by treating with T3 or T4, although T3 was more potent than T4. Importantly, metamorphosis could be blocked by the TR antagonist NH3. They also searched the amphioxus genome and found genes that encode proteins with sequence similarity to vertebrate enzymes involved in thyroid hormone metabolism, and a single homologue (amphiTR) of vertebrate thyroid hormone receptor genes. The authors isolated a full-length cDNA for amphiTR and found that the encoded protein can bind to thyroid hormone response elements in DNA in vitro, as a homodimer or a heterodimer with amphioxus RXR. Despite their earlier finding that T3 had biological activity in amphioxus in vivo, however, they were unable to detect T3-binding activity in nuclear extracts of amphioxus tissues, or with recombinant amphiTR in vitro. Furthermore, T3 could not activate amphiTR in a transient transfection assay conducted in a mammalian cell line. The authors note that, in the ligand binding domain of amphiTR, two of three amino acid residues known to be important for thyroid hormone binding differ from the equivalent residues of human TRα. From this they concluded that amphiTR is not a T3 binding protein, but the fact that T3 can induce metamorphosis suggests that amphioxus does have a functional thyroid hormone receptor that mediates the actions of T3 or its metabolites in vivo. The findings suggested two alternative hypotheses: first, that a protein other than the amphiTR mediates the actions of T3 on metamorphosis; or second, that T3 is not the endogenous ligand for amphiTR, but that exogenous T3 is converted to the endogenous ligand by amphioxus cells. Upon testing several iodothyronines Paris et al. [8Paris M. Escriva H. Schubert M. Brunet F. Brtko J. Ciesielski F. Roecklin D. Vivat-Hannah V. Jamin E. Cravedi J.P. et al.Amphioxus post-embryonic development reveals the homology of chordate metamorphosis.Curr. Biol. 2008; 18: 825-830Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar] discovered that triiodothyroacetic acid (TRIAC) is capable of binding to and activating amphiTR. Importantly, treatment with TRIAC induced metamorphosis in amphioxus, and there is evidence that amphioxus produces TRIAC. Thus, the findings support the conclusion that amphiTR can mediate a hormonal signal, and that the endogenous ligand is not T3, but instead TRIAC or perhaps a closely related iodothyronine. A very early gene regulation event caused by T3 during amphibian metamorphosis is the upregulation of TRβ [17Yaoita Y. Brown D.D. A correlation of thyroid hormone receptor gene expression with amphibian metamorphosis.Genes Dev. 1990; 4: 1917-1924Crossref PubMed Scopus (316) Google Scholar], a phenomenon known as receptor autoinduction [18Tata J.R. Autoinduction of nuclear hormone receptors during metamorphosis and its significance.Insect Biochem. Mol. Biol. 2000; 30: 645-651Crossref PubMed Scopus (35) Google Scholar]. Autoinduction depends on thyroid hormone receptors binding to thyroid hormone response elements in the TRβ gene, and is thought to be essential for driving metamorphosis [18Tata J.R. Autoinduction of nuclear hormone receptors during metamorphosis and its significance.Insect Biochem. Mol. Biol. 2000; 30: 645-651Crossref PubMed Scopus (35) Google Scholar]. Paris et al. [8Paris M. Escriva H. Schubert M. Brunet F. Brtko J. Ciesielski F. Roecklin D. Vivat-Hannah V. Jamin E. Cravedi J.P. et al.Amphioxus post-embryonic development reveals the homology of chordate metamorphosis.Curr. Biol. 2008; 18: 825-830Abstract Full Text Full Text PDF PubMed Scopus (99) Google Scholar] found that expression of amphiTR mRNA increased during spontaneous metamorphosis, and could be induced by T3 or TRIAC. They also showed that the 5′ flanking region of the amphiTR gene contains a putative thyroid hormone response element. Thus, receptor autoinduction likely existed in the earliest chordates and has been maintained by natural selection owing to its importance for the gene expression programs that drive metamorphosis. These new findings show that hormone signaling mediated by thyroid hormone receptors is phylogenetically ancient, and suggest that iodothyronine-induced metamorphosis is an ancestral feature of the chordates. However, the hormone conveys no detailed instructions to particular cells, but acts to turn on or off sets of genes that underlie specific developmental processes. The number and types of genes that are regulated by iodothyronines, and variation in their temporal and spatial expression patterns likely underlie the morphological diversity seen among different taxa. Thus, within a taxonomic group, a core set of regulators comprising nuclear hormone receptors and their ligands initiate life history transitions [19Truman J.W. Riddiford L.M. Endocrine insights into the evolution of metamorphosis in insects.Annu. Rev. Entomol. 2002; 47: 467-500Crossref PubMed Scopus (297) Google Scholar], but the generation of morphological diversity may have depended on selection for the types and nature of regulation of the downstream targets of the core regulators." @default.
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• W2023422445 title "Chordate Metamorphosis: Ancient Control by Iodothyronines" @default.
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