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Chapter 7 Chapter 7 The HypothalamusPituitary Thyroid (HPT) Axis of Non- Mammalian Vertebrates Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-1 Location of thyroid tissue in non-mammalian vertebrates. (A) Scattered thyroid follicles in a hagfish (Eptatretus burgeri). (B) Discrete thyroid gland of the shark Triakis scyllium. (C) Diffuse thyroids of the Japanese eel (Anguilla japonica) (left) and the Pacific salmon (Oncorhynchus masou) (right). (D) Paired thyroids in the bullfrog (Rana catesbeiana). (E) Medial thyroid gland in neck of the lizard Takydromas tachydromoides. (F) Paired thyroid glands in a bird, the Japanese quail (Coturnix coturnix japonicus). (Dissections of thyroid regions adapted with permission from Matsumoto, A. and Ishii, S., Atlas of Endocrine Organs, Springer-Verlag,Berlin, 1989.) 2 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-2 Salmon thyroid follicles. Cross-section through the lower jaw of a fingerling chinook salmon (Oncorhynchus tshawytscha) near the second aortic arch. Five thyroid follicles filled with colloid appear to the right of the ventral aorta (VA) and below the supporting cartilage (C). 3 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-3 Evolution of major events in thyroid physiology. Thyroid receptors (TRs) appeared prior to the divergence of the proterostome and deuterostome invertebrates (1). Endogenous thyroid hormone production was next (2), and linkage to TRs and involvement with metamorphosis represent perhaps the earliest roles of thyroid hormone, appearing first among deuterostome invertebrates (3). A thyroid-synthesizing organ first appears among the protochordates (4), but neuroendocrine control probably originated among the first vertebrates as evidence from extant cyclostomes (5). (Adapted with permission from Paris, M. et al., Integrative and Comparative Biology, 50, 63–74, 2008.) 4 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-4 Generalized pattern for evolution of the thyroid gland. (A) Initially, iodinated mucoproteins were distributed over the body surface of marine invertebrates and in the anterior digestive tract and later became restricted more to the mouth region, where iodinated mucoproteins related to a ciliary–mucus feeding mode were released from the mouth region and entered the gut. Once in the gut, the iodinated mucoproteins were digested, liberating iodinated tyrosines and thyronines. (B) The cephalochordate amphioxus has iodinated protein production confined to the endostyle in the mouth and pharynx. (C) Metamorphosis of the larval endostyle to a thyroid gland occurs during transformation of the ammocete larvae to the adult lamprey. 5 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-5 Amphioxus thyroid hormone events. Genomic evidence for the beginnings of the thyroid hormone synthesis and mode of action of thyroid hormones is present in this protochordate. Extracellular iodide is transported by a sodium-iodide pump symporter (NIS), incorporated into a glycoprotein forming T 4 through the actions of a thyroid peroxidase (TPO). The T 4 -containing glycoprotein is hydrolyzed to release T 4, which is converted to triiodothyronine (T 3 ) by a deiodinase. T 3 binds to a thyroid receptor (TR) and forms a dimer with the RXR receptor prior to binding to a thyroid response element (TRE) and altering the target genes activity (transcription). A gene coding for thyroglobulin apparently is absent in amphioxus. 6 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-6 Metamorphosis of the cephalochordate amphioxus. This process is controlled by thyroid hormones synthesized in the endostyle. The adult amphioxus closely resembles the ammocoetes larva of the vertebrate lamprey (Agnatha, Cyclostomata). (Photographs courtesy of Dr. Mathilde Paris.) 7 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-7 Oocytes of control (A) and radioiodide-treated (B) yearling rainbow trout (Oncorhynchus mykiss). The ovaries of fishes and other non-mammalian vertebrates readily concentrate iodide in the oocytes. The control ovary at the left exhibits a size range of developing oocytes. The ovary at the right is from a fish that accumulated radiodide ( 131 I) shortly after hatching. Although the radioactivity quickly decayed to undetectable levels, the ovary at the right contained only the largest class of oocytes when examined a year later. 8 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-8 Heterotopic thyroid tissue. This teleostean fish Xiphophorus maculatus has thyroid follicles (yellow dots) located not only throughout the pharyngeal region but also in the heart, head kidney, and sometimes even in the gonads and liver. (Adapted with permission from Baker-Cohen, K.F., in Comparative Endocrinology (A. Gorbman, Ed.), John Wiley & Sons, New York, 1959, pp. 283–319.) 9 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-9 Phylogeny of deiodinase genes in vertebrates. Some species are omitted for whom there is evidence for deiodinases because the responsible genes have not been analyzed. Note that Xenopus has all three genes although evidence for other amphibians does not support the presence of a D1 deiodinase. (Adapted with permission from Johnson, K.M. and Lema, S.C., General and Comparative Endocrinology, 172, 505–517, 2011.) 10 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-10 Phylogeny of vertebrate thyroid receptors. Tissue-specific thyroid hormone regulation of gene transcripts encoding thyroid hormone receptors in striped parrotfish (Scarus iseri). (Adapted with permission from Johnson, K.M. and Lema, S.C., General and Comparative Endocrinology, 172, 505–517, 2011.) 11 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-11 Metamorphosis of the flounder Pleuronectes platessa. During metamorphosis (C-F), which is controlled by thyroid hormones, one eye migrates from one side of the body to the other. (Adapted with permission from Blaxter, J.H.S., in Fish Physiology (W.S. Hoar and D.J. Randall, Eds.), Academic Press, San Diego, CA, 1988, pp. 11A, 1–58.) 12 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-12 Life cycle of Pacific salmon and steelhead (Oncorhynchus spp.). This pattern is characteristic of most species; however, in pink and chum salmon that spawn in coastal streams, the fry are washed directly into the ocean. (Adapted with permission from Ueda, H., General and Comparative Endocrinology, 170, 222– 232, 2011.) 13 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-13 Plasma hormone levels during Parr smoltification of coho salmon. Prolactin, growth hormone, thyroxine, and cortisol all peak during smoltification. Insulin peaks in the parr and declines as smoltification gets under way. (Adapted with permission from Dickhoff, W. et al., Journal of Experimental Zoology, 256 (Suppl. S4), 90–97, © John Wiley & Sons.) 14 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-14 Smolting in steelhead trout (Oncorhyncus mykiss). Thyroid hormone stimulates deposition of guanine in the scales. (A) Smolts. (B) Parr. 15 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-15 Histological appearance of thyroid epithelium of a migrating adult sockeye salmon (Oncorhynchus nerka). Note that the epithelium appears goitrous in that it is highly columnar, indicative of intense TSH stimulation. Little colloid is associated with the lumen, suggesting depletion. Arrow indicates colloid droplet endosome in the apical end of the follicle cell. Would you consider this a hyperthyroid or hypothyroid condition? Why? 16 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-16 Effect of T 4 treatment on growth of radiothyroidectomized steelhead trout. (Adapted with permission from Norris, D.O., Transactions of the American Fisheries Society, 97, 204–206, 1969.) 17 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-17 Comparison of morphological changes during metamorphosis of an anuran (left) and a urodele (right) amphibian. Urodeles quickly reach stage 4 and remain in this stage with external gills most of their larval lives. Anurans may spend a few weeks or up to 2 years at stage 2 before limbs emerge. Resorption of the anuran tail (metamorphic climax) may be delayed for some time after emergence of the hind limbs but occurs rapidly once the forelimbs emerge. Note that when urodeles undergo metamorphosis, the external gills are resorbed as is the tail fin (stages 5 and 6). 18 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-18 Urea–ammonia excretion during anuran metamorphosis. Aquatic animals excrete ammonia as their principal nitrogenous wastes, whereas terrestrial amphibians produce urea. Immersion of tadpoles in water containing thyroxine induces a switch from ammonia excretion to urea excretion similar to that observed during normal metamorphosis. A similar pattern to the ammonia change is seen for other metamorphic changes such as regression of tail whereas growth of hind limbs exhibits a urea-like pattern. 19 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-19 Effects of TRH and CRH on metamorphosis of the coqui (Eutherodactylus coqui). Neither saline nor TRH affected the rate of metamorphosis, but CRH treatment accelerated metamorphosis. Note tail regression and changes in body and head shape. (Adapted with permission from Kulkarni, S.S. et al., General and Comparative Endocrinology, 169, 225–230, 2010.) 20 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-20 Hormonal changes during bullfrog metamorphosis. Thyroxine, prolactin, and corticosterone all peak at metamorphic climax. These changes are characteristic of both anurans and urodeles. Compare to the pattern of hormone secretion in smoltification of salmonid fishes (Figure 7-13). (Adapted with permission from Dickhoff, W. et al., Journal of Experimental Zoology, 256 (Suppl. S4), 90–97, © John Wiley & Sons.) 21 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-21 Changes in deiodinase activities during metamorphosis. The reduction of D3 deiodinase activity in liver and increases in D2 deiodinase activity in skin and gut leads to increased conversion of T 4 to T 3 and metamorphic climax. (Adapted with permission from Galton, V.A., Trends in Endocrinology & Metabolism, 3, 96–100, © Elsevier Science, Inc.) 22 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-22 Expression of thyroid hormone receptors (TR α and TR β ) as well as RXRs during early embryonic development and metamorphosis. (A) TRs are expressed very early in embryonic development, even before the thyroid gland differentiates, possibly to respond to TH deposited into the egg by the mother. Note the increase in tadpole synthesis of thyroid hormones (TH). (B) Na + -I symporter (NIS) and thyrotropin (TSH) during metamorphic climax. (Adapted with permission from Furlow, J.D. and Neff, E.S., Trends in Endocrinology & Metabolism, 17, 38–45, 2006; Korte, J.J. et al., Gen. Comp. Endocrinol., 171, 319–325, 2011; Opitz, R. et al., J. Endocrinol., 190, 157–170, 2006.) 23 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-23 Environmental factors affecting metamorphosis in amphibians. Stress (e.g., pond drying, high population densities, salinity changes) and long photoperiods can stimulate metamorphosis in populations of amphibians through effects on hypothalamic regulation of pituitary secretion and release of T 4 and increased conversion of T 4 to T 3 as well as elevations in corticosterone (B) from the interrenal (adrenal). (Adapted with permission from Denver, R.J., Comparative Biochemistry and Physiology C, 119, 219–228, 1998.) 24 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-24 Skin changes associated with metamorphosis in a urodele amphibian. (A) Histological section through skin of larval tiger salamander (Ambystoma tigrinum) showing prominent Leydig cells (arrows). (B) During metamorphosis, the Leydig cells degenerate and release their secretions that are thought to contribute to the relative impermesbility of the skin of a terrestrial adult. Arrow indicates mucous cell (slightly lower magnification). 25 Copyright © 2013 Elsevier Inc. All rights reserved.
Figure 7-25 Distribution of developmental and thermogenic action of thyroid hormones in vertetrates. Perhaps developmental and/or permissive actions were the initial roles for thyroid hormones. Thermogenesis appears with the acquisition of homeothermy possibly in the reptilian ancestors of birds and mammals. (Adapted with permission from Oppenheimer, J.H. et al., in Molecular Endocrinology: Basic Concepts and Clinical Correlations (B.D. Weintraub, Ed.), Raven Press, New York, 1995, pp. 249–268.) 26 Copyright © 2013 Elsevier Inc. All rights reserved.
Box Figure 7A-1 Environmental perchlorate and frog thyroid histology. Thyroid tissue in a chorus frog from a reference site in Texas appears at the left. On the right is a hyperstimulated thyroid gland from a perchlorate- contaminated site, presumably a result of increased thyrotropin secretion. (Photomicrographs courtesy of Dr. James A. Carr, Texas Tech University.) 27 Copyright © 2013 Elsevier Inc. All rights reserved.
Box Figure 7A-2 Effect of perchlorate exposure in the laboratory. The paired thyroid glands of a control frog can be seen at the left in marked contrast to the goitrous thyroids in the frog exposed to 14 ppm of ammonium perchlorate. (Photomicrograph courtesy of Dr. James A. Carr, Texas Tech University.) 28 Copyright © 2013 Elsevier Inc. All rights reserved.
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