The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction

Critical Reviews in Toxicology

Volumn 37, Issue 1-2, 2007, Pages 97-115

  Blanton, Michael L ^a   Specker, Jennifer L ^b  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

Chemical Screen; Development; Endocrine Disruption; Reproduction; Teleostean Thyroid

Indexed keywords

ANTITHYROID AGENT; ENDOCRINE DISRUPTOR; IODINE; LIOTHYRONINE; THIOUREA; THYROXINE;

CENTRAL NERVOUS SYSTEM; DEIODINATION; DEVELOPMENTAL STAGE; ENDOCRINE SYSTEM; EX VIVO STUDY; EXPERIMENTAL MODEL; HORMONE ACTION; HORMONE BLOOD LEVEL; HORMONE DETERMINATION; HORMONE RELEASE; HORMONE SYNTHESIS; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IN VITRO STUDY; IN VIVO STUDY; LABORATORY; LARVA; METHODOLOGY; MOLECULAR BIOLOGY; NEGATIVE FEEDBACK; NONHUMAN; REPRODUCTION; REVIEW; SCREENING; SEX DIFFERENCE; SPECIES IDENTIFICATION; THYROID FOLLICLE; THYROID FUNCTION; THYROID GLAND; THYROID HORMONE METABOLISM; VERTEBRATE;

ANIMALS; ENDOCRINE DISRUPTORS; FISHES; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MODELS, BIOLOGICAL; REPRODUCTION; THYROID GLAND;

ANIMALIA; MAMMALIA; OSTEICHTHYES; PISCES; VERTEBRATA;

EID: 33847043562     PISSN: 10408444     EISSN: 15476898     Source Type: Journal    
DOI: 10.1080/10408440601123529     Document Type: Review

References (100)

1. Abrahams, M.V., and Pratt, T.C. (2000). Hormonal manipulations of growth rate and its influence on predator avoidance: Foraging tradeoffs. Can. J. Zool. 78(1):121-127.
2. Adams, B.A., Cyr, D.G., and Eales, J.G. (2000). Thyroid hormone deiodination in tissues of American plaice, Hippoglossoides platessoides: Characterization and short-term responses to polychlorinated biphenyls (PCBs) 77 and 126. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 127:367-378.
3. Alestrom, P., Husebye, H., Kavumpurath, S., and Kisen, G. (1994). Zebrafish: A vertebrate model for transgene expression and biological function. Anim. Biotechnol. 5(2):147-154.
4. Ayson, F.G., and Lam, T.J. (1993). Thyroxine injection of female rabbitfish (Siganus guttatus) broodstock: Changes in thyroid hormone levels in plasma, eggs, and yolksac larvae, and its effect on larval growth and survival. Aquaculture 109:83-93.
5. Batten, T.F.C., and Ingleton, P.M. (1987). The structure and function of the hypothalamus and pituitary gland. In: Comparative Vertebrate Endocrinology, I. Chester-Jones, P.M. Ingleton, and J.G. Phillips, eds., pp. 285-412. Academic Press, London.
6. Bently, P.J. (1998). Comparative Vertebrate Endocrinology, 3rd ed. Cambridge University Press, Cambridge, UK.
7. Bowen, R. (1999). Chemistry of thyroid hormones. Available online: www.vivo.colostate.edu/hbooks/pathphys/endocrine/thyroid/chem.html.
8. Bres, O., MacLatchy, D.L., and Eales, J.G. (1994). Thyroid hormone: Deiodinase and receptor assays. In: Biochemistry and Molecular Biology of Fishes, Volume 3, P.W. Hochachka and T.P. Mommsen, eds. Elsevier, Amsterdam.
9. Brouwer, A., Klassonwehler, E., Bokdam, M., Morse, D.C., and Traag, W.A. (1990). Competitive-inhibition of thyroxine binding to transthyretin by monohydroxy metabolites of 3,4,3′,4′-tetrachlorobiphenyl. Chemosphere 20(7-9):1257-1262.
10. Brown, B.S., Adams, A.B., Cyr, G.D., and Eales, G.J. (2004). Review: Contaminant effects on the teleost fish thyroid. Environ. Toxicol. Chem. 23(7):1680-1701.
11. Brown, C.L., Sullivan, C.V., Bern, H.A., and Dickhoff, W.W. (1987). Occurrences of thyroid hormones in early developmental stages of teleost fish. Am. Fisheries Soc. Symp. 2:144-150.
12. Brown, D.D. (1997). The role of thyroid hormone in zebrafish and axolotl development. Proc. Natl. Acad. Sci. USA 94:13011-13016.
13. Cerda-Reverter, J., Zanuy, S., Carrillo, M., and Kah, O. (1996). Development of enzyme immunoassays for 3,5,3-triiodo-l-thyronine and l-thyroxine: Time-course studies on the effect of food deprivation on plasma thyroid horomones in two marine teleosts, sea bass (Dicentrarchus labrax L.) and sea bream (Sparus aurata L.). Gen. Comp. Endocrinol. 103:290-300
14. Chatterjee, A., Hsieh, Y.L., and Yu, J.Y.L. (2001), Molecular cloning of cDNA encoding thyroid stimulating hormone beta subunit of bighead carp Aristichthys nobilis and regulation of its gene expression. Mol. and Cell. Endocrinol. 174(1-2):1-9.
15. Creech, M.M., Arnold, E.V., Boyle, B., Muzinich, M.C., Montville, C., Bohle, D.S., and Atherton, R.W. (1998). Sperm motility enhancement by nitric oxide produced by the oocytes of fathead minnows, Pimephthales promelas. J. Androl. 19(6):667-674.
16. Cyr, D.G., and Eales, J.G. (1988a). Influence of thyroidal status on ovarian function in rainbow trout, Salmo gairdneri. J. Exp. Zool. 248(1):81-87.
17. Cyr, D.G., and Eales, J.G. (1988b). In vitro effects of thyroid-hormones on gonadotropin-induced estradiol-17-beta secretion by ovarian follicles of rainbow trout, Salmo gairdneri. Gen. Comp. Endocrinol. 69(1):80-87.
18. Cyr, D.G., and Eales, J.G. (1989). T3 Enhancement of in vitro estradiol-17-beta secretion by oocytes of Rainbow trout, Salmo gairdneri, is dependent on camp. Fish. Physiol. Biochem. 6(4):255-259.
19. Cyr, D.G., and Eales, J.G. (1996). Interrelationships between thyroidal and reproductive endocrine systems in fish. Rev. Fish. Biol. Fisheries 6(2):165-200.
20. Damstra, T., Barlow, S., Bergman, A., Kavlock, R., and Van Der Kraak, G. (2002). Global assessment of the state-of-the-science of endocrine disruptors. International Programme on Chemical Safety, prepared by an expert group on behalf of the World Health Organisation, the International Labour Organisation, and the United Nations Environment Programme.
21. Darras, V.M., Mol, K.A., Van der Geyten, S., and Kuhn, E.R. (1998). Control of peripheral thyroid hormone levels by activating and inactivating deiodinases. Trends Comp. Endocrinol. Neurobiol. 839:80-86.
22. DeJesus, E.J., Inui, Y., and Hirano, T. (1990). Cortisol enhances the stimulating action of thyroid hormones on dorsal fin-ray resorption of flounder larvae in vitro. Gen. Comp. Endocrinol. 79:167-173.
23. DeJesus, E.J., Hirano, T., and Inui, Y. (1991). Changes in cortoisol and thyroid hormones concentrations during early development and metamorphosis in the Japanese flounder, Paralichthys olivaceus. Gen. Comp. Endocrinol. 82:369-376.
24. DeJesus, E.G., Toledo, J.D., and Simpas, M.S. (1998). Thyroid hormones promote early metamorphosis in grouper (Epinephelus coioides) larvae. Gen. Comp. Endocrinol. 112:10-16.
25. De Vito, M., Biegel, L., Brouwer, A., Brown, S., Brucker-Davis, F., Cheek, A., Christensen, R., Colborn, T., Cooke, P., Crissman, J., Crofton, K., Doerge, D., Gray, E., Hauser, P., Hurley, P., Kohn, M., Lazar, J., McMaster, S., McClain, M., McConnell, E., Meier, C., Miller, R., Tietge, J., and Tyl, R. (1999). Screening methods for thyroid hormone disruptors. Environ. Health Perspect. 107:407-415.
26. Dickhoff, W.W., Folmar, L.C., and Gorbman, A. (1978). Changes in plasma thyroxine during smoltification of coho salmon, Oncorhynchus kisutch. Gen. and Comp. Endocrinol. 36:229-232.
27. Eales, J.G. (1979). Thyroid function in cyclostomes and fishes. In: Hormones and Evolution, Volume 1, E.J. Barrington, ed., pp. 341-436. Academic Press, New York.
28. Eales, J.G., and Brown, S.B. (1993). Measurement and regulation of thyroidal status in teleost fish. Rev. Fish. Biol. Fisheries 3(4):299-347.
29. Eales, J.G., Brown, S.B., Cyr, D.G., Adams, B.A., and Finnson, K.R. (1999). Deiodination as an index of chemical disruption of thyroid hormone homeostasis and thyroidal status in fish. In: Environmental Toxicology and Risk Assessment: Standardization of Biomarkers for Endocrine Disruption and Environmental Assessment, Volume 8, ASTM STP 1364, D.S.Henshel, M.C. Black, and M.C. Harrass, eds. American Society for Testing and Materials, West Conshohocken, PA.
30. Fentress, J.A., Brouwer, T.H., Brouwer, M., McLachlan, J.A., and Cheek, A.O. (2000). Examination of a potential environmental antiestrogen, Am. Zool. 40(6):1013-1014.
31. Fujiwara, N. (1980). Effects of thyroid hormones on the gonad and the secondary sex characteristic of Medaka Oryzias-latipes. Biol. J. Nara. Women's Univ. No. 29-30:1-2.
32. Gavlik, S., Albino, M., and Specker, J.L. (2002). Metamorphosis in summer flounder: Manipulation of thyroid status to synchronize settling behavior, growth, and development. Aquaculture 203:359-373.
33. Harder, S., Dammann, O., Buck, F., Zwiers, H., Lederis, K., Richter, D., and Bruhn, T.O. (2001). Cloning of two thyrotropin-releasing hormone receptor subtypes from a lower vertebrate (Catostomus commersoni): Functional expression, gene structure, and evolution. Gen. Comp. Endocrinol. 124(2):236-245.
34. Higgs, D.A., and Eales, J.G. (1971). Iodide and thyroxine metabolism in brook trout, Salvelinus fontinalis (Mitchill) during sustained exercise. Can. J. Zool. 49:1255-69.
35. Hoar, W.S. (1939). The thyroid gland of the Atlantic salmon. J. Morphol. 65:257-295.
36. Holmes, J.A., and Youson, J.H. (1993). Induction of metramorphosis in landlocked sea lampreys, Petromyson marinus. J. Exp. Zool. 276:598-604.
37. Huang, L., Schreiber, A.M., Soffientino, B., Bengtson, D.A. and Specker, J.L. (1998). Metamorphosis of summer flounder (Paralichthys dentatus): Thyroid status and the timing of gastric gland formation. J. Exp. Zool. 280:413-420.
38. Inui, Y., and Miwa, S. (1985). Thyroid hormone induces metamorphosis of flounder larvae. Gen. Comp. Endocrinol. 60:450-454.
39. Ishwar, S. Parhar, Tomoko, S., and Yasuo, S. (2000). Thyroid hormone and estrogen regulate brain region-specific messenger ribonucleic acids encoding three gonadotropin-releasing hormone genes in sexuality immature male fish, Oreochromis niloticus. Endocrinology 141(5).
40. Iwamatsu, T., Kobayashi, H., Hamaguchi, S., Sagegami, R., and Shuo, T. (2000). Sex reversal of Medaka (Oryzias latipes) by a short exposure of embryos to sex steroids. Zool. Sci. (Tokyo), 17(Suppl):15.
41. Janz, D.M. (2000). Endocrine system. In: The Laboratory Fish, G.K.Ostrander, ed., Chap. 25. Academic Press, San Diego.
42. Kime, D.E. (1998). Endocrine disruption in fish. Kluwer Academic Publishers, Boston.
43. Kobuke, L., Specker, J.L., and Bern, H.A. (1987). Thyroxine content of eggs and larvae of coho salmon, Oncorhynchus kisutch. J. Exp. Zool. 242:89-94.
44. Kumar, R.S., Ijiri, S., Kight, K., Swanson, P., Dittman, A., Alok, D., Zohar, Y., and Trant, J.M. (2000). Cloning and functional expression of a thyrotropin receptor from the gonads of a vertebrate (bony fish): Potential thyroid-independent role for thyrotropin in reproduction. Mol. Cell. Endocrinol. 167(1-2):1-9.
45. Lagler, K., Bardach, J., Miller, R., and Passino, D. (1977). Ichthyology, 2nd ed. John Wiley & Sons, New York.
46. Lanno, R.P., and Dixon, D.G. (1990). Chronic effects of thiocyanate in fathead minnows: A model for the effects of a waterborne antithyroid on reproduction in fish. In: Proceedings of the 17th Annual Aquatic Toxicity Workshop, November 5-7, 1990, Vancouver, BC. Can. Tech. Rep. Fish. Aquat. Sci. 1(2):496-500.
47. Lanno, R.P., and Dixon, D.G. (1994). Chronic toxicity of waterborne thiocyanate to the fathead minnow (Pimephales promelas): A partial life-cycle study. Environ. Toxicol. and Chem. 13(9):1423-1432.
48. Leatherland, J.F. (1982). Environmental physiology of the teleostean thyroid gland: A review. Env. Biol. Fishes 7:83-110.
49. Leatherland, J.F. (1985). Effects of 17β-estradiol and methyl testosterone on the activity of the thyroid gland in rainbow trout, Salmo gairdneri Richardson. Gen. Comp. Endocrinol. 60:343-352.
50. Leatherland, J.F., Lin, L., Down, N.E., and Donaldson, E.M. (1989). Thyroid hormone content of eggs and early development stages of five Oncorhynchus species. Can. J. Fish. Aquat. Sci. 46:2140-2145.
51. Leatherland, J.F., Reddy, P.K., Yong, A.N., Leatherland, A., and Lam, T.J. (1990). Hepatic 5′-monodeiodinase activity in teleosts in vitro - A survey of 33 species. Fish. Physiol. Biochem. 8(1):1-10.
52. Legler, J., Broekhof Jose, L.M., Brouwer, A., Lanser, P.H., Murk, A.J., Van Der Saag, P.T., Vethaak, A.D., Wester, P., Zivkovic, D., and Van Der Burg, B. (2000). A novel in vivo bioassay for (xeno-) estrogens using transgenic zebrafish. Environ. Sci. Technol. 34(20):4439-4444.
53. Maurer, F. (1886). Schilddrüse und thymus der teleostier. Morphol. Jahrbuch. 11:129-175.
54. Miwa, S., and Inui, Y. (1987). Effects of various doses of thyroxine and triiodothyronine on the metamorphosis of flounder (Paralichthys olivaceus). Gen. Comp. Endocrinol. 67:356-363.
55. Miwa, S., Yamano, K., and Inui, Y. (1992). Thyroid hormone stimulates gastric development in flounder larvae during metamorphosis. J. Exp. Zool. 261:424-430.
56. Mol, K.A., Van der Geyten, S., Darras, V.M., Visser, T.J., and K̈uhn, E.R. (1997). Characterization of iodothyronine outer ring and inner ring deiodinase activities in the blue tilapia, Oreochromis aureus. Endocrinology 138(5):1787-1793.
57. Mol, K.A., Van der Geyten, S., Burel, C., K̈uhn, E.R., Boujard, T., and Darras, V.M. (1998). Comparative study of iodothyronine outer ring and inner ring deiodinase activities in five teleostean fishes. Fish. Physiol. Biochem. 18:253-266.
58. Mukhi, S., Carr, J.A., Anderson, T.A., and Patino, R. (2005). Novel biomarkers of perchlorate exposure in zebrafish. Envir. Toxicol. Chem. 24(5):1107-1115.
59. Nacario, J.F. (1983). The effect of thyroxine on the larvae and fry of Sarotherodon niloticus L. (Tilapia nilotica). Aquaculture 34:78-83.
60. Nayak, P.K., Mishra, T.K., Mishra, J., Ayyappan, S., and Singh, B.N. (2000). Changes in thyroid hormones and 5-monodeiodinase activity during embryonic and larval developments in freshwater cat-fish, Heteropneustes fossilis. Indian J. Anim. Sci. 70(11):1191-1195.
61. Nishikawa, K. (1976). Influence of methyl testosterone on the thyroid gland of the medaka Oryzias-latipes. Bull. Fac. Fish. Hokkaido Univ. 27(3-4)121-128.
62. Nishioka, R.S., Grau, E.G., Lai, K.V., and Bern, H.A. (1987). Effect of thyroid-stimulating hormone on the physiology and morphology of the thyroid gland in coho salmon, Oncorhynchus kisutch. Fish. Physiol. Biochem. 3(2):63-71.
63. Oba, Y., Hirai, T., Yoshiura, Y., Kobayashi, T., and Nagahama, Y. (2001). Fish gonadotropin and thyrotropin receptors: The evolution of glycoprotein hormone receptors in vertebrates. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 29(23):441-448.
64. Orozco, A., Silva, J.E., and Valverde, R.C. (1997). Rainbow trout liver expresses two iodothyronine phenolic ring deiodinase pathways with the characteristics of mammalian types I and II deiodinases. Endocrinology 138(1):254-8.
65. Patino, R., Wainscoft, M.R., Cruz-Li, E.I., Balakrishnan, S., McMurry, C., Blazer, V.S., and Anderson, T.A. (2003). Effects of ammonium perchlorate on the reproductive performance and thyroid follicle histology of zebrafish. Environ. Toxicol. Chem. 22(5):1115-1121.
66. Pavlidis, M., Greenwood, L., Mourot, B., Kokkari, C., Le Menn, F. Divanach, P., and Scott, A.P. (2000). Seasonal variations and maturity stages in relation to differences in serum levels of gonadal steroids, vitellogenin and thyroid hormones in the common dentex (Dentex dentex). Gen. Comp. Endocrinol. 118:14-25.
67. Peter, R.E., Yu, K-L., Marchant, T.A., and Rosenblum, P.M. (1990). Direct neural regulation of the teleost adenohypophysis. J. Exp. Zool. Suppl. 4:84-89.
68. Pickford, G.E., and Atz, J.W. (1957) The physiology of the pituitary gland of fishes. New York Zoological Society, New York.
69. Power, D.M., Llewellyn, L., Faustino, M., Nowell, M., Bjornsson, B., Einarsdottir, I., Canario, A., and Sweeney, G. (2001). Thyroid hormones in growth and development of fish. Comp. Biochem. Physiol. C130:447-459.
70. Pradet-Balade, B., Schmitz, M., Salmon, C., Dufour, S., and Querat, B. (1997). Down-regulation of TSH subunit mRNA levels by thyroid hormones in the European eel. Gen. Comp. Endocrinol. 108(2):191-198.
71. Pradet-Balade, B., Burel, C., Dufour, S., Boujard, T., Kaushik, S.J., Querat, B., and Boeuf, G. (1999). Thyroid hormones down-regulate thyrotropin beta mRNA level in vivo in the turbot (Psetta maxima). Fish. Physiol. Biochem. 20(3):193-199.
72. Raine, J.C., Takemura, A., and Leatherland, J.F. (2001). Assessment of thyroid function in adult medaka (Oryzias latipes) and juvenile rainbow trout (Oncorhynchus mykiss) using immunostaining methods. J. Exp. Zool. 290(4):366-378.
73. Sathyanesan, A.G., Joy, K.P., and Kulkarni, R.S. (1978). Endocrine changes in fishes in response to pollutants. Q. J. Surg. Sci. 14(1, 2):67-77.
74. Schnurstein, A., and Braunbeck, T. (2001). Tail moment versus tail length: Application of an in vitro version of the comet assay in biomonitoring for genotoxicity in native surface waters using primary hepatocytes and gill cells from zebrafish (Danio rerio). Ecotoxicol. Environ. Safety 49(2):187-196.
75. Schreiber, A.M., and Specker J.L. (1998). Metamorphosis in the summer flounder (Paralichthys dentatus): Stage-specific developmental response to altered thyroid status. Gen. Comp. Endocrinol. 111(2):156-166.
76. Schreiber, A.M., and Specker, J.L. (1999a). Metamorphosis in the summer flounder (Paralichthys dentatus): Thyroidal status influences salinity tolerance. J. Exp. Zool. 284:414-424.
77. Schreiber, A.M., and Specker, J.L. (1999b). Early larval development and metamorphosis in the summer flounder: Changes in percent whole-body water content and effects of altered thyroid status. J. Fish. Biol. 55:148-157.
78. Schreiber, A.M., and Specker, J.L. (1999c). Metamorphosis in the summer flounder (Paralichthys dentatus): Changes in gill mitochondriarich cells. J. Exp. Biol. 202:2475-2484.
79. Scott, A.P. (1987). Reproductive Endocrinology of Fish. In: Comparative Vertebrate Endocrinology, I. Chester-Jones, P.M. Ingleton, and J.G. Phillips, eds., pp. 223-256. Academic Press, London.
80. Siwik, P.L., Van Meer, T., Mackinnon, M.D., and Paszkowski, C. (2000). Growth of fathead minnows in oils and-processed wastewater in laboratory and field. Environ. Toxicol. Chem. 19(7):1837-1845.
81. Soffientino, B., and Specker, J.L. (2001). Metamorphosis of summer flounder, Paralichthys dentatus: Cell proliferation and differentiation of the gastric mucosa and developmental effects of altered thyroidal status. J. Exp. Zool. 290(1):31-40.
82. Soffientino, B., and Specker, J.L. (2003). Age-dependent changes in the response of the stomach to thyroidal signaling in developmentally arrested larval summer flounder. Gen. Comp. Endocrinol. 134(3):237-43.
83. Soyano, K., Saito, T., Nagae, M., and Yamauchi, K. (1993). Effects of thyroid hormone on gonadotropin-induced steroid production in medaka, Oryzias latipes, ovarian follicles. Proc. Second Int. Symp. Fish. Endocrinol. 11(1-6):265-272.
84. Specker, J.L., Brown, C.L., and Bern, H.A. (1992). Asynchrony of tissue and plasma thyroid hormone contents during parr-smolt transformation of salmon. Gen. Comp. Endocrinol. 88:397-405.
85. Specker, J.L, Eales, J.G., Tagawa, M., and Tyler, III, W. A. (2000). Parr-smolt transformation in Atlantic salmon: Thyroid hormone deiodination in liver and brain and endocrine correlates of change in rheotactic behavior. Can. J. Zool. 78:696-705.
86. Specker, J.L., and Schreck, C.B. (1982). Changes in plasma corticosteroids during smoltification of coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 46:53-58.
87. Sweeting, R.M., and Eales, J.G. (1992). HPLC analysis of in vitro deiodination products of thyroid hormones in the rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 85:367-375.
88. Tagawa, M., and Hirano, T. (1989). Changes in tissue and blood concentrations of thyroid hormones in developing chum salmon. Gen. Comp. Endocrinol. 76:437-443.
89. Tagawa, M., and Hirano, T. (1991). Effects of thyroid hormone deficiency in eggs on early development of the medaka Oryzias-latipes. J. Exp. Zool. 257(3):360-366.
90. Tagawa, M., Tanaka, M., Matsumoto, S., and Hirano, T. (1990). Thyroid hormones in eggs of various freshwater, marine, and diadromous teleosts and their changes during egg development. Fish. Physiol. Biochem. 8:515-20.
91. Tanaka, M. (1971). Studies on the structure and function of the digestive system in teleost larvae. apn J. Ichthyol. 18:164-174.
92. Tomas, M.J, and Thomas, J.A. (2001). Hormone Assays and Endocrine Function. In: Principles and Methods of Toxicology, Fourth Edition, A.W. Hayes, ed., pp. 1383-1413. CRC Press, Boca Raton, FL.
93. Van Oordt, P.G.W.J., and Peute, J. (1983). The cellular origin of pituitary gondotropins in teleosts. In: Fish Physiology, W.E. Hoar and D.J. Randall, eds., pp. 137-186. Academic Press, San Diego, CA.
94. Wabuke-Bunoti, M.A.N., and Firling, C.E. (1983). The prehatching development of the thyroid-gland of the fathead minnow, Pimephalespromelas (Rafinesque). Gen. Comp. Endocrinol. 49(2):320-331.
95. Wendelaar Bonga, S.E. (1993). Endocrinology. In: The Physiology of Fishes, D. H. Evans, ed., pp. 469-502. CRC Press, Boca Raton, FL.
96. Wester, P.W., Canton, J.H., and Dormans, J.A.M.A. (1988). Pathological effects in fresh-water fish Poecilia-reticulata (Guppy) and Oryzias-latipes (Medaka) following methyl-bromide and sodium-bromide exposure. Aquatic Toxicology 12:323-343.
97. Yamano, K., Arakai, K., Sekikawa, K., and Inui, Y. (1994). Cloning of thyroid hormone receptor genes expressed in metamorphosing flounder. Dev. Gen. 15:378-382.
98. Yamano, K., and Inui, Y. (1995). cDNA cloning of thyroid hormone receptor β from the Japanese flounder. Gen. Comp. Endocrinol. 99:197-203.
99. Yoshiura, Y., Sohn, Y.C., Munakata, A., Kobayashi, M., and Aida, K. (1999). Molecular cloning of the cDNA encoding the beta subunit of thyrotropin and regulation of its gene expression by thyroid hormones in the goldfish, Carassius auratus. Fish. Physiol. Biochem. 21(3):201-210.
100. Youson, J.H. (1988). First metamorphosis. In: Fish Physiology, XI, W.S. Hoar and D.J. Randall, eds., pp. 135-196. Academic Press, San Diego.