Abstract
Thyroid hormones transiently increase during parr-smolt transformation in coho salmon, Oncorhynchus kisutch, and are believed to trigger morphological, physiological, behavioural, and neural changes. The effectiveness of propylthiouracil (PTU) to induce hypothyroidism in smolting coho salmon was determined by immersing coho salmon, Oncorhynchus kisutch, in 30 mg l−1 PTU from May 1, two weeks prior to the consistent annual total thyroxine (TT4) peak in mid-May, until the last sampling date. Plasma was obtained at two sampling dates from control and PTU -treated coho salmon: May 15, during the plasma TT4 peak; and May 26, after the TT4 peak. Radioimmunoassays were used to measure plasma TT4, total triiodothyronine (TT3), free thyroxine (FT4), and salmon growth hormone (sGH). The PTU -treatment inhibited the natural smoltification-related increases in plasma TT4, TT3 and GH levels compared with controls, but PTU-treatment did not affect these hormone levels when they were low. PTU -treatment increased FT4 and decreased TT3 and sGH levels in the May 26 sample. In the May 15 sample, FT4 levels were unaffected by PTU-treatment, whereas TT4 levels were decreased. These data demonstrate the ability of PTU to induce hypothyroidism in salmonids as shown by the decrease in TT4 and TT3. These data demonstrate that PTU treatment by immersion can induce hypothyroidism in salmonids as shown by: (1) the inhibition of the natural increases of TT4 and TT3; (2) the increase in FT4 levels corresponding to the lowered TT3 levels, suggesting an inhibition of thyroxine 5′-monodeiodinase activity. We also show for the first time that PTU treatment can lower plasma GH levels in salmonids. This lowering of plasma GH level is associated with the decrease in TT3 levels and the increase in FT4 levels. The PTU induced lowering in GH levels may contribute to the observed changes in FT4 and TT3, since GH is known to increase thyroxine 5′-monodeiodinase activity.
Similar content being viewed by others
References
Ahmed, M. T., Sinha, A. K., Pickard, M. R., Kim, K. D. and Ekins, R. P. 1993. Hypothyroidism in the adult rat causes brain regionspecific biochemical dysfunction. J. Endocrinol. 138: 299–305.
Behnam-Rassoli, M., Herbert, L. C., Howard, V., Pharoah, P. O. D. and Stanisstreet, M. 1991. Effect of propylthiouracil treatment during prenatal and early postnatal development on the neocortex of rat pups. Neuroendocrinology 53: 321–327.
Bernal, J. and Nuñez, J. 1995. Thyroid hormones and brain development. Eur. J. Endocrinol. 133: 390–398.
Björnsson, B. Th., Stefansson, S. O. and Hansen, T. 1995. Photoperiod regulation of plasma growth hormone levels during parrsmolt transformation of Atlantic salmon: Implications for hypoosmoregulatory ability and growth. Gen. Comp. Endocrinol. 100: 73–82.
Björnsson, B. Th., Taranger, G. L., Hansen, T., Stefansson, S. O. and Haux, C. 1994. The interrelation between photoperiod, growth hormone, and sexual maturation of adult Atlantic salmon (Salmo salar). Gen. Comp. Endocrinol. 93: 70–81.
Björnsson, B. Th., Thorarensen, H., Hirano, T., Ogasawara, T. and Kristinsson, J. B. 1989. Photoperiod and temperature affect plasma growth hormone levels growth condition factor and hypoosmoregulatory ability of juvenile Atlantic salmon (Salmo salar) during parr-smolt transformation. Aquaculture 82: 77–92.
Björnsson, B. Th., Yamauchi, K., Nishioka, R. S., Deftos, L. J. and Bern, H. A. 1987. Effects of hypophysectomy and subsequent hormonal replacement therapy on hormonal and osmoregulatory status of coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 68: 421–430.
Boeuf, G. and Gaignon, J. L. 1989. Effects of rearing conditions on growth and thyroid hormones during smolting of Atlantic salmon, Salmo salar. Aquaculture 82: 29–38.
Boeuf, G., Le Bail, P. Y. and Prunet, P. 1989. Growth hormone and thyroid hormones during Atlantic salmon (Salmo salar L.) smolting and after transfer to seawater. Aquaculture 82: 257–268.
Boeuf, G., Uin, L. M. and Eales, J. G. 1989. Plasma levels of free and bound thyroid hormones during parr-smolt transformation in Atlantic salmon (Salmo salar L.). Can. J. Zool. 67: 1654–1658.
Browman, H. I. 1989. Embryology, ethology and ecology of ontogenetic critical periods in fish. Brain Behav. Evol. 34: 5–12.
Burman, P., Hetta, J., Wide, L., Mansson, J. E., Ekman, R. and Karlsson, F. A. 1996. Growth hormone treatment affects brain neurotransmitters and thyroxine. Clin. Endocrinol. 44: 319–324.
Böckers, T. M., Sourgens, H., Wittkowski, W., Jekat, A. and Pera, F. 1990. Changes in TSH-immunoreactivity in the pars tuberalis and pars distalis of the fetal rat hypophysis following maternal administration of propylthiouracil and thyroxine. Cell Tissue Res. 260: 403–408.
Chaudhuri, H. 1994. History of induced breeding in fishes and its application to aquaculture. Proc. Zool. Soc.: 1–31.
Cheek, L. M. 1990. Thyroid Hormone Binding to Brain Nuclear Extracts During Smoltification in Coho Salmon. Ph.D. Thesis. Institute of Marine Sciences, University of Alaska Fairbanks, Fairbanks. 154.
Childs, G. V., Taub, K., Jones, K. E. and Chin, W. W. 1991. Triiodothyronine receptor beta-2 messenger ribonucleic acid expression by somatotropes and thyrotropes effect of propylthiouracil-induced hypothyroidism in rats. Endocrinology 129: 2767–2773.
Clarke, W. C. and Shelbourn, J. E. 1986. Delayed photoperiod produces more uniform growth and greater seawater adaptability in underyearling coho salmon (Oncorhynchus kisutch). Aquaculture 56: 287–299.
Coiro, V., Braverman, L. E., Christianson, D., Fang, S. L. and Goodman, H. M. 1979. Effect of hypothyroidism and thyroxine replacement on growth hormone in the rat. Endocrinology 105: 641–646.
Davis, S. L. and Borger, M. L. 1973. The effect of thyroidectomy on the secretion of prolactin and on plasma levels of thyrotrophin, luteinizing hormone and growth hormone in lambs. Endocrinology 92: 1736–1739.
Dickhoff, W. W. and Sullivan, C. V. 1987. Involvement of the thyroid gland in smoltification, with special reference to metabolic and developmental processes. Am. Fish. Soc. Sym. 1: 197–210.
Donaldson, E. M., Fagerlund, U. H. M., Higgs, D. A. and McBride, J. R. 1979. Hormonal enhancement of growth. In Fish Physiology. Vol. 3. pp. 456–598. Edited by W. S. Hoar and D.J. Randall. Academic Press, New York.
Eales, J. G. 1985. The peripheral metabolism of thyroid hormones and regulation of thyroidal status in poikilotherms. Can. J. Zool. 63: 1217–1231.
Eales, J. G. 1987. Kinetics of T4 and T3 binding to plasma sites in salmonid teleost fish. Gen. Comp. Endocrinol. 65: 288–299.
Eales, J. G. 1995. Regulation and measurement of thyroidal status in fish. Neth. J. Zool. 45: 175–180.
Eales, J. G. and Finnson, K. R. 1991. Response of hepatic thyroxine 5'-deiodinase of rainbow trout (Oncorhynchus mykiss) to chronic ingestion of 3,5,3'-triiodo-L-thyronine. J. Exp. Zool. 257: 230–235.
Eales, J. G., Morin, P. P., Tsang, P. and Hara, T. J. 1993. Thyroid hormone deiodination in brain, liver, gill, heart, and muscle of Atlantic salmon (Salmo salar) during photoperiodically-induced parr-smolt transformation ii. outer and inner-ring 3,5,3'-triiodo-L-thyronine and 3,3,5'-triiodo-L-thyronine reverse T3 deiodination. Gen. Comp. Endocrinol. 90: 157–167.
Eales, J. G. and Shostak, S. 1985. Free L-thyroxine and 3,5,3'-triiodo-L-thyronine in relation to total hormone, free hormone indices, and protein in plasma of rainbow trout and arctic charr. Gen. Comp. Endocrinol. 58: 291–302.
Eales, J. G. and Shostak, S. 1986. Influences of temperature and pH on free L-thyroxine and free 3,5,3'-triiodo-L-thyronine in charr (Salvelinus alpinus) and trout (Salmo gairdneri) plasma. Gen. Comp. Endocrinol. 61: 272–277.
Ebbesson, L. O. E., Deviche, P. and Ebbesson, S. O. E. 1996a. Distribution and changes in mu-and kappa-opiate receptors during the midlife neurodevelopmental period of coho salmon, Oncorhynchus kisutch. J. Comp. Neurol. 366: 448–464.
Ebbesson, L. O. E., Drew, K. and Ebbesson, S. O. E. 1994. Brain development during smolt transformation in salmon may be affected by environmental conditions. Soc. Neurosci. Abstr. 20: 1301.
Ebbesson, S. O. E. 1980. The parcellation theory and its relation to interspecific variability in brain organization, evolutionary and ontogenetic development, and neuronal plasticity. Cell Tiss. Res. 213: 179–212.
Ebbesson, S. O. E., Smith, J., Co, C. and Cheek, L. M. 1989. Brain neurotransmitters increase during olfactory imprinting in coho salmon (Oncorhynchus kisutch) and are affected by exposure to propylthiouracil. Soc. Neurosci. Abstr. 15: 10–19.
Ebbesson, S. O. E., Smith, J., Co, C. and Ebbesson, L. O. E. 1996b. Transient alterations in neurotransmitter levels during a critical period of neural development in coho salmon (Oncorhynchus kisutch). Brain Res. 742: 339–342.
Frith, S. D. and Eales, J. G. 1996. Thyroid hormone deiodination pathways in brain liver of rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 101: 323–332.
Gelineau, A., Mambrini, M., Leatherland, J. F. and Boujard, T. 1996. Effect of feeding time on hepatic nucleic acid, plasma T3, T4, and GH concentrations in rainbow trout. Physiology and Behavior 59: 1061–1067.
Folmar, L. C., and Dickhoff, W. W. 1980. The parr-smolt transformation (smoltification) and sea water adaptation in salmonids: a review. Aquaculture 21: 1–38.
Glass, C. K., Franco, R., Weinberger, C., Albert, V. R., Evans, R. M. and Rosenfeld, M. G. 1987. A c-erb-A binding site in rat growth hormone gene mediates trans-activation by thyroid hormone. Nature 329: 738–741.
Gorbman, A., Dickhoff, W., Vigna, S. R., Clark, N. B. and Ralph, C. L. 1983. Comparative Endocrinology. John Wiley, New York.
Grau, E. G., Dickhoff, W. W., Nishioka, R. S., Bern, H. A. and Folmar, L. C. 1981. Lunar phasing of the thyroxine surge preparatory to seaward migration of salmonid fish. Science 221: 607–609.
Gross, M. R. 1987. Evolution of diadromy in fishes. Am. Fish. Soc. Sym. 1: 14–25.
Hoar, W. C. 1988. The physiology of smolting salmonids. Fish Physiology. Vol. XIB pp. 275–343. Edited by W. S. Hoar and D. Randall. Academic Press, New York.
Hoar, W. S. 1939. The thyroid gland of the Atlantic salmon. J. Morphol. 65: 257–295.
Holtby, L. B., Andersen, B. C. and Kadowaki, R. K. 1990. Importance of smolt size and early ocean growth to interannual variability in marine survival of coho salmon (Oncorhynchus kisutch). Can. J. Fish. Aquat. Sci. 47: 2181–2194.
Irvine, J. R. and Ward, B. R. 1989. Patterns of timing and size of wild coho salmon (Oncorhynchus kisutch) smolts migrating from the Keogh River watershed on northern Vancouver Island, Canada. Can. J. Fish. Aquat. Sci. 46: 1086–1094.
Koenig, R. J., Brent, G. A., Warne, R. L., Larsen, P. R. and Moore, D. M. 1987. Thyroid hormone receptor binds to a site in the rat growth hormone promoter required for induction by thyroid hormone. Proc. Natl. Acad. Sci. USA. 84: 5670–5674.
Lam, T. J. 1994. Hormones and egg-larval quality in fish. Aquaculture 25: 2–12.
Leung, F. C., Taylor, J. E. and Van, I.-A. 1985. Effects of dietary thyroid hormones on growth, plasma triiodothyronine, thyroxine, and growth hormone in normal and hypothyroid chickens. Gen. Comp. Endocrinol. 59: 91–99.
Lloyd, R. V., Jin, L., Song, J., Terry, L. C., Horvath, E. and Kovacs, K. 1990. Effects of propylthiouracil on growth hormone and prolactin messenger RNA in the rat pituitary. Lab. Invest. 62: 347–354.
Maclatchy, D. L. and Eales, J. D. 1992a. Intra-and extra-cellular sources of T3 binding to putative thyroid hormone receptors in liver, kidney, and gill nuclei of immature rainbow trout (Oncorhynchus mykiss). J. Exp. Zool. 262: 22–29.
Maclatchy, D. L. and Eales, J. G. 1990. Growth hormone stimulates hepatic thyroxine 5'-monodeiodinase activity and 3,5,3'-triiodothyronine levels in rainbow trout (Salmo gairdneri). Gen. Comp. Endocrinol. 78: 164–172.
Maclatchy, D. L. and Eales, J. G. 1992b. Properties of T4 5'-deiodinating systems in various tissues of the rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 86: 313–322.
Maclatchy, D. L., Kawauchi, H. and Eales, J. G. 1992. Stimulation of hepatic thyroxine 5'-deiodinase activity in rainbow trout (Oncorhynchus mykiss) by Pacific salmon growth hormone. Comp. Biochem. Physiol. A Comp. Physiol. 101: 689–691.
Martinoli, M. G. and Pelletier, G. 1989. Thyroid and glucocorticoid hormone regulation of rat pituitary growth hormone messenger RNA as revealed by in situ hybridization. Endocrinology 125: 1246–1252.
McCormick, S. D. and Björnsson, B. Th. 1994. Physiological and hormonal differences among Atlantic salmon parr and smolts reared in the wild, and hatchery smolts. Aquaculture 121: 235–244.
McCormick, S. D., Björnsson, B. Th., Sheridan, M., Eilertson, C., Carey, J. B. and O'Dea, M. 1995. Increased daylength stimulates plasma growth hormone and gill Na+, K+-ATPase in Atlantic salmon (Salmo salar). J. Comp. Physiol. B. 165: 245–254.
McCormick, S. D. and Saunders, R. L. 1990. Influence of ration level and salinity on circulating thyroid hormones in juvenile Atlantic salmon (Salmo salar). Gen. Comp. Endocrinol. 78: 224–230.
McLeese, J. M. and Eales, J. G. 1996a. 3,5,3'-Triiodo-L-thyronine and L-thyroxine uptake into red blood cells of rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 102: 47–55.
McLeese, J. M. and Eales, J. G. 1996b. Characteristics of the uptake of 3,5,3'-triiodo-L-thyronine and L-thyroxine into red blood cells of rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 103: 200–208.
Moav, B. and McKeown, B. A. 1992. Thyroid hormone increases transcription of growth hormone mRNA in rainbow trout pituitary. Horm. Metab. Res. 24: 10–14.
Morin, P. P., Hara, T. J. and Eales, J. G. 1993. Thyroid hormone deiodination in brain, liver, gill, heart, and muscle of Atlantic salmon (Salmo salar) during photoperiodically-induced parr-smolt transformation i. outer and inner-ring thyroxine deiodination. Gen. Comp. Endocrinol. 90: 142–156.
Peake, G. T., Birge, C. A. and Daughaday, W. H. 1973. Alterations of radioimmunoassayable growth hormone and prolactin during hypothyroidism. Endocrinology 92: 487–493.
Porterfield, S. P. and Hendrich, C. E. 1993. The role of thyroid hormones in prenatal and neonatal neurological development: Ccurrent perspectives. Endocr. Rev. 14: 94–106.
Powell, J. F. F. and McKeown, B. A. 1986. The influence of size on ion regulation and sea-water survival of acid-exposed coho salmon smolts (Oncorhynchus kisutch). Comp. Biochem. Physiol. C. 85: 369–374.
Shields, C. A. and Eales, J. G. 1986. Thyroxine 5'-monodeiodinase activity in hepatocytes of rainbow trout (Salmo gairdneri): distribution, effects of starvation, and exogenous inhibitors. Gen. Comp. Endocrinol. 63: 334–343.
Singh, H., Griffith, R. W., Takahashi, A., Kawauchi, H., Thomas, P. and Stegeman, J. J. 1988. Regulation of gonadal steroidogenesis in Fundulus heteroclitus by recombinant salmon growth hormone and purified salmon prolactin. Gen. Comp. Endocrinol. 72: 144–153.
Skilbrei, O. T. 1988. Growth pattern of pre-smolt Atlantic salmon (Salmo salar L.): the percentile increment method (PIM) as a new method to estimate length dependent growth. Aquaculture 69: 129–143.
Specker, J. L., Brown, C. L. and Bern, H. A. 1992. Asynchrony of changes in tissue and plasma thyroid hormones during the parrsmolt transformation of coho salmon. Gen. Comp. Endocrinol. 88: 397–405.
Stefansson, S. O., Björnsson, B. Th., Hansen, T., Haux, C., Taranger, G. L. and Saunders, R. L. 1991. Growth parr-smolt transformation and changes in growth hormone of Atlantic salmon (Salmo salar) reared under different photoperiods. Can. J. Fish. Aquat. Sci. 48: 2100–2108.
Sullivan, C. V., Darling, D. S. and Dickhoff, W. W. 1987a. Effects of triiodothyronine and propylthiouracil on thyroid function and smoltification of coho salmon (Oncorhynchus kisutch). Fish Physiol. Biochem. 4: 121–135.
Sullivan, C. V., Darling, D. S. and Dickhoff, W. W. 1987b. Nuclear receptors for L-triiodothyronine in trout erythrocytes. Gen. Comp. Endocrinol. 65: 149–160.
Sullivan, C. V., Dickhoff, W. W., Mahnken, C. V. W. and Hershberger, W. K. 1985. Changes in the hemoglobin system of the coho salmon (Oncorhynchus kisutch) during smoltification and triiodothyronine and propylthiouracil treatment. Comp. Biochem. Physiol. A. 81: 807–814.
Sweeting, R. M., Alexander, G. P., Eales, J. G. and McKeown, B. A. 1994. Hepatic and branchial thyroid hormone deiodinase activities associated with the parr-smolt transformation of coho salmon (Oncorhynchus kisutch). Gen. Comp. Endocrinol. 94: 171–181.
Sweeting, R. M. and Eales, J. G. 1992a. The acute influence of ingested thyroid hormones on hepatic deiodination pathways in the rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 85: 376–384.
Sweeting, R. M. and Eales, J. G. 1992b. Thyroxine 5'-monodeiodinase activity in microsomes from isolated hepatocytes of rainbow trout effects of growth hormone and 3,5,3'-triiodo-L-thyronine. Gen. Comp. Endocrinol. 88: 169–177.
Tam, S. P., Lam, K. S. L. and Srivastava, G. 1996. Gene expression of hypothalamic somatostatin, growth hormone releasing factor, and their pituitary receptors in hypothyroidism. Endocrinology 137: 418–424.
Thorpe, J. E. 1987. Smolting versus residency. Am. Fish. Soc. Sym. 1: 244–252.
Thorpe, J. E., Villarreal, C. and Talbot, C. 1982. Bi-modality of growth and smolting in Atlantic salmon (Salmo salar). Aquaculture 28: 123–132.
Ueta, Y., Levy, A., Chowdrey, H. S. and Lightman, S. L. 1995. Hypothalamic nitric oxide synthase gene expression is regulated by thyroid hormones. Endocrinology. 136: 4182–4187.
Wright, M. L., Pikula, A., Cykowski, L. J. and Kuliga, K. 1996. Effect of melatonin on the anuran thyroid gland: Follicle cell proliferation, morphometry, and subsequent thyroid hormone secretion in vitro after melatonin treatment in vivo. Gen. Comp. Endocrinol. 103: 182–191.
Young, G., Björnsson, B. Th., Prunet, P., Lin, R. J. and Bern, H. A. 1989. Plasma levels of prolactin and growth hormone during parr-smolt transformation of coho salmon, Oncorhynchus kisutch: plasma prolactin, growth hormone, thyroid hormones and cortisol. Aquaculture 82: 382–383.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ebbesson, L., Björnsson, B.T., Stefansson, S. et al. Propylthiouracil-induced hypothyroidism in coho salmon, Oncorhynchus kisutch: effects on plasma total thyroxine, total triiodothyronine, free thyroxine, and growth hormone. Fish Physiology and Biochemistry 19, 305–314 (1998). https://doi.org/10.1023/A:1007775516113
Issue Date:
DOI: https://doi.org/10.1023/A:1007775516113