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Propylthiouracil-induced hypothyroidism in coho salmon, Oncorhynchus kisutch: effects on plasma total thyroxine, total triiodothyronine, free thyroxine, and growth hormone

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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.

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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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Bernal, J. and Nuñez, J. 1995. Thyroid hormones and brain development. Eur. J. Endocrinol. 133: 390–398.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Browman, H. I. 1989. Embryology, ethology and ecology of ontogenetic critical periods in fish. Brain Behav. Evol. 34: 5–12.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Eales, J. G. 1985. The peripheral metabolism of thyroid hormones and regulation of thyroidal status in poikilotherms. Can. J. Zool. 63: 1217–1231.

    Google Scholar 

  • Eales, J. G. 1987. Kinetics of T4 and T3 binding to plasma sites in salmonid teleost fish. Gen. Comp. Endocrinol. 65: 288–299.

    Google Scholar 

  • Eales, J. G. 1995. Regulation and measurement of thyroidal status in fish. Neth. J. Zool. 45: 175–180.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Gorbman, A., Dickhoff, W., Vigna, S. R., Clark, N. B. and Ralph, C. L. 1983. Comparative Endocrinology. John Wiley, New York.

    Google Scholar 

  • 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.

    Google Scholar 

  • Gross, M. R. 1987. Evolution of diadromy in fishes. Am. Fish. Soc. Sym. 1: 14–25.

    Google Scholar 

  • 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.

    Google Scholar 

  • Hoar, W. S. 1939. The thyroid gland of the Atlantic salmon. J. Morphol. 65: 257–295.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Lam, T. J. 1994. Hormones and egg-larval quality in fish. Aquaculture 25: 2–12.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Peake, G. T., Birge, C. A. and Daughaday, W. H. 1973. Alterations of radioimmunoassayable growth hormone and prolactin during hypothyroidism. Endocrinology 92: 487–493.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Thorpe, J. E. 1987. Smolting versus residency. Am. Fish. Soc. Sym. 1: 244–252.

    Google Scholar 

  • Thorpe, J. E., Villarreal, C. and Talbot, C. 1982. Bi-modality of growth and smolting in Atlantic salmon (Salmo salar). Aquaculture 28: 123–132.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

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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

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