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Comparative study of iodothyronine outer ring and inner ring deiodinase activities in five teleostean fishes

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Abstract

The presence of outer ring deiodinating (ORD) and inner ring deiodinating (IRD) activities was investigated in different tissues of Oreochromis niloticus (Nile tilapia), Clarias gariepinus (African catfish), Oncorhynchus mykiss (rainbow trout) and halmus maximus (turbot). High-Km rT3 ORD is present in the kidney of most of the fishes studied, except in catfish. In turbot, besides the kidney, rT3 ORD is also present in liver, heart and ovary. Low-Km T4 ORD is found in the liver and low-Km T3 IR the brain of all the fishes studied. In addition, low levels of low-Km T3 IRD were demonstrated in gill and skin of Nile tilapia, liver of rainbow trout and gill and kidney of turbot. For the different teleosts, the biochemical properties of the different rT3-deiodinating enzymes mentioned, T4 ORD in liver and T3 IRD in brain and tilapia gill were compared to those of the deiodinases formerly characterized in Oreochromis aureus (blue tilapia). In general, the different deiodinases demonstrate analogous sensitivities to iodothyronines and inhibitors, although minor differences occur. The various deiodinating enzymes all depend on addition of dithiothreitol and demonstrate maximal activity pH between 6.5 and 7. The optimal incubation temperature of rT3 ORD and T4 ORD in tilapia and catfish is 37 °C, in trout and turbot it varies, depending on the tissue, between 25 ° and 37 °C. For the different T3 IRD activities the optimal temperature is 37 °C in warmwater as well as in coldwater species. The apparent Km values for rT3 ORD lay in the μM range, for T4 ORD and T3 IRD they lay in the nM range. Vmax values are usually higher in tilapia as compared to the other teleosts studied. Based on the similarities in susceptibility to inhibition by different iodothyronines and inhibitors and the agreement of the apparent Km values, we conclude that the deiodinating enzymes in teleosts are more similar to mammalian deiodinases than is generally accepted.

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References cited

  • Berry, M.J., Banu, L. and Larsen, P.R. 1991. Type I iodothyronine deiodinase is a selenocysteine-containing enzyme. Nature, Lond. 349: 438-440.

    Google Scholar 

  • Croteau, W., Whitemore, S.L., Schneider, M.J. and St. Germain, D.L. 1995. Cloning and expression of a cDNA for a mammalian type III iodothyronine deiodinase. J. Biol. Chem. 270: 16569-16575.

    PubMed  Google Scholar 

  • Croteau, W., Davey, J.C., Galton, V.A. and St. Germain, D.L. 1996. Cloning of the mammalian type II iodothyronine deiodinase: a selenoprotein differentially expressed and regulated in human and rat brain and other tissues. J. Clin. Invest. 98: 405-417.

    PubMed  Google Scholar 

  • Darras, V.M., Mol, K. and Kühn, E.R. 1994. Presence of highand low-Km iodothyronine deiodinases in different vertebrate classes. Abstracts 17 Conf. Eur. Comp. Endocrinol., Cordoba, Spain.

    Google Scholar 

  • Davey, J.C., Becker, K.B., Schneider, M.J., St. Germain, D.L. and Galton, V.A. 1995. Cloning of a cDNA for type II iodothyronine deiodinase. J. Biol. Chem. 270: 26786-26789.

    PubMed  Google Scholar 

  • Eales, J.G. and Brown, S.B. 1993. Measurement and regulation of thyroidal status in teleost fish. Rev. Fish. Fish Biol. 3: 299-347.

    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.

    PubMed  Google Scholar 

  • Eelkman Rooda, S.J., Otten, M.H., van Loon, M.A.C., Kaptein, E. and Visser, T.J. 1989. Metabolism of triiodothyronine in rat hepatocytes. Endocrinology 125: 2187-2197.

    PubMed  Google Scholar 

  • Erickson, V.J., Cavalieri, R.R. and Rosenberg, L.L. 1981. Phenolic and non-phenolic ring iodothyronine deiodinases from rat thyroid gland. Endocrinology 108: 1257-1264.

    PubMed  Google Scholar 

  • Fay, M., Roti, E., Fang, S.L., Wright, G., Braverman, L.E. and Emerson, C.H. 1984. The effects of propylthiouracil, iodothyronines and other agents on thyroid hormone metabolism in human placenta. J. Clin. Endocrin. Metab. 58: 280-285.

    Google Scholar 

  • Frith, S.D. and Eales, J.G. 1996. Thyroid hormone deiodination pathways in brain and liver of rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 101: 323-332.

    PubMed  Google Scholar 

  • Galton, V.A. and Hiebert, A. 1988. The ontogeny of iodothyronine 5'-monodeiodinase activity in Rana catesbeiana tadpoles. Endocrinology 122: 640-645.

    PubMed  Google Scholar 

  • Green, W.L. 1978. Metabolism of thyroid hormones by rat thyroid tissue in vitro. Endocrinology 103: 826-837.

    PubMed  Google Scholar 

  • Johnston, C.E. and Eales, J.G. 1995. Effects of acclimation and assay temperature on outer-and inner-ring thyroxine and 3,5,3'-triiodo-L-thyronine deiodination by liver microsomes of rainbow trout, Oncorhynchus mykiss. J. Exp. Zool. 272, 426-434.

    Google Scholar 

  • Laurberg, P. and Boye, N. 1982. Outer and inner ring monodeiodination of thyroxine by dog thyroid and liver: a comparative study using a particulate cell fraction. Endocrinology 110: 2124-2130.

    PubMed  Google Scholar 

  • Leatherland, J.F. 1981. Conversion of L-thyroxine to triiodo-L-thyronine in rainbow trout (Salmo gairdneri) liver and kidney homogenates. Comp. Biochem. Physiol. 69B: 311-314.

    Google Scholar 

  • 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 thirty-three species. Fish Physiol. Biochem. 8: 1-10.

    Google Scholar 

  • Leonard, J.L. 1990. Identification and structure analysis of iodothyronine deiodinases. In The Thyroid Gland. pp. 285-305. Edited by. Monte A. Greer. Raven Press Ltd., New York.

    Google Scholar 

  • Leonard, J.L. and Visser, T.J. 1986. Biochemistry of deiodination. In Thyroid Hormone Metabolism. pp. 189-229. Edited by G. Henneman. Marcel Dekker Inc., New York.

    Google Scholar 

  • MacLatchy, D.L. and Eales, J.G. 1992. Properties of T4 5'-deiodinating enzymes in various tissues of the rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 86: 313-322.

    PubMed  Google Scholar 

  • MacLatchy, D.L. and Eales, J.G 1993. Effect of T3 and T4 challenge on inner-and outer-ring deiodination of T3 and T4 in the liver, kidney and gill of rainbow trout, Oncorhynchus mykiss. J. Exp. Zool. 265: 637-645.

    Google Scholar 

  • Mol, K.A., Van der Geyten, S., Darras, V.M., Visser, T.J. and Kühn, E.R. 1997. Characterization of outer ring and inner ring deiodinating enzymes in the blue tilapia, Oreochromis aureus. Endocrinology 138: 1787-1793.

    PubMed  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 parrsmolt transformation. I. Outer-and inner-ring thyroxine deiodination. Gen. Comp. Endocrinol. 90: 142-156.

    PubMed  Google Scholar 

  • Morin, P.-P., Hara, T.J. and Eales, J.G. 1995. T4 depresses olfactory responses to L-alanine and plasma T3 and T3 production in smoltifying Atlantic salmon. Am. J. Physiol. 269, R1434-R1440.

    PubMed  Google Scholar 

  • 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 type I and II 5'-deiodinases. Endocrinology 138: 254-258.

    PubMed  Google Scholar 

  • Rieman, J.D. and McNabb, F.M.A. 1991. Assay validation and characterization of hepatic 5'-deiodinase activity in ring doves using reverse-T3 as substrate. Gen. Comp. Endocrinol. 82: 53-59.

    PubMed  Google Scholar 

  • Rudas, P. 1986. Comparison of type I 5'-deiodination of thyroxine and of reverse triiodothyronine in rat and chicken liver homogenates. Gen. Comp. Endocrinol. 63: 400-407.

    PubMed  Google Scholar 

  • Salvatore, D., Low, S.C., Berry, M.J., Maia, A.L., Harney, J.W., Croteau, W., St. Germain, D.L. and Larsen, P.R. 1995. Type 3 deiodinase: cloning, in vitro expression and functional analysis of the placental selenoenzyme. J. Clin. Invest. 96: 2421-2430.

    PubMed  Google Scholar 

  • Salvatore, D., Bartha, T., Harney, J.W. and Larsen, P.R. 1996. Molecular biological and biochemical characterization of the human type 2 selenodeiodinase. Endocrinology 137: 3308-3315.

    PubMed  Google Scholar 

  • Schoenmakers, C.H.H., Pigmans, I.G.A.J. and Visser, T.J. 1992. Species differences in liver type I iodothyronine deiodinase. Biochim. Biophys. Acta 1121: 160-166.

    PubMed  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.

    PubMed  Google Scholar 

  • Toyoda, N., Harney, J.W., Berry, M.J. and Larsen, P.R. 1994. Identification of critical amino acids for 3,5,3'-triiodothyronine deiodination by human type I deiodinase based on comparative functional structural analyses of the human, dog and rat enzymes. J. Biol. Chem. 269: 20329-20334.

    PubMed  Google Scholar 

  • Toyoda, N., Kaptein, E., Berry, M.J., Harney, J.W., Larsen, P.R. and Visser, T.J. 1997. Structure-activity relationships for thyroid hormone deiodination by mammalian type I iodothyronine deiodinases. Endocrinology 138: 213-219.

    PubMed  Google Scholar 

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Authors
  1. K.A. Mol
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  2. S. Van der Geyten
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  3. C. Burel
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  4. E.R. Kühn
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  5. T. Boujard
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  6. V.M. Darras
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Mol, K., Van der Geyten, S., Burel, C. et al. Comparative study of iodothyronine outer ring and inner ring deiodinase activities in five teleostean fishes. Fish Physiology and Biochemistry 18, 253–266 (1998). https://doi.org/10.1023/A:1007722812697

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  • DOI: https://doi.org/10.1023/A:1007722812697

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