Advertisement

Fisheries Science

, Volume 77, Issue 3, pp 301–311 | Cite as

Expression patterns of type II and III iodothyronine deiodinase genes in the liver of the goldlined spinefoot, Siganus guttatus

  • Nina Wambiji
  • Yong-Ju Park
  • Ji-Gweon Park
  • Se-Jae Kim
  • Sung-Pyo Hur
  • Yuki Takeuchi
  • Akihiro Takemura
Original Article Biology

Abstract

Iodothyronine deiodinases play an important role in thyroid hormone regulation in vertebrates. The aim of this study was to clone type II (SgD2) and type III (SgD3) iodothyronine deiodinase cDNA from the goldlined spinefoot (Siganus guttatus) using 3′- and 5′-rapid amplification of cDNA ends and then to assess their expression patterns in the liver under several experimental conditions by using quantitative real-time PCR. SgD2 (1013 bp) and SgD3 (1492 bp) contained open reading frames of 810 and 804 bp and encoded 270 and 269 amino acids, respectively. They were characterized by an in-frame TGA codon that was considered to be selenocysteine. An abundance of SgD2 and SgD3 mRNA was expressed in several tissues, with an increase at 1200 hours and a decrease at 2400 hours. Food deprivation suppressed the expression of SgD2, but not SgD3. Higher SgD2 and SgD3 mRNA levels in the liver were found in fish reared at 25°C than in those reared at 20 and 30°C. These results suggest that exogenous factors influence the mRNA levels of iodothyronine deiodinase genes in the liver and that transcription of the genes in certain tissues is partially regulated in a circadian manner.

Keywords

Cloning Day–night variations Food availability Rabbitfish Quantitative real-time PCR Temperature 

Notes

Acknowledgments

This study was supported in part by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (JSPS) and a Joint Research Project under the Japan–Korea Basic Scientific Cooperation Program from JSPS to AT.

References

  1. 1.
    Leatherland JF (1982) Environmental physiology of the teleostean thyroid gland: a review. Environ Biol Fish 7:83–110CrossRefGoogle Scholar
  2. 2.
    Eales JG, Brown SB (1993) Measurement and regulation of thyroidal status in teleost fish. Rev Fish Biol Fish 3:299–347CrossRefGoogle Scholar
  3. 3.
    Sanders JP, Van der Geyten S, Kaptein E, Darras VM, Kühn ER, Leonard JL, Visser TJ (1997) Characterization of a propylthiouracil-insensitive type I iodothyronine deiodinase. Endocrinology 138:5153–5160PubMedCrossRefGoogle Scholar
  4. 4.
    St Germain DL, Galton VA (1997) The deiodinase family of selenoproteins. Thyroid 7:655–668PubMedCrossRefGoogle Scholar
  5. 5.
    Mol KA, Van der Geyten S, Burel C, Kühn ER, Boujard T, Darras VM (1998) Comparative study of iodothyronine outer ring and inner ring deiodinase activities in five teleostean fishes. Fish Physiol Biochem 18:253–266CrossRefGoogle Scholar
  6. 6.
    García-G C, Jeziorski MC, Valverde-R C, Orozco A (2004) Effects of iodothyronines on the hepatic outer-ring deiodinating pathway in killifish. Gen Comp Endocrinol 135:201–209PubMedCrossRefGoogle Scholar
  7. 7.
    Bianco AC, Salvatore D, Gereben B, Berry MJ, Larsen PR (2002) Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr Rev 23:38–89PubMedCrossRefGoogle Scholar
  8. 8.
    Salvatore D, Low SC, Berry MJ, Maia AL, Harney JW, Croteau W, St. Germain D, Larsen PR (1995) Type 3 iodothyronine deiodinase: cloning, in vitro expression, and functional analysis of the placental selenoenzyme. J Clin Invest 96:2421–2430PubMedCrossRefGoogle Scholar
  9. 9.
    Van der Geyten S, Van den Eynde I, Segers IB, Kühn ER, Darras VM (2002) Differential expression of iodothyronine deiodinases in chicken tissues during the last week of embryonic development. Gen Comp Endocrinol 128:65–73PubMedCrossRefGoogle Scholar
  10. 10.
    MacLatchy DL, Eales JG (1992) Properties of T4 5′-deiodinating systems in various tissues of the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 86:313–322PubMedCrossRefGoogle Scholar
  11. 11.
    Mol K, Kaptein E, Darras VM, de Greef WJ, Kühn ER, Visser TJ (1993) Different thyroid hormone-deiodinating enzymes in tilapia (Oreochromis niloticus) liver and kidney. FEBS Lett 321:140–144PubMedCrossRefGoogle Scholar
  12. 12.
    Frith SD, Eales JG (1996) Thyroid hormone deiodination pathways in brain and liver of rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 101:323–332PubMedCrossRefGoogle Scholar
  13. 13.
    Moore VanPutte CL, MacKenzie DS, Eales JG (2001) Characterization of hepatic low-Km outer-ring deiodination in red drum (Sciaenops ocellatus). Comp Biochem Physiol B 128:413–423CrossRefGoogle Scholar
  14. 14.
    Cyr DG, Idler DR, Audet C, McLeese JM, Eales JG (1998) Effects of long-term temperature acclimation on thyroid hormone deiodinase function, plasma thyroid hormone levels, growth, and reproductive status of male Atlantic cod, Gadus morhua. Gen Comp Endocrinol 109:24–36PubMedCrossRefGoogle Scholar
  15. 15.
    Orozco A, Linser P, Valverde-R C (2000) Kinetic characterization of outer-ring deiodinase activity (ORD) in the liver, gill and retina of the killifish Fundulus heteroclitus. Comp Biochem Physiol B 126:283–290PubMedCrossRefGoogle Scholar
  16. 16.
    Morin PP, Hara TJ, Eales JG (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 90:142–156PubMedCrossRefGoogle Scholar
  17. 17.
    Johnston CE, Eales JG (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 272:426–434CrossRefGoogle Scholar
  18. 18.
    Specker JL, Eales JG, Tagawa M, Tyler WA III (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 78:696–705CrossRefGoogle Scholar
  19. 19.
    Plohman JC, Dick TA, Eales JG (2002) Thyroid of lake sturgeon, Acipenser fulvescens II. Deiodination properties, distribution, and effects of diet, growth, and a T3 challenge. Gen Comp Endocrinol 125:56–66PubMedCrossRefGoogle Scholar
  20. 20.
    Picard-Aitken M, Fournier H, Pariseau R, Marcogliese DJ, Cyr DG (2007) Thyroid disruption in walleye (Sander vitreus) exposed to environmental contaminants: cloning and use of iodothyronine deiodinases as molecular biomarkers. Aquat Toxicol 83:200–211PubMedCrossRefGoogle Scholar
  21. 21.
    Adams BA, Cyr DG, Eales JG (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 127:367–378Google Scholar
  22. 22.
    Sanders JP, Van der Geyten S, Kaptein E, Darras VM, Kühn ER, Leonard JL, Visser TJ (1999) Cloning and characterization of type III iodothyronine deiodinase from the fish Oreochromis niloticus. Endocrinology 140:3666–3673PubMedCrossRefGoogle Scholar
  23. 23.
    Finnson KR, Eales JG (1999) Effect of T3 treatment and food ration on hepatic deiodination and conjugation of thyroid hormones in rainbow trout Oncorhynchus mykiss. Gen Comp Endocrinol 115:379–386PubMedCrossRefGoogle Scholar
  24. 24.
    Mol KA, Van der Geyten S, Kühn ER, Darras VM (1999) Effects of experimental hypo- and hyperthyroidism on iodothyronine deiodinases in Nile tilapia, Oreochromis niloticus. Fish Physiol Biochem 20:201–207CrossRefGoogle Scholar
  25. 25.
    Van der Geyten S, Byamungu N, Reyns GE, Kühn ER, Darras VM (2005) Iodothyronine deiodinases and the control of plasma and tissue thyroid hormone levels in hyperthyroid tilapia (Oreochromis niloticus). J Endocrinol 184:467–479PubMedCrossRefGoogle Scholar
  26. 26.
    Plate EM, Adams BA, Allison WT, Martens G, Hawryshyn CW, Eales JG (2002) The effects on thyroxine or a GnRH analogue on thyroid hormone deiodination in the olfactory epithelium and retina of rainbow trout, Oncorhynchus mykiss, and sockeye salmon, Oncorhynchus mykiss nerka. Gen Comp Endocrinol 127:59–65PubMedCrossRefGoogle Scholar
  27. 27.
    Van der Geyten S, Mol KA, Pluymers W, Kühn ER, Darras VM (1998) Changes in plasma T3 during fasting/refeeding in tilapia (Oreochromis niloticus) are mainly regulated through changes in hepatic type II iodothyronine deiodinase. Fish Physiol Biochem 19:135–143CrossRefGoogle Scholar
  28. 28.
    Walpita CN, Grommen SVH, Darras VM, Van der Geyten S (2007) The influence of stress on thyroid hormone production and peripheral deiodination in the Nile tilapia Oreochromis niloticus. Gen Comp Endocrinol 150:18–25PubMedCrossRefGoogle Scholar
  29. 29.
    Cyr DG, Eales JG (1988) In vitro effects of thyroid hormones on gonadotropin-induced estradiol-17β secretion by ovarian follicles of rainbow trout, Salmo gairdneri. Gen Comp Endocrinol 69:80–87PubMedCrossRefGoogle Scholar
  30. 30.
    MacLatchy DL, Eales JG (1988) Short-term treatment with testosterone increases plasma 3, 5, 3′-triiodo-l-thyronine and hepatic l-thyroxine 5′-monodeiodinase levels in arctic charr, Salvelinus fontinalis. Gen Comp Endocrinol 71:10–16PubMedCrossRefGoogle Scholar
  31. 31.
    MacLatchy DL, Eales JG (1990) Growth hormone stimulates hepatic thyroxine 5′-monodeiodinase activity and 3, 5, 3′-triiodothyronine levels in rainbow trout (Salmo gairdneri). Gen Comp Endocrinol 78:164–172PubMedCrossRefGoogle Scholar
  32. 32.
    Sambroni E, Gutieres S, Cauty C, Guiguen Y, Breton B, Lareyre JJ (2001) Type II iodothyronine deiodinase is preferentially expressed in rainbow trout (Oncorhynchus mykiss) liver and gonads. Mol Reprod Dev 60:338–350PubMedCrossRefGoogle Scholar
  33. 33.
    Park YJ, Park JG, Hiyakawa N, Lee YD, Kim SJ, Takemura A (2007) Diurnal and circadian regulation of a melatonin receptor, MT1, in the golden rabbitfish, Siganus guttatus. Gen Comp Endocrinol 150:253–262PubMedCrossRefGoogle Scholar
  34. 34.
    Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔC T method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  35. 35.
    Berry MJ, Banu L, Larsen PR (1991) Type I iodothyronine deiodinase is a selenocysteine-containing enzyme. Nature 349:438–440PubMedCrossRefGoogle Scholar
  36. 36.
    Celi FS, Canettieri G, Yarnall DP, Burns DK, Andreoli M, Schuldiner AR, Centanni M (1998) Genomic characterization of the coding region of the human type II 5′ deiodinase gene. Mol Cell Endocrinol 141:49–52PubMedCrossRefGoogle Scholar
  37. 37.
    Isorna E, Obregon MJ, Calvo RM, Vázquez R, Pendón C, Falcón J, Muñoz-Cueto JA (2009) Iodothyronine deiodinases and thyroid hormone receptors regulation during flatfish (Solea senegalensis) metamorphosis. J Exp Zool (Mol Dev Evol) 312B:231–246CrossRefGoogle Scholar
  38. 38.
    Valverde-R C, Croteau W, LaFleur Jr GJ, Orozco A, St. Germain DL (1997) Cloning and expression of a 5′-iodothyronine deiodinase from the liver of Fundulus heteroclitus. Endocrinology 138:642–648CrossRefGoogle Scholar
  39. 39.
    Davey JC, Schneider MJ, Becker KB, Galton VA (1999) Cloning of a 5.8 kb cDNA for a type 2 deiodinase. Endocrinology 140:1022–1025PubMedCrossRefGoogle Scholar
  40. 40.
    Orozco A, Jeziorski MC, Linser PJ, Greenberg RM, Valverde-R C (2002) Cloning of the gene and complete cDNA encoding a type 2 deiodinase in Fundulus heteroclitus. Gen Comp Endocrinol 128:162–167PubMedCrossRefGoogle Scholar
  41. 41.
    Wagner MS, Morimoto R, Dora JM, Benneman A, Pavan R, Maia AL (2003) Hypothyroidism induces type 2 iodothyronine deiodinase expression in mouse heart and testis. J Mol Endocrinol 31:541–550PubMedCrossRefGoogle Scholar
  42. 42.
    Mol KA, Van der Geyten S, Darras VM, Visser TJ, Kühn ER (1997) Characterization of iodothyronine outer ring and inner ring deiodinase activities in the blue tilapia, Oreochromis aureus. Endocrinology 138:1787–1793PubMedCrossRefGoogle Scholar
  43. 43.
    Eales JG, MacLatchy DL, Sweeting RM (1993) Thyroid hormone deiodinase systems in salmonids, and their involvement in the regulation of thyroidal status. Fish Physiol Biochem 11:313–321CrossRefGoogle Scholar
  44. 44.
    Leiner KA, Han GS, MacKenzie DS (2000) The effects of photoperiod and feeding on the diurnal rhythm of circulating thyroid hormones in the red drum, Sciaenops ocellatus. Gen Comp Endocrinol 120:88–98PubMedCrossRefGoogle Scholar
  45. 45.
    Chopra IJ (1980) Alterations in monodeiodination of iodothyronines in the fasting rat: effects of reduced nonprotein sulfhydryl groups and hypothyroidism. Metabolism 29:161–167PubMedCrossRefGoogle Scholar
  46. 46.
    Chopra IJ, Wiersinga W, Frank H (1981) Alterations in hepatic monodeiodination of iodothyronines in the diabetic rat. Life Sci 28:1765–1776PubMedCrossRefGoogle Scholar
  47. 47.
    O’Mara BA, Dittrich W, Lauterio TJ, St Germain DL (1993) Pretranslational regulation of type I 5′-deiodinase by thyroid hormones and in fasted and diabetic rats. Endocrinology 133:1715–1723PubMedCrossRefGoogle Scholar
  48. 48.
    Darras VM, Mol KA, Van der Geyten S, Kühn ER (1998) Control of peripheral thyroid hormone levels by activating and inactivating deiodinases. Ann NY Acad Sci 839:80–86PubMedCrossRefGoogle Scholar
  49. 49.
    Gomez JM, Boujard T, Boeuf G, Solari A, Le Bail PY (1997) Individual diurnal plasma profiles of thyroid hormones in rainbow trout (Oncorhynchus mykiss) in relation to cortisol, growth hormone, and growth rate. Gen Comp Endocrinol 107:74–83PubMedCrossRefGoogle Scholar
  50. 50.
    Leiner KA, MacKenzie DS (2003) Central regulation of thyroidal status in a teleost fish: nutrient stimulation of T4 secretion and negative feedback of T3. J Exp Zool 298A:32–43CrossRefGoogle Scholar
  51. 51.
    Ebbesson LOE, Björnsson BT, Ekström P, Stefansson SO (2008) Daily endocrine profiles in parr and smolt Atlantic salmon. Comp Biochem Physiol A 151:698–704CrossRefGoogle Scholar
  52. 52.
    Spieler RE, Noeske TA (1981) Timing of a single daily meal and diel variations of serum thyroxine, triiodothyronine and cortisol in goldfish Carassius auratus. Life Sci 28:2939–2944PubMedCrossRefGoogle Scholar
  53. 53.
    Loter TC, MacKenzie DS, McLeese J, Eales JG (2007) Seasonal changes in channel catfish thyroid hormones reflect increased magnitude of daily thyroid hormone cycles. Aquaculture 262:451–460CrossRefGoogle Scholar
  54. 54.
    Leiner KA, MacKenzie DS (2001) The effects of photoperiod on growth rate and circulating thyroid hormone levels in the red drum, Sciaenops ocellatus: evidence for a free-running circadian rhythm of T4 secretion. Comp Biochem Physiol A 130:141–149CrossRefGoogle Scholar
  55. 55.
    Shoemaker CA, Klesius PH, Lim C, Yildirim M (2003) Feed deprivation of channel catfish, Ictalurus punctatus (Rafinesque), influences organosomatic indices, chemical composition and susceptibility to Flavobacterium columnare. J Fish Dis 26:553–561PubMedCrossRefGoogle Scholar
  56. 56.
    Toguyeni A, Baroiller JF, Fostier A, Le Bail PY, Kühn ER, Mol KA, Fauconneau B (1996) Consequences of food restriction on short-term growth variation and on plasma circulating hormones in Oreochromis niloticus in relation to sex. Gen Comp Endocrinol 103:167–175PubMedCrossRefGoogle Scholar
  57. 57.
    Flood CG, Eales JG (1983) Effects of starvation and refeeding on plasma T4 and T3 levels and T4 deiodination in rainbow trout, Salmo gairdneri. Can J Zool 61:1949–1953CrossRefGoogle Scholar
  58. 58.
    Saoud IP, Mohanna C, Ghanawi J (2008) Effects of temperature on survival and growth of juvenile spinefoot rabbitfish (Siganus rivulatus). Aquac Res 39:491–497CrossRefGoogle Scholar
  59. 59.
    Bapary MAJ, Fainuulelei P, Takemura A (2009) Environmental control of gonadal development in the tropical damselfish Chrysiptera cyanea. Mar Biol Res 5:462–469CrossRefGoogle Scholar
  60. 60.
    Bapary MAJ, Takemura A (2010) Effect of temperature and photoperiod on the reproductive condition and performance of a tropical damselfish Chrysiptera cyanea during different phases of reproductive season. Fish Sci 76:769–776CrossRefGoogle Scholar

Copyright information

© The Japanese Society of Fisheries Science 2011

Authors and Affiliations

  • Nina Wambiji
    • 1
  • Yong-Ju Park
    • 3
  • Ji-Gweon Park
    • 2
  • Se-Jae Kim
    • 2
  • Sung-Pyo Hur
    • 1
  • Yuki Takeuchi
    • 1
  • Akihiro Takemura
    • 1
  1. 1.Department of Chemistry, Biology and Marine Sciences, Faculty of ScienceUniversity of the RyukyusNishiharaJapan
  2. 2.Department of BiologyJeju National UniversityJeju CityRepublic of Korea
  3. 3.Marine and Environmental Research InstituteJeju National UniversityJocheonRepublic of Korea

Personalised recommendations