Tissue-specific thyroid hormone regulation of gene transcripts encoding iodothyronine deiodinases and thyroid hormone receptors in striped parrotfish (Scarus iseri)

General and Comparative Endocrinology

Volumn 172, Issue 3, 2011, Pages 505-517

  Johnson, Kaitlin M ^a   Lema, Sean C ^a  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

Brain; Deiodinase; Enzyme; Fish; Gene expression; Gonad; Liver; MRNA; Receptor; Thyroid hormones

Indexed keywords

LIOTHYRONINE; MESSENGER RNA; THIAMAZOLE; THYROID HORMONE RECEPTOR; THYROID HORMONE RECEPTOR ALPHA A; THYROID HORMONE RECEPTOR ALPHA B; THYROID HORMONE RECEPTOR BETA; THYROXINE; THYROXINE DEIODINASE; THYROXINE DEIODINASE DIO1; THYROXINE DEIODINASE DIO2; THYROXINE DEIODINASE DIO3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DEIODINATION; FISH; GENE CONTROL; GENE EXPRESSION; LIOTHYRONINE BLOOD LEVEL; LIVER; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY; PRIORITY JOURNAL; SCARUS ISERI; TESTIS; THYROXINE BLOOD LEVEL; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION;

EID: 79957826692     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.04.022     Document Type: Article

References (81)

1. Amma L.L., Campos-Barros A., Wang Z., Vennström B., Forrest D. Distinct tissue-specific roles for thyroid hormone receptors β and α1 in regulation of type 1 deiodinase expression. Mol. Endocrinol. 2001, 15:467-475.
2. An K.W., An M.I., Nelson E.R., Habibi H.R., Choi C.Y. Gender-related expression of TRα and TRβ in the protandrous black porgy, Acanthopagrus schlegeli, during sex change processes. Gen. Comp. Endocrinol. 2010, 165:11-18.
3. Bates J.M., St.Germain D.L., Galton V.A. Expression profiles of the three iodothyronine deiodinases, D1, D2, and D3, in the developing rat. Endocrinology 1999, 140:844-851.
4. Bianco A.C., Salvatore D., Gereben B., Berry M.J., Larsen P.R. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr. Rev. 2002, 23:38-89.
5. Bres O., Plohman J.C., Eales J.G. A cDNA for a putative type III deiodinase in the trout (Oncorhynchus mykiss): influence of holding conditions and thyroid hormone treatment on its hepatic expression. Gen. Comp. Endocrinol. 2006, 145:92-100.
6. Brown S.B., Adams B.A., Cyr D.G., Eales J.G. Contaminant effects on the teleost fish thyroid. Environ. Toxicol. Chem. 2004, 23:1680-1701.
7. Burmeister L.A., Pachucki J., St.Germain D.L. Thyroid hormones inhibit type 2 iodothyronine deiodinase in the rat cerebral cortex by both pre- and posttranslational mechanisms. Endocrinology 1997, 138:5231-5237.
8. Campinho M.A., Galay-Burgos M., Sweeney G.E., Power D.M. Coordination of deiodinase and thyroid hormone receptor expression during the larval to juvenile transition in sea bream (Sparus aurata, Linnaeus). Gen. Comp. Endocrinol. 2010, 165:181-194.
9. Cardwell J.R., Liley N.R. Hormonal control of sex and color change in the stoplight parrotfish, Sparisoma viride. Gen. Comp. Endocrinol. 1991, 81:7-20.
10. Constantinou C., Margarity M., Valcana T. Region-specific effects of hypothyroidism on the relative expression of thyroid hormone receptors in adult rat brain. Mol. Cell. Biochem. 2005, 278:93-100.
11. Cyr D.G., Eales J.G. Interrelationships between thyroidal and reproductive endocrine systems in fish. Rev. Fish Biol. Fish. 1996, 6:165-200.
12. Dickhoff W.W., Folmar L.A., Gorbman A. Changes in plasma thyroxine during smoltification of coho salmon. Gen. Comp. Endocrinol. 1978, 36:229-232.
13. Edeline E., Bardonnet A., Bolliet V., Dufour S., Pierre E. Endocrine control of Anguilla Anguilla glass eel dispersal: effect of thyroid hormones on locomotor activity and rheotactic behavior. Horm. Behav. 2005, 48:53-63.
14. Fines G.A., Plohman J., Eales J.G. Effect of experimental 3,5,3'-triiodothyronine hyperthyroidism on thyroid hormone deiodination in brain regions and liver of rainbow trout, Oncorhynchus mykiss. Can. J. Zool. 1999, 77:1185-1191.
15. Finnson K.W., Eales J.G. Effect of T3 treatment and food ration on hepatic deiodination and conjugation of thyroid hormones in rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 1999, 115:379-386.
16. Firth S.D., Eales J.G. Thyroid hormone deiodination pathways in brain and liver of rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 1996, 101:323-332.
17. García-G C., Jeziorski M.C., Valverde-R C., Orozco A. Effects of iodothyronines on the hepatic outer-ring deiodinating pathway in killifish. Gen. Comp. Endocrinol. 2004, 135:201-209.
18. Glatt C.M., Ouyang M., Welsh W., Green J.W., Connor J.O., Frame S.R., Everds N.E., Poindexter G., Snajdr S., Delker D.A. Molecular characterization of thyroid toxicity: anchoring gene expression profiles to biochemical and pathological end points. Environ. Health Perspect. 2005, 113:1354-1361.
19. Grau E.G., Helms L.M.H., Shimoda S.K., Ford C.-A., LeGrand J., Yamauchi K. The thyroid gland of the Hawaiian parrotfish and its use as an in vitro model system. Gen. Comp. Endocrinol. 1986, 61:100-108.
20. Hodin R.A., Lazar M.A., Chin W.W. Differential and tissue-specific regulation of the multiple rat c-erbA messenger RNA species by thyroid hormone. J. Clin. Invest. 1990, 85:101-105.
21. Isorna E., Vallés R., Servili A., Falcón J., Muñoz-Cueto J.A. Cloning and gene expression of deiodinase enzymes and thyroid hormone receptors in the European sea bass, Dicentrarchus labrax. Cybium 2008, 32(Suppl. 2):64.
22. Jakobs T.C., Schmutzler C., Meissner J., Köhrle J. The promoter of the human type 1 5'-deiodinase gene - mapping of the transcription state site and identification of a DR+4 thyroid-hormone-responsive element. Eur. J. Biochem. 1997, 247:288-297.
23. Jayewardene D. A factorial experiment quantifying the influence of parrotfish density and size on algal reduction on Hawaiian coral reefs. J. Exp. Mar. Biol. Ecol. 2009, 375:64-69.
24. Kang D.-Y., Chang Y.J. Effects of maternal injection of 3,5,3'-triidod-l-thyronine (T3) on growth of newborn offspring of rockfish, Sebastes schlegeli. Aquaculture 2004, 234:641-655.
25. Kawakami Y., Shin D.-H., Kitano T., Adachi S., Yamauchi K., Ohta H. Transactivation activity of thyroid hormone receptors in fish (Conger myriaster) in response to thyroid hormones. Comp. Biochem. Physiol. B 2006, 144:503-509.
26. Kawakami Y., Adachi S., Yamauchi K., Ohta H. Thyroid hormone receptor β is widely expressed in the brain and pituitary of the Japanese eel, Anguilla japonica. Gen. Comp. Endocrinol. 2007, 150:386-394.
27. Kim S.W., Harney J.W., Larsen P.R. Studies of the hormonal regulation of type 2 5'-iodothyronine deiodinase messenger ribonucleic acid in pituitary tumor cells using semiquantitative reverse transcription-polymerase chain reaction. Endocrinology 1998, 139:4895-4905.
28. Kim S.W., Hong S.J., Kim K.M., Ho S.C., So E.V., Harney J.W., Larsen P.R. A novel cell type-specific mechanism for thyroid hormone-dependent negative regulation of the human type 1 deiodinase gene. Mol. Endocrinol. 2004, 18:2924-2936.
29. Köhrl J. Local activation and inactivation of thyroid hormones: the deiodinase family. Mol. Cell. Endocrinol. 1999, 151:103-119.
30. Köhrl J. The deiodinase family: selenoenzymes regulating thyroid hormone availability and action. Cell. Mol. Life Sci. 2000, 57:1853-1863.
31. Kume G., Kubo Y., Yoshimura T., Kiriyama T., Yamaguchi A. Life history characteristics of the protogynouse parrotfish Calotomus japonicas from northwest Kyushu, Japan. Ichthyol. Res. 2010, 57:113-120.
32. Larhammar D., Sundstrom G., Dreborg S., Daza D.O., Larsson T.A. Major genomic events and their consequences for vertebrate evolution and endocrinology. Trends Comp. Endocrinol. Neurobiol. 2009, 1163:201-208.
33. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
34. Lema S.C., Dickey J.T., Schultz I.R., Swanson P. Thyroid regulation of mRNAs encoding thyrotropin β-subunit, glycoprotein α-subunit, and thyroid hormone receptors α and β in brain, pituitary gland, liver, and gonads of an adult teleost, Pimephales promelas. J. Endocrinol. 2009, 202:43-54.
35. Lema S.C., Dickey J.T., Schultz I.R., Swanson P. Dietary exposure to 2,2',4,4'-tetrabromodiphenyl ether (PBDE-47) alters thyroid status and thyroid hormone-regulated gene transcription in the pituitary and brain. Environ. Health Perspect. 2008, 116:1694-1699.
36. Lema S.C., Nevitt G.A. An ecophysiological mechanism for morphological plasticity in pupfish and its relevance to conservation efforts for endangered Devils Hole pupfish. J. Exp. Biol. 2006, 209:3499-3509.
37. Lema S.C., Nevitt G.A. Evidence that thyroid hormone induces olfactory cellular proliferation in salmon during a sensitive period for imprinting. J. Exp. Biol. 2004, 207:3317-3327.
38. Li W., Zha J.M., Spear P.A., Li Z.L., Yang L.H., Wang Z.J. Changes of thyroid hormone levels and related gene expression in Chinese rare minnow (Gobiocypris rarus) during 3-amino-1,2,4-triazole exposure and recovery. Aquat. Toxicol. 2009, 92:50-57.
39. Liu Y.-W., Lo L.-J., Chan W.-K. Temporal expression and T3 induction of thyroid hormone receptors α1 and β1 during early embryonic and larval development in zebrafish, Danio rerio. Mol. Cell. Endocrinol. 2000, 159:187-195.
40. Manchado M., Infante C., Rebordinos L., Canavate J.P. Molecular characterization, gene expression and transcriptional regulation of thyroid hormone receptors in Senegalese sole. Gen. Comp. Endocrinol. 2009, 160:139-147.
41. Marinez deMena R., Scanlan T.S., Obregon M.-J. The T3 receptor β1 isoform regulates UCP1 and D2 deiodinase in rat brown adipocytes. Endocrinology 2010, 151:5074-5083.
42. Matta S.L.P., Vilela D.A.R., Godinho H.P., Franca L.R. The goitrogen 6-n-propyl-2-thiouracil (PTU) given during testis development increase sertoli germ cell numbers per cyst in fish: the tilapia (Oreochromis niloticus) model. Endocrinology 2002, 143:970-978.
43. Matthews S.A. The thyroid gland of the Bermuda parrot fish, Pseudoscarus guacamaia. Anat. Rec. 1948, 101:251-263.
44. Matthews S.A., Smith D.C. Concentration of radioactive iodine by the thyroid gland of the parrot fish, Sparisoma sp. Am. J. Physiol. 1948, 222-225.
45. McCormick S.D. Endocrine control of osmoregulation in teleost fish. Integr. Comp. Biol. 2001, 41:781-794.
46. Mol K.A., Van der Geyten S., Burel C., Kuhn E.R., Boujard T., Darras V.M. Comparative study of iodothyronine outer ring and inner ring deiodinase activities in five teleostean fishes. Fish Physiol. Biochem. 1998, 18:253-266.
47. Mol K., Van der Geyton S., Kuhn E., Darras V. Effects of experimental hypo- and hyperthyroidism on iodothyronine deiodinases in Nile tilapia Oreochromis niloticus. Fish Physiol. Biochem. 1999, 20:201-207.
48. Morgado I., Campinho M.A., Costa R., Jacinto R., Power D.M. Disruption of the thyroid system by diethylstilbestrol and ioxynil in the sea bream (Sparus aurata). Aquat. Toxicol. 2009, 92:271-280.
49. Morin P.P., Hara T.J., Eales J.G. T4 depresses olfactory responses to l-alanine and plasma T3 and T3 production in smoltifying Atlantic salmon. Am. J. Physiol. Reg. Integr. Comp. Physiol. 1995, 269:R1434-R1440.
50. Mortensen A.S., Arukwe A. The persistent DDT metabolite, 1,1-dichloro-2,2-bis(ρ-chlrorphenyl)ethylene, alters thyroid hormone-dependent genes, hepatic cytochrome P4503A, and pregnane X receptor gene expression in Atlantic salmon (Salmo salar) parr. Environ. Toxicol. Chem. 2006, 25:1607-1615.
51. Nelson E.R., Habibi H.R. Thyroid receptor subtypes: structure and function in fish. Gen. Comp. Endocrinol. 2009, 161:90-96.
52. Nelson E.R., Habibi H.R. Functional significance of a truncated thyroid receptor subtype lacking a hormone-binding domain in goldfish. Endocrinology 2008, 149:4702-4709.
53. Nelson E.R., Habibi H.R. Molecular characterization and sex-related seasonal expression of thyroid receptor subtypes in goldfish. Mol. Cell. Endocrinol. 2006, 253:83095.
54. Orozco A., Valverde R.C. Thyroid hormone deiodination in fish. Thyroid 2005, 15:799-813.
55. Picard-Aitken M., Fournier H., Pariseau R., Marcogliese D.J., Cyr D.G. Thyroid disruption in walleye (Sander vitreus) exposed to environmental contaminants: cloning and use of iodothyronine deiodinases as molecular biomarkers. Aquat. Toxicol. 2007, 83:200-211.
56. Plate E.M., Adams B.A., Allison W.T., Martens G., Hawryshyn C.W., Eales J.G. The effects of thyroxine or a GnRH analogue on thyroid hormone deiodination in the olfactory epithelium and retina of rainbow trout, Oncorhynchus mykiss, and sockeye salmon, Oncorhynchus nerka. Gen. Comp. Endocrinol. 2002, 127:59-65.
57. Robertson D.R., Warner R.R. Sexual patterns of the labroid fishes of the western Caribbean, II. The parrotfishes (Scaridae). Smith. Contr. Zool. 1978, 255:1-26.
58. Sadow P.M., Chassande O., Koo E.K., Gauthier K., Samarut J., Xu J., O'Malley B.W., Weiss R.E. Regulation of expression of thyroid hormone receptor isoforms and coactivators in liver and heart by thyroid hormone. Mol. Cell. Endocrinol. 2003, 203:65-75.
59. Saitou N., Nei M. The Neighbor-Joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
60. Sambroni E., Gutieres S., Cauty C., Guiguen Y., Breton B., La Reyre J.-J. Type II iodothyronine deiodinase is preferentially expressed in rainbow trout (Oncorhynchus mykiss) liver and gonads. Mol. Reprod. Develop. 2001, 60:338-350.
61. Sanders J.P., Van der Geyten S., Kaptein E., Darras V.M., Kühn E.R., Leonard J.L., Visser T.J. Cloning and characterization of type III iodothyronine deiodinase from the fish Oreochromis niloticus. Endocrinology 1999, 140:3666-3673.
62. Sanders J.P., Van der Geyten S., Kaptein E., Darras V.M., Kuhn E.R., Leonard J.L., Visser T.J. Characterization of a propylthiouracil-insensitive type 1 iodothyronine deiodinase. Endocrinology 1997, 138:5153-5160.
63. Santos E.M., Kille P., Workman V.L., Paull G.C., Tyler C.R. Sexually dimorphic gene expression in the brains of mature zebrafish. Comp. Biochem. Physiol. A 2008, 149:314-324.
64. Schmutzler C., Gotthardt I., Hofmann P.J., Radovic B., Kovacs G., Stemmier L., Nobis I., Bacinski A., Mentrup B., Ambrugger P., Gruters A., Malendowicz L.K., Christoffel J., Jarry H., Seidlova-Wuttke D., Wuttke W., Kohrle J. Endocrine disruptors and the thyroid gland: a combined in vitro and in vivo analysis of potential new biomarkers. Environ. Health Perspect. 2007, 115:77-83.
65. Shi X., Liu C., Wu G., Zhou B. Waterborn exposure to PFOS causes disruption of the hypothalamus-pituitary-thyroid axis in zebrafish larvae. Chemosphere 2009, 77:1010-1018.
66. Smith L.L., Fessler J.L., Alfaro M.E., Streelman J.T., Westneat M.W. Phylogenteic relationships and the evolution of regulatory gene sequences in the parrotfishes. Mol. Phylogen. Evol. 2008, 49:136-152.
67. St.Germain D.L., Galton V.A., Hernandez A. Defining the roles of the iodothyronine deiodinases: current concepts and challenges. Endocrinology 2009, 150:1097-1107.
68. Sutija M., Longhurst T.J., Joss J.M.P. Deiodinase type II and tissue specific mRNA alternative splicing in the Australian lungfish, Neoceratodus forsteri. Gen. Comp. Endocrinol. 2003, 132:409-417.
69. Swapna I., Rajasekhar A., Supriya A., Raghuveer K., Rasheeda M.K., Majumdar K.C., Kagawa H., Tanaka H., Dutta-Gupta A., Senthilkumaran B. Thiourea-induced thyroid hormone depletion impairs testicular recrudescence in the air-breathing catfish, Clarias gariepinus. Comp. Biochem. Physiol. A 2006, 144:1-10.
70. Swanson P., Grau E.G., Helms L.M.H., Dickhoff W.W. Thyrotropic activity of salmon pituitary glycoprotein hormones in the Hawaiian parrotfish thyroid in vitro. J. Exp. Zool. 1988, 245:194-199.
71. Szabo D.T., Richardson V.M., Ross D.G., Diliberto J.J., Kodavanti P.R.S., Birnbaum L.S. Effects of perinatal PBD exposure on hepatic phase I, phase II, phase III, and deiodinase 1 gene expression involved in thyroid hormone metabolism in male rat pups. Toxicol. Sci. 2009, 107:27-39.
72. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
73. Tu H.M., Kim S.W., Salvatore D., Bartha T., Legradi G., Larsen P.R., Lechan R.M. Regional distribution of type 2 thyroxine deiodinase messenger ribonucleic acid in rat hypothalamus and pituitary and its regulation by thyroid hormone. Endocrinology 1997, 138:3359-3368.
74. Van der Geyten S., Toguyeni A., Baroiller J.F., Fauconneau B., Fostier A., Sanders J.P., Visser T.J., Kühn E.R., Darras V.M. Hypothyroidism induces type 1 iodothyronine deiodinase expression in tilapia liver. Gen. Comp. Endocrinol. 2001, 124:333-342.
75. Van der Geyten S., Byamungu N., Reyns G.E., Kühn E.R., Darras V.M. Iodothyronine deiodinases and the control of plasma and tissue thyroid hormone levels in hyperthyroid tilapia (Oreochromis niloticus). J. Endocrinol. 2005, 184:467-479.
76. Wagner M.S., Morimoto R., Dora J.M., Benneman A., Pavan R., Maia A.L. Hypothyroidism induces type 2 iodothyronine deiodinase expression in mouse heart and testis. J. Endocrinol. 2003, 31:541-550.
77. Wajner, S.M., Wagner, M. dS., Melo, R.C.N., Parreira, G.G., Chiarini-Garcia, H., Bianco, A.C., Fekete, C., Sanchez, E., Lechan, R.M., Maia, A.L., 2007. Type 2 iodothyronine deiodinase is highly expressed in germ cells of adult rat testis. J. Endocrinol. 194, 47-54.
78. Walpita C.N., Van der Geyten S., Rurangwa E., Darras V.M. The effect of 3,5,3'-triiodothyronine supplementation on zebrafish (Danio rerio) embyronic development and expression of iodothyronine deiodinases and thyroid hormone receptors. Gen. Comp. Endocrinol. 2007, 152:206-214.
79. Yen P.M., Ando S., Feng X., Liu Y., Maruvanda P., Xia X. Thyroid hormone action at the cellular, genomic and target gene levels. Mol. Cell. Endocrinol. 2006, 246:121-127.
80. Zavacki A.M., Ying H., Christoffolete M.A., Aerts G., So E., Harney J.W., Cheng S.-Y., Larsen P.R., Bianco A.C. Type 1 iodothyronine deiodinase is a sensitive marker of peripheral thyroid status in the mouse. Endocrinology 2005, 146:1568-1575.
81. E.R. Nelson, E.R.O. Allan, F.Y. Pang, H.R. Habibi, Auto-regulation of thyroid hormone receptors in the goldfish ovary and testis, Gen. Comp. Endocrinol., in press, doi:10.1016/j.ygcen.2010.12.017.