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Iodothyronine deiodinase gene analysis of the Pacific oyster Crassostrea gigas reveals possible conservation of thyroid hormone feedback regulation mechanism in mollusks

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Abstract

Iodothyronine deiodinase catalyzes the initiation and termination of thyroid hormones (THs) effects, and plays a central role in the regulation of thyroid hormone level in vertebrates. In non-chordate invertebrates, only one deiodinase has been identified in the scallop Chlamys farreri. Here, two deiodinases were cloned in the Pacific oyster Crassostrea gigas (CgDx and CgDy). The characteristic in-frame TGA codons and selenocysteine insertion sequence elements in the oyster deiodinase cDNAs supported the activity of them. Furthermore, seven orthologs of deiodinases were found by a tblastn search in the mollusk Lottia gigantea and the annelid Capitella teleta. A phylogenetic analysis revealed that the deiodinase gene originated from an common ancestor and a clade-specific gene duplication occurred independently during the differentiation of the mollusk, annelid, and vertebrate lineages. The distinct spatiotemporal expression patterns implied functional divergence of the two deiodinases. The expression of CgDx and CgDy was influenced by L-thyroxine T4, and putative thyroid hormone responsive elements were found in their promoters, which suggested that the oyster deiodinases were feedback regulated by TH. Epinephrine stimulated the expression level of CgDx and CgDy, suggesting an interaction effect between different hormones. This study provides the first evidence for the existence of a conserved TH feedback regulation mechanism in mollusks, providing insights into TH evolution.

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References

  • Barca-Mayo O, Liao X H, Alonso M, Di Cosmo C, Hernandez A, Refetoff S, Weiss R E. 2011. Thyroid hormone receptor α and regulation of type 3 deiodinase. Mol. Endocrinol., 25(4): 575–583.

    Article  Google Scholar 

  • Berry M J, Banu L, Harney J W, Larsen P R. 1993. Functional characterization of the eukaryotic secis elements which direct selenocysteine insertion at UGA codons. EMBO J., 12(8): 3 315–3 322.

    Google Scholar 

  • Bianco A C, Salvatore D, Gereben B, Berry M J, Larsen P R. 2002. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr. Rev., 23(1): 38–89.

    Article  Google Scholar 

  • Coon S L, Bonar D B, Weiner R M. 1985. Induction of settlement and metamorphosis of the Pacific oyster, Crassostrea gigas (Thunberg), by l-Dopa and catecholamines. J. Exp. Mar. Biol. Ecol., 94(1–3): 211–221.

    Article  Google Scholar 

  • Croteau W, Davey J C, Galton V A, 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. C lini. I nvest., 98(2): 405–417.

    Google Scholar 

  • Das B, Heimeier R A, Buchholz D R, Shi Y B. 2009. Identification of direct thyroid hormone response genes reveals the earliest gene regulation programs during frog metamorphosis. J. Biol. Chem., 284(49): 34 167–34 178.

    Article  Google Scholar 

  • Du Y S, Zhang L L, Xu F, Huang B Y, Zhang G F, Li L. 2013. Validation of housekeeping genes as internal controls for studying gene expression during Pacific oyster (Crassostrea gigas) development by quantitative realtime PCR. Fish Shellfish Immunol., 34(3): 939–945.

    Article  Google Scholar 

  • Fukazawa H, Hirai H, Hori H, Roberts R D, Nukaya H, Ishida H, Tsuji K. 2001. Induction of abalone larval metamorphosis by thyroid hormones. Fisheries Sci., 67(5): 985–987.

    Article  Google Scholar 

  • Heyland A, Price D A, Bodnarova-Buganova M, Moroz L L. 2006. Thyroid hormone metabolism and peroxidase function in two non-chordate animals. J. Exp. Zool. B Mol. Dev. Evol., 306B(6): 551–566.

    Article  Google Scholar 

  • Jakobs T C, Schmutzler C, Meissner J, Köhrle J. 1997. The promoter of the human type I 5′-deiodinase gene—mapping of the transcription start site and identification of a DR+4 thyroid-hormone-responsive element. Eur. J. Biochem., 247(1): 288–297.

    Article  Google Scholar 

  • Köhrle J. 2002. Iodothyronine deiodinases. Methods Enzymol., 347: 125–167.

    Article  Google Scholar 

  • Laudet V. 2011. The origins and evolution of vertebrate metamorphosis. Curr. Biol., 21(18): R726–R737.

    Article  Google Scholar 

  • Lobanov A V, Fomenko D E, Zhang Y, Sengupta A, Hatfield D L, Gladyshev V N. 2007. Evolutionary dynamics of eukaryotic selenoproteomes: large selenoproteomes may associate with aquatic life and small with terrestrial life. Genome Biol., 8(9): R198.

    Article  Google Scholar 

  • Mariotti M, Lobanov A V, Guigo R, Gladyshev V N. 2013. SECISearch3 and Seblastian: new tools for prediction of SECIS elements and selenoproteins. Nucleic Acids Res., 41(15): e149.

    Article  Google Scholar 

  • Morvan-Dubois G, Demeneix B A, Sachs L M. 2008. Xenopus laevis as a model for studying thyroid hormone signalling: From development to metamorphosis. Mol. Cell. Endocrinol., 293(1–2): 71–79.

    Article  Google Scholar 

  • Nakajima K, Fujimoto K, Yaoita Y. 2012. Regulation of thyroid hormone sensitivity by differential expression of the thyroid hormone receptor during Xenopus metamorphosis. Genes Cells, 17(8): 645–659.

    Article  Google Scholar 

  • Qu T, Huang B Y, Zhang L L, Li L, Xu F, Huang W, Li C Y, Du Y S, Zhang G F. 2014. Identification and functional characterization of two executioner caspases in Crassostrea gigas. PloS One, 9(2): e89040.

    Article  Google Scholar 

  • Roustaian P, Gaik L A. 2006. Effect of thyroxine immersion on larval survival, growth and postlarvae production of freshwater prawn, Macrobrachium rosenbergii (de Man). Aquac. Res., 37(13): 1 378–1 380.

    Article  Google Scholar 

  • Schweizer U, Schlicker C, Braun D, Kohrle J, Steegborn C. 2014. Crystal structure of mammalian selenocysteine-dependent iodothyronine deiodinase suggests a peroxiredoxin-like catalytic mechanism. Proc. Natl. Acad. Sci. USA, 111(29): 10 526–10 531.

    Article  Google Scholar 

  • Shepherdley C A, Klootwijk W, Makabe K W, Visser T J, Kuiper G G J M. 2003. An ascidian homolog of vertebrate iodothyronine deiodinases. Endocrinology, 145(3): 1 255–1 268.

    Article  Google Scholar 

  • Tata J R. 2006. Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Mol. Cell. Endocrinol., 246(1–2): 10–20.

    Article  Google Scholar 

  • Wu T T, Shi X W, Zhou Z, Wang L L, Wang M Q, Wang L L, Huang M M, Yang C Y, Song L S. 2012. An iodothyronine deiodinase from Chlamys farreri and its induced mRNA expression after LPS stimulation. Fish Shellfish Immunol., 33(2): 286–293.

    Article  Google Scholar 

  • Wu W J, Niles E G, Loverde P T. 2007. Thyroid hormone receptor orthologues from invertebrate species with emphasis on Schistosoma mansoni. BMC Evol. Biol., 7: 150.

    Article  Google Scholar 

  • Yen P M. 2001. Physiological and molecular basis of thyroid hormone action. Physiol. Rev., 81(3): 1 097–1 142.

    Google Scholar 

  • Zavacki A M, Ying H, Christoffolete M A, Aerts G, So E, Harney J W, Cheng S Y, Larsen P R, Bianco A C. 2005. Type 1 iodothyronine deiodinase is a sensitive marker of peripheral thyroid status in the mouse. Endocrinology, 146(3): 1 568–1 575.

    Article  Google Scholar 

  • Zhang G F, Fang X D, Guo X M, Li L, Luo R B, Xu F, Yang P C, Zhang L L, Wang X T, Qi H G, Xiong Z Q, Que H Y, Xie Y L, Holland P W H, Paps J, Zhu Y B, Wu F C, Chen Y X, Wang J F, Peng C F, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z Y, Zhu Q H, Feng Y, Mount A, Hedgecock D, Xu Z, Liu Y J, Domazet-Lošo T, Du Y S, Sun X Q, Zhang S D, Liu B H, Cheng P Z, Jiang X T, Li J, Fan D D, Wang W, Fu W J, Wang T, Wang B, Zhang J B, Peng Z Y, Li Y X, Li N, Wang J P, Chen M S, He Y, Tan F J, Song X R, Zheng Q M, Huang R L, Yang H L, Du X D, Chen L, Yang M, Gaffney P M, Wang S, Luo L H, She Z C, Ming Y, Huang W, Zhang S, Huang B Y, Zhang Y, Qu T, Ni P X, Miao G Y, Wang J Y, Wang Q, Steinberg C E W, Wang H Y, Li N, Qian L M, Zhang G J, Li Y R, Yang H M, Liu X, Wang J, Yin Y, Wang J. 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature, 490(7418): 49–54.

    Article  Google Scholar 

  • Zhang J S, Lazar M A. 2000. The mechanism of action of thyroid hormones. Annu. Rev. Physiol., 62: 439–466.

    Article  Google Scholar 

  • Zhang L L, Li L, Zhang G F. 2011. Gene discovery, comparative analysis and expression profile reveal the complexity of the Crassostrea gigas apoptosis system. Dev. Comp. Immunol., 35(5): 603–610.

    Article  Google Scholar 

Download references

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Authors and Affiliations

  1. National & Local Joint Engineering Laboratory of Ecological Mariculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Wen Huang  (黄雯), Fei Xu  (许飞), Tao Qu  (曲涛), Li Li  (李莉), Huayong Que  (阙华勇) & Guofan Zhang  (张国范)

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Wen Huang  (黄雯)

Authors
  1. Wen Huang  (黄雯)
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  2. Fei Xu  (许飞)
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  3. Tao Qu  (曲涛)
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  4. Li Li  (李莉)
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  5. Huayong Que  (阙华勇)
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  6. Guofan Zhang  (张国范)
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Corresponding authors

Correspondence to Huayong Que  (阙华勇) or Guofan Zhang  (张国范).

Additional information

Supported by the National Natural Science Foundation of China (Nos. 31372515, 31402285), the National Basic Research Program of China (973 Program) (No. 2010CB126401), and the National High Technology Research and Development Program (863 Program) (No. 2012AA10A405)

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Huang, W., Xu, F., Qu, T. et al. Iodothyronine deiodinase gene analysis of the Pacific oyster Crassostrea gigas reveals possible conservation of thyroid hormone feedback regulation mechanism in mollusks. Chin. J. Ocean. Limnol. 33, 997–1006 (2015). https://doi.org/10.1007/s00343-015-4300-x

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  • DOI: https://doi.org/10.1007/s00343-015-4300-x

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