Cite this paper:
WANG Guodong, ZHANG Lili, XU Jianbo, YIN Cheng, ZHANG Ziping, WANG Yilei. The roles of thyroid hormone receptor and T3 in metamorphosis of Haliotis diversicolor[J]. Journal of Oceanology and Limnology, 2019, 37(2): 745-758

The roles of thyroid hormone receptor and T3 in metamorphosis of Haliotis diversicolor

WANG Guodong1, ZHANG Lili1, XU Jianbo1, YIN Cheng1, ZHANG Ziping2, WANG Yilei1
1 Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture, Fisheries College, Jimei University, Xiamen 361021, China;
2 College of Animal Science, Fujian Agriculture and Forestry University, Fuzhou 350002, China
Abstract:
Thyroid hormone is a kind of important hormone which regulates metamorphosis. Its role is well described in amphibian metamorphosis. Thyroid hormones (T3 and T4) have also been demonstrated to play a role in metamorphosis of marine invertebrates. However, the mechanism of thyroid hormone in metamorphosis of marine invertebrates remains unknown. A homolog of vertebrate thyroid hormone receptor (TR) was cloned and identified in abalone Haliotis diversicolor and was named HdTR. The mRNA expressions of HdTR, thyroid peroxidase (TPO), thyroid peroxidase 1 (TPO1), idothyronine deiodinase Ⅲ (IDⅢ) and integrin alpha-V (ITGAV) had significant difference in metamorphosis of H. diversicolor. Metamorphosis rate and mortality rate were significantly different in HdTR RNAi experiment and T3 inducing experiment. In RNAi experiment, ITGAV and CCND1 (cyclin D1) expression of dsRNA HdTR exposing group were significantly lower than those of blank control and negative control. But CTNNB (catenin beta) expression of dsRNA HdTR exposing group was higher than that those of blank control and negative control. ERK (extracellular signal regulated kinases) and PI3K (phosphoinositide-3-kinase) had no significant difference in RNAi experiment. Moreover, ITGAV of 1 μmol/L T3 group was significantly lower than that of 0 μmol/L T3 group, PI3K expression of 10 μmol/L T3 group was higher than that of 0 μmol/L T3 group, and the other genes expression had no significant difference in T3 inducing experiment. The data of genes expression suggested that CCND1 might be an effector gene of TR genomic action, while CTNNB might be regulated by unliganded TR. CCND1 and CTNNB may be involved in cell proliferation of metamorphosis. T3 might regulate the expression level of PI3K via nongenomic way. These results shed light on the mechanism of thyroid hormone in abalone metamorphosis.
Key words:    thyroid hormone receptor|thyroid hormone (TH) (T3)|abalone|metamorphosis   
Received: 2018-01-22   Revised: 2018-04-28
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References:
Baldin V, Lukas J, Marcote M J, Pagano M, Draetta G. 1993. Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes & Development, 7(5):812-821.
Bergh J J, Lin H Y, Lansing L, Mohamed S N, Davis F B, Mousa S, Davis P J. 2005. Integrin αVβ3 contains a cell surface receptor site for thyroid hormone that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology, 146(7):2 864-2 871.
Bernal J, Morte B. 2013. Thyroid hormone receptor activity in the absence of ligand:physiological and developmental implications. Biochimica et Biophysica Acta (BBA)-General Subjects, 1830(7):3 893-3 899.
Bertrand S, Brunet F G, Escriva H, Parmentier G, Laudet V, Robinson-Rechavi M. 2004. Evolutionary genomics of nuclear receptors:from twenty-five ancestral genes to derived endocrine systems. Molecular Biology and Evolution, 21(10):1 923-1 937.
Bishop C D, Erezyilmaz D F, Flatt T, Georgiou C D, Hadfield M G, Heyland A, Hodin J, Jacobs M W, Maslakova S A, Pires A, Reitzel A M, Santagata S, Tanaka K, Youson J H. 2006. What is metamorphosis? Integrative and Comparative Biology, 46(6):655-661.
Bryan P J, Qian P Y. 1998. Induction of larval attachment and metamorphosis in the abalone Haliotis diversicolor(Reeve). Journal of Experimental Marine Biology and Ecology, 223(1):39-51.
Cheng S Y, Leonard J L, Davis P J. 2010.Molecular aspects of thyroid hormone actions. Endocrine Reviews, 31(2):139-170.
Degroot L J, Niepomniszcze H. 1977. Biosynthesis of thyroid hormone:basic and clinical aspects. Metabolism, 26(6):665-718.
Flatt T, Moroz L L, Tatar M, Heyland A. 2006. Comparing thyroid and insect hormone signaling. Integrative and Comparative Biology, 46(6):777-794.
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 Science, 67(5):985-988.
Gottardi C J, Gumbiner B M. 2001. Adhesion signaling:how β-catenin interacts with its partners. Current Biology, 11(19):R792-R794.
Heyland A, Hodin J. 2004. Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implications for phenotypic plasticity and the evolution of nonfeeding development. Evolution, 58(3):524-538.
Heyland A, Moroz L L. 2005. Cross-kingdom hormonal signaling:an insight from thyroid hormone functions in marine larvae. Journal of Experimental Biology, 208(Pt 23):4 355-4 361.
Heyland A, Moroz L L. 2006. Signaling mechanisms underlying metamorphic transitions in animals.Integrative and Comparative Biology, 46(6):743-759.
Heyland A, Price D A, Bodnarova-Buganova M, Moroz L L. 2006a. Thyroid hormone metabolism and peroxidase function in two non-chordate animals. Journal of Experimental Zoology, 306B(6):551-566.
Heyland A, Reitzel A M, Price D A, Moroz L L. 2006b.Endogenous thyroid hormone synthesis in facultative planktotrophic larvae of the sand dollar Clypeaster rosaceus:implications for the evolutionary loss of larval feeding. Evolution & Development, 8(6):568-579.
Holstein T W, Laudet V. 2014. Life-history evolution:at the origins of metamorphosis. Current Biology, 24(4):R159-R161.
Huang W, Xu F, Qu T, Zhang R, Li L, Que H Y, Zhang G F. 2015. Identification of thyroid hormones and functional characterization of thyroid hormone receptor in the pacific oyster Crassostrea gigas provide insight into evolution of the thyroid hormone system. PLoS One, 10(12):e0144991.
Huang Z X, Chen Z S, Ke C H, Zhao J, You W W, Zhang J, Dong W T, Chen J. 2012. Pyrosequencing of Haliotis diversicolor transcriptomes:insights into early developmental molluscan gene expression. PLoS One, 7(12):e51279.
Jiang J Z, Zhang W, Guo Z X, Cai C C, Su Y L, Wang R X, Wang J Y. 2011. Functional annotation of an expressed sequence tag library from Haliotis diversicolor and analysis of its plant-like sequences. Marine Genomics, 4(3):189-196.
Johnson L G. 1998. Stage-dependent thyroxine effects on sea urchin development. New Zealand Journal of Marine and Freshwater Research, 32(4):531-536.
Kimura S, Kotani T, McBride O W, Umeki K, Hirai K, Nakayama T, Ohtaki S. 1987. Human thyroid peroxidase:complete cDNA and protein sequence, chromosome mapping, and identification of two alternately spliced mRNAs. Proceedings of the National Academy of Sciences of the United States of America, 84(16):5 555-5 559.
Lei J X, Mariash C N, Bhargava M, Wattenberg E V, Ingbar D H. 2008. T3 increases Na-K-ATPase activity via a MAPK/ERK1/2-dependent pathway in rat adult alveolar epithelial cells. American Journal of Physiology-Lung Cellular and Molecular Physiology, 294(4):L749-L754.
Lei J X, Mariash C N, Ingbar D H. 2004. 3,3',5-Triiodo-lthyronine up-regulation of Na, K-ATPase activity and cell surface expression in alveolar epithelial cells is Src kinase-and phosphoinositide 3-kinase-dependent.Journal of Biological Chemistry, 279(46):47 589-47 600.
Li H F, Lin W, Zhang G, Cai Z H, Cai G P, Chang Y Q, Xing K Z. 2006. Enhancement of larval settlement and metamorphosis through biological and chemical cues in the abalone Haliotis diversicolor supertexta. Aquaculture, 258(1-4):416-423.
Li N, Zhang Z P, Zhang L L, Wang S H, Zou Z H, Wang G D, Wang Y L. 2012. Insulin-like growth factor binding protein 7, a member of insulin-like growth factor signal pathway, involved in immune response of small abalone Haliotis diversicolor. Fish & Shellfish Immunology, 33(2):229-242.
Lin H Y, Tang H Y, Keating T, Wu Y H, Shih A, Hammond D, Sun M Z, Hercbergs A, Davis F B, Davis P J. 2008. Resveratrol is pro-apoptotic and thyroid hormone is antiapoptotic in glioma cells:both actions are integrin and ERK mediated. Carcinogenesis, 29(1):62-69.
Moon R T, Bowerman B, Boutros M, Perrimon N. 2002. The promise and perils of Wnt signaling through β-catenin.Science, 296(5573):1 644-1 646.
Muñoz A, Wrighton C, Seliger B, Bernal J, Beug H. 1993. Thyroid hormone receptor/c-erbA:control of commitment and differentiation in the neuronal/chromaffin progenitor line PC12. Journal of Cell Biology, 121(2):423-438.
Orozco A, Valverde-R C, Olvera A, Garcia-G C. 2012. Iodothyronine deiodinases:a functional and evolutionary perspective. Journal of Endocrinology, 215(2):207-219.
Pakharukova M Y, Ershov N I, Vorontsova E V, Shilov A G, Merkulova T I, Mordvinov V A. 2014. Identification of thyroid hormone receptor homologs in the fluke Opisthorchis felineus (platyhelminthes). Molecular and Biochemical Parasitology, 194(1-2):64-68.
Paris M, Escriva H, Schubert M, Brunet F, Brtko J, Ciesielski F, Roecklin D, Vivat-Hannah V, Jamin E L, Cravedi J P, Scanlan T S, Renaud J P, Holland N D, Laudet V. 2008. Amphioxus postembryonic development reveals the homology of chordate metamorphosis. Current Biology, 18(11):825-830.
Pascual A, Aranda A. 2013. Thyroid hormone receptors, cell growth and differentiation. Biochimica et Biophysica Acta(BBA)-General Subjects, 1830(7):3 908-3 916.
Pibiri M, Ledda-Columbano G M, Cossu C, Simbula G, Menegazzi M, Shinozuka H, Columbano A. 2001. Cyclin D1 is an early target in hepatocyte proliferation induced by thyroid hormone (T3). The FASEB Journal, 15(6):1 006-1 013.
Roberts R D, Lapworth C, Barker R J. 2001. Effect of starvation on the growth and survival of post-larval abalone (Haliotis iris). Aquaculture, 200(3-4):323-338.
Sato Y, Buchholz D R, Paul B D, Shi Y B. 2007. A role of unliganded thyroid hormone receptor in postembryonic development in Xenopus laevis. Mechanisms of Development, 124(6):476-488.
Wang G D, Li N, Zhang L L, Zhang L H, Zhang Z P, Wang Y L. 2016. IGFBP7 is involved in abalone metamorphosis.Aquaculture, 451:377-384.
Williams E A, Degnan B M, Gunter H, Jackson D J, Woodcroft B J, Degnan S M. 2009. Widespread transcriptional changes pre-empt the critical pelagic-benthic transition in the vetigastropod Haliotis asinina. Molecular Ecology, 18(5):1 006-1 025.
Wu W J, Niles E G, El-Sayed N, Berriman M, Loverde P T. 2006. Schistosoma mansoni (Platyhelminthes, Trematoda)nuclear receptors:sixteen new members and a novel subfamily. Gene, 366(2):303-315.
Wu W J, Niles E G, Hirai H, Loverde P T. 2007. Evolution of a novel subfamily of nuclear receptors with members that each contain two DNA binding domains. BMC Evolutionary Biology, 7:27.
Yen P M, Feng X, Flamant F, Chen Y D, Walker R L, Weiss R E, Chassande O, Samarut J, Refetoff S, Meltzer P S. 2003. Effects of ligand and thyroid hormone receptor isoforms on hepatic gene expression profiles of thyroid hormone receptor knockout mice. EMBO Reports, 4(6):581-587.
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