Advertisement

Fish Physiology and Biochemistry

, Volume 45, Issue 1, pp 299–309 | Cite as

Proteomic variation in metamorphosing Paralichthys olivaceus induced by exogenous thyroid hormone

  • Jie Yu
  • Yuanshuai Fu
  • Suping Liu
  • Zhiyi ShiEmail author
Article

Abstract

Thyroid hormone (TH) is essential for Paralichthys olivaceus metamorphosis. Exogenous TH treatment induces premature metamorphosis in P. olivaceus larvae and a series of studies have been conducted to identify thyroid hormone-regulated functional genes and microRNAs involved in the metamorphosis of P. olivaceus; however, the proteins involved in this process remain to be fully clarified. In this study, the differential proteomic responses of P. olivaceus larvae to exogenous TH treatment were examined using tandem mass tags (TMT) for quantitation labeling followed by liquid chromatography tandem mass spectrometry (LC-MS/MS). The expression levels of 629 cellular proteins were identified to be significantly affected by TH treatment. The reliability of our TMT-labeled LC-MS/MS analysis was verified by examining the mRNA and protein levels of four selected proteins using quantitative real-time reverse-transcription PCR and western blot analyses. The possible biological significance of these proteins was further investigated by Gene Ontology (GO) enrichment, Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment, and protein-protein interaction analyses. Notably, we identified and described five groups of proteins involved in different important life events that were significantly regulated by exogenous TH treatment. Our study provides an improved understanding of the molecular mechanisms by which TH regulates the metamorphosis of P. olivaceus.

Keywords

Paralichthys olivaceus Metamorphosis Thyroid hormone TMT-labeled LC-MS/MS analysis Proteomics 

Notes

Acknowledgments

The authors thank Prof. Haijin Liu (Chinese Academy of Fishery Sciences) for providing the experimental fish.

Funding information

This work was supported by the National Natural Science Foundation of China (No. 41676138).

Compliance with ethical standards

All animal experiments complied with the Chinese Legislation and Shanghai Ocean University Review Committee for the use of animal subjects.

Supplementary material

10695_2018_562_MOESM1_ESM.doc (64 kb)
ESM 1 (DOC 63 kb)

References

  1. Campinho MA, Galay-Burgos M, Sweeney GE, Power DM (2010) Coordination of deiodinase and thyroid hormone receptor expression during the larval to juvenile transition in sea bream (Sparus aurata, Linnaeus). Gen Comp Endocrinol 165:181–194.  https://doi.org/10.1016/j.ygcen.2009.06.020 CrossRefGoogle Scholar
  2. Chawla A, Repa JJ, Evans RM, Mangelsdorf DJ (2001) Nuclear receptors and lipid physiology: opening the x-files. Science 294:1866–1870.  https://doi.org/10.1126/science.294.5548.1866 CrossRefGoogle Scholar
  3. Collery R, Mcloughlin S, Vendrell V, Finnegan J, Crabb JW, Saari JC, Kennedy BN (2008) Duplication and divergence of zebrafish CRALBP genes uncovers novel role for RPE- and Muller-CRALBP in cone vision. Invest Ophthalmol Vis Sci 49:3812–3820Google Scholar
  4. Desvergne B, Wahli W (1999) Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev 20:649–688Google Scholar
  5. Franceschini A et al (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41:D808–D815.  https://doi.org/10.1093/nar/gks1094 CrossRefGoogle Scholar
  6. Fu Y-S, Shi Z-Y, Wang G-Y, Li W-J, Zhang J-L, Jia L (2012) Expression and regulation of miR-1, -133a, -206a, and MRFs by thyroid hormone during larval development in Paralichthys olivaceus. Comp Biochem Physiol B: Biochem Mol Biol 161:226–232.  https://doi.org/10.1016/j.cbpb.2011.11.009 CrossRefGoogle Scholar
  7. Gao X et al (2017) Thyroid hormone receptor beta and NCOA4 regulate terminal erythrocyte differentiation. Proc Natl Acad Sci 114:10107–10112.  https://doi.org/10.1073/pnas.1711058114 CrossRefGoogle Scholar
  8. Guerreiro ACL et al (2014) Daily rhythms in the cyanobacterium Synechococcus elongatus probed by high-resolution mass spectrometry–based proteomics reveals a small defined set of cyclic proteins. Mol Cell Proteomics 13:2042–2055.  https://doi.org/10.1074/mcp.M113.035840 CrossRefGoogle Scholar
  9. Guoliang F, Xiaohong H (2013) Progress on research of functions of glyceraldehyde-3-phosphate dehydrogenase. Acta Biophysica Sinica 29:181–191CrossRefGoogle Scholar
  10. Inui Y, Miwa S (1985) Thyroid hormone induces metamorphosis of flounder larvae. Gen Comp Endocrinol 60:450–454CrossRefGoogle Scholar
  11. Inui Y, Yamano K, Miwa S (1995) The role of thyroid hormone in tissue development in metamorphosing flounder. Aquaculture 135:87–98CrossRefGoogle Scholar
  12. Lee C-H, Olson P, Evans RM (2003) Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 144:2201–2207.  https://doi.org/10.1210/en.2003-0288 CrossRefGoogle Scholar
  13. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408CrossRefGoogle Scholar
  14. Ma S et al (2018) Tandem mass tags labeled quantitative proteomics to study the effect of tobacco smoke exposure on the rat lung. Biochim Biophys Acta 1866:496–506.  https://doi.org/10.1016/j.bbapap.2018.01.002 CrossRefGoogle Scholar
  15. Minami T (1982) The early life history of a flounder Paralichthys olivaceus. Nippon Suisan Gakkaishi 48:1581–1588Google Scholar
  16. Miwa S, Inui Y (1991) Thyroid hormone stimulates the shift of erythrocyte populations during metamorphosis of the flounder. J Exp Zool 259:222–228.  https://doi.org/10.1002/jez.1402590211 CrossRefGoogle Scholar
  17. Miwa S, Tagawa M, Inui Y, Hirano T (1988) Thyroxine surge in metamorphosing flounder larvae. Gen Comp Endocrinol 70:158–163CrossRefGoogle Scholar
  18. Power D et al (2001) Thyroid hormones in growth and development of fish. Comp Biochem Physiol C Toxicol Pharmacol 130:447–459CrossRefGoogle Scholar
  19. Shichida Y, Imai H (1998) Visual pigment: G-protein-coupled receptor for light signals. Cell Mol Life Sci 54:1299–1315.  https://doi.org/10.1007/s000180050256 CrossRefGoogle Scholar
  20. Sinclair J, Timms JF (2011) Quantitative profiling of serum samples using TMT protein labelling, fractionation and LC–MS/MS. Methods 54:361–369.  https://doi.org/10.1016/j.ymeth.2011.03.004 CrossRefGoogle Scholar
  21. Su Y, Fu Y, Zhang H, Shi Z, Zhang J, Gao L (2015) Identification and expression of SRF targeted by miR-133a during early development of Paralichthys olivaceus. Fish Physiol Biochem 41:1093–1104.  https://doi.org/10.1007/s10695-015-0071-8 CrossRefGoogle Scholar
  22. Thompson A et al (2003) Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 75:1895–1904CrossRefGoogle Scholar
  23. Wang DY et al (2005) Gene mutations in retinitis pigmentosa and their clinical implications. Clin Chim Acta 351:5–16.  https://doi.org/10.1016/j.cccn.2004.08.004 CrossRefGoogle Scholar
  24. Xiao H et al (2016) Differential proteomic analysis of human saliva using tandem mass tags quantification for gastric cancer detection. Sci Rep 6:22165.  https://doi.org/10.1038/srep22165 CrossRefGoogle Scholar
  25. Xiao-yu D, Xiu-mei Z, Pei-dong Z (2008) Study on the effect of dissolved oxygen and stocking density on blood cell count and haemoglobin concentration in juvenile Japanese flounder. Marine Fisheries Research 29:40–46Google Scholar
  26. Yamano K, Miwa S, Obinata T, Inui Y (1991) Thyroid hormone regulates developmental changes in muscle during flounder metamorphosis. Gen Comp Endocrinol 81:464–472CrossRefGoogle Scholar
  27. Yamano K, Araki K, Sekikawa K, Inui Y (1994a) Cloning of thyroid hormone receptor genes expressed in metamorphosing flounder. Dev Genet 15:378–382CrossRefGoogle Scholar
  28. Yamano K, Takano-Ohmuro H, Obinata T, Inui Y (1994b) Effect of thyroid hormone on developmental transition of myosin light chains during flounder metamorphosis. Gen Comp Endocrinol 93:321–326CrossRefGoogle Scholar
  29. Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419.  https://doi.org/10.1016/S1350-9462(00)00002-1 CrossRefGoogle Scholar
  30. Yu J, Fu Y, Shi Z (2017) Coordinated expression and regulation of deiodinases and thyroid hormone receptors during metamorphosis in the Japanese flounder (Paralichthys olivaceus). Fish Physiol Biochem 43:321–336.  https://doi.org/10.1007/s10695-016-0289-0 CrossRefGoogle Scholar
  31. Zhang X-H, Rao X-L, Shi H-T, Li R-J, Lu Y-T (2011) Overexpression of a cytosolic glyceraldehyde-3-phosphate dehydrogenase gene OsGAPC3 confers salt tolerance in rice. Plant Cell Tissue Organ Cult 107:1.  https://doi.org/10.1007/s11240-011-9950-6 CrossRefGoogle Scholar
  32. Zhang H-M, Su Y-F, Shi Z-Y, Fu Y-S (2014) cDNA clone and expression analysis of α-Tropomyosin during Japanese flounder (Paralichthys olivaceus) metamorphosis. Zool Res 35:307–312.  https://doi.org/10.13918/j.issn.2095-8137.2014.4.307 Google Scholar
  33. Zhang H, Fu Y, Shi Z, Su Y, Zhang J (2016) miR-17 is involved in Japanese Flounder (Paralichthys olivaceus) development by targeting the Cdc42 mRNA. Comp Biochem Physiol B: Biochem Mol Biol 191:163–170.  https://doi.org/10.1016/j.cbpb.2015.10.005 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Jie Yu
    • 1
    • 2
    • 3
  • Yuanshuai Fu
    • 1
    • 2
    • 3
  • Suping Liu
    • 1
    • 2
    • 3
  • Zhiyi Shi
    • 1
    • 2
    • 3
    Email author
  1. 1.Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of AgricultureShanghai Ocean UniversityShanghaiChina
  2. 2.Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of EducationShanghai Ocean UniversityShanghaiChina
  3. 3.Shanghai Collaborative Innovation for Aquatic Animal Genetics and BreedingShanghai Ocean UniversityShanghaiChina

Personalised recommendations