iTRAQ-based analysis of 17β-estradiol induced proteome in Chinese tongue sole <italic style="font-style: italic">Cynoglossus semilaevis</italic>

Ying ZHU; Yangzhen LI; Hailong LI; Lei WANG; Ning ZHANG; Yang LIU; Liang MENG; Xiwen XU; Zhongdian DONG; Min WEI; Hua GUO; Zhongkai CUI; Xihong LI; Changwei SHAO; Wenteng XU

doi:10.1007/s00343-019-8222-x

Your Location：

Home >

Browse articles >

iTRAQ-based analysis of 17β-estradiol induced proteome in Chinese tongue sole Cynoglossus semilaevis

Biology | Updated：2023-05-20

- iTRAQ-based analysis of 17β-estradiol induced proteome in Chinese tongue sole Cynoglossus semilaevis
- Journal of Oceanology and Limnology Vol. 37, Issue 5, Pages: 1659-1668(2019)
- Affiliations：
  
  1.Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
  2.Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
  3.Research Institute of Metabolic Disease, Qingdao University, Qingdao 266003, China
- Author bio：
  
  XU Wenteng, xuwt@ysfri.ac.cn
- Funds：
- DOI：10.1007/s00343-019-8222-x
  CLC：
- Received：31 August 2018，
  
  Accepted：21 November 2018，
  
  Online First：07 January 2019，
  
  Published：2019-09
- Accepted：
Scan QR Code
Ying ZHU, Yangzhen LI, Hailong LI, et al. iTRAQ-based analysis of 17β-estradiol induced proteome in Chinese tongue sole Cynoglossus semilaevis[J]. Journal of Oceanology and Limnology, 2019, 37(5): 1659-1668.
DOI：

Ying ZHU, Yangzhen LI, Hailong LI, et al. iTRAQ-based analysis of 17β-estradiol induced proteome in Chinese tongue sole Cynoglossus semilaevis[J]. Journal of Oceanology and Limnology, 2019, 37(5): 1659-1668. DOI： 10.1007/s00343-019-8222-x.

摘要

Abstract

The phenomenon of sex dimorphism prevails among many fish species. It has attracted the general research interest due to its close relationship to fish growth and thus aquaculture productivity. In Chinese tongue sole (

Cynoglossus semilaevis

)

17β-estradiol (E2) can be used reportedly to induce the feminization of fish

although the detailed regulatory network remained elusive. We treated the tongue sole fry before sex differentiation with E2 (10 and 30 μg/L) to identify potential targets of E2 in Chinese tongue sole. The E2 treatment indeed induced genetic male fish sex-reversal to phenotypic female. Using an iTRAQ-based comparative proteomic analysis

409 proteins that differentially expressed after E2 induction were identified

including 259 up-regulated and 150 down-regulated proteins. Furthermore

19 differentially expressed proteins identified in the comparative proteomic analysis were selected to assess their transcription and eight of them exhibited the same tendency. Functions of the eight proteins included mainly nucleotide and protein binding. Interestingly

a far upstream element-binding protein 3-like isoform exhibited the significant upregulation both at transcription and translation levels after E2 treatment. This work identified a set of candidate proteins for E2 response and deepened our understanding of E2 regulatory mechanism.

关键词

Keywords

references

Baarends W M, Hoogerbrugge J W, Roest H P, Ooms M, Vreeburg J, Hoeijmakers J H J, Grootegoed J A. 1999.Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Developmental Biology, 207(2):322-333, https://doi.org/10.1006/dbio.1998.9155.

Beardmore J A, Mair G C, Lewis R I. 2001. Monosex male production in finfish as exemplified by tilapia:applications, problems, and prospects. Aquaculture, 197(1-4):283-301, https://doi.org/10.1016/S0044-8486(01)00590-7.

Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2):248-254, https://doi.org/10.1016/0003-2697(76)90527-3.

Casciola-Rosen L A, Miller D K, Anhalt G J, Rosen A. 1994.Specific cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. The Journal of Biological Chemistry, 269(49):30 757-30 760.

Chen S L, Ji X S, Shao C W, Li W L, Yang J F, Liang Z, Liao X L, Xu G B, Xu Y, Song W T. 2012. Induction of mitogynogenetic diploids and identification of WW superfemale using sex-specific SSR markers in half-smooth tongue sole ( Cynoglossus semilaevis ). Marine Biotechnology, 14(1):120-128, https://doi.org/10.1007/s10126-011-9395-2..

Chen S L, Li J, Deng S P, Tian Y S, Wang Q Y, Zhuang Z M, Sha Z X, Xu J Y. 2007. Isolation of female-specific AFLP markers and molecular identification of genetic sex in half-smooth tongue sole ( Cynoglossus semilaevis ).Marine Biotechnology, 9(2):273-280, https://doi.org/10.1007/s10126-006-6081-x..

Chen S L, Zhang G J, Shao C W, Huang Q F, Liu G, Zhang P, Song W T, An N, Chalopin D, Volff J N, Hong Y H, Li Q Y, Sha Z X, Zhou H L, Xie M S, Yu Q L, Liu Y, Xiang H, Wang N, Wu K, Yang C G, Zhou Q, Liao X L, Yang L F, Hu Q M, Zhang J L, Meng L, Jin L J, Tian Y S, Lian J M, Yang J F, Miao G D, Liu S S, Liang Z, Yan F, Li Y Z, Sun B, Zhang H, Zhang J, Zhu Y, Du M, Zhao Y F, Schartl M, Tang Q S, Wang J. 2014. Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nature Genetics, 46(3):253-260, https://doi.org/10.1038/ng.2890.

Choi C Y, Habibi H R. 2003. Molecular cloning of estrogen receptor α and expression pattern of estrogen receptor subtypes in male and female goldfish. Molecular and Cellular Endocrinology, 204(1-2):169-177, https://doi.org/10.1016/S0303-7207(02)00182-X.

Cholia R P, Nayyar H, Kumar R, Mantha A K. 2015.Understanding the multifaceted role of ectonucleotide pyrophosphatase/phosphodiesterase 2 (ENPP2) and its altered behaviour in human diseases. Current Molecular Medicine, 15(10):932-943, https://doi.org/10.2174/1566524015666150921104804.

Cui Z K, Liu Y, Wang W W, Wang Q, Zhang N, Lin F, Wang N, Shao C W, Dong Z D, Li Y Z, Yang Y M, Hu M Z, Li H L, Gao F T, Wei Z F, Meng L, Liu Y, Wei M, Zhu Y, Guo H, Cheng C H K, Schartl M, Chen S L. 2017. Genome editing reveals dmrt1 as an essential male sex-determining gene in Chinese tongue sole ( Cynoglossus semilaevis ). Scientific Reports, 7:42 213, https://doi.org/10.1038/srep42213..

Felty Q. 2011. Proteomic 2D DIGE profiling of human vascular endothelial cells exposed to environmentally relevant concentration of endocrine disruptor PCB153 and physiological concentration of 17β-estradiol. Cell Biology and Toxicology, 27(1):49-68, https://doi.org/10.1007/s10565-010-9170-6.

Feswick A, Isaacs M, Biales A, Flick R W, Bencic D C, Wang R L, Vulpe C, Brown-Augustine M, Loguinov A, Falciani F, Antczak P, Herbert J, Brown L, Denslow N D, Kroll K J, Lavelle C, Dang V, Escalon L, Garcia-Reyero N, Martyniuk C J, Munkittrick K R. 2017. How consistent are we? Interlaboratory comparison study in fathead minnows using the model estrogen 17α-ethinylestradiol to develop recommendations for environmental transcriptomics.Environmental Toxicology and Chemistry, 36(10):2 614-2 623, https://doi.org/10.1002/etc.3799.

Frisca F, Colquhoun D, Goldshmit Y, Änkö M L, Pébay A, Kaslin J. 2016. Role of ectonucleotide pyrophosphatase/phosphodiesterase 2 in the midline axis formation of zebrafish. Scientific Reports, 6:37 678, https://doi.org/10.1038/srep37678.

George S, Gubbins M, MacIntosh A, Reynolds W, Sabine V, Scott A, Thain J. 2004. A comparison of pollutant biomarker responses with transcriptional responses in European flounders ( Platicthys flesus ) subjected to estuarine pollution. Marine Environmental Research, 58(2-5):571-575, https://doi.org/10.1016/j.marenvres.2004.03.047..

Hall J M, Couse J F, Korach K S. 2001. The multifaceted mechanisms of estradiol and estrogen receptor signaling.The Journal of Biological Chemistry, 276(40):36 869-36 872, https://doi.org/10.1074/jbc.R100029200.

Han D, Haunerland N H, Williams T D. 2009. Variation in yolk precursor receptor mRNA expression is a key determinant of reproductive phenotype in the zebra finch ( Taeniopygia guttata ). Journal of Experimental Biology, 212(9):1 277-1 283, https://doi.org/10.1242/jeb.026906..

Hawkins M B, Thornton J W, Crews D, Skipper J K, Dotte A, Thomas P. 2000. Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. Proceedings of the National Academy of Sciences of the United States of America, 97(20):10 751-10 756, https://doi.org/10.1073/pnas.97.20.10751.

Hock R, Furusawa T, Ueda T, Bustin M. 2007. HMG chromosomal proteins in development and disease. Trends in Cell Biology, 17(2):72-79, https://doi.org/10.1016/j.tcb.2006.12.001.

Hu Q M, Chen S L. 2013. Cloning, genomic structure and expression analysis of ubc9 in the course of development in the half-smooth tongue sole ( Cynoglossus semilaevis ). Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 165(3):181-188, https://doi.org/10.1016/j.cbpb.2013.03.007..

Ibarz A, Pinto P I S, Power D M. 2013. Proteomic approach to skin regeneration in a marine teleost:modulation by oestradiol-17β. Marine Biotechnology (NY), 15(6):629-646, https://doi.org/10.1007/s10126-013-9513-4.

Jia W Y, Yao Z Y, Zhao J J, Guan Q B, Gao L. 2017. New perspectives of physiological and pathological functions of nucleolin (NCL). Life Sciences, 186:1-10, https://doi.org/10.1016/j.lfs.2017.07.025.

Khieokhajonkhet A, Kaneko G, Hirano Y, Wang L, Ushio H. 2016. Different effects of growth hormone and fasting on the induction patterns of two hormone-sensitive lipase genes in red seabream Pagrus major . General and Comparative Endocrinology, 236:121-130, https://doi.org/10.1016/j.ygcen.2016.06.025..

Klein S L, Marriott I, Fish E N. 2015. Sex-based differences in immune function and responses to vaccination.Transactions of the Royal Society of Tropical Medicine and Hygiene, 109(1):9-15, https://doi.org/10.1093/trstmh/tru167.

Kobayashi H, Iwamatsu T. 2005. Sex reversal in the medaka Oryzias latipes by brief exposure of early embryos to estradiol-17β. Zoological Science, 22(10):1 163-1 167, https://doi.org/10.2108/zsj.22.1163..

Leelatanawit R, Sittikankeaw K, Yocawibun P, Klinbunga S, Roytrakul S, Aoki T, Hirono I, Menasveta P. 2009.Identification, characterization and expression of sexrelated genes in testes of the giant tiger shrimp Penaeus monodon . Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 152(1):66-76, https://doi.org/10.1016/j.cbpa.2008.09.004..

Li H L, Xu W T, Zhang N, Shao C W, Zhu Y, Dong Z D, Wang N, Jia X D, Xu H, Chen S L. 2016. Two Figla homologues have disparate functions during sex differentiation in halfsmooth tongue sole ( Cynoglossus semilaevis ). Scientific Reports, 6:28 219, https://doi.org/10.1038/srep28219..

Li Z J, Yang L J, Wang J, Shi W C, Pawar R A, Liu Y M, Xu C G, Cong W H, Hu Q R, Lu T Y, Xia F, Guo W, Zhao M, Zhang Y Y. 2010. β-Actin is a useful internal control for tissue-specific gene expression studies using quantitative real-time PCR in the half-smooth tongue sole Cynoglossus semilaevis challenged with LPS or Vibrio anguillarum . Fish & Shellfish Immunology, 29(1):89-93, https://doi.org/10.1016/j.fsi.2010.02.021..

Ma C H, Dong K W, Yu K L. 2000. cDNA cloning and expression of a novel estrogen receptor β-subtype in goldfish ( Carassius auratus ). Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 1490(1-2):145-152, https://doi.org/10.1016/S0167-4781(99)00235-3..

Martyniuk C J, Kroll K J, Doperalski N J, Barber D S, Denslow N D. 2010. Environmentally relevant exposure to 17α-ethinylestradiol affects the telencephalic proteome of male fathead minnows. Aquatic Toxicology, 98(4):344-353, https://doi.org/10.1016/j.aquatox.2010.03.007.

Melamed P, Koh M, Preklathan P, Bei L, Hew C. 2002.Multiple mechanisms for Pitx-1 transactivation of a luteinizing hormone β subunit gene. The Journal of Biological Chemistry, 277:26 200-26 207, https://doi.org/10.1074/jbc.M201605200.

Nagler J J, Cavileer T, Sullivan J, Cyr D G, Rexroad Ⅲ C. 2007. The complete nuclear estrogen receptor family in the rainbow trout:discovery of the novel ERα2 and both ERβ isoforms. Gene, 392(1-2):164-173, https://doi.org/10.1016/j.gene.2006.12.030..

Nagler J J, Davis T L, Modi N, Vijayan M M, Schultz I. 2010.Intracellular, not membrane, estrogen receptors control vitellogenin synthesis in the rainbow trout. General and Comparative Endocrinology, 167(1):326-330, https://doi.org/10.1016/j.ygcen.2010.03.022.

Palin S L, McTernan P G, Anderson L A, Sturdee D W, Barnett A H, Kumar S. 2003. 17β-estradiol and anti-estrogen ICI:compound 182, 780 regulate expression of lipoprotein lipase and hormone-sensitive lipase in isolated subcutaneous abdominal adipocytes. Metabolism, 52(4):383-388, https://doi.org/10.1053/meta.2003.50088.

Pinto P I S, Estêvão M D, Power D M. 2014. Effects of estrogens and estrogenic disrupting compounds on fish mineralized tissues. Marine Drugs, 12(8):4 474-4 494, https://doi.org/10.3390/md12084474.

Schilling J, Nepomuceno A I, Planchart A, Yoder J A, Kelly R M, Muddiman D C, Daniels H V, Hiramatsu N, Reading B J. 2015. Machine learning reveals sex-specific 17β-estradiol-responsive expression patterns in white perch ( Morone americana ) plasma proteins. Proteomics, 15(15):2 678-2 690, https://doi.org/10.1002/pmic.201400606..

Shao C W, Bao B L, Xie Z Y, Chen X Y, Li B, Jia X D, Yao Q L, Ortí G, Li W H, Li X H, Hamre K, Xu J, Wang L, Chen F Y, Tian Y S, Schreiber A M, Wang N, Wei F, Zhang J L, Dong Z D, Gao L, Gai J W, Sakamoto T, Mo S D, Chen W J, Shi Q, Li H, Xiu Y J, Li Y Z, Xu W T, Shi Z Y, Zhang G J, Power D M, Wang Q Y, Schartl M, Chen S L. 2017. The genome and transcriptome of Japanese flounder provide insights into flatfish asymmetry. Nature Genetics, 49(1):119-124, https://doi.org/10.1038/ng.3732.

Shao C W, Li Q Y, Chen S L, Zhang P, Lian J M, Hu Q M, Sun B, Jin L J, Liu S S, Wang Z J, Zhao H M, Jin Z H, Liang Z, Li Y Z, Zheng Q M, Zhang Y, Wang J, Zhang G J. 2014.Epigenetic modification and inheritance in sexual reversal of fish. Genome Research, 24(4):604-615, https://doi.org/10.1101/gr.162172.113.

Sun A, Wang T Z, Wang N, Liu X F, Sha Z X, Chen S L. 2015.Establishment and characterization of an ovarian cell line from half-smooth tongue sole Cynoglossus semilaevis . Journal of Fish Biology, 86(1):46-59, https://doi.org/10.1111/jfb.12535..

Sun J, Yang Z, Xiao P Z, Liu Y, Ji H, Du Z Y, Chen L Q. 2017.Two isoforms of hormone-sensitive lipase b are generated by alternative exons usage and transcriptional regulation by insulin in grass carp ( Ctenopharyngodon idella ). Fish Physiology and Biochemistry, 43(2):539-547, https://doi.org/10.1007/s10695-016-0308-1..

Tang R Y, Dodd A, Lai D, McNabb W C, Love D R. 2007.Validation of zebrafish ( Danio rerio ) reference genes for quantitative real-time RT-PCR normalization. Acta Biochimica et Biophysica Sinica, 39(5):384-390, https://doi.org/10.1111/j.1745-7270.2007.00283.x..

Tewari M, Beidler D R, Dixit V M. 1995. CrmA-inhibitable cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein during Fas-and tumor necrosis factor-induced apoptosis. The Journal of Biological Chemistry, 270(32):18 738-18 741, https://doi.org/10.1074/jbc.270.32.18738.

Thomas P. 2012. Rapid steroid hormone actions initiated at the cell surface and the receptors that mediate them with an emphasis on recent progress in fish models. General and Comparative Endocrinology, 175(3):367-383, https://doi.org/10.1016/j.ygcen.2011.11.032.

Wang D, Mao H L, Chen H X, Liu H Q, Gui J F. 2009. Isolation of Y-and X-linked SCAR markers in yellow catfish and application in the production of all-male populations.Animal Genetics, 40(6):978-981, https://doi.org/10.1111/j.1365-2052.2009.01941.x.

West K L, Ito Y, Birger Y, Postnikov Y, Shirakawa H, Bustin M. 2001. HMGN3a and HMGN3b, two protein isoforms with a tissue-specific expression pattern, expand the cellular repertoire of nucleosome-binding proteins. The Journal of Biological Chemistry, 276(28):25 959-25 969, https://doi.org/10.1074/jbc.M101692200.

Xu W T, Li H L, Dong Z D, Cui Z K, Zhang N, Meng L, Zhu Y, Liu Y, Li Y Z, Guo H, Ma J L, Wei Z F, Zhang N W, Yang Y M, Chen S L. 2016. Ubiquitin ligase gene neurl3 plays a role in spermatogenesis of half-smooth tongue sole ( Cynoglossus semilaevis ) by regulating testis protein ubiquitination. Gene, 592(1):215-220, https://doi.org/10.1016/j.gene.2016.07.062..

Yaşar P, Ayaz G, Muyan M. 2016. Estradiol-Estrogen receptor α mediates the expression of the CXXC5 gene through the estrogen response element-dependent signaling pathway.Scientific Reports, 6:37 808, https://doi.org/10.1038/srep37808.

Yoneda M, Kurita Y, Kitagawa D, Ito M, Tomiyama T, Goto T, Takahashi K. 2007. Age validation and growth variability of Japanese flounder Paralichthys olivaceus off the Pacific coast of northern Japan. Fisheries Science, 73(3):585-592, https://doi.org/10.1111/j.1444-2906.2007.01371.x..

Zhang B, Wang X L, Sha Z X, Yang C G, Liu S S, Wang N, Chen S L. 2011. Establishment and characterization of a testicular cell line from the half-smooth tongue sole, Cynoglossus semilaevis . International Journal of Biological Sciences, 7(4):452-459, https://doi.org/10.7150/ijbs.7.452..

Zhang J, Chen Q M. 2012. Far upstream element binding protein 1:a commander of transcription, translation and beyond. Oncogene, 32(24):2 907-2 916, https://doi.org/10.1038/onc.2012.350.

Zhang X Y, Liu H J. 2009. Effects of 17 β -Estradiol on sex differentiation and growth in half-smooth tongue-sole( Cynoglossus semilaevis ). Journal of Northeast Agricultural University, 40(6):67-72. (in Chinese with English abstract)..

Zhu Y, Hu Q M, Xu W T, Li H L, Guo H, Meng L, Wei M, Lu S, Shao C W, Wang N, Yang G P, Chen S L. 2017.Identification and analysis of the β-catenin1 gene in halfsmooth tongue sole ( Cynoglossus semilaevis ). PLoS One, 12(5):e0176122, https://doi.org/10.1371/journal.pone.0176122..

Zupanc G K H, Ilieş I, Sîrbulescu R F, Zupanc M M. 2014.Large-scale identification of proteins involved in the development of a sexually dimorphic behavior. Journal of Neurophysiology, 111(8):1 646-1 654, https://doi.org/10.1152/jn.00750.2013.

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

Recovery of gonadal development in tiger puffer Takifugu rubripes after exposure to 17β-estradiol during early life stages

Effect of fasting on protein metabolism in muscle tissue of Larimichthys crocea revealed by transcriptome and proteome

Establishment and characterization of a new cell line derived from half-smooth tongue sole Cynoglossus semilaevis kidney

Isolation, characterization and expression analysis of TRPV4 in half-smooth tongue sole Cynoglossus semilaevis

Genome-wide identification and prediction of long noncoding RNAs in half-smooth tongue sole Cynoglossus semilaevis

Related Author

Peng Hu

Bin Liu

Zhen Meng

Xinfu Liu

Yudong Jia

Zhi Yang

Jilin Lei

Weiliang SHEN

Related Institution

Tianyuan Aquaculture Co. Ltd. of Yantai Economic Development Zone

Municipal Key Laboratory of Marine Fish Breeding and Biotechnology Yellow Sea Fisheries Research Institute Chinese Academy of Fishery Sciences

Key Laboratory of Mariculture of Ministry of Education Ocean University of China

Ningbo Institute of Marine and Fisheries

School of Life Science, Taizhou University

Address：Editorial Office of JOL, 88 Haijun Rd. Qingdao, 266000, China
Tel：+86-532-82898754 Email：jol@qdio.ac.cn
Technical support is provided by Beijing Founder electronics co., LTD 京ICP备09064830号-19 京公网安备11010802024621
It is recommended to read the content of this site in Chrome&IE9+. Please switch to extreme mode in browser 360.
Cookies We use cookies to help provide and enhance our service and tailor content. By continuing, you agree to the use of cookies.

⁰

iTRAQ-based analysis of 17β-estradiol induced proteome in Chinese tongue sole Cynoglossus semilaevis

DOI：10.1007/s00343-019-8222-x

摘要

Abstract

关键词

Keywords

references