Skip to main content
SpringerLink
Log in

Characterization and Transcriptional Response of Ecdysone Receptor Gene in the Mud Crab Macrophthalmus japonicus: Effects of Osmotic Stress and Endocrine Disrupting Chemicals

  • Article
  • Published:
Ocean Science Journal Aims and scope Submit manuscript

Abstract

The ecdysone receptor (EcR) induces hormonal pathways by binding ecdysteroids to other nuclear receptors for development, reproduction, and molting processes. To further understand the role of EcR in polluted environments, we characterized EcR and assessed the transcriptional responses of the EcR gene to osmotic stress, and to endocrine disrupting chemicals (EDCs) such as bisphenol A (BPA) and di-(2-ethylhexyl) phthalate (DEHP) in the intertidal mud crab Macrophthalmus japonicus. Phylogenetic analysis showed that the ligand binding domain of M. japonicus EcR formed two different clusters among crab species. Osmotic stress prompted different expression patterns of EcR mRNA in M. japonicus crabs under low and high salinities. BPA exposure induced significant up-regulation of EcR as early as day 1 in M. japonicus gills and hepatopancreas. However, the expression levels of EcR returned to similar, or lower, levels as controls, by days 4 and 7. In contrast, EcR mRNA expression was significantly induced in M. japonicus gills and hepatopancreas exposed to most of the DEHP concentrations over all exposure times. Hepatopancreatic tissue is more sensitive than gill tissue in terms of EcR gene responses to EDCs. Taken together, these results suggest that the role of EcR in endocrine protection may involve different processes according to the type of EDCs and up-regulatory responses of the EcR transcript could be used as an indicator for detecting changes in hormonal systems caused by environmental stressors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Al-Mohanna SY, Nott JA (1987) R-cells and the digestive cycle in Penaeus semisulcatus, (Crustacea: Decapoda). Mar Biol 95:129–137

    Google Scholar 

  • Belfroid A, van Velzen M, van der Horst B, Vethaak D (2002) Occurrence of bisphenol A in surface water and uptake in fish: evaluation of field measurements. Chemosphere 49:97–103

    Google Scholar 

  • Brander SM (2013) Thinking outside the box: assessing endocrine disruption in aquatic life. In: Ajuha S (ed) Monitoring water quality: Pollution assessment, analysis, and remediation. Elsevier, Amsterdam, pp 103–147

    Google Scholar 

  • Cerkvenik-Flajs V, Fonda I, Gombač M (2018) Analysis and occurrence of bisphenol A in mediterranean mussels (Mytilus galloprovincialis) sampled from the Slovenian Coastal Waters of the North Adriatic Sea. B Environ Contam Tox 101:439–445

    Google Scholar 

  • Chand BK, Trivedi RK, Dubey SK, Rout SK, Beg MM, Das UK (2015) Effect of salinity on survival and growth of giant freshwater prawn Macrobrachium rosenbergii, (de Man). Aquac Res 2:26–33

    Google Scholar 

  • Chen JC, Chia PG (1997) Osmotic and ionic concentrations of Scylla serrata (Forskal) subjected to different salinity levels. Comp Biochem Phys A 117:239–244

    Google Scholar 

  • Chen YF, Ai CX, Lin QW, Shen YH (2007) Effect of salinity stress on the activities of phenoloxidase and superoxide dismutase of the serum, tissue and organ of mud crab, Scylla serrate. J Oceanogr 26:569–575 (in Chinese)

    Google Scholar 

  • Chen X, Wang J, Yue W, Huang S, Chen J, Chen Y, Wang C (2017) Structure and function of the alternatively spliced isoforms of the ecdysone receptor gene in the Chinese mitten crab, Eriocheir sinensis. Sci Rep 7:12993. doi:https://doi.org/10.1038/s41598-017-13474-1

    Google Scholar 

  • Chung AC, Durica DS, Clifton SW, Roe BA, Hopkins PM (1998) Cloning of crustacean ecdysteroid receptor and retinoid-X receptor gene homologs and elevation of retinoid-X receptor mRNA by retinoic acid. Mol Cell Endocrinol 139:209–227

    Google Scholar 

  • Girish BP, Swetha CH, Reddy PS (2015) Induction of ecdysteroidogenesis, methyl farnesoate synthesis and expression of ecdysteroid receptor and retinoid X receptor in the hepatopancreas and ovary of the giant mud crab, Scylla serrata by melatonin. Gen Comp Endocr 217–218:37–42

    Google Scholar 

  • Colin A, Bach C, Rosin C, Munoz JF, Dauchy X (2014) Is drinking water a major route of human exposure to alkylphenol and bisphenol contaminants in France? Arch Environ Con Tox 66:86–99

    Google Scholar 

  • Goff AD, Saranjampour P, Ryan LM, Hladik ML, Covi JA, Armbrust KL, Brander SM (2017) The effects of fipronil and the photodegradation product fipronil desulfinyl on growth and gene expression in juvenile blue crabs, Callinectes sapidus, at different salinities. Aquat Toxicol 186:96–104

    Google Scholar 

  • Gong J, Ye H, Xie Y, Yang Y, Huang H, Li S, Zeng C (2015) Ecdysone receptor in the mud crab Scylla paramamosain: A possible role in promoting ovarian development. J Endocrinol 224:273–287

    Google Scholar 

  • Gong J, Huang C, Shu L, Bao C, Huang H, Ye H, Zeng C, Li S (2016) The retinoid X receptor from mud crab: new insights into its roles in ovarian development and related signaling pathway. Sci Rep 6:23654. doi:https://doi.org/10.1038/srep23654

    Google Scholar 

  • Herrero Ó, Morcillo G, Planelló R (2017) Transcriptional deregulation of genetic biomarkers in Chironomus riparius larvae exposed to ecologically relevant concentrations of di (2-ethylhexyl) phthalate (DEHP). PLoS One 12:e0171719. doi:https://doi.org/10.1371/journal.pone.0171719

    Google Scholar 

  • Herrero Ó, Aquilino M, Sánchez-Argüello P, Planelló R (2018) The BPA-substitute bisphenol S alters the transcription of genes related to endocrine, stress response and biotransformation pathways in the aquatic midge Chironomus riparius (Diptera, Chironomidae). PLoS One 13:e0193387. doi:https://doi.org/10.1371/journal.pone.0193387

    Google Scholar 

  • Kim HW, Lee SG, Mykles DL (2005) Ecdysteroid-responsive genes, RXR and E75, in the tropical land crab, Gecarcinus lateralis: differential tissue expression of multiple RXR isoforms generated at three alternative splicing sites in the hinge and ligand-binding domains. Mol Cell Endocrinol 242:80–95

    Google Scholar 

  • Kitaura J, Nishida M, Wada K (2002) Genetic and behavioral diversity in the Macrophthalmus japonicus species complex (Crustacea: Brachyura: Ocypodidae). Mar Biol 140:1–8

    Google Scholar 

  • LeBlanc GA (2007) Crustacean endocrine toxicity: A review. Ecotoxicology 16:61–81

    Google Scholar 

  • Li X, Yin P, Zhao L (2016) Phthalate esters in water and surface sediments of the Pearl River Estuary: Distribution, ecological, and human health risks. Environ Sci Pollut R 23:1–9

    Google Scholar 

  • Liu W, Xie Y, Ma J, Luo X, Nie P, Zuo Z, Lahrmann U, Zhao Q, Zheng Y, Zhao Y, Xue Y, Ren J (2015) IBS: An illustrator for the presentation and visualization of biological sequences. Bioinformatics 31:3359–3361

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−ΔΔct method. Methods 25:402–408

    Google Scholar 

  • Long X, Wu X, Zhao L, Ye H, Cheng Y, Zeng C (2017) Effects of salinity on gonadal development, osmoregulation and metabolism of adult male Chinese mitten crab, Eriocheir sinensis. PLoS One 12:e0179036. doi:https://doi.org/10.1371/journal.pone.0179036

    Google Scholar 

  • Lu JY, Shu MA, Xu BP, Liu GX, Ma YZ, Guo XL, Liu Y (2015) Mud crab Scylla paramamosain, glutamate dehydrogenase: Molecular cloning, tissue expression and response to hyposmotic stress. Fish Sci 81:175–186

    Google Scholar 

  • Ma T, Zhou W, Chen L, Wu L, Christie P, Zhang H, Luo Y (2017) Toxicity effects of di-(2-ethylhexyl) phthalate to Eisenia fetida at enzyme, cellular and genetic levels. PLoS One 12:e0173957. doi:https://doi.org/10.1371/journal.pone.0173957

    Google Scholar 

  • Martínez-Paz P, Morales M, Urien J, Morcillo G, Martínez-Guitarte JL (2017) Endocrine-related genes are altered by antibacterial agent triclosan in Chironomus riparius aquatic larvae. Ecotox Environ Safe 140:185–190

    Google Scholar 

  • Medwid S, Guan H, Yang K (2019) Bisphenol A stimulates steroidogenic acute regulatory protein expression via an unknown mechanism in adrenal cortical cells. J Cell Biochem 120:2429–2438

    Google Scholar 

  • Mu X, LeBlanc GA (2002) Environmental antiecdysteroids alter embryo development in the crustacean Daphnia magna. J Exp Zool 292:287–292

    Google Scholar 

  • Nakagawa Y, Henrich VC (2009) Arthropod nuclear receptors and their role in molting. FEBS J 276:6128–6157

    Google Scholar 

  • Nair PM, Choi J (2012) Modulation in the mRNA expression of ecdysone receptor gene in aquatic midge, Chironomus riparius upon exposure to nonylphenol and silver nanoparticles. Environ Toxicol Phar 33:98–106

    Google Scholar 

  • Nikapitiya C, Kim WS, Park K, Kwak IS (2014) Identification of potential markers and sensitive tissues for low or high salinity stress in an intertidal mud crab (Macrophthalmus japonicus). Fish Shellfish Immun 41:407–416

    Google Scholar 

  • Nikapitiya C, Kim WS, Park K, Kim J, Lee MO, Kwak IS (2015) Chitinase gene responses and tissue sensitivity in an intertidal mud crab (Macrophthalmus japonicus) following low or high salinity stress. Cell Stress Chaperon 20:517–526

    Google Scholar 

  • Park K, Kwak IS (2008) Characterization of heat shock protein 40 and 90 in Chironomus riparius larvae: effects of di (2-ethylhexyl) phthalate exposure on gene expressions and mouthpart deformities. Chemosphere 74:89–95

    Google Scholar 

  • Park K, Kwak IS (2013) Expression of stress response HSP70 gene in Asian paddle crabs, Charybdis japonica, exposure to endocrine disrupting chemicals, bisphenol A (BPA) and 4-nonylphenol (NP). Ocean Sci J 48:207–214

    Google Scholar 

  • Park K, Kwak IS (2014) The effect of temperature gradients on endocrine signaling and antioxidant gene expression during Chironomus riparius development. Sci Total Environ 470–471:1003–1011

    Google Scholar 

  • Park K, Kwak TS, Kwak IS (2014) Vitellogenin gene characterization and expression of Asian paddle crabs (Charybdis japonica) following endocrine disrupting chemicals. Ocean Sci J 49:207–214

    Google Scholar 

  • Park K, Nikapitiya C, Kwak TS, Kwak IS (2015) Antioxidativerelated genes expression following perfluorooctane sulfonate (PFOS) exposure in the intertidal mud crab, Macrophthalmus japonicus. Ocean Sci J 50:547–556

    Google Scholar 

  • Park K, Nikapitiya C, Kim WS, Kwak TS, Kwak IS (2016a) Changes of exoskeleton surface roughness and expression of crucial participation genes for chitin formation and digestion in the mud crab (Macrophthalmus japonicus) following the antifouling biocide irgarol. Ecotox Environ Safe 132:186–195

    Google Scholar 

  • Park K, Nikapitiya C, Kwak IS (2016b) Identification and expression of proteolysis-response genes for Macrophthalmus japonicus exposure to irgarol toxicity. Ann Limnol-Int J Lim 52:65–74

    Google Scholar 

  • Park K, Kwak IS (2018) Disrupting effects of antibiotic sulfathiazole on developmental process during sensitive life-cycle stage of Chironomus riparius. Chemosphere 190:25–34

    Google Scholar 

  • Péqueux A (1995) Osmotic regulation in crustaceans. J Crustacean Biol 15:1–60

    Google Scholar 

  • Romano N, Zeng C (2011) Importance of balanced Na+/K+ ratios for blue swimmer crabs, Portunus pelagicus, to cope with elevated ammonia- N and differences between in vitro and in vivo gill Na+/K+-ATPase responses. Aquaculture 318:154–161

    Google Scholar 

  • Sang HM, Fotedar R (2004) Growth, survival, haemolymph osmolality and organosomatic indices of the western king prawn (Penaeus latisulcatus, Kishinouye, 1896) reared at different salinities. Aquaculture 234:601–614

    Google Scholar 

  • Segner H, Caroll K, Fenske M, Janssen CR, Maack G, Pascoe D, Schäfers C, Vandenbergh GF, Watts M, Wenzel A (2003) Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: Report from the European IDEA project. Ecotox Environ Safe 54:302–314

    Google Scholar 

  • Shinji J, Wilder MN (2012) Dynamics of free amino acids in the hemolymph of Pacific whiteleg shrimp Litopenaeus vannamei, exposed to different types of stress. Fish Sci 78:1187–1194

    Google Scholar 

  • Techa S, Alvarez JV, Sook Chung J (2015) Changes in ecdysteroid levels and expression patterns of ecdysteroid-responsive factors and neuropeptide hormones during the embryogenesis of the blue crab, Callinectes sapidus. Gen Comp Endocr 214:157–166

    Google Scholar 

  • Verhaegen Y, Parmentier K, Swevers L, Renders E, Rougé P, De Coen W, Cooreman K, Smagghe G (2011) The heterodimeric ecdysteroid receptor complex in the brown shrimp Crangon crangon: EcR and RXR isoform characteristics and sensitivity towards the marine pollutant tributyltin. Gen Comp Endocr 172:158–169

    Google Scholar 

  • Wang H, Wei H, Tang L, Lu J, Mu C, Wang C (2018a) Identification and characterization of miRNAs in the gills of the mud crab (Scylla paramamosain) in response to a sudden drop in salinity. BMC Genomics 19:609. doi:https://doi.org/10.1186/s12864-018-4981-6

    Google Scholar 

  • Wang S, Zhu Z, He J, Yue X, Pan J, Wang Z (2018b) Steroidal and phenolic endocrine disrupting chemicals (EDCs) in surface water of Bahe River, China: distribution, bioaccumulation, risk assessment and estrogenic effect on Hemiculter leucisculus. Environ Pollut 243:103–114

    Google Scholar 

  • Wang Y, Wang T, Ban Y, Shen C, Shen Q, Chai X, Zhao W, Wei J (2018c) Di-(2-ethylhexyl) Phthalate exposure modulates antioxidant enzyme activity and gene expression in juvenile and adult Daphnia magna. Arch Environ Con Tox 75:145–156

    Google Scholar 

  • Wang H, Wei H, Tang L, Lu J, Mu C, Wang C (2018d) A proteomics of gills approach to understanding salinity adaptation of Scylla paramamosain. Gene 677:119–131

    Google Scholar 

  • Wu X, Hopkins PM, Palli SR, Durica DS (2004) Crustacean retinoid-X receptor isoforms: distinctive DNA binding and receptor–receptor interaction with a cognate ecdysteroid receptor. Mol Cell Endocrinol 218:21–38

    Google Scholar 

  • Wu M, Wang L, Xu G, Liu N, Tang L, Zheng J, Bu T, Lei B (2013) Seasonal and spatial distribution of 4-tert-octylphenol, 4-nonylphenol and bisphenolA in the Huangpu River and its tributaries, Shanghai, China. Environ Monit Assess 185:3149–3161

    Google Scholar 

  • Yamazaki E, Yamashita N, Taniyasu S, Lam J, Lam PK, Moon HB, Jeong Y, Kannan P, Achyuthan H, Munuswamy N, Kannan K (2015) Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China, Korea and India. Ecotox Environ Safe 122:565–572

    Google Scholar 

  • Zhang D, Liu J, Qi T, Ge B, Liu Q, Jiang S, Zhang H, Wang Z, Ding G, Tang B (2018a) Comparative transcriptome analysis of Eriocheir japonica sinensis response to environmental salinity. PLoS One 13:e0203280. doi:https://doi.org/10.1371/journal.pone.0203280

    Google Scholar 

  • Zhang L, Hu Y, Sun W, Chen S, Jia X, Cai W (2018b) Transcriptomic responses of Nile tilapia (Oreochromis niloticus) liver to environmental concentration of di (2-ethylhexyl)phthalate. Ecotox Environ Safe 165:70–77

    Google Scholar 

Download references

Acknowledgements

This study was supported by the National Research Foundation of Korea, which is funded by the Korean Government [NRF-2018-R1A6A1A-03024314] and [NRF- 2019-R1I1A1A-01056855].

Author information

Authors and Affiliations

  1. Fisheries Science Institute, Chonnam National University, Yeosu, 59626, South Korea

    Kiyun Park & Ihn-Sil Kwak

  2. School of Marine Technology, Chonnam National University, Yeosu, 59626, South Korea

    Won-Seok Kim & Ihn-Sil Kwak

Authors
  1. Kiyun Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Won-Seok Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ihn-Sil Kwak
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ihn-Sil Kwak.

Additional information

Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Park, K., Kim, WS. & Kwak, IS. Characterization and Transcriptional Response of Ecdysone Receptor Gene in the Mud Crab Macrophthalmus japonicus: Effects of Osmotic Stress and Endocrine Disrupting Chemicals. Ocean Sci. J. 54, 611–620 (2019). https://doi.org/10.1007/s12601-019-0029-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12601-019-0029-3

Keywords

Search

Navigation