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Time-dependent Effects of Bisphenol Analogs on Ecdysteroid Pathway Related Genes in the Brackish Water Flea Diaphanosoma celebensis

Bisphenol 구조 유사체가 기수산 물벼룩 Ecdysteroid 경로에 미치는 영향

  • In, Soyeon (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Lee, Young-Mi (Department of Biotechnology, College of Convergence Engineering, Sangmyung University)
  • 인소연 (상명대학교 융합공과대학 생명공학과) ;
  • 이영미 (상명대학교 융합공과대학 생명공학과)
  • Received : 2021.07.28
  • Accepted : 2021.09.02
  • Published : 2021.12.15

Abstract

Bisphenol A is a representative endocrine disruptor and continuously detected in aquatic environment due to wide use, resulting in adverse effects on growth, development, and reproduction in diverse organisms as well as human. Structural analogs have been developed to substitute BPA are also suspected to have endocrine disrupting effects. In the present study, the time-dependent expression patterns of ecdysteroid synthesis (nvd, cyp314a1), receptors (EcRA, EcRB, USP, ERR), and downstream signaling pathway - related genes (HR3, E75, Vtg, VtgR) were investigated using quantitative real time reverse transcription polymerase chain reaction (qRT-PCR) in the brackish water flea Diaphanosoma celebensis exposed to Bisphenol analogs (BPs; BPA, BPF, and BPS) for 6, 12, and 24 h. As results, the expression of nvd, cyp314a1, EcRs, USP, ERR and E75 mRNA was upregulated at 6 h exposure to BPF, which is earlier than BPA and BPS (12 h). On the other hand, HR3, E75 and VtgR mRNA levels were elevated at 6 h earlier at BPS and BPF than at BPA (12 h), but Vtg mRNA level was slightly changed within 24 h. These findings suggest that like BPA, BPF and BPS can also modulate the transcription of ecdysteroid pathway - related genes with different mechanisms, and have a potential as endocrine disruptors. This study will provide a better understanding the molecular mode of action of bisphenols on ecdysteroid pathway in the brackish water flea.

비스페놀A(BPA)는 대표적인 내분비계 교란물질로 광범위한 사용으로 인해 환경 내에서 지속적으로 검출됨에 따라 인간을 비롯한 다양한 생물에서 성장, 발생, 생식 등에 유해한 영향을 미치는 것으로 알려져 있다. 따라서 BPA를 대체하기 위한 구조 유사체들이 개발되어 널리 사용되고 있으나 이러한 대체제들이 내분비계 교란 작용을 갖는지에 대한 연구가 필요하다. 본 연구에서는 BPA와 그 구조 유사체인 BPS와 BPF에 노출시킨 기수산 물벼룩 Diaphanosoma celebensis에서 탈피과정에 관여하는 ecdysteroid 합성(nvd, cyp314a1), receptors (EcRA, EcRB, USP, ERR), 그리고 하위 경로에 있는 유전자(HR3, E75, Vtg, VtgR)의 시간 별 발현 변화를 조사하였다. nvd와 cyp314a1 유전자의 발현은 BPA 보다 BPF에서 6시간 일찍 발현이 증가하는 양상을 보인 반면, BPS의 경우에는 이들 유전자의 발현이 24시간 내내 감소하는 양상을 보였다. BPA와 BPF 노출 시 EcR 유전자들의 발현 양상도 이와 유사한 경향을 보였다. ERR 유전자의 발현은 BPF와 BPS에서 BPA 보다 6시간 일찍 발현이 증가하는 양상을 보였고, HR3, E75, VtgR의 유전자 발현도 노출군에서 시간 차이는 있지만 유의하게 증가하는 양상을 보였다. 반면 Vtg는 24시간 이내에서는 크게 증가하지는 않았다. 이러한 결과는 BPA 뿐 아니라 BPF와 BPS도 탈피에 관여하는 호르몬의 합성 및 조절 경로의 유전자의 발현을 조절할 수 있으며, 서로 다른 기전으로 기수산 물벼룩의 내분비계를 교란시킬 수 있는 능력을 갖는다고 볼 수 있다. 본 연구는 비스페놀 구조 유사체가 기수산 물벼룩의 탈피과정에 관여하는 분자 경로 어떻게 영향을 미치는지를 이해하는데 도움이 될 것이다.

Keywords

References

  1. Andersen HR, Wollenberger L, Halling-Sorensen B, Kusk KO. 2001. Development of copepod nauplii to copepodites - a parameter for chronic toxicity including endocrine disruption. Environ Toxicol Chem 20: 2821-2829. https://doi.org/10.1897/1551-5028(2001)020<2821:DOCNTC>2.0.CO;2
  2. Bae C, Kim RO, Kim JS, Lee YM. 2018. Acute Toxicity and Modulation of an Antioxidant Defence System in the Brackish Water Flea Diaphanosoma celebensis Exposed to Cadmium and Copper. Toxicol Environ Health Sci 10: 186-193. https://doi.org/10.1007/s13530-018-0363-3
  3. Bardet PL, Laudet V, Vanacker JM. 2006. Studying non-mammalian models? Not a fool's ERRand! Trends Endocrinol Metab 17: 166-171. https://doi.org/10.1016/j.tem.2006.03.005
  4. Beausoleil C, Emond C, Cravedi JP, Antignac JP, Applanat M, Appenzeller BMR, Beaudouin R, Belzunces LP, Canivenc-Lavier MC, Chevalier N, Chevrier C, Elefant E, Eustache F, Habert R, Kolf-Clauw M, Le Magueresse-Battistoni B, Mhaouty-Kodja S, Minier C, Multigner L, Schroeder H, Thonneau P, Viguie C, Pouzaud F, Ormsby JN, Rousselle C, Verines-Jouin L, Pasquier E, Michel C. 2018. Regulatory identification of BPA as an endocrine disruptor: Context and methodology. Mol Cell Endocrinol 475: 4-9. https://doi.org/10.1016/j.mce.2018.02.001
  5. Cabaton N, Dumont C, Severin I, Perdu E, Zalko D, Cherkaoui-Malki M, Chagnon MC. 2009. Genotoxic and endocrine activities of bis(hydroxyphenyl)methane (bisphenol F) and its derivatives in the HepG2 cell line. Toxicology 255: 15-24. https://doi.org/10.1016/j.tox.2008.09.024
  6. Canesi L, Fabbri E. 2015. Environmental effects of BPA: Focus on aquatic species. Dose Response 13: 1-14.
  7. Chen D, Kannan K, Tan H, Zheng Z, Feng YL, Wu Y, Widelka M. 2016. Bisphenol analogues other than BPA: Environmental occurrence, human exposure, and toxicity - A review. Environ Sci Technol 50: 5438-5453. https://doi.org/10.1021/acs.est.5b05387
  8. Ghekiere A, Verslycke T, Janssen C. 2006. Effects of methoprene, nonylphenol, and estrone on the vitellogenesis of the mysid Neomysis integer. Gen Comp Endocrinol 147: 190-195. https://doi.org/10.1016/j.ygcen.2005.12.021
  9. Gismondi E. 2018. Identification of molt-inhibiting hormone and ecdysteroid receptor cDNA sequences in Gammarus pulex, and variations after endocrine disruptor exposures. Ecotoxicol Environ Saf 158: 9-17. https://doi.org/10.1016/j.ecoenv.2018.04.017
  10. Hannas BR, LeBlanc GA. 2010. Expression and ecdysteroid responsiveness of the nuclear receptors HR3 and E75 in the crustacean Daphnia magna. Mol Cell Endocrinol 315: 208-218. https://doi.org/10.1016/j.mce.2009.07.013
  11. Hannas BR, Wang YH, Thomson S, Kwon G, Li H, LeBlanc GA. 2011. Regulation and dysregulation of vitellogenin mRNA accumulation in daphnids (Daphnia magna). Aquat Toxicol 101: 351-357. https://doi.org/10.1016/j.aquatox.2010.11.006
  12. Hayward A, Takahashi T, Bendena WG, Tobe SS, Hui JHL. 2010. Comparative genomic and phylogenetic analysis of vitellogenin and other large lipid transfer proteins in metazoans. FEBS Letters 584: 1273-1278. https://doi.org/10.1016/j.febslet.2010.02.056
  13. Herrero O, Aquilino M, Scanchez-Arguello P, Planello 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. https://doi.org/10.1371/journal.pone.0193387.
  14. Hwang DS, Han J, Won EJ, Kim DK, Jeong CB, Hwang UK, Zhou B, Choe J, Lee JS. 2016. BDE-47 causes developmental retardation with downregulated expression profiles of ecdysteroid signaling pathway-involved nuclear receptor (NR) genes in the copepod Tigriopus japonicus. Aquat Toxicol 177: 285-294. https://doi.org/10.1016/j.aquatox.2016.06.004
  15. In S, Cho H, Lee KW, Won EJ, Lee YM. 2020. Cloning and molecular characterization of estrogen-related receptor (ERR) and vitellogenin genes in the brackish water flea Diaphanosoma celebensis exposed to bisphenol A and its structural analogues. Mar Pollut Bullet 154: 111063. https://doi.org/10.1016/j.marpolbul.2020.111063
  16. In S, Cho H, Lee YM. 2021. Identification of ecdysteroid pathwayrelated genes and their transcriptional modulation in the brackish water flea Diaphanosoma celebensis exposed to bisphenol analogs. Toxicol Environ Health Sci 13: 261-268. https://doi.org/10.1007/s13530-021-00103-8
  17. In S, Yoon HW, Yoo JW, Cho H, Kim RO, Lee YM. 2019. Acute toxicity of bisphenol A and its structural analogues and transcriptional modulation of the ecdysone-mediated pathway in the brackish water flea Diaphanosoma celebensis. Ecotoxicol Environ Saf 179: 310-317. https://doi.org/10.1016/j.ecoenv.2019.04.065
  18. Jin W, Jia Y, Tan E, Xi G. 2017. Relevance of estrogen-related receptor gene and ecdysone receptor gene in adult testis of the cricket Teleogryllus emma (Orthoptera: Gryllidae). Sci Nat 104: 97. https://doi.org/10.1007/s00114-017-1518-9
  19. Kim BM, Kang S, Kim RO, Jung JH, Lee KW, Rhee JS, Lee YM. 2018. De novo transcriptome assembly of brackish water flea Diaphanosoma celebensis based on short-term cadmium and benzo[a]pyrene exposure experiments. Hereditas 155: 36. https://doi.org/10.1186/s41065-018-0075-3
  20. Lafont R, Dauphin-Villemant C, Warren JT, Rees H. 2005. Ecdysteroid chemistry and biochemistry. In: Gilbert LI, Iatrou K, Gill S. (Eds.), Comprehensive Molecular Insect Science, vol. 3. Elsevier, Oxford, pp 125-195.
  21. Lafont R, Mathieu M. 2007. Steroids in aquatic invertebrates. Ecotoxicology 16: 109-130. https://doi.org/10.1007/s10646-006-0113-1
  22. Laudet V. 1997. Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor. J Mol Endocrinol 19: 207-226. https://doi.org/10.1677/jme.0.0190207
  23. Liao C, Liu F, Moon H-B, Yamashita N, Yun S, Kannan K. 2012. Bisphenol analogues in sediments from industrialized areas in the United States, Japan, and Korea: spatial and temporal distributions. Environ Sci Technol 46: 11558-11565. https://doi.org/10.1021/es303191g
  24. Marcial HS, Hagiwara A. 2007. Multigenerational effects of 17b-estradiol and nonylphenol on euryhaline cladoceran Diaphanosoma celebensis. Fish Sci 73: 324-330. https://doi.org/10.1111/j.1444-2906.2007.01338.x
  25. Miyakawa H, Sato T, Song Y, Tollefsen KE, Iguchi T. 2018. Ecdysteroid and juvenile hormone biosynthesis, receptors and their signaling in the freshwater microcrustacean Daphnia. J Steroid Biochem Mol Biol 184: 62-68. https://doi.org/10.1016/j.jsbmb.2017.12.006
  26. Morales M, Martinez-Paz P, Martin R, Planello R, Urien J, Martinez-Guitarte JL, Morcillo G. 2014. Transcriptional changes induced by in vivo exposure to pentachlorophenol (PCP) in Chironomus riparius (Diptera) aquatic larvae. Aquat Toxicol 157: 1-9. https://doi.org/10.1016/j.aquatox.2014.09.009
  27. Naderi M, Wong MY, Gholami F. 2014. Developmental exposure of zebrafish (Danio rerio) to bisphenol-S impairs subsequent reproduction potential and hormonal balance in adults. Aquat Toxicol 148: 195-203. https://doi.org/10.1016/j.aquatox.2014.01.009
  28. Nagasawa K, Treen N, Kondo R, Otoki Y, Itoh N, Rotchell JM, Osada M. 2015. Molecular characterization of an estrogen receptor and estrogen-related receptor and their autoregulatory capabilities in two Mytilus species. Gene 564: 153-159. https://doi.org/10.1016/j.gene.2015.03.073
  29. Nair PMG, 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 Pharmacol 33: 98-106. https://doi.org/10.1016/j.etap.2011.09.006
  30. Nakagawa Y, Henrich VC. 2009. Arthropod nuclear receptors and their role in molting. FEBS J 276: 6128-6157. https://doi.org/10.1111/j.1742-4658.2009.07347.x
  31. Park K, Kwak I-S. 2010. Molecular effects of endocrine-disrupting chemicals on the Chironomus riparius estrogen-related receptor gene. Chemosphere 79: 934-941. https://doi.org/10.1016/j.chemosphere.2010.03.002
  32. Planello R, Martinez-Guitarte JL, Morcillo G. 2008. The endocrine disruptor bisphenol A increases the expression of HSP70 and ecdysone receptor genes in the aquatic larvae of Chironomus riparius. Chemosphere 71: 1870-1876. https://doi.org/10.1016/j.chemosphere.2008.01.033
  33. Rochester JR, Bolden AL. 2015. Bisphenol S and F: A systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ Health Perspect 123: 643-650. https://doi.org/10.1289/ehp.1408989
  34. Roth Z, Khalaila I. 2012. Identification and characterization of the vitellogenin receptor in Macrobrachium rosenbergii and its expression during vitellogenesis. Mol Reprod Dev 79: 478-487. https://doi.org/10.1002/mrd.22055
  35. Segner H, Caroll K, Genske M, Janssen CR, Maack G, Pascoe D, Schafers C, Vandenbergh GF, Watts M, Wenzel A. 2003. Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotoxicol Environ Saf 54: 302-314. https://doi.org/10.1016/S0147-6513(02)00039-8
  36. Sumiya E, Ogino Y, Miyakawa H, Hiruta C, Toyota K, Miyagawa S, Iguchi T. 2014. Roles of ecdysteroids for progression of reproductive cycle in the fresh water crustacean Daphnia magna. Front Zool 11: 60. https://doi.org/10.1186/s12983-014-0060-2
  37. Sumiya E, Ogino Y, Toyota K, Miyakawa H, Miyagawa S, Iguchi T. 2016. Neverland regulates embryonic moltings through the regulation of ecdysteroid synthesis in the water flea Daphnia magna, and may thus act as a target for chemical disruption of molting. J Appl Toxicol 36: 1476-1485. https://doi.org/10.1002/jat.3306
  38. Talbot WS, Swyryd EA, Hogness DS. 1993. Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73: 1323-1337. https://doi.org/10.1016/0092-8674(93)90359-X
  39. Won EJ, Kim D, Yoo JW, In S, Shin KH, Lee YM. 2021. Oxidative stress responses in brackish water flea exposed to microcystin-LR and algal bloom waters from Nakdong River, Republic of Korea. Mar Pollut Bull 162: 111868. https://doi.org/10.1016/j.marpolbul.2020.111868
  40. Yao TP, Forman BM, Jiang Z, Cherbas L, Chen JD, McKeown M, Cherbas P, Evans RM. 1993. Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366: 476-479. https://doi.org/10.1038/366476a0
  41. Yoo JW, Cho H, Lee KW, Won EJ, Lee YM. 2021. Combined effects of heavy metals (Cd, As, and Pb): Comparative study using conceptual models and the antioxidant responses in the brackish water flea. Comp Biochem Physiol Part C 239: 108863. https://doi.org/10.1016/j.cbpc.2020.108863
  42. Zhong L, Yuan L, Rao Y, Li Z, Zhang X, Liao T, Xu Y, Dai H. 2014. Distribution of vitellogenin in zebrafish (Danio rerio) tissues for biomarker analysis. Aquat Toxicol 149: 1-7. https://doi.org/10.1016/j.aquatox.2014.01.022
  43. Zhu J, Chen L, Sun G, Raikhel AS. 2006. The competence factor βFtz-F1 potentiates ecdysone receptor activity via recruiting a p160/SRC coactivator. Mol Cell Biol 26: 9402-9412. https://doi.org/10.1128/MCB.01318-06