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Identification and molecular characterization of doublesex and mab-3-related transcription factor(dmrt) in brackish water flea, Diaphanosoma celebensis, exposed to bisphenol analogs

  • Cho, Hayoung (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Jeon, Min Jeong (Department of Biotechnology, College of Convergence Engineering, Sangmyung University) ;
  • Lee, Young-Mi (Department of Biotechnology, College of Convergence Engineering, Sangmyung University)
  • Received : 2021.04.12
  • Accepted : 2021.05.13
  • Published : 2021.06.30

Abstract

Doublesex and mab-3 related transcription factor(dmrt) play crucial roles in sex determination and sex differentiation in vertebrates and invertebrates. Although dmrt genes have been identified in vertebrates, little is known about aquatic invertebrates. In this study, two dmrt genes, namely, Dc_dmrt93B and Dc_dmrt99B, were identified from brackish water flea, Diaphanosoma celebensis. Transcriptional changes were observed in the dmrt genes when the flea was exposed to bisphenol(BP), an endocrine disruptor. Sequence and phylogenetic analyses showed that both dmrt genes contained two conserved domains, namely, DM and DMA, closely clustered with those of Daphnia spp. Additionally, a significant increase in the Dc_dmrt99B mRNA expression level was observed upon exposure to intermediate concentrations of BP (bisphenol A>bisphenol S=bisphenol F, p<0.05), while the expression of Dc_dmrt93B mRNA was slightly modulated. These findings imply that the two dmrt genes may be involved in sex differentiation of D. celebensis. Furthermore, it was found that the ability of BP to modulate dmrt genes could affect development and reproduction. This study provides a basis for understanding the function of the dmrt genes and the molecular mode of action of BP in small crustaceans.

Keywords

Acknowledgement

This work was supported by a grant from Sangmyung University(2020) funded to Young-Mi Lee.

References

  1. Bellefroid EJ, L Leclere, A Saulnier, M Keruzore, M Sirakov, M Vervoort and S De Clercq. 2013. Expanding roles for the evolutionarily conserved Dmrt sex transcriptional regulators during embryogenesis. Cell. Mol. Life Sci. 70:3829-3845. https://doi.org/10.1007/s00018-013-1288-2
  2. Beronius A and LN Vandenberg. 2015. Using systematic reviews for hazard and risk assessment of endocrine disrupting chemicals. Rev. Endocr. Metab. Disord. 16:273-287. https://doi.org/10.1007/s11154-016-9334-7
  3. Caballero-Casero N, L Lunar and S Rubio. 2016. Analytical methods for the determination of mixtures of bisphenols and derivatives in human and environmental exposure sources and biological fluids. Anal. Chim. Acta 908:22-53. https://doi.org/10.1016/j.aca.2015.12.034
  4. Canesi L and E Fabbri. 2015. Environmental effects of BPA: focus on aquatic species. Dose-Response 13:1-14.
  5. Chen D, K Kannan, H Tan, Z Zheng, YL Feng, Y Wu and M Widelka. 2016. Bisphenol analogues other than BPA: Environmental occurrence, human exposure, and toxicity. Environ. Sci. Technol. 50:5438-5453. https://doi.org/10.1021/acs.est.5b05387
  6. Drastichova J, Z Svobodova, R Dobikova and V IIabek. 2005. Effect of exposure to bisphenol A and 17β-estradiol on the sex differentiation in zebrafish (Danio rerio). Acta Vet. Brno. 74:278-291.
  7. Hu Y, Q Zhu, X Yan, C Liao and G Jiang. 2019. Occurrence, fate and risk assessment of BPA and its substituents in wastewater treatment plant: A review. Environ. Res. 178:108732. https://doi.org/10.1016/j.envres.2019.108732
  8. Iguchi T, H Watanabe and Y Katsu. 2006. Application of ecotoxicogenomics for studying endocrine disruption in vertebrates and invertebrates. Environ. Health Perspect. 114:101-105. https://doi.org/10.1289/ehp.8061
  9. In S, HW Yoon, JW Yoo, H Cho, RO Kim and YM Lee. 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. Ecotox. Environ. Safe. 179:310-317. https://doi.org/10.1016/j.ecoenv.2019.04.065
  10. In S, H Cho, KW Lee, EJ Won and YM Lee. 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. Bull. 154:111063. https://doi.org/10.1016/j.marpolbul.2020.111063
  11. Kato Y, K Kobayashi, S Oda, JK Colbourn, N Tatarazako, H Watanabe and T Iguchi. 2008. Molecular cloning and sexually dimorphic expression of DM-domain genes in Daphnia magna. Genomics 91:94-101. https://doi.org/10.1016/j.ygeno.2007.09.002
  12. Kato Y, K Kobayashi, H Watanabe and T Iguchi. 2011. Environmental sex determination in the branchiopod crustacean Daphnia magna: Deep conservation of a doublesex gene in the sexdetermining pathway. PLoS Genet. 7:e1001345. https://doi.org/10.1371/journal.pgen.1001345
  13. Kim BM, CB Jeong, IC Kim, JH Yim, YS Lee, JS Rhee and JS Lee. 2014. Identification of three doublesex genes in the monogonont rotifer Brachionus koreanus and their transcriptional responses to environmental stressor-triggered population growth retardation. Comp. Biochem. Physiol. B-Biochem. Mol. Biol. 174:36-44. https://doi.org/10.1016/j.cbpb.2014.05.003
  14. Kim BM, S Kang, RO Kim, JH Jung, KW Lee, JS Rhee and YM Lee. 2018. De novo transcriptome assembly of brackish water flea Diaphanosoma celebensis based on short-term cadmium and benzo[a]pyrene exposure experiments. Hereditas 155:1-7. https://doi.org/10.1186/s41065-017-0036-2
  15. Kim J, Y Kim, S Lee, K Kwak, WJ Chung and K Choi. 2011. Determination of mRNA expression of DMRT93B, vitellogenin, and cuticle 12 in Daphnia magna and their biomarker potential for endocrine disruption. Ecotoxicology 20:1741-1748. https://doi.org/10.1007/s10646-011-0707-0
  16. Kopp A. 2012. Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet. 28:175-184. https://doi.org/10.1016/j.tig.2012.02.002
  17. Lagarde F, C Beausoleil, SM Belcher, LP Belzunces, C Emond, M Guerbet and C Rousselle. 2015. Non-monotonic dose-response relationships and endocrine disruptors: a qualitative method of assessment. Environ. Health 14:1-15. https://doi.org/10.1186/1476-069X-14-1
  18. Lee S, C Liao, GJ Song, K Ra, K Kannan and HB Moon. 2015. Emission of bisphenol analogues including bisphenol A and bisphenol F from wastewater treatment plants in Korea. Chemosphere 119:1000-1006. https://doi.org/10.1016/j.chemosphere.2014.09.011
  19. Liu Y, Z Yan, L Zhang, Z Deng, J Yuan, S Zhang, J Chen and R Guo. 2019. Food up-take and reproduction performance of Daphnia magna under the exposure of Bisphenols. Ecotox. Environ. Safe. 170:47-54. https://doi.org/10.1016/j.ecoenv.2018.11.106
  20. Liu J, L Zhang, G Lu, R Jiang, Z Yan and Y Li. 2021. Occurrence, toxicity and ecological risk of Bisphenol A analogues in aquatic environment - A review. Ecotox. Environ. Safe. 208:111481. https://doi.org/10.1016/j.ecoenv.2020.111481
  21. Marcial HS and A Hagiwara. 2007. Multigenerational effects of 17ss-estradiol and nonylphenol on euryhaline cladoceran Diaphanosoma celebensis. Fish. Sci. 73:324-330. https://doi.org/10.1111/j.1444-2906.2007.01338.x
  22. Mawaribuchi S, Y Ito and M Ito. 2019. Independent evolution for sex determination and differentiation in the DMRT family in animals. Biol. Open 8:bio041962. https://doi.org/10.1242/bio.041962
  23. Meli R, A Monnolo, C Annunziata, C Pirozzi and MC Ferrante. 2020. Oxidative stress and BPA toxicity: An antioxidant approach for male and female reproductive dysfunction. Antioxidants 9:405. https://doi.org/10.3390/antiox9050405
  24. Morales M, M Fuente and R Martin-Folgar. 2020. BPA and its analogues(BPS and BPF) modify the expression of genes involved in the endocrine pathway and apoptosis and a multi drug resistance gene of the aquatic midge Chironomus riparius (Diptera). Environ. Pollut. 265:114806. https://doi.org/10.1016/j.envpol.2020.114806
  25. Naderia M, MYL Wong and F Gholami. 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
  26. Narendra U, L Zhu, B Li, J Wilken and MA Weiss. 2002. Sex-specific gene regulation: The doublesex DM motif is a bipartite DNA-binding domain. J. Biol. Chem. 277:43463-43473. https://doi.org/10.1074/jbc.M204616200
  27. Oehlmann J, U Schulte-Oehlmann, J Bachmann, M Oetken, I Lutz, W Kloas and TA Ternes. 2006. Bisphenol A induces superfeminization in the ramshorn snail Marisa cornuarietis (Gastropoda: Prosobranchia) at environmentally relevant concentrations. Environ. Health Perspect. 114:127-133. https://doi.org/10.1289/ehp.8065
  28. Rhee JS, BM Kim, CJ Lee, YD Yoon, YM Lee and JS Lee. 2011. Bisphenol A modulates expression of sex differentiation genes in the self-fertilizing fish, Kryptolebias marmoratus. Aquat. Toxicol. 104:218-229. https://doi.org/10.1016/j.aquatox.2011.04.020
  29. Ruan T, D Liang, S Song, M Song, H Wang and G Jiang. 2015. Evaluation of the in vitro estrogenicity of emerging bisphenol analogs and their respective estrogenic contributions in municipal sewage sludge in China. Chemosphere 124:150-155. https://doi.org/10.1016/j.chemosphere.2014.12.017
  30. Toyota K, H Miyakawa, C Hiruta, T Sato, H Katayama, T Ohira and T Iguchi. 2021. Sex determination and differentiation in decapod and cladoceran crustaceans: An overview of endocrine regulation. Genes 12:305. https://doi.org/10.3390/genes12020305
  31. Vandenberg LN. 2013. Non-monotonic dose responses in studies of endocrine disrupting chemicals: Bisphenol A as a case study. Dose-Response 12:259-276. https://doi.org/10.2203/dose-response.13-020.Vandenberg
  32. Wang Y, S Jin, H Fu, H Qiao, S Sun, W Zhang, S Jiang, Y Gong, Y Xiong and Y Wu. 2019. Identification and characterization of the DMRT11E gene in the oriental river prawn Macrobrachium nipponense. Int. J. Mol. Sci. 20:1734. https://doi.org/10.3390/ijms20071734
  33. Wu LH, XM Zhang, F Wang, CJ Gao, D Chen, JR Palumbo and EY Zeng. 2018. Occurrence of bisphenol S in the environment and implications for human exposure: A short review. Sci. Total Environ. 615:87-98. https://doi.org/10.1016/j.scitotenv.2017.09.194
  34. Yamazaki E, N Yamashita, S Taniyasu, J Lam, PK Lam, HB Moon, Y Jeong, P Kannan, H Achyuthan, N Munuswamy and K Kannan. 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. https://doi.org/10.1016/j.ecoenv.2015.09.029
  35. Yoo J, J Cha, H Kim, J Pyo and YM Lee. 2019. Modulation of antioxidant defense system in the brackish water flea Diaphanosoma celebensis exposed to bisphenol A. Korean J. Environ. Biol. 37:72-81. https://doi.org/10.11626/KJEB.2019.37.1.072
  36. Yu YQ, WM Ma, QG Zeng, YQ Qian, JS Yang and WJ Yang. 2014. Molecular cloning and sexually dimorphic expression of two Dmrt genes in the giant freshwater prawn, Macrobrachium rosenbergii. Agric. Res. 3:181-191. https://doi.org/10.1007/s40003-014-0106-x
  37. Zhang EF and GF Qiu. 2010. A novel Dmrt gene is specifically expressed in the testis of Chinese mitten crab, Eriocheir sinensis. Dev. Genes Evol. 220:151-159. https://doi.org/10.1007/s00427-010-0336-2
  38. Zhang X, M Hecker, JW Park, AR Tompsett, J Newsted, K Nakayama, PD Jones, D Au, R Kong, RSS Wu and JP Giesy. 2008. Real-time PCR array to study effects of chemicals on the Hypothalamic-Pituitary-Gonadal axis of the Japanese medaka. Aquat. Toxicol. 88:173-182. https://doi.org/10.1016/j.aquatox.2008.04.009
  39. Zhang Y, S Tao, C Yuan, Y Liu and Z Wang. 2016. Non-monotonic dose-response effect of bisphenol A on rare minnow Gobiocypris rarus ovarian development. Chemosphere 144:304-311. https://doi.org/10.1016/j.chemosphere.2015.08.079