DOI QR코드

DOI QR Code

Modulation of antioxidant defense system in the brackish water flea Diaphanosoma celebensis exposed to bisphenol A

비스페놀 A에 대한 기수산 물벼룩의 항산화 시스템의 변화

  • Yoo, Jewon (Department of Life Science, College of Natural Sciences, Sangmyung University) ;
  • Cha, Jooseon (Department of Life Science, College of Natural Sciences, Sangmyung University) ;
  • Kim, Hyeri (Department of Life Science, College of Natural Sciences, Sangmyung University) ;
  • Pyo, Jinwoo (Department of Life Science, College of Natural Sciences, Sangmyung University) ;
  • Lee, Young-Mi (Department of Life Science, College of Natural Sciences, Sangmyung University)
  • 유제원 (상명대학교 자연과학대학 생명과학과) ;
  • 차주선 (상명대학교 자연과학대학 생명과학과) ;
  • 김혜리 (상명대학교 자연과학대학 생명과학과) ;
  • 표진우 (상명대학교 자연과학대학 생명과학과) ;
  • 이영미 (상명대학교 자연과학대학 생명과학과)
  • Received : 2019.02.22
  • Accepted : 2019.03.12
  • Published : 2019.03.31

Abstract

Bisphenol A (BPA), a representative endocrine disrupting chemicals, has adverse effects on growth, development and reproduction in aquatic organisms. The object of this study was to investigate the modulation of antioxidant enzyme-coding genes using quantitative real time RT-PCR (qRT-PCR), enzyme activity and total protein content, to understand oxidative stress responses after exposure to BPA for 48 h in brackish water flea Diaphanosoma celebensis. The BPA ($3mg\;L^{-1}$) significantly upregulated the expression of Cu/Zn-SOD, Mn-SOD, and catalase (CAT) mRNA. Three GST isoforms (GST-kappa, GST-mu, and GST-theta) mRNA levels significantly increased at the rate of $0.12mg\;L^{-1}$ of BPA. In particular, GST-mu showed the highest expression level, indicating its key role in antioxidant response to BPA. SOD activity was induced with a concentration-dependent manner, and total protein contents was reduced. These findings indicate that BPA can induce oxidative stress in this species, and these antioxidants may be involved in cellular protection against BPA exposure. This study will provide a better understanding of molecular mode of action of BPA toxicity in aquatic organisms.

Bisphenol A (BPA)는 대표적인 내분비계장애물질로 수서생물의 성장, 발생, 그리고 생식에 유해한 영향을 주는 것으로 알려져 있다. 본 연구는 기수산 물벼룩(Diaphanosoma celebensis)에서 48시간 BPA 노출 후 산화적 스트레스 반응을 조사하기 위하여 qRT-PCR을 이용한 항산화 유전자 발현 변화, 항산화 효소 활성, 총 단백질 함량 분석을 수행하였다. $3mg\;L^{-1}$의 BPA에 48시간 노출된 D. celebensis에서 모든 항산화 유전자(Cu/Zn-SOD, Mn-SOD, CAT)의 발현량이 유의하게 증가하였다. 특히 세 종류의 GST isoforms (GST-kappa, GST-mu, GST-theta)는 가장 낮은 농도인 $0.12mg\;L^{-1}$ BPA에 48시간 노출된 실험군에서도 유의하게 증가하였으며, GST-mu의 발현양이 상대적으로 가장 높게 나타났다. SOD 활성은 BPA 농도에 의존적으로 유의하게 증가하였으며, 총 단백질 함량은 BPA 노출에 대해 감소되는 양상을 보였다. 이러한 결과는 BPA가 D. celebensis에서 산화적 스트레스를 유발하였고, 이 과정에서 이들 항산화 유전자가 생물방어기전으로 참여한다는 것을 의미한다. 본 연구는 BPA가 해양생물에 미치는 영향에 대한 분자적 기전을 이해하는 데 도움이 될 것이다.

Keywords

References

  1. Alexander HC, DC Dill, LW Smith, PD Guiney and P Dorn. 1988. Bisphenol A: Acute aquatic toxicity. Environ. Toxicol. Chem. 7:19-26. https://doi.org/10.1002/etc.5620070104
  2. Atkinson A and D Roy. 1995. In vitro conversion of environmental estrogenic chemical bisphenol -A to DNA binding metabolites. Biochem. Biophys. Res. Commun. 210:424-433. https://doi.org/10.1006/bbrc.1995.1678
  3. Bae C, RO Kim, JS Kim and YM Lee. 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
  4. Barbosa IA, RM Martins, ML Sa e Melo and AMVM Soares. 2003. Acute and chronic toxicity of dimethyl sulfoxide to Daphnia magna. Bull. Environ. Contam. Toxicol. 70:1264-1268. https://doi.org/10.1007/s00128-003-0119-9
  5. Barzilai A and K Yamamoto. 2004. DNA damage responses to oxidative stress. DNA Repair 3:1109-1115. https://doi.org/10.1016/j.dnarep.2004.03.002
  6. Bindhumol V, KC Chitra and PP Mathur. 2003. Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology 188:117-124. https://doi.org/10.1016/S0300-483X(03)00056-8
  7. Blanchette B, X Feng and BR Singh. 2007. Marine glutathione S-transferase. Mar. Biotechnol. 5:513-542. https://doi.org/10.1007/s10126-007-9034-0
  8. Boutet I, A Tanguy and D Moraga. 2004. Characterization and expression of four mRNA sequences encoding glutathione S-transferases pi, mu, omega and sigma classes in the Pacific oyster Crassostrea gigas exposed to hydrocarbons and pesticides. Mar. Biol. 146:53-64. https://doi.org/10.1007/s00227-004-1423-6
  9. Burridge E. 2003. Bisphenol A: product profile. Eur. Chem. News 17:14-20.
  10. 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 - A review. Environ. Sci. Technol. 50:5438-5453. https://doi.org/10.1021/acs.est.5b05387
  11. Chen MY, M Ike and M Fujita. 2002. Acute toxicity, mutagenicity, and estrogenicity of bisphenol-A and other bisphenols. Environ. Toxicol. 17:80-86. https://doi.org/10.1002/tox.10035
  12. Contreras-Vergara CA, C Harris-Valle, RR Sotelo-Mundo and G Yepiz-Plascencia. 2004. A mu-class glutathione S-transferase from the marine shrimp Litopenaeus vannamei: molecular cloning and active-site structural modeling. J. Biochem. Mol. Toxicol. 18:245-252. https://doi.org/10.1002/jbt.20033
  13. Dutta M and G Paul. 2018. Bisphenol A dose- and time -dependently induces oxidative stress in rat liver mitochondria ex vivo. Asian J. Pharm. Clin. Res. 11:98. https://doi.org/10.22159/ajpcr.2018.v11i9.26750
  14. Edori OS, IB Nwoke and ES Edori. 2013. Sublethal effects of diesel on total protein levels and cholesterol in Tympanotonus Fuscatus. J. Appl. Sci. Environ. Manage. 17:21-26.
  15. Eid JI, SM Eissa and AA El-Ghor. 2015. Bisphenol A induces oxidative stress and DNA damage in hepatic tissue of female rat offspring. J. Basic Appl. Zool. 71:10-19. https://doi.org/10.1016/j.jobaz.2015.01.006
  16. Garcia-Espineira MC, LP Tejeda-Benitez and J Olivero-Verbel. 2018. Toxic effects of bisphenol A, propyl paraben, and triclosan on Caenorhabditis elegans. Int. J. Environ. Res. Public Health 15:684. https://doi.org/10.3390/ijerph15040684
  17. Geetharathan T and P Josthna. 2016. Effect of BPA on protein, lipid profile and immuno-histo chemical changes in placenta and uterine tissues of albino rat. Int. J. Pharm. Clin. Res. 8:260-268.
  18. Hassan ZK, MA Elobeid, P Virk, SA Omer, M ElAmin, MH Daghestani and EM AlOlayan. 2012. Bisphenol A induces hepatotoxicity through oxidative stress in rat model. Oxid. Med. Cell. Longev. 2012:194829.
  19. Hejmej A, M Kotula -Balak and B Bilinsk. 2011. Antiandrogenic and estrogenic compounds: Effect on development and function of male reproductive system. Steroids - Clinical Aspect. doi:10.5772/28538
  20. Hwang GS. 2006. Embryotoxicity of bisphenol A in Daphnia magna. J. Environ. Toxicol. 21:81-86.
  21. Inyang IR, ER Daka and EN Ogamba. 2010. Effect of sub-lethal concentrations of diazinon on total protein and transaminase activities in Clarias gariepinus. Curr. Res. J. Biol. Sci. 2:390-395.
  22. Izzotti A, S Kanitz, F D'Agostini, A Camoirano and S De Flora. 2009. Formation of adducts by bisphenol A, an endocrine disruptor, in DNA in vitro and in liver and mammary tissue of mice. Mutat. Res. 679:28-32. https://doi.org/10.1016/j.mrgentox.2009.07.011
  23. Kabuto H, S Hasuike, N Minagawa and T Shishibori. 2003. Effects of bisphenol A on the metabolisms of active oxygen species in mouse tissues. Environ. Res. 93:31-35. https://doi.org/10.1016/S0013-9351(03)00062-8
  24. Kang JH, D Aasi and Y Katayama. 2007. Bisphenol A in the aquatic environment and its endocrine-disruptive effects on aquatic organisms. Crit. Rev. Toxicol. 37:607-625. https://doi.org/10.1080/10408440701493103
  25. Kaya O and B Kaptaner. 2016. Antioxidant defense system parameters in isolated fish hepatocytes exposed to bisphenol A - Effect of vitamin C. Acta Biol. Hung. 67:225-235. https://doi.org/10.1556/018.67.2016.3.1
  26. Ke C, X Liu, H Zuo, J Zhao, X Yang and J Yuan. 2013. The oxidative damage of Bisphenol A on the organs of the mice. Health 5:1190-1194. https://doi.org/10.4236/health.2013.57160
  27. Khim JS, K Kannan, DL Villeneuve, CH Koh and JP Giesy. 1999. Characterization and distribution of trace organic contaminants in sediment from Masan Bay, Korea. 1. Instrumental analysis. Environ. Sci. Technol. 33:4199-4205. https://doi.org/10.1021/es9904484
  28. 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 155:36. https://doi.org/10.1186/s41065-018-0075-3
  29. Kim H, BR Yim, CH Bae and YM Lee. 2017. Acute toxicity and antioxidant responses in the water flea Daphnia magna to xenobiotics (cadmium, lead, mercury, bisphenol A, and 4-nonylphenol). Toxicol. Environ. Health Sci. 9:41-49. https://doi.org/10.1007/s13530-017-0302-8
  30. Kim H, JS Kim, PJ Kim, EJ Won and YM Lee. 2018. Response of antioxidant enzymes to Cd and Pb exposure in water flea Daphnia magna: Differential metal and age-Specific patterns. Comp. Biochem. Physiol. C 209:28-36.
  31. Kim RO, H Kim and YM Lee. 2019. Evaluation of 4-nonylphenol and bisphenol A toxicity using multiple molecular biomarkers in the water flea Daphnia magna. Ecotoxicology 28:167-174. https://doi.org/10.1007/s10646-018-2009-2
  32. Kitamura S, T Suzuki, S Sanoh, R Kohta, N Jinno, K Sugihara, S Yoshihara, N Fujimoto, H Watanabe and S Ohta. 2005. Comparative study of the endocrine-disrupting activity of bisphenol A and 19 related compounds. Toxicol. Sci. 84:249-259. https://doi.org/10.1093/toxsci/kfi074
  33. Lee JS and S Raisuddin. 2008. Modulation of expression of oxidative stress genes of the intertidal copepod Tigriopus japonicus after exposure to environmental chemicals. pp. 95-105. In Interdisciplinary Studies on Environmental Chemistry- Biological Responses to Chemical Pollutants (Murakami et al. eds.). TERRAPUB, Tokyo.
  34. Liao C, F Liu, HB Moon, N Yamashita, S Yun and K Kannan. 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
  35. Livak KJ and TD Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) Method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  36. Mandich A, S Bottero, E Benfenati, A Cevasco, C Erratico, S Maggioni, A Massari, F Pedemonte and L Vigano. 2007. In vivo exposure of carp to graded concentrations of bisphenol A. Gen. Comp. Endocrinol. 153:15-24. https://doi.org/10.1016/j.ygcen.2007.01.004
  37. Manoj K. 1999. Mercury, copper and cadmium induced changes in the total protein levels in muscle tissue of an edible estuarine fish Boleophthalmus dussumieri (Cuv). J. Environ. Biol. 20:231-234.
  38. Marcial HS and A Hagiwara. 2007. Multigenerational effects of 17${\beta}$-estradiol and nonylphenol on euryhaline cladoceran Diaphanosoma celebensis. Fish. Sci. 73:324-330. https://doi.org/10.1111/j.1444-2906.2007.01338.x
  39. Miller AF. 2012. Superoxide dismutases: ancient enzymes and new insights. FEBS Lett. 586:585-595. https://doi.org/10.1016/j.febslet.2011.10.048
  40. Mu X, CV Rider, GS Hwang, H Hoy and GA LeBlanc. 2005. Covert signal disruption: anti-ecdysteroidal activity of bisphenol A involves cross talk between signaling pathways. Environ. Toxicol. Chem. 24: 146-152. https://doi.org/10.1897/04-063R.1
  41. Myrnes B and IW Nilsen. 2007. Glutathione S-transferase from the Icelandic scallop (Chlamys islandica): isolation and partial characterization. Comp. Biochem. Physiol. 144C:403-407.
  42. Nomura Y, N Mitsui, UK Bhawal, M Sawajiri, O Tooi, T Takahashi and M Okazaki. 2006. Estrogenic activity of phthalate esters by In Vitro VTG assay using primary-cultured Xenopus Hepatocytes. Dent. Mater. J. 25:533-537. https://doi.org/10.4012/dmj.25.533
  43. Nunomura A, RJ Castellani, X Zhu, PI Moreira, G Perry and MA Smith. 2006. Involvement of oxidative stress in Alzheimer disease. J. Neuropathol. Exp. Neurol. 65:631-641. https://doi.org/10.1097/01.jnen.0000228136.58062.bf
  44. Oehlmann J, U Schulte-Oehlmann, M Tillmann and B Markert. 2000. Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part I: Bisphenol A and octylphenol as xeno-estrogens. Ecotoxicology 9:383-397. https://doi.org/10.1023/A:1008972518019
  45. Oehlmann J, U Schulte -Oehlmann, W Kloas, O Jagnytsch, I Lutz, KO Kusk, L Wollenberger, EM Santos, GC Paull, KJ Van Look and CR Tyler. 2009. A critical analysis of the biological impacts of plasticizers on wildlife. Philos. Trans. R. Soc. B-Biol. Sci. 364:2047-2062. https://doi.org/10.1098/rstb.2008.0242
  46. Park JC, DH Kim, MC Lee, J Han, HJ Kim, A Hagiwara, UK Hwang, HG Park and JS Lee. 2018a. Genome-wide identification of the entire 90 glutathione S-transferase (GST) subfamily genes in four rotifer Brachionus species and transcriptional modulation in response to endocrine disrupting chemicals. Comp. Biochem. Physiol. D 28:183-195.
  47. Park JC, MC Lee, DS Yoon, J Han, M Kim, UK Hwang, JH Jung and JS Lee. 2018b. Effects of bisphenol A and its analogs bisphenol F and S on life parameters, antioxidant system, and response of defensome in the marine rotifer Brachionus koreanus. Aquat. Toxicol. 199:21-29. https://doi.org/10.1016/j.aquatox.2018.03.024
  48. Park JC, MC Lee, DS Yoon, J Han, HG Park, UK Hwang and JS Lee. 2019. Genome-wide identification and expression of the entire 52 glutathione S-transferase (GST) subfamily genes in the $Cu^{2+}$-exposed marine copepods Tigriopus japonicus and Paracyclopina nana. Aquat. Toxicol. 209:56-69. https://doi.org/10.1016/j.aquatox.2019.01.020
  49. Peng YQ, MJ Wang, HG Chen, JH Chen, H Gao and HH Huang. 2018. Immunological responses in haemolymph and histologic changes in the hepatopancreas of Charybdis japonica (A. Milne-Edwards, 1861) (Decapoda: Brachyura: Portunidae) exposed to bisphenol A. J. Crust. Biol. 38:489-496. https://doi.org/10.1093/jcbiol/ruy046
  50. Pinto S, VN Sato, EA De-Souza, RC Ferraz, H Camara, APF Pinca, DR Mazzotti, MT Lovci, G Tonon, CM Lopes-Ramos, RB Parmigiani, M Wurtele, KB Massirer and MA Mori. 2018. Enoxacin extends lifespan of C. elegans by inhibiting miR-34-5p and promoting mitohormesis. Redox Biol. 18:84-92. https://doi.org/10.1016/j.redox.2018.06.006
  51. Regoli F, GB Principato, E Bertoli, M Nigro and E Orlando. 1997. Biochemical characterization of the antioxidant system in the scallop Adamussium colbecki, a sentinel organism for monitoring the Antarctic environment. Polar Biol. 17:251-258. https://doi.org/10.1007/s003000050129
  52. Rhee JS, S Raisuddin, DS Hwang, T Horiguchi, HS Cho and JS Lee. 2008. A Mu-class glutathione S-transferase (GSTM) from the rock shell Thais clavigera. Comp. Biochem. Physiol. C 148:195-203.
  53. Sajiki J and J Yonekubo. 2003. Leaching of bisphenol A (BPA) to seawater from polycarbonate plastic and its degradation by reactive oxygen species. Chemosphere 51:55-62. https://doi.org/10.1016/S0045-6535(02)00789-0
  54. Squier TC. 2001. Oxidative stress and protein aggregation during biological aging. Exp. Gerontol. 36:1539-1550. https://doi.org/10.1016/S0531-5565(01)00139-5
  55. Staples CA, PB Dome, GM Klecka, ST Oblock and LR Harris. 1998. A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere 36:2149-2173. https://doi.org/10.1016/S0045-6535(97)10133-3
  56. Strange RC, MA Spiteri, S Ramachandran and AA Fryer. 2001. Glutathione S-transferase family of enzymes. Mutat. Res. 482:21-26. https://doi.org/10.1016/S0027-5107(01)00206-8
  57. Tan L, S Wang, Y Wang, M He and D Liu. 2015. Bisphenol A exposure accelerated the aging process in the nematode Caenorhabditis elegans. Toxicol. Lett. 235:75-83. https://doi.org/10.1016/j.toxlet.2015.03.010
  58. Valavanidis A, T Vlahogianni, M Dassenakis and M Scoullos. 2006. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol. Environ. Saf. 64:178-189. https://doi.org/10.1016/j.ecoenv.2005.03.013
  59. Yokota H, H Iwano, M Endo, T Kobayashi, H Inoue, S Ikushiro and A Yuasa. 1999. Glucuronidation of the environmental oestrogen bisphenol A by an isoform of UDP-lucuronosyltransferase, UGT2B1, in the rat liver. Biochem. J. 340:405-409. https://doi.org/10.1042/bj3400405