Effects of xenostrogen treatment (4-Nonylphenol, Bisphenol A) on vitellogenin expression in juvenile Cyprinus carpio

Document Type : Research Paper

Authors

1 Department of Environmental Sciences, Faculty of Natural Resource and Environment, Malayer University, Hamedan, Iran

2 Department of Environmental Sciences, Faculty of Natural Resource and Marine Science, Tarbiat Modares University, Noor, Mazandaran, Iran

3 Department of Medical Biotechnology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran

Abstract

The aim of this study was to examine some potential effects of 4-Nonylphenol (4-NP), Bisphenol A (BPA), and mixture of them on common carp, Cyprinus carpio and demonstrate induction of vitellogenin (Vtg) as a biomarker for screening aquatic ecosystems. These compounds with other estrogenic chemicals may be responsible for disrupting effects observed in fish. A total of 100 juvenile carp were treated experimentally with 17β-estradiol (E2), and increasing doses of 4-NP, BPA and also mixture of them. Then the plasma Vtg levels were measured using indirect competitive ELISA. Results showed a significant (P<0.05) increase in Vtg levels of exposed carps with E2, maximum 4-NP, BPA and their mixture. The group treated with E2 showed high induction (490%) with respect to controls. The groups treated with maximum dose of 4-NP and BPA showed also induction of Vtg, whereas the group treated with their mixture (3 mg kg−1 b.w. 4-NP and 0.01 mg kg−1 b.w. BPA) showed the highest induction (2126%). Finally, results showed that mixture of 4-NP and BPA exhibited stronger (synergistic) effects. So that, large scale monitoring of estrogenic effects caused by contamination may be considered as a biomarker in urban and industrial effluents.

Keywords

References

Ahel, M, Scully, FE, Hoigné, J & Giger, W 1994, Photochemical degradation of nonylphenol and nonylphenol polyethoxylates in natural waters. Chemosphere, 28: 1361–1368.
Arukwe, A, Celius, T, Walther, BT & Goksøyr, A 2000, Effects of xenoestrogen treatment on zona radiata protein and vitellogenin expression in Atlantic salmon (Salmo salar). Aquatic Toxicology, 49: 159–170.
Arukwe, A, Knudsen, FR & Goksoyr, A 1997, Fish zona radiate (egg shell) protein: A sensibile biomarker for environmental estrogens. Environmental Health Perspectives, 105: 418–422.
Atkinson, S, Atkinson, MJ & Tarrant, AM 2003, Estrogens from sewage in coastal marine environments. Environmental Health Perspectives, 111: 531–535.
Benjonathan, N & Steinmetz, R 1998, Xenoestrogens the emerging story of bisphenol A. Trends in Endocrinology and Metabolism, 9: 124–128.
Casini, S, Fossi, MC, Mori, G & Bjornstad, A 2002, Vitellogenin duction in Cyprinus carpio treated with 17β-Estradiol and 4-Nonylphenol. Environmental Monitoring and Assessment, 75, 235–239.
Christensen, LB, Pedersen, KL, Korsgaard, B & Bjerregaard, P 1998, Estrogenicity of xenobiotics in rainbow trout (Oncorhynchus mykiss) using in vivo synthesis of vitellogenin as a biomarker. Marine Environmental Research, 46: 137–140.
De los Rios, A, Juanes, JA, Ortiz-Zarragoitia, M, de Alda, ML, Barcel, D & Cajaraville, MP 2012, Assessment of the effects of a marine urban outfall discharge on caged mussels using chemical and biomarker analysis. Marine Pollution Bulletin, 64: 563–573.
Del Pilar Ruso, Y, de la Ossa, JA, Giménez, F & Sanchez-Lizaso, JL 2010, Sewage treatment level and flow rates affect polychaete assemblages. Marine Pollution Bulletin, 60: 1930–1938.
Denslow, ND, Chow, MC, Kroll, KJ & Green, L 1999, Vitellogenin as a biomarker of exposure for estrogen or estrogen mimics. Ecotoxicology, 8: 385–398.
Esacio, FJ, Garcia-Diego, EM, Garcia-Gomez, DA, Daza, JL, Hortas, F & Gomez-Ariza, JL 1997, Ecological analysis in a polluted area of Algeciras Bay (Southern Spain): external ‘versus’ internal outfalls and environmental implications. Marine Pollution Bulletin, 34: 780–793.
Folmar, LC, Denslow, ND, Rao, V, Chow, M, Crain, DA, Enblom, J, Marcino, J & Guillette Jr, LJ 1996, Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a mayor metropolitan sewage treatment plant. Environmental Health Perspectives, 104: 1096–1101.
Giesy, JP, Pierens, SL, Snyder, EM, Miles-Richardson, SM, Kramer, VJ, Snyder, SA, Nichols, KM & Villeneuve, DL 2000, Effects of 4-nonyl phenol on fecundity and biomarkers of estrogenicity in fathead minnows (Pimephales promelas). Environmental Toxicology and Chemistry, 19: 1368–1377.
Gilannejad, N, Dorafshan, S, Heyrati, FP, Soofiani, NM, Asadollah, S, Martos-Sitcha, JA, Prat, F, Yúfera, M & Martínez-Rodríguez, G 2016, Vitellogenin expression in wild cyprinid Petroleuciscus esfahani as a biomarker of endocrine disruption along the Zayandeh Roud River, Iran. Chemosphere, 144: 1342-1350.
Goodbred, SL, Gilliom, RJ, Gross, TS, Denslow, NP, Bryant, WB & Schoeb, TR 1997, Reconnaissance of 17-bestradiol, 11-ketotestosterone, vitellogenin, and gonad histopathology in common carpof United States streams: potential for contaminant-induced endocrine disruption. United States Department of the Interior-US Geological Survey, Sacramento, CA, USA, pp. 20-28.
Gutendorf, B & Westendorf, J 2001, Comparison of an array of in vitro assays for the assessment of the estrogenic potential of natural and synthetic estrogens, phytoestrogens and xenoestrogens. Toxicology, 166: 79–89.
Hohenblum, P, Gans, O, Moche, W, Scharf, S & Lorbeer, G 2004, Monitoring of selected estrogenic hormones and industrial chemicals in ground waters and surface waters in Austria. Sci. Total Environment, 333: 185–193.
Hylland, K & Haux, C 1997, Effects of environmental oestrogens on marine fish species. Trends in Analytical Chemistry, 16: 606–612.
In the fathead minnow (Pimephales promelas). Ecotoxicology Environmental Safety, 64: 101–105.
Jensen, KM, Ankley, GT 2006, Evaluation of a commercial kit for measuring vitellogenin.
Jobling, S, Casey, D, Rodgers-Gray, T, Oehlmann, J, Schulte-Oehlmann, U, Pawlowski, S, Baunbeck, T, Turner, AP & Tyler, CR 2003, Comparative responses of molluscs and fish to environmental estrogens and an estrogenic effluent. Aquatic Toxicology, 65: 205–220.
Jobling, S, Sheahan, D, Osborne, JA, Matthiessen, P, Sumpter, JP 1996, Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environmental Toxicology and Chemistry, 15: 194–202.
Kuster, M, Lopezde Alda, MJ & Barceló, D 2004, Analysis and distribution of estrogens and progestogens in sewage sludge, soils and sediments. Trends in Analytical Chemistry, 23: 790–798.
Kwack, SJ, Kwon, O, Kim, HS, Kim, SS, Kim, SH, Sohn, KH, Lee, RD, Park, CH, Jeung, EB, An, BS, Park, KL 2002, Comparative evaluation of alkylphenolic compounds on estrogenic activity in vitro and in vivo. J. Toxicology and Environmental Health, A. 65: 419–431.
Lai, KM, Johnson, KL, Scrimshaw, MD & Lester, JN 2000, Binding of water born esteroid estrogens to solid phases in river and estuarine systems. Environmental Science and Technology, 34: 3890–3894.
Lee, HB 1999, Review of analytical methods for the determination of nonylphenol and related compounds in environmental samples. Water Quality Research Journal of Canada, 34: 3–35.
Li, J, Ma, M & Wang, Z 2010, In vitro profiling of endocrine disrupting effects of phenols. Toxicology, in Vitro. 24: 201–207.
Li, W, Seifert, MXu, Y & Hock, B 2004, Comparative study of estrogenic potencies of estradiol, tamoxifen, bisphenol-A and resveratrol with two in vitro bioassays. Environmental International. 30: 329– 335.
Lindholst, C, Pedersen, KL & Pedersen. SN 2000, Estrogenic response of bisphenol A in rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology, 48: 87–94.
Mandich, A, Bottero, S, Benfenati, E, Cevasco, A, Erratico, C, Maggioni, S, Massari, A, Pedemonte, F & Viganò, L 2007, In vivo exposure of carp to graded concentrations of bisphenol A. General and Comparative Endocrinology, 153: 15–24.
Marin, MG & Matozzo, V 2004, Vitellogenin induction as a biomarker of exposure to estrogenic compounds in aquatic environments. Marine Pollution Bulletin, 48: 835–839.
Matozzo, M, Gagné, F, Marin, MG, Ricciardi, F & Blaise, C 2008, Vitellogenin as a biomarker of exposure to estrogenic compounds in Aquatic invertebrates: A review. Environmental International, 34: 531–545.
Montorzi, M, Falchuk, KH & Vallee, BL 1994, Xenopus laevis vitellogenin is a zinc protein. Biochemical and Biophysical Research Communications, 200: 1407–1413.
Mortazavi, S, Riyahi Bakhtiari, AR, Esmaili Sari, A, Bahramifar, N & Rahbarizade, F 2012, Phenolic Endocrine Disrupting Chemicals (EDCs) in Anzali Wetland, Iran: Elevated concentrations of 4-Nonylphenol, Octhylphenol and Bisphenol A. Marine Pollution Bulletin,46: 1067–1073
Okus, E, Ozturk, I, Ibrahim, H, Yukseka, A, Tasa, S, Aslan-Yilmaza, A, Altioka, H, Balkisa, N, Dogana, E, Ovezb, S & Aydinb, AF 2008, Critical evaluation of waste water treatment and disposal strategies for Istanbul with regards to water quality monitoring study results. Desalination, 226: 231–248.
Orlando, EF, Kolok, AS, Binzcik, GA, Gates, JL, Horton, MK, Lambright, CS, Gray Jr. LE, Soto, AM, Guillette, Jr & Louis, J 2004, Endocrine-disrupting effects of cattle feed lot effluent on an aquatic sentinel species, the fathead minnow. Environmental Health Perspectives, 112: 353–358.
 Ratna, WN, Bhatt, VD, Chaudhary, K, Ariff, AB, Bavadekar, SA & Ratna, HN 2016,
Estrogen-responsive genes encoding egg yolk proteins vitellogenin and apolipoprotein II in chicken are differentially regulated by selective estrogen receptor modulators. Theriogenology, 85(3): 376-383.
Reinen, Jl Suter, MJFl Voeli, AC, Fernandez, MF, Kiviranta, H, Eggen, RIL & Vermeulen, NPE 2012, Endocrine disrupting chemicals—Linking internal exposure to vitellogenin levels and ovotestis in Abramis brama from Dutch surface waters. Environmental Toxicology and Pharmacology, 30: 209–223.
Riva, C, Porte, C, Binelli, A & Provini, A 2010, Evaluationof 4-nonylphenol in vivo exposure in Dreissena polymorpha: Bioaccumulation, steroid levels and oxidative stress. Comparative Biochemistry and Physiology Part C, 152: 175–181.
Robinson, CD, Brown, E, Craft, JA, Davies, IM, Moffat, CF, Pirie, D, Robertson, F, Stagg, RM & Struthers, S 2003, Effects of sewage effluent and ethynyl oestradiol upon molecular markers of oestrogenic exposure, maturation and reproductive successs in the sand goby (Pomatoschistus minutus, Pallas). Aquatic Toxicology, 62: 119–134.
Scognamiglio, V, Antonacci, A, Patrolecco, L, Lambreva, MD, Litescu, SC, Ghuge, SA & Rea, G 2016, Analytical tools monitoring endocrine disrupting chemicals. Trends in Analytical Chemistry, 80: 555-567.
Seifert, M, Haindl, S & Hock, B 1999, Development of an enzyme linked receptor assay (ELRA) for estrogens and xenoestrogens. Analytica Chimica Acta, 386: 191–199.
Silva, E, Rajapakse, N, Kortenkamp, A 2002, Something from nothing eight weak estrogenic chemicals combined at concentrations below NOECs produce significant mixture effects. Environmental Science and Technology, 15: 1751– 1756.
Smith, J, Shackley, SE 2006, Effects of closure of a major sewage outfall on sublittoral, soft sediment benthic communities. Marine Pollution Bulletin, 52: 645–658.
Snyder, EM 2001, Use of fish as bioassay organisms to assess wastewater effluents for reproductive endocrine modulating chemicals. Ph.D. Dissertation. Michigan State University, East Lansing, MI, USA.
Solé, M, Lopez de Alda, MJ, Castillo, M, Porte, C, Ladegaard- Pedersen, K & Barcelo, D 2000, Estrogenicity determination in sewage treatment plants and surface waters from the Catalonian area (NE Spain). Environmental Science and Technology, 34: 5076–5083.
Solè, M, Porte, D & Barceló, D 2000, Vitellogeninin duction and other biochemical responses in Carp, Cyprinus carpio, after experimentally injection with17β-Ethynylestradiol. Arch. Environmental Contamination and Toxicology, 38: 494–500.
Soto, AM, Calabro, JM, Prechtl, NV, Yau, AY, Orlando, EF, Daxenberger, A, Kolok, AS, Guillette Jr, LJ, Bizec, BL, Lange, IG & Sonnenschein, C 2004, Androgenic and estrogenic activity in water bodies receiving cattle feed lot effluent in eastern Nebraska, USA. Environmental Health Perspectives, 112: 346–352.
Staples, CA, Dorn, PB, Klecka, GM, O’Block, ST & Harris, LR 1998, A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere, 36: 2149– 2173.
Stein, ED & Cadien, DB 2009, Ecosystem response to regulatory and management actions: the southern California experience in long-term monitoring. Marine Pollution Bulletin, 59: 91–100.
Tashiro, Y, Takemura, A, Fujii, H, Takahira, K & Nakanishi, Y 2003, Livestock wastes as a source of estrogens and their effects on wild life of Manko tidal flat, Okinawa. Marine Pollution Bulletin, 47: 143–147.
Taylor, MR & Harrison, PTC 1999, Ecological effects of endocrine disruption: current evidence and research priorities. Chemosphere, 8: 1237–1248.
Tremblay, L & Van Der Kraak, G 1998, Use of a series of homologous in vitro and in vivo assays to evaluate the endocrine modulating actions of b-sitosterol in rainbow trout. Aquatic Toxicology, 43: 149–162.
Truscott, BSo, YP, Nagler, JJ & Idler, DR 1992, Steroids involved with final oocyte maturation in the winter flounder. The Journal of Steroid Biochemistry and Molecular Biology, 42: 351–356.
Vega-Lopez, A, Martinez-Tabche, L, Dominguez-Lopez, ML, Garcia-Latorre, E Ramon-Gallegos, E & Garcia-Gasca, A 2006, Vitellogenin induction in the endangered goodeid fish Girardinichthys viviparus: Vitellogenin characterization and estrogenic effects of polychlorinated biphenyls. Comparative Biochemistry and Physiology C, Toxicology and Pharmacology, 142: 356–364.
Villeneuve, DL, Villalobos, SA, Keith, TL, Snyder, EM, Fitzgerald, SD, Giesy, JP 2002, Effects of waterborne exposure to 4-nonylphenol on plasma sex steroid and vitellogenin concentrations in sexually mature male carp (Cyprinus carpio). Chemosphere, 47: 15–28.
Xu, LC, Sun, H, Chen., JF, Bian, Q, Qian, J,  Song, L & Wang, XR 2005, Evaluation of androgen receptor transcriptional activities of bisphenol A, octylphenol and nonylphenol in vitro. Toxicology, 216: 197–203.
Ying, GG, Kookana, RS & Ru, YJ 2002, Occurrence and fate of hormone esteroids in the environment. Environment International, 28: 545–51.
Zha, J, Wang, Z, Schlenk, D 2006, Effects of pentachlorophenol on the reproduction of Japanese medaka (Oryzias latipes). Chemico-Biological Interactions, 161: 26–36.
Caspian Journal of Environmental Sciences
Volume 17, Issue 1
March 2019
Pages 43-53

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