Alteration in the histology of gonads and hormone levels of fish Channa punctatus on exposure to 17-α ethynylestradiol
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Abstract
It has been demonstrated that effluents discharged from sewage treatment facilities allow synthetic estrogens, widely employed in contraceptives and other pharmaceutical applications, to reach the aquatic environment. One of the most biologically active xenoestrogens in the aquatic environment is the synthetic hormone 17-α ethynylestradiol(EE2), raisingreproductive issues in the fish population. The present study chose Channa punctatus fish to study the effects of EE2 on gonad histology and the calculation of estrogen and testosterone levels. The experimental setting was separated into four groups, with Group I as control with 0 ng/L of EE2. The other three groups viz., Group II to IV, had 5 ng/L, 10 ng/L, and 20 ng/L concentrations of EE2, respectively, and samples were obtained after the durations of 7, 14, 21, and 28 days. The findings showed that as 17-α ethynylestradiol concentrations increased, testosterone levels decreased from 10.88±0.24 ng/dL to 4.91±0.24 ng/dL,while estrogen levels increased from 42.7±2.22 pg/mL to 120.18±4.54 pg/mL. The number percentage of primary growth oocytes, previtellogenic oocytes and vitellogenic oocytes in the histology of ovary decreased from 28.45±1.42 to 10.43±0.47; 16.22±0.81 to 3.15±0.16 and 14.81±0.89 to 2.14±0.11 respectively while in testis, the number percentage of spermatogonia, spermatocytes decreased from 21.4±0.86 to 15.1±0.68 and 97.1±3.88 to 54.2±3.25. In contrast, the percentage of mature spermatids increased from 20.8±0.94 to 40.2±2.41. Since synthetic estrogens adversely affect aquatic animals, especially fish, they should be treated properly before releasing them into the aquatic environment.
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Keywords
17-α ethynylestradiol, Channa punctatus Estrogen, Histology, Testosterone
References
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Amenyogbe, E., Chen, G., Wang, Z., Lu, X., Lin, M.& Lin,A. (2020). A review on sex steroid hormone estrogen receptors in mammals and fish. Int. J. Endocrinol.2020,1–9. doi: 10.1155/2020/5386193. [PMC free article] [PubMed] [CrossRef] [Google Scholar].
Ankley, G.T., Jensen, K.M., Makynen, E.A., Kahl, M.D., Korte, J.J., Hornung, M.W.& Gray, L.E. (2003). Effects of the androgenic growth promoter 17-β-trebolone on fecundity and reproductive endocrinology of the fathead minnow. Environmental Toxicology and Chemistry: An International Journal, 22(6), 1350-1360.
APHA (2017). Standard methods for the examination of water and wastewater (23rd ed.). Washington DC:American Public Health Association.
Aris, A.Z., Shamsuddin, A.S.& Praveena, S.M. ( 2014). Occurrence of 17α-ethynylestradiol (EE2) in the environment and effect on exposed biota: a review. Environment International. 69,104-119.
Delbès, G., Blázquez, M., Fernandino, J. I., Grigorova, P., Hales, B. F., Metcalfe, C., & Marlatt, V. (2022). Effects of endocrine disrupting chemicals on gonad development: Mechanistic insights from fish and mammals. Environmental Research, 204, 112040.
De, Wit, M., Keil, D., Van, Der, Ven, K., Vandamme, S., Witter, E. &De, Coen, W. (2010). An integratedtranscriptomic and proteomic approach characterizing estrogenic and metaboliceffects of 17α-ethinylestradiol in zebrafish (Danio rerio). Gen Comp Endocrinol.16,190–210.
Farid, M. A., Rahman, M. A., Aktar, S., Choudhury, M., Yeasmin, S. M., Biswas, A., & Rahman, M. A. (2020). Comparative Studies on Gonad Development, Fecundity and Oocyte Maturation of Spotted Snakehead, Channa punctatus (Bloch, 1793) in Different Water Bodies. Annual Research & Review in Biology, 75-87.
Foster, D., & Brown, K. H. (2018). Dose Duration Effects of 17-α Ethynylestradiol in Zebrafish Toxicology. Recent Advances in Zebrafish Researches.
Gong, J., Duan, D., Yang, Y., Ran, Y., and Chen, D. ( 2016).Seasonal variation and partitioning of endocrine disrupting chemicals in waters and sediments of the Pearl River system, South China,Environ. Pollut. 219:735-741. doi: 10.1016/j.envpol.2016.07.015.
Grier, H. J. (2012). Development of the follicle complex and oocyte staging in red drum. Sciaenops ocellatus. Linnaeus, 1776 (Perciformes, Sciaenidae), Journal of Morphology, 273(8), 801-829.
Gunnarsson, L., Snape, J.R., Verbruggen, B., Owen, S.F., Kristiansson, E., Margiotta-Casaluci, L., Österlund, T., Hutchinson, K., Leverett, D., Marks,B.&Tyler C.R. (2019). Pharmacology beyond the patient – the environmental risks of human drugs. Environ. Int., 129 , pp. 320-332, 10.1016/j.envint.2019.04.075
Gupta, T.& Mullins, M.C.(2010). Dissection of organs from the adult zebrafish. Journal of Visualized Experiments. 37.article e1717; doi:10.3791/1717.
Haniffs, D.M., Sing, S.V.A. & Ramakrishna, C.M. (2009). Antibacterial activity of skin and mucus of five different freshwater fish species Vicz. C.striatus, C. microplates, C. marulius, C. puncttatus and C. gachua. Mal J Sci., 28(3): 257 – 262.
Hernández‐Gómez, R. E., Contreras‐Sánchez, W. M., Hernández‐Franyutti, A., Perera‐García, M. A. & Torres‐Martínez, A. (2022). Testicular structure and development of the male germinal epithelium in the freshwater drum Aplodinotus grunniens (Perciformes: Sciaenidae) from the Usumacinta River, Southern Mexico. Acta Zoologica, 103(4), 414-432.
Hill, Jr, R.L.& Janz, D.M. (2002). Developmental estrogenic exposure in zebrafish (Danio rerio): I. Effects on sex ratio and breeding success. Aquat. Toxicol. 63 (4), 417–429.
Jackson, L.M., Felgenhauer, B.E.& Klerks, P.L. (2019). Feminization, altered gonadal development, and liver damage in the least killifish (Heterandria formosa) exposed to sublethal concentrations of 17alpha-ethinylestradiol. Ecotoxicol Environ Saf 170. 331–337.
Kidd, K.A., Blanchfield, P.J., Mills, K.H., Palace, V.P., Evans, R.E., Lazorchak, J.M.& Flick, R.W., (2007). Collapse of a fish population after exposure to a synthetic estrogen. Proc. Natl. Acad. Sci.,104 (21), 8897-8901.
Lange, R., Hutchinson, T.H., Croudace, C.P., Siegmund, F., Schweinfurth, H., Hampe, P., Panter, G.H.& Sumpter, J.P. (2001). Effects of the synthetic estrogen 17 alpha ethynylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem., 20(6), 1216-1227.
Lawrence, M.J., Raby, G.D., Teffer, A. K.& Jeffries, K.M. (2020). Danylchuk AJ, Eliason EJ, et al. Best Practices for Non‐lethal Blood Sampling of Fish via the Caudal Vasculature. J. Fish. Biol., 97 (1), 4–15. 10.1111/jfb.14339
Maack, G.& Segner, H. (2004). Life-stage-dependent sensitivity of zebrafish (Danio rerio) to estrogen exposure. Comp. Biochem. Physiol. C 139, 47–55.
Mousavi-Sabet, H. (2001). The Effect of 17-Alpha Methyl testosterone on Masculinization, Mortality Rate and growth in Convict Cichild (Cichlasoma nigrofasciatum). Journal of Fish and Marine Sciences. X, 3: 422-426. IDOSI Publications.
Richard, L., Leino, Jensen, K. M., & Ankley, G.T. (2005). Gonadal histology and characteristic histopathology associated with endocrine disruption in the adult fathead minnow (Pimephalespromelas). Environmental Toxicology and Pharmacology, 19(1), 85-98.
Rinchard, J., Kestemont, P., Kuhn, E.R., and Foster, A. (1993). Seasonal changes in plasma levels of steroid hormones in an asynchronous fish, the Gudgeon Gobio gobio. General Comparative Endocrinology., 92 , 168 -187.
Rougeot, C., Krim, A., Mandiki, S.N.M., Kestemont, P.& Melard, C. (2007). Sex steroid dynamics during embryogenesis and sexual differentiation in Eurasian perch, Perca fluviatilis Theriogenology, vol. 67 (pg. 1046-52).
Runnalls, T.J., Margiotta-Casaluci, L., Kugatha, L.& Sumpter, J.P. (2010). Pharmaceuticals in the aquatic environment: steroids and anti-steroids as high priorities for research. Hum. Ecol. Risk. Assess., 16 (6), pp. 1318-1338.
Selman, K., Wallace, Robin, A., Sarka, A.& Qi, X. (1993). Stages of oocyte development in the zebrafish, Brachydanio rerio. J. Morp., 218, 203–224.
Shimizu, A., Aida, K. & Hanyu, I. (1985). Endocrine profiles during the short reproductive cycle of an autumn-spawning bitterling, Acheilognathusrhombea.General and Comparative Endocrinology. 60, 361 -371.
Shirdel, I., Kalbassi, M. R., Esmaeilbeigi, M. & Tinoush, B. (2020). Disruptive effects of nonylphenol on reproductive hormones, antioxidant enzymes, and histology of liver, kidney and gonads in Caspian trout smolts. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 232:108756. doi: 10.1016/j.cbpc.2020.108756
Stefan, O., Holbech, H., & Norrgren, L. (2016). Sexual disruption in zebrafish (Danio rerio) exposed to mixtures of 17α-ethinylestradiol and 17β-trenbolone. Environmental Toxicology and Pharmacology.41, 225-231.
Sun, S. X., Zhang, Y. N., Lu, D. L., Wang, W. L., Limbu, S. M., Chen, L. Q. & Du, Z. Y. (2019). Concentration-dependent effects of 17β-estradiol and bisphenol A on lipid deposition, inflammation and antioxidant response in male zebrafish (Danio rerio). Chemosphere, 237, 124422.
Thorpe, K.L., Cummings, R.I., Hutchinson,T.H., Scholze, M., Brighty,. G, Sumpter, J.P. &Tyler, C.R. (2003). Relative potencies and combination effects of steroidal estrogens in fish, Environ. Sci. Technol., 37 (6), pp. 1142-1149.
Van, den, Belt, K., Verheyen, R.& Witters, H. (2003). Effects of 17alpha-ethynylestradiol in a partial life-cycle test with zebrafish (Danio rerio): effects on growth, gonads and female reproductive success. Sci. Total Environ. X, 309, 127–213.
Van, Der, Ven, L.T., Wester, P.W.& Vos, J.G. (2003). Histopathology is a tool for evaluating endocrine disruption in zebrafish (Danio rerio). Environ Toxicol Chem.22, 908–913
Xie, X., Nóbrega, R. & Pšenička, M. (2020). Spermatogonial stem cells in fish: characterization, isolation, enrichment, and recent advances of in vitro culture systems. Biomolecules, 10(4), 644.
Zeilinger, J., Steger‐Hartmann, T., Maser, E., Goller,S., Vonk, R. & Länge, R. (2009). Effects of synthetic gestagens on fish reproduction. Environmental Toxicology and Chemistry., 28(12), 2663-2670.
Amenyogbe, E., Chen, G., Wang, Z., Lu, X., Lin, M.& Lin,A. (2020). A review on sex steroid hormone estrogen receptors in mammals and fish. Int. J. Endocrinol.2020,1–9. doi: 10.1155/2020/5386193. [PMC free article] [PubMed] [CrossRef] [Google Scholar].
Ankley, G.T., Jensen, K.M., Makynen, E.A., Kahl, M.D., Korte, J.J., Hornung, M.W.& Gray, L.E. (2003). Effects of the androgenic growth promoter 17-β-trebolone on fecundity and reproductive endocrinology of the fathead minnow. Environmental Toxicology and Chemistry: An International Journal, 22(6), 1350-1360.
APHA (2017). Standard methods for the examination of water and wastewater (23rd ed.). Washington DC:American Public Health Association.
Aris, A.Z., Shamsuddin, A.S.& Praveena, S.M. ( 2014). Occurrence of 17α-ethynylestradiol (EE2) in the environment and effect on exposed biota: a review. Environment International. 69,104-119.
Delbès, G., Blázquez, M., Fernandino, J. I., Grigorova, P., Hales, B. F., Metcalfe, C., & Marlatt, V. (2022). Effects of endocrine disrupting chemicals on gonad development: Mechanistic insights from fish and mammals. Environmental Research, 204, 112040.
De, Wit, M., Keil, D., Van, Der, Ven, K., Vandamme, S., Witter, E. &De, Coen, W. (2010). An integratedtranscriptomic and proteomic approach characterizing estrogenic and metaboliceffects of 17α-ethinylestradiol in zebrafish (Danio rerio). Gen Comp Endocrinol.16,190–210.
Farid, M. A., Rahman, M. A., Aktar, S., Choudhury, M., Yeasmin, S. M., Biswas, A., & Rahman, M. A. (2020). Comparative Studies on Gonad Development, Fecundity and Oocyte Maturation of Spotted Snakehead, Channa punctatus (Bloch, 1793) in Different Water Bodies. Annual Research & Review in Biology, 75-87.
Foster, D., & Brown, K. H. (2018). Dose Duration Effects of 17-α Ethynylestradiol in Zebrafish Toxicology. Recent Advances in Zebrafish Researches.
Gong, J., Duan, D., Yang, Y., Ran, Y., and Chen, D. ( 2016).Seasonal variation and partitioning of endocrine disrupting chemicals in waters and sediments of the Pearl River system, South China,Environ. Pollut. 219:735-741. doi: 10.1016/j.envpol.2016.07.015.
Grier, H. J. (2012). Development of the follicle complex and oocyte staging in red drum. Sciaenops ocellatus. Linnaeus, 1776 (Perciformes, Sciaenidae), Journal of Morphology, 273(8), 801-829.
Gunnarsson, L., Snape, J.R., Verbruggen, B., Owen, S.F., Kristiansson, E., Margiotta-Casaluci, L., Österlund, T., Hutchinson, K., Leverett, D., Marks,B.&Tyler C.R. (2019). Pharmacology beyond the patient – the environmental risks of human drugs. Environ. Int., 129 , pp. 320-332, 10.1016/j.envint.2019.04.075
Gupta, T.& Mullins, M.C.(2010). Dissection of organs from the adult zebrafish. Journal of Visualized Experiments. 37.article e1717; doi:10.3791/1717.
Haniffs, D.M., Sing, S.V.A. & Ramakrishna, C.M. (2009). Antibacterial activity of skin and mucus of five different freshwater fish species Vicz. C.striatus, C. microplates, C. marulius, C. puncttatus and C. gachua. Mal J Sci., 28(3): 257 – 262.
Hernández‐Gómez, R. E., Contreras‐Sánchez, W. M., Hernández‐Franyutti, A., Perera‐García, M. A. & Torres‐Martínez, A. (2022). Testicular structure and development of the male germinal epithelium in the freshwater drum Aplodinotus grunniens (Perciformes: Sciaenidae) from the Usumacinta River, Southern Mexico. Acta Zoologica, 103(4), 414-432.
Hill, Jr, R.L.& Janz, D.M. (2002). Developmental estrogenic exposure in zebrafish (Danio rerio): I. Effects on sex ratio and breeding success. Aquat. Toxicol. 63 (4), 417–429.
Jackson, L.M., Felgenhauer, B.E.& Klerks, P.L. (2019). Feminization, altered gonadal development, and liver damage in the least killifish (Heterandria formosa) exposed to sublethal concentrations of 17alpha-ethinylestradiol. Ecotoxicol Environ Saf 170. 331–337.
Kidd, K.A., Blanchfield, P.J., Mills, K.H., Palace, V.P., Evans, R.E., Lazorchak, J.M.& Flick, R.W., (2007). Collapse of a fish population after exposure to a synthetic estrogen. Proc. Natl. Acad. Sci.,104 (21), 8897-8901.
Lange, R., Hutchinson, T.H., Croudace, C.P., Siegmund, F., Schweinfurth, H., Hampe, P., Panter, G.H.& Sumpter, J.P. (2001). Effects of the synthetic estrogen 17 alpha ethynylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem., 20(6), 1216-1227.
Lawrence, M.J., Raby, G.D., Teffer, A. K.& Jeffries, K.M. (2020). Danylchuk AJ, Eliason EJ, et al. Best Practices for Non‐lethal Blood Sampling of Fish via the Caudal Vasculature. J. Fish. Biol., 97 (1), 4–15. 10.1111/jfb.14339
Maack, G.& Segner, H. (2004). Life-stage-dependent sensitivity of zebrafish (Danio rerio) to estrogen exposure. Comp. Biochem. Physiol. C 139, 47–55.
Mousavi-Sabet, H. (2001). The Effect of 17-Alpha Methyl testosterone on Masculinization, Mortality Rate and growth in Convict Cichild (Cichlasoma nigrofasciatum). Journal of Fish and Marine Sciences. X, 3: 422-426. IDOSI Publications.
Richard, L., Leino, Jensen, K. M., & Ankley, G.T. (2005). Gonadal histology and characteristic histopathology associated with endocrine disruption in the adult fathead minnow (Pimephalespromelas). Environmental Toxicology and Pharmacology, 19(1), 85-98.
Rinchard, J., Kestemont, P., Kuhn, E.R., and Foster, A. (1993). Seasonal changes in plasma levels of steroid hormones in an asynchronous fish, the Gudgeon Gobio gobio. General Comparative Endocrinology., 92 , 168 -187.
Rougeot, C., Krim, A., Mandiki, S.N.M., Kestemont, P.& Melard, C. (2007). Sex steroid dynamics during embryogenesis and sexual differentiation in Eurasian perch, Perca fluviatilis Theriogenology, vol. 67 (pg. 1046-52).
Runnalls, T.J., Margiotta-Casaluci, L., Kugatha, L.& Sumpter, J.P. (2010). Pharmaceuticals in the aquatic environment: steroids and anti-steroids as high priorities for research. Hum. Ecol. Risk. Assess., 16 (6), pp. 1318-1338.
Selman, K., Wallace, Robin, A., Sarka, A.& Qi, X. (1993). Stages of oocyte development in the zebrafish, Brachydanio rerio. J. Morp., 218, 203–224.
Shimizu, A., Aida, K. & Hanyu, I. (1985). Endocrine profiles during the short reproductive cycle of an autumn-spawning bitterling, Acheilognathusrhombea.General and Comparative Endocrinology. 60, 361 -371.
Shirdel, I., Kalbassi, M. R., Esmaeilbeigi, M. & Tinoush, B. (2020). Disruptive effects of nonylphenol on reproductive hormones, antioxidant enzymes, and histology of liver, kidney and gonads in Caspian trout smolts. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 232:108756. doi: 10.1016/j.cbpc.2020.108756
Stefan, O., Holbech, H., & Norrgren, L. (2016). Sexual disruption in zebrafish (Danio rerio) exposed to mixtures of 17α-ethinylestradiol and 17β-trenbolone. Environmental Toxicology and Pharmacology.41, 225-231.
Sun, S. X., Zhang, Y. N., Lu, D. L., Wang, W. L., Limbu, S. M., Chen, L. Q. & Du, Z. Y. (2019). Concentration-dependent effects of 17β-estradiol and bisphenol A on lipid deposition, inflammation and antioxidant response in male zebrafish (Danio rerio). Chemosphere, 237, 124422.
Thorpe, K.L., Cummings, R.I., Hutchinson,T.H., Scholze, M., Brighty,. G, Sumpter, J.P. &Tyler, C.R. (2003). Relative potencies and combination effects of steroidal estrogens in fish, Environ. Sci. Technol., 37 (6), pp. 1142-1149.
Van, den, Belt, K., Verheyen, R.& Witters, H. (2003). Effects of 17alpha-ethynylestradiol in a partial life-cycle test with zebrafish (Danio rerio): effects on growth, gonads and female reproductive success. Sci. Total Environ. X, 309, 127–213.
Van, Der, Ven, L.T., Wester, P.W.& Vos, J.G. (2003). Histopathology is a tool for evaluating endocrine disruption in zebrafish (Danio rerio). Environ Toxicol Chem.22, 908–913
Xie, X., Nóbrega, R. & Pšenička, M. (2020). Spermatogonial stem cells in fish: characterization, isolation, enrichment, and recent advances of in vitro culture systems. Biomolecules, 10(4), 644.
Zeilinger, J., Steger‐Hartmann, T., Maser, E., Goller,S., Vonk, R. & Länge, R. (2009). Effects of synthetic gestagens on fish reproduction. Environmental Toxicology and Chemistry., 28(12), 2663-2670.
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Alteration in the histology of gonads and hormone levels of fish Channa punctatus on exposure to 17-α ethynylestradiol. (2023). Journal of Applied and Natural Science, 15(4), 1339-1346. https://doi.org/10.31018/jans.v15i4.4876
