Abstract
Exposure to xenoestrogens like 4-nonylphenol (NP) is recognized by disrupting endocrine functions and causes reproductive dysfunction in male fish. The present study aimed at investigating the 4-nonylphenol propensity to induce oxidative stress and hormonal disturbances in male catfish and at studying the protective role of quince (Cydonia oblonga). To fulfill this aim, catfish Clarias gariepinus were exposed to pure 100 μg/L 4-NP and to quince the leaf extract added to 4-NP, both for 15 days. The 4-NP exposure induced a marked increase in 17ß-estradiol (E2), LH, and cortisol, while thyroid hormone (TSH, T3), testosterone (T), and FSH levels noticeably decreased; however, 4-NP had no effect on T4 level. Moreover, 4-NP exposure was accompanied by histological impairments in testes. Existence of 4-NP was associated with oxidative damage as evidenced by the significant increase (p < 0.05) of the enzymes, superoxidase dismutase (SOD), catalase (CAT), acetylcholinesterase (AchE), glutathione s-transferase, total antioxidant capacity (TAC), and malondialdehyde (MDA). Adding quince was effective to neutralize hormonal levels and to repair the testicular histological alterations. In response to quince remedy, the enzymes AchE and MDA reduced significantly (p < 0.05), while limited or no response was detected for other tested enzymes. Our results concluded that quince can antagonize 4-NP toxicity in catfish, confirming that quince leaf extract displayed antioxidant activities against the toxicity of hazardous chemicals.
Similar content being viewed by others
References
Aly HA, Domenech O, Banjar ZM (2012) Effect of nonylphenol on male reproduction: analysis of rat epididymal biochemical markers and antioxidant defense enzymes. Toxicol Appl Pharmacol 261:134–141
Arukwe A, Förlin L, Goksøyr A (1997) Xenobiotic and steroid biotransformation enzymes in Atlantic salmon (Salmo salar) liver treated with an estrogenic compound, 4-nonylphenol. Environ Toxicol Chem 16:2576–2583. doi:10.1002/etc.5620161220
Basile A, Giordano S, Lopez-Saez JA, Cobianchi RC (1999) Antibacterial activity of pure flavonoids isolated from mosses. Phytochemistry 52:1479–1482
Chaudhuri S, Banerjee A, Basu K, Sengupta B, Sengupta PK (2007) Interaction of flavonoids with red blood cell membrane lipids and proteins: antioxidant and antihemolytic effects. Int J Biol Macromol 41:42–48
Check JH, Ubelacker L, Lauer CC (1995) Falsely elevated steroidal assay levels related to heterophile antibodies against various animal species. Gynecol Obstet Investig 40:139–140
Choi MS, Park HJ, Oh JH, Lee EH, Park SM, Yoon S (2014) Nonylphenol-induced apoptotic cell death in mouse TM4 sertoli cells via the generation of reactive oxygen species and activation of the ERK signaling pathway. J Appl Toxicol 34:628–636
Choi S, Lee CH, Park W, Kim DJ, Sohn YC (2010) Effects of shortened photoperiod on gonadotropin-releasing hormone, gonadotropin, and vitellogenin gene expression associated with ovarian maturation in rainbow trout. Zool Sci 27:24–32
Christensen LJ, Korsgaard B, Bjerregaard P (1999) The effect of 4-nonylphenol on the synthesis of vitellogenin in the flounder Platichthys flesus. Aquat Toxicol 46:211–219. doi:10.1016/S0166-445X(98)00129-5
Cionna C, Maradonna F, Olivotto I, Pizzonia G, Carnevali O (2006) Effects of nonylphenol on juveniles and adults in the grey mullet, Liza aurata. Reprod Toxicol 22:449–454. doi:10.1016/j.reprotox.2006.04.025
Clairborne A (1995) Handbook of methods for oxygen radical research. CRC Press, Boca Raton
Cobb WE, Lamberton RP, Jackson IM (1984) Use of a rapid, sensitive immunoradiometric assay for thyrotropin to distinguish normal from hyperthyroid subjects. Clin Chem 30:1558–1560
Commission E (1997) Environment and climate research programme DG XII of the report of European Commission. Paper presented at the Proceedings EUR 17549. European Workshop on the Impact of Endocrine Disruptors on Human Health and Wildlife, London, UK
Costa RM, Magalhaes AS, Pereira JA, Andrade PB, Valentao P, Carvalho M, Silva BM (2009) Evaluation of free radical-scavenging and antihemolytic activities of quince (Cydonia oblonga) leaf: a comparative study with green tea (Camellia sinensis). Food Chem Toxicol 47:860–865
Cumming DC, Vickovic MM, Wall SR, Fluker MR (1985) Defects in pulsatile LH release in normally menstruating runners. J Clin Endocrinol Metab 60:810–812
Dickey JT, Swanson P (1998) Effects of sex steroids on gonadotropin (FSH and LH) regulation in coho salmon (Oncorhynchus kisutch). J Mol Endocrinol 21:291–306
Folmar LC et al (1996) Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ Health Perspect 104:1096–1101
Foster LB, Dunn RT (1974) Single-antibody technique for radioimmunoassay of cortisol in unextracted serum or plasma. Clin Chem 20:365–368
Gao X, Björk L, Trajkovski V, Uggla M (2000) Evaluation of antioxidant activities of rosehip ethanol extracts in different test systems. J Sci Food Agric 80:2021–2027. doi:10.1002/1097-0010(200011)80:14<2021::aid-jsfa745>3.0.co;2-2
Garcia-Reyero N et al (2004) Use of vitellogenin mRNA as a biomarker for endocrine disruption in feral and cultured fish. Anal Bioanal Chem 378:670–675
Giesy JP et al (2000) Effects of 4-nonylphenol on fecundity and biomarkers of estrogenicity in fathead minnows (Pimephales promelas). Environ Toxicol Chem 19:1368–1377. doi:10.1002/etc.5620190520
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Harris CA, Santos EM, Janbakhsh A, Pottinger TG, Tyler CR, Sumpter JP (2001) Nonylphenol affects gonadotropin levels in the pituitary gland and plasma of female rainbow trout. Environ Sci Technol 35:2909–2916
Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP (1998) Widespread sexual disruption in wild fish. Environ Sci Technol 32:2498–2506
Knedel M, Böttger R (1967) Eine kinetische Methode zur Bestimmung der Aktivität der Pseudocholinesterase (Acylcholin-acylhydrolase 3.1.1.8.) Klin Wochenschr 45:325–327. doi:10.1007/bf01747115
Knobil E (1980) The neuroendocrine control of the menstrual cycle. Recent Prog Horm Res 36:53–88
Koracevic D, Koracevic G, Djordjevic V, Andrejevic S, Cosic V (2001) Method for the measurement of antioxidant activity in human fluids. J Clin Pathol 54:356–361. doi:10.1136/jcp.54.5.356
Laurenzana EM, Weis CC, Bryant CW, Newbold R, Delclos KB (2002) Effect of dietary administration of genistein, nonylphenol or ethinyl estradiol on hepatic testosterone metabolism, cytochrome P-450 enzymes, and estrogen receptor alpha expression. Food Chem Toxicol 40:53–63. doi:10.1016/S0278-6915(01)00095-3
Lavado R, Thibaut R, Raldúa D, Martín R, Porte C (2004) First evidence of endocrine disruption in feral carp from the Ebro River. Toxicol Appl Pharmacol 196:247–257. doi:10.1016/j.taap.2003.12.012
Leatherland JF (1992) Endocrine and reproductive function in Great Lakes salmon. In: Colborn T, Clement C (eds) Chemically induced alterations in sexual and functional development: the wildlife/human connection. Princeton Scientific Publishing, Princeton, pp 129–146
Maeng S, Jung Y, Choi E, Jeon JK, Kim S, Gen K, Sohn YC (2005) Expression of gonadotropin subunit genes following 4-nonylphenol exposure in masu salmon: effects on transcript levels and promoter activities via estrogen receptor alpha. Comp Biochem Physiol B Biochem Mol Biol 142:383–390
Magwere T, Naik YS, Hasler JA (1997) Effects of chloroquine treatment on antioxidant enzymes in rat liver and kidney. Free Radic Biol Med 22:321–327
Maradonna F, Carnevali O (2007) Vitellogenin, zona radiata protein, cathepsin D and heat shock protein 70 as biomarkers of exposure to xenobiotics. Biomarkers 12:240–255
McCormick SD, O’Dea MF, Moeckel AM, Lerner DT, Bjornsson BT (2005) Endocrine disruption of parr-smolt transformation and seawater tolerance of Atlantic salmon by 4-nonylphenol and 17beta-estradiol. Gen Comp Endocrinol 142:280–288
Mekkawy IA, Mahmoud UM, Sayed Ael D (2011) Effects of 4-nonylphenol on blood cells of the African catfish Clarias gariepinus (Burchell, 1822). Tissue Cell 43:223–229. doi:10.1016/j.tice.2011.03.006
Miles-Richardson SR, Kramer VJ, Fitzgerald SD, Render JA, Yamini B, Barbee SJ, Giesy JP (1999a) Effects of waterborne exposure of 17 β-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Aquat Toxicol 47:129–145. doi:10.1016/S0166-445X(99)00009-0
Miles-Richardson SR et al (1999b) Effects of waterborne exposure to 4-nonylphenol and nonylphenol ethoxylate on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Environ Res 80:S122–S137
Mitchelmore CL, Rice CP (2006) Correlations of nonylphenol-ethoxylates and nonylphenol with biomarkers of reproductive function in carp (Cyprinus carpio) from the Cuyahoga River. Sci Total Environ 371:391–401
Nagao T, Wada K, Marumo H, Yoshimura S, Ono H (2001) Reproductive effects of nonylphenol in rats after gavage administration: a two-generation study. Reprod Toxicol 15:293–315
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358. doi:10.1016/0003-2697(79)90738-3
Osman AG, Koutb M, Sayed Ael D (2010) Use of hematological parameters to assess the efficiency of quince (Cydonia oblonga Miller) leaf extract in alleviation of the effect of ultraviolet—a radiation on African catfish Clarias gariepinus (Burchell, 1822). J Photochem Photobiol B 99:1–8. doi:10.1016/j.jphotobiol.2010.01.002
Park KH (2015) Alteration of hepatic anti-oxidant systems by 4-nonylphenol, a metabolite of alkylphenol polyethoxylate detergents, in Far Eastern catfish Silurus asotus Environ Health Toxicol 2
Park W, Lee CH, Lee CS, Kim D-J, Kim J-H, Tamaru CS, Sohn YC (2007) Effects of a gonadotropin-releasing hormone analog combined with pimozide on plasma sex steroid hormones, ovulation and egg quality in freshwater-exposed female chum salmon (Oncorhynchus keta). Aquaculture 271:488–497. doi:10.1016/j.aquaculture.2007.04.061
Petrovic M, Sole M, Lopez de Alda MJ, Barcelo D (2002) Endocrine disruptors in sewage treatment plants, receiving river waters, and sediments: integration of chemical analysis and biological effects on feral carp. Environ Toxicol Chem 21:2146–2156
Raine JC, Leatherland JF (2003) Trafficking of l-triiodothyronine between ovarian fluid and oocytes of rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B: Biochem Mol Biol 136:267–274. doi:10.1016/S1096-4959(03)00203-3
Reddy PK, Leatherland JF (1998) Stress physiology. In: Leatherland JF, Woo PTK (eds) Fish disease and disorders—non-infections disorders, vol 2. Cabi Publishing pp 279–301
Sayed AH, Abdel-Tawab HS, Abdel Hakeem SS, Mekkawy IA (2013) The protective role of quince leaf extract against the adverse impacts of ultraviolet—a radiation on some tissues of Clarias gariepinus (Burchell, 1822). J Photochem Photobiol B 119:9–14. doi:10.1016/j.jphotobiol.2012.11.006
Sayed AH, Hamed HS (2017) Induction of apoptosis and DNA damage by 4-nonylphenol in African catfish (Clarias gariepinus) and the antioxidant role of Cydonia oblonga. Ecotoxicol Environ Saf 139:197–101
Sayed AH, Mahmoud UM, Mekkawy IA (2012a) Reproductive biomarkers to identify endocrine disruption in Clarias gariepinus exposed to 4-nonylphenol. Ecotoxicol Environ Saf 78:310–319. doi:10.1016/j.ecoenv.2011.11.041
Sayed AH, Mekkawy IA, Mahmoud UM (2012b) Histopathological alterations in some body organs of adult Clarias gariepinus (Burchell, 1822) exposed to 4-nonylphenol In: Garcia MD (ed) Zoology. pp 163–184
Sayed AH, Mohamed NH, Ismail MA, Abdel-Mageed WM, Shoreit AA (2016) Antioxidant and antiapoptotic activities of Calotropis procera latex on catfish (Clarias gariepinus) exposed to toxic 4-nonylphenol. Ecotoxicol Environ Saf 128:189–194. doi:10.1016/j.ecoenv.2016.02.023
Singh N, Rajini PS (2008) Antioxidant-mediated protective effect of potato peel extract in erythrocytes against oxidative damage. Chem Biol Interact 173:97–104. doi:10.1016/j.cbi.2008.03.008
Singh PB, Canario AVM (2004) Reproductive endocrine disruption in the freshwater catfish, Heteropneustes fossilis, in response to the pesticide gamma-hexachlorocyclohexane. Ecotoxicol Environ Saf 58:77–83. doi:10.1016/j.ecoenv.2003.07.014
Skelley D, Brown L, Besch P (1973) Radioimmunoassay Clin Chem 146
Supriya A et al (2005) Thyroid hormone modulation of ovarian recrudescence of air-breathing catfish Clarias gariepinus. Fish Physiol Biochem 31:267–270
Swanson P (1991) Salmon gonadotropins: reconciling old and new ideas. Paper presented at the Reproductive Physiology of Fish, UK
Uno T, Ishizuka M, Itakura T (2012) Cytochrome P450 (CYP) in fish. Environ Toxicol Pharmacol 34:1–13. doi:10.1016/j.etap.2012.02.004
van Aerle R, Nolanusan M, Jobling S, Christiansen LB, Sumpter JP, Tyler CR (2001) Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom. Freshwaters Environmental Toxicology and Chemistry 20:2841–2847. doi:10.1002/etc.5620201225
Van Baal J, Hassing GAM, Goos HJT, Schulz RW (2000) Modulatory effects of 4-nonylphenol on LH production in the African catfish pituitary Reproductive Physiology of Fish 373
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. doi:10.1016/S0045-6535(01)00212-0
Weber LP, Hill RL Jr, Janz DM (2003) Developmental estrogenic exposure in zebrafish (Danio rerio): II. Histological evaluation of gametogenesis and organ toxicity. Aquat Toxicol 63:431–446. doi:10.1016/S0166-445X(02)00208-4
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625
Xu H, Yang M, Qiu W, Pan C, Wu M (2013) The impact of endocrine-disrupting chemicals on oxidative stress and innate immune response in zebrafish embryos. Environ Toxicol Chem 32:1793–1799. doi:10.1002/etc.2245
Yadetie F, Arukwe A, Goksøyr A, Male R (1999) Induction of hepatic estrogen receptor in juvenile Atlantic salmon in vivo by the environmental estrogen, 4-nonylphenol. Sci Total Environ 233:201–210. doi:10.1016/S0048-9697(99)00226-0
Yadetie F, Male R (2002) Effects of 4-nonylphenol on gene expression of pituitary hormones in juvenile Atlantic salmon (Salmo salar). Aquat Toxicol 58:113–129. doi:10.1016/S0166-445X(01)00242-9
Yang L, Lin L, Weng S, Feng Z, Luan T (2008) Sexually disrupting effects of nonylphenol and diethylstilbestrol on male silver carp (Carassius auratus) in aquatic microcosms. Ecotoxicol Environ Saf 71:400–411. doi:10.1016/j.ecoenv.2008.01.007
Yaron Z, Sivan B (2006) Reproduction. In: Evans DH, Claibourne JB (eds) The physiology of fishes. Taylor & Francis, Boca Raton, pp 343–386
Zaccaroni A et al (2009) Thyroid hormones as a potential early biomarker of exposure to 4-nonylphenol in adult male shubunkins (Carassius auratus). Sci Total Environ 407:3301–3306. doi:10.1016/j.scitotenv.2009.01.036
Zha J, Wang Z, Wang N, Ingersoll C (2007) Histological alternation and vitellogenin induction in adult rare minnow (Gobiocypris rarus) after exposure to ethynylestradiol and nonylphenol. Chemosphere 66:488–495. doi:10.1016/j.chemosphere.2006.05.071
Zohar Y, Muñoz-Cueto JA, Elizur A, Kah O (2010) Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 165:438–455. doi:10.1016/j.ygcen.2009.04.017
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Experimental setup and fish handling were approved by the Research Ethical Committee of the Faculty of Science, Assuit University, Assuit, Egypt.
Conflict of interest
The authors declare that there is no conflict of interest.
Rights and permissions
About this article
Cite this article
Sayed, A.ED.H., Ismail, R.F.K. Endocrine disruption, oxidative stress, and testicular damage induced by 4-nonylphenol in Clarias gariepinus: the protective role of Cydonia oblonga . Fish Physiol Biochem 43, 1095–1104 (2017). https://doi.org/10.1007/s10695-017-0355-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-017-0355-2