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Combined effects of copper and cadmium exposure on ovarian function and structure in Nile Tilapia (Oreochromis niloticus)

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Abstract

With the rapid development of industrialization and urbanization, the issue of copper (Cu) and cadmium (Cd) pollution in aquatic ecosystems has become increasingly severe, posing threats to the ovarian tissue and reproductive capacity of aquatic organisms. However, the combined effects of Cu and Cd on the ovarian development of fish and other aquatic species remain unclear. In this study, female Nile tilapia (Oreochromis niloticus) were individually or co-exposed to Cu and/or Cd in water. Ovarian and serum samples were collected at 15, 30, 60, 90, and 120 days, and the bioaccumulation, ovarian development, and hormone secretion were analyzed. Results showed that both single and combined exposure significantly reduced the gonadosomatic index and serum hormone levels, upregulated estrogen receptor (er) and progesterone receptor (pr) gene transcription levels, and markedly affected ovarian metabolite levels. Combined exposure led to more adverse effects than single exposure. The data demonstrate that the Cu and Cd exposure can impair ovarian function and structure, with more pronounced adverse effects under Cu and Cd co-exposure. The Cu and Cd affect the metabolic pathways of nucleotides and amino acids, leading to ovarian damage. This study highlights the importance of considering combined toxicant exposure in aquatic toxicology research and provides insights into the potential mechanisms underlying heavy metal-induced reproductive toxicity in fish.

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References

  • Akan JC, Mohmoud S, Yikala BS, Ogugbuaja VO (2012) Bioaccumulation of Some Heavy Metals in Fish Samples from River Benue in Vinikilang, Adamawa State, Nigeria. Am J Analyt Chem 3:727–736

    Article  Google Scholar 

  • Ali I, Penttinen-Damdimopoulou PE, Mäkelä SI, Berglund M, Stenius U, Åkesson A, Håkansson H, Halldin K (2010) Estrogen-like effects of cadmium in vivo do not appear to be mediated via the classical estrogen receptor transcriptional pathway. Environ Health Persp 118:1389–1394

    Article  CAS  Google Scholar 

  • Almeida J, Diniz Y, Marques S, Faine L, Ribas B, Burneiko R, Novelli E (2002) The use of the oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environ Int 27:673–679

    Article  CAS  Google Scholar 

  • Aquili L (2020) The role of tryptophan and tyrosine in executive function and reward processing. Int J Tryptophan Res 13:1178646920964825

    Article  Google Scholar 

  • Atli G, Canli M (2010) Response of antioxidant system of freshwater fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicol Environ Safety 73:1884–1889

    Article  CAS  Google Scholar 

  • Babich H, Shopsis C, Borenfreund E (1986) In vitro cytotoxicity testing of aquatic pollutants (cadmium, copper, zinc, nickel) using established fish cell lines. Ecotoxicol Environ Safety 11:91–99

    Article  CAS  Google Scholar 

  • Barbier O, Jacquillet G, Tauc M, Cougnon M, Poujeol P (2005) Effect of heavy metals on, and handling by, the kidney. Nephron Physiol 99:p105–p110

    Article  CAS  Google Scholar 

  • Bettini S, Ciani F, Franceschini V (2006) Recovery of the olfactory receptor neurons in the African Tilapia mariae following exposure to low copper level. Aquatic Toxicol 76:321–328

    Article  CAS  Google Scholar 

  • Brosnan JT, Brosnan ME (2006) The sulfur-containing amino acids: an overview. J Nutr 136:1636S–1640S

    Article  CAS  Google Scholar 

  • Capriello T, Grimaldi MC, Cofone R, D’Aniello S, Ferrandino I (2019) Effects of aluminium and cadmium on hatching and swimming ability in developing zebrafish. Chemosphere 222:243–249

    Article  CAS  Google Scholar 

  • Cavas T, Garanko NN, Arkhipchuk VV (2005) Induction of micronuclei and binuclei in blood, gill and liver cells of fishes subchronically exposed to cadmium chloride and copper sulphate. Food Chem Toxicol 43:569–574

    Article  CAS  Google Scholar 

  • Chen J, Hu W, Zhu Z (2013) Progress in studies of fish reproductive development regulation. Chinese Sci Bull 58:7–16

    Article  Google Scholar 

  • Driessnack MK, Matthews AL, Raine JC, Niyogi S (2016) Interactive effects of chronic waterborne copper and cadmium exposure on tissue-specific metal accumulation and reproduction in fathead minnow (Pimephales promelas). Comparative Biochem Physiol Part C: Toxicol Pharmacol 179:165–173

    CAS  Google Scholar 

  • Du H, Wang K, Su L, Zhao H, Gao S, Lin Q, Ma X, Zhu B, Dong X, Lou Z (2016) Metabonomic identification of the effects of the Zhimu-Baihe saponins on a chronic unpredictable mild stress-induced rat model of depression. J Pharma Biomed Anal 128:469–479

    Article  CAS  Google Scholar 

  • El Asely AM, Reda RM, Salah AS, Mahmoud MA, Dawood MA (2020) Overall performances of Nile tilapia (Oreochromis niloticus) associated with using vegetable oil sources under suboptimal temperature. Aquacul Nutr 26:1154–1163

    Article  CAS  Google Scholar 

  • 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 major metropolitan sewage treatment plant. Environ Health Persp 104:1096–1101

    Article  CAS  Google Scholar 

  • Funk AE, Day FA, Brady FO (1987) Displacement of zinc and copper from copper-induced metallothionein by cadmium and by mercury: in vivo and ex vivo studies. Comparative Biochem Physiol Part C: Comparative Pharmacol 86:1–6

    Article  CAS  Google Scholar 

  • Galaris D, Pantopoulos K (2008) Oxidative stress and iron homeostasis: mechanistic and health aspects. Crit Rev Clin Labor Sci 45:1–23

    Article  CAS  Google Scholar 

  • Garcia‐Santos S, Fontaínhas‐Fernandes A, Wilson JM (2006) Cadmium tolerance in the Nile tilapia (Oreochromis niloticus) following acute exposure: Assessment of some ionoregulatory parameters. Environ Toxicol: Int J 21:33–46

    Article  Google Scholar 

  • Genchi G, Sinicropi MS, Lauria G, Carocci A, Catalano A (2020) The effects of cadmium toxicity. Int J Environ Res Public Health 17:3782

    Article  CAS  Google Scholar 

  • Giltay EJ, Bunck MC, Gooren LJ, Zitman FG, Diamant M, Teerlink T (2008) Effects of sex steroids on the neurotransmitter-specific aromatic amino acids phenylalanine, tyrosine, and tryptophan in transsexual subjects. Neuroendocrinology 88:103–110

    Article  CAS  Google Scholar 

  • Giustarini D, Dalle-Donne I, Colombo R, Milzani A, Rossi R (2008) Is ascorbate able to reduce disulfide bridges? A cautionary note. Nitric Oxide 19:252–258

    Article  CAS  Google Scholar 

  • Jezierska B, Witeska M, The metal uptake and accumulation in fish living in polluted waters. Soil and water pollution monitoring, protection and remediation. Springer (2006) pp. 107–114

  • Kamunde C, MacPhail R (2011) Metal–metal interactions of dietary cadmium, copper and zinc in rainbow trout, Oncorhynchus mykiss. Ecotoxicol Environ Safety 74:658–667

    Article  CAS  Google Scholar 

  • Kavanaugh SI, Nozaki M, Sower SA (2008) Origins of gonadotropin-releasing hormone (GnRH) in vertebrates: identification of a novel GnRH in a basal vertebrate, the sea lamprey. Endocrinology 149:3860–3869

    Article  CAS  Google Scholar 

  • Keun HC (2006) Metabonomic modeling of drug toxicity. Pharmacol Ther 109:92–106

    Article  CAS  Google Scholar 

  • Kozera B, Rapacz M (2013) Reference genes in real-time PCR. J Appl Genet 54:391–406

    Article  CAS  Google Scholar 

  • Leonardi R, Zhang Y-M, Rock CO, Jackowski S (2005) Coenzyme A: back in action. Prog Lipid Res 44:125–153

    Article  CAS  Google Scholar 

  • Li X, Wu Y, Xie G, Tan Z (2022) Effects of chronic cadmium exposure on the structure and function of intestinal mucosal flora in mice. Toxin Rev 41:904–917

    Article  CAS  Google Scholar 

  • Li Z-H, Zlabek V, Velisek J, Grabic R, Machova J, Kolarova J, Li P, Randak T (2011) Acute toxicity of carbamazepine to juvenile rainbow trout (Oncorhynchus mykiss): effects on antioxidant responses, hematological parameters and hepatic EROD. Ecotoxicol Environ Safety 74:319–327

    Article  CAS  Google Scholar 

  • Li Z, Ma Z, van der Kuijp TJ, Yuan Z, Huang L (2014) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Tot Environ 468:843–853

    Article  Google Scholar 

  • Li ZH, Li P, Randak T (2010) Effect of a human pharmaceutical carbamazepine on antioxidant responses in brain of a model teleost in vitro: an efficient approach to biomonitoring. J Appl Toxicol 30:644–648

    Article  Google Scholar 

  • Ling J, Söll D (2010) Severe oxidative stress induces protein mistranslation through impairment of an aminoacyl-tRNA synthetase editing site. Proc Natl Acad Sci 107:4028–4033

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Luo Y, Shan D, Zhong H, Zhou Y, Chen W, Cao J, Guo Z, Xiao J, He F, Huang Y (2015) Subchronic effects of cadmium on the gonads, expressions of steroid hormones and sex-related genes in tilapia Oreochromis niloticus. Ecotoxicology 24:2213–2223

    Article  CAS  Google Scholar 

  • Maiuolo J, Oppedisano F, Gratteri S, Muscoli C, Mollace V (2016) Regulation of uric acid metabolism and excretion. Int J Cardiol 213:8–14

    Article  Google Scholar 

  • Manolescu AR, Witkowska K, Kinnaird A, Cessford T, Cheeseman C (2007) Facilitated hexose transporters: new perspectives on form and function. Physiology 22:234–240

    Article  CAS  Google Scholar 

  • Marques S, Antunes S, Pissarra H, Pereira M, Gonçalves F, Pereira R (2009) Histopathological changes and erythrocytic nuclear abnormalities in Iberian green frogs (Rana perezi Seoane) from a uranium mine pond. Aquat Toxicol 91:187–195

    Article  CAS  Google Scholar 

  • Matés JM, Sánchez-Jiménez F (1999) Antioxidant enzymes and their implications in pathophysiologic processes. Front Biosci-Landmark 4:339–345

    Article  Google Scholar 

  • Matos M (2002) Encyclopedia of life sciences. Biotech Softw Int Rep: Comp Softw J Scientists 3:94–96

    Article  Google Scholar 

  • Meghana S, Kabra P, Chakraborty S, Padmavathy N (2015) Understanding the pathway of antibacterial activity of copper oxide nanoparticles. RSC Adv 5:12293–12299

    Article  CAS  Google Scholar 

  • Milla S, Depiereux S, Kestemont P (2011) The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review. Ecotoxicology 20:305–319

    Article  CAS  Google Scholar 

  • Miller WL (1988) Molecular biology of steroid hormone synthesis. Endocrine Rev 9:295–318

    Article  CAS  Google Scholar 

  • Moffatt BA, Ashihara H (2002) Purine and pyrimidine nucleotide synthesis and metabolism. The Arabidopsis Book/American Society of Plant Biologists. 1:e0018.

  • Mowat F, Bundy K (2002) A mathematical algorithm to identify toxicity and prioritize pollutants in field sediments. Chemosphere 49:499–513

    Article  CAS  Google Scholar 

  • Pang B, McFaline JL, Burgis NE, Dong M, Taghizadeh K, Sullivan MR, Elmquist CE, Cunningham RP, Dedon PC (2012) Defects in purine nucleotide metabolism lead to substantial incorporation of xanthine and hypoxanthine into DNA and RNA. Proc Natl Acad Sci 109:2319–2324

    Article  CAS  Google Scholar 

  • Papagiannis I, Kagalou I, Leonardos J, Petridis D, Kalfakakou V (2004) Copper and zinc in four freshwater fish species from Lake Pamvotis (Greece). Environ Int 30:357–362

    Article  CAS  Google Scholar 

  • Pelgrom S, Lock R, Balm P, Bonga SW (1995) Integrated physiological response of tilapia, Oreochromis mossambicus, to sublethal copper exposure. Aquat Toxicol 32:303–320

    Article  CAS  Google Scholar 

  • Pinto J, Rivlin R (2013) Riboflavin (vitamin B2). Handbook of vitamins. 191–266

  • Powers HJ (2003) Riboflavin (vitamin B-2) and health. Am J Clin Nutr 77:1352–1360

    Article  CAS  Google Scholar 

  • Rai AN, Ullah A, Haider J (2015) Determination of acute toxicity of copper and cobalt for Tilapia nilotica. J Bioresource Manag 2:3

    Article  Google Scholar 

  • Rana S (2014) Perspectives in endocrine toxicity of heavy metals—a review. Biol Trace Element Res 160:1–14

    Article  CAS  Google Scholar 

  • Scholtes C, Giguère V (2022) Transcriptional control of energy metabolism by nuclear receptors. Nat Rev Mol Cell Biol 23:750–770

    Article  CAS  Google Scholar 

  • Schreck CB, Tort L, The concept of stress in fish. Fish physiology. Elsevier (2016) pp. 1–34

  • Siegert W, Rodehutscord M (2019) The relevance of glycine and serine in poultry nutrition: a review. Br Poultry Sci 60:579–588

    Article  CAS  Google Scholar 

  • Simpson ER, Davis SR (2001) Minireview: aromatase and the regulation of estrogen biosynthesis—some new perspectives. Endocrinology 142:4589–4594

    Article  CAS  Google Scholar 

  • Stipanuk MH (2004) Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu Rev Nutr 24:539–577

    Article  CAS  Google Scholar 

  • Stocco DM (2001) StAR protein and the regulation of steroid hormone biosynthesis. Ann Rev Physiol 63:193–213

    Article  CAS  Google Scholar 

  • Suvi R, Giovanna M, Katja A (2020) Experimental copper exposure, but not heat stress, leads to elevated intraovarian thyroid hormone levels in three-spined sticklebacks (Gasterosteus aculeatus). Ecotoxicology 29:1431–1440

    Article  CAS  Google Scholar 

  • Tilton SC, Foran CM, Benson WH (2003) Effects of cadmium on the reproductive axis of Japanese medaka (Oryzias latipes). Comparative Biochem Physiol Part C: Toxicol Pharmacol 136:265–276

    Google Scholar 

  • ValkoM L, Moncol J, Cronin M, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84

    Article  Google Scholar 

  • Wang H, Zhang Q, Wen Q, Zheng Y, Lazarovici P, Jiang H, Lin J, Zheng W (2012) Proline-rich Akt substrate of 40 kDa (PRAS40): a novel downstream target of PI3k/Akt signaling pathway. Cell Signal 24:17–24

    Article  CAS  Google Scholar 

  • Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27:195–226

    Article  Google Scholar 

  • Wang J, Xiao J, Zhang J, Chen H, Li D, Li L, Cao J, Xie L, Luo Y (2020) Effects of dietary Cu and Zn on the accumulation, oxidative stress and the expressions of immune-related genes in the livers of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 100:198–207

    Article  CAS  Google Scholar 

  • Wang W, Lampi MA, Huang XD, Gerhardt K, Dixon DG, Greenberg BM (2009) Assessment of mixture toxicity of copper, cadmium, and phenanthrenequinone to the marine bacterium Vibrio fischeri. Environ Toxicol: Int J 24:166–177

    Article  CAS  Google Scholar 

  • Wang Y, Yu W, Li S, Guo D, He J, Wang Y (2022) Acetyl-CoA carboxylases and diseases. Front Oncol 12:836058

    Article  CAS  Google Scholar 

  • Wen Y, Li R, Piao X, Lin G, He P (2022) Different copper sources and levels affect growth performance, copper content, carcass characteristics, intestinal microorganism and metabolism of finishing pigs. Animal Nutr 8:321–330

    Article  CAS  Google Scholar 

  • Widhalm R, Ellinger I, Granitzer S, Forsthuber M, Bajtela R, Gelles K, Hartig P-Y, Hengstschläger M, Zeisler H, Salzer H (2020) Human placental cell line HTR-8/SVneo accumulates cadmium by divalent metal transporters DMT1 and ZIP14. Metallomics 12:1822–1833

    Article  CAS  Google Scholar 

  • Working EIFAC (1969) Water quality criteria for European freshwater fish—extreme pH values and inland fisheries. Water Res 3:593–611

    Article  Google Scholar 

  • Wu S, Lin H, Yang W (2008) The effects of maternal Cd on the metallothionein expression in tilapia (Oreochromis mossambicus) embryos and larvae. Aquatic Toxicol 87:296–302

    Article  CAS  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Int Scholarly Res Notices 2011:402647

    Google Scholar 

  • Xu J, Green NJ, Gibard C, Krishnamurthy R, Sutherland JD (2019) Prebiotic phosphorylation of 2-thiouridine provides either nucleotides or DNA building blocks via photoreduction. Nat Chem 11:457–462

    Article  CAS  Google Scholar 

  • Yang Y, Zheng N, Zhao X, Zhang Y, Han R, Yang J, Zhao S, Li S, Guo T, Zang C (2016) Metabolomic biomarkers identify differences in milk produced by Holstein cows and other minor dairy animals. J Proteom 136:174–182

    Article  CAS  Google Scholar 

  • Younis NA, Laban SE, Al-Mokaddem AK, Attia MM (2020) Immunological status and histopathological appraisal of farmed Oreochromis niloticus exposed to parasitic infections and heavy metal toxicity. Aquaculture Int 28:2247–2262

    Article  CAS  Google Scholar 

  • Zhou L, Zhang W, Xie W, Chen H, Yu W, Li H, Shen G (2017) Tributyl phosphate impairs the urea cycle and alters liver pathology and metabolism in mice after short-term exposure based on a metabonomics study. Sci Total Environ 603:77–85

    Article  Google Scholar 

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Acknowledgements

This study was supported by National Natural Science Foundation of China (31960733, 42177256), the Construction Project of National Modern Agricultural Industrial Technology System (CARS-46), National Key Research and Development Program of China “Technological Innovation of Blue Granary” (2018YFD0900601), National Modern Agricultural Industrial Technology System Guangxi Characteristic Freshwater Fish Innovation Team Disease Prevention and Control post Functional Expert Project (nycytxgxcxtd-2021–08).

Author contributions

Yijie Wu: Data curation, Formal analysis, Writing – original draft. Ting Huang: Data curation, Formal analysis, Writing – original draft. Qiyu Wei: Data curation, Formal analysis, Writing – original draft. Xin Yan: Review, Formal analysis, Visualization. Liting Chen: Methodology, Investigation. Zhirui Ma: Methodology, Investigation. Liming Luo: Methodology, Formal analysis, Validation. Jinling Cao: Methodology, Conceptualization. Hongxing Chen: Methodology, Conceptualization. Xinxian Wei: Methodology, Formal analysis. Honglian Tan: Formal analysis. Fuyan Chen: Formal analysis. Guixiang Tong: Formal analysis. Liping Li: Formal analysis. Zhanyang Tang: Formal analysis. Yongju Luo:Writing – review & editing, Validation, Supervision, Project administration.

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  1. These authors contributed equally: Yijie Wu, Ting Huang, Qiyu Wei

Authors and Affiliations

  1. Guangxi Key Laboratory of Aquatic Genetic Breeding and Healthy Aquaculture, Guangxi Academy of Fishery Science, Nanning, 530021, Guangxi, China

    Yijie Wu, Ting Huang, Qiyu Wei, Xin Yan, Liting Chen, Zhirui Ma, Liming Luo, Xinxian Wei, Honglian Tan, Fuyan Chen, Guixiang Tong, Liping Li, Zhanyang Tang & Yongju Luo

  2. Key Laboratory of Comprehensive Development and Utilization of Aquatic Germplasm Resources of China (Guangxi) and ASEAN (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Nanning, 530021, China

    Yijie Wu, Ting Huang, Qiyu Wei, Xin Yan, Liting Chen, Zhirui Ma, Liming Luo, Xinxian Wei, Honglian Tan, Fuyan Chen, Guixiang Tong, Liping Li, Zhanyang Tang & Yongju Luo

  3. College of Aquaculture and life sciences, Shanghai Ocean University, Shanghai, 201306, China

    Yijie Wu & Liming Luo

  4. College of Food Science and Technology, Shanxi Agricultural University, Taigu, Shanxi, 030801, China

    Jinling Cao

  5. SCNU Environmental Research Institute, Guangdong Provincial Key Laboratory of Chemical Pollution and Environmental Safety & MOE Key Laboratory of Environmental Theoretical Chemistry, South China Normal University, Guangzhou, 510006, China

    Hongxing Chen

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Wu, Y., Huang, T., Wei, Q. et al. Combined effects of copper and cadmium exposure on ovarian function and structure in Nile Tilapia (Oreochromis niloticus). Ecotoxicology 33, 266–280 (2024). https://doi.org/10.1007/s10646-024-02744-0

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