Copper affects steroidogenesis and viability of human adrenocortical carcinoma (NCI-H295R) cell line in vitro

References

• Sanderson, J. T. The Steroid Hormone Biosynthesis Pathway as a Target for Endocrine-Disrupting Chemicals. Toxicol. Sci. 2006, 94, 3–21. DOI: 10.1093/toxsci/kfl051.
   PubMed Web of Science ®Google Scholar
• Kabir, E. R.; Rahman, M. S.; Rahman, I. A Review on Endocrine Disruptors and Their Possible Impacts on Human Health. Environ. Toxicol. Pharmacol. 2015, 40, 241–258. DOI: 10.1016/j.etap.2015.06.009.
   PubMed Web of Science ®Google Scholar
• Sanderson, J. T.; Berg, M. Interactions of Xenobiotics with the Steroid Hormone Biosynthesis Pathway. Pure Appl. Chem. 2003, 75, 1957–1971. DOI: 10.1351/pac200375111957.
   Web of Science ®Google Scholar
• Arabi, M.; Mohammadpour, A. A. Adverse Effects of Cadmium on Bull Spermatozoa. Vet. Res. Commun. 2006, 30, 943–951. DOI: 10.1007/s11259-006-3384-3.
   PubMed Web of Science ®Google Scholar
• Roychoudhury, S.; Massanyi, P. In vitro Copper Inhibition of the Rabbit Spermatozoa Motility. J. Environ. Sci. Health Part A 2008, 43, 658–663.
   Web of Science ®Google Scholar
• Knazicka, Z.; Lukac, N.; Forgacs, Z.; Tvrda, E.; Lukacova, J.; Slivkova, J.; Binkowski, Ł.; Massanyi, P. Effects of Mercury on the Steroidogenesis of Human Adrenocarcinoma (NCI-H295R) Cell Line. J. Environ. Sci. Health A. 2013, 48, 348–353. DOI: 10.1080/10934529.2013.726908.
   PubMed Web of Science ®Google Scholar
• Knazicka, Z.; Forgacs, Z.; Lukacova, J.; Roychoudhury, S.; Massanyi, P.; Lukac, N. Endocrine Disruptive Effects of Cadmium on Steroidogenesis: Human Adrenocortical Carcinoma Cell Line NCI-H295R As a Cellular Model for Reproductive Toxicity Testing. J. Environ. Sci. Health, Part A 2015, 50, 348–356. DOI: 10.1080/10934529.2015.987520.
   PubMed Web of Science ®Google Scholar
• Knazicka, Z.; Bezakova, J.; Bistakova, J.; Jambor, T.; Massanyi, P.; Bojnanska, T.; Lukac, N. Dávkovo a časovo závislý účinok chloridu meďnatého na samčí reprodukčný system in vitro. Folia Medica Cassoviensia 2016, 70, 9–16.
   Google Scholar
• Lukacova, J.; Knazicka, Z.; Tvrda, E.; Gren, A.; Lukac, N.; Massanyi, P. The Impact of Nonylphenol (NP) on the Spermatozoa Motility in vitro. J. Microbiol. Biotechnol. Food Sci. 2012, 1, 1551–1560.
   Google Scholar
• Lukac, N.; Lukacova, J.; Pinto, B.; Knazicka, Z.; Tvrda, E.; Massanyi, P. The Effect of Nonylphenol on the Motility and Viability of Bovine Spermatozoa in vitro. J. Environ. Sci. Health Part A 2013, 48, 973–979. DOI: 10.1080/10934529.2013.762744.
   PubMed Web of Science ®Google Scholar
• Jambor, T.; Lukacova, J.; Tvrda, E.; Knazicka, Z.; Forgacs, Z.; Lukac, N. The Impact of 4-Nonylphenol on the Viability and Hormone Production of Mouse Leydig Cells. Folia Biol (Praha) 2016, 62, 34–39.
   PubMed Web of Science ®Google Scholar
• Bistakova, J.; Forgacs, Z.; Bartos, Z.; Szivosne, M. R.; Jambor, T.; Knazicka, Z.; Tvrda, E.; Libova, L.; Goc, Z.; Massanyi, P.; Lukac, N. Effects of 4-Nonylphenol on the Steroidogenesis of Human Adrenocarcinoma Cell Line (NCI-H295R). J. Environ. Sci. Health A. 2017, 52, 221–227. DOI: 10.1080/10934529.2016.1246936.
   PubMed Web of Science ®Google Scholar
• Pinto, B.; Garritano, S. L.; Cristofani, R.; Ortaggi, G.; Giuliano, A.; Amodio Cocchieri, R.; Cirillo, T.; De Giusti, M.; Boccia, A.; Reali, D. Monitoring of Polychlorinated Biphenyl Contamination and Estrogenic Activity in Water, Commercial Feed and Farmed Seafood. Environ. Monit. Assess. 2008, 144, 445–453. DOI: 10.1007/s10661-007-0007-6.
   PubMed Web of Science ®Google Scholar
• Kendig, E. L.; Buesing, D. R.; Christie, S. M.; Cookman, C. J.; Gear, R. B.; Hugo, E. R.; Kasper, S. N.; Kendziorski, J. A.; Ungi, K. R.; Williams, K.; Belcher, S. M. Estrogen-Like Disruptive Effects of Dietary Exposure to Bisphenol A or 17α-Ethinyl Estradiol in CD1 Mice. Int. J. Toxicol. 2012, 31, 537–550. DOI: 10.1177/1091581812463254.
   PubMed Web of Science ®Google Scholar
• Lukacova, J.; Jambor, T.; Knazicka, Z.; Tvrda, E.; Kolesarova, A.; Lukac, N. Dose- and Time-Dependent Effects of Bisphenol A on Bovine Spermatozoa in vitro. J. Environ. Sci. Health, Part A 2015, 50, 669–676. DOI: 10.1080/10934529.2015.1011963.
   PubMed Web of Science ®Google Scholar
• Craig, P. M.; Galus, M.; Wood, C. H. M.; McClelland, G. B. Dietary Iron Alters Waterborne Copper-Induced Gene Expression in Soft Water Acclimated Zebrafish (Danio rerio). Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 296, 362–373.
   PubMed Web of Science ®Google Scholar
• Yunus, E. U.; Mustafa, S.; Mustafa, A. T.; Baki, H. Determination of Lead, Copper and Iron in Cosmetics, Water, Soil and Food Using Polyhydroxybutyrate-B-Polydimethyl Siloxane Preconcentration and Flame Atomic Absorption Spectroscopy. Anal. Lett. 2015, 48, 1163–1179.
   Web of Science ®Google Scholar
• Dobrzanski, Z.; Kolacz, R.; Bodak, E. Heavy Metals in Animal Environment. Medycyna Weterynaryjna 1996, 52, 570–574.
   Google Scholar
• Tang, S. H. Study of Interaction between Gelatin and Copper (II) Using Synchronours Fluorescence Spectroscopy. J. Photographic Sci. Photochem. 2005, 23, 102–107.
   Google Scholar
• Agarwal, K.; Sharma, A.; Talukder, G. Clastogenic Effects of Copper Sulphate on the Bone Marrow Chromosomes of Mice in vivo. Mutat. Res. 1990, 243, 1–6. DOI: 10.1016/0165-7992(90)90115-Z.
   PubMed Web of Science ®Google Scholar
• Kong, Y. Q.; Chen, L. Q.; Li, E. C.; Du, Z. Y.; Ding, Z. L. Growth and Antioxidant Activity of Juvenile Oriental River Prawn Macrobrachium Nipponense, Fed Diets Containing Different Copper Levels Under Nitrite Exposure. Global Adv. Res. J. Agricul. Sci. 2014, 3, 119–122.
   Google Scholar
• Gaetke, L. M.; Chow, C. K. Copper Toxicity, Oxidative Stress and Antioxidant Nutriens. Toxicology 2003, 189, 147–163. DOI: 10.1016/S0300-483X(03)00159-8.
   PubMed Web of Science ®Google Scholar
• Aydemir, B.; Kiziler, A. R.; Onaran, I.; Alici, B.; Ozkara, H.; Akyolcu, M. C. Impact of Cu and Fe Concentrations on Oxidative Damage in Male Infertility. BTER 2006, 112, 193–203. DOI: 10.1385/BTER:112:3:193.
   PubMed Web of Science ®Google Scholar
• Prohaska, J. R. Copper. In: Present Knowledge in Nutrition; Erdman, J., Macdonald, I., Zeisel, S., Eds. Wiley, Blackwell, Oxford; 2012; pp 873–896
   Google Scholar
• Prohaska, J. R. Impact of Copper Deficiency in Humans. Ann. N.Y. Acad. Sci. 2014, 1314, 1–5. DOI: 10.1111/nyas.12354.
   PubMed Web of Science ®Google Scholar
• Kumar, N.; Crum, B.; Petersen, R. C.; Vernino, S. A.; Ahlskog, J. E. Copper Deficiency Myelopathy. Arch. Neurol. 2004, 61, 762–766. DOI: 10.1001/archneur.61.5.762.
   PubMed Web of Science ®Google Scholar
• Matak, P.; Zumerle, S.; Mastrogiannaki, M.; El Balkhi, S.; Delga, S.; Mathieu, J. R. R.; Canonne-Hergaux, F.; Poupon, J.; Sharp, P. A.; Vaulont, S.; Peyssonnaux, C. Copper Deficiency Leads to Anemia, Duodenal Hypoxia, Upregulation of HIF-2α and Altered Expression of Iron Absorption Genes in Mice. PLoS One 2013, 8, e59538DOI: 10.1371/journal.pone.0059538.
   PubMed Web of Science ®Google Scholar
• Georgopoulos, A. R.; Yonone-Lioy, M. J.; Opiekun, R. E.; Lioy, P. J. Environmental Copper: Its Dynamics and Human Exposure Issues. J. Toxicol. Environ. Health Part B Crit. Rev. 2001, 4, 341–394.
   PubMed Web of Science ®Google Scholar
• Romic, M.; Romic, D. Heavy Metals Distribution in Agricultural Topsoils in Urban Area. Environ. Geol. 2003, 43, 795–805. DOI: 10.1007/s00254-002-0694-9.
   Web of Science ®Google Scholar
• WHO. 1996. Trace elements in human nutrition and health. Copper. Geneva, Switzerland: World Health Organization, 123–143.
   Google Scholar
• Agency for Toxic Substances and Disease Registry (ATSDR). 2004. Toxicological profile for Copper. U.S. Department of Health and Human Services, Public Health Service: Atlanta, GA.
   Google Scholar
• Ishola, A. B.; Okechukwu, I. M.; Ashimedua, U. G.; Uchechukwu, D.; Michael, E. A.; Moses, O. O.; Okwudili, I. H.; Vaima, H. M.; Itakure, A. U.; Ifeanyichukwu, O. K. Serum Level of Lead, Zinc, Cadmium, Copper and Chromium among Occupationally Exposed Automotive Workers in Benin City. Int. J. Environ. Pollut. Res. 2017, 5, 70–79.
   Google Scholar
• Burtis, C. A.; Ashwood, E. R.; Bruns, D. E. Tietz Textbook of Clinical Chemistry and Molecular Diagnostics (e-book). 5th ed.; Saunders Elsevier: St. Louis, 2012, 2238.
   Google Scholar
• Saha, A.; Karnik, A.; Sathawara, N.; Kulkarni, P.; Singh, V. Ceruloplasmin as a Marker of Occupational Copper Exposure. J. Expo. Sci. Environ. Epidemiol. 2008, 18, 332–337. DOI: 10.1038/jes.2008.2.
   PubMed Web of Science ®Google Scholar
• Sabir, S. M.; Khan, S. W.; Hayat, I. Effect of Environmental Pollution on Quality of Meat in District Bagh, Azad Kashmir. Pakistan J. Nutr. 2003, 2, 98–101. DOI: 10.3923/pjn.2003.98.101.
   Google Scholar
• Ahasan, H. A.; Rafiqueuddin, A. K.; Chowdhury, M. A.; Azhar, M. A.; Kabir, F. Neuromyelitis Optica (Devic’s Disease) Following Chicken Pox. Trop Doct. 1994, 24, 75–76. DOI: 10.1177/004947559402400211.
   PubMed Web of Science ®Google Scholar
• Olivares, M.; Araya, M.; Pizarro, F.; Uauy, R. Uauy, R. Nausea Threshold in Apparently Healthy Individuals Who Drink Fluids Containing Graded Concentrations of Copper. Regul. Toxicol. Pharmacol. 2001, 33, 271–275. DOI: 10.1006/rtph.2000.1440.
   PubMed Web of Science ®Google Scholar
• Bandmann, O.; Weiss, K. H.; Kaler, S. G. Wilson’s Disease and Other Neurological Copper Disorders. Lancet Neurol. 2015, 14, 103–113. DOI: 10.1016/S1474-4422(14)70190-5.
   PubMed Web of Science ®Google Scholar
• Roychoudhury, S.; Nath, S.; Massanyi, P.; Stawarz, R.; Kacaniova, M.; Kolesarova, A. Copper-Induced Changes in Reproductive Functions: In Vivo and In Vitro Effects (Review). Physiol Res. 2016, 65, 11–22. DOI: 10.33549/physiolres.933063.
   PubMed Web of Science ®Google Scholar
• Roychoudhury, S.; Massanyi, P.; Bulla, J.; Choudhury, M. D.; Straka, L.; Lukac, N.; Formicki, G.; Dankova, M.; Bardos, L. In vitro Copper Toxicity on Rabbit Spermatozoa Motility, Morphology and Cell Membrane Integrity. J. Environ. Sci. Health. Part A 2010, 45, 1482–1491. DOI: 10.1080/10934529.2010.506092.
   Web of Science ®Google Scholar
• Chattopadhyay, A.; Biswas, N. Testosterone Supplemented Protection on Inhibition of Testicular Function Induced by Copper Chloride. DHR Int. J. Biomed. Life Sci. 2013, 4, 212–223.
   Google Scholar
• Kolesarova, A.; Capcarova, M.; Roychoudhury, S. Metal Induced Ovarian Signaling. 1st ed.; Slovak University of Agriculture in Nitra, Nitra, 2010.
   Google Scholar
• Roychoudhury, S.; Bulla, J.; Sirotkin, A. V.; Kolesarova, A. In vitro Changes in Porcine Ovarian Granulosa Cells Induced by Copper. J. Environ. Sci. Health A 2014, 49, 625–633. DOI: 10.1080/10934529.2014.865404.
   PubMed Web of Science ®Google Scholar
• Jockenhovel, F.; Bals-Pratsch, M.; Bertram, H. P.; Nieschlag, E. Seminal Lead and Copper in Fertile and Infertile Men. Andrologia 1990, 22, 503–511. DOI: 10.1111/j.1439-0272.1990.tb02041.x.
   PubMed Web of Science ®Google Scholar
• Katayose, H.; Shinohara, A.; Chiba, M.; Yamada, H.; Tominaga, K.; Sato, A.; Yanagida, K. Effects of Various Elements in Seminal Plasma on Semen Profiles. J. Mamm. Ova Res. 2004, 21, 141–148. DOI: 10.1274/jmor.21.141.
   Google Scholar
• Xu, Y.; Xiao, F. L.; Xu, N.; Qian, S. Z. Effect of Intra-Epididymal Injection of Copper Particles on Fertility, Spermatogenesis and Tissue Copper Levels in Rats. Int. J. Androl. 1985, 8, 168–174. DOI: 10.1111/j.1365-2605.1985.tb00830.x.
   PubMed Web of Science ®Google Scholar
• Skandhan, K. P. Review on Copper in Male Reproduction and Contraception. Rev. Fr. Gynecol. Obstet. 1992, 87, 594–608.
   PubMedGoogle Scholar
• Eidi, M.; Eidi, A.; Pouyan, O.; Shahmohammadi, P.; Fazaeli, R.; Bahar, M. Seminal Plasma Levels of Copper and Its Relationship with Seminal Parameters. Iran. J. Reprod. Med. 2010, 8, 60–65.
   Web of Science ®Google Scholar
• Scialli, R. A.; Zinaman, J. M. Reproductive toxicology and infertility. McGraw, Hill: New York, 1993.
   Google Scholar
• Roychoudhury, S.; Slivkova, J.; Bulla, J.; Massanyi, P. Copper Administration Alerts Fine Parameters of Spermatozoa Motility in vitro. Folia Vet. 2008, 52, 64–68.
   Google Scholar
• Knazicka, Z.; Tusimova, E.; Bezakova, J.; Miskeje, M.; Bojnanska, T.; Lukac, N. Relationship between Copper in Different Culture Media and Bovine Spermatozoa Motility Parametres in vitro. J. Microbiol. Biotech. Food Sci. 2017/2018, 7, 226–234.
   Web of Science ®Google Scholar
• Pesch, S.; Bergmann, M.; Bostedt, H. Determination of Some Enzymes and Macro- and Microelements in Stallion Seminal Plasma and Their Correlations to Semen Quality. Theriogenology 2006, 66, 307–313. DOI: 10.1016/j.theriogenology.2005.11.015.
   PubMed Web of Science ®Google Scholar
• Zhang, L. H.; Luo, Z.; Song, Y. F.; Shi, X.; Pan, Y. X.; Fan, Y. F.; Xu, Y. H. Effects and Mechanisms of Waterborne Copper Exposure Influencing Ovary Development and Related Hormones Secretion in Yellow Catfish Pelteobagrus Fulvidraco. Aquat. Toxicol. 2016, 178, 88–98. DOI: 10.1016/j.aquatox.2016.07.014.
   PubMed Web of Science ®Google Scholar
• Hoseini, S. M.; Rajabiesterabadi, H.; Kordrostami, S. Chronic Exposure of Rutilus Rutilus Caspicus Fingerlings to Ambient Copper: Effects on Food Intake, Growth Performance, Biochemistry and Stress Resistance. Toxicol. Ind. Health 2016, 32, 375–383. DOI: 10.1177/0748233713500825.
   PubMed Web of Science ®Google Scholar
• Yang, J.; Hu, S.; Rao, M.; Hu, L.; Lei, H.; Wu, Y.; Wang, Y.; Ke, D.; Xia, W.; Zhu, C.-H. Copper Nanoparticle-Induced Ovarian Injury, Follicular Atresia, Apoptosis, and Gene Expression Alterations in Female Rats. Int. J. Nanomed. 2017, 12, 5959–5971. DOI: 10.2147/IJN.S139215.
   PubMed Web of Science ®Google Scholar
• Klevay, L. M.; Christopherson, D. M. Copper Deficiency Halves Serum Dehydroepiandrosterone in Rats. J. Trace Elem. Med. Biol. 2000, 14, 143–145. DOI: 10.1016/S0946-672X(00)80002-4.
   PubMed Web of Science ®Google Scholar
• Zheng, G.; Wang, L.; Guo, Z.; Sun, L.; Wang, L.; Wang, C.; Zuo, Z.; Qiu, H. Association of Serum Heavy Metals and Trace Element Concentrations with Reproductive Hormone Levels and Polycystic Ovary Syndrome in Chinese Population. Biol. Trace Elem. Res. 2015, 167, 1–10. DOI: 10.1007/s12011-015-0294-7.
   PubMed Web of Science ®Google Scholar
• Hecker, M.; Giesy, J. P. Novel Trends in Endocrine Disruptor Testing: The H295R Steroidogenesis Assay to Identify Inducers and Inhibitors of Hormone Production. Anal. Bioanal. Chem. 2008, 390, 287–291. DOI: 10.1007/s00216-007-1657-5.
   PubMed Web of Science ®Google Scholar
• Hilscherova, K.; Jones, P. D.; Gracia, T.; Newsted, J. L.; Zhang, X.; Sanderson, J. T.; Yu, R. M. K.; Wu, R. S. S.; Giesy, J. P. Assessment of the Effects of Chemicals on the Expression of Ten Steroidogenic Genes in the H295R Cell Line Using Real-Time PCR. Toxicol. Sci. 2004, 81, 78–89. DOI: 10.1093/toxsci/kfh191.
   PubMed Web of Science ®Google Scholar
• Hecker, M.; Newsted, J. L.; Murphy, M. B.; Higley, E. B.; Jones, P. D.; Wu, R. S. S.; Giesy, J. P. Human Adrenocarcinoma (H295R) Cells for Rapid in vitro Determination of Effects on Steroidogenesis: Hormone Production. Toxicol. Appl. Pharmacol. 2006, 217, 114–124. DOI: 10.1016/j.taap.2006.07.007.
   PubMed Web of Science ®Google Scholar
• OECD 2011. H295R Steroidogenesis Assay, OECD Guideline for the Testing of Chemicals No. 456, Paris. http://www.oecd;ilibrary.org/environment/test;no;456;h295r;steroidogenesis;assay_9789264122642. ;en.
   Google Scholar
• Zhang, X.; Yu, R. M. K.; Jones, P. D.; Lam, G. K. W.; Newsted, J. L.; Gracia, T.; Hecker, M.; Hilscherova, K.; Sanderson, J. T.; Wu, R. S. S.; Giesy, J. P. Quantitative RT-PCR Methods for Evaluating Toxicant-Induced Effects on Steroidogenesis Using the H295R Cell Line. Environ. Sci. Technol. 2005, 39, 2777–2785. DOI: 10.1021/es048679k.
   PubMed Web of Science ®Google Scholar
• United States Environmental Protection Agency, Endocrine Disruptor Screening Program Test Guidelines OPPTS 890.1550: Steroidogenesis (Human Cell Line – H295R), EPA 640-C-09-003, 2009 http://www.epa.gov/ocspp/pubs/frs/publications/TestGuidelines/series890.htm.
   Google Scholar
• Mosmann, T. Rapid Colorimetric Assay for Cellular Growth and Surrival: Application to Proliferation and Cytotoxicity Assays. J. Immunol. Methods 1983, 65, 55–63. DOI: 10.1016/0022-1759(83)90303-4.
   PubMed Web of Science ®Google Scholar
• Gazdar, A. F.; Oie, H. K.; Shackleton, C. H.; Chen, T. R.; Triche, T. J.; Myers, C. E.; Chrousos, G. P.; Brennan, M. F.; Stein, C. A.; La Rocca, R. V. Establishment and Characterization of a Human Adrenocortical Carcinoma Cell Line That Expresses Multiple Pathways of Steroid Biosynthesis. Cancer Res. 1990, 50, 5488–5496.
   PubMed Web of Science ®Google Scholar
• Rainey, W. E.; Saner, K.; Schimmer, B. P. Adrenocortical Cell Lines. Mol. Cell. Endocrinol. 2004, 228, 23–28. DOI: 10.1016/j.mce.2003.12.020.
   PubMed Web of Science ®Google Scholar
• Gracia, T.; Hilscherova, K.; Jones, P. D.; Newsted, J. L.; Zhang, X. W.; Hecker, M.; Higley, E. B.; Sanderson, J. T.; Yu, R. M. K.; Wu, R. S. S.; Giesy, J. P. The H295R System for Evaluation of Endocrine-Disrupting Effects. Ecotoxicol. Environ. Saf. 2006, 65, 293–305. DOI: 10.1016/j.ecoenv.2006.06.012.
   PubMed Web of Science ®Google Scholar
• Ding, L.; Murphy, M. B.; He, Y.; Xu, Y.; Yeung, L. W.; Wang, J.; Zhou, B.; Lam, P. K.; Wu, R. S.; Giesy, J. P. Effects of Brominated Flame Retardants and Brominated Dioxins on Steroidogenesis in H295R Human Adrenocortical Carcinoma Cell Line. Environ. Toxicol. Chem. 2007, 26, 764–772. DOI: 10.1897/06-388R1.1.
   PubMed Web of Science ®Google Scholar
• Strajhar, P.; Tonoli, D.; Jeanneret, F.; Imhof, R. M.; Malagnino, V.; Patt, M.; Kratschmar, D. V.; Boccard, J.; Rudaz, S.; Odermatt, A. Steroid Profiling in H295R Cells to Identify Chemicals Potentially Disrupting the Production of Adrenal Steroids. Toxicology 2017, 381, 51–53. DOI: 10.1016/j.tox.2017.02.010.
   PubMed Web of Science ®Google Scholar
• Jumhawan, U.; Yamashita, T.; Ishida, K.; Fukusaki, E.; Bamba, T. Simultaneous Profiling of 17 Steroid Hormones for the Evaluation of Endocrine-Disrupting Chemicals in H295R Cells. Bioanalysis 2017, 9, 67–69. DOI: 10.4155/bio-2016-0149.
   PubMed Web of Science ®Google Scholar
• Chattopadhyay, A.; Sarkar, M.; Biswas, N. M. Dose-Dependent Effect of Copper Chloride on Male Reproductive Function in Immature Rats. Kathmandu Univ. Med. J. 2005, 3, 392–400.
   PubMedGoogle Scholar
• Khushboo, M.; Murthy, M. K.; Devi, M. S.; Sanjeev, S.; Ibrahim, K. S.; Kumar, N. S.; Roy, V. K.; Gurusubramanian, G. Testicular Toxicity and Sperm Quality Following Copper Exposure in Wistar Albino Rats: Ameliorative Potentials of L-Carnitine. Environ. Sci. Pollut. Res. Int. 2018, 25, 1837–1862. DOI: 10.1007/s11356-017-0624-8.
   PubMed Web of Science ®Google Scholar
• Chattopadhyay, A.; Sarkar, M.; Biswas, N. M. Effect of Copper Chloride on Adrenocortical Activities in Adult and Immature Male Rats. Environ. Toxicol. Pharmacol. 2002, 11, 79–84. DOI: 10.1016/S1382-6689(01)00107-7.
   PubMed Web of Science ®Google Scholar
• Bhardwaj, J. K.; Sharma, P. K. Changes in Trace Elements during Follicular Atresia in Goat (Capra hircus) Ovary. Biol. Trace Elem. Res. 2011, 140, 291–298. DOI: 10.1007/s12011-010-8700-7.
   PubMed Web of Science ®Google Scholar
• Kendall, N. R.; Marsters, P.; Guo, L.; Scaramuzzi, R. J.; Campbell, B. K. Effect of Copper and Thiomolybdates on Bovine Theca Cell Differentiation in vitro. J. Endocrinol. 2006, 189, 455–463. DOI: 10.1677/joe.1.06278.
   PubMed Web of Science ®Google Scholar
• Kendall, N. R.; Marsters, P.; Scaramuzzi, R. J.; Campbell, B. K. Expression of Lysyl Oxidase and Effect of Copper Chloride and Ammonium Tetrathiomolybdate on Bovine Ovarian Follicle Granulosa Cells Cultured in Serum-Free Media. Reproduction 2003, 125, 657–665. DOI: 10.1530/reprod/125.5.657.
   PubMed Web of Science ®Google Scholar
• Sun, Y.; Wang, W.; Guo, Y.; Zheng, B.; Li, H.; Chen, J.; Zhang, W. High Copper Levels in Follicular Fluid Affect Follicle Development in Polycystic Ovary Syndrome Patients: Population-Based and in vitro Studies. Toxicol. Appl. Pharmacol. 2019, 365, 101–111. DOI: 10.1016/j.taap.2019.01.008.
   PubMed Web of Science ®Google Scholar
• Chang, C. S.; Park, S. B.; Choi, J. B.; Kim, H. J. Correlation between Serum Testosterone Level and Concentrations of Copper and Zinc in Hair Tissue. Biol. Trace Elem. Res. 2011, 144, 264–271. DOI: 10.1007/s12011-011-9085-y.
   PubMed Web of Science ®Google Scholar
• Laskey, J. W.; Phelps, P. V. Effect of Cadmium and Other Metal Cations on in vitro Leydig Cell Testosterone Production. Toxicol. Appl. Pharmacol. 1991, 108, 296–306. DOI: 10.1016/0041-008X(91)90119-Y.
   PubMed Web of Science ®Google Scholar
• Ng, T. B.; Liu, W. K. Toxic Effect of Heavy Metals on Cell Isolated from the Rat Adrenal and Testis. In Vitro Cell. Dev. Biol. 1990, 26, 24–28. DOI: 10.1007/BF02624150.
   PubMed Web of Science ®Google Scholar
• Nishiyama, S.; Nakamura, K.; Ogawa, M. Effects of Heavy Metals on Corticosteroid Production in Cultured Rat Adrenolcortical Cells. Toxicol. Appl. Pharmacol. 1985, 81, 174–176. DOI: 10.1016/0041-008X(85)90132-2.
   PubMed Web of Science ®Google Scholar