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Vitamin E and genistein generate a cytoprotective effect on polychlorinated biphenyl- induced oxidative stress in testicular Leydig cells

Yıl 2024, Cilt: 25 Sayı: 1, 55 - 64, 15.04.2024
https://doi.org/10.23902/trkjnat.1398909

Öz

Polychlorinated biphenyls (PCBs) are industrial substances which were widely used in industrial applications starting from the 1930s until the mid-1970s. Aroclor 1242 (A1242) is a commercial PCB mixture with 42% chlorine manufactured by the Monsanto Chemical Company in St. Louis, Missouri, USA. Previous studies suggested that PCBs have inhibitory effect on reproductive function, developmental abnormality, and impaired reproductive ability. PCBs may also affect the endocrine system by reducing the testosterone synthesis and the activity of steroidogenic enzymes in Leydig cells. This study was performed to investigate the specific effects of A1242 on the via-bility of Leydig cells, oxidative damage, and the profile of steroidogenic enzymes in an in vitro culture. The therapeutic effects of vitamin E (VitE) and genistein (Gen), as two antioxidants, in mitigating the damage produced by A1242 were also evaluated. TM3 Leydig cells were exposed to 10-8 and 10-6 M of A1242 and VitE (50µM) and Gen (10µM) as antioxidant for 24 h. After the exposure period, the Leydig cells were assessed to determine their viability using a cell viability assay. Measurements were performed for lipid peroxidation, reactive oxygen species (ROS), and steroidogenic enzymes. The results showed that cell viability was reduced after A1242 exposure, while lipid peroxidation and ROS increased. Steroidogenesis was interrupted in a concentration-dependent manner. Following A1242 exposure, administrations of VitE or Gen as an antioxidant reduced hazardous effects of A1242 on Leydig cells. Our results showed that exposure to A1242 may impair Leydig cell function and cause toxicity in Leydig cells and that VitE and Gen treatment exhibited therapeutic effects against this toxicity.

Etik Beyan

Since the article does not contain any studies with human or animal subject, its approval to the ethics committee was not required.

Destekleyen Kurum

Istanbul University Scientific Research Projects

Proje Numarası

T-2857, 2858

Teşekkür

We would like to thank Mikro-Gen Drug Co. for supplying of “Genistein”.

Kaynakça

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  • 2. Ahlborg, U.G., Becking, G.C., Birnbaum, L.S., Brouwer, A., Derks, H.J.G.M., Feeley, M., Golor, G., Hanberg, A., Larsen, J.C., Liem, A.K.D., Safe, S.H., Schlatter, C., Waern, F., Younes, M. & Yrjänheikki, E. 1994. Toxic equivalency factors for dioxinlike PCBs. Chemosphere, 28(6): 1049-1067. https://doi.org/10.1016/0045-6535(94)90324-7
  • 3. Ahmad, S.U., Tariq, S., Jalali, S. & Ahmad, M.M. 2003. Environmental pollutant Aroclor 1242 (PCB) disrupts reproduction in adult male rhesus monkeys (Macaca mulatta). Environmental Research, 93(3): 272-278. https://doi.org/10.1016/S0013-9351(03)00110-5
  • 4. Aly, H.A.A., Alahdal A.M., Nagy, A.A., Abdallah, H.M., Abdel-Sattar, E.A. & Azhar, A.S. 2017. Lipoic acid and Calligonum comosumon attenuate aroclor 1260‐induced testicular toxicity in adult rats. Environmental Toxicology, 32(4): 1147-1157. https://doi.org/10.1002/tox.22310
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  • 9. Behan-Bush, R.M., Liszewski, J.N., Schrodt, M.V., Vats, B., Li, X., Lehmler, H.J., Klingelhutz, A.J. & Ankrum, J.A. 2022. Toxicity impacts on human adipose MSCs acutely exposed to Aroclor and non-Aroclor mixtures of PCBs. BioRxiv, 2022-2011. https://doi.org/10.1101/2022.11.17.516943
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Yıl 2024, Cilt: 25 Sayı: 1, 55 - 64, 15.04.2024
https://doi.org/10.23902/trkjnat.1398909

Öz

Poliklorlu bifeniller (PCB'ler), 1930'lardan 1970'lerin ortalarına kadar endüstriyel uygulamalarda yaygın olarak kullanılan endüstriyel maddelerdir. Aroclor 1242 (A1242), St. Louis, Missouri'deki Monsanto Chemical Company tarafından üretilen %42 klor içeren ticari bir PCB karışımıdır. Önceki çalışmalarda PCB'lerin üreme fonksiyonu, gelişimsel anormallik ve bozulmuş üreme yeteneği üzerinde inhibitör etkisi olduğu öne sürülmüştür. Ayrıca Leydig hücrelerinde testosteron sentezini ve steroidojenik enzimlerin aktivitesini azaltarak endokrin sistemi etkileyebilirler. Bu çalışmanın amacı, A1242'nin Leydig hücrelerinin canlılığı, oksidatif hasar ve steroidojenik enzim-lerin profili üzerindeki spesifik etkilerini in vitro kültürde araştırmaktır. Ayrıca çalışma, iki anti-oksidan olan E vitamini (VitE) ve genisteinin (Gen) A1242'nin neden olduğu hasarı hafifletmede-ki terapötik etkilerini değerlendirmeyi amaçlamaktadır. TM3 Leydig hücreleri, 24 saat boyunca 10-8 ve 10-6 M A1242’ye ve antioksidan olarak VitE (50μM) ve Gen’e (10 μM) maruz bırakıldı. Ma-ruz kalma süresinden sonra Leydig hücreleri, bir hücre canlılığı tahlili kullanılarak canlılıklarının belirlenmesi için değerlendirildi. Lipid peroksidasyonu, reaktif oksijen türleri (ROS) ve steroido-jenik enzimler için ölçümler yapıldı. Sonuçlar, A1242 maruziyetinden sonra hücre canlılığının azaldığını, lipid peroksidasyonunun ve ROS'un arttığını gösterdi. Steroidogenez, konsantrasyona bağlı bir şekilde kesintiye uğradı. A1242'yi takiben, bir antioksidan olarak VitE veya Gen'in uy-gulanması, A1242'nin Leydig hücreleri üzerindeki zararlı etkilerini azalttı. Bulgularımız A1242'ye maruz kalmanın Leydig hücre fonksiyonuna zarar verebileceğini ve Leydig hücrelerinde toksisit-eye neden olabileceğini, VitE ve Gen tedavilerinin bu toksisiteye karşı terapötik etkileri olduğunu göstermektedir.

Proje Numarası

T-2857, 2858

Kaynakça

  • 1. Ahd, K., Dhibi, S., Akermi, S., Bouzenna, H., Samout, N., Elfeki, A. & Hfaiedh, N. 2019. Protective effect of ginger (Zingiber officinale) against PCB-induced acute hepatotoxicity in male rats. Royal Society of Chemistry Advances, 9(50): 29120-29130. https://doi.org/10.1039/C9RA03136G
  • 2. Ahlborg, U.G., Becking, G.C., Birnbaum, L.S., Brouwer, A., Derks, H.J.G.M., Feeley, M., Golor, G., Hanberg, A., Larsen, J.C., Liem, A.K.D., Safe, S.H., Schlatter, C., Waern, F., Younes, M. & Yrjänheikki, E. 1994. Toxic equivalency factors for dioxinlike PCBs. Chemosphere, 28(6): 1049-1067. https://doi.org/10.1016/0045-6535(94)90324-7
  • 3. Ahmad, S.U., Tariq, S., Jalali, S. & Ahmad, M.M. 2003. Environmental pollutant Aroclor 1242 (PCB) disrupts reproduction in adult male rhesus monkeys (Macaca mulatta). Environmental Research, 93(3): 272-278. https://doi.org/10.1016/S0013-9351(03)00110-5
  • 4. Aly, H.A.A., Alahdal A.M., Nagy, A.A., Abdallah, H.M., Abdel-Sattar, E.A. & Azhar, A.S. 2017. Lipoic acid and Calligonum comosumon attenuate aroclor 1260‐induced testicular toxicity in adult rats. Environmental Toxicology, 32(4): 1147-1157. https://doi.org/10.1002/tox.22310
  • 5. Andric, S.A., Kostic, T.S., Stojilkovic, S.S. & Kovacevic, R.Z. 2000. Inhibition of rat testicular androgenesis by a polychlorinated biphenyl mixture Aroclor 1248. Biology of Reproduction, 62(6): 1882-1888. https://doi.org/10.1095/biolreprod62.6.1882
  • 6. Apostoli, P., Mangili, A., Carasi, S. & Manno, M. 2003. Relationship between PCBs in blood and D-glucaric acid in urine. Toxicology Letters, 144(1): 17-26. https://doi.org/10.1016/S0378-4274(03)00226-1
  • 7. ATSDR. 2000 Toxicological Profile for Polychlorinated Biphenyls (PCBs), Atlanta: US Department of Health and Human Services. https://www.atsdr.cdc.gov/toxprofiles/tp17.pdf
  • 8. Aydin, Y. & Erkan, M. 2017. The toxic effects of polychlorinated biphenyl (Aroclor 1242) on Tm3 Leydig cells. Toxicology & Industrial Health, 33(8): 636-645. https://doi.org/10.1177/0748233717699783
  • 9. Behan-Bush, R.M., Liszewski, J.N., Schrodt, M.V., Vats, B., Li, X., Lehmler, H.J., Klingelhutz, A.J. & Ankrum, J.A. 2022. Toxicity impacts on human adipose MSCs acutely exposed to Aroclor and non-Aroclor mixtures of PCBs. BioRxiv, 2022-2011. https://doi.org/10.1101/2022.11.17.516943
  • 10. Bergmeyer, H.U. 1974. Steroid dehydrogenase, pp. 476-477. In: Bergmeyer H.U. (ed.). Methods of Enzymatic Analysis, New York: Academic Press, XLIII-LXXV pp.
  • 11. Carpenter, D.O. 1998. Polichlorinated biphenyls and human health. International Journal of Occupational Medicine and Environmental Health, 11: 291-303.
  • 12. Coşkun, T. 2005. Fonksiyonel besinlerin sağlığımız üzerine etkileri. Çocuk Sağlığı ve Hastalıkları Dergisi, 48(1): 61-84.
  • 13. Deng, P., Barney, J., Petriello, M.C., Morris, A.J., Wahlang, B & Hennig, B. 2019. Hepatic metabolomics reveals that liver injury increases PCB 126-induced oxidative stress and metabolic dysfunction. Chemosphere, 217: 140-149. https://doi.org/10.1016/j.chemosphere.2018.10.196
  • 14. Devasagayam, T.P.A. & Tarachand, U. 1987. Decreased lipid peroxidation in the rat kidney during gestation. Biochemical and Biophysical Research Communications, 145(1): 134-138. https://doi.org/10.1016/0006-291X(87)91297-6
  • 15. Djuric, Z., Chen, G., Doerge, D.R., Heilbrun, L.K. & Küçük, Ö. 2001. Effect of soy isoflavone supplementation on markers of oxidative stress in men and women. Cancer Letters, 172(1): 1-6. https://doi.org/10.1016/S0304-3835(01)00627-9
  • 16. Elayapillai, S.P., Teekaraman, D., Paulraj, R.S. & Jagadeesan, A. 2017. Ameliorative effect of α-tocopherol on polychlorinated biphenyl (PCBs) induced testicular Sertoli cell dysfunction in F1 prepuberal rats. Experimental and Toxicologic Pathology, 69(8): 681-694. https://doi.org/10.1016/j.etp.2017.07.001
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  • 25. Kimbrough, R.D. 1995. Polychlorinated biphenyls (PCBs) and human health: an update. Critical Reviews in Toxicology, 25(2): 133-163. https://doi.org/10.3109/10408449509021611
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  • 28. Lloyd, J.W., Moore, Jr R.M., Woolf, B.S. & Stein, H.P. 1976. Polychlorinated biphenyls. Journal of Occupational and Environmental Medicine, 18(2): 109-113.
  • 29. ⁠Lowry, O.H., Rosebrough, N.J., Farr, A.L., & Randall, R.J. 1951. Protein measurement with folin phenol reagent. The Journal of Biological Chemistry, 193: 265–275.
  • 30. Marklund, S. & Marklund, G. 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry, 47(3): 469-474.
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  • 32. Mega OO, Edesiri TP, Victor E, Kingsley, N.E., Rume, R.A., Faith, F.Y., Simon, O.I., Oghenetega, B.O. & Agbonifo-Chijiokwu, E. 2022. D‐ribose‐L‐cysteine abrogates testicular maladaptive responses induced by polychlorinated bisphenol intoxication in rats via activation of the mTOR signaling pathway mediating inhibition of apoptosis, inflammation, and oxidonitrergic flux. The Journal of Biochemical and Molecular Toxicology, 36(10): e23161. https://doi.org/10.1002/jbt.23161
  • 33. Montano, L., Pironti, C., Pinto, G., Ricciardi, M., Buono, A., Brogna, C., Venier, M., Piscopo, M., Amoresano, A. & Motta, O. 2022. Polychlorinated biphenyls (PCBs) in the environment: occupational and exposure events, effects on human health and fertility. Toxics, 10(7): 365. https://doi.org/10.3390/toxics10070365
  • 34. Mossman, T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. The Journal of Immunological Methods, 65(1-2): 55–63. https://doi.org/10.1016/0022-1759(83)90303-4
  • 35. Murati, T., Šimić, B., Pleadin J., Vukmirović, M., Miletić, M., Durgo, K., Kniewald, J. & Kmetič, I. 2017. Reduced cytotoxicity in PCB-exposed Chinese Hamster Ovary (CHO) cells pretreated with vitamin E. Food and Chemical Toxicology, 99: 17-23. https://doi.org/10.1016/j.fct.2016.11.014
  • 36. Murugesan, P., Balaganesh, M., Balasubramanian, K. & Arunakaran, J. 2007b. Effects of polychlorinated biphenyl (Aroclor 1254) on steroidogenesis and antioxidant system in cultured adult rat Leydig cells. Journal of Endocrinology, 192(2): 325-338. https://doi.org/10.1677/joe.1.06874
  • 37. Murugesan, P., Kanagaraj, P., Yuvaraj, S., Balasubramanian, K., Aruldhas, M.M. & Arunakaran, J. 2005a. The inhibitory effects of polychlorinated biphenyl Aroclor 1254 on Leydig cell LH receptors, steroidogenic enzymes and antioxidant enzymes in adult rats. Reproductive Toxicology, 20(1): 117-126. https://doi.org/10.1016/j.reprotox.2004.11.011
  • 38. Murugesan, P., Muthusamy, T., Balasubramanian, K., Aruldhas, M.M. & Arunakaran, J. 2005b. Studies on the protective role of vitamin C and E against polychlorinated biphenyl (Aroclor 1254)—induced oxidative damage in Leydig cells. Free Radical Research, 39(11): 1259-1272. https://doi.org/10.1016/j.reprotox.2004.11.011
  • 39. Murugesan, P., Muthusamy, T., Balasubramanian, K. & Arunakaran, J. 2007a. Effects of vitamins C and E on steroidogenic enzymes mRNA expression in polychlorinated biphenyl (Aroclor 1254) exposed adult rat Leydig cells. Toxicology, 232(3): 170-182. https://doi.org/10.1016/j.tox.2007.01.008
  • 40. Murugesan, P., Muthusamy, T., Balasubramanian, K. & Arunakaran, J. 2008. Polychlorinated biphenyl (Aroclor 1254) inhibits testosterone biosynthesis and antioxidant enzymes in cultured rat Leydig cells. Reproductive Toxicology, 25(4): 447-454. https://doi.org/10.1016/j.reprotox.2008.04.003
  • 41. Oakley, G.G., Devanaboyina, U.S., Robertson, L.W. & Gupta, R.C. 1996. Oxidative DNA damage induced by activation of polychlorinated biphenyls (PCBs): implications for PCB-induced oxidative stress in breast cancer. Chemical Research in Toxicology, 9(8): 1285-1292. https://doi.org/10.1021/tx960103o
  • 42. Payne, A.H. & Youngblood, G.L. 1995. Regulation of expression of steroidogenic enzymes in Leydig cells. Biology of Reproduction, 52(2): 217-225. https://doi.org/10.1095/biolreprod52.2.217
  • 43. Pistollato, F., de Gyves, E.M., Carpi, D., Bopp, S.K., Nunes C., Worth, A. & Bal-Price, A. 2020. Assessment of developmental neurotoxicity induced by chemical mixtures using an adverse outcome pathway concept. Environmental Health, 19(1): 1-26. https://doi.org/10.1186/s12940-020-00578-x
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  • 45. Quensen, J.F., Boyd, S.A. & Tiedje, J.M. 1990. Dechlorination of four commercial polychlorinated biphenyl mixtures (Aroclors) by anaerobic microorganisms from sediments. Applied and Environmental Microbiology, 56(8): 2360-2369. https://doi.org/10.1128/aem.56.8.2360-2369.1990
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  • 47. Sandal, S., Yilmaz, B. & Carpenter, D.O. 2008. Genotoxic effects of PCB 52 and PCB 77 on cultured human peripheral lymphocytes. Mutation Research: Genetic Toxicology and Environmental Mutagenesis, 654(1): 88-92. https://doi.org/10.1016/j.mrgentox.2008.05.005
  • 48. Selvaraju, V., Baskaran, S., Agarwal, A. & Henkel, R. 2021. Environmental contaminants and male infertility: Effects and mechanisms. Andrologia, 53(1): e13646. https://doi.org/10.1111/and.13646
  • 49. Senthilkumar, J., Banudevi, S., Sharmila, M., Murugesan, P., Srinivasan, N., Balasubramanian, K., Aruldhas, M.M. & Arunakaran, J. 2004. Effects of Vitamin C and E on PCB (Aroclor 1254) induced oxidative stress, androgen binding protein and lactate in rat Sertoli cells. Reproductive Toxicology, 19(2): 201-208. https://doi.org/10.1016/j.reprotox.2004.08.001
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  • 51. Sinha, A.K. 1972. Colorimetric assay of catalase. Analytical Biochemistry, 47(2): 389-394. https://doi.org/10.1016/0003-2697(72)90132-7
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  • 53. Su, L.J., Zhang, J.H., Gomez, H., Murugan, R., Hong, X., Xu, D., Jiang, F. & Peng, Z.Y. 2019. Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxidative Medicine and Cellular Longevity, 2019: 5080843. https://doi.org/10.1155/2019/5080843
  • 54. Thangavelu, S.K., Priya, E.S., Ilangovan, R., Sankar, B.R. & Arunakaran, J. 2018. Lactational exposure of polychlorinated biphenyls impair Leydig cellular steroidogenesis in F1 progeny rats. Reproductive Toxicology, 75: 73-85. https://doi.org/10.1016/j.reprotox.2017.11.009
  • 55. Toda, S. & Shirataki, Y. 1999. Inhibitory effects of isoflavones on lipid peroxidation by reactive oxygen species. Phytotherapy Research, 13(2): 163-165. https://doi.org/10.1002/(SICI)1099-1573(199903)13:2<163::AID-PTR405>3.0.CO;2-%23
  • 56. Venkataraman, P., Krishnamoorthy, G., Vengatesh, G., Srinivasan, N., Aruldhas, M.M. & Arunakaran, J. 2008. Protective role of melatonin on PCB (Aroclor 1254) induced oxidative stress and changes in acetylcholine esterase and membrane bound ATPases in cerebellum, cerebral cortex and hippocampus of adult rat brain. International Journal of Developmental Neuroscience, 26(6): 585-591. https://doi.org/10.1016/j.ijdevneu.2008.05.002
  • 57. Zhang, D.L., Mi, Y.L., Wang, K.M., Zeng, W.D. & Zhang, C.Q. 2008. Attenuating effect of daidzein on polychlorinated biphenyls-induced oxidative toxicity in mouse testicular cells. Journal of Zheijang University Science B- Biomedicine & Biotechnology, 9(7): 567. https://doi.org/10.1631/jzus.B0820048
Toplam 57 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Biyokimya ve Hücre Biyolojisi (Diğer), Hayvan Bilimi (Diğer)
Bölüm Araştırma Makalesi/Research Article
Yazarlar

Yasemin Aydin 0000-0002-4338-4687

Banu Orta Yılmaz 0000-0002-8006-1107

Melike Erkan 0000-0002-6906-4753

Proje Numarası T-2857, 2858
Erken Görünüm Tarihi 26 Şubat 2024
Yayımlanma Tarihi 15 Nisan 2024
Gönderilme Tarihi 1 Aralık 2023
Kabul Tarihi 29 Ocak 2024
Yayımlandığı Sayı Yıl 2024 Cilt: 25 Sayı: 1

Kaynak Göster

APA Aydin, Y., Orta Yılmaz, B., & Erkan, M. (2024). Vitamin E and genistein generate a cytoprotective effect on polychlorinated biphenyl- induced oxidative stress in testicular Leydig cells. Trakya University Journal of Natural Sciences, 25(1), 55-64. https://doi.org/10.23902/trkjnat.1398909
AMA Aydin Y, Orta Yılmaz B, Erkan M. Vitamin E and genistein generate a cytoprotective effect on polychlorinated biphenyl- induced oxidative stress in testicular Leydig cells. Trakya Univ J Nat Sci. Nisan 2024;25(1):55-64. doi:10.23902/trkjnat.1398909
Chicago Aydin, Yasemin, Banu Orta Yılmaz, ve Melike Erkan. “Vitamin E and Genistein Generate a Cytoprotective Effect on Polychlorinated Biphenyl- Induced Oxidative Stress in Testicular Leydig Cells”. Trakya University Journal of Natural Sciences 25, sy. 1 (Nisan 2024): 55-64. https://doi.org/10.23902/trkjnat.1398909.
EndNote Aydin Y, Orta Yılmaz B, Erkan M (01 Nisan 2024) Vitamin E and genistein generate a cytoprotective effect on polychlorinated biphenyl- induced oxidative stress in testicular Leydig cells. Trakya University Journal of Natural Sciences 25 1 55–64.
IEEE Y. Aydin, B. Orta Yılmaz, ve M. Erkan, “Vitamin E and genistein generate a cytoprotective effect on polychlorinated biphenyl- induced oxidative stress in testicular Leydig cells”, Trakya Univ J Nat Sci, c. 25, sy. 1, ss. 55–64, 2024, doi: 10.23902/trkjnat.1398909.
ISNAD Aydin, Yasemin vd. “Vitamin E and Genistein Generate a Cytoprotective Effect on Polychlorinated Biphenyl- Induced Oxidative Stress in Testicular Leydig Cells”. Trakya University Journal of Natural Sciences 25/1 (Nisan 2024), 55-64. https://doi.org/10.23902/trkjnat.1398909.
JAMA Aydin Y, Orta Yılmaz B, Erkan M. Vitamin E and genistein generate a cytoprotective effect on polychlorinated biphenyl- induced oxidative stress in testicular Leydig cells. Trakya Univ J Nat Sci. 2024;25:55–64.
MLA Aydin, Yasemin vd. “Vitamin E and Genistein Generate a Cytoprotective Effect on Polychlorinated Biphenyl- Induced Oxidative Stress in Testicular Leydig Cells”. Trakya University Journal of Natural Sciences, c. 25, sy. 1, 2024, ss. 55-64, doi:10.23902/trkjnat.1398909.
Vancouver Aydin Y, Orta Yılmaz B, Erkan M. Vitamin E and genistein generate a cytoprotective effect on polychlorinated biphenyl- induced oxidative stress in testicular Leydig cells. Trakya Univ J Nat Sci. 2024;25(1):55-64.

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