Bisfenol F’nin Sıçan Pankreası Üzerindeki Toksik Etkileri
Year 2022,
, 436 - 451, 30.08.2022
Emine Doğan
,
Burak Kaptaner
,
Abdulahad Doğan
Abstract
Bu çalışmada, bisfenol F (BPF)’nin sıçan pankreası üzerindeki toksik etkilerinin belirlenmesi amaçlandı. Bu amaç doğrultusunda yirmi sekiz adet Wistar albino erkek sıçan, BPF’ye 0, 20, 100 ve 500 mg/kg vücut ağırlığı (v.a.) konsantrasyonlarda, 28 gün boyunca oral gavaj ile maruz bırakıldı. Histolojik incelemelere göre BPF maruziyeti sonrasında, pankreatik Langerhans adacıklarında vakuolar dejenerasyon gösteren hücrelerin varlığı tespit edildi. Histomorfolojik ölçümler, BPF’nin 100 ve 500 mg/kg v.a. konsantrasyonlarına maruz bırakılan gruplarda, adacık çap ve alan ortalamalarının düştüğünü gösterdi. Ek olarak, adacıklarda immunohistokimyasal olarak boyayan insülin pozitif hücre yüzdesinin, BPF uygulanan bütün gruplarda, anlamlı bir şekilde azaldığı tespit edildi. Serum açlık glukoz, total kan HbA1c ve serum C-peptid ile insülin seviyelerinin, BPF maruziyeti sonrasında anlamlı değişimler göstermedikleri gözlendi. BPF’nin malondialdehit düzeyi dışında, pankreas antioksidan savunma sistemi belirteçlerinde anlamlı değişimlere yol açtığı belirlendi. Elde edilen sonuçlar BPF’nin endüstriyel alanlarda, bisfenol A yerine güvenilir bir alternatif olarak, kullanımına daha fazla dikkat edilmesi gerektiğini göstermektedir.
Supporting Institution
Van Yüzüncü Yıl Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi
Project Number
FYL-2021-9360
Thanks
Bu çalışma Van Yüzüncü Yıl Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi (Van YYÜ BAPB) tarafından, “FYL-2021-9360” numaralı proje olarak desteklenmiştir. Van YYÜ BAPB’na, sağladığı maddi destekten dolayı, teşekkür ederiz.
References
- Abdel-Wahab, W. M. (2014). Thymoquinone attenuates toxicity and oxidative stress induced by bisphenol A in liver of male rats. Pakistan Journal of Biological Sciences, 17(11), 1152-1160. doi: 10.3923/pjbs.2014.l 152.1160
- Aboul Ezz, H. S., Khadrawy, Y. A., & Mourad, I. M. (2015). The effect of bisphenol A on some oxidative stress parameters and acetylcholinesterase activity in the heart of male albino rats. Cytotechnology, 6 (1), 145-155. doi: 10.1007/s10616-013-9672-1
- Aebi, H. (1974). Catalase. In H. U. Bergemeyer (Ed.), Methods of Enzymatic Analysis (pp. 673–684). Academic Press.
- Agustine, F. N., Prasetyarini, S., & Hamzah, Z. (2019). Effect of BPA (Bisphenol A) on blood serum insulin levels in adult male wistar ras. Stomatognatic-Jurnal Kedokteran Gigi, 16 (1), 28-32.
- Ahn, C., Kang, H. S., Lee, J. H., Hong, E. J., Jung, E. M., Yoo, Y. M., & Jeung, E. B. (2018). Bisphenol A and octylphenol exacerbate type 1 diabetes mellitus by disrupting calcium homeostasis in mouse pancreas. Toxicology Letters, 295, 162-172. doi: 10.1016/j.toxlet.2018.06.1071
- Alonso-Magdalena, P., Morimoto, S., Ripoll, C., Fuentes, E., & Nadal, A. (2006). The estrogenic effect of bisphenol A disrupts pancreatic β-cell function in vivo and induces insulin resistance. Environmental Health Perspectives, 114(1), 106-112. doi: 10.1289/ehp.8451
- Alonso-Magdalena, P., Ropero, A. B., Carrera, M. P., Cederroth, C. R., Baquie, M., Gauthier, B. R., Nef, S., Stefani, E., & Nadal, A. (2008). Pancreatic insulin content regulation by the estrogen receptor ERα. PLoS One, 3(4), e2069. doi: 10.1371/journal.pone.0002069
- Andújar, N., Gálvez-Ontiveros, Y., Zafra-Gómez, A., Rodrigo, L., Álvarez-Cubero, M. J., Aguilera, M., Monteagudo, C., & Rivas, A. (2019). Bisphenol A analogues in food and their hormonal and obesogenic effects: a review. Nutrients, 11(9), 2136. doi: 10.3390/nu11092136
- Arroyo-Salgado, B., Garcia-Espiñeira, M., & Olivero-Verbel, J. (2018). Effects of bisphenol A on streptozotocin treated female mice. Indian Journal of Experimental Biology, 56(6), 419-429.
- Ayala, A., Muñoz, M. F., & Argüelles, S. (2014). Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine & Cellular Longevity, 2014: 360438. doi: 10.1155/2014/360438
- Aydoğan, M., Korkmaz, A., Barlas, N., & Kolankaya, D. (2008). The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicology, 249(1), 35-39. doi: 10.1016/j.tox.2008.04.002
- Aykut, H., & Kaptaner, B. (2021). In vitro effects of bisphenol F on antioxidant system indicators in the isolated hepatocytes of rainbow trout (Oncorhyncus mykiss). Molecular Biology Reports, 48(3), 2591-2599. doi: 10.1007/s11033-021-06310-3
- Beutler, E. (1984). Red cell metabolism. In E. Beutler (Eds), A Manual of Biochemical Methods. 3rd, ed. (pp. 105–106). Orlando, FL: Grune & Startton.
- Bindhumol, V., Chitra, K. C., & Mathur, P. P. (2003). Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology, 188(2-3), 117-124. doi: 10.1016/s0300-483x(03)00056-8
- Bodin, J., Bølling, A. K., Samuelsen, M., Becher, R., Løvik, M., & Nygaard, U. C. (2013). Long-term bisphenol A exposure accelerates insulitis development in diabetes-prone NOD mice. Immunopharmacology & Immunotoxicology, 35(3), 349-358. doi: 10.3109/08923973.2013.772195
- Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2): 248-254. doi: 10.1006/abio.1976.9999
- Buege, J. A., & Aust, S. D. (1978). Microsomal lipid peroxidation. Methods in Enzymology, 52, 302-310. doi: 10.1016/s0076-6879(78)52032-6
- Carchia, E., Porreca, I., Almeida, P. J., D'angelo, F., Cuomo, D., Ceccarelli, M., Felice, M. De., Mallardo M., & Ambrosino, C. (2015). Evaluation of low doses BPA-induced perturbation of glycemia by toxicogenomics points to a primary role of pancreatic islets and to the mechanism of toxicity. Cell death & Disease, 6(10), e1959. doi: 10.1038/cddis.2015.319
- Chen, D., Kannan, K., Tan, H., Zheng, Z., Feng, Y. L., Wu, Y., & Widelka, M. (2016). Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity- a review. Environmental Science & Technology, 50(11), 5438-5453. doi: 10.1021/acs.est.5b05387
- Ding, S., Fan, Y., Zhao, N., Yang, H., Ye, X., He, D., Jin, X., Liu, J., Tian, C., Li, H., Xu, S., & Ying, C. (2014). High-fat diet aggravates glucose homeostasis disorder caused by chronic exposure to bisphenol A. Journal of Endocrinology, 221(1), 167–179. doi: 10.1530/JOE-13-0386
- Dra, L. A., Sellami, S., Rais, H., Aziz, F., Aghraz, A., Bekkouche, K., Markouk, M., & Larhsini, M., (2019). Antidiabetic potential of Caralluma europaea against alloxan-induced diabetes in mice. Saudi Journal of Biological Sciences, 26(6), 1171-1178. doi: 10.1016/j.sjbs.2018.05.028
- García-Arévalo, M., Alonso-Magdalena, P., Servitja, J. M., Boronat-Belda, T., Merino, B., Villar-Pazos, S., Medina-Gómez, G., Novials, A., Quesada, I., & Nadal, A. (2016). Maternal exposure to bisphenol-A during pregnancy increases pancreatic β-cell growth during early life in male mice offspring. Endocrinology, 157(11), 4158-4171. doi: 10.1210/en.2016-1390
- Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130-7139. doi: 10.1016/S0021-9258(19)42083-8
- Hanalp, H. C., Kaptaner, B., & Doğan, A. (2021). Protective Effects of Lyophilized Ethanolic Extract of Achillea arabica Kotschy. On the Islet β Cells of Streptozotocin-Induced Diabetic Rats. KSU Journal of Agriculture & Nature 24(4), 689-700. doi: 10.18016/ksutarimdoga.vi.811253
- Hassan, Z. K., Elobeid, M. A., Virk, P., Omer, S. A., ElAmin, M., Daghestani, M. H., & AlOlayan, E. M. (2012). Bisphenol A induces hepatotoxicity through oxidative stress in rat model. Oxidative Medicine & Cellular Longevity, 2012, 194829. doi: 10.1155/2012/194829
- Higashihara, N., Shiraishi, K., Miyata, K., Oshima, Y., Minobe, Y., & Yamasaki, K. (2007). Subacute oral toxicity study of bisphenol F based on the draft protocol for the “Enhanced OECD Test Guideline no. 407”. Archives of Toxicology, 81(12), 825-832. doi: 10.1007/s00204-007-0223-4
- Hwang, S., Lim, J. E., Choi, Y., & Jee, S. H. (2018). Bisphenol A exposure and type 2 diabetes mellitus risk: a meta-analysis. BMC Endocrine Disorders, 18(1), 81. doi:10.1186/s12902-018-0310-y
- Indumathi, D., Jayashree, S., Selvaraj, J., Sathish, S., Mayilvanan, C., Akilavalli, N., & Balasubramanian, K. (2013). Effect of bisphenol-A on insulin signal transduction and glucose oxidation in skeletal muscle of adult male albino rat. Human and Experimental Toxicology, 32(9), 960-971. doi: 10.1177/0960327112470273
- İyigündoğdu, İ., Üstündağ, A., & Duydu, Y. (2020). Toxicological evaluation of bisphenol A and its analogues. Turkish Journal of Pharmaceutical Sciences, 17(4), 457-462. doi: 10.4274/tjps.galenos.2019.58219
- Kabuto, H., Hasuike, S., Minagawa, N., & Shishibori, T., (2003). Effects of bisphenol A on the metabolisms of active oxygen species in mouse tissues. Environmental Research, 93(1), 31-35. doi: 10.1016/s0013-9351(03)00062-8
- Kaya, Ö., & Kaptaner, B. (2016). Antioxidant defense system parameters in isolated fish hepatocytes exposed to bisphenol A - Effect of vitamin C. Acta Biologica Hungarica, 67(3), 225-235. doi: 10.1556/018.67.2016.3.1
- Korkmaz, A., Ahbab, M. A., Kolankaya, D., & Barlas, N. (2010). Influence of vitamin C on bisphenol A, nonylphenol and octylphenol induced oxidative damages in liver of male rats. Food & Chemical Toxicology, 48(10), 2865-2871. doi: 10.1016/j.fct.2010.07.019
- Li, X. (2009). Glutathione and glutathione‐s‐transferase in detoxification mechanisms. General, Applied & Systems Toxicology. doi: 10.1002/9780470744307.gat166
- Lin, Y., Sun, X., Qiu, L., Wei, J., Huang, Q., Fang, C., Ye, T., Kang, M., Shen, H., & Dong, S. (2013). Exposure to bisphenol A induces dysfunction of insulin secretion and apoptosis through the damage of mitochondria in rat insulinoma (INS-1) cells. Cell Death & Disease, 4(1), e460-e460. doi: 10.1038/cddis.2012.206
- Łukaszewicz-Hussain, A. (2003). The role of glutathione and glutathione-related enzymes in antioxidative process. Medycyna Pracy, 54(5), 473-479.
- Maćczak, A., Cyrkler, M., Bukowska, B., & Michałowicz, J. (2017). Bisphenol A, bisphenol S, bisphenol F and bisphenol AF induce different oxidative stress and damage in human red blood cells (in vitro study). Toxicology in Vitro, 41, 143-149. doi: 10.1016/j.tiv.2017.02.018
- Marroqui, L., Martinez-Pinna, J., Castellano-Muñoz, M., Dos Santos, R. S., Medina-Gali, R. M., Soriano, S., Quesada, I., Gustafsson, J. A., Encinar, J. A., & Nadal, A. (2021). Bisphenol-S and Bisphenol-F alter mouse pancreatic β-cell ion channel expression and activity and insulin release through an estrogen receptor ERβ mediated pathway. Chemosphere, 265, 129051. doi: 10.1016/j.chemosphere.2020.129051
- Meister, A., & Anderson, M. E. (1983). Glutathione. Annual Review of Biochemistry, 52(1), 711-760. doi: 10.1146/annurev.bi.52.070183.003431
- Minghong, W., Hai, X., Ming, Y. & Gag, X. (2011) Effects of chronic bisphenol A exposure on hepatic antioxidant parameters in medaka (Oryzias latipes). Toxicological & Environmental Chemistry 93(2), 270–278. doi: 10.1080/02772248.2010.530136
- Modesto, K. A., & Martinez, C. B. R. (2010). Roundup causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere, 78, 294–299. doi:10.1016/j.chemosphere.2009.10.047
- Mohamed, H. Z., & Bastwrous, A. E. (2021). A Histological study on the effects of bisphenol an administration on the liver, spleen and pancreas of adult male albino rats and the possible protective role of lycopene. Egyptian Academic Journal of Biological Sciences, D. Histology & Histochemistry, 13(1), 43-61. doi: 10.21608/eajbsd.2021.159174
- Mustieles, V., D'Cruz, S. C., Couderq, S., Rodríguez-Carrillo, A., Fini, J. B., Hofer, T., Steffensen, I. L., Dirven, H., Baroukig, R., Olea, N., Fernández, M. F., & David, A. (2020). Bisphenol A and its analogues: a comprehensive review to identify and prioritize effect biomarkers for human biomonitoring. Environment International, 144, 105811. doi: 10.1016/j.envint.2020.105811
- Nadal, A., Alonso-Magdalena, P., Soriano, S., Quesada, I., & Ropero, A. B. (2009). The pancreatic β-cell as a target of estrogens and xenoestrogens: implications for blood glucose homeostasis and diabetes. Molecular & Cellular Endocrinology, 304(1-2), 63-68. doi: 10.1016/j.mce.2009.02.016
- Özaydın, T., Öznurlu, Y., Sur, E., Çelik, I., Uluışık, D., & Dayan, M. O. (2018). Effects of bisphenol A on antioxidant system and lipid profile in rats. Biotechnic & Histochemistry, 93(4), 231-238. doi: 10.1080/10520295.2017.1420821
- Paglia, D. E., & Valentine, W. N. (1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory & Clinical Medicine, 70(1), 158-169.
- Pal, S., Sarkar, K., Nath, P. P., Mondal, M., Khatun, A., & Paul, G. (2017). Bisphenol S impairs blood functions and induces cardiovascular risks in rats. Toxicology Reports, 4, 560-565. doi: 10.1016/j.toxrep.2017.10.006
- Pigeolet, E., Corbisier, P., Houbion, A., Lambert, D., Michiels, C., Raes, M., & Remacle, J. (1990). Glutathione peroxidase, superoxide dismutase, and catalase inactivation by peroxides and oxygen derived free radicals. Mechanisms of Ageing & Development, 51(3), 283-297. doi: 10.1016/0047-6374(90)90078-t
- Provvisiero, D. P., Pivonello, C., Muscogiuri, G., Negri, M., De Angelis, C., Simeoli, C., Pivonello, R., & Colao, A. (2016). Influence of bisphenol A on type 2 diabetes mellitus. International Journal of Environmental Research & Public Health, 13(10), 989. doi: 10.3390/ijerph13100989
- Ropero, A. B., Alonso‐Magdalena, P., Garcia‐Garcia, E., Ripoll, C., Fuentes, E., & Nadal, A. (2008). Bisphenol‐A disruption of the endocrine pancreas and blood glucose homeostasis. International Journal of Andrology, 31(2), 194-200. doi: 10.1111/j.1365-2605.2007.00832.x
- Silva, M. M. D., Xavier, L. L. F., Gonçalves, C. F. L., Santos-Silva, A. P., Paiva-Melo, F. D., De Freitas, M. L., Fortunato, R. S., Miranda-Alves, L., & Ferreira, A. C. F. (2018). Bisphenol A increases hydrogen peroxide generation by thyrocytes both in vivo and in vitro. Endocrine Connections, 7(11), 1196-1207. doi: 10.1530/EC-18-0348
- Soriano, S., Alonso-Magdalena, P., Garcia-Arevalo, M., Novials, A., Muhammed, S. J., Salehi, A., Gustafsson, J. A., Quesada, I., & Nadal, A. (2012). Rapid insulinotropic action of low doses of bisphenol-A on mouse and human islets of Langerhans: role of estrogen receptor . PLoS One, 7, e31109. doi: 10.1371/journal.pone.0031109
- Soriano, S., Ropero, A. B., Alonso-Magdalena, P., Ripoll, C., Quesada, I., Gassner, B., Kuhn, M., Gustafsson, J. A., & Nadal, A. (2009). Rapid regulation of KATP channel activity by 17β-estradiol in pancreatic β-cells involves the estrogen receptor β and the atrial natriuretic peptide receptor. Molecular Endocrinology, 23(12), 1973-1982. doi: 10.1210/me.2009-0287
- Ullah, A., Pirzada, M., Afsar, T., Razak, S., Almajwal, A., & Jahan, S. (2019). Effect of bisphenol F, an analog of bisphenol A, on the reproductive functions of male rats. Environmental Health & Preventive Medicine, 24(1), 1-11. doi: 10.1186/s12199-019-0797-5
- Usman, A., Ikhlas, S., & Ahmad, M. (2019). Occurrence, toxicity and endocrine disrupting potential of Bisphenol-B and Bisphenol-F: A mini-review. Toxicology Letters, 312, 222-227. doi: 10.1016/j.toxlet.2019.05.018
- Weldingh, N. M., Jørgensen-Kaur, L., Becher, R., Holme, J. A., Bodin, J., Nygaard, U. C., & Bølling, A. K. (2017). Bisphenol A is more potent than phthalate metabolites in reducing pancreatic β-cell function. BioMed Research International, 2017, 4614379. doi: 10.1155/2017/4614379
- Whitehead, R., Guan, H., Arany, E., Cernea, M., & Yang, K. (2016). Prenatal exposure to bisphenol A alters mouse fetal pancreatic morphology and islet composition. Hormone Molecular Biology & Clinical Investigation, 25(3), 171-179. doi: 10.1515/hmbci-2015-0052
- Yıldız, M., Güleş, Ö., Sandıkçı, M., & Kum, Ş. (2020). Sıçanlarda bisfenol A’nın neden olduğu pankreatik değişimler üzerine koenzim Q10’un etkileri. Harran Üniversitesi Tıp Fakültesi Dergisi, 17(3), 335-341. doi: 10.35440/hutfd.688689
Toxic Effects of Bisphenol F on Rat Pancreas
Year 2022,
, 436 - 451, 30.08.2022
Emine Doğan
,
Burak Kaptaner
,
Abdulahad Doğan
Abstract
In this study, it was aimed to investigate the toxic effects of bisphenol F (BPF) on rat pancreas. Toward this aim, twenty eight male Wistar albino rats were exposed to BPF at concentrations of 0, 20, 100, and 500 mg/kg of body weight (b.w.) via oral gavage for 28 days. According to the histological examinations, the presence of cells displaying vacuolar degeneration in the pancreatic Langerhans islets was determined after BPF exposure. Histomorphometric measurements demonstrated that averages of the islet diameter and area decreased in the groups exposed to BPF concentrations of 100 and 500 mg/kg of b.w. In addition, the percentage of immunohistochemically-stained insulin-positive cells in the islets was determined to have diminished significantly at all of the groups exposed to BPF. The levels of serum fasting glucose, total blood HbA1c, serum C-peptide or insulin did not display significant changes after BPF exposure. BPF was determined to lead significant changes in the antioxidant defense system indicators of the pancreas, except for the malondialdehyde level. The results obtained herein showed that more attention should be given regarding the usage of BPF instead of bisphenol A as a safe alternative in industrial areas.
Project Number
FYL-2021-9360
References
- Abdel-Wahab, W. M. (2014). Thymoquinone attenuates toxicity and oxidative stress induced by bisphenol A in liver of male rats. Pakistan Journal of Biological Sciences, 17(11), 1152-1160. doi: 10.3923/pjbs.2014.l 152.1160
- Aboul Ezz, H. S., Khadrawy, Y. A., & Mourad, I. M. (2015). The effect of bisphenol A on some oxidative stress parameters and acetylcholinesterase activity in the heart of male albino rats. Cytotechnology, 6 (1), 145-155. doi: 10.1007/s10616-013-9672-1
- Aebi, H. (1974). Catalase. In H. U. Bergemeyer (Ed.), Methods of Enzymatic Analysis (pp. 673–684). Academic Press.
- Agustine, F. N., Prasetyarini, S., & Hamzah, Z. (2019). Effect of BPA (Bisphenol A) on blood serum insulin levels in adult male wistar ras. Stomatognatic-Jurnal Kedokteran Gigi, 16 (1), 28-32.
- Ahn, C., Kang, H. S., Lee, J. H., Hong, E. J., Jung, E. M., Yoo, Y. M., & Jeung, E. B. (2018). Bisphenol A and octylphenol exacerbate type 1 diabetes mellitus by disrupting calcium homeostasis in mouse pancreas. Toxicology Letters, 295, 162-172. doi: 10.1016/j.toxlet.2018.06.1071
- Alonso-Magdalena, P., Morimoto, S., Ripoll, C., Fuentes, E., & Nadal, A. (2006). The estrogenic effect of bisphenol A disrupts pancreatic β-cell function in vivo and induces insulin resistance. Environmental Health Perspectives, 114(1), 106-112. doi: 10.1289/ehp.8451
- Alonso-Magdalena, P., Ropero, A. B., Carrera, M. P., Cederroth, C. R., Baquie, M., Gauthier, B. R., Nef, S., Stefani, E., & Nadal, A. (2008). Pancreatic insulin content regulation by the estrogen receptor ERα. PLoS One, 3(4), e2069. doi: 10.1371/journal.pone.0002069
- Andújar, N., Gálvez-Ontiveros, Y., Zafra-Gómez, A., Rodrigo, L., Álvarez-Cubero, M. J., Aguilera, M., Monteagudo, C., & Rivas, A. (2019). Bisphenol A analogues in food and their hormonal and obesogenic effects: a review. Nutrients, 11(9), 2136. doi: 10.3390/nu11092136
- Arroyo-Salgado, B., Garcia-Espiñeira, M., & Olivero-Verbel, J. (2018). Effects of bisphenol A on streptozotocin treated female mice. Indian Journal of Experimental Biology, 56(6), 419-429.
- Ayala, A., Muñoz, M. F., & Argüelles, S. (2014). Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine & Cellular Longevity, 2014: 360438. doi: 10.1155/2014/360438
- Aydoğan, M., Korkmaz, A., Barlas, N., & Kolankaya, D. (2008). The effect of vitamin C on bisphenol A, nonylphenol and octylphenol induced brain damages of male rats. Toxicology, 249(1), 35-39. doi: 10.1016/j.tox.2008.04.002
- Aykut, H., & Kaptaner, B. (2021). In vitro effects of bisphenol F on antioxidant system indicators in the isolated hepatocytes of rainbow trout (Oncorhyncus mykiss). Molecular Biology Reports, 48(3), 2591-2599. doi: 10.1007/s11033-021-06310-3
- Beutler, E. (1984). Red cell metabolism. In E. Beutler (Eds), A Manual of Biochemical Methods. 3rd, ed. (pp. 105–106). Orlando, FL: Grune & Startton.
- Bindhumol, V., Chitra, K. C., & Mathur, P. P. (2003). Bisphenol A induces reactive oxygen species generation in the liver of male rats. Toxicology, 188(2-3), 117-124. doi: 10.1016/s0300-483x(03)00056-8
- Bodin, J., Bølling, A. K., Samuelsen, M., Becher, R., Løvik, M., & Nygaard, U. C. (2013). Long-term bisphenol A exposure accelerates insulitis development in diabetes-prone NOD mice. Immunopharmacology & Immunotoxicology, 35(3), 349-358. doi: 10.3109/08923973.2013.772195
- Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2): 248-254. doi: 10.1006/abio.1976.9999
- Buege, J. A., & Aust, S. D. (1978). Microsomal lipid peroxidation. Methods in Enzymology, 52, 302-310. doi: 10.1016/s0076-6879(78)52032-6
- Carchia, E., Porreca, I., Almeida, P. J., D'angelo, F., Cuomo, D., Ceccarelli, M., Felice, M. De., Mallardo M., & Ambrosino, C. (2015). Evaluation of low doses BPA-induced perturbation of glycemia by toxicogenomics points to a primary role of pancreatic islets and to the mechanism of toxicity. Cell death & Disease, 6(10), e1959. doi: 10.1038/cddis.2015.319
- Chen, D., Kannan, K., Tan, H., Zheng, Z., Feng, Y. L., Wu, Y., & Widelka, M. (2016). Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity- a review. Environmental Science & Technology, 50(11), 5438-5453. doi: 10.1021/acs.est.5b05387
- Ding, S., Fan, Y., Zhao, N., Yang, H., Ye, X., He, D., Jin, X., Liu, J., Tian, C., Li, H., Xu, S., & Ying, C. (2014). High-fat diet aggravates glucose homeostasis disorder caused by chronic exposure to bisphenol A. Journal of Endocrinology, 221(1), 167–179. doi: 10.1530/JOE-13-0386
- Dra, L. A., Sellami, S., Rais, H., Aziz, F., Aghraz, A., Bekkouche, K., Markouk, M., & Larhsini, M., (2019). Antidiabetic potential of Caralluma europaea against alloxan-induced diabetes in mice. Saudi Journal of Biological Sciences, 26(6), 1171-1178. doi: 10.1016/j.sjbs.2018.05.028
- García-Arévalo, M., Alonso-Magdalena, P., Servitja, J. M., Boronat-Belda, T., Merino, B., Villar-Pazos, S., Medina-Gómez, G., Novials, A., Quesada, I., & Nadal, A. (2016). Maternal exposure to bisphenol-A during pregnancy increases pancreatic β-cell growth during early life in male mice offspring. Endocrinology, 157(11), 4158-4171. doi: 10.1210/en.2016-1390
- Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130-7139. doi: 10.1016/S0021-9258(19)42083-8
- Hanalp, H. C., Kaptaner, B., & Doğan, A. (2021). Protective Effects of Lyophilized Ethanolic Extract of Achillea arabica Kotschy. On the Islet β Cells of Streptozotocin-Induced Diabetic Rats. KSU Journal of Agriculture & Nature 24(4), 689-700. doi: 10.18016/ksutarimdoga.vi.811253
- Hassan, Z. K., Elobeid, M. A., Virk, P., Omer, S. A., ElAmin, M., Daghestani, M. H., & AlOlayan, E. M. (2012). Bisphenol A induces hepatotoxicity through oxidative stress in rat model. Oxidative Medicine & Cellular Longevity, 2012, 194829. doi: 10.1155/2012/194829
- Higashihara, N., Shiraishi, K., Miyata, K., Oshima, Y., Minobe, Y., & Yamasaki, K. (2007). Subacute oral toxicity study of bisphenol F based on the draft protocol for the “Enhanced OECD Test Guideline no. 407”. Archives of Toxicology, 81(12), 825-832. doi: 10.1007/s00204-007-0223-4
- Hwang, S., Lim, J. E., Choi, Y., & Jee, S. H. (2018). Bisphenol A exposure and type 2 diabetes mellitus risk: a meta-analysis. BMC Endocrine Disorders, 18(1), 81. doi:10.1186/s12902-018-0310-y
- Indumathi, D., Jayashree, S., Selvaraj, J., Sathish, S., Mayilvanan, C., Akilavalli, N., & Balasubramanian, K. (2013). Effect of bisphenol-A on insulin signal transduction and glucose oxidation in skeletal muscle of adult male albino rat. Human and Experimental Toxicology, 32(9), 960-971. doi: 10.1177/0960327112470273
- İyigündoğdu, İ., Üstündağ, A., & Duydu, Y. (2020). Toxicological evaluation of bisphenol A and its analogues. Turkish Journal of Pharmaceutical Sciences, 17(4), 457-462. doi: 10.4274/tjps.galenos.2019.58219
- Kabuto, H., Hasuike, S., Minagawa, N., & Shishibori, T., (2003). Effects of bisphenol A on the metabolisms of active oxygen species in mouse tissues. Environmental Research, 93(1), 31-35. doi: 10.1016/s0013-9351(03)00062-8
- Kaya, Ö., & Kaptaner, B. (2016). Antioxidant defense system parameters in isolated fish hepatocytes exposed to bisphenol A - Effect of vitamin C. Acta Biologica Hungarica, 67(3), 225-235. doi: 10.1556/018.67.2016.3.1
- Korkmaz, A., Ahbab, M. A., Kolankaya, D., & Barlas, N. (2010). Influence of vitamin C on bisphenol A, nonylphenol and octylphenol induced oxidative damages in liver of male rats. Food & Chemical Toxicology, 48(10), 2865-2871. doi: 10.1016/j.fct.2010.07.019
- Li, X. (2009). Glutathione and glutathione‐s‐transferase in detoxification mechanisms. General, Applied & Systems Toxicology. doi: 10.1002/9780470744307.gat166
- Lin, Y., Sun, X., Qiu, L., Wei, J., Huang, Q., Fang, C., Ye, T., Kang, M., Shen, H., & Dong, S. (2013). Exposure to bisphenol A induces dysfunction of insulin secretion and apoptosis through the damage of mitochondria in rat insulinoma (INS-1) cells. Cell Death & Disease, 4(1), e460-e460. doi: 10.1038/cddis.2012.206
- Łukaszewicz-Hussain, A. (2003). The role of glutathione and glutathione-related enzymes in antioxidative process. Medycyna Pracy, 54(5), 473-479.
- Maćczak, A., Cyrkler, M., Bukowska, B., & Michałowicz, J. (2017). Bisphenol A, bisphenol S, bisphenol F and bisphenol AF induce different oxidative stress and damage in human red blood cells (in vitro study). Toxicology in Vitro, 41, 143-149. doi: 10.1016/j.tiv.2017.02.018
- Marroqui, L., Martinez-Pinna, J., Castellano-Muñoz, M., Dos Santos, R. S., Medina-Gali, R. M., Soriano, S., Quesada, I., Gustafsson, J. A., Encinar, J. A., & Nadal, A. (2021). Bisphenol-S and Bisphenol-F alter mouse pancreatic β-cell ion channel expression and activity and insulin release through an estrogen receptor ERβ mediated pathway. Chemosphere, 265, 129051. doi: 10.1016/j.chemosphere.2020.129051
- Meister, A., & Anderson, M. E. (1983). Glutathione. Annual Review of Biochemistry, 52(1), 711-760. doi: 10.1146/annurev.bi.52.070183.003431
- Minghong, W., Hai, X., Ming, Y. & Gag, X. (2011) Effects of chronic bisphenol A exposure on hepatic antioxidant parameters in medaka (Oryzias latipes). Toxicological & Environmental Chemistry 93(2), 270–278. doi: 10.1080/02772248.2010.530136
- Modesto, K. A., & Martinez, C. B. R. (2010). Roundup causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere, 78, 294–299. doi:10.1016/j.chemosphere.2009.10.047
- Mohamed, H. Z., & Bastwrous, A. E. (2021). A Histological study on the effects of bisphenol an administration on the liver, spleen and pancreas of adult male albino rats and the possible protective role of lycopene. Egyptian Academic Journal of Biological Sciences, D. Histology & Histochemistry, 13(1), 43-61. doi: 10.21608/eajbsd.2021.159174
- Mustieles, V., D'Cruz, S. C., Couderq, S., Rodríguez-Carrillo, A., Fini, J. B., Hofer, T., Steffensen, I. L., Dirven, H., Baroukig, R., Olea, N., Fernández, M. F., & David, A. (2020). Bisphenol A and its analogues: a comprehensive review to identify and prioritize effect biomarkers for human biomonitoring. Environment International, 144, 105811. doi: 10.1016/j.envint.2020.105811
- Nadal, A., Alonso-Magdalena, P., Soriano, S., Quesada, I., & Ropero, A. B. (2009). The pancreatic β-cell as a target of estrogens and xenoestrogens: implications for blood glucose homeostasis and diabetes. Molecular & Cellular Endocrinology, 304(1-2), 63-68. doi: 10.1016/j.mce.2009.02.016
- Özaydın, T., Öznurlu, Y., Sur, E., Çelik, I., Uluışık, D., & Dayan, M. O. (2018). Effects of bisphenol A on antioxidant system and lipid profile in rats. Biotechnic & Histochemistry, 93(4), 231-238. doi: 10.1080/10520295.2017.1420821
- Paglia, D. E., & Valentine, W. N. (1967). Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. Journal of Laboratory & Clinical Medicine, 70(1), 158-169.
- Pal, S., Sarkar, K., Nath, P. P., Mondal, M., Khatun, A., & Paul, G. (2017). Bisphenol S impairs blood functions and induces cardiovascular risks in rats. Toxicology Reports, 4, 560-565. doi: 10.1016/j.toxrep.2017.10.006
- Pigeolet, E., Corbisier, P., Houbion, A., Lambert, D., Michiels, C., Raes, M., & Remacle, J. (1990). Glutathione peroxidase, superoxide dismutase, and catalase inactivation by peroxides and oxygen derived free radicals. Mechanisms of Ageing & Development, 51(3), 283-297. doi: 10.1016/0047-6374(90)90078-t
- Provvisiero, D. P., Pivonello, C., Muscogiuri, G., Negri, M., De Angelis, C., Simeoli, C., Pivonello, R., & Colao, A. (2016). Influence of bisphenol A on type 2 diabetes mellitus. International Journal of Environmental Research & Public Health, 13(10), 989. doi: 10.3390/ijerph13100989
- Ropero, A. B., Alonso‐Magdalena, P., Garcia‐Garcia, E., Ripoll, C., Fuentes, E., & Nadal, A. (2008). Bisphenol‐A disruption of the endocrine pancreas and blood glucose homeostasis. International Journal of Andrology, 31(2), 194-200. doi: 10.1111/j.1365-2605.2007.00832.x
- Silva, M. M. D., Xavier, L. L. F., Gonçalves, C. F. L., Santos-Silva, A. P., Paiva-Melo, F. D., De Freitas, M. L., Fortunato, R. S., Miranda-Alves, L., & Ferreira, A. C. F. (2018). Bisphenol A increases hydrogen peroxide generation by thyrocytes both in vivo and in vitro. Endocrine Connections, 7(11), 1196-1207. doi: 10.1530/EC-18-0348
- Soriano, S., Alonso-Magdalena, P., Garcia-Arevalo, M., Novials, A., Muhammed, S. J., Salehi, A., Gustafsson, J. A., Quesada, I., & Nadal, A. (2012). Rapid insulinotropic action of low doses of bisphenol-A on mouse and human islets of Langerhans: role of estrogen receptor . PLoS One, 7, e31109. doi: 10.1371/journal.pone.0031109
- Soriano, S., Ropero, A. B., Alonso-Magdalena, P., Ripoll, C., Quesada, I., Gassner, B., Kuhn, M., Gustafsson, J. A., & Nadal, A. (2009). Rapid regulation of KATP channel activity by 17β-estradiol in pancreatic β-cells involves the estrogen receptor β and the atrial natriuretic peptide receptor. Molecular Endocrinology, 23(12), 1973-1982. doi: 10.1210/me.2009-0287
- Ullah, A., Pirzada, M., Afsar, T., Razak, S., Almajwal, A., & Jahan, S. (2019). Effect of bisphenol F, an analog of bisphenol A, on the reproductive functions of male rats. Environmental Health & Preventive Medicine, 24(1), 1-11. doi: 10.1186/s12199-019-0797-5
- Usman, A., Ikhlas, S., & Ahmad, M. (2019). Occurrence, toxicity and endocrine disrupting potential of Bisphenol-B and Bisphenol-F: A mini-review. Toxicology Letters, 312, 222-227. doi: 10.1016/j.toxlet.2019.05.018
- Weldingh, N. M., Jørgensen-Kaur, L., Becher, R., Holme, J. A., Bodin, J., Nygaard, U. C., & Bølling, A. K. (2017). Bisphenol A is more potent than phthalate metabolites in reducing pancreatic β-cell function. BioMed Research International, 2017, 4614379. doi: 10.1155/2017/4614379
- Whitehead, R., Guan, H., Arany, E., Cernea, M., & Yang, K. (2016). Prenatal exposure to bisphenol A alters mouse fetal pancreatic morphology and islet composition. Hormone Molecular Biology & Clinical Investigation, 25(3), 171-179. doi: 10.1515/hmbci-2015-0052
- Yıldız, M., Güleş, Ö., Sandıkçı, M., & Kum, Ş. (2020). Sıçanlarda bisfenol A’nın neden olduğu pankreatik değişimler üzerine koenzim Q10’un etkileri. Harran Üniversitesi Tıp Fakültesi Dergisi, 17(3), 335-341. doi: 10.35440/hutfd.688689