Protective effect of coenzyme Q10 supplementation on the oxidative stress and histological injury caused by nicotine in the ovary of rats
Subject Areas :
Veterinary Clinical Pathology
Shahnaz Yousefizadeh
1
(
Assistant Professor, Department of Laboratory and Clinical Sciences, Faculty of Paraveterinary Medicine, Ilam University, Ilam, Iran.
)
Ali Louei monfared
2
(
Associate Professor, Department of Histology and Microbiology, Faculty of Paraveterinary, Ilam University, Ilam, Iran.
)
Yahya Mohammadi
3
(
Associate Professor, Department of Animal Sciences, Faculty of Agriculture, Ilam University, Ilam, Iran.
)
Received: 2023-02-01
Accepted : 2023-05-28
Published : 2023-01-21
Keywords:
Ovary,
Oxidative stress,
Rat,
nicotine,
Coenzyme Q10 supplement,
Abstract :
As a poison, nicotine leaves irreparable effects on various tissues of the body, including the reproductive system. Coenzyme Q10 has a tremendous effect in raising the body's antioxidant level and preventing poisoning. In the current study, the protective effect of coenzyme Q10 supplementation on the changes induced by nicotine in the rat ovary was investigated. For this purpose, 32 adult female Wistar rats were randomly divided into 4 groups of 8. The rats of the first group (control) were only fed with the usual diet, but the animals of the second group were treated with nicotine at the rate of 0.2 mg/kg, the rats of the third group were treated with coenzyme Q10 at the rate of 75 mg/kg and the animals of the fourth group were treated simultaneously using nicotine and coenzyme Q10 (with the same amounts) through gavage. At the end of the study period (45 days), the animals were euthanised and blood samples were taken for hormonal and antioxidant tests. Also, ovarian tissue was sampled for histological studies. In animals treated with nicotine, there was an increase in follicular atresia, tissue damage, an increase in malondialdehyde and nitric oxide, along with a decrease in the number of ovarian follicles, a decrease in the amount of estrogen and follicle stimulating hormones, and the activity of superoxide dismutase, glutathione peroxidase and catalase. But in animals receiving nicotine and coenzyme Q10 at the same time, there was a significant improvement in ovarian function and structure. This study shows coenzyme Q10 can play a protective role against oxidative stress and tissue changes caused by nicotine in the ovaries of rats with the mechanism of balancing the antioxidant status and reproductive hormones.
References:
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Cheng, S.F., Qin, X.S., Han, Z.L., Sun, X.F., Feng, Y.N., Yang, F., et al. (2018). Nicotine exposure impairs germ cell development in human fetal ovaries cultured in vitro. Aging, (Albany NY),10(7): 1556-1574.
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Dechanet, C., Anahory, T., Mathieu Daude, J.C., Quantin, X., Reyftmann, L., Hamamah, S., et al. (2011). Effects of cigarette smoking on reproduction. Human Reproduction Update, 17(1): 76-95.
Emmen, J.M., Couse, J.F., Elmore, S.A., Yates, M.M., Kissling, G.E. and Korach, K.S. (2005). In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER){alpha} and ER{beta} null mice indicate a role for ER{beta} in follicular maturation. Endocrinology, 146(6): 2817-2826.
Faghani, M., Saedi, S., Khanaki, K. and Mohammadghasemi, F. (2022). Ginseng alleviates folliculogenesis disorders via induction of cell proliferation and downregulation of apoptotic markers in nicotine-treated mice. Journal of Ovarian Research, 15(1): 14.
Florou, P., Anagnostis, P., Theocharis, P., Chourdakis, M. and Goulis, D.G. (2020). Does coenzyme Q10 supplementation improve fertility outcomes in women undergoing assisted reproductive technology procedures? A systematic review and meta-analysis of randomized-controlled trials. Journal of Assisted Reproduction and Genetics, 37(10): 2377-2387.
Gutierrez-Mariscal, F.M., Arenas-de Larriva, A.P., Limia-Perez, L., Romero-Cabrera, J.L., Yubero-Serrano, E.M. and López-Miranda, J. (2020). Coenzyme Q10 supplementation for the reduction of oxidative stress: Clinical implications in the treatment of chronic diseases. International Journal of Molecular Sciences, 21(21): 7870.
Halliwell, B. (2012). Free radicals and antioxidants: updating a personal view. Nutrition Reviews, 70(5): 257-265.
Heaton, R.A., Heales, S., Rahman, K., Sexton, D.W. and Hargreaves, I. (2020). The effect of cellular coenzyme Q(10) deficiency on lysosomal acidification. Journal of Clinical Medicine, 9(6): 1923.
Holloway, A.C., Kellenberger, L.D. and Petrik, J.J. (2006). Fetal and neonatal exposure to nicotine disrupts ovarian function and fertility in adult female rats. Endocrinology, 30(2): 213-216.
Hornos Carneiro, M.F., Shin, N., Karthikraj, R., Barbosa, F.Jr., Kannan, K. and Colaiácovo, M.P. (2020). Antioxidant CoQ10 Restores Fertility by Rescuing Bisphenol A-Induced Oxidative DNA Damage in the Caenorhabditis elegans Germline. Genetics, 214(2): 381-395.
Jennings, P.C., Merriman, J.A., Beckett, E.L., Hansbro, P.M. and Jones, K.T. (2011). Increased zona pellucida thickness and meiotic spindle disruption in oocytes from cigarette smoking mice. Human Reproduction, 26(4): 878-884.
Karami, E., Goodarzi, Z., Ghanbari, A., Dehdashti, A., Bandegi, A.R. and Yosefi, S. (2022). Dataset on biochemical markers and histological alterations in rat kidney intoxicated with cadmium chloride and treated with antioxidant. Data in Brief, 43: 1-11.
Kharrazi, M., DeLorenze, G.N., Kaufman, F.L., Eskenazi, B., Bernert, J.T.Jr, Graham, S., et al. (2004). Environmental tobacco smoke and pregnancy outcome. Epidemiology, 15(6): 660-670.
Kiremitli, T., Kiremitli, S., Akselim, B., Yilmaz, B., Mammadov, R., Tor, I.H., et al. (2021). Protective effect of Coenzyme Q10 on oxidative ovarian and uterine damage induced by methotrexate in rats. Human & Experimental Toxicology, 40(9): 1537-1544.
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MacMahon, B., Trichopoulos, D., Cole, P. and Brown, J. (1982). Cigarette smoking and urinary estrogens. The New England Journal of Medicine, 307(17): 1062-1065.
Marcondes, F., Bianchi, F. and Tanno, A. (2002). Determination of the estrous cycle phases of rats: some helpful considerations. Brazilian Journal of Biology, 62(4A): 609-614.
Mohammadghasemi, F., Jahromi, S.K., Hajizadeh, H., Homafar, M.A. and Saadat, N. (2012). The Protective Effects of Exogenous Melatonin on Nicotine-induced Changes in Mouse Ovarian Follicles. Journal of Reproduction and Fertility, 13(3): 143-150.
Mohammadghasemi, F. and Jahromi, S.K. (2018). Melatonin ameliorates testicular damages induced by nicotine in mice. Iranian Journal of Basic Medical Sciences, 21(6): 639-644.
Mohammadghasemi, F., Khanaki, K., Moravati, H. and Faghani, M. (2021). The amelioration of nicotine-induced reproductive impairment in male mouse by Sambucus ebulus fruit extract. Anatomy and Cell Biology, 54(2): 232-240.
Moshtaghi-Kashanian, G.R., Esmaeeli, F. and Dabiri, S. (2005). Enhanced prolactin levels in opium smokers. Addiction Biology, 10(4): 345-349.
Overvad, K., Diamant, B., Holm, L., Holmer, G., Mortensen, S.A. and Stender, S. (1999). Coenzyme Q10 in health and disease. European Journal of Clinical Nutrition, 53(10): 764-770.
Ozcan, P., Fıçıcıoğlu, C., Kizilkale, O., Yesiladali, M., Tok, O.E., Ozkan, F., et al. (2016). Can Coenzyme Q10 supplementation protect the ovarian reserve against oxidative damage? Journal of Assisted Reproduction and Genetics, 33(9): 1223-1230.
Ozcan, P., Ficicioglu, C. and Yesiladali, M. (2015). The protective effect of Coenzyme Q10 supplementation on decreased ovarian reserve in female Sprague-Dawley rats. Fertility and Sterility Abstract Only, 104(3): E255:437.
Ozlem, K., Emin, K. and Birkan Y. (2022). Protective effect of edaravone on cisplatin‑induced injury in rat ovary. Archives of Gynecology and Obstetrics, 306(5): 1673-1678.
Quinzii, C.M., Hirano, M. and DiMauro, S. (2007). CoQ10 Deficiency Diseases in Adults. Mitochondrion. 7(Supp): S122-126.
Rahmani Kahnemoei, J. (2016). The effect of passive inhalation of cigarette smoke on serum fat profile in rats. Journal of Veterinary Clinical Pathology, 10(3): 245-250. [In Persian]
Reuter, S., Gupta, S.C., Chaturvedi, M.M. and Aggarwal, B.B. (2010). Oxidative stress, inflammation, and cancer: how are they linked? Free Radical Biology and Medicine, 49(11): 1603-1616.
Selvaraju, S., Raghavendra, B.S., Subramani, T.S., Priyadharsini, R., Reddy, I.J., and Ravindra, J.P. (2010). Changes in luteal cells distribution, apoptotic rate, lipid peroxidation levels and antioxidant enzyme activities in buffalo (Bubalus bubalis) corpus luteum. Animal Reproduction Science, 120(1-4): 39-46.
Shahin, A.M., Bahrami, A.M., Delkhosh, A. and Shakarami, N. (2022). Evaluation of the effect of Aloevera gel on ovarian tissue structure in Nicotine-receiving Rats. Veterinary Clinical Pathology, 15(4): 319-331. [In Persian]
Sinha-Hikim, I., Friedman, T.C., Falz, M., Chalfant, V., Hasan, M.K., Espinoza-Derout, J., et al. (2017). Nicotine plus a high-fat diet triggers cardiomyocyte apoptosis. Cell and Tissue Research, 368(1): 159-170.
Valavanidis, A., Vlachogianni, T. and Fiotakis, K. (2009). Tobacco smoke: involvement of reactive oxygen species and stable free radicals in mechanisms of oxidative damage, carcinogenesis and synergistic effects with other respirable particles. International Journal of Environmental Research and Public Health, 6(2): 445-462.
Wang, Y.F., Sun, X.F., Han, Z.L., Li, L., Ge, W., Zhao, Y., et al. (2018). Protective effects of melatonin against nicotine-induced disorder of mouse early folliculogenesis. Aging (Albany NY), 10(3): 463-480.
Weydert, C.J. and Cullen, J.J. (2010). Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nature Protocols, 5(1): 51-66.
Xu, Y., Nisenblat, V., Lu, C., Li, R., Qiao, J., Zhen, X. and Wang, S. (2018). Pretreatment with coenzyme Q10 improves ovarian response and embryo quality in low-prognosis young women with decreased ovarian reserve: a randomized controlled trial. Reproductive Biology and Endocrinology, 16(1): 29.
Zhang, T., He, Q., Xiu, H., Zhang, Z., Liu, Y., Chen, Z. and Hu, H. (2022). Efficacy and Safety of Coenzyme Q10 Supplementation in the Treatment of Polycystic Ovary Syndrome: a Systematic Review and Meta-analysis. Reproductive Sciences, 30(4): 1033-1048.
Zhao, S., Wu, W., Liao, J., Zhang, X., Shen, M., Li, X., Lin, Q. and Cao, C. (2022). Molecular mechanisms underlying the renal protective effects of coenzyme Q10 in acute kidney injury. Cellular & Molecular Biology Letters, 27(1): 57.
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Bentov, Y., Esfandiari, N., Burstein, E. and Casper, R.F. (2010). The use of mitochondrial nutrients to improve the outcome of infertility treatment in older patients. Fertility and Sterility, 93(1): 272-275.
Bentov, Y., Yavorska, T., Esfandiari, N., Jurisicova, A. and Casper, R.F. (2011). The contribution of mitochondrial function to reproductive aging. Journal of Assisted Reproduction and Genetics, 28(9): 773-783.
Bruin, J.E., Gerstein, H.C. and Holloway, A.C. (2010). Long-term consequences of fetal and neonatal nicotine exposure: a critical review. Toxicolical Sciences, 116(2): 364-374.
Cheng, S.F., Qin, X.S., Han, Z.L., Sun, X.F., Feng, Y.N., Yang, F., et al. (2018). Nicotine exposure impairs germ cell development in human fetal ovaries cultured in vitro. Aging, (Albany NY),10(7): 1556-1574.
Darabi, Z., Basir, Z., Tabandeh, M. R. and Ghotbeddin, Z. (2022). Coenzyme Q10 improves ovarian histology and attenuates the expression of angiogenesis-associated proteins in the ovary of rats with experimental hyperstimulation syndrome. Iranian Journal of Basic Medical Sciences, 25(8): 989-996.
Dechanet, C., Anahory, T., Mathieu Daude, J.C., Quantin, X., Reyftmann, L., Hamamah, S., et al. (2011). Effects of cigarette smoking on reproduction. Human Reproduction Update, 17(1): 76-95.
Emmen, J.M., Couse, J.F., Elmore, S.A., Yates, M.M., Kissling, G.E. and Korach, K.S. (2005). In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER){alpha} and ER{beta} null mice indicate a role for ER{beta} in follicular maturation. Endocrinology, 146(6): 2817-2826.
Faghani, M., Saedi, S., Khanaki, K. and Mohammadghasemi, F. (2022). Ginseng alleviates folliculogenesis disorders via induction of cell proliferation and downregulation of apoptotic markers in nicotine-treated mice. Journal of Ovarian Research, 15(1): 14.
Florou, P., Anagnostis, P., Theocharis, P., Chourdakis, M. and Goulis, D.G. (2020). Does coenzyme Q10 supplementation improve fertility outcomes in women undergoing assisted reproductive technology procedures? A systematic review and meta-analysis of randomized-controlled trials. Journal of Assisted Reproduction and Genetics, 37(10): 2377-2387.
Gutierrez-Mariscal, F.M., Arenas-de Larriva, A.P., Limia-Perez, L., Romero-Cabrera, J.L., Yubero-Serrano, E.M. and López-Miranda, J. (2020). Coenzyme Q10 supplementation for the reduction of oxidative stress: Clinical implications in the treatment of chronic diseases. International Journal of Molecular Sciences, 21(21): 7870.
Halliwell, B. (2012). Free radicals and antioxidants: updating a personal view. Nutrition Reviews, 70(5): 257-265.
Heaton, R.A., Heales, S., Rahman, K., Sexton, D.W. and Hargreaves, I. (2020). The effect of cellular coenzyme Q(10) deficiency on lysosomal acidification. Journal of Clinical Medicine, 9(6): 1923.
Holloway, A.C., Kellenberger, L.D. and Petrik, J.J. (2006). Fetal and neonatal exposure to nicotine disrupts ovarian function and fertility in adult female rats. Endocrinology, 30(2): 213-216.
Hornos Carneiro, M.F., Shin, N., Karthikraj, R., Barbosa, F.Jr., Kannan, K. and Colaiácovo, M.P. (2020). Antioxidant CoQ10 Restores Fertility by Rescuing Bisphenol A-Induced Oxidative DNA Damage in the Caenorhabditis elegans Germline. Genetics, 214(2): 381-395.
Jennings, P.C., Merriman, J.A., Beckett, E.L., Hansbro, P.M. and Jones, K.T. (2011). Increased zona pellucida thickness and meiotic spindle disruption in oocytes from cigarette smoking mice. Human Reproduction, 26(4): 878-884.
Karami, E., Goodarzi, Z., Ghanbari, A., Dehdashti, A., Bandegi, A.R. and Yosefi, S. (2022). Dataset on biochemical markers and histological alterations in rat kidney intoxicated with cadmium chloride and treated with antioxidant. Data in Brief, 43: 1-11.
Kharrazi, M., DeLorenze, G.N., Kaufman, F.L., Eskenazi, B., Bernert, J.T.Jr, Graham, S., et al. (2004). Environmental tobacco smoke and pregnancy outcome. Epidemiology, 15(6): 660-670.
Kiremitli, T., Kiremitli, S., Akselim, B., Yilmaz, B., Mammadov, R., Tor, I.H., et al. (2021). Protective effect of Coenzyme Q10 on oxidative ovarian and uterine damage induced by methotrexate in rats. Human & Experimental Toxicology, 40(9): 1537-1544.
Kole, E., Ozkan, S.O., Eraldemir, C., Akar, F.Y., Ozbek, S.K., Kole, M.C., et al. (2020). Effects of melatonin on ovarian reserve in cigarette smoking: an experimental study. Archives of Medical Science, 16(6): 1376-1386.
MacMahon, B., Trichopoulos, D., Cole, P. and Brown, J. (1982). Cigarette smoking and urinary estrogens. The New England Journal of Medicine, 307(17): 1062-1065.
Marcondes, F., Bianchi, F. and Tanno, A. (2002). Determination of the estrous cycle phases of rats: some helpful considerations. Brazilian Journal of Biology, 62(4A): 609-614.
Mohammadghasemi, F., Jahromi, S.K., Hajizadeh, H., Homafar, M.A. and Saadat, N. (2012). The Protective Effects of Exogenous Melatonin on Nicotine-induced Changes in Mouse Ovarian Follicles. Journal of Reproduction and Fertility, 13(3): 143-150.
Mohammadghasemi, F. and Jahromi, S.K. (2018). Melatonin ameliorates testicular damages induced by nicotine in mice. Iranian Journal of Basic Medical Sciences, 21(6): 639-644.
Mohammadghasemi, F., Khanaki, K., Moravati, H. and Faghani, M. (2021). The amelioration of nicotine-induced reproductive impairment in male mouse by Sambucus ebulus fruit extract. Anatomy and Cell Biology, 54(2): 232-240.
Moshtaghi-Kashanian, G.R., Esmaeeli, F. and Dabiri, S. (2005). Enhanced prolactin levels in opium smokers. Addiction Biology, 10(4): 345-349.
Overvad, K., Diamant, B., Holm, L., Holmer, G., Mortensen, S.A. and Stender, S. (1999). Coenzyme Q10 in health and disease. European Journal of Clinical Nutrition, 53(10): 764-770.
Ozcan, P., Fıçıcıoğlu, C., Kizilkale, O., Yesiladali, M., Tok, O.E., Ozkan, F., et al. (2016). Can Coenzyme Q10 supplementation protect the ovarian reserve against oxidative damage? Journal of Assisted Reproduction and Genetics, 33(9): 1223-1230.
Ozcan, P., Ficicioglu, C. and Yesiladali, M. (2015). The protective effect of Coenzyme Q10 supplementation on decreased ovarian reserve in female Sprague-Dawley rats. Fertility and Sterility Abstract Only, 104(3): E255:437.
Ozlem, K., Emin, K. and Birkan Y. (2022). Protective effect of edaravone on cisplatin‑induced injury in rat ovary. Archives of Gynecology and Obstetrics, 306(5): 1673-1678.
Quinzii, C.M., Hirano, M. and DiMauro, S. (2007). CoQ10 Deficiency Diseases in Adults. Mitochondrion. 7(Supp): S122-126.
Rahmani Kahnemoei, J. (2016). The effect of passive inhalation of cigarette smoke on serum fat profile in rats. Journal of Veterinary Clinical Pathology, 10(3): 245-250. [In Persian]
Reuter, S., Gupta, S.C., Chaturvedi, M.M. and Aggarwal, B.B. (2010). Oxidative stress, inflammation, and cancer: how are they linked? Free Radical Biology and Medicine, 49(11): 1603-1616.
Selvaraju, S., Raghavendra, B.S., Subramani, T.S., Priyadharsini, R., Reddy, I.J., and Ravindra, J.P. (2010). Changes in luteal cells distribution, apoptotic rate, lipid peroxidation levels and antioxidant enzyme activities in buffalo (Bubalus bubalis) corpus luteum. Animal Reproduction Science, 120(1-4): 39-46.
Shahin, A.M., Bahrami, A.M., Delkhosh, A. and Shakarami, N. (2022). Evaluation of the effect of Aloevera gel on ovarian tissue structure in Nicotine-receiving Rats. Veterinary Clinical Pathology, 15(4): 319-331. [In Persian]
Sinha-Hikim, I., Friedman, T.C., Falz, M., Chalfant, V., Hasan, M.K., Espinoza-Derout, J., et al. (2017). Nicotine plus a high-fat diet triggers cardiomyocyte apoptosis. Cell and Tissue Research, 368(1): 159-170.
Valavanidis, A., Vlachogianni, T. and Fiotakis, K. (2009). Tobacco smoke: involvement of reactive oxygen species and stable free radicals in mechanisms of oxidative damage, carcinogenesis and synergistic effects with other respirable particles. International Journal of Environmental Research and Public Health, 6(2): 445-462.
Wang, Y.F., Sun, X.F., Han, Z.L., Li, L., Ge, W., Zhao, Y., et al. (2018). Protective effects of melatonin against nicotine-induced disorder of mouse early folliculogenesis. Aging (Albany NY), 10(3): 463-480.
Weydert, C.J. and Cullen, J.J. (2010). Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nature Protocols, 5(1): 51-66.
Xu, Y., Nisenblat, V., Lu, C., Li, R., Qiao, J., Zhen, X. and Wang, S. (2018). Pretreatment with coenzyme Q10 improves ovarian response and embryo quality in low-prognosis young women with decreased ovarian reserve: a randomized controlled trial. Reproductive Biology and Endocrinology, 16(1): 29.
Zhang, T., He, Q., Xiu, H., Zhang, Z., Liu, Y., Chen, Z. and Hu, H. (2022). Efficacy and Safety of Coenzyme Q10 Supplementation in the Treatment of Polycystic Ovary Syndrome: a Systematic Review and Meta-analysis. Reproductive Sciences, 30(4): 1033-1048.
Zhao, S., Wu, W., Liao, J., Zhang, X., Shen, M., Li, X., Lin, Q. and Cao, C. (2022). Molecular mechanisms underlying the renal protective effects of coenzyme Q10 in acute kidney injury. Cellular & Molecular Biology Letters, 27(1): 57.
