Expression of Apoptosis-Related Genes in Cultured Ovarian Tissue of Mouse in Presence of Coenzyme Q10
Abstract
Objective: Oxidative stress affects the development of ovarian follicles during in vitro culture thus applying an antioxidant is necessary. The aim of this study was to investigate the effect of coenzyme Q10 (CoQ10) on the expression of apoptosis-related genes of mouse ovaries during in vitro culture.
Materials and methods: The immature mouse ovaries were cultured in the presence of 50 μM CoQ10 for 7 days. Histological examinations were performed and the 17 beta-estradiol concentration was measured on the seventh day of culture. The relative expression of Caspase 3, Bax, Bad, and Bcl 2 genes were investigated by real-time RT-PCR.
Results: The rates of normal follicles in the presence of CoQ10 was significantly increased compared to the control group. Also, in CoQ10-trated group a significant increase in the level of 17 beta-estradiol was seen compared to the control group. The mRNA expression of anti-apoptotic gene Bcl2 was significantly increased while the expression of pro-apoptotic genes (Caspase3, Bax and Bad) significantly declined in CoQ10 treated group compared to those of control group.
Conclusion: The supplementation of the ovarian culture media with CoQ10 improved the follicular development through alteration in expression of apoptosis-related genes and stimulated the production of estradiol.
Ferreri J, Fàbregues F, Calafell JM, Solernou R, Borrás A, Saco A, et al. Drug-free in-vitro activation of follicles and fresh tissue autotransplantation as a therapeutic option in patients with primary ovarian insufficiency. Reprod Biomed Online. 2020;40(2):254-60.
2. Devenutto L, Quintana R, Quintana T. In vitro activation of ovarian cortex and autologous transplantation: A novel approach to primary ovarian insufficiency and diminished ovarian reserve. Hum Reprod Open. 2020;2020(4):hoaa046.
3. Lee HN, Chang EM. Primordial follicle activation as new treatment for primary ovarian insufficiency. Clin Exp Reprod Med. 2019;46(2):43-9.
4. Ghezelayagh Z, Abtahi NS, Valojerdi MR, Mehdizadeh A, Ebrahimi B. The combination of basic fibroblast growth factor and kit ligand promotes the proliferation, activity and steroidogenesis of granulosa cells during human ovarian cortical culture. Cryobiology. 2020;96:30-6.
5. Cavalcante BN, Matos‐Brito BG, Paulino LR, Silva BR, Aguiar AWM, de Almeida EFM, et al. Effects of melatonin on morphology and development of primordial follicles during in vitro culture of bovine ovarian tissue. Reprod Domest Anim. 2019;54(12):1567-73.
6. Hovatta O, Silye R, Abir R, Krausz T, Winston R. Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum Reprod. 1997;12(5):1032-6.
7. Abedpour N, Salehnia M, Ghorbanmehr N. The Effects of Lysophosphatidic Acid on the incidence of cell death in cultured vitrified and non-vitrified mouse ovarian tissue: separation of necrosis and apoptosis border. Cell J. 2018;20(3):403-11.
8. Mirończuk-Chodakowska I, Witkowska AM, Zujko ME. Endogenous non-enzymatic antioxidants in the human body. Adv Med Sci. 2018;63(1):68-78.
9. Nimse SB, Pal D. Free radicals, natural antioxidants, and their reaction mechanisms. RSC Adv. 2015;5(35):27986-8006.
10. Bhagavan HN, Chopra RK. Coenzyme Q10: absorption, tissue uptake, metabolism and pharmacokinetics. Free Radic Res. 2006;40(5):445-53.
11. Bentinger M, Tekle M, Dallner G. Coenzyme
Q–biosynthesis and functions. Biochem Biophys Res Commun. 2010;396(1):74-9.
12. Lee CH, Kang MK, Sohn DH, Kim HM, Yang J, Han
SJ. Coenzyme Q10 ameliorates the quality of mouse oocytes during in vitro culture. Zygote. 2022;30(2):249-57.
13. Hosseinzadeh E, Zavareh S, Lashkarbolouki T. Antioxidant properties of coenzyme Q10‐pretreated mouse pre‐antral follicles derived from vitrified ovaries. J Obstet Gynaecol Res. 2017;43(1):140-8.
14. Ruiz‐Conca M, Vendrell M, Sabés‐Alsina M, Mogas T, Lopez‐Bejar M. Coenzyme Q10 supplementation during in vitro maturation of bovine oocytes (Bos taurus) helps to preserve oocyte integrity after vitrification. Reprod Domest Anim. 2017;52:52-4.
15. Kashka RH, Zavareh S, Lashkarboluki T. The role of Coenzyme Q10on the Total Antioxidant Capacity of Mouse Vitrified Pre-Antral Follicles. Arch Adv Biosci. 2015;6(3):1-9.
16. Heydarnejad A, Ostadhosseini S, Varnosfaderani SR, Jafarpour F, Moghimi A, Nasr‐Esfahani MH. Supplementation of maturation medium with CoQ10 enhances developmental competence of ovine oocytes through improvement of mitochondrial function. Mol Reprod Dev. 2019;86:812-24.
17. Abdulhasan M, Li Q, Dai J, Abu-Soud H, Puscheck E, Rappolee D. CoQ10 increases mitochondrial mass and polarization, ATP and Oct4 potency levels, and bovine oocyte MII during IVM while decreasing AMPK activity and oocyte death. J Assist Reprod Genet. 2017;34(12):1595-607.
18. Ben‐Meir A, Burstein E, Borrego‐Alvarez A, Chong J, Wong E, Yavorska T, et al. Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging. Aging Cell. 2015;14(5):887-95.
19. Zhang M, ShiYang X, Zhang Y, Miao Y, Chen Y, Cui Z, et al. Coenzyme Q10 ameliorates the quality of postovulatory aged oocytes by suppressing DNA damage and apoptosis. Free Radic Biol Med. 2019;143:84-94.
20. Liang S, Niu YJ, Shin K-T, Cui X-S. Protective effects of coenzyme q10 on developmental competence of porcine early embryos. Microsc Microanal. 2017;23(4):849-58.
21. Sinha K, Das J, Pal PB, Sil PC. Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol. 2013;87(7):
1157-80.
22. Dehghan M, Shahbazi S, Salehnia M. Lysophosphatidic acid alters the expression of apoptosis related genes and miR-22 in cultured and autotransplanted ovaries. Cell J. 2021;23(5):584.
23. Sadeu J, Adriaenssens T, Smitz J. Expression of growth differentiation factor 9, bone morphogenetic protein 15, and anti-Mullerian hormone in cultured mouse primary follicles. Reproduction. 2008;136(2):195-203.
24. Nasiri M, Saadat M, Karimi MH, Azarpira N, Saadat I. Evaluating mRNA Expression Levels of the TLR4/IRF5 Signaling Axis During Hepatic Ischemia-Reperfusion Injuries. Experimental and clinical transplantation : official journal of the Middle East Society for Organ Transplantation. 2019;17(5):648-52.
25. Ma L, Hu M, Ma X, Cui Y, Liu J. CoQ10 decreases aneuploidy rate and increases mitochondrial mass during in vitro maturation of human immature oocytes. Fertil Steril. 2018;110(4):e312.
26. Casper R, Ben-Meir A, Bentov Y, Esfandiari N, Jurisicova A. Cumulus cell CoQ10 synthesis and mitochondrial function in aged mice: effect of CoQ10 supplementation. Fertil Steril. 2012;98(3):S152.
27. Yang C-X, Liu S, Miao J-K, Mou Q, Liu X-M, Wang P-C, et al. CoQ10 improves meiotic maturation of pig oocytes through enhancing mitochondrial function and suppressing oxidative stress. Theriogenology. 2021;159:77-86.
28. Sharideh H, Zhandi M, Zeinoaldini S, Zaghari M, Sadeghi M, Akhlaghi A, et al. Beneficial effects of dietary coenzyme Q10 on the productive and reproductive variables of broiler breeder hens. Anim Reprod Sci. 2020;213:106256.
29. Delkhosh A, Delashoub M, Tehrani AA, Bahrami AM, Niazi V, Shoorei H, et al. Upregulation of FSHR and PCNA by administration of coenzyme Q10 on cyclophosphamide‐induced premature ovarian failure in a mouse model. J Biochem Mol Toxicol. 2019;33(11):e22398.
30. Lee HJ, Park MJ, Joo BS, Joo JK, Kim YH, Yang SW, et al. Effects of coenzyme Q10 on ovarian surface epithelium-derived ovarian stem cells and ovarian function in a 4-vinylcyclohexene diepoxide-induced murine model of ovarian failure. Reprod Biol Endocrinol. 2021;19(1): 59.
31. Pajokh M, Salehnia M. Evaluation of the Follicular Growth during Mouse Ovarian Culture in Medium Supplemented with Different Doses of Growth Differentiation Factor 9B. Pathobiol Res. 2013;16(3):43-51.
32. Kumari S, Mehta SL, Milledge GZ, Huang X, Li H,
Li PA. Ubisol-Q10 prevents glutamate-induced cell death by blocking mitochondrial fragmentation and permeability transition pore opening. Int J Biol Sci. 2016;12(6):688.
2. Devenutto L, Quintana R, Quintana T. In vitro activation of ovarian cortex and autologous transplantation: A novel approach to primary ovarian insufficiency and diminished ovarian reserve. Hum Reprod Open. 2020;2020(4):hoaa046.
3. Lee HN, Chang EM. Primordial follicle activation as new treatment for primary ovarian insufficiency. Clin Exp Reprod Med. 2019;46(2):43-9.
4. Ghezelayagh Z, Abtahi NS, Valojerdi MR, Mehdizadeh A, Ebrahimi B. The combination of basic fibroblast growth factor and kit ligand promotes the proliferation, activity and steroidogenesis of granulosa cells during human ovarian cortical culture. Cryobiology. 2020;96:30-6.
5. Cavalcante BN, Matos‐Brito BG, Paulino LR, Silva BR, Aguiar AWM, de Almeida EFM, et al. Effects of melatonin on morphology and development of primordial follicles during in vitro culture of bovine ovarian tissue. Reprod Domest Anim. 2019;54(12):1567-73.
6. Hovatta O, Silye R, Abir R, Krausz T, Winston R. Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum Reprod. 1997;12(5):1032-6.
7. Abedpour N, Salehnia M, Ghorbanmehr N. The Effects of Lysophosphatidic Acid on the incidence of cell death in cultured vitrified and non-vitrified mouse ovarian tissue: separation of necrosis and apoptosis border. Cell J. 2018;20(3):403-11.
8. Mirończuk-Chodakowska I, Witkowska AM, Zujko ME. Endogenous non-enzymatic antioxidants in the human body. Adv Med Sci. 2018;63(1):68-78.
9. Nimse SB, Pal D. Free radicals, natural antioxidants, and their reaction mechanisms. RSC Adv. 2015;5(35):27986-8006.
10. Bhagavan HN, Chopra RK. Coenzyme Q10: absorption, tissue uptake, metabolism and pharmacokinetics. Free Radic Res. 2006;40(5):445-53.
11. Bentinger M, Tekle M, Dallner G. Coenzyme
Q–biosynthesis and functions. Biochem Biophys Res Commun. 2010;396(1):74-9.
12. Lee CH, Kang MK, Sohn DH, Kim HM, Yang J, Han
SJ. Coenzyme Q10 ameliorates the quality of mouse oocytes during in vitro culture. Zygote. 2022;30(2):249-57.
13. Hosseinzadeh E, Zavareh S, Lashkarbolouki T. Antioxidant properties of coenzyme Q10‐pretreated mouse pre‐antral follicles derived from vitrified ovaries. J Obstet Gynaecol Res. 2017;43(1):140-8.
14. Ruiz‐Conca M, Vendrell M, Sabés‐Alsina M, Mogas T, Lopez‐Bejar M. Coenzyme Q10 supplementation during in vitro maturation of bovine oocytes (Bos taurus) helps to preserve oocyte integrity after vitrification. Reprod Domest Anim. 2017;52:52-4.
15. Kashka RH, Zavareh S, Lashkarboluki T. The role of Coenzyme Q10on the Total Antioxidant Capacity of Mouse Vitrified Pre-Antral Follicles. Arch Adv Biosci. 2015;6(3):1-9.
16. Heydarnejad A, Ostadhosseini S, Varnosfaderani SR, Jafarpour F, Moghimi A, Nasr‐Esfahani MH. Supplementation of maturation medium with CoQ10 enhances developmental competence of ovine oocytes through improvement of mitochondrial function. Mol Reprod Dev. 2019;86:812-24.
17. Abdulhasan M, Li Q, Dai J, Abu-Soud H, Puscheck E, Rappolee D. CoQ10 increases mitochondrial mass and polarization, ATP and Oct4 potency levels, and bovine oocyte MII during IVM while decreasing AMPK activity and oocyte death. J Assist Reprod Genet. 2017;34(12):1595-607.
18. Ben‐Meir A, Burstein E, Borrego‐Alvarez A, Chong J, Wong E, Yavorska T, et al. Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging. Aging Cell. 2015;14(5):887-95.
19. Zhang M, ShiYang X, Zhang Y, Miao Y, Chen Y, Cui Z, et al. Coenzyme Q10 ameliorates the quality of postovulatory aged oocytes by suppressing DNA damage and apoptosis. Free Radic Biol Med. 2019;143:84-94.
20. Liang S, Niu YJ, Shin K-T, Cui X-S. Protective effects of coenzyme q10 on developmental competence of porcine early embryos. Microsc Microanal. 2017;23(4):849-58.
21. Sinha K, Das J, Pal PB, Sil PC. Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol. 2013;87(7):
1157-80.
22. Dehghan M, Shahbazi S, Salehnia M. Lysophosphatidic acid alters the expression of apoptosis related genes and miR-22 in cultured and autotransplanted ovaries. Cell J. 2021;23(5):584.
23. Sadeu J, Adriaenssens T, Smitz J. Expression of growth differentiation factor 9, bone morphogenetic protein 15, and anti-Mullerian hormone in cultured mouse primary follicles. Reproduction. 2008;136(2):195-203.
24. Nasiri M, Saadat M, Karimi MH, Azarpira N, Saadat I. Evaluating mRNA Expression Levels of the TLR4/IRF5 Signaling Axis During Hepatic Ischemia-Reperfusion Injuries. Experimental and clinical transplantation : official journal of the Middle East Society for Organ Transplantation. 2019;17(5):648-52.
25. Ma L, Hu M, Ma X, Cui Y, Liu J. CoQ10 decreases aneuploidy rate and increases mitochondrial mass during in vitro maturation of human immature oocytes. Fertil Steril. 2018;110(4):e312.
26. Casper R, Ben-Meir A, Bentov Y, Esfandiari N, Jurisicova A. Cumulus cell CoQ10 synthesis and mitochondrial function in aged mice: effect of CoQ10 supplementation. Fertil Steril. 2012;98(3):S152.
27. Yang C-X, Liu S, Miao J-K, Mou Q, Liu X-M, Wang P-C, et al. CoQ10 improves meiotic maturation of pig oocytes through enhancing mitochondrial function and suppressing oxidative stress. Theriogenology. 2021;159:77-86.
28. Sharideh H, Zhandi M, Zeinoaldini S, Zaghari M, Sadeghi M, Akhlaghi A, et al. Beneficial effects of dietary coenzyme Q10 on the productive and reproductive variables of broiler breeder hens. Anim Reprod Sci. 2020;213:106256.
29. Delkhosh A, Delashoub M, Tehrani AA, Bahrami AM, Niazi V, Shoorei H, et al. Upregulation of FSHR and PCNA by administration of coenzyme Q10 on cyclophosphamide‐induced premature ovarian failure in a mouse model. J Biochem Mol Toxicol. 2019;33(11):e22398.
30. Lee HJ, Park MJ, Joo BS, Joo JK, Kim YH, Yang SW, et al. Effects of coenzyme Q10 on ovarian surface epithelium-derived ovarian stem cells and ovarian function in a 4-vinylcyclohexene diepoxide-induced murine model of ovarian failure. Reprod Biol Endocrinol. 2021;19(1): 59.
31. Pajokh M, Salehnia M. Evaluation of the Follicular Growth during Mouse Ovarian Culture in Medium Supplemented with Different Doses of Growth Differentiation Factor 9B. Pathobiol Res. 2013;16(3):43-51.
32. Kumari S, Mehta SL, Milledge GZ, Huang X, Li H,
Li PA. Ubisol-Q10 prevents glutamate-induced cell death by blocking mitochondrial fragmentation and permeability transition pore opening. Int J Biol Sci. 2016;12(6):688.
| Files | ||
| Issue | Vol 17, No 2 (June 2023) | |
| Section | Original Articles | |
| DOI | https://doi.org/10.18502/jfrh.v17i2.12868 | |
| Keywords | ||
| Apoptosis Coenzyme Q10 In Vitro Culture Ovarian Tissue | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Behnam S, Zavareh S, Salehnia M. Expression of Apoptosis-Related Genes in Cultured Ovarian Tissue of Mouse in Presence of Coenzyme Q10. J Family Reprod Health. 2023;17(2):65-72.
