Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-05-05T09:57:52.975Z Has data issue: false hasContentIssue false
  • English
  • Français

Kisspeptin decreases the adverse effects of human ovarian vitrification by regulating ROS-related apoptotic occurrences

Published online by Cambridge University Press:  01 September 2023

Anahita Tavakoli Open the ORCID record for Anahita Tavakoli [Opens in a new window] ,
Fereshteh Aliakbari  and
Malek Soleimani Mehranjani
Anahita Tavakoli
Affiliation:
Department of Biology, Faculty of Science, Arak University, Arak, Iran
Fereshteh Aliakbari
Affiliation:
Fereshteh Aliakbari, Men’s Health and Reproductive Health Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
Malek Soleimani Mehranjani*
Affiliation:
Department of Biology, Faculty of Science, Arak University, Arak, Iran
*
Corresponding author: Malek Soleimani Mehranjani; Email: m-soleimani@araku.ac.ir
Get access Rights & Permissions [Opens in a new window]

Summary

Kisspeptin is characterized as a neuropeptide with a pivotal function in female and male infertility, and its antioxidant properties have been demonstrated. In this study, the effects of kisspeptin on the improvement of the vitrification and thawing results of human ovarian tissues were investigated. In this work, 12 ovaries from patients who underwent hysterectomy were collected laparoscopically, and then 32 samples from each of their tissues were taken. Haematoxylin and eosin (H&E) staining was performed to check the normality of the ovarian tissue and, subsequently, the samples were allocated randomly into four groups, including: (1) fresh (control), (2) vitrification, (3) vitrified + 1 μM kisspeptin, and (4) vitrified + 10 μM kisspeptin groups. After vitrification, thawing, and tissue culture processes, H&E staining for tissue quality assessment, terminal deoxynucleotidyl transferase dUTP nick end labelling assay for apoptosis evaluation, and malondialdehyde (MDA), superoxide dismutase (SOD), and ferric reducing ability of plasma tests for oxidative stress appraisal were carried out. Our histological results showed incoherency of ovarian tissue morphology in the vitrification group compared with other groups. Other findings implicated increased apoptosis rate and MDA concentration and reduced SOD activity and total antioxidant capacity (TAC) in the vitrification group compared with the control group (P < 0.05). Moreover, decreased apoptosis rate and MDA concentration, and increased TAC and SOD function were observed in the vitrification with kisspeptin groups (1 μM and 10 μM) compared with the vitrified group (P < 0.05). Our reports express that kisspeptin is an effective agent to overcome the negative effects of vitrification by regulating reactive oxygen species-related apoptotic processes.

Keywords

ApoptosisHuman ovarian cryopreservationKisspeptinOxidative stress
Type
Research Article
Information
Zygote , Volume 31 , Issue 6 , December 2023 , pp. 537 - 543
Check for updates
Copyright
© The Author(s), 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdollahi, M., Salehnia, M., Salehpour, S. and Ghorbanmehr, N. (2013). Human ovarian tissue vitrification/warming has minor effect on the expression of apoptosis-related genes. Iranian Biomedical Journal, 17(4), 179–186. doi: 10.6091/ibj.1243.2013 Google ScholarPubMed
Abou Khalil, N. S. and Mahmoud, G. B. (2020). Reproductive, antioxidant and metabolic responses of Ossimi rams to kisspeptin. Theriogenology, 142, 414–420. doi: 10.1016/j.theriogenology.2019.10.039 CrossRefGoogle ScholarPubMed
Agarwal, A., Gupta, S. and Sikka, S. (2006). The role of free radicals and antioxidants in reproduction. Current Opinion in Obstetrics and Gynecology, 18(3), 325–332. doi: 10.1097/01.gco.0000193003.58158.4e CrossRefGoogle ScholarPubMed
Akkaya, H., Eyuboglu, S., Erkanlı Senturk, G. and Yilmaz, B. (2017). Investigation of the effects of kisspeptin-10 in methionine-induced lipid peroxidation in testicle tissue of young rats. Journal of Biochemical and Molecular Toxicology, 31(5), e21881. doi: 10.1002/jbt.21881 CrossRefGoogle ScholarPubMed
Akkaya, H., Kilic, E., Dinc, S. E. and Yilmaz, B. (2014). Postacute effects of kisspeptin-10 on neuronal injury induced by L-methionine in rats. Journal of Biochemical and Molecular Toxicology, 28(8), 373–377. doi: 10.1002/jbt.21573 CrossRefGoogle ScholarPubMed
Aslan, M., Erkanli Senturk, G., Akkaya, H., Sahin, S. and Yılmaz, B. (2017). The effect of oxytocin and kisspeptin-10 in ovary and uterus of ischemia-reperfusion injured rats. Taiwanese Journal of Obstetrics and Gynecology, 56(4), 456–462. doi: 10.1016/j.tjog.2016.12.018 CrossRefGoogle ScholarPubMed
Aydin, M., Oktar, S., Yonden, Z., Ozturk, O. H. and Yilmaz, B. (2010). Direct and indirect effects of kisspeptin on liver oxidant and antioxidant systems in young male rats. Cell Biochemistry and Function 28(4), 293–299. doi: 10.1002/cbf.1656 CrossRefGoogle ScholarPubMed
Benzie, I. F. and Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Analytical Biochemistry, 239(1), 70–76. doi: 10.1006/abio.1996.0292 CrossRefGoogle ScholarPubMed
Diamanti-Kandarakis, E. and Bergiele, A. (2001). The influence of obesity on hyperandrogenism and infertility in the female. Obesity Reviews, 2(4), 231–238. doi: 10.1046/j.1467-789x.2001.00041.x CrossRefGoogle ScholarPubMed
Dolmans, M. M. and Donnez, J. (2021). Fertility preservation in women for medical and social reasons: Oocytes vs ovarian tissue. Best Practice and Research. Clinical Obstetrics and Gynaecology, 70, 63–80. doi: 10.1016/j.bpobgyn.2020.06.011 CrossRefGoogle ScholarPubMed
Dos Santos Morais, M. L. G., de Brito, D. C. C., Pinto, Y., Mascena Silva, L., Montano Vizcarra, D., Silva, R. F., Weber Santos Cibin, F., Cabral Campello, C., Alves, B. G., Rocha Araújo, V., da Chagas Pinto, F., Pessoa, O. D. L., Figueiredo, J. R. and Ribeiro Rodrigues, A. P. (2019). Natural antioxidants in the vitrification solution improve the ovine ovarian tissue preservation. Reproductive Biology, 19(3), 270–278. doi: 10.1016/j.repbio.2019.07.008 CrossRefGoogle ScholarPubMed
Görlach, A., Bertram, K., Hudecova, S. and Krizanova, O. (2015). Calcium and ROS: A mutual interplay. Redox Biology, 6, 260–271. doi: 10.1016/j.redox.2015.08.010 CrossRefGoogle Scholar
Gualtieri, R., Kalthur, G., Barbato, V., Di Nardo, M., Adiga, S. K. and Talevi, R. (2021). Mitochondrial dysfunction and oxidative stress caused by cryopreservation in reproductive cells. Antioxidants, 10(3), 337. doi: 10.3390/antiox10030337 CrossRefGoogle ScholarPubMed
Gumus, E., Kaloglu, C., Sari, I., Yilmaz, M. and Cetin, A. (2018). Effects of vitrification and transplantation on follicular development and expression of EphrinB1 and PDGFA in mouse ovaries. Cryobiology, 80, 101–113. doi: 10.1016/j.cryobiol.2017.11.006 CrossRefGoogle ScholarPubMed
Güvenç, M. and Aksakal, M. (2018). Ameliorating effect of kisspeptin-10 on methotrexate-induced sperm damages and testicular oxidative stress in rats. Andrologia, 50(8), e13057. doi: 10.1111/and.13057 CrossRefGoogle ScholarPubMed
Hardiany, N. S., Sucitra, S. and Paramita, R. (2019). Profile of malondialdehyde (MDA) and catalase specific activity in plasma of elderly woman. Health Science Journal of Indonesia, 10(2), 132–136. doi: 10.22435/hsji.v12i2.2239 CrossRefGoogle Scholar
Hardy, T. M. (2018). Chronic stress and reproductive function in female childhood cancer survivors. Marquette University. PhD thesis.Google Scholar
Hou, Y., Wang, X., Ping, J., Lei, Z., Gao, Y., Ma, Z., Jia, C., Zhang, Z., Li, X., Jin, M., Li, X., Suo, C., Zhang, Y. and Su, J. (2017). Metabonomics approach to assessing the modulatory effects of Kisspeptin-10 on liver injury induced by heat stress in rats. Scientific Reports, 7(1), 7020. doi: 10.1038/s41598-017-06017-1 CrossRefGoogle ScholarPubMed
Hu, K. L., Zhao, H., Chang, H. M., Yu, Y. and Qiao, J. (2017). Kisspeptin/kisspeptin receptor system in the ovary. Frontiers in Endocrinology, 8, 365. doi: 10.3389/fendo.2017.00365 CrossRefGoogle ScholarPubMed
Huang, P., Feng, L., Oldham, E. A., Keating, M. J. and Plunkett, W. (2000). Superoxide dismutase as a target for the selective killing of cancer cells. Nature, 407(6802), 390–395. doi: 10.1038/35030140 CrossRefGoogle ScholarPubMed
Kagawa, N., Silber, S. and Kuwayama, M. (2009). Successful vitrification of bovine and human ovarian tissue. Reproductive Biomedicine Online, 18(4), 568–577. doi: 10.1016/s1472-6483(10)60136-8 CrossRefGoogle ScholarPubMed
Kashka, R. H., Zavareh, S. and Lashkarbolouki, T. (2016). Augmenting effect of vitrification on lipid peroxidation in mouse preantral follicle during cultivation: Modulation by coenzyme Q10. Systems Biology in Reproductive Medicine, 62(6), 404–414. doi: 10.1080/19396368.2016.1235236 CrossRefGoogle Scholar
Kasum, M., Franulić, D., Čehić, E., Orešković, S., Lila, A. and Ejubović, E. (2017). Kisspeptin as a promising oocyte maturation trigger for in vitro fertilisation in humans. Gynecological Endocrinology, 33(8), 583–587. doi: 10.1080/09513590.2017.1309019 CrossRefGoogle ScholarPubMed
Kim, S. K., Youm, H. W., Lee, J. R. and Suh, C. S. (2017). Chapter 4 Role of antioxidants and antifreeze proteins in cryopreservation/vitrification. In: Nagy, Z., Varghese, A. and Agarwal, A. (eds). Cryopreservation of Mammalian Gametes and Embryos. Methods in Molecular Biology, vol. 1568. Humana Press, New York, NY. doi: 10.1007/978-1-4939-6828-2_4 Google Scholar
Klocke, S., Tappehorn, C. and Griesinger, G. (2014). Effects of supra-zero storage on human ovarian cortex prior to vitrification–warming. Reproductive Biomedicine Online, 29(2), 251–258. doi: 10.1016/j.rbmo.2014.03.025 CrossRefGoogle ScholarPubMed
Kometas, M., Christman, G. M., Kramer, J. and Rhoton-Vlasak, A. (2021). Methods of ovarian tissue cryopreservation: Is vitrification superior to slow freezing?—Ovarian tissue freezing methods. Reproductive Sciences, 28(12), 3291–3302. doi: 10.1007/s43032-021-00591-6 CrossRefGoogle ScholarPubMed
Kotani, M., Detheux, M., Vandenbogaerde, A., Communi, D., Vanderwinden, J. M., Le Poul, E., Brézillon, S., Tyldesley, R., Suarez-Huerta, N., Vandeput, F., Blanpain, C., Schiffmann, S. N., Vassart, G. and Parmentier, M. (2001). The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. Journal of Biological Chemistry, 276(37), 34631–34636. doi: 10.1074/jbc.M104847200 CrossRefGoogle ScholarPubMed
Leonel, E. C. R., Corral, A., Risco, R., Camboni, A., Taboga, S. R., Kilbride, P., Vazquez, M., Morris, J., Dolmans, M. M. and Amorim, C. A. (2019). Stepped vitrification technique for human ovarian tissue cryopreservation. Scientific Reports, 9(1), 20008. doi: 10.1038/s41598-019-56585-7 CrossRefGoogle ScholarPubMed
Li, Y., Ruan, X., Liebenthron, J., Montag, M., Zhou, Q., Kong, W., et al. (2019). Ovarian tissue cryopreservation for patients with premature ovary insufficiency caused by cancer treatment: optimal protocol. Climacteric, 22(4), 383–389.CrossRefGoogle ScholarPubMed
Liang, L. F., Qi, S. T., Xian, Y. X., Huang, L., Sun, X. F. and Wang, W. H. (2017). Protective effect of antioxidants on the pre-maturation aging of mouse oocytes. Scientific Reports, 7(1), 1434. doi: 10.1038/s41598-017-01609-3 CrossRefGoogle ScholarPubMed
Lim, J., Ali, S., Liao, L. S., Nguyen, E. S., Ortiz, L., Reshel, S. and Luderer, U. (2020). Antioxidant supplementation partially rescues accelerated ovarian follicle loss, but not oocyte quality, of glutathione-deficient mice. Biology of Reproduction, 102(5), 1065–1079. doi: 10.1093/biolre/ioaa009 CrossRefGoogle Scholar
Lin, J. and Wang, L. (2021). Oxidative stress in oocytes and embryo development: Implications for in vitro systems. Antioxidants and Redox Signaling, 34(17), 1394–1406. doi: 10.1089/ars.2020.8209 CrossRefGoogle Scholar
Long, J., Wang, X., Gao, H., Liu, Z., Liu, C., Miao, M. and Liu, J. (2006). Malonaldehyde acts as a mitochondrial toxin: Inhibitory effects on respiratory function and enzyme activities in isolated rat liver mitochondria. Life Sciences, 79(15), 1466–1472. doi: 10.1016/j.lfs.2006.04.024 CrossRefGoogle ScholarPubMed
MacManes, M. D., Austin, S. H., Lang, A. S., Booth, A., Farrar, V. and Calisi, R. M. (2017). Widespread patterns of sexually dimorphic gene expression in an avian hypothalamic–pituitary–gonadal (HPG) axis. Scientific Reports, 7(1), 45125. doi: 10.1038/srep45125 CrossRefGoogle Scholar
Magamage, M. P. S., Sathagopam, S., Avula, K., Madushanka, D. N. N. and Velmurugan, S. (2021). Kisspeptin regulates the development of caprine primordial follicles in vitro. Journal of Animal Reproduction and Biotechnology, 36(1), 51–58. doi: 10.12750/JARB.36.1.51 CrossRefGoogle Scholar
Mazoochi, T., Salehnia, M., Valojerdi, M. R. and Mowla, S. J. (2008). Morphologic, ultrastructural, and biochemical identification of apoptosis in vitrified-warmed mouse ovarian tissue. Fertility and Sterility, 90(4), Suppl., 1480–1486. doi: 10.1016/j.fertnstert.2007.07.1384 CrossRefGoogle ScholarPubMed
Migishima, F., Suzuki-Migishima, R., Song, S. Y., Kuramochi, T., Azuma, S., Nishijima, M. and Yokoyama, M. (2003). Successful cryopreservation of mouse ovaries by vitrification. Biology of Reproduction, 68(3), 881–887. doi: 10.1095/biolreprod.102.007948 CrossRefGoogle ScholarPubMed
Mofarahe, Z. S., Salehnia, M., Novin, M. G., Ghorbanmehr, N. and Fesharaki, M. G. (2017). Expression of folliculogenesis-related genes in vitrified human ovarian tissue after two weeks in vitro culture. Cell Journal (Yakhteh), 19(1), 18–26. doi: 10.22074/cellj.2016.4890 Google Scholar
Nori-Garavand, R., Hormozi, M., Narimani, L., Beigi Boroujeni, N., Rajabzadeh, A., Zarei, L., Beigi Boroujeni, M. and Beigi Boroujeni, M. (2020). Effect of selenium on expression of apoptosis-related genes in cryomedia of mice ovary after vitrification. BioMed Research International, 2020, 5389731. doi: 10.1155/2020/5389731 CrossRefGoogle ScholarPubMed
Perez, J. D., Rubinstein, N. D. and Dulac, C. (2016). New perspectives on genomic imprinting, an essential and multifaceted mode of epigenetic control in the developing and adult brain. Annual Review of Neuroscience, 39, 347–384. doi: 10.1146/annurev-neuro-061010-113708 CrossRefGoogle ScholarPubMed
Pineda, R., Plaisier, F., Millar, R. P. and Ludwig, M. (2017). Amygdala kisspeptin neurons: Putative mediators of olfactory control of the gonadotropic axis. Neuroendocrinology, 104(3), 223–238. doi: 10.1159/000445895 CrossRefGoogle ScholarPubMed
Rivas Leonel, E. C. R., Lucci, C. M. and Amorim, C. A. (2019). Cryopreservation of human ovarian tissue: A review. Transfusion Medicine and Hemotherapy, 46(3), 173–181. doi: 10.1159/000499054 CrossRefGoogle ScholarPubMed
Rocha, C. D., Soares, M. M., de Cássia Antonino, D., Júnior, J. M., Freitas Mohallem, R. F., Ribeiro Rodrigues, A. P., Figueiredo, J. R., Beletti, M. E., Jacomini, J. O., Alves, B. G. and Alves, K. A. (2018). Positive effect of resveratrol against preantral follicles degeneration after ovarian tissue vitrification. Theriogenology, 114, 244–251. doi: 10.1016/j.theriogenology.2018.04.004 CrossRefGoogle ScholarPubMed
Shi, Q., Xie, Y., Wang, Y. and Li, S. (2017). Vitrification versus slow freezing for human ovarian tissue cryopreservation: A systematic review and meta-anlaysis. Scientific Reports, 7(1), 8538. doi: 10.1038/s41598-017-09005-7 CrossRefGoogle ScholarPubMed
Silber, S. (2016). Ovarian tissue cryopreservation and transplantation: Scientific implications. Journal of Assisted Reproduction and Genetics, 33(12), 1595–1603. doi: 10.1007/s10815-016-0814-1 CrossRefGoogle ScholarPubMed
Skorupskaite, K., George, J. T. and Anderson, R. A. (2014). The kisspeptin-GnRH pathway in human reproductive health and disease. Human Reproduction Update, 20(4), 485–500. doi: 10.1093/humupd/dmu009 CrossRefGoogle ScholarPubMed
Taghizabet, N., Khalili, M. A., Anbari, F., Agha-Rahimi, A., Nottola, S. A., Macchiarelli, G. and Palmerini, M. G. (2018). Human cumulus cell sensitivity to vitrification, an ultrastructural study. Zygote, 26(3), 224–231. doi: 10.1017/S0967199418000138 CrossRefGoogle ScholarPubMed
Taniguchi, Y., Kuwahara, A., Tachibana, A., Yano, Y., Yano, K., Yamamoto, Y., Yamasaki, M., Iwasa, T., Hinokio, K., Matsuzaki, T. and Irahara, M. (2017). Intra-follicular kisspeptin levels are related to oocyte maturation and gonadal hormones in patients who are undergoing assisted reproductive technology. Reproductive Medicine and Biology, 16(4), 380–385. doi: 10.1002/rmb2.12056 CrossRefGoogle ScholarPubMed
Vilela, J. d. M. V., Dolmans, M.-M., Maruhashi, E., Blackman, M. C., Sonveaux, P., Miranda-Vilela, A. L. and Amorim, C. A. (2020). Evidence of metabolic activity during low-temperature ovarian tissue preservation in different media. Journal of Assisted Reproduction and Genetics 37(10), 2477–2486. doi: 10.1007/s10815-020-01935-y CrossRefGoogle ScholarPubMed
Wang, H. Q., Zhang, W. D., Yuan, B. and Zhang, J. B. (2021). Advances in the regulation of mammalian follicle-stimulating hormone secretion. Animals: An Open Access Journal from MDPI, 11(4), 1134. doi: 10.3390/ani11041134 CrossRefGoogle ScholarPubMed
Xiang, D. C., Jia, B. Y., Fu, X. W., Guo, J. X., Hong, Q. H., Quan, G. B. and Wu, G. Q. (2021). Role of astaxanthin as an efficient antioxidant on the in vitro maturation and vitrification of porcine oocytes. Theriogenology, 167, 13–23. doi: 10.1016/j.theriogenology.2021.03.006 CrossRefGoogle ScholarPubMed
Yang, L., Chen, Y., Liu, Y., Xing, Y., Miao, C., Zhao, Y., Chang, X. and Zhang, Q. (2020). The role of oxidative stress and natural antioxidants in ovarian aging. Frontiers in Pharmacology, 11, 617843. doi: 10.3389/fphar.2020.617843 CrossRefGoogle ScholarPubMed
Yong, K. W., Choi, J. R. and Wan Safwani, W. K. Z. (2016). Biobanking of human mesenchymal stem cells: future strategy to facilitate clinical applications. In: Karimi-Busheri, F. and Weinfeld, M. (eds). Biobanking and Cryopreservation of Stem Cells. Advances in Experimental Medicine and Biology, vol 951. Springer, Cham. doi: 10.1007/978-3-319-45457-3_8 Google Scholar
Youm, H. W, Lee, J. R., Lee, J., Jee, B. C., Suh, C. S. and Kim, S. H. (2014). Optimal vitrification protocol for mouse ovarian tissue cryopreservation: effect of cryoprotective agents and in vitro culture on vitrified–warmed ovarian tissue survival. Human Reproduction, 29(4), 720–730.CrossRefGoogle ScholarPubMed
Zhang, M., Harashima, N., Moritani, T., Huang, W. and Harada, M. (2015). The roles of ROS and caspases in TRAIL-induced apoptosis and necroptosis in human pancreatic cancer cells. PLOS ONE, 10(5), e0127386. doi: 10.1371/journal.pone.0127386 CrossRefGoogle ScholarPubMed