Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-29T16:59:28.277Z Has data issue: false hasContentIssue false

Alterations in the expression pattern of some epigenetic-related genes and microRNAs subsequent to oocyte cryopreservation

Published online by Cambridge University Press:  20 June 2023

Ali Shadmanesh*
Affiliation:
Reproductive Biotechnology in Veterinary, Islamic Azad University, Eqlid Branch, Iran
Hassan Nazari
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran
*
Corresponding author: Ali Shadmanesh; Emails: shadmanesh39@iaueghlid.ac.ir; shad_39606@yahoo.com

Summary

MicroRNAs (miRNAs) are small non-encoding RNAs that actively regulate biological and physiological processes, and play an important role in regulating gene expression in all cells, especially in most animal cells, including oocytes and embryos. The expression of miRNAs at the right time and place is crucial for the oocyte’s maturation and the embryo’s subsequent development. Although assisted reproductive techniques (ART) have helped to solve many infertility problems, they cause changes in the expression of miRNA and genes in oocytes and preimplantation embryos, and the effect of these changes on the future of offspring is unknown, and has caused concerns. The relevant genomic alterations commonly imposed on embryos during cryopreservation may have potential epigenetic risks. Understanding the biological functions of miRNAs in frozen maturated oocytes may provide a better understanding of embryonic development and a comparison of fertility conservation in female mammals. With the development of new techniques for genomic evaluation of preimplantation embryos, it has been possible to better understand the effects of ART. The results of various articles have shown that freezing of oocytes and the cryopreservation method are effective for the expression of miRNAs and, in some cases, cause changes in the expression of miRNAs and epigenetic changes in the resulting embryo. This literature review study aimed to investigate the effects of oocyte cryopreservation in both pre-maturation and post-maturation stages, the cryopreservation method and the type of cryoprotectants (CPA) used on the expression of some epigenetic-related genes and miRNAs.

Type
Review Article
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

Alcolak, E., Abu Marar, E., Mytas, S. C., Chalvatzas, N., Palapelas, V., Schöpper, B., Diedrich, K. and Al-Hasani, S. (2011) Comparison of two different media for vitrification and rewarming of human zygotes: Prospective randomized study. Middle East Fertility Society Journal, 16(3), 189193. doi: 10.1016/j.mefs.2011.02.003 CrossRefGoogle Scholar
Anchamparuthy, V. M., Pearson, R. E. and Gwazdauskas, F. C. (2010). Expression pattern of apoptotic genes in vitrified-thawed bovine oocytes. Reproduction in Domestic Animals, 45(5), e83e90. doi: 10.1111/j.1439-0531.2009.01527.x Google ScholarPubMed
Antinori, M., Licata, E., Dani, G., Cerusico, F., Versaci, C. and Antinori, S. (2007). Cryotop vitrification of human oocytes results in high survival rate and healthy deliveries. Reproductive Biomedicine Online, 14(1), 7279. doi: 10.1016/s1472-6483(10)60766-3 CrossRefGoogle ScholarPubMed
Assou, S., Anahory, T., Pantesco, V., Le Carrour, T., Pellestor, F., Klein, B., Reyftmann, L., Dechaud, H., De Vos, J. and Hamamah, S. (2006). The human cumulus–oocyte complex gene-expression profile. Human Reproduction, 21(7), 17051719. doi: 10.1093/humrep/del065 CrossRefGoogle ScholarPubMed
Assou, S., Al-Edani, T., Haouzi, D., Philippe, N., Lecellier, C. H., Piquemal, D., Commes, T., Aït-Ahmed, O., Dechaud, H. and Hamamah, S. (2013). MicroRNAs: New candidates for the regulation of the human cumulus–oocyte complex. Human Reproduction, 28(11), 30383049. doi: 10.1093/humrep/det321 CrossRefGoogle ScholarPubMed
Azizi, E., Ghaffari Novin, M., Naji, M., Amidi, F., Hosseinirad, H. and Shams Mofarahe, Z. (2021). Effect of vitrification on biogenesis pathway and expression of development-related microRNAs in preimplantation mouse embryos. Cell and Tissue Banking, 22(1), 103114. doi: 10.1007/s10561-020-09870-z CrossRefGoogle ScholarPubMed
Bahr, J. C., Robey, R. W., Luchenko, V., Basseville, A., Chakraborty, A. R., Kozlowski, H., Pauly, G. T., Patel, P., Schneider, J. P., Gottesman, M. M. and Bates, S. E. (2016). Blocking downstream signaling pathways in the context of HDAC inhibition promotes apoptosis preferentially in cells harboring mutant Ras. Oncotarget, 7(43), 6980469815. doi: 10.18632/oncotarget.12001 CrossRefGoogle ScholarPubMed
Barberet, J., Ducreux, B., Bruno, C., Guilleman, M., Simonot, R., Lieury, N., Guilloteau, A., Bourc’his, D. and Fauque, P. (2022). Comparison of oocyte vitrification using a semi-automated or a manual closed system in human siblings: Survival and transcriptomic analyses. Journal of Ovarian Research, 15(1), 128. doi: 10.1186/s13048-022-01064-3 CrossRefGoogle ScholarPubMed
Battaglia, R., Vento, M. E., Ragusa, M., Barbagallo, D., La Ferlita, A., Di Emidio, G., Borzí, P., Artini, P. G., Scollo, P., Tatone, C., Purrello, M. and Di Pietro, C. (2016). MicroRNAs are stored in human MII oocyte and their expression profile changes in reproductive ageing. Biology of Reproduction, 95(6), 131. doi: 10.1095/biolreprod.116.142711 CrossRefGoogle Scholar
Bonnet, A., Tran, R. D. and Sirard, M. (2007). Opportunities and challenges in applying genomics to the study of oogenesis and follicullogenesis in farm animals. 2. International Meeting on Mammalian Embryogenomics. doi:10.1530/rep-07–0331 CrossRefGoogle Scholar
Borini, A. and Bianchi, V. (2010). Cryopreservation of mature and immature oocytes. Clinical Obstetrics and Gynecology, 53(4), 763774. doi: 10.1097/GRF.0b013e3181f96f01 CrossRefGoogle ScholarPubMed
Brison, D., Cutting, R., Clarke, H. and Wood, M. (2012). ACE consensus meeting report. ACE consensus meeting report: Oocyte and embryo cryopreservation Sheffield 17.05.11. Human Fertility, 15(2), 6974. doi: 10.3109/14647273.2012.687124 CrossRefGoogle ScholarPubMed
Cao, Y., Xing, Q., Zhang, Z. G., Wei, Z. L., Zhou, P. and Cong, L. (2009). Cryopreservation of immature and in-vitro matured human oocytes by vitrification. Reproductive Biomedicine Online, 19(3), 369373. doi: 10.1016/s1472-6483(10)60170-8 CrossRefGoogle ScholarPubMed
Capra, E., Turri, F., Lazzari, B., Cremonesi, P., Gliozzi, T. M., Fojadelli, I., Stella, A. and Pizzi, F. (2017). Small RNA sequencing of cryopreserved semen from single bull revealed altered miRNAs and piRNAs expression between high- and low-motile sperm populations. BMC Genomics, 18(1), 14. doi: 10.1186/s12864-016-3394-7 CrossRefGoogle ScholarPubMed
Chamayou, S., Bonaventura, G., Alecci, C., Tibullo, D., Di Raimondo, F., Guglielmino, A. and Barcellona, M. L. (2011). Consequences of metaphase II oocyte cryopreservation on mRNA content. Cryobiology, 62(2), 130134. doi: 10.1016/j.cryobiol.2011.01.014 CrossRefGoogle ScholarPubMed
Chen, H., Zhang, L., Deng, T., Zou, P., Wang, Y., Quan, F. and Zhang, Y. (2016). Effects of oocyte vitrification on epigenetic status in early bovine embryos. Theriogenology, 86(3), 868878. doi: 10.1016/j.theriogenology.2016.03.008 CrossRefGoogle ScholarPubMed
Cheng, K. R., Fu, X. W., Zhang, R. N., Jia, G. X., Hou, Y. P. and Zhu, S. E. (2014). Effect of oocyte vitrification on deoxyribonucleic acid methylation of H19, Peg3, and Snrpn differentially methylated regions in mouse blastocysts. Fertility and Sterility, 102(4), 11831190.e3. e1183. doi: 10.1016/j.fertnstert.2014.06.037 CrossRefGoogle ScholarPubMed
Cobo, A. and Diaz, C. (2011). Clinical application of oocyte vitrification: A systematic review and meta-analysis of randomized controlled trials. Fertility and Sterility, 96(2), 277285. doi: 10.1016/j.fertnstert.2011.06.030 CrossRefGoogle ScholarPubMed
Daneshvar, M., Movahedin, M., Salehi, M. and Noruzinia, M. (2021). Alterations of miR-16, miR-let-7a and their target genes expression in human blastocysts following vitrification and re-vitrification. Reproductive Biology and Endocrinology: RB&E, 19(1), 155. doi: 10.1186/s12958-021-00842-w CrossRefGoogle ScholarPubMed
Dessolle, L., de Larouzière, V., Ravel, C., Berthaut, I., Antoine, J. M. and Mandelbaum, J. (2009). Slow freezing and vitrification of human mature and immature oocytes. Gynecologie, Obstetrique et Fertilite, 37(9), 712719. doi: 10.1016/j.gyobfe.2009.04.026 CrossRefGoogle ScholarPubMed
Di Pietro, C., Vento, M., Guglielmino, M. R., Borzì, P., Santonocito, M., Ragusa, M., Barbagallo, D., Duro, L. R., Majorana, A., De Palma, A., Garofalo, M. R., Minutolo, E., Scollo, P. and Purrello, M. (2010). Molecular profiling of human oocytes after vitrification strongly suggests that they are biologically comparable with freshly isolated gametes. Fertility and Sterility, 94(7), 28042807. doi: 10.1016/j.fertnstert.2010.04.060 CrossRefGoogle ScholarPubMed
Fadini, R., Brambillasca, F., Renzini, M. M., Merola, M., Comi, R., De Ponti, E. and Dal Canto, M. B. (2009). Human oocyte cryopreservation: Comparison between slow and ultrarapid methods. Reproductive Biomedicine Online, 19(2), 171180. doi: 10.1016/s1472-6483(10)60069-7 CrossRefGoogle ScholarPubMed
Flynt, A. S. and Lai, E. C. (2008). Biological principles of microRNA-mediated regulation: Shared themes amid diversity. Nature Reviews. Genetics, 9(11), 831842. doi: 10.1038/nrg2455 CrossRefGoogle ScholarPubMed
Friedman, R. C., Farh, K. K.-H., Burge, C. B. and Bartel, D. P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Research, 19(1), 92105. doi: 10.1101/gr.082701.108 CrossRefGoogle ScholarPubMed
Gao, L., Jia, G., Li, A., Ma, H., Huang, Z., Zhu, S., Hou, Y. and Fu, X. (2017). RNA-Seq transcriptome profiling of mouse oocytes after in vitro maturation and/or vitrification. Scientific Reports, 7(1), 13245. doi: 10.1038/s41598-017-13381-5 CrossRefGoogle ScholarPubMed
Gilchrist, G. C., Tscherner, A., Nalpathamkalam, T., Merico, D. and LaMarre, J. (2016). MicroRNA expression during bovine oocyte maturation and fertilization. International Journal of Molecular Sciences, 17(3), 396. doi: 10.3390/ijms17030396 CrossRefGoogle ScholarPubMed
Glujovsky, D., Riestra, B., Sueldo, C., Fiszbajn, G., Repping, S., Nodar, F., Papier, S. and Ciapponi, A. (2014). Vitrification versus slow freezing for women undergoing oocyte cryopreservation. Cochrane Database of Systematic Reviews, 9(9), CD010047. doi: 10.1002/14651858.CD010047.pub2 Google Scholar
Goldman, K. N., Kramer, Y., Hodes-Wertz, B., Noyes, N., McCaffrey, C. and Grifo, J. A. (2015). Long-term cryopreservation of human oocytes does not increase embryonic aneuploidy. Fertility and Sterility, 103(3), 662668. doi: 10.1016/j.fertnstert.2014.11.025 CrossRefGoogle Scholar
Hargreave, M., Jensen, A., Hansen, M. K., Dehlendorff, C., Winther, J. F., Schmiegelow, K. and Kjær, S. K. (2019). Association between fertility treatment and cancer risk in children. JAMA, 322(22), 22032210. doi: 10.1001/jama.2019.18037 CrossRefGoogle ScholarPubMed
Hayashi, T., Kansaku, K., Abe, T., Ueda, S. and Iwata, H. (2019). Effects of resveratrol treatment on mitochondria and subsequent embryonic development of bovine blastocysts cryopreserved by slow freezing. Animal Science Journal, 90(7), 849856. doi: 10.1111/asj.13219 CrossRefGoogle ScholarPubMed
Hu, W., Marchesi, D., Qiao, J. and Feng, H. L. (2012). Effect of slow freeze versus vitrification on the oocyte: An animal model. Fertility and Sterility, 98(3), 752760.e3. e753. doi: 10.1016/j.fertnstert.2012.05.037 CrossRefGoogle ScholarPubMed
Hu, Y., Rao, S. S., Wang, Z. X., Cao, J., Tan, Y. J., Luo, J., Li, H. M., Zhang, W. S., Chen, C. Y. and Xie, H. (2018). Exosomes from human umbilical cord blood accelerate cutaneous wound healing through miR-21–3p-mediated promotion of angiogenesis and fibroblast function. Theranostics, 8(1), 169184. doi: 10.7150/thno.21234 CrossRefGoogle ScholarPubMed
Kim, S. S., Kang, H. G., Kim, N. H., Lee, H. C. and Lee, H. H. (2005). Assessment of the integrity of human oocytes retrieved from cryopreserved ovarian tissue after xenotransplantation. Human Reproduction, 20(9), 25022508. doi: 10.1093/humrep/dei099 Google ScholarPubMed
Kim, Y. J., Ku, S. Y., Kim, Y. Y., Liu, H. C., Chi, S. W., Kim, S. H., Choi, Y. M., Kim, J. G. and Moon, S. Y. (2013). MicroRNAs transfected into granulosa cells may regulate oocyte meiotic competence during in vitro maturation of mouse follicles. Human Reproduction, 28(11), 30503061. doi: 10.1093/humrep/det338 CrossRefGoogle ScholarPubMed
Kopeika, J., Thornhill, A. and Khalaf, Y. (2015). The effect of cryopreservation on the genome of gametes and embryos: Principles of cryobiology and critical appraisal of the evidence. Human Reproduction Update, 21(2), 209227. doi: 10.1093/humupd/dmu063 CrossRefGoogle ScholarPubMed
Kuwayama, M., Vajta, G., Ieda, S. and Kato, O. (2005). Comparison of open and closed methods for vitrification of human embryos and the elimination of potential contamination. Reproductive Biomedicine Online, 11(5), 608614. doi: 10.1016/s1472-6483(10)61169-8 CrossRefGoogle ScholarPubMed
Lee, R. K.-K., Li, S. H., Lu, C. H., Ho, H. Y., Chen, Y. J. and Yeh, H. I. (2008). Abnormally low expression of connexin 37 and connexin 43 in subcutaneously transplanted cryopreserved mouse ovarian tissue. Journal of Assisted Reproduction and Genetics, 25(9–10), 489497. doi: 10.1007/s10815-008-9264-8 CrossRefGoogle ScholarPubMed
Leem, Y. E., Han, J. W., Lee, H. J., Ha, H. L., Kwon, Y. L., Ho, S. M., Kim, B. G., Tran, P., Bae, G. U. and Kang, J. S. (2011). Gas1 cooperates with CDO and promotes myogenic differentiation via activation of p38MAPK. Cellular Signalling, 23(12), 20212029. doi: 10.1016/j.cellsig.2011.07.016 CrossRefGoogle ScholarPubMed
Li, P., Mao, W. M., Zheng, Z. G., Dong, Z. M. and Ling, Z. Q. (2013). Down-regulation of PTEN expression modulated by dysregulated miR-21 contributes to the progression of esophageal cancer. Digestive Diseases and Sciences, 58(12), 34833493. doi: 10.1007/s10620-013-2854-z CrossRefGoogle Scholar
Li, X., Wang, H., Sheng, Y. and Wang, Z. (2017). MicroRNA-224 delays oocyte maturation through targeting Ptx3 in cumulus cells. Mechanisms of Development, 143, 2025. doi: 10.1016/j.mod.2016.12.004 CrossRefGoogle ScholarPubMed
Li, J., Yang, X., Liu, F., Song, Y. and Liu, Y. (2019). Evaluation of differentially expressed microRNAs in vitrified oocytes by next generation sequencing. International Journal of Biochemistry and Cell Biology, 112, 134140. doi: 10.1016/j.biocel.2019.05.006 CrossRefGoogle ScholarPubMed
Liu, H. C., He, Z. and Rosenwaks, Z. (2003). Mouse ovarian tissue cryopreservation has only a minor effect on in vitro follicular maturation and gene expression. Journal of Assisted Reproduction and Genetics, 20(10), 421431. doi: 10.1023/a:1026284609730 CrossRefGoogle Scholar
Ma, P., Pan, H., Montgomery, R. L., Olson, E. N. and Schultz, R. M. (2012). Compensatory functions of histone deacetylase 1 (HDAC1) and HDAC2 regulate transcription and apoptosis during mouse oocyte development. Proceedings of the National Academy of Sciences of the United States of America, 109(8), E481E489. doi: 10.1073/pnas.1118403109 Google ScholarPubMed
Martin, C. and Zhang, Y. (2007). Mechanisms of epigenetic inheritance. Current Opinion in Cell Biology, 19(3), 266272. doi: 10.1016/j.ceb.2007.04.002 CrossRefGoogle ScholarPubMed
Matsuda, S., Nakagawa, Y., Kitagishi, Y., Nakanishi, A. and Murai, T. (2018). Reactive oxygen species, superoxide dimutases, and PTEN-p53-AKT-MDM2 signaling loop network in mesenchymal stem/stromal cells regulation. Cells, 7(5), 36. doi: 10.3390/cells7050036 CrossRefGoogle Scholar
Men, H., Monson, R. L., Parrish, J. J. and Rutledge, J. J. (2003). Degeneration of cryopreserved bovine oocytes via apoptosis during subsequent culture. Cryobiology, 47(1), 7381. doi: 10.1016/s0011-2240(03)00070-1 CrossRefGoogle ScholarPubMed
Mogas, T. (2019). Update on the vitrification of bovine oocytes and in vitro-produced embryos. Reproduction, Fertility, and Development, 31(1), 105117. doi: 10.1071/RD18345 CrossRefGoogle Scholar
Monzo, C., Haouzi, D., Roman, K., Assou, S., Dechaud, H. and Hamamah, S. (2012). Slow freezing and vitrification differentially modify the gene expression profile of human metaphase II oocytes. Human Reproduction, 27(7), 21602168. doi: 10.1093/humrep/des153 CrossRefGoogle ScholarPubMed
Murchison, E. P., Stein, P., Xuan, Z., Pan, H., Zhang, M. Q., Schultz, R. M. and Hannon, G. J. (2007). Critical roles for Dicer in the female germline. Genes and Development, 21(6), 682693. doi: 10.1101/gad.1521307 CrossRefGoogle ScholarPubMed
Noh, E. M., Park, J., Song, H. R., Kim, J. M., Lee, M., Song, H. K., Hong, O. Y., Whang, P. H., Han, M. K., Kwon, K. B., Kim, J. S. and Lee, Y. R. (2016). Skin aging-dependent activation of the PI3K signaling pathway via downregulation of PTEN increases intracellular ROS in human dermal fibroblasts. Oxidative Medicine and Cellular Longevity, 2016, 6354261. doi: 10.1155/2016/6354261 CrossRefGoogle ScholarPubMed
Nohales-Córcoles, M., Sevillano-Almerich, G., Di Emidio, G., Tatone, C., Cobo, A. C., Dumollard, R. and De los Santos Molina, M. J. (2016). Impact of vitrification on the mitochondrial activity and redox homeostasis of human oocyte. Human Reproduction, 31(8), 18501858. doi: 10.1093/humrep/dew130 CrossRefGoogle ScholarPubMed
Nottola, S. A., Albani, E., Coticchio, G., Palmerini, M. G., Lorenzo, C., Scaravelli, G., Borini, A., Levi-Setti, P. E. and Macchiarelli, G. (2016). Freeze/thaw stress induces organelle remodeling and membrane recycling in cryopreserved human mature oocytes. Journal of Assisted Reproduction and Genetics, 33(12), 15591570. doi: 10.1007/s10815-016-0798-x CrossRefGoogle ScholarPubMed
O’Connell, R. M., Chaudhuri, A. A., Rao, D. S. and Baltimore, D. (2009). Inositol phosphatase SHIP1 is a primary target of miR-155. Proceedings of the National Academy of Sciences of the United States of America, 106(17), 71137118. doi: 10.1073/pnas.0902636106 CrossRefGoogle ScholarPubMed
Pan, B., Toms, D., Shen, W. and Li, J. (2015). MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells. American Journal of Physiology. Endocrinology and Metabolism, 308(6), E525E534. doi: 10.1152/ajpendo.00480.2014 CrossRefGoogle ScholarPubMed
Quan, G., Wu, G. and Hong, Q. (2017). Oocyte cryopreservation based in sheep: The current status and future perspective. Biopreservation and Biobanking, 15(6), 535547. doi: 10.1089/bio.2017.0074 CrossRefGoogle ScholarPubMed
Rasti, G. and Vaquero, A. (2018). Epigenetic modifications of histones. In Epigenetics and assisted reproduction (pp. 1728). CRC Press. E-book ISBN 9781315208701.CrossRefGoogle Scholar
Rienzi, L., Cobo, A., Paffoni, A., Scarduelli, C., Capalbo, A., Vajta, G., Remohí, J., Ragni, G. and Ubaldi, F. M. (2012). Consistent and predictable delivery rates after oocyte vitrification: An observational longitudinal cohort multicentric study. Human Reproduction, 27(6), 16061612. doi: 10.1093/humrep/des088 CrossRefGoogle ScholarPubMed
Saenz-de-Juano, M. D., Marco-Jimenez, F., Viudes-de-Castro, M. P., Lavara, R. and Vicente, J. S. (2014). Direct comparison of the effects of slow freezing and vitrification on late blastocyst gene expression, development, implantation and offspring of rabbit morulae. Reproduction in Domestic Animals, 49(3), 505511. doi: 10.1111/rda.12320 CrossRefGoogle ScholarPubMed
Saragusty, J. and Arav, A. (2011). Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction, 141(1), 119. doi: 10.1530/REP-10-0236 CrossRefGoogle ScholarPubMed
Sargisian, N., Lannering, B., Petzold, M., Opdahl, S., Gissler, M., Pinborg, A., Henningsen, A.-K. A., Tiitinen, A., Romundstad, L. B., Spangmose, A. L., Bergh, C. and Wennerholm, U. B. (2022). Cancer in children born after frozen–thawed embryo transfer: A cohort study. PLOS Medicine, 19(9), e1004078. doi: 10.1371/journal.pmed.1004078 CrossRefGoogle ScholarPubMed
Sevignani, C., Calin, G. A., Siracusa, L. D. and Croce, C. M. (2006). Mammalian microRNAs: A small world for fine-tuning gene expression. Mammalian Genome, 17(3), 189202. doi: 10.1007/s00335-005-0066-3 CrossRefGoogle ScholarPubMed
Shahedi, A., Hosseini, A., Ali Khalili, M. and Yeganeh, F. (2017). Vitrification affects nuclear maturation and gene expression of immature human oocytes. Research in Molecular Medicine, 5(1), 2733. doi: 10.29252/rmm.5.1.27 Google Scholar
Solé, M., Santaló, J., Boada, M., Clua, E., Rodríguez, I., Martínez, F., Coroleu, B., Barri, P. N. and Veiga, A. (2013). How does vitrification affect oocyte viability in oocyte donation cycles? A prospective study to compare outcomes achieved with fresh versus vitrified sibling oocytes. Human Reproduction, 28(8), 20872092. doi: 10.1093/humrep/det242 CrossRefGoogle ScholarPubMed
Somoskoi, B., Martino, N. A., Cardone, R. A., Lacalandra, G. M., Dell’Aquila, M. E. and Cseh, S. (2015). Different chromatin and energy/redox responses of mouse morulae and blastocysts to slow freezing and vitrification. Reproductive Biology and Endocrinology: RB&E, 13, 22. doi: 10.1186/s12958-015-0018-z CrossRefGoogle ScholarPubMed
Song, W. Y., Peng, Z. F., Chen, X. M., Jin, H. X., Yao, G. D., Shi, S. L., Yang, H. Y., Zhang, X. Y. and Sun, Y. P. (2016). Effects of vitrification on outcomes of in vivo-mature, in vitro-mature and immature human oocytes. Cellular Physiology and Biochemistry, 38(5), 20532062. doi: 10.1159/000445564 CrossRefGoogle ScholarPubMed
Spinaci, M., Vallorani, C., Bucci, D., Tamanini, C., Porcu, E. and Galeati, G. (2012). Vitrification of pig oocytes induces changes in histone H4 acetylation and histone H3 lysine 9 methylation (H3K9). Veterinary Research Communications, 36(3), 165171. doi: 10.1007/s11259-012-9527-9 CrossRefGoogle ScholarPubMed
Stigliani, S., Moretti, S., Anserini, P., Casciano, I., Venturini, P. L. and Scaruffi, P. (2015). Storage time does not modify the gene expression profile of cryopreserved human metaphase II oocytes. Human Reproduction, 30(11), 25192526. doi: 10.1093/humrep/dev232 CrossRefGoogle Scholar
Succu, S., Leoni, G. G., Berlinguer, F., Madeddu, M., Bebbere, D., Mossa, F., Bogliolo, L., Ledda, S. and Naitana, S. (2007). Effect of vitrification solutions and cooling upon in vitro matured prepubertal ovine oocytes. Theriogenology, 68(1), 107114. doi: 10.1016/j.theriogenology.2007.04.035 CrossRefGoogle ScholarPubMed
Sun, K. and Lai, E. C. (2013). Adult-specific functions of animal microRNAs. Nature Reviews. Genetics, 14(8), 535548. doi: 10.1038/nrg3471 CrossRefGoogle ScholarPubMed
Takahashi, N., Nakaoka, T. and Yamashita, N. (2012). Profiling of immune-related microRNA expression in human cord blood and adult peripheral blood cells upon proinflammatory stimulation. European Journal of Haematology, 88(1), 3138. doi: 10.1111/j.1600-0609.2011.01707.x CrossRefGoogle ScholarPubMed
Tesfaye, D., Worku, D., Rings, F., Phatsara, C., Tholen, E., Schellander, K. and Hoelker, M. (2009). Identification and expression profiling of microRNAs during bovine oocyte maturation using heterologous approach. Molecular Reproduction and Development, 76(7), 665677. doi: 10.1002/mrd.21005 CrossRefGoogle ScholarPubMed
Tomek, W. and Smiljakovic, T. (2005). Activation of Akt (protein kinase B) stimulates metaphase I to metaphase II transition in bovine oocytes. Reproduction, 130(4), 423430. doi: 10.1530/rep.1.00754 CrossRefGoogle ScholarPubMed
Trapphoff, T., Heiligentag, M., Simon, J., Staubach, N., Seidel, T., Otte, K., Fröhlich, T., Arnold, G. J. and Eichenlaub-Ritter, U. (2016). Improved cryotolerance and developmental potential of in vitro and in vivo matured mouse oocytes by supplementing with a glutathione donor prior to vitrification. Molecular Human Reproduction, 22(12), 867881. doi: 10.1093/molehr/gaw059 Google ScholarPubMed
Tscherner, A., Brown, A. C., Stalker, L., Kao, J., Dufort, I., Sirard, M. A. and LaMarre, J. (2018). STAT3 signaling stimulates miR-21 expression in bovine cumulus cells during in vitro oocyte maturation. Scientific Reports, 8(1), 11527. doi: 10.1038/s41598-018-29874-w CrossRefGoogle ScholarPubMed
Tulay, P., Naja, R. P., Cascales-Roman, O., Doshi, A., Serhal, P. and SenGupta, S. B. (2015). Investigation of microRNA expression and DNA repair gene transcripts in human oocytes and blastocysts. Journal of Assisted Reproduction and Genetics, 32(12), 17571764. doi: 10.1007/s10815-015-0585-0 CrossRefGoogle ScholarPubMed
Turathum, B., Saikhun, K., Sangsuwan, P. and Kitiyanant, Y. (2010). Effects of vitrification on nuclear maturation, ultrastructural changes and gene expression of canine oocytes. Reproductive Biology and Endocrinology: RB&E, 8, 70. doi: 10.1186/1477-7827-8-70 CrossRefGoogle ScholarPubMed
Verheijen, M., Lienhard, M., Schrooders, Y., Clayton, O., Nudischer, R., Boerno, S., Timmermann, B., Selevsek, N., Schlapbach, R., Gmuender, H., Gotta, S., Geraedts, J., Herwig, R., Kleinjans, J. and Caiment, F. (2019). DMSO induces drastic changes in human cellular processes and epigenetic landscape in vitro . Scientific Reports, 9(1), 4641. doi: 10.1038/s41598-019-40660-0 CrossRefGoogle ScholarPubMed
Walls, M., Junk, S., Ryan, J. P. and Hart, R. (2012). IVF versus ICSI for the fertilization of in-vitro matured human oocytes. Reproductive Biomedicine Online, 25(6), 603607. doi: 10.1016/j.rbmo.2012.08.001 CrossRefGoogle ScholarPubMed
Wang, N., Li, C. Y., Zhu, H. B., Hao, H. S., Wang, H. Y., Yan, C. L., Zhao, S. J., Du, W. H., Wang, D., Liu, Y., Pang, Y. W. and Zhao, X. M. (2017a). Effect of vitrification on the mRNA transcriptome of bovine oocytes. Reproduction in Domestic Animals, 52(4), 531541. doi: 10.1111/rda.12942 CrossRefGoogle ScholarPubMed
Wang, T. Y., Zhang, J., Zhu, J., Lian, H. Y., Yuan, H. J., Gao, M., Luo, M. J. and Tan, J. H. (2017b). Expression profiles and function analysis of microRNAs in postovulatory aging mouse oocytes. Aging, 9(4), 11861201. doi: 10.18632/aging.101219 CrossRefGoogle ScholarPubMed
Wang, Y., Zhang, M. L., Zhao, L. W., Kuang, Y. P. and Xue, S. G. (2018). Enhancement of the efficiency of oocyte vitrification through regulation of histone deacetylase 6 expression. In Journal of Assisted Reproduction and Genetics (2018/07/04. Springer, 35(7), 11791185). doi: 10.1007/s10815-018-1221-6 CrossRefGoogle ScholarPubMed
Wen, Y., Zhao, S., Chao, L., Yu, H., Song, C., Shen, Y., Chen, H. and Deng, X. (2014). The protective role of antifreeze protein 3 on the structure and function of mature mouse oocytes in vitrification. Cryobiology, 69(3), 394401. doi: 10.1016/j.cryobiol.2014.09.006 CrossRefGoogle ScholarPubMed
Wilczynska, A., Git, A., Argasinska, J., Belloc, E. and Standart, N. (2016). CPEB and miR-15/16 co-regulate translation of cyclin E1 mRNA during Xenopus oocyte maturation. PLOS ONE, 11(2), e0146792. doi: 10.1371/journal.pone.0146792 CrossRefGoogle ScholarPubMed
Wright, E. C., Hale, B. J., Yang, C. X., Njoka, J. G. and Ross, J. W. (2016). MicroRNA-21 and PDCD4 expression during in vitro oocyte maturation in pigs. Reproductive Biology and Endocrinology: RB&E, 14(1), 21. doi: 10.1186/s12958-016-0152-2 CrossRefGoogle ScholarPubMed
Xia, B., Lu, J., Wang, R., Yang, Z., Zhou, X. and Huang, P. (2018). miR-21–3p regulates influenza A virus replication by targeting histone deacetylase-8. Frontiers in Cellular and Infection Microbiology, 8, 175. doi: 10.3389/fcimb.2018.00175 CrossRefGoogle ScholarPubMed
Xiao, G., Xia, C., Yang, J., Liu, J., Du, H., Kang, X., Lin, Y., Guan, R., Yan, P. and Tang, S. (2014). MiR-133b regulates the expression of the actin protein TAGLN2 during oocyte growth and maturation: A potential target for infertility therapy. PLOS ONE, 9(6), e100751. doi: 10.1371/journal.pone.0100751 CrossRefGoogle ScholarPubMed
Xu, Y. W., Wang, B., Ding, C. H., Li, T., Gu, F. and Zhou, C. (2011). Differentially expressed micoRNAs in human oocytes. Journal of Assisted Reproduction and Genetics, 28(6), 559566. doi: 10.1007/s10815-011-9590-0 CrossRefGoogle ScholarPubMed
Yamanaka, Y., Tagawa, H., Takahashi, N., Watanabe, A., Guo, Y. M., Iwamoto, K., Yamashita, J., Saitoh, H., Kameoka, Y., Shimizu, N., Ichinohasama, R. and Sawada, K. (2009). Aberrant overexpression of microRNAs activate AKT signaling via down-regulation of tumor suppressors in natural killer-cell lymphoma/leukemia. Blood, 114(15), 32653275. doi: 10.1182/blood-2009-06-222794 CrossRefGoogle ScholarPubMed
Yan, L. Y., Yan, J., Qiao, J., Zhao, P. L. and Liu, P. (2010). Effects of oocyte vitrification on histone modifications. Reproduction, Fertility, and Development, 22(6), 920925. doi: 10.1071/RD09312 CrossRefGoogle ScholarPubMed
Yan, M., Chen, C., Gong, W., Yin, Z., Zhou, L., Chaugai, S. and Wang, D. W. (2015). miR-21–3p regulates cardiac hypertrophic response by targeting histone deacetylase-8. Cardiovascular Research, 105(3), 340352. doi: 10.1093/cvr/cvu254 CrossRefGoogle ScholarPubMed
Zhang, C. X., Cui, W., Zhang, M., Zhang, J., Wang, T. Y., Zhu, J., Jiao, G. Z. and Tan, J. H. (2014). Role of Na+/Ca2+ exchanger (NCX) in modulating postovulatory aging of mouse and rat oocytes. PLOS ONE, 9(4), e93446. doi: 10.1371/journal.pone.0093446 CrossRefGoogle ScholarPubMed
Zhang, Z., Mu, Y., Ding, D., Zou, W., Li, X., Chen, B., Leung, P. C., Chang, H. M., Zhu, Q., Wang, K., Xue, R., Xu, Y., Zou, H., Zhou, P., Wei, Z. and Cao, Y. (2021). Melatonin improves the effect of cryopreservation on human oocytes by suppressing oxidative stress and maintaining the permeability of the oolemma. Journal of Pineal Research, 70(2), e12707. doi: 10.1111/jpi.12707 CrossRefGoogle ScholarPubMed
Zhao, X. M., Ren, J. J., Du, W. H., Hao, H. S., Wang, D., Qin, T., Liu, Y. and Zhu, H. B. (2013). Effect of vitrification on promoter CpG island methylation patterns and expression levels of DNA methyltransferase 1o, histone acetyltransferase 1, and deacetylase 1 in metaphase II mouse oocytes. Fertility and Sterility, 100(1), 256261. doi: 10.1016/j.fertnstert.2013.03.009 CrossRefGoogle ScholarPubMed
Zhao, X., Hao, H., Du, W. and Zhu, H. (2015). Effect of vitrification on the microRNA transcriptome in mouse blastocysts. PLOS ONE, 10(4), e0123451. doi: 10.1371/journal.pone.0123451 CrossRefGoogle ScholarPubMed
Zhu, Q., Ding, D., Yang, H., Zou, W., Yang, D., Wang, K., Zhang, C., Chen, B., Ji, D., Hao, Y., Xue, R., Xu, Y., Wang, Q., Wang, J., Yan, B., Cao, Y., Zou, H. and Zhang, Z. (2022). Melatonin protects mitochondrial function and inhibits oxidative damage against the decline of human oocytes development caused by prolonged cryopreservation. Cells, 11(24), 4018. doi: 10.3390/cells11244018 CrossRefGoogle ScholarPubMed