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Oocyte vitrification induces loss of DNA methylation and histone acetylation in the resulting embryos derived using ICSI in dromedary camel

Published online by Cambridge University Press:  18 March 2021

F. Moulavi
Affiliation:
Department of Embryology, Camel Advanced Reproductive Technologies Centre, Government of Dubai, Dubai, United Arab Emirates
I.M. Saadeldin
Affiliation:
Department of Animal Production, College of Food and Agricultural Sciences, King Saud University, 11451 Riyadh, Saudi Arabia Department of Physiology, Faculty of Veterinary Medicine, Zagazig University, 44519 Zagazig, Egypt
A.A. Swelum
Affiliation:
Department of Animal Production, College of Food and Agricultural Sciences, King Saud University, 11451 Riyadh, Saudi Arabia
F. Tasdighi
Affiliation:
Department of Pharmacology, Iranian Hospital in Dubai, United Arab Emirates
H. Hosseini-Fahraji
Affiliation:
Department of Embryology, Camel Advanced Reproductive Technologies Centre, Government of Dubai, Dubai, United Arab Emirates
S.M. Hosseini*
Affiliation:
Department of Embryology, Camel Advanced Reproductive Technologies Centre, Government of Dubai, Dubai, United Arab Emirates
*
Author for correspondence: S.M. Hosseini. Department of Embryology, Camel Advanced Reproductive Technologies Centre, Government of Dubai, Dubai, United Arab Emirates. Tel: +971 48326836. Fax: +971 48326836. E-mail: huteistmeintag@gmail.com

Summary

Oocyte cryopreservation has become an important component of assisted reproductive technology with increasing implication in female fertility preservation and animal reproduction. However, the possible adverse effects of oocyte cryopreservation on epigenetic status of the resulting embryos is still an open question. This study evaluated the effects of MII-oocyte vitrification on gene transcripts linked to epigenetic reprogramming in association with the developmental competence and epigenetic status of the resulting embryos at 2-cell and blastocyst stages in dromedary camel. The cleavage rate of vitrified oocytes following intracytoplasmic sperm injection was significantly increased compared with the control (98.2 ± 2 vs. 72.7 ± 4.1%, respectively), possibly due to the higher susceptibility of vitrified oocytes to spontaneous activation. Nonetheless, the competence of cleaved embryos derived from vitrified oocytes for development to the blastocyst and hatched blastocyst was significantly reduced compared with the control (7.7 ± 1.2 and 11.1 ± 11.1 compared with 28.1 ± 2.6 and 52.4 ± 9.9%, respectively). The relative transcript abundances of epigenetic reprogramming genes DNMT1, DNMT3B, HDAC1, and SUV39H1 were all significantly reduced in vitrified oocytes relative to the control. Evaluation of the epigenetic marks showed significant reductions in the levels of DNA methylation (6.1 ± 0.3 vs. 9.9 ± 0.5, respectively) and H3K9 acetylation (7.8 ± 0.2 vs. 10.7 ± 0.3, respectively) in 2-cell embryos in the vitrification group relative to the control. Development to the blastocyst stage partially adjusted the effects that oocyte vitrification had on the epigenetic status of embryos (DNA methylation: 4.9 ± 0.4 vs. 6.2 ± 0.6; H3K9 acetylation: 5.8 ± 0.3 vs. 8 ± 0.9, respectively). To conclude, oocyte vitrification may interfere with the critical stages of epigenetic reprogramming during preimplantation embryo development.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Anchamparuthy, VM, Pearson, RE and Gwazdauskas, FC (2010). Expression pattern of apoptotic genes in vitrified-thawed bovine oocytes. Reprod Domest Anim 45, e8390.Google ScholarPubMed
Asgari, V, Hosseini, SM, Ostadhosseini, S, Hajian, M, Azhdari, ZT, Mosaie, M and Nasr-Esfahani, MH (2012). Specific activation requirements of in vitro-matured sheep oocytes following vitrification-warming. Mol Reprod Dev 79, 434–44.CrossRefGoogle ScholarPubMed
Cao, Z, Zhang, M, Xu, T, Chen, Z, Tong, X, Zhang, D, Wang, Y, Zhang, L, Gao, D, Luo, L and Khan, IM (2019). Vitrification of murine mature metaphase II oocytes perturbs DNA methylation reprogramming during preimplantation embryo development. Cryobiology 87, 91–8.CrossRefGoogle ScholarPubMed
Chamayou, S, Bonaventura, G, Alecci, C, Tibullo, D, Di Raimondo, F, Guglielmino, A and Barcellona, ML (2011). Consequences of metaphase II oocyte cryopreservation on mRNA content. Cryobiology 62, 130–4.CrossRefGoogle ScholarPubMed
Chang, CC, Elliott, TA, Wright, G, Shapiro, DB, Toledo, AA and Nagy, ZP (2013). Prospective controlled study to evaluate laboratory and clinical outcomes of oocyte vitrification obtained in in vitro fertilization patients aged 30 to 39 years. Fertil Steril 99, 1891–7.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, 868–78.CrossRefGoogle ScholarPubMed
Cheng, KR, Fu, XW, Zhang, RN, Jia, GX, Hou, YP and Zhu, SE (2014). Effect of oocyte vitrification on deoxyribonucleic acid methylation of H19, Peg3, and Snrpn differentially methylated regions in mouse blastocysts. Fertil Steril 102, 118390e3.CrossRefGoogle ScholarPubMed
de Oliveira Leme, L, Dufort, I, Spricigo, JFW, Braga, TF, Sirard, MA, Franco, MM and Dode, MAN (2016). Effect of vitrification using the Cryotop method on the gene expression profile of in vitro-produced bovine embryos. Theriogenology 85, 724–33.CrossRefGoogle ScholarPubMed
Di Pietro, C, Vento, M, Guglielmino, MR, Borzì, P, Santonocito, M, Ragusa, M, Barbagallo, D, Duro, LR, Majorana, A, De Palma, A and Garofalo, MR (2010). Molecular profiling of human oocytes after vitrification strongly suggests that they are biologically comparable with freshly isolated gametes. Fertil Steril 94, 2804–7.CrossRefGoogle ScholarPubMed
Dupont, C and Sifer, C (2012). A review of outcome data concerning children born following assisted reproductive technologies. ISRN Obstet Gynecol 2012, 405382.CrossRefGoogle ScholarPubMed
Eroglu, B, Szurek, EA, Schall, P, Latham, KE and Eroglu, A (2020). Probing lasting cryoinjuries to oocyte-embryo transcriptome. PLoS One 15, e0231108.CrossRefGoogle ScholarPubMed
Eroglu, A, Bailey, SE, Toner, M and Toth, TL (2009). Successful cryopreservation of mouse oocytes by using low concentrations of trehalose and dimethylsulfoxide. Biol Reprod 80, 70–8.CrossRefGoogle ScholarPubMed
Fathi, M, Moawad, AR and Badr, MR (2018). Production of blastocysts following in vitro maturation and fertilization of dromedary camel oocytes vitrified at the germinal vesicle stage. PLoS One 15, e0194602.CrossRefGoogle Scholar
Fu, L, Chang, H, Wang, Z, Xie, X, Zhang, Y and Quan, F (2019). The effects of TETs on DNA methylation and hydroxymethylation of mouse oocytes after vitrification and warming. Cryobiology 90, 4146.CrossRefGoogle ScholarPubMed
Garcia-Dominguez, X, Marco-Jiménez, F, Peñaranda, DS, Diretto, G, García-Carpintero, V, Cañizares, J and Vicente, JS (2020). Long-term and transgenerational phenotypic, transcriptional and metabolic effects in rabbit males born following vitrified embryo transfer. Sci Rep 10, 15.CrossRefGoogle ScholarPubMed
Gardner, DK, Sheehan, CB, Rienzi, L, Katz-Jaffe, M and Larman, MG (2007). Analysis of oocyte physiology to improve cryopreservation procedures. Theriogenology 67, 6472.CrossRefGoogle ScholarPubMed
Hackett, JA and Surani, MA (2013). DNA methylation dynamics during the mammalian life cycle. Philos Trans R Soc Lond B Biol Sci 368, 20110328.CrossRefGoogle ScholarPubMed
El, Hajj N and Haaf, T (2013). Epigenetic disturbances in in vitro cultured gametes and embryos: implications for human assisted reproduction. Fertil Steril 99, 632–41.Google Scholar
Hosseini, SM, Asgari, V, Ostadhosseini, S, Hajian, M, Ghanaei, HR and Nasr-Esfahani, MH (2015). Developmental competence of ovine oocytes after vitrification: differential effects of vitrification steps, embryo production methods, and parental origin of pronuclei. Theriogenology 83, 366–76.CrossRefGoogle ScholarPubMed
Hosseini, SM and Nasr-Esfahani, MH (2016). What does the cryopreserved oocyte look like? A fresh look at the characteristic oocyte features following cryopreservation. Reprod Biomed Online 32, 377–87.CrossRefGoogle Scholar
Hosseini, SM, Dufor, I, Niemine, J, Moulav, F, Ghanae, HR, Hajia, M, Jafarpou, F, Forouzanfa, M, Gourba, H, Shahverd, AH and Nasr-Esfahani, MH (2016). Epigenetic modification with trichostatin A does not correct specific errors of somatic cell nuclear transfer at the transcriptomic level; highlighting the non-random nature of oocyte-mediated reprogramming errors. BMC Genomics 17, 16.CrossRefGoogle ScholarPubMed
Hu, W, Marchesi, D, Qiao, J and Feng, HL (2012). Effect of slow freeze versus vitrification on the oocyte: an animal model. Fertil Steril 98, 75260.e3.CrossRefGoogle ScholarPubMed
Li, B, Chen, S, Tang, N, Xiao, X, Huang, J, Jiang, F, Huang, X, Sun, F and Wang, X (2016). Assisted reproduction causes reduced fetal growth associated with downregulation of paternally expressed imprinted genes that enhance fetal growth in mice. Biol Reprod 94, 45.CrossRefGoogle ScholarPubMed
Liang, Y, Fu, XW, Li, JJ, Yuan, DS and Zhu, SE (2014). DNA methylation pattern in mouse oocytes and their in vitro fertilized early embryos: effect of oocyte vitrification. Zygote 22, 138–45.CrossRefGoogle ScholarPubMed
Maclellan, LJ, Carnevale, EM, Da Silva, MC, Scoggin, CF, Bruemmer JE and Squires EL 2002 Pregnancies from vitrified equine oocytes collected from super-stimulated and non-stimulated mares. Theriogenology 58, 911–9.CrossRefGoogle Scholar
Martinez-Pastor, F, Garcia-Macias, V, Alvarez, M, Chamorro, C, Herraez, P, de Paz, P and Anel, L (2006). Comparison of two methods for obtaining spermatozoa from the cauda epididymis of Iberian red deer. Theriogenology 65, 471–85.CrossRefGoogle ScholarPubMed
McGraw, S, Robert, C, Massicotte, L, Sirard, MA (2003). Quantification of histone acetyltransferase and histone deacetylase transcripts during early bovine embryo development. Biol Reprod 68, 383–9.CrossRefGoogle ScholarPubMed
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. Hum Reprod 27, 2160–8.CrossRefGoogle ScholarPubMed
Moulavi, F and Hosseini, SM (2019). Effect of macromolecule supplement on nuclear and cytoplasmic maturation, cryosurvival and in vitro embryo development of dromedary camel oocytes. Theriogenology 132, 6271.CrossRefGoogle ScholarPubMed
Moulavi, F, Asadi-Moghadam, B, Omidi, M, Yarmohammadi, M, Ozegovic, M, Rastegar, A and Hosseini, SM (2020). Pregnancy and calving rates of cloned dromedary camels produced by conventional and handmade cloning techniques and in vitro and in vivo matured oocytes. Mol Biotechnol 62, 433–42.CrossRefGoogle ScholarPubMed
O’Neill, CL, Chow, S, Rosenwaks, Z and Palermo, GD (2018). Development of ICSI. Reproduction 156, F518.CrossRefGoogle ScholarPubMed
Otoi, T, Yamamoto, K, Koyama, N, Tachikawa, S and Suzuki, T (1996). A frozen–thawed in vitro-matured bovine oocyte derived calf with normal growth and fertility. J Vet Med Sci 58, 811–3.CrossRefGoogle ScholarPubMed
Reader, KL, Stanton, JAL and Juengel, JL (2017). The role of oocyte organelles in determining developmental competence. Biology (Basel) 6, pii: E35.Google ScholarPubMed
Rienzi, L, Romano, S, Albricci, L, Maggiulli, R, Capalbo, A, Baroni, E, Colamaria, S, Sapienza, F and Ubaldi, F (2010). Embryo development of fresh ‘versus’ vitrified metaphase II oocytes after ICSI: a prospective randomized sibling-oocyte study. Hum Reprod 25, 6673.CrossRefGoogle ScholarPubMed
Saadeldin, IM, Swelum, AAA, Elsafadi, M, Mahmood, A, Yaqoob, SH, Alfayez, M and Alowaimer, AN (2019). Effects of all-trans retinoic acid on the in vitro maturation of camel (Camelus dromedarius) cumulus–oocyte complexes. J Reprod Dev 65, 215–21.CrossRefGoogle ScholarPubMed
Saadeldin, IM, Moulavi, F, Swelum, AA, Khorshid, SS, Hamid, HF and Hosseini, SM (2020). Vitrification of camel oocytes transiently impacts mitochondrial functions without affecting the developmental potential after intracytoplasmic sperm injection and parthenogenetic activation. Environ Sci Pollut Res Int 27, 44604–13.CrossRefGoogle ScholarPubMed
Saenz-de-Juano, MD, Marco-Jiménez, F, Schmaltz-Panneau, B, Jimenez-Trigos, E, Viudes-de-Castro, MP, Peñaranda, DS, Jouneau, L, Lecardonnel, J, Lavara, R, Naturil-Alfonso, C and Duranthon, V (2014). Vitrification alters rabbit foetal placenta at transcriptomic and proteomic level. Reproduction 147, 789801.CrossRefGoogle ScholarPubMed
Sekhavati, MH, Shadanloo, F, Hosseini, MS, Tahmoorespur, M, Nasiri, MR, Hajian, M and Nasr-Esfahani, MH (2012). Improved bovine ICSI outcomes by sperm selected after combined heparin-glutathione treatment. Cell Reprogram 14, 295304.CrossRefGoogle ScholarPubMed
Schattman, GL (2015). Cryopreservation of oocytes. N Engl J Med 373, 1755–60.CrossRefGoogle ScholarPubMed
Shahedi, A, Hosseini, A, Ali Khalili, M and Yeganeh, F (2017). Vitrification affects nuclear maturation and gene expression of immature human oocytes. Res Mol Med 5, 2733.Google Scholar
Shirazi, A, Naderi, MM, Hassanpour, H, Heidari, M, Borjian, S, Sarvari, A and Akhondi, MM (2016). The effect of ovine oocyte vitrification on expression of subset of genes involved in epigenetic modifications during oocyte maturation and early embryo development. Theriogenology 86, 2136–46.CrossRefGoogle ScholarPubMed
Sirard, MA (2012). Factors affecting oocyte and embryo transcriptomes. Reprod Domes Anim 4, 4855.Google Scholar
Somfai, T, Yoshioka, K, Tanihara, F, Kaneko, H, Noguchi, J, Kashiwazaki, N, Nagai, T and Kikuchi, K (2014). Generation of live piglets from cryopreserved oocytes for the first time using a defined system for in vitro embryo production. PLoS One 9, e97731.CrossRefGoogle ScholarPubMed
Spricigo, JF, Diogenes, MN, Leme, LO, Guimaraes, AL, Muterlle, CV, Silva, BDM, Solà-Oriol, D, Pivato, I, Silva, LP and Dode, MA (2015). Effects of different maturation systems on bovine oocyte quality, plasma membrane phospholipid composition and resistance to vitrification and warming. PLoS One 10, 6.CrossRefGoogle ScholarPubMed
Srirattana, K, Sripunya, N, Sangmalee, A, Imsoonthornruksa, S, Liang, Y, Ketudat-Cairns, M and Parnpai, R (2013). Developmental potential of vitrified goat oocytes following somatic cell nuclear transfer and parthenogenetic activation. Small Rum Res 112, 141–6.CrossRefGoogle Scholar
Suo, L, Meng, Q, Pei, Y, Fu, X, Wang, Y, Bunch, TD and Zhu, S (2010). Effect of cryopreservation on acetylation patterns of lysine 12 of histone H4 (acH4K12) in mouse oocytes and zygotes. J Assist Reprod Genet 27, 735–41.CrossRefGoogle ScholarPubMed
Trasler, JM, Trasler, DG, Bestor, TH, Li, E and Ghibu, F (1996). DNA methyltransferase in normal and Dnmtn/Dnmtn mouse embryos. Dev Dyn 206, 239–47.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Wu, YT, Li, C, Zhu, YM, Zou, SH, Wu, QF, Wang, LP, Wu, Y, Yin, R, Shi, CY, Lin, J, Jiang, ZR, Xu, YJ, Su, YF, Zhang, J, Sheng, JZ, Fraser, WD, Liu, ZW and Huang, HF (2018). Outcomes of neonates born following transfers of frozen–thawed cleavage-stage embryos with blastomere loss: a prospective, multicenter, cohort study BMC Med 16, 96.CrossRefGoogle ScholarPubMed
Yoder, JA, Soman, NS, Verdine, GL and Bestor, TH (1997). DNA (cytosine-5)-methyltransferases in mouse cells and tissues studies with a mechanism-based probe. J Mol Biol 270, 385–95.CrossRefGoogle ScholarPubMed