玻璃化冷冻对哺乳动物MⅡ期卵母细胞表观遗传学的影响

doi:10.16431/j.cnki.1671-7236.2020.09.020

Abstract

Abstract: As a cell preservation method with simple operation and high success rate,vitrification has many advantages,and it is widely used in agriculture,medicine,biology and other fields.However,compared with fresh oocytes,oocytes after vitrification and freezing still have many problems,such as oocytes after vitrification and freezing have lower pregnancy rate and live birth rate than fresh oocytes,abnormal gene expression and so on.Epigenetic modification allows interaction between genes and the environment without changing the DNA sequence.In the process of in vitro embryo production,external environmental factors will affect the modification of apparent heritage.This article reviewed the effects of vitrification on DNA and whole-genome methylation,histone methylation and acetylation,phosphorylation and ubiquitination,genetic imprinting,and microRNA of mammalian MⅡ oocytes in terms of epigenetics,and the effect of changes in epigenetic modification after vitrified frozen MⅡ oocytes on gene expression during transcription.It provided a reference for revealing and regulating epigenetic modification events after vitrified frozen oocytes,and further improved the quality of vitrified frozen oocytes.

Key words: vitrification; MⅡ oocytes; epigenetic modification

CLC Number:

S814.6

HAO Tong, WANG Jingjing, HAO Haisheng, DU Weihua, PANG Yunwei, ZHAO Shanjiang, ZOU Huiying, ZHANG Peipei, ZHU Huabin, ZHAO Xueming. Effect of Vitrification on Epigenetics of Mammalian MⅡ Oocytes[J]. China Animal Husbandry and Veterinary Medicine, 2020, 47(9): 2866-2875.

References

[1] LIU M H,ZHOU W H,CHU D P,et al.Ultrastructural changes and methylation of human oocytes vitrified at the germinal vesicle stage and matured in vitro after thawing[J].Gynecologic and Obstetric Investigation,2017,82(3):252-261.
[2] JONES A,VAN BLERKOM J,DAVIS P,et al.Cryopreservation of metaphase Ⅱ human oocytes effects mitochondrial membrane potential:Implications for developmental competence[J].Human Reproduction,2004,19(8):1861-1866.
[3] MANDAWALA A A,HARVEY S C,ROY T K,et al.Cryopreservation of animal oocytes and embryos:Current progress and future prospects[J].Theriogeno-logy,2016,86(7):1637-1644.
[4] COHEN Y,ST-ONGE-ST-HILAIRE A,TANNUS S,et al.Decreased pregnancy and live birth rates after vitrification of in vitro matured oocytes[J].Journal of Assisted Reproduction and Genetics,2018,35(9):1683-1689.
[5] AMIDI F,KHODABANDEH Z,NORI MOGAHI M H.Comparison of the effects of vitrification on gene expression of mature mouse oocytes using cryotop and open pulled straw[J].Fertility and Sterility Interna-tional Journal of Fertility & Sterility,2018,12(1):61-67.
[6] MILROY C,LIU L,HAMMOUD S,et al.Differential methylation of pluripotency gene promoters in in vitro matured and vitrified, in vivo-matured mouse oocytes[J].Fertility and Sterility,2011,95(6):2094-2099.
[7] BANG S,SHIN H,SONG H,et al.Autophagic activation in vitrified-warmed mouse oocytes[J].Reproduction,2014,148(1):11-19.
[8] PEREIRA B A,ZANGERONIMO M G,CASTILLO-MARTIN M,et al.Supplementing maturation medium with insulin growth factor Ⅰ and vitrification-warming solutions with reduced glutathione enhances survival rates and development ability of in vitro matured vitrified-warmed pig oocytes[J].Frontiers in Physiology Frontiers in Physiology,2018,9:1894.
[9] WOLFFE A P,MATZKE M A.Epigenetics:Regula-tion through repression[J].Science,1999,286(5439):481-486.
[10] OSMAN E,FRANASIAK J,SCOTT R.Oocyte and embryo manipulation and epigenetics[J].Seminars in Reproductive Medicine,2018,36(3-04):e1-e9.
[11] ROUGIER N,BOURC'HIS D,GOMES D M,et al.Chromosome methylation patterns during mammalian preimplantation development[J].Genes Development,1998,12(14):2108-2113.
[12] WOLFFE A P,JONES P L,WADE P A.DNA demethyla-tion[J].Proceedings of the National Academy of Sciences of the United States of America,1999,96(11):5894-5896.
[13] REIK W,DEAN W,WALTER J.Epigenetic repro-gramming in mammalian development[J].Science,2001,293(5532):1089-1093.
[14] KANG Y K,KOO D B,PARK J S,et al.Aberrant methylation of donor genome in cloned bovine embryos[J].Nature Genetics,2001,28(2):173-177.
[15] WEI Y,LANG J,ZHANG Q,et al.DNA methylation analysis and editing in single mammalian oocytes[J].Proceedings of the National Academy of Sciences of the United States of America,2019,116(20):9883-9892.
[16] CLARKE H J,VIEUX K F.Epigenetic inheritance through the female germ-line:The known,the unknown,and the possible[J].Seminars in Cell and Developmental Biology,2015,43:106-116.
[17] BIRD A W,YU D Y,PRAY-GRANT M G,et al.Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair[J].Nature,2002,419(6905):411-415.
[18] MASUMOTO H,HAWKE D,KOBAYASHI R,et al.A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response[J].Nature,2005,436(7048):294-298.
[19] RACEDO S E,WRENZYCKI C,LEPIKHOV K,et al.Epigenetic modifications and related mRNA expre-ssion during bovine oocyte in vitro maturation[J].Reproduction,Fertility and Development,2009,21(6):738-748.
[20] XU M,QIAN J,SI L,et al.The effect of epigenetic changes on the extrusion of the first polar body in pig oocytes during in vitro maturation[J].Cell Reprogram,2019,21(3):129-140.
[21] WANG Z,XU L,HE F.Embryo vitrification affects the methylation of the H19/Igf2 differentially methylated domain and the expression of H19 and Igf2[J].Fertility and Sterility,2010,93(8):2729-2733.
[22] LIANG Y,FU X W,LI J J,et al.DNA methylation pattern in mouse oocytes and their in vitro fertilized early embryos:Effect of oocyte vitrification[J].Zygote,2014,22(2):138-145.
[23] FU L,CHANG H,WANG Z,et al.The effects of TETs on DNA methylation and hydroxymethylation of mouse oocytes after vitrification and warming[J].Cryobiology,2019,90:41-46.
[24] CHEN H,ZHANG L,DENG T,et al.Effects of oocyte vitrification on epigenetic status in early bovine embryos[J].Theriogenology,2016,86(3):868-878.
[25] 贾功雪.配子冷冻对小鼠体外受精早期胚胎DNA甲基化模式的影响[D].北京:中国农业大学,2016. JIA G X.Effect of gamete cryopreservation on DNA methylation pattern in mouse in vitro fertilized early embryos[D].Beijing:China Agricultural University,2016.(in Chinese)
[26] ZHAO X M,REN J J,DU W H,et al.Effect of vitrification on prmoter CpG island methylation patterns and expression levels of DNA methyltransferase 1o,histone acetyltransferase 1,and deacetylase 1 in metaphase Ⅱ mouse oocytes[J].Fertility and Sterility,2013,100(1):256-261.
[27] NAKAYAMA J,RICE J C,STRAHL B D,et al.Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly[J].Science,2001,292(5514):110-113.
[28] RODDA D J,CHEW J L,LIM L H,et al.Transcriptional regulation of nanog by Oct4 and Sox2[J].The Journal of Biological Chemistry,2005,280(26):24731-24737.
[29] ARCARONS N,VENDRELL-FLOTATS M,YESTE M,et al.Cryoprotectant role of exopolysaccharide of Pseudomonas sp.ID1 in the vitrification of IVM cow oocytes[J].Reproduction Fertility and Development,2019,31(9):1507-1519.
[30] PARTHUN M R.Histone acetyltransferase 1:More than just an enzyme?[J].Biochimica et Biophysica Acta,2012,1819(3-4):256-263.
[31] MA P,SCHULTZ R M.Histone deacetylase 1(HDAC1) regulates histone acetylation,development,and gene expression in preimplantation mouse embryos[J].Developmental Biology,2008,319(1):110-120.
[32] CHAMBERS I,COLBY D,ROBERTSON M,et al.Functional expression cloning of Nanog,a pluripotency sustaining factor in embryonic stem cells[J].Cell,2003,113(5):643-655.
[33] YEAP L S,HAYASHI K,SURANI M A.ERG-associated protein with SET domain (ESET)-Oct4 interaction regulates pluripotency and represses the trophectoderm lineage[J].Epigenetics Chromatin,2009,2(1):12.
[34] CHENG H,ZHANG J,ZHANG S,et al.Tet3 is required for normal in vitro fertilization preimplan-tation embryos development of bovine[J].Molecular Reproduction and Development,2019,86(3):298-307.
[35] MOORE L D,LE T,FAN G.DNA methylation and its basic function[J].Neuropsychopharmacology,2013,38(1):23-38.
[36] WU X,ZHANG Y.TET-mediated active DNA demethylation:Mechanism,function and beyond[J].Nature Reviews Genetics,2017,18(9):517-534.
[37] 王振强.白藜芦醇对小鼠卵母细胞玻璃化冷冻后胚胎发育及表观遗传修饰的影响[D].杨凌:西北农林科技大学,2018. WANG Z Q.Effect of resveratrol on embryo development and epigenetic modification of mouse oocytes after vitrification[D].Yangling:Northwest A&F University,2018.(in Chinese)
[38] 傅良政.TET蛋白对玻璃化冷冻卵母细胞DNA甲基化和羟甲基化的影响[D].杨凌:西北农林科技大学,2018. FU L Z.The effect of TET proteins on DNA methylation and hydroxymethilation of vitrified oocyte[D].Yangling:Northwest A&F University,2018.(in Chinese)
[39] CAO Z,ZHANG M,XU T,et al.Vitrification of murine mature metaphase Ⅱ oocytes perturbs DNA methylation reprogramming during preimplantation embryo development[J].Cryobiology,2019,87:91-98.
[40] HU W,MARCHESI D,QIAO J,et al.Effect of slow freeze versus vitrification on the oocyte:An animal model[J].Fertility and Sterility,2012,98(3):752.e3-760.e3.
[41] TORRES-PADILLA M E,PARFITT D E,KOUZARIDES T,et al.Histone arginine methylation regulates pluripotency in the early mouse embryo[J].Nature,2007,445(7124):214-218.
[42] FREITAG M,SELKER E U.Controlling DNA methylation:Many roads to one modification[J].Current Opinion in Genetics & Development,2005,15(2):191-199.
[43] YAN L Y,YAN J,QIAO J,et al.Effects of oocyte vitrification on histone modifications[J].Repro-duction,Fertility,and Development,2010,22(6):920-925.
[44] SPINACI M,VALLORANI C,BUCCI D,et al.Vitrification of pig oocytes induces changes in histone H4 acetylation and histone H3 lysine 9 methylation (H3K9)[J].Veterinary Research Communications,2012,36(3):165-171.
[45] ZHANG K,WILLIAMS K E,HUANG L,et al.Histone acetylation and deacetylation:Identification of acetylation and methylation sites of HeLa histone H4 by mass spectrometry[J].Molecular & Cellular Pro-teomics,2002,1(7):500-508.
[46] KOUZARIDES T.Chromatin modifications and their function[J].Cell,2007,128(4):693-705.
[47] 周光斌,曾艳,孟庆勇,等.超低温冷冻对牛卵母细胞组蛋白乙酰化和膜蛋白CD9表达的影响[J].中国兽医学报,2014,34(6):999-1004. ZHOU G B,ZENG Y,MENG Q Y,et al.The effect of bovine oocyte cryopreservation on the histone acetylation and CD9 expression[J].Chinese Journal of Veterinary Science,2014,34(6):999-1004.(in Chinese)
[48] SUO L,MENG Q,PEI Y,et al.Effect of cryopreservation on acetylation patterns of lysine 12 of histone H4(acH4K12) in mouse oocytes and zygotes[J].Journal of Assisted Reproduction and Genetics,2010,27(12):735-741.
[49] GHAZIFARD A,SALEHI M,GHAFFARI NOVIN M,et al.Anacardic acid reduces acetylation of H4K12 in mouse oocytes during vitrification[J].Cell Journal,2019,20(4):552-558.
[50] LI J J,FU X W,MO X H,et al.Vitrification alters acH4K12 and acH4K16 levels in sheep oocytes at various developmental stages[J].Small Ruminant Research,2013,112(1-3):108-113.
[51] LI J J,PEI Y,ZHOU G B,et al.Histone deacetyltransferase1 expression in mouse oocyte and their in vitro-fertilized embryo:Effect of oocyte vitrification[J].Cryo Letters,2011,32(1):13-20.
[52] 梁前进,王鹏程,白燕荣.蛋白质磷酸化修饰研究进展[J].科技导报,2012,30(31):73-79. LIANG Q J,WANG P C,BAI Y R.Summarization on the progress in protein phosphorylation[J].Science & Technology Review,2012,30(31):73-79.(in Chinese)
[53] TAN Y J,ZHANG X Y,DING G L,et al.Aquaporin7 plays a crucial role in tolerance to hyperosmotic stress and in the survival of oocytes during cryopreservation[J].Scientific Reports,2015,5:17741.
[54] SARKISSIAN M,MENDEZ R,RICHTER J D.Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3[J].Genes & Deve-lopment,2004,18(1):48-61.
[55] GOLDSTEIN G,SCHEID M,HAMMERLING U,et al.Isolation of a polypeptide that has lymphocyte-differentiating properties and is probably represented universally in living cells[J].Proceedings of the National Academy of Sciences of the United States of America,1975,72(1):11-15.
[56] HERRMANN J,LERMAN L O,LERMAN A.Ubiquitin and ubiquitin-like proteins in protein regulation[J].Circulation Research,2007,100(9):1276-1291.
[57] MURATANI M,TANSEY W P.How the ubiquitin-proteasome system controls transcription[J].Nature Reviews:Molecular Cell Biology,2003,4(3):192-201.
[58] SHAID S,BRANDTS C H,SERVE H,et al.Ubiquitination and selective autophagy[J].Cell Death and Differentiation,2013,20(1):21-30.
[59] ULRICH H D,WALDEN H.Ubiquitin signalling in DNA replication and repair[J].Nature Reviews:Molecular Cell Biology,2010,11(7):479-489.
[60] MONZO C,HAOUZI D,ROMAN K,et al.Slow freezing and vitrification differentially modify the gene expression profile of human metaphase Ⅱ oocytes[J].Human Reproduction,2012,27(7):2160-2168.
[61] BARLOW D P.Gametic imprinting in mammals[J].Science,1995,270(5242):1610-1613.
[62] MORGAN H D,SANTOS F,GREEN K,et al.Epigenetic reprogramming in mammals[J].Human Molecular Genetics,2005,14(1):R47-R58.
[63] LEFF S E,BRANNAN C I,REED M L,et al.Maternal imprinting of the mouse Snrpn gene and conserved linkage homology with the human Prader-Willi syndrome region[J].Nature Genetics,1992,2(4):259-264.
[64] CHENG K R,FU X W,ZHANG R N,et al.Effect of oocyte vitrification on deoxyribonucleic acid methyla-tion of H19,Peg3,and Snrpn differentially methylated regions in mouse blastocysts[J].Fertility and Sterility,2014,102(4):1183.e3-1190.e3.
[65] KOPPES E,HIMES K P,CHAILLET J R.Partial loss of genomic imprinting reveals important roles for Kcnq1 and Peg10 imprinted domains in placental development[J].PLoS One,2015,10(8):e0135202.
[66] AUGUI S,NORA E P,HEARD E.Regulation of X-chromosome inactivation by the X-inactivation centre[J].Nature Reviews Genetics,2011,12(6):429-442.
[67] CHEN H,ZHANG L,WANG Z,et al.Resveratrol improved the developmental potential of oocytes after vitrification by modifying the epigenetics[J].Molecular Reproduction and Development,2019,86(7):862-870.
[68] POWELL K,ROOKE J A,MCEVOY T G,et al.Zygote donor nitrogen metabolism and in vitro embryo culture perturbs in utero development and IGF2R expression in ovine fetal tissues[J].Theriogeno-logy,2006,66(8):1901-1912.
[69] TAKADA S,TEVENDALE M,BAKER J,et al.Delta-like and gtl2 are reciprocally expressed,differentially methylated linked imprinted genes on mouse chromosome 12[J].Current Biology,2000,10(18):1135-1138.
[70] LAU N C,LIM L P,WEINSTEIN E G,et al.An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans[J].Science,2001,294(5543):858-862.
[71] LAURENT L C.microRNAs in embryonic stem cells and early embryonic development[J].Journal of Cellular and Molecular Medicine,2008,12(6a):2181-2188.
[72] AMBROS V.microRNAs:Tiny regulators with great potential[J].Cell,2001,107(7):823-826.
[73] MCGINNIS L K,LUENSE L J,CHRISTENSON L K.microRNA in ovarian biology and disease[J].Cold Spring Harbor Perspectives in Medicine,2015,5(9):a022962.
[74] GILCHRIST G C,TSCHERNER A,NALPATHAMK-ALAM T,et al.microRNA expression during bovine oocyte maturation and fertilization[J].International Journal of Molecular Sciences,2016,17(3):396.
[75] BATTAGLIA R,VENTO M E,RAGUSA M,et al.microRNAs are stored in human MⅡ oocyte and their expression profile changes in reproductive aging[J].Biology of Reproduction,2016,95(6):131.
[76] LI J,YANG X,LIU F,et al.Evaluation of differentially expressed microRNAs in vitrified oocytes by next generation sequencing[J].International Journal of Biochemistry & Cell Biology,2019,112:134-140.
[77] MAIDARTI M,CLARKSON Y L,MCLAUGHLIN M,et al.Inhibition of PTEN activates bovine non-growing follicles in vitro but increases DNA damage and reduces DNA repair response[J].Human Reproduc-tion,2019,34(2):297-307.
[78] MATSUDA S,NAKAGAWA Y,KITAGISHI Y,et al.Reactive oxygen species,superoxide dimutases,and PTEN-p53-AKT-MDM2 signaling loop network in mesenchymal stem/stromal cells regulation[J].Cells,2018,7(5):36.
[79] PAN B,YANG H,WU Z,et al.Melatonin improves parthenogenetic development of vitrified-warmed mouse oocytes potentially by promoting G1/S cell cycle progression[J].International Journal of Molecular Sciences,2018,19(12):4029.
[80] ZHANG Y,LI W,MA Y,et al.Improved development by melatonin treatment after vitrification of mouse metaphase Ⅱ oocytes[J].Cryobiology,2016,73(3):335-342.
[81] HABIBI A,FARROKHI N,MOREIRA DA SILVA F,et al.The effects of vitrification on gene expression in mature mouse oocytes by nested quantitative PCR[J].Journal of Assisted Reproduction and Genetics,2010,27(11):599-604.
[82] KAJI K,ODA S,SHIKANO T,et al.The gamete fusion process is defective in eggs of CD9-deficient mice[J].Nature Genetics,2000,24(3):279-282.
[83] TAN Y J,XIONG Y,DING G L,et al.Cryopro-tectants up-regulate expression of mouse oocyte AQP7,which facilitates water diffusion during cryopreserva-tion[J].Fertility and Sterility,2013,99(5):1428-1435.
[84] EL MOUATASSIM S,GUERIN P,MENEZO Y.Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation[J].Molecular Human Reproduction,1999,5(8):720-725.
[85] DI PIETRO C,VENTO M,GUGLIELMINO M R,et al.Molecular profiling of human oocytes after vitrifica-tion strongly suggests that they are biologically comparable with freshly isolated gametes[J].Fertility and Sterility,2010,94(7):2804-2807.
[86] DAI J,WU C,MUNERI C W,et al.Changes in mitochondrial function in porcine vitrified MⅡ-stage oocytes and their impacts on apoptosis and developmental ability[J].Cryobiology,2015,71(2):291-298.
[87] NIU Y,DAI J,CHEN Y,et al.Positive effect of apoptotic inhibitor z-vad-fmk on vitrified-thawed porcine mii stage oocytes[J].Cryo Letters,2016,37(3):188-195.
[88] DAI J J,NIU Y F,WU C F,et al.Both death receptor and mitochondria mediated apoptotic pathways participated the occurrence of apoptosis in porcine vitrified MⅡ stage oocytes[J].Cryo Letters,2016,37(2):129-136.
[89] HIROSE M,KAMOSHITA M,FUJIWARA K,et al.Vitrification procedure decreases inositol 1,4,5-trisphophate receptor expression,resulting in low fertility of pig oocytes[J].Journal of Animal Science,2013,84(10):693-701.
[90] WEI X,SIJIE Y,WEIBIN Z,et al.Cytoskeleton genes expression and survival rate comparison between immature and mature yak oocyte after OPS vitrification[J].Animal Biotechnology,2018,29(4):247-251.
[91] ZHAO X M,HAO H S,DU W H,et al.Melatonin inhibits apoptosis and improves the developmental potential of vitrified bovine oocytes[J].Journal of Pineal Research,2016,60(2):132-141.
[92] ZHOU G B,ZENG Y,MENG Q G,et al.Decreased expression of CD9 in bovine oocytes after cryopreservation and the relationship to fertilization capacity[J].Molecular Reproduction and Deve-lopment,2013,80(6):451-459.
[93] YANG M Y,RAJAMAHENDRAN R.Expression of Bcl-2 and Bax proteins in relation to quality of bovine oocytes and embryos produced in vitro[J].Animal Reproduction Science,2002,70(3-4):159-169.
[94] LAZZARI G,WRENZYCKI C,HERRMANN D,et al.Cellular and molecular deviations in bovine in vitro-produced embryos are related to the large offspring syndrome[J].Biology of Reproduction,2002,67(3):767-775.
[95] MAECKER H T,TODD S C,LEVY S.The tetraspanin superfamily:Molecular facilitators[J].FASEB Journal,1997,11(6):428-442.
[96] SHIRAZI A,NADERI M M,HASSANPOUR H,et al.The effect of ovine oocyte vitrification on expression of subset of genes involved in epigenetic modifications during oocyte maturation and early embryo deve-lopment[J].Theriogenology,2016,86(9):2136-2146.
[97] EBRAHIMI B,VALOJERDI M R,EFTEKHARI-YAZDI P,et al.IVM and gene expression of sheep cumulus-oocyte complexes following different methods of vitrification[J].Reproductive BioMedicine Online,2010,20(1):26-34.
[98] HOSSEINI S M,ASGARI V,OSTADHOSSEINI S,et al.Potential applications of sheep oocytes as affected by vitrification and in vitro aging[J].Theriogenology,2012,77(9):1741-1753.
[99] SUCCU S,BEBBERE D,BOGLIOLO L,et al.Vitrification of in vitro matured ovine oocytes affects in vitro pre-implantation development and mRNA abundance[J].Molecular Reproduction and Development,2008,75(3):538-546.
[100] GAO L,JIA G,LI A,et al.RNA-Seq transcriptome profiling of mouse oocytes after in vitro maturation and/or vitrification[J].Scientific Reports,2017,7(1):13245.
[101] WANG N,LI C Y,ZHU H B,et al.Effect of vitrification on the mRNA transcriptome of bovine oocytes[J].Reproduction in Domestic Animals,2017,52(4):531-541.
[102] CHAMAYOU S,BONAVENTURA G,ALECCI C,et al.Consequences of metaphase Ⅱ oocyte cryopreser-vation on mRNA content[J].Cryobiology,2011,62(2):130-134.

Effect of Vitrification on Epigenetics of Mammalian MⅡ Oocytes

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[11]	JIANG Ze, XUAN Biao, LI Zuo-chen, WANG Yi-nan, JIN Yi. Effect of LDL on the Mitochondrial Transmembrane Potential and ZP Protein Ubiquitination in Vitrified-warmed MⅡ Oocytes [J]. , 2017, 44(7): 1961-1966.
[12]	WANG Na, LI Chong-yang, ZHU Hua-bin, HAO Hai-sheng, WANG Hao-yu, YAN Chang-liang, DU Wei-hua, WANG Dong, LIU Yan, PANG Yun-wei, ZHAO Xue-ming. Regulation of Mitochondrial Ca²⁺ in Vitrified Bovine Oocytes by Ruthenium Red [J]. , 2017, 44(5): 1431-1437.
[13]	WU Guo-quan, QUAN Guo-bo, LV Chun-rong, SHAO Qing-yong, HONG Qiong-hua. Comparative Effects of Porcine Oocytes Vitrified at the GV and MⅡ Stages [J]. , 2017, 44(3): 807-812.
[14]	WANG Na, HAO Hai-sheng, WANG Hao-yu, DU Wei-hua, QIN Tong, LIU Yan, ZHU Hua-bin, ZHAO Xue-ming. The Influencing Mechanism of Vitrification on the Intracellular Calcium of Mammalian Oocytes [J]. , 2016, 43(3): 768-775.
[15]	SONG Min-yan, YU Ying. The Main Research Fields and Progress of Livestock Epigenetics [J]. , 2016, 43(10): 2701-2709.