钙离子在哺乳动物卵母细胞发育关键时期的作用
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摘要
Ca~(2+)是广泛存在的信号分子,钙信号转导对多种细胞生理生化活动有重要的调控作用,越来越多的证据表明钙信号参与卵母细胞减数分裂。钙稳态是细胞内Ca~(2+)信号在时间和空间上的动态平衡,对卵母细胞钙稳态的研究是目前重要的研究热点之一。本文综述了钙稳态及钙离子对卵母细胞成熟和发育过程中的双线期阻滞恢复、MII期阻滞恢复和细胞凋亡的作用,发现某些哺乳动物双线期及MII期适当增加胞内钙离子水平可以使卵母细胞退出阻滞,而超出生理水平的胞内钙则会诱导细胞凋亡,并通过探究钙离子在卵母细胞减数分裂恢复和调控凋亡过程中的作用机制,为辅助生殖技术的进一步研究提供依据。
Ca~(2+)is a ubiquitous signaling molecule.Calcium signal transduction plays an important regulatory role in a variety of physiological and biochemical activities of cells.More and more evidence shows that Calcium signal is involved in oocytes meiosis.Calcium homeostasis is the dynamic balance of intracellular Ca~(2+)signals in both time and space.The study of calcium homeostasis in oocytes is one of the important research hotspots.This article reviews the effects of calcium homeostasis and calcium on the meiotic resumption from diplotene arrest,meiotic resumption from MII arrest and apoptosis.Studies have found that in certain mammals,oocyte exit the block from both the diplotene and MII phases by appropriately increasing intracellular calcium levels,however,intracellular calcium that exceeds the physiological level will induce apoptosis.To explore the mechanism of calcium ions in meiotic resumption and apoptosis in oocytes is beneficial to the further study of assisted reproductive technology.
Ca~(2+)is a ubiquitous signaling molecule.Calcium signal transduction plays an important regulatory role in a variety of physiological and biochemical activities of cells.More and more evidence shows that Calcium signal is involved in oocytes meiosis.Calcium homeostasis is the dynamic balance of intracellular Ca~(2+)signals in both time and space.The study of calcium homeostasis in oocytes is one of the important research hotspots.This article reviews the effects of calcium homeostasis and calcium on the meiotic resumption from diplotene arrest,meiotic resumption from MII arrest and apoptosis.Studies have found that in certain mammals,oocyte exit the block from both the diplotene and MII phases by appropriately increasing intracellular calcium levels,however,intracellular calcium that exceeds the physiological level will induce apoptosis.To explore the mechanism of calcium ions in meiotic resumption and apoptosis in oocytes is beneficial to the further study of assisted reproductive technology.
引文
[1] Paleos G A,Powers R D.The effect of calcium on the first meiotic division of the mammalian oocyte[J].Journal of Experimental Zoology,1981,217(3):409-416
[2] Carroll J,Swann K.Spontaneous cytosolic calcium oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes[J].Journal of Biological Chemistry,1992,267(16):11196-11201
[3] Tombes R M,Simerly C,Borisy G G,Schatten G.Meiosis,egg activation, and nuclear envelope breakdownare differentially reliant on Ca2+, whereas germinal vesicle breakdown is Ca2+independent in the mouse oocyte[J].Journal of Cell Biology,1992,117(4):799-811
[4] Homa S T,Carroll J,Swann K.Fertilization and early embryology:The role of calcium in mammalian oocyte maturation and egg activation[J].Human Reproduction,1993,8(8):1274-1281
[5] Homa S T.Calcium and meiotic maturation of the mammalian oocyte[J].Molecular Reproduction and Development,1995,40(1):122-134
[6] Machaca K. Ca2+signaling differentiation during oocyte maturation[J].Journal of Cellular Physiology,2007,213(2):331-340
[7] Duesbery N S,Masui Y.The role of Ca2+in progesteroneinduced germinal vesicle breakdown of Xenopus laevis oocytes:the synergic effects of microtubule depolymerization and Ca2+[J].Development Genes and Evolution,1996,206(2):110-124
[8] Mehlmann L M.Stops and starts in mammalian oocytes:recent advances in understanding the regulation of meiotic arrest and oocyte maturation[J].Reproduction,2005,130(6):791-799
[9] Sun L,Hodeify R,Haun S,Charlesworth A,MacNicol A M,Ponnappan S,Ponnappan U,Prigent C,Machaca K.Ca2+homeostasis regulates Xenopus oocyte maturation[J].Biology of Reproduction 2008,78(4):726-735
[10] Liang S L,Zhao Q J,Li X C,Jin Y P,WangY P,Su X H,Guan W J,Ma Y H.Dynamic analysis of Ca2+level during bovine oocytes maturation and early embryonic development[J].Journal of Veterinary Science,2011,12(2):133-142
[11] Courjaret R,Dib M,Machaca K.Store-operated Ca2+entry in oocytes modulate the dynamics of IP3-dependent Ca2+release from oscillatory to tonic[J].Journal of Cellular Physiology,2017,232(5):1095-1103
[12] Bagur R,Hajnóczky G.Intracellular Ca2+sensing:Its role in calcium homeostasis and signaling[J].Molecular Cell,2017,66(6):780-788
[13] Clapham D E.Calcium signaling[J].Cell,2007,131(6):1047-1058
[14] Hajnóczky G,Csords G,Das S,Garcia-Perez C,Saotome M Q,Sinha Roy S,Yi M Q.Mitochondrial calcium signalling and cell death:Approaches for assessing the role of mitochondrial Ca2+uptake in apoptosis[J].Cell Calcium,2006,40(5-6):553-560
[15] Bygrave F L.Mitochondria and the control of intracellular calcium[J].Biological Reviews of the Cambridge Philosophical Society,1978,53(1):43-79
[16] Carafoli E,Crompton M.The regulation of intracellular calcium by mitochondria[J].Annals of the New York Academy of Sciences,1978,307:269-284
[17] Guerini D,Coletto L,Carafoli E.Exporting calcium from cells[J].Cell Calcium,2005,38(3-4):281-289
[18] Strehler E,Treiman M.Calcium pumps of plasma membrane and cell interior[J].Current Molecular Medicine,2004,4(3):323-335
[19] MacHaty Z.Signal transduction in mammalian oocytes during fertilization[J].Cell and Tissue Research,2016,363(1):169-183
[20] Tripathi A,Kumar K V,Chaube S K.Meiotic cell cycle arrest in mammalian oocytes[J].Journal of Cellular Physiology,2010,223(3):592-600
[21] Chaube S K,Khatun S,Misra S K,Shrivastav T G.Calcium ionophore-induced egg activation and apoptosis are associated with the generation of intracellular hydrogen peroxide[J].Free Radical Research,2008,42(3):212-220
[22] Tosti E.Calcium ion currents mediating oocyte maturation events[J].Reproductive Biology and Endocrinology,2006,4:26
[23] Prasad S,Tiwari M,Tripathi A,Pandey A N,Chaube S K.Changes in signal molecules and maturation promoting factor levels associate with spontaneous resumption of meiosis in rat oocytes[J].Cell Biology International,2015,39(6):759-769
[24] Cheon Y P,Kim S W,Kim S J,Yeom Y I,Cheong C,Ha K S.The role of RhoA in the germinal vesicle breakdown of mouse oocytes[J].Biochemical and Biophysical Research Communications,2000,273(3):997-1002
[25] Ito J,Kaneko R,Hirabayashi M.The regulation of calcium/calmodulin-dependent protein kinase II during oocyte activation in the rat[J].The Journal of Reproduction and Development,2006,52(3):439-447
[26] Lu Q,Chen Z J,Gao X,Ma S Y,Li M,Feng H L.Oocyte activation with calcium ionophore A23187and puromycin on human oocytes that failed to fertilize after intracytoplasmic sperm injection[J].Zhonghua Fu Chan Ke Za Zhi,2006,41(3):182-185
[27] Yoo J G,Smith L C.Extracellular calcium induces activation of Ca2+/calmodulin-dependent protein kinase II and mediates spontaneous activation in rat oocytes[J].Biochemical and Biophysical Research Communications,2007,359(4):854-859
[28] Hwang H, Cheon Y P. Adenosine receptors mediated intracellular calcium in cumulus cells involved in the maintenance of first meiotic arrest[J]. Biology of Deproduction,2013,17(2):141-147
[29] Tosti E,Boni R,Cuomo A.Ca2+current activity decreases during meiotic progression in bovine oocytes[J].American Journal of Physiology-Cell Physiology,2000,279(6):C1795-800
[30] Bae I H,Channing C P.Effect of calcium ion on the maturation of cumulus-enclosed pig follicular oocytes isolated from medium-sized graafian follicles[J]. Biology of Reproduction,1985,33(1):79-87
[31] Lefèvre B,Pesty A,Testart J.Cytoplasmic and nucleic calcium oscillations in immature mouse oocytes:Evidence of wave polarization by confocal imaging[J].Experimental Cell Research,1995,218(1):166-173
[32] Boni R,Cuomo A,Tosti E.Developmental potential in bovine oocytes is related to cumulus-oocyte complex grade,calcium current activity,and calcium stores[J].Biology of Reproduction,2002,66(3):836-842
[33] Fan H Y,Huo L J,Meng X Q,Zhong Z S,Hou Y,Chen D Y,Sun Q Y.Involvement of calcium/calmodulin-dependent protein kinase II(CaMKII)in meiotic maturation and activation of pig oocytes[J].Biology of Reproduction,2003,69(5):1552-1564
[34] Petr J,Rozinek J,Hruban V,Jílek F,SedmíkovM,VanˇourkovZ,Němecˇk Z.Ultrastructural localization of calcium deposits during in vitro culture of pig oocytes[J].Molecular Reproduction and Development,2001,58(2):196-204
[35] Madgwick S,Jones K T.How eggs arrest at metaphase II:MPF stabilisation plus APC/C inhibition equals cytostatic factor[J].Cell Division,2007,2:4
[36] Whitaker M.Calcium at fertilization and in early development[J].Physiological Reviews,2006,86(1):25-88
[37] Wakai T,Fissore R A.Ca2+homeostasis and regulation of ER Ca2+in mammalian oocytes/eggs[J].Cell Calcium,2013,53(1):63-67
[38] Xu Z,Abbott A,Kopf G S,Schultz R M,Ducibella T.Spontaneous activation of ovulated mouse eggs:Timedependent effects on M-phase exit, cortical granule exocytosis,maternal messenger ribonucleic acid recruitment,and inositol 1,4,5-trisphosphate sensitivity[J].Biology of Reproduction,1997,57(4):743-750
[39] Premkumar K V,Chaube S K.An insufficient increase of cytosolic free calcium level results postovulatory aginginduced abortive spontaneous egg activation in rat[J].Journal of Assisted Reproduction and Genetics,2013,30(1):117-123
[40] Nader N,Kulkarni R P,Dib M,Machaca K.How to make a good egg!:The need for remodeling of oocyte Ca2+signaling to mediate the egg-to-embryo transition[J].Cell Calcium,2013,53(1):41-54
[41] Premkumar K V, Chaube S K. RyR channel-mediated increase of cytosolic free calcium level signals cyclin B1degradation during abortive spontaneous egg activation in rat[J].In Vitro Cellular&Developmental Biology,2014,50(7):640-647
[42] Premkumar K V, Chaube S K. Nitric oxide signals postovulatoryaging-inducedabortivespontaneousegg activation in rats[J].Redox Report:Communications in Free Radical Research,2015,20(4):184-192
[43] Hu H M,Mo X H,Li X,Fu X W,Hou Y P.BAPTA-AM dramatically improves maturation and development of bovine oocytes from grade-3 cumulus-oocyte complexes[J].Molecular Reproduction and Development,2018,85(1):38-45
[44] Orrenius S,Zhivotovsky B,Nicotera P.Regulation of cell death:The calcium-apoptosis link[J].Nature Reviews.Molecular Cell Biology,2003,4(7):552-565
[45] Tripathi A,Chaube S K.High cytosolic free calcium level signals apoptosis through mitochondria-caspase mediated pathway in rat eggs cultured in vitro[J].Apoptosis,2012,17(5):439-448
[46] Ma W,Zhang D,Hou Y,Li Y H,Sun Q Y,Sun X F,Wang W H.Reduced expression of MAD2,BCL2,and MAP kinase activity in pig oocytes after in vitro aging are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation[J].Biology of Reproduction,2005,72(2):373-383
[47] Sergeev I N,Norman A W.Calcium as a mediator of apoptosis in bovine oocytes and preimplantation embryos[J].Endocrine,2003,22(2):169-176
[48] Wang Z G,Wang W,Yu S D,Xu Z R.Effects of different activationprotocolsonpreimplantationdevelopment,apoptosis and ploidy of bovine parthenogenetic embryos[J].Animal Reproduction Science,2008,105(3-4):292-301
[49] Liu L, Trimarchi J R, Keefe D L.Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes[J].Biology of Reproduction,2000,62(6):1745-1753
[50] Zhang N,Fissore R A.Role of caspase-3cleaved IP3 R1on Ca2+homeostasis and developmental competence of mouse oocytes and eggs[J].Journal of Cellular Physiology,2014,229(11):1842-1854
[51] Gordo A C,Rodrigues P,Kurokawa M,Jellerette T,Exley G E,Warner C,Fissore R.Intracellular calcium oscillations signal apoptosis rather than activation in invitroaged mouse eggs[J].Biology of Reproduction,2002,66(6):1828-1837
[52] Chaube S K,Prasad P V,Thakur S C,Shrivastav T G.Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro[J].Apoptosis:An International Journal on Programmed Cell Death,2005,10(4):863-874
[53] Zhu J,Lin F H,Zhang J,Lin J,Li H,Li Y W,Tan X W,Tan J H.The signaling pathways by which the Fas/FasL system accelerates oocyte aging[J].Aging,2016,8(2):291-303
[54] Oh J S,Susor A,Conti M.Protein tyrosine kinase Wee1Bis essential for metaphase II exit in mouse oocytes[J].Science,2011,332(6028):462-465
[55] Kubiak J Z,Ciemerych M A, Hupalowska A,SikoraPolaczek M,Polanski Z.On the transition from the meiotic to mitotic cell cycle during early mouse development[J].The International Journal of Developmental Biology,2008,52(2-3):201-217
[2] Carroll J,Swann K.Spontaneous cytosolic calcium oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes[J].Journal of Biological Chemistry,1992,267(16):11196-11201
[3] Tombes R M,Simerly C,Borisy G G,Schatten G.Meiosis,egg activation, and nuclear envelope breakdownare differentially reliant on Ca2+, whereas germinal vesicle breakdown is Ca2+independent in the mouse oocyte[J].Journal of Cell Biology,1992,117(4):799-811
[4] Homa S T,Carroll J,Swann K.Fertilization and early embryology:The role of calcium in mammalian oocyte maturation and egg activation[J].Human Reproduction,1993,8(8):1274-1281
[5] Homa S T.Calcium and meiotic maturation of the mammalian oocyte[J].Molecular Reproduction and Development,1995,40(1):122-134
[6] Machaca K. Ca2+signaling differentiation during oocyte maturation[J].Journal of Cellular Physiology,2007,213(2):331-340
[7] Duesbery N S,Masui Y.The role of Ca2+in progesteroneinduced germinal vesicle breakdown of Xenopus laevis oocytes:the synergic effects of microtubule depolymerization and Ca2+[J].Development Genes and Evolution,1996,206(2):110-124
[8] Mehlmann L M.Stops and starts in mammalian oocytes:recent advances in understanding the regulation of meiotic arrest and oocyte maturation[J].Reproduction,2005,130(6):791-799
[9] Sun L,Hodeify R,Haun S,Charlesworth A,MacNicol A M,Ponnappan S,Ponnappan U,Prigent C,Machaca K.Ca2+homeostasis regulates Xenopus oocyte maturation[J].Biology of Reproduction 2008,78(4):726-735
[10] Liang S L,Zhao Q J,Li X C,Jin Y P,WangY P,Su X H,Guan W J,Ma Y H.Dynamic analysis of Ca2+level during bovine oocytes maturation and early embryonic development[J].Journal of Veterinary Science,2011,12(2):133-142
[11] Courjaret R,Dib M,Machaca K.Store-operated Ca2+entry in oocytes modulate the dynamics of IP3-dependent Ca2+release from oscillatory to tonic[J].Journal of Cellular Physiology,2017,232(5):1095-1103
[12] Bagur R,Hajnóczky G.Intracellular Ca2+sensing:Its role in calcium homeostasis and signaling[J].Molecular Cell,2017,66(6):780-788
[13] Clapham D E.Calcium signaling[J].Cell,2007,131(6):1047-1058
[14] Hajnóczky G,Csords G,Das S,Garcia-Perez C,Saotome M Q,Sinha Roy S,Yi M Q.Mitochondrial calcium signalling and cell death:Approaches for assessing the role of mitochondrial Ca2+uptake in apoptosis[J].Cell Calcium,2006,40(5-6):553-560
[15] Bygrave F L.Mitochondria and the control of intracellular calcium[J].Biological Reviews of the Cambridge Philosophical Society,1978,53(1):43-79
[16] Carafoli E,Crompton M.The regulation of intracellular calcium by mitochondria[J].Annals of the New York Academy of Sciences,1978,307:269-284
[17] Guerini D,Coletto L,Carafoli E.Exporting calcium from cells[J].Cell Calcium,2005,38(3-4):281-289
[18] Strehler E,Treiman M.Calcium pumps of plasma membrane and cell interior[J].Current Molecular Medicine,2004,4(3):323-335
[19] MacHaty Z.Signal transduction in mammalian oocytes during fertilization[J].Cell and Tissue Research,2016,363(1):169-183
[20] Tripathi A,Kumar K V,Chaube S K.Meiotic cell cycle arrest in mammalian oocytes[J].Journal of Cellular Physiology,2010,223(3):592-600
[21] Chaube S K,Khatun S,Misra S K,Shrivastav T G.Calcium ionophore-induced egg activation and apoptosis are associated with the generation of intracellular hydrogen peroxide[J].Free Radical Research,2008,42(3):212-220
[22] Tosti E.Calcium ion currents mediating oocyte maturation events[J].Reproductive Biology and Endocrinology,2006,4:26
[23] Prasad S,Tiwari M,Tripathi A,Pandey A N,Chaube S K.Changes in signal molecules and maturation promoting factor levels associate with spontaneous resumption of meiosis in rat oocytes[J].Cell Biology International,2015,39(6):759-769
[24] Cheon Y P,Kim S W,Kim S J,Yeom Y I,Cheong C,Ha K S.The role of RhoA in the germinal vesicle breakdown of mouse oocytes[J].Biochemical and Biophysical Research Communications,2000,273(3):997-1002
[25] Ito J,Kaneko R,Hirabayashi M.The regulation of calcium/calmodulin-dependent protein kinase II during oocyte activation in the rat[J].The Journal of Reproduction and Development,2006,52(3):439-447
[26] Lu Q,Chen Z J,Gao X,Ma S Y,Li M,Feng H L.Oocyte activation with calcium ionophore A23187and puromycin on human oocytes that failed to fertilize after intracytoplasmic sperm injection[J].Zhonghua Fu Chan Ke Za Zhi,2006,41(3):182-185
[27] Yoo J G,Smith L C.Extracellular calcium induces activation of Ca2+/calmodulin-dependent protein kinase II and mediates spontaneous activation in rat oocytes[J].Biochemical and Biophysical Research Communications,2007,359(4):854-859
[28] Hwang H, Cheon Y P. Adenosine receptors mediated intracellular calcium in cumulus cells involved in the maintenance of first meiotic arrest[J]. Biology of Deproduction,2013,17(2):141-147
[29] Tosti E,Boni R,Cuomo A.Ca2+current activity decreases during meiotic progression in bovine oocytes[J].American Journal of Physiology-Cell Physiology,2000,279(6):C1795-800
[30] Bae I H,Channing C P.Effect of calcium ion on the maturation of cumulus-enclosed pig follicular oocytes isolated from medium-sized graafian follicles[J]. Biology of Reproduction,1985,33(1):79-87
[31] Lefèvre B,Pesty A,Testart J.Cytoplasmic and nucleic calcium oscillations in immature mouse oocytes:Evidence of wave polarization by confocal imaging[J].Experimental Cell Research,1995,218(1):166-173
[32] Boni R,Cuomo A,Tosti E.Developmental potential in bovine oocytes is related to cumulus-oocyte complex grade,calcium current activity,and calcium stores[J].Biology of Reproduction,2002,66(3):836-842
[33] Fan H Y,Huo L J,Meng X Q,Zhong Z S,Hou Y,Chen D Y,Sun Q Y.Involvement of calcium/calmodulin-dependent protein kinase II(CaMKII)in meiotic maturation and activation of pig oocytes[J].Biology of Reproduction,2003,69(5):1552-1564
[34] Petr J,Rozinek J,Hruban V,Jílek F,SedmíkovM,VanˇourkovZ,Němecˇk Z.Ultrastructural localization of calcium deposits during in vitro culture of pig oocytes[J].Molecular Reproduction and Development,2001,58(2):196-204
[35] Madgwick S,Jones K T.How eggs arrest at metaphase II:MPF stabilisation plus APC/C inhibition equals cytostatic factor[J].Cell Division,2007,2:4
[36] Whitaker M.Calcium at fertilization and in early development[J].Physiological Reviews,2006,86(1):25-88
[37] Wakai T,Fissore R A.Ca2+homeostasis and regulation of ER Ca2+in mammalian oocytes/eggs[J].Cell Calcium,2013,53(1):63-67
[38] Xu Z,Abbott A,Kopf G S,Schultz R M,Ducibella T.Spontaneous activation of ovulated mouse eggs:Timedependent effects on M-phase exit, cortical granule exocytosis,maternal messenger ribonucleic acid recruitment,and inositol 1,4,5-trisphosphate sensitivity[J].Biology of Reproduction,1997,57(4):743-750
[39] Premkumar K V,Chaube S K.An insufficient increase of cytosolic free calcium level results postovulatory aginginduced abortive spontaneous egg activation in rat[J].Journal of Assisted Reproduction and Genetics,2013,30(1):117-123
[40] Nader N,Kulkarni R P,Dib M,Machaca K.How to make a good egg!:The need for remodeling of oocyte Ca2+signaling to mediate the egg-to-embryo transition[J].Cell Calcium,2013,53(1):41-54
[41] Premkumar K V, Chaube S K. RyR channel-mediated increase of cytosolic free calcium level signals cyclin B1degradation during abortive spontaneous egg activation in rat[J].In Vitro Cellular&Developmental Biology,2014,50(7):640-647
[42] Premkumar K V, Chaube S K. Nitric oxide signals postovulatoryaging-inducedabortivespontaneousegg activation in rats[J].Redox Report:Communications in Free Radical Research,2015,20(4):184-192
[43] Hu H M,Mo X H,Li X,Fu X W,Hou Y P.BAPTA-AM dramatically improves maturation and development of bovine oocytes from grade-3 cumulus-oocyte complexes[J].Molecular Reproduction and Development,2018,85(1):38-45
[44] Orrenius S,Zhivotovsky B,Nicotera P.Regulation of cell death:The calcium-apoptosis link[J].Nature Reviews.Molecular Cell Biology,2003,4(7):552-565
[45] Tripathi A,Chaube S K.High cytosolic free calcium level signals apoptosis through mitochondria-caspase mediated pathway in rat eggs cultured in vitro[J].Apoptosis,2012,17(5):439-448
[46] Ma W,Zhang D,Hou Y,Li Y H,Sun Q Y,Sun X F,Wang W H.Reduced expression of MAD2,BCL2,and MAP kinase activity in pig oocytes after in vitro aging are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation[J].Biology of Reproduction,2005,72(2):373-383
[47] Sergeev I N,Norman A W.Calcium as a mediator of apoptosis in bovine oocytes and preimplantation embryos[J].Endocrine,2003,22(2):169-176
[48] Wang Z G,Wang W,Yu S D,Xu Z R.Effects of different activationprotocolsonpreimplantationdevelopment,apoptosis and ploidy of bovine parthenogenetic embryos[J].Animal Reproduction Science,2008,105(3-4):292-301
[49] Liu L, Trimarchi J R, Keefe D L.Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes[J].Biology of Reproduction,2000,62(6):1745-1753
[50] Zhang N,Fissore R A.Role of caspase-3cleaved IP3 R1on Ca2+homeostasis and developmental competence of mouse oocytes and eggs[J].Journal of Cellular Physiology,2014,229(11):1842-1854
[51] Gordo A C,Rodrigues P,Kurokawa M,Jellerette T,Exley G E,Warner C,Fissore R.Intracellular calcium oscillations signal apoptosis rather than activation in invitroaged mouse eggs[J].Biology of Reproduction,2002,66(6):1828-1837
[52] Chaube S K,Prasad P V,Thakur S C,Shrivastav T G.Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro[J].Apoptosis:An International Journal on Programmed Cell Death,2005,10(4):863-874
[53] Zhu J,Lin F H,Zhang J,Lin J,Li H,Li Y W,Tan X W,Tan J H.The signaling pathways by which the Fas/FasL system accelerates oocyte aging[J].Aging,2016,8(2):291-303
[54] Oh J S,Susor A,Conti M.Protein tyrosine kinase Wee1Bis essential for metaphase II exit in mouse oocytes[J].Science,2011,332(6028):462-465
[55] Kubiak J Z,Ciemerych M A, Hupalowska A,SikoraPolaczek M,Polanski Z.On the transition from the meiotic to mitotic cell cycle during early mouse development[J].The International Journal of Developmental Biology,2008,52(2-3):201-217