Effect of maternal age on mitochondrial DNA copy number, ATP content and IVF outcome of bovine oocytes
Hisataka Iwata A C , Hiroya Goto A , Hiroshi Tanaka A , Yosuke Sakaguchi A , Koji Kimura B , Takehito Kuwayama A and Yashunori Monji A
+ Author Affiliations
- Author Affiliations
A Tokyo University of Agriculture, Funako 1737, Atugi City 243-0034, Japan.
B National Institute of Livestock and Grassland Science, Senbonmatsu 768,Nasushiobara City 329-2793, Japan.
C Corresponding author. Email: h1iwata@nodai.ac.jp
Reproduction, Fertility and Development 23(3) 424-432 https://doi.org/10.1071/RD10133
Submitted: 8 June 2010 Accepted: 15 September 2010 Published: 3 February 2011
Abstract
The primary aim of the present study was to examine the effect of maternal age (in months) on mitochondrial DNA copy number (Mt number), ATP content and IVF outcome of bovine oocytes. We also compared the Mt number of oocytes with fertilisation outcome and ATP content. Oocytes were collected from cows aged 20–204 months and the Mt number was determined by real-time polymerase chain reaction. The Mt number in immature and mature oocytes was determined to be 368 118 and 807 794, respectively; the ATP content in these oocytes was 1.2 and 2.0 pM, respectively. Both Mt number and ATP content increased during oocyte maturation. However, after 90 months of age, the Mt number of mature oocytes decreased with increasing maternal age, whereas the ATP content of mature oocytes was positively correlated with maternal age (P < 0.01); there was no obvious relationship observed between Mt number and ATP content. Furthermore, maternal age was positively correlated with the abnormal fertilisation rate (P < 0.01). Mt number and fertilisation outcome were unrelated, but the nature of this relationship differed between young (21–89 months) and old (>89 months) cows. Thus, we conclude that Mt number, the ATP content and fertilisation outcome of bovine oocytes are affected by maternal age.
Additional keyword: cow.
References
Barritt, J. A., Kokot, M., Cohen, J., Steuerwald, N., and Brenner, C. A. (2002). Quantification of human ooplasmic mitochondria. Reprod. Biomed. Online 4, 243–247.| Quantification of human ooplasmic mitochondria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmt1yjtb8%3D&md5=01ebaf501516f57a9ad2739986400cacCAS | 12709274PubMed |
Bartmann, A. K., Romão, G. S., da Silveira Ramos, E., and Ferriani, R. A. (2004). Why do older women have poor implantation rates? A possible role of the mitochondria. J. Assist. Reprod. Genet. 21, 79–83.
| Why do older women have poor implantation rates? A possible role of the mitochondria.Crossref | GoogleScholarGoogle Scholar | 15202735PubMed |
Brevini, T. A., Vassena, R., Francisci, C., and Gandolfi, F. (2005). Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes. Biol. Reprod. 72, 1218–1223.
| Role of adenosine triphosphate, active mitochondria, and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslSntrc%3D&md5=f1cecc794620246e1a8f6c249a2d0019CAS | 15659704PubMed |
Chiaratti, M. R., and Meirelles, F. V. (2010). Mitochondrial DNA copy number, a marker of viability for oocytes. Biol. Reprod. 83, 1–2.
| Mitochondrial DNA copy number, a marker of viability for oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlWqt7k%3D&md5=fdae31f5a6761c0d5cf0717f868b23f2CAS | 20220127PubMed |
Chiaratti, M. R., Bressan, F. F., Ferreira, C. R., Caetano, A. R., Smith, L. C., Vercesi, A. E., and Meirelles, F. V. (2010). Embryo mitochondrial DNA depletion is reversed during early embryogenesis in cattle. Biol. Reprod. 82, 76–85.
| Embryo mitochondrial DNA depletion is reversed during early embryogenesis in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WgsrrI&md5=3a9cdf42e2a422698a47f280ad8aa48bCAS | 19696017PubMed |
Durocher, J., Morin, N., and Blondin, P. (2006). Effect of hormonal stimulation on bovine follicular response and oocyte developmental competence in a commercial operation. Theriogenology 65, 102–115.
| Effect of hormonal stimulation on bovine follicular response and oocyte developmental competence in a commercial operation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1GitrzK&md5=9d727f1f1740b127c63232a923b578b4CAS | 16269174PubMed |
Ebner, T., Yaman, C., Moser, M., Sommergruber, M., Feichtinger, O., and Tews, G. (2000). Prognostic value of first polar body morphology on fertilization rate and embryo quality in intracytoplasmic sperm injection. Hum. Reprod. 15, 427–430.
| Prognostic value of first polar body morphology on fertilization rate and embryo quality in intracytoplasmic sperm injection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7it1eqsQ%3D%3D&md5=a7117faeb930eaf2114d432d1bf17528CAS | 10655316PubMed |
El Shourbagy, S. H., Spikings, E. C., Freitas, M., and St John, J. C. (2006). Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233–245.
| Mitochondria directly influence fertilisation outcome in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsL4%3D&md5=3d6f1cb076e2a0ee795438c7fa80de81CAS | 16452717PubMed |
Erickson, B. H., Reynolds, R. A., and Murphree, R. L. (1976). Ovarian characteristics and reproductive performance of the aged cow. Biol. Reprod. 15, 555–560.
| Ovarian characteristics and reproductive performance of the aged cow.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s%2Fit1eqsg%3D%3D&md5=8c7000f9c5b239cee88e0e0858b72217CAS | 974208PubMed |
European Society of Human Reproduction and Embryology Capri Workshop Group (2005). Fertility and ageing. Hum. Reprod. Update 11, 261–276.
| Fertility and ageing.Crossref | GoogleScholarGoogle Scholar | 15831503PubMed |
Fernández-Silva, P., Enriquez, J. A., and Montoya, J. (2003). Replication and transcription of mammalian mitochondrial DNA. Exp. Physiol. 88, 41–56.
| Replication and transcription of mammalian mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 12525854PubMed |
Hamatani, T., Falco, G., Carter, M. G., Akutsu, H., Stagg, C. A., Sharov, A. A., Dudekula, D. B., VanBuren, V., and Ko, M. S. (2004). Age-associated alteration of gene expression patterns in mouse oocytes. Hum. Mol. Genet. 13, 2263–2278.
| Age-associated alteration of gene expression patterns in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXns1Onu7k%3D&md5=1fa8258b63ea23ae31113a718fede801CAS | 15317747PubMed |
Jansen, R. P., and Burton, G. J. (2004). Mitochondrial dysfunction in reproduction. Mitochondrion 4, 577–600.
| Mitochondrial dysfunction in reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVCgs7nL&md5=e8d8294ea1bf935683b6ad0e01794a8dCAS | 16120416PubMed |
Jansen, R. P., and de Boer, K. (1998). The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol. Cell. Endocrinol. 145, 81–88.
| The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnt1eitrY%3D&md5=9fd13fc3d1b194f83a280b53dd69e1d1CAS | 9922103PubMed |
Jeng, J. Y., Yeh, T. S., Lee, J. W., Lin, S. H., Fong, T. H., and Hsieh, R. H. (2008). Maintenance of mitochondrial DNA copy number and expression are essential for preservation of mitochondrial function and cell growth. J. Cell. Biochem. 103, 347–357.
| Maintenance of mitochondrial DNA copy number and expression are essential for preservation of mitochondrial function and cell growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFOnsr4%3D&md5=3e70fe251d0c703c15a62b511879748eCAS | 18072287PubMed |
Jiao, F., Yan, J. B., Yang, X. Y., Li, H., Wang, Q., Huang, S. Z., Zeng, F., and Zeng, Y. T. (2007). Effect of oocyte mitochondrial DNA haplotype on bovine somatic cell nuclear transfer efficiency. Mol. Reprod. Dev. 74, 1278–1286.
| Effect of oocyte mitochondrial DNA haplotype on bovine somatic cell nuclear transfer efficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVCmsbfI&md5=5e4d2dcca12ecfcb25c3472c65959208CAS | 17290429PubMed |
Krisher, R. L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, E14–E23.
| 15471793PubMed |
Kujoth, G. C., Hiona, A., Pugh, T. D., Someya, S., Panzer, K., Wohlgemuth, S. E., Hofer, T., Seo, A. Y., Sullivan, R., Jobling, W. A., Morrow, J. D., Van Remmen, H., Sedivy, J. M., Yamasoba, T., Tanokura, M., Weindruch, R., Leeuwenburgh, C., and Prolla, T. A. (2005). Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309, 481–484.
| Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVersb4%3D&md5=d23fbc5e59ca9e4de10bb0655fd5cdb0CAS | 16020738PubMed |
Liu, L., Hammar, K., Smith, P. J., Inoue, S., and Keefe, D. L. (2001). Mitochondrial modulation of calcium signaling at the initiation of development. Cell Calcium 30, 423–433.
| Mitochondrial modulation of calcium signaling at the initiation of development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptlKlurc%3D&md5=ea7c6af618f1d95bbd48f3b1a327c2f5CAS | 11728137PubMed |
Malhi, P. S., Adams, G. P., Mapletoft, R. J., and Singh, J. (2007). Oocyte developmental competence in a bovine model of reproductive aging. Reproduction 134, 233–239.
| Oocyte developmental competence in a bovine model of reproductive aging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKlsrfI&md5=bb61759cdc9729aba44ff4312dadb2b9CAS | 17660233PubMed |
May-Panloup, P., Chretien, M. F., Malthiery, Y., and Reynier, P. (2007). Mitochondrial DNA in the oocyte and the developing embryo. Curr. Top. Dev. Biol. 77, 51–83.
| Mitochondrial DNA in the oocyte and the developing embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmt1Gltbw%3D&md5=b216ce317d5cb3c44701a132aa77c6aaCAS | 17222700PubMed |
Nagano, M., Katagiri, S., and Takahashi, Y. (2006). ATP content and maturational/developmental ability of bovine oocytes with various cytoplasmic morphologies. Zygote 14, 299–304.
| ATP content and maturational/developmental ability of bovine oocytes with various cytoplasmic morphologies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1OntLrP&md5=099b795e1f26877d70c5ce44c8c8e84bCAS | 17266788PubMed |
Piko, L., and Matsumoto, L. (1976). Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev. Biol. 49, 1–10.
| Number of mitochondria and some properties of mitochondrial DNA in the mouse egg.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XhtlWlt7w%3D&md5=91d17fbf7b3e2a7d5f19752e31e3d878CAS | 943339PubMed |
Piko, L., and Taylor, K. D. (1987). Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryo. Dev. Biol. 123, 364–374.
| Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlvFGmtLY%3D&md5=65d57a29a57d03285153817710f76911CAS | 2443405PubMed |
Ramalho-Santos, J., Varum, S., Amaral, S., Mota, P. C., Sousa, A. P., and Amaral, A. (2009). Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum. Reprod. Update 15, 553–572.
| Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVals7nI&md5=a5d21f33a477f66c698315e19999bd83CAS | 19414527PubMed |
Reynier, P., May-Panloup, P., Chrétien, M. F., Morgan, C. J., Jean, M., Savagner, F., Barrière, P., and Malthièry, Y. (2001). Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod. 7, 425–429.
| Mitochondrial DNA content affects the fertilizability of human oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1CqsLg%3D&md5=6a66fd9b86d61c353b97871b74725f33CAS | 11331664PubMed |
Santos, T. A., El Shourbagy, S., and St John, J. C. (2006). Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil. Steril. 85, 584–591.
| Mitochondrial content reflects oocyte variability and fertilization outcome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVChsr0%3D&md5=364200edf9eab8b8af7c9993a88d6eecCAS | 16500323PubMed |
Singh, J., Domínguez, M., Jaiswal, R., and Adams, G. P. (2004). A simple ultrasound test to predict the superstimulatory response in cattle. Theriogenology 62, 227–243.
| A simple ultrasound test to predict the superstimulatory response in cattle.Crossref | GoogleScholarGoogle Scholar | 15159116PubMed |
Smith, L. C., Thundathil, J., and Filion, F. (2005). Role of the mitochondrial genome in preimplantation development and assisted reproductive technologies. Reprod. Fertil. Dev. 17, 15–22.
| Role of the mitochondrial genome in preimplantation development and assisted reproductive technologies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKrurnE&md5=a040ba002c1db2add5fc6197e1f4abe0CAS | 15745628PubMed |
Steuerwald, N., Barritt, J. A., Henry Malter, R. A., Schimmel, T., Cohen, J., and Brenner, C. A. (2000). Quantification of mtDNA in single oocytes, polar bodies and subcellular components by real-time rapid cycle fluorescence monitored PCR. Zygote 8, 209–215.
| Quantification of mtDNA in single oocytes, polar bodies and subcellular components by real-time rapid cycle fluorescence monitored PCR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1OitLs%3D&md5=a684edf82ecff4ac7c6f418e1114c22dCAS | 11014500PubMed |
Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
| Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVKjtrk%3D&md5=1c33fa33a77fabe3ffd8504ad8c8ffc9CAS | 11207207PubMed |
Sun, Q. Y., Wu, G. M., Lai, L., Park, K. W., Cabot, R., Cheong, H. T., Day, B. N., Prather, R. S., and Schatten, H. (2001). Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155–163.
| Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis7g%3D&md5=f3bd0daf3ae7c954ed66960d68b01ed8CAS | 11425340PubMed |
Takahashi, Y., and First, N. L. (1992). In vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acids and vitamins. Theriogenology 37, 963–978.
| In vitro development of bovine one-cell embryos: influence of glucose, lactate, pyruvate, amino acids and vitamins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpvVOmtg%3D%3D&md5=84ea7b1c72559f281a41d47aa18630b1CAS | 16727096PubMed |
Takeuchi, T., Neri, Q. V., Katagiri, Y., Rosenwaks, Z., and Palermo, G. D. (2005). Effect of treating induced mitochondrial damage on embryonic development and epigenesis. Biol. Reprod. 72, 584–592.
| Effect of treating induced mitochondrial damage on embryonic development and epigenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVeis7s%3D&md5=52c3d85b3f5a4e4ef046d98acd8edc34CAS | 15525817PubMed |
Tamassia, M., Nuttinck, F., May-Panloup, P., Reynier, P., Heyman, Y., Charpigny, G., Stojkovic, M., Hiendleder, S., Renard, J. P., and Chastant-Maillard, S. (2004). In vitro embryo production efficiency in cattle and its association with oocyte adenosine triphosphate content, quantity of mitochondrial DNA, and mitochondrial DNA haplogroup. Biol. Reprod. 71, 697–704.
| In vitro embryo production efficiency in cattle and its association with oocyte adenosine triphosphate content, quantity of mitochondrial DNA, and mitochondrial DNA haplogroup.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWgu7c%3D&md5=544b6a56ff8c90c6b5cf01b092e513c7CAS | 15084486PubMed |
Thouas, G. A., Trounson, A. O., Wolvetang, E. J., and Jones, G. M. (2004). Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol. Reprod. 71, 1936–1942.
| Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsr3O&md5=b477d4a0df34fef026cd34f6896432e7CAS | 15286028PubMed |
Van Blerkom, J., and Davis, P. (2007). Mitochondrial signaling and fertilization. Mol. Hum. Reprod. 13, 759–770.
| Mitochondrial signaling and fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqtr3O&md5=3390f8054515df030ad3a0b10f0a01a0CAS | 17893093PubMed |
Van Blerkom, J., Davis, P. W., and Lee, J. (1995). ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum. Reprod. 10, 415–424.
| 1:STN:280:DyaK2M3os1OrtQ%3D%3D&md5=6f1c7b0141f286ad15ff0c55290f462fCAS | 7769073PubMed |
Wai, T., Ao, A., Zhang, X., Dufort, D., and Shoubridge, E. A. (2010). The role of mitochondrial DNA copy number in mammalian fertility. Biol. Reprod. 83, 52–62.
| The role of mitochondrial DNA copy number in mammalian fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlWqtLo%3D&md5=7f23944687763eb106261421a74db20fCAS | 20130269PubMed |
Wang, Q., and Moley, K. H. (2010). Maternal diabetes and oocyte quality. Mitochondrion. 10, 403–410.
| 20226883PubMed |
Wang, L. Y., Wang, D. H., Zou, X. Y., and Xu, C. M. (2009a). Mitochondrial functions on oocytes and preimplantation embryos. J. Zhejiang Univ. Sci. B 10, 483–492.
| Mitochondrial functions on oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotV2qtbo%3D&md5=bd3f6b7e90909fe3e36b7bb522553013CAS | 19585665PubMed |
Wang, Q., Ratchford, A. M., Chi, M. M., Schoeller, E., Frolova, A., Schedl, T., and Moley, K. H. (2009b). Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes. Mol. Endocrinol. 23, 1603–1612.
| Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSitb%2FF&md5=1d0419b67598fe77e43240fd6548fc9aCAS | 19574447PubMed |
Wilding, M., Dale, B., Marino, M., di Matteo, L., Alviggi, C., Pisaturo, M. L., Lombardi, L., and De Placido, G. (2001). Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum. Reprod. 16, 909–917.
| Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvitlCktw%3D%3D&md5=b85d4154f0af9cc86b9b720a1bc5f55dCAS | 11331637PubMed |
Yamamoto, T., Iwata, H., Goto, H., Shiratuki, S., Tanaka, H., Monji, Y., and Kuwayama, T. (2010). Effect of maternal age on the developmental competence and progression of nuclear maturation in bovine oocytes. Mol. Reprod. Dev. 77, 595–604.
| Effect of maternal age on the developmental competence and progression of nuclear maturation in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVahsL0%3D&md5=0c27eb7e5c87452275a85c6b864b2701CAS | 20575084PubMed |
Yu, Y., Dumollard, R., Rossbach, A., Lai, F. A., and Swann, K. (2010). Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J. Cell. Physiol. 224, 672–680.
| Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosVWntLo%3D&md5=72478d66035798e59f7b77cef72d83afCAS | 20578238PubMed |
Zeng, H. T., Yeung, W. S., Cheung, M. P., Ho, P. C., Lee, C. K., Zhuang, G. L., Liang, X. Y., and O, W. S. (2009). In vitro-matured rat oocytes have low mitochondrial deoxyribonucleic acid and adenosine triphosphate contents and have abnormal mitochondrial redistribution. Fertil. Steril. 91, 900–907.
| In vitro-matured rat oocytes have low mitochondrial deoxyribonucleic acid and adenosine triphosphate contents and have abnormal mitochondrial redistribution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnslWmsb4%3D&md5=904e0b5dfbbe4522110deae9ce08cabeCAS | 18321496PubMed |
Zhang, X., Wu, X. Q., Lu, S., Guo, Y. L., and Ma, X. (2006). Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res. 16, 841–850.
| Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOmu7fF&md5=67f520f02e547e63c71931641184ace4CAS | 16983401PubMed |
