Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Reproductive competency and mitochondrial variation in aged Syrian hamster oocytes

Fang Li A D , Frank J. Castora B G , Wentia Ford A F , Khalid Alarid A , Howard W. Jones Jr C and R. James Swanson A E
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, Old Dominion University, 5115 Hampton Blvd, Norfolk, VA 23529, USA.

B Department of Physiological Sciences, Eastern Virginia Medical School, 721 Fairfax Ave, Norfolk, VA 23507, USA.

C The Jones Institute for Reproductive Medicine, Eastern Virginia Medical School, 601 Colley Ave, Norfolk, VA 23507, USA.

D Present address: Laboratory of Embryology, IVF Michigan, 37000 Woodward Ave, Ste 350, Bloomfield Hills, MI 48304, USA.

E Present address: Department of Anatomical Sciences, College of Osteopathic Medicine, Liberty University, 306 Liberty View Lane, Lynchburg, VA 24502, USA.

F Present address: 5010 Juno Court Edinburg, TX 78539, USA.

G Corresponding author. Email: castorfj@evms.edu

Reproduction, Fertility and Development 29(7) 1384-1391 https://doi.org/10.1071/RD15404
Submitted: 8 October 2015  Accepted: 9 May 2016   Published: 22 June 2016

Abstract

The hamster is a useful model of human reproductive biology because its oocytes are similar to those in humans in terms of size and structural stability. In the present study we evaluated fecundity rate, ovarian follicular numbers, ova production, mitochondrial number, structure and function, and cytoplasmic lamellae (CL) in young (2–4 months) and old (12–18 months) Syrian hamsters (Mesocricetus auratus). Young hamsters had higher fertilisation rates and larger litters than old hamsters (100 vs 50% and 9.3 ± 0.6 vs 5.5 ± 0.6, respectively). Ovarian tissue from superovulated animals showed a 46% decrease in preantral follicles in old versus young hamsters. There was a 39% reduction in MII oocyte number in old versus young hamsters. Young ova had no collapsed CL, whereas old ova were replete with areas of collapsed, non-luminal CL. Eighty-nine per cent of young ova were expanded against the zona pellucida with a clear indentation at the polar body, compared with 58.64% for old ova; the remaining old ova had increased perivitelline space with no polar body indentation. Higher reactive oxygen species levels and lower mitochondrial membrane potentials were seen in ova from old versus young hamsters. A significant decrease in mitochondrial number (36%) and lower frequency of clear mitochondria (31%) were observed in MII oocytes from old versus young hamster. In conclusion, the results of the present study support the theory of oocyte depletion during mammalian aging, and suggest that morphological changes of mitochondria and CL in oocytes may be contributing factors in the age-related decline in fertility rates.

Additional keywords: aging, lamellae, mitochondria, organelle structure, reactive oxygen species (ROS).


References

Alviggi, C., Humaidan, P., Howles, C. M., Tredway, D., and Hillier, S. G. (2009). Biological versus chronological ovarian age: implications for assisted reproductive technology. Reprod. Biol. Endocrinol. 7, 101.
Biological versus chronological ovarian age: implications for assisted reproductive technology.CrossRef | 19772632PubMed |

Araújo, V. R., Gastal, M. O., Figueiredo, J. R., and Gastal, E. L. (2014). In vitro culture of bovine preantral follicles: a review. Reprod. Biol. Endocrinol. 12, 78–91.
In vitro culture of bovine preantral follicles: a review.CrossRef | 25117631PubMed |

Båge, R., Petyim, S., Larsson, B., Hallap, T., Bergqvist, A. S., Gustafsson, H., and Rodriguez-Martinez, H. (2003). Oocyte competence in repeat-breeder heifers: effects of an optimized ovum pick-up schedule on expression of oestrus, follicular development and fertility. Reprod. Fertil. Dev. 15, 115–123.
Oocyte competence in repeat-breeder heifers: effects of an optimized ovum pick-up schedule on expression of oestrus, follicular development and fertility.CrossRef | 12895408PubMed |

Banno, T., and Kohno, K. (1996). Conformational changes of smooth endoplasmic reticulum induced by brief anoxia in rat Purkinje cells. J. Comp. Neurol. 369, 462–471.
Conformational changes of smooth endoplasmic reticulum induced by brief anoxia in rat Purkinje cells.CrossRef | 1:STN:280:DyaK28zjs1Gjug%3D%3D&md5=f38680d4dda326bfbad661350d293202CAS | 8743425PubMed |

Bellanti, F., Romano, A. D., Giudetti, A. M., Rollo, T., Blonda, M., Tamborra, R., Vendemiale, G., and Serviddio, G. (2013). Many faces of mitochondrial uncoupling during age: damage or defense? J. Gerontol. A Biol. Sci. Med. Sci. 68, 892–902.
Many faces of mitochondrial uncoupling during age: damage or defense?CrossRef | 1:CAS:528:DC%2BC3sXhtFOgt7fO&md5=875a9da0644daefde1130cb8a3eaa5ffCAS | 23292290PubMed |

Bianchi, S., Macchiarelli, G., Micara, G., Linari, A., Boninsegna, C., Aragona, C., Rossi, G., Cecconi, S., and Nottola, S. A. (2015). Ultrastructural markers of quality are impaired in human metaphase II aged oocytes: a comparison between reproductive and in vitro aging. J. Assist. Reprod. Genet. 32, 1343–1358.
Ultrastructural markers of quality are impaired in human metaphase II aged oocytes: a comparison between reproductive and in vitro aging.CrossRef | 1:STN:280:DC%2BC287jtFKksw%3D%3D&md5=d4cc167912a65fe22c9d48759fb85e27CAS | 26276431PubMed |

Boren, J., and Brindle, K. M. (2012). Apoptosis-induced mitochondrial dysfunction causes cytoplasmic lipid droplet formation. Cell Death Differ. 19, 1561–1570.
Apoptosis-induced mitochondrial dysfunction causes cytoplasmic lipid droplet formation.CrossRef | 1:CAS:528:DC%2BC38Xht1WltbzO&md5=53896ecf14cd01299cacb031fa77ed0bCAS | 22460322PubMed |

Britton, A. P., Moon, Y. S., and Yuen, B. H. (1991). A simple handling technique for mammalian oocytes and embryos during preparation for transmission electron microscopy. J. Microsc. 161, 497–499.
A simple handling technique for mammalian oocytes and embryos during preparation for transmission electron microscopy.CrossRef | 1:STN:280:DyaK3M3lvFGrtg%3D%3D&md5=942f2f49d41fb1c568f3470e1ad58982CAS | 1904499PubMed |

Brookes, P. S. (2005). Mitochondrial H(+) leak and ROS generation: an odd couple. Free Radic. Biol. Med. 38, 12–23.
Mitochondrial H(+) leak and ROS generation: an odd couple.CrossRef | 1:CAS:528:DC%2BD2cXhtVKrt7fK&md5=f96d6ef23fc140304a64f74a7194a5aeCAS | 15589367PubMed |

Bunn, H. F., and Poyton, R. O. (1996). Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 76, 839–885.
| 1:CAS:528:DyaK28XltVags70%3D&md5=2babd5d724004ac78ffde6046f77f99aCAS | 8757790PubMed |

David, J., Cohet, Y., and Foluillet, P. (1975). The variability between individuals as a measure of senescence: a study of the number of eggs laid and the percentage of hatched eggs in the case of Drosophila melanogaster. Exp. Gerontol. 10, 17–25.
The variability between individuals as a measure of senescence: a study of the number of eggs laid and the percentage of hatched eggs in the case of Drosophila melanogaster.CrossRef | 1:STN:280:DyaE2M7mvVShtg%3D%3D&md5=b0e2ad4899a499990319ec8ec4e6ba78CAS | 805709PubMed |

de Bruin, J. P., Dorland, M., Spek, E. R., Posthuma, G., van Haaften, M., Looman, C. W., and te Velde, E. R. (2004). Age-related changes in the ultrastructure of the resting follicle pool in human ovaries. Biol. Reprod. 70, 419–424.
Age-related changes in the ultrastructure of the resting follicle pool in human ovaries.CrossRef | 1:CAS:528:DC%2BD2cXnsl2jsQ%3D%3D&md5=fe8bfa3f9f9b39ef5185a1966c0a6d25CAS | 14561658PubMed |

Ducibella, T., Duffy, P., Reindollar, R., and Su, B. (1990). Changes in the distribution of mouse oocyte cortical granules and ability to undergo the cortical reaction during gonadotropin-stimulated meiotic maturation and aging in vivo. Biol. Reprod. 43, 870–876.
Changes in the distribution of mouse oocyte cortical granules and ability to undergo the cortical reaction during gonadotropin-stimulated meiotic maturation and aging in vivo.CrossRef | 1:CAS:528:DyaK3cXmt1Clu78%3D&md5=04080591508f93ef827f7ee52b1b6446CAS | 2291919PubMed |

Duicu, O. M., Mirica, S. N., Gheorgheosu, D. E., Privistirescu, A. I., Fira-Mladinescu, O., and Muntean, D. M. (2013). Ageing-induced decrease in cardiac mitochondrial function in healthy rats. Can. J. Physiol. Pharmacol. 91, 593–600.
Ageing-induced decrease in cardiac mitochondrial function in healthy rats.CrossRef | 1:CAS:528:DC%2BC3sXhtFSqtrnO&md5=328c92b3fd24371cd9242a124cff64c4CAS | 23889593PubMed |

Elizur, S. E., Lebovitz, O., Orvieto, R., Dor, J., and Zan-Bar, T. (2014). Reactive oxygen species in follicular fluid may serve as biochemical markers to determine ovarian aging and follicular metabolic age. Gynecol. Endocrinol. 30, 705–707.
Reactive oxygen species in follicular fluid may serve as biochemical markers to determine ovarian aging and follicular metabolic age.CrossRef | 1:CAS:528:DC%2BC2cXhs1eis7jP&md5=edf58b1d8fbad588c939651a3cf91afaCAS | 25014488PubMed |

Fox, J. G. (1985). Laboratory animal medicine. Changes and challenges. Cornell Vet. 75, 159–170.
| 1:STN:280:DyaL2M7ltlaqtg%3D%3D&md5=f67d7837e7d20c288fe2e09d46114dd1CAS | 3884262PubMed |

Giesel, J. T. (1979). Associations between age specific mortality and fecundity rates in mammals. Exp. Gerontol. 14, 189–192.
Associations between age specific mortality and fecundity rates in mammals.CrossRef | 1:STN:280:DyaL3c%2FgtlOqsA%3D%3D&md5=0886777d240c09b08facc91bcb6a8667CAS | 477762PubMed |

Graham, J., Ford, T., and Rickwood, D. (1994). The preparation of subcellular organelles from mouse liver in self-generated gradients of iodixanol. Anal. Biochem. 220, 367–373.
The preparation of subcellular organelles from mouse liver in self-generated gradients of iodixanol.CrossRef | 1:CAS:528:DyaK2cXlt12iur8%3D&md5=d302008f565906a0efdd0819bff75ebdCAS | 7978280PubMed |

Griffin, J., Emery, B. R., Huang, I., Peterson, C. M., and Carrell, D. T. (2006). Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human). J. Exp. Clin. Assist. Reprod. 3, 2.
Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human).CrossRef | 16509981PubMed |

Hendry, W. J., Sheehan, D. M., Khan, S. A., and May, J. V. (2002). Developing a laboratory animal model for perinatal endocrine disruption: the hamster chronicles. Exp. Biol. Med. (Maywood) 227, 709–723.
| 1:CAS:528:DC%2BD38XntlyqsLs%3D&md5=34f67ab680c7478b50012d64cdee74c5CAS | 12324652PubMed |

Ishida, A., Mashima, H., and Tanaka, S. (1979). Intracellular distribution of calcium in cardiac muscles studied by electron microscope autoradiography. Jpn. J. Physiol. 29, 37–48.
Intracellular distribution of calcium in cardiac muscles studied by electron microscope autoradiography.CrossRef | 1:CAS:528:DyaE1MXitVWmsr0%3D&md5=4a9f70749673a1b1e91d5f6cc921e931CAS | 449121PubMed |

Jansen, R. P., and Burton, G. J. (2004). Mitochondrial dysfunction in reproduction. Mitochondrion 4, 577–600.
Mitochondrial dysfunction in reproduction.CrossRef | 1:CAS:528:DC%2BD2cXhtVCgs7nL&md5=0507fb9faa12b04cc1aecce27a56d62bCAS | 16120416PubMed |

Klamt, F., and Shacter, E. (2005). Taurine chloramine, an oxidant derived from neutrophils, induces apoptosis in human B lymphoma cells through mitochondrial damage. J. Biol. Chem. 280, 21 346–21 352.
Taurine chloramine, an oxidant derived from neutrophils, induces apoptosis in human B lymphoma cells through mitochondrial damage.CrossRef | 1:CAS:528:DC%2BD2MXks1elsLc%3D&md5=897aaebdce1e1c8fefa8bebd0ecc5156CAS |

Kweon, S. M., Kim, H. J., Lee, Z. W., Kim, S. J., Kim, S. I., Paik, S. G., and Ha, K. S. (2001). Real-time measurement of intracellular reactive oxygen species using Mito tracker orange (CMH2TMRos). Biosci. Rep. 21, 341–352.
Real-time measurement of intracellular reactive oxygen species using Mito tracker orange (CMH2TMRos).CrossRef | 1:CAS:528:DC%2BD38XitFSmtb8%3D&md5=8e566ba8454997ec6a57dfa2732c5a09CAS | 11893000PubMed |

Lee, H. C., and Wei, Y. H. (2012). Mitochondria and aging. Adv. Exp. Med. Biol. 942, 311–327.
Mitochondria and aging.CrossRef | 1:CAS:528:DC%2BC38Xhs1GltrzF&md5=70695db66aada8e737330ed8899e1e5eCAS | 22399429PubMed |

Mizoguchi, H., and Dukelow, W. R. (1981). Fertilizability of ova from young or old hamsters after spontaneous or induced ovulation. Fertil. Steril. 35, 79–83.
Fertilizability of ova from young or old hamsters after spontaneous or induced ovulation.CrossRef | 1:STN:280:DyaL3M7hsVOgsw%3D%3D&md5=86beb87e3ad6a0c0e4f9fcedf57a9831CAS | 7461158PubMed |

Motta, P. M., Nottola, S. A., Makabe, S., and Heyn, R. (2000). Mitochondrial morphology in human fetal and adult female germ cells. Hum. Reprod. 15, 129–147.
Mitochondrial morphology in human fetal and adult female germ cells.CrossRef | 11041520PubMed |

Nagai, S., Mabuchi, T., Hirata, S., Shoda, T., Kasai, T., Yokota, S., Shitara, H., Yonekawa, H., and Hoshi, K. (2006). Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence. Tohoku J. Exp. Med. 210, 137–144.
Correlation of abnormal mitochondrial distribution in mouse oocytes with reduced developmental competence.CrossRef | 1:CAS:528:DC%2BD28XhtF2rtbjN&md5=c909d859f69b0bd641974cd3f749ed06CAS | 17023767PubMed |

National Academy of Science (1996) ‘Guide for care and use of laboratory animals.’ Available at http://www.nap.edu/catalog/5140/guide-for-the-care-and-use-of-laboratory-animals [Verified 23 May 2016]

Park, E. S., Gao, X., Chung, J. M., and Chung, K. (2006). Levels of mitochondrial reactive oxygen species increase in rat neuropathic spinal dorsal horn neurons. Neurosci. Lett. 391, 108–111.
Levels of mitochondrial reactive oxygen species increase in rat neuropathic spinal dorsal horn neurons.CrossRef | 1:CAS:528:DC%2BD2MXht1OksrvJ&md5=f22ff87c7c31d5138d3c005ea0f71080CAS | 16183198PubMed |

Parkening, T. A., Collins, T. J., Lau, I. F., and Saksena, S. K. (1982). The pituitary–ovarian complex in the aged anoestrous golden hamster. J. Reprod. Fertil. 64, 37–46.
The pituitary–ovarian complex in the aged anoestrous golden hamster.CrossRef | 1:CAS:528:DyaL38XotVahtQ%3D%3D&md5=bacd267201c3f49f08a0b834700b4d74CAS | 7198689PubMed |

Pozzan, T., Magalhaes, P., and Rizzuto, R. (2000). The comeback of mitochondria to calcium signalling. Cell Calcium 28, 279–283.
The comeback of mitochondria to calcium signalling.CrossRef | 1:CAS:528:DC%2BD3MXlvFOgtg%3D%3D&md5=8519770c8e8e9fae7e6aee7b4888de03CAS | 11115367PubMed |

Quintero, M., Colombo, S. L., Godfrey, A., and Moncada, S. (2006). Mitochondria as signaling organelles in the vascular endothelium. Proc. Natl Acad. Sci. USA 103, 5379–5384.
Mitochondria as signaling organelles in the vascular endothelium.CrossRef | 1:CAS:528:DC%2BD28Xjslaqu74%3D&md5=916483455a0d86a9f6a61c9698629a51CAS | 16565215PubMed |

Reynier, P., May-Panloup, P., Chretien, M. F., Morgan, C. J., Jean, M., Savagner, F., Barriere, P., and Malthiery, 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 | 1:CAS:528:DC%2BD3MXkt1CqsLg%3D&md5=c642f727f1d8648d3f2d266efdab37caCAS | 11331664PubMed |

Rienzi, L., Ubaldi, F. M., Iacobelli, M., Minasi, M. G., Romano, S., Ferrero, S., Sapienza, F., Baroni, E., Litwicka, K., and Greco, E. (2008). Significance of metaphase II human oocyte morphology on ICSI outcome. Fertil. Steril. 90, 1692–1700.
Significance of metaphase II human oocyte morphology on ICSI outcome.CrossRef | 18249393PubMed |

Roy, M. K., Thalang, V. N., Trakoontivakorn, G., and Nakahara, K. (2004). Mechanism of mahanine-induced apoptosis in human leukemia cells (HL-60). Biochem. Pharmacol. 67, 41–51.
Mechanism of mahanine-induced apoptosis in human leukemia cells (HL-60).CrossRef | 1:CAS:528:DC%2BD3sXps1Oksbs%3D&md5=e263c5c4985248291e8a8d4719519f6dCAS | 14667927PubMed |

Sathananthan, A. H. (1997). Ultrastructure of the human egg. Hum. Cell 10, 21–38.
| 1:STN:280:DyaK2sznvVCnsQ%3D%3D&md5=8a9eb786282ad54684db3c6ae5402341CAS | 9234062PubMed |

Simsek-Duran, F., Li, F., Ford, W., Swanson, R. J., Jones, H. W., and Castora, F. J. (2013). Age-associated metabolic and morphologic changes in mitochondria of individual mouse and hamster oocytes. PLoS One 8, e64955.
Age-associated metabolic and morphologic changes in mitochondria of individual mouse and hamster oocytes.CrossRef | 1:CAS:528:DC%2BC3sXpslOnsb8%3D&md5=8a8b01ee43601a32c019c1fe66d277cdCAS | 23741435PubMed |

Speakman, J. R., Talbot, D. A., Selman, C., Snart, S., McLaren, J. S., Redman, P., Krol, E., Jackson, D. M., Johnson, M. S., and Brand, M. D. (2004). Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3, 87–95.
Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer.CrossRef | 1:CAS:528:DC%2BD2cXkvFOktL8%3D&md5=dad225c2e8e0a61b3dc704f62cf5e0cfCAS | 15153176PubMed |

Tang, D. W., Fang, Y., Liu, Z. X., Wu, Y., Wang, X. L., Zhao, S., Han, G. C., and Zeng, S. M. (2013). The disturbances of endoplasmic reticulum calcium homeostasis caused by increased intracellular reactive oxygen species contributes to fragmentation in aged porcine oocytes. Biol. Reprod. 89, 124.
The disturbances of endoplasmic reticulum calcium homeostasis caused by increased intracellular reactive oxygen species contributes to fragmentation in aged porcine oocytes.CrossRef | 24089204PubMed |

Tatone, C., Di Emidio, G., Barbaro, R., Vento, M., Ciriminna, R., and Artini, P. G. (2011). Effects of reproductive aging and postovulatory aging on the maintenance of biological competence after oocyte vitrification: insights from the mouse model. Theriogenology 76, 864–873.
Effects of reproductive aging and postovulatory aging on the maintenance of biological competence after oocyte vitrification: insights from the mouse model.CrossRef | 21705053PubMed |

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 | 1:CAS:528:DC%2BD2cXhtVWgsr3O&md5=b0e71189515ac685532ab662885d968eCAS | 15286028PubMed |

Van Blerkom, J. (2008). Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells. Reprod. Biomed. Online 16, 553–569.
Mitochondria as regulatory forces in oocytes, preimplantation embryos and stem cells.CrossRef | 18413065PubMed |

Van Blerkom, J. (2011). Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion 11, 797–813.
Mitochondrial function in the human oocyte and embryo and their role in developmental competence.CrossRef | 1:CAS:528:DC%2BC3MXhtVWrsrzM&md5=e79f56d1afcd71cadf1251b829ae64aaCAS | 20933103PubMed |

Van Blerkom, J., Davis, P., Mathwig, V., and Alexander, S. (2002). Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos. Hum. Reprod. 17, 393–406.
Domains of high-polarized and low-polarized mitochondria may occur in mouse and human oocytes and early embryos.CrossRef | 11821285PubMed |

Weakley, B. S. (1976). Variations in mitochondrial size and ultrastructure during germ cell development. Cell Tissue Res. 169, 531–550.
Variations in mitochondrial size and ultrastructure during germ cell development.CrossRef | 1:STN:280:DyaE2s%2FkslSntg%3D%3D&md5=91bd68c05c0e92fda989db40dbb9eb0aCAS | 991199PubMed |

Weakley, B. S., and James, J. L. (1982). Differentiation of endoplasmic reticulum in the developing oocyte of the golden hamster (Mesocricetus auratus). Cell Tissue Res. 223, 127–139.
Differentiation of endoplasmic reticulum in the developing oocyte of the golden hamster (Mesocricetus auratus).CrossRef | 1:STN:280:DyaL387mt1Kktg%3D%3D&md5=32fbf17922e5ffa33495fae6b2dce574CAS | 6175423PubMed |

Weibel, E. R., Kistler, G. S., and Scherle, W. F. (1966). Practical stereological methods for morphometric cytology. J. Cell Biol. 30, 23–38.
Practical stereological methods for morphometric cytology.CrossRef | 1:STN:280:DyaF2s7msFersg%3D%3D&md5=9083c08ebe7a7e9c686f88112d8856b4CAS | 5338131PubMed |

Xia, P. (1997). Intracytoplasmic sperm injection: correlation of oocyte grade based on polar body, perivitelline space and cytoplasmic inclusions with fertilization rate and embryo quality. Hum. Reprod. 12, 1750–1755.
Intracytoplasmic sperm injection: correlation of oocyte grade based on polar body, perivitelline space and cytoplasmic inclusions with fertilization rate and embryo quality.CrossRef | 1:STN:280:DyaK2svlt1eqsA%3D%3D&md5=410db90dab0f28544ad90978d75d5177CAS | 9308806PubMed |

Yamauchi, Y., Yanagimachi, R., and Horiuchi, T. (2002). Full-term development of golden hamster oocytes following intracytoplasmic sperm head injection. Biol. Reprod. 67, 534–539.
Full-term development of golden hamster oocytes following intracytoplasmic sperm head injection.CrossRef | 1:CAS:528:DC%2BD38XlsFKqtLw%3D&md5=11b1248c63eef119e498aa17bb507b02CAS | 12135892PubMed |

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 | 1:CAS:528:DC%2BD1MXnslWmsb4%3D&md5=366b6af8c6007f0d5dfd5eef84c45072CAS | 18321496PubMed |



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