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

Gene expression profile differences in embryos derived from prepubertal and adult Japanese Black cattle during in vitro development

Dorji A , Yukihiro Ohkubo B , Kazuchika Miyoshi A and Mitsutoshi Yoshida A C
+ Author Affiliations
- Author Affiliations

A Laboratory of Animal Reproduction, United Graduate School of Agricultural Science, Kagoshima University, Korimoto 1-21-24, Kagoshima 890-0065, Japan.

B Nippon Zenyaku Kogyo Co., Ltd, Koriyama, Fukushima 963-0196, Japan.

C Corresponding author. Email: myoshida@ms.kagoshima-u.ac.jp

Reproduction, Fertility and Development 24(2) 370-381 https://doi.org/10.1071/RD11048
Submitted: 17 February 2011  Accepted: 3 June 2011   Published: 4 November 2011

Abstract

The present study was carried out to compare the gene expression profiles of in vitro-generated embryos derived from adult and prepubertal Japanese Black cattle oocytes using GeneChip Bovine Genome Array (containing 24 072 probe sets representing over 23 000 transcripts). Microarray experiments were performed on populations of 8- to 16-cell stage embryos and blastocysts derived from adult (24–35 months old) versus prepubertal (9–10 months old) Japanese Black cattle oocytes matured and fertilised in vitro. In total, 591 (2.4%) and 490 (2.0%) genes were differentially expressed in prepubertal and adult bovine in 8- to 16-cell and blastocyst stage embryos, respectively. Out of these, 218 and 248 genes were upregulated, while 373 and 242 were downregulated in prepubertal and adult 8- to 16-cell and blastocysts stage embryos, respectively. Gene ontology classification regarding biological process, molecular functions and cellular component revealed diversity in transcript abundances between prepubertal and adult groups in both the distinct developmental stages. Quantitative reverse transcription–PCR validated the expression differences of some selected transcripts as identified by microarray analysis. To our knowledge, this is the first report indicating the significant number of genes differentially expression (>2-fold, P < 0.01) in preimplantition embryos between adult and prepubertal Japanese Black cattle during in vitro development.

Additional keywords: bovine, developmental competence.


References

Adashi, E. Y., Resnick, C. E., D’Ercole, A. J., Svoboda, M. E., and Van Wyk, J. J. (1985). Insulin-like growth factors as intraovarian regulators of granulosa cell growth and function. Endocr. Rev. 6, 400–420.
Insulin-like growth factors as intraovarian regulators of granulosa cell growth and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlvV2qsbo%3D&md5=cf7806b141a273f2e528faf65c1c54ddCAS | 2992919PubMed |

Archipong, A. E., England, D. C., and Stormshak, F. (1987). Factors contributing to early embryonic mortality in gilts bred at first estrus. J. Anim. Sci. 64, 474–478.

Armstrong, D. T. (2001). Effects of maternal age on oocyte developmental competence. Theriogenology 55, 1303–1322.
Effects of maternal age on oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSis78%3D&md5=670e6e53fa96bcf3302f646d79c18e2dCAS | 11327686PubMed |

Armstrong, D. T., Kotaras, P. J., and Earl, C. R. (1997). Advances in production of embryos in vitro from juvenile and prepubertal oocytes from the calf and lamb. Reprod. Fertil. Dev. 9, 333–339.
Advances in production of embryos in vitro from juvenile and prepubertal oocytes from the calf and lamb.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svgsFaisw%3D%3D&md5=dde49fcbc6c069ce5c22b1780c7df195CAS | 9261881PubMed |

Bettegowda, A., Patel, O. V., Ireland, J. J., and Smith, G. W. (2006). Quantitative analysis of messenger RNA abundance for ribosomal protein L-15, cyclophilin-A, phosphoglycerokinase, beta-glucuronidase, glyceraldehyde 3-phosphate dehydrogenase, beta-actin, and histone H2A during bovine oocyte maturation and early embryogenesis in vitro. Mol. Reprod. Dev. 73, 267–278.
Quantitative analysis of messenger RNA abundance for ribosomal protein L-15, cyclophilin-A, phosphoglycerokinase, beta-glucuronidase, glyceraldehyde 3-phosphate dehydrogenase, beta-actin, and histone H2A during bovine oocyte maturation and early embryogenesis in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsVKht78%3D&md5=5066fa68a0c1d23c4f0f9cd097cc87d9CAS | 16261607PubMed |

Brackett, B. G., and Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–274.
Capacitation of rabbit spermatozoa in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28Xnt1WltQ%3D%3D&md5=51c4d5f0dde1ab549aba305b3a2fce83CAS | 1122333PubMed |

Breitling, R., Armengaud, P., Amtmann, A., and Herzyk, P. (2004). Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett. 573, 83–92.
Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFyrtr4%3D&md5=02b79ae3b8f1baf19c2c38be87e97a7aCAS | 15327980PubMed |

Brevini-Gandolfi, T., Favetta, L. A., Lonergan, P., and Gandolfi, F. (2000). The mechanism regulating maternal mRNA stability and translation is affected in bovine embryos with low developmental competence. Theriogenology 53, 268.

Candenas, L., Lecci, A., Pinto, F. M., Patak, E., Maggi, C. A., and Pennefather, J. N. (2005). Tachykinins and tachykinin receptors: effects in the genitourinary tract. Life Sci. 76, 835–862.
Tachykinins and tachykinin receptors: effects in the genitourinary tract.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKktrjN&md5=1a11f945452c1cd1e7e1df0b20f63e5cCAS | 15589963PubMed |

Corcoran, D., Fair, T., Park, S., Rizos, D., Patel, O. V., Smith, G. W., Coussens, P. M., Ireland, J. J., Boland, M. P., Evans, A. C. O., and Lonergan, P. (2006). Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos. Reproduction 131, 651–660.
Suppressed expression of genes involved in transcription and translation in in vitro compared with in vivo cultured bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltV2jtr8%3D&md5=12547053da663fc3011fff6759af19abCAS | 16595716PubMed |

Cui, X. S., Song, H., and Kim, N. H. (2005). Identification of metaphase II-specific gene transcripts in porcine oocytes and their expression in early stage embryos. Reprod. Fertil. Dev. 17, 625–631.
Identification of metaphase II-specific gene transcripts in porcine oocytes and their expression in early stage embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXms1yhtL0%3D&md5=c08f5c1d588fdb9831ff55d19c3377d6CAS | 16263068PubMed |

Cui, X. S., Li, X. Y., Jeong, Y. J., Jun, J. H., and Kim, N. H. (2006). Gene expression of cox5a, 5b or 6b1 and their roles in preimplantation mouse embryos. Biol. Reprod. 74, 601–610.
Gene expression of cox5a, 5b or 6b1 and their roles in preimplantation mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhslejsLY%3D&md5=80d9cfb716b0f84eb6e496b6669c94b4CAS | 16291927PubMed |

Cui, X. S., Li, X. Y., Yin, X. J., Kong, I. K., Kang, J. J., and Kim, N. H. (2007). Maternal gene transcription in mouse oocytes: genes implicated in oocyte maturation and fertilization. J. Reprod. Dev. 53, 405–418.
Maternal gene transcription in mouse oocytes: genes implicated in oocyte maturation and fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlslOjsbs%3D&md5=baa194546b7431a48f0828e015e6bb03CAS | 17179655PubMed |

Dalbiès-Tran, R., and Mermillod, P. (2003). Use of heterologous complementary DNA array screening to analyze bovine oocyte transcriptome and its evolution during in vitro maturation. Biol. Reprod. 68, 252–261.
Use of heterologous complementary DNA array screening to analyze bovine oocyte transcriptome and its evolution during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 12493721PubMed |

Damiani, P., Fissore, R. A., Cibelli, J. B., Long, C. R., Balise, J. J., Robl, J. M., and Duby, R. T. (1996). Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes. Mol. Reprod. Dev. 45, 521–534.
Evaluation of developmental competence, nuclear and ooplasmic maturation of calf oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsVWgt7k%3D&md5=5df64c298be4f991e289903c9d9173ceCAS | 8956291PubMed |

Do, H. J., Kim, J. H., Abeydeera, L. R., Han, Y. M., Green, J., Roberts, R. M., Matteri, R. L., Day, B. N., and Prather, R. S. (2001). Expression of pregnancy-associated glycoprotein 1 and 2 genes in in vitro-, in vivo- and parthenogenetically-derived preimplantation pig embryos. Zygote 9, 245–250.
Expression of pregnancy-associated glycoprotein 1 and 2 genes in in vitro-, in vivo- and parthenogenetically-derived preimplantation pig embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmsVOltbc%3D&md5=d0d98b25515d18d13afc7d15672466a9CAS | 11508744PubMed |

Donnison, M., and Pfeffer, P. L. (2004). Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development. Biol. Reprod. 71, 1813–1821.
Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWgsr%2FL&md5=33790237928b3de3427b513302a936d5CAS | 15286031PubMed |

Duby, R. T., Damiani, P., Looney, R., Long, C. R., Balise, J. J., and Roble, J. M. (1995). Cytological characterization of maturation and fertilization in prepubertal calf oocytes. Theriogenology 43, 202.
Cytological characterization of maturation and fertilization in prepubertal calf oocytes.Crossref | GoogleScholarGoogle Scholar |

Duranthon, V. S., and Renard, J. P. (2001). The developmental competence of mammalian oocytes: a convenient but biologically fuzzy concept. Theriogenology 55, 1277–1289.
The developmental competence of mammalian oocytes: a convenient but biologically fuzzy concept.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSisrk%3D&md5=06e6fb4e672ec759a8f7d84bd1017814CAS |

Eppig, J. J., and Schroeder, A. C. (1989). Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol. Reprod. 41, 268–276.
Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2FivVGhsA%3D%3D&md5=50b6efc96722af0f6203388c32f45917CAS | 2508774PubMed |

Fair, T., Carter, F., Park, S., Evans, A. C. O., and Lonergan, P. (2007). Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology 68, S91–S97.
Global gene expression analysis during bovine oocyte in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaiu74%3D&md5=0c6b219bb658cdf3a060b0a8afe32c19CAS | 17512044PubMed |

Fernández, C., Debeljuk, L., Diaz, E., and Diaz, B. (2002). Age differences in neurokinin A and substance P from the hypothalamus, pituitary, pineal gland, and striatum of the rat: effect of exogenous melatonin. Peptides 23, 941–945.
Age differences in neurokinin A and substance P from the hypothalamus, pituitary, pineal gland, and striatum of the rat: effect of exogenous melatonin.Crossref | GoogleScholarGoogle Scholar | 12084526PubMed |

Ghanem, N., Holker, M., Rings, F., Jennen, D., Tholen, E., Sirard, M. A., Torner, H., Kanitz, W., Schellander, K., and Tesfaye, D. (2007). Alterations in transcript abundance of bovine oocytes recovered at growth and dominance phases of the first follicular wave. BMC Dev. Biol. 7, 90.
Alterations in transcript abundance of bovine oocytes recovered at growth and dominance phases of the first follicular wave.Crossref | GoogleScholarGoogle Scholar | 17662127PubMed |

Goossens, K., Van Poucke, M., Van Soom, A., Vandesompele, J., Van Zeveren, A., and Peelman, L. J. (2005). Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos. BMC Dev. Biol. 5, 27.
Selection of reference genes for quantitative real-time PCR in bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 16324220PubMed |

Green, J. A., Xie, S., Quan, X., Bao, B., Gan, X., Mathialagan, N., Beckers, J.-F., and Roberts, R. M. (2000). Pregnancy-associated bovine and ovine glycoproteins exhibit spatially and temporally distinct expression patterns during pregnancy. Biol. Reprod. 62, 1624–1631.
| 1:CAS:528:DC%2BD3cXjsF2hsL8%3D&md5=c99aef871a0040ce6c1726dc8f148fb3CAS | 10819764PubMed |

Hershko, A., and Ciechanover, A. (1998). The ubiquitin system. Annu. Rev. Biochem. 67, 425–479.
The ubiquitin system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsFOmsLc%3D&md5=68af20efe58924ff53293efe8632748bCAS | 9759494PubMed |

Hochstrasser, M. (1996). Ubiquitin-dependent protein degradation. Annu. Rev. Genet. 30, 405–439.
Ubiquitin-dependent protein degradation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1yk&md5=ece12087e93557748c57fb13e51bbaf6CAS | 8982460PubMed |

Hosack, D. A., Dennis, G., Sherman, B. T., Lane, H. C., and Lempicki, R. A. (2003). Identifying biological themes within lists of genes with EASE. Genome Biol. 4, R70.
Identifying biological themes within lists of genes with EASE.Crossref | GoogleScholarGoogle Scholar | 14519205PubMed |

Izquierdo, D., Mogas, T., Palomo, M. J., and Paramio, M. T. (1995). Effect of sperm treatment on the in vitro fertilization and early cleavage of prepubertal goat oocytes. J. Reprod. Fert. Abst. Ser. 15, 69..

Kamada, S., Kubota, T., Taguchi, M., Ho, W. R., Sakamoto, S., and Aso, T. (1992). Effects of insulin-like growth factor-II on proliferation and differentiation of ovarian granulosa cells. Horm. Res. 37, 141–149.
Effects of insulin-like growth factor-II on proliferation and differentiation of ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXnsVaksQ%3D%3D&md5=1cd3f9318be59c0098b0d4835d976c96CAS | 1337056PubMed |

Kanka, J. (2003). Gene expression and chromatin structure in the pre-implantation embryo. Theriogenology 59, 3–19.
Gene expression and chromatin structure in the pre-implantation embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpslSmuro%3D&md5=a637ccf498e382e13e6c4a221e56478fCAS | 12499014PubMed |

Ko, M. S. H. (2004). Embryogenomics of pre-implantation mammalian development: current status. Reprod. Fertil. Dev. 16, 79–85.
Embryogenomics of pre-implantation mammalian development: current status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvVOqug%3D%3D&md5=6466b67ff23dd0bfb77641084833d50fCAS |

Koenig, J. L. F., and Stormshak, F. (1993). Cytogenic evaluation of ova from pubertal and third-estrous gilts. Biol. Reprod. 49, 1158–1162.
Cytogenic evaluation of ova from pubertal and third-estrous gilts.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7hsVOltw%3D%3D&md5=67d2960c3bfa39f6a898b3cbd791e68bCAS |

Kuijk, E. W., du Puy, L., van Tol, H. T., Haagsman, H. P., Colenbrander, B., and Roelen, B. A. (2007). Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos. BMC Dev. Biol. 7, 58.
Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 17540017PubMed |

Ledda, S., Bogliolo, L., Calvia, P., Leoni, G., and Naitana, S. (1997). Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes. J. Reprod. Fertil. 109, 73–78.
Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs1Gntbs%3D&md5=b584c3351b42707ac84269d2ffaa3c6aCAS | 9068416PubMed |

Leoni, G. G., Bebbere, D., Succu, S., Berlinguer, F., Mossa, F., Galioto, M., Bogliolo, L., Ledda, S., and Naitana, S. (2007). Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol. Reprod. Dev. 74, 249–257.
Relations between relative mRNA abundance and developmental competence of ovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsV2qtg%3D%3D&md5=28d92f32dc7ea8ce7457de623f244c08CAS | 16941675PubMed |

Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=e0ea026c02920b4196beca401ea8984bCAS | 11846609PubMed |

Lohuis, M. M. (1995). Potential benefits of bovine embryo manipulation technologies in genetic improvement programs. Theriogenology 43, 51–60.
Potential benefits of bovine embryo manipulation technologies in genetic improvement programs.Crossref | GoogleScholarGoogle Scholar |

Lonergan, P., Khatir, H., Piumi, F., Rieger, D., Humblot, P., and Boland, M. P. (1999). Effect of time interval from insemination to first cleavage on the developmental characteristics, sex and pregnancy rates following transfer of bovine preimplantation embryos. J. Reprod. Fertil. 117, 159–167.
Effect of time interval from insemination to first cleavage on the developmental characteristics, sex and pregnancy rates following transfer of bovine preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlaltLo%3D&md5=84e0d36c534120be1be92a6dd8f977c1CAS | 10645257PubMed |

Lonergan, P., Gutierrez-Adan, A., Pintado, B., Fair, T., Ward, F. A., de la Fuente, J., and Boland, M. P. (2000). Relationship between time of first cleavage and the expression of IGF-I growth factor, its receptor and two housekeeping genes in bovine two cell embryos and blastocysts produced in vitro. Mol. Reprod. Dev. 57, 146–152.
Relationship between time of first cleavage and the expression of IGF-I growth factor, its receptor and two housekeeping genes in bovine two cell embryos and blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsVeisb0%3D&md5=8426bbd678688c5f6daafcfcfca693e5CAS | 10984414PubMed |

Matsui, M., Takahashi, Y., Hishinuma, M., and Kanagawa, H. (1997). Stimulation of the development of bovine embryos by insulin and insulin-like growth factor-I (IGF-I) is mediated through the IGF-I receptor. Theriogenology 48, 605–616.
Stimulation of the development of bovine embryos by insulin and insulin-like growth factor-I (IGF-I) is mediated through the IGF-I receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmt1WhsL8%3D&md5=0ff828bc566baaf75cb612ecdf8edf0bCAS | 16728156PubMed |

Mogas, T., Palomo, M. J., Izquierdo, D., and Paramio, M. T. (1995). Effect of granulosa cell source on in vitro maturation, fertilization and embryo development of prepubertal goat oocytes. J.. Reprod. Fert. Abst. Ser. 15, 68..

Moss, T. N., Vo, A., McKeehan, W. L., and Liu, L. (2007). UXT (ubiquitously expressed transcript) causes mitochondrial aggregation. In Vitro Cell. Dev. Biol. Anim. 43, 139–146.
UXT (ubiquitously expressed transcript) causes mitochondrial aggregation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSqsbnI&md5=b55c156c7f29ef3878c94147bc2d4dd1CAS | 17554592PubMed |

O’Brien, J. K., Dwarte, D., Ryan, J. P., Maxwell, W. M. C., and Evans, G. (1996). Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reprod. Fertil. Dev. 8, 1029–1037.
Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2FntlGmtg%3D%3D&md5=9c57ee5914ba5cc03ee5e15210c45a1dCAS | 8916278PubMed |

O’Brien, J. K., Catt, S. L., Ireland, K. A., Maxwell, W. M. C., and Evans, G. (1997). In vitro and in vivo developmental capacity of oocytes from prepubertal and adult sheep. Theriogenology 47, 1433–1443.
In vitro and in vivo developmental capacity of oocytes from prepubertal and adult sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtVynsw%3D%3D&md5=ec90e79a1ed5dea871dca66c3480ffbdCAS | 16728089PubMed |

Oropeza, A., Wrenzycki, C., Hermmann, D., Hadeler, K. G., and Niemann, H. (2004). Improvement of the developmental capacity of oocytes from prepubertal cattle by intraovarian insulin-like growth factor-I application. Biol. Reprod. 70, 1634–1643.
Improvement of the developmental capacity of oocytes from prepubertal cattle by intraovarian insulin-like growth factor-I application.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOmtr8%3D&md5=c27955f9c1195b346148c5a2e98bde52CAS | 14766727PubMed |

Otoi, T., Yamamoto, K., Koyama, N., Hayashi, S., and Suzuki, T. (1995). Development capacity of bovine follicular oocytes collected from ovaries of pubertal heifers obtained through a spay device. J. Reprod. Dev. 41, 109–111.
Development capacity of bovine follicular oocytes collected from ovaries of pubertal heifers obtained through a spay device.Crossref | GoogleScholarGoogle Scholar |

Pintado, C. O., Pinto, F. M., Pennefather, J. N., Hidalgo, A., Baamonde, A., Sanchez, T., and Candenas, M. L. (2003). A role for tachykinins in female mouse and rat reproductive function. Biol. Reprod. 69, 940–946.
A role for tachykinins in female mouse and rat reproductive function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvVeitbg%3D&md5=99aa7e5f210cd64862cf1c65032aeb99CAS | 12773411PubMed |

Rance, N. E. (2009). Menopause and the human hypothalamus: evidence for the role of kisspeptin/neurokinin B neurons in the regulation of estrogen negative feedback. Peptides 30, 111–122.
Menopause and the human hypothalamus: evidence for the role of kisspeptin/neurokinin B neurons in the regulation of estrogen negative feedback.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFCmsbbO&md5=8fb112d06a68b87db5367b0b83990dabCAS | 18614256PubMed |

Revel, F., Mermillod, P., Peynot, N., Renard, J. P., and Heyman, Y. (1995). Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows. J. Reprod. Fertil. 103, 115–120.
Low developmental capacity of in vitro matured and fertilized oocytes from calves compared with that of cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M3it1CqsA%3D%3D&md5=4a1838ec359c5d488e5c4ebd76e785d8CAS | 7707286PubMed |

Rifkin, D. B., Mazzieri, R., Munger, J. S., Noguera, I., and Sung, J. (1999). Proteolytic control of growth factor availability. APMIS 107, 80–85.
Proteolytic control of growth factor availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitFals7s%3D&md5=fd93bad2ae936fa06d273bf37b011e96CAS | 10190283PubMed |

Rosenkrans, F., and First, N. (1991). Culture of bovine zygotes to the blastocyst stage: effect of amino-acids and vitamins. Theriogenology. 35, 266.

Rozen, S., and Skaletsky, H. J. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132, 365–386.
| 1:CAS:528:DyaK1MXmslKqsbo%3D&md5=5890392ec27be7d27225017ba8e7a16bCAS | 10547847PubMed |

Ryu, K. Y., Maehr, R., Gilchrist, C. A., Long, M. A., Bouley, D. M., Mueller, B., Ploegh, H. L., and Kopito, R. R. (2007). The mouse polyubiquitin gene UbC is essential for fetal liver development, cell-cycle progression and stress tolerance. EMBO J. 26, 2693–2706.
The mouse polyubiquitin gene UbC is essential for fetal liver development, cell-cycle progression and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtFSju7g%3D&md5=4aec89f9cc1684c4e7460c738949b4e8CAS | 17491588PubMed |

Sirard, M. A. (2001). Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–1254.
Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSisr0%3D&md5=c2da294887e856cdd87a4ae73021caf8CAS | 11327682PubMed |

Sirard, M. A., Richard, F., Blondin, P., and Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–136.
Contribution of the oocyte to embryo quality.Crossref | GoogleScholarGoogle Scholar | 16256189PubMed |

Telford, N. A., Watson, A. J., and Schultz, G. A. (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Reprod. Dev. 26, 90–100.
Transition from maternal to embryonic control in early mammalian development: a comparison of several species.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c3mslOhtQ%3D%3D&md5=9fba85bb0339b45b5570cc49f8f79f96CAS | 2189447PubMed |

Tong, Z. B., Gold, L., Pfeifer, K. E., Dorward, H., Lee, E., Bondy, C. A., Dean, J., and Nelson, L. M. (2002). Mater, a maternal effect gene required for early embryonic development in mice. Nat. Genet. 26, 267–268.

Trounson, A., Anderiesz, C., and Jones, G. (2001). Maturation of human oocytes in vitro and their developmental competence. Reproduction 121, 51–75.
Maturation of human oocytes in vitro and their developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslakuw%3D%3D&md5=15d034b220c245845b6feb2118f563adCAS | 11226029PubMed |

Van Blerkom, J. (2004). Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence. Reproduction 128, 269–280.
Mitochondria in human oogenesis and preimplantation embryogenesis: engines of metabolism, ionic regulation and developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXot1KitL0%3D&md5=9c9ed43afacc5ad9db4dfb53a13c4497CAS | 15333778PubMed |

Wang, J., Mayernik, L., and Armant, D. R. (2002). Integrin signaling regulates blastocyst adhesion to fibronectin at implantation: intracellular calcium transients and vesicle trafficking in primary trophoblast cells. Dev. Biol. 245, 270–279.
Integrin signaling regulates blastocyst adhesion to fibronectin at implantation: intracellular calcium transients and vesicle trafficking in primary trophoblast cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtFyju7Y%3D&md5=f47aec0691f8fb4336329ada05a12077CAS | 11977980PubMed |

Wooding, F. B., Roberts, R. M., and Green, J. A. (2005). Light and electron microscope immunocytochemical studies of the distribution of pregnancy associated glycoproteins (PAGs) throughout pregnancy in the cow: possible functional implications. Placenta 26, 807–827.
Light and electron microscope immunocytochemical studies of the distribution of pregnancy associated glycoproteins (PAGs) throughout pregnancy in the cow: possible functional implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFSmsbvL&md5=124f0f521c88e085eca9d9bbe71da36fCAS | 16226131PubMed |

Wrenzycki, C., Herrmann, D., Carnwath, J. W., and Niemann, H. (1996). Expression of the gap junction gene connexin43 (Cx43) in preimplantation bovine embryos derived in vitro or in vivo. J. Reprod. Fertil. 108, 17–24.
| 1:CAS:528:DyaK28XntFOlu7w%3D&md5=558954a757f0cc9f9bb3a94e24e74e8eCAS | 8958823PubMed |

Wrenzycki, C., Herrmann, D., Lucas-Hahn, A., Korsawe, K., Lemme, E., and Niemann, H. (2005). Messenger RNA expression patterns in bovine embryos derived from in vitro procedures and their implications for development. Reprod. Fertil. Dev. 17, 23–35.
Messenger RNA expression patterns in bovine embryos derived from in vitro procedures and their implications for development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKrurbL&md5=119ad08e4f54a81039b635d7dd968981CAS | 15745629PubMed |

Wu, X., Viveiros, M. M., Eppig, J. J., Bai, Y., Fitzpatrick, S. L., and Matzuk, M. M. (2003). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat. Genet. 33, 187–191.
Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsFSktg%3D%3D&md5=1d19f071bf7f177800200ecf20f5c8caCAS | 12539046PubMed |

Xie, S. C., Low, B. G., Nagel, R. J., Kramer, K. K., Anthony, R. V. S., and Zoli, A. P. (1991). Identification of the major pregnancy-specific antigens of cattle and sheep as inactive members of the aspartic proteinase family. Proc. Natl. Acad. Sci. USA 88, 10 247–10 251.
Identification of the major pregnancy-specific antigens of cattle and sheep as inactive members of the aspartic proteinase family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXnsFGgug%3D%3D&md5=6b5eb101de7879ebcfd33263f4dc6d77CAS |

Yang, X., Kubota, C., Suzuki, H., Taneja, M., Bols, P. E., and Presicce, G. A. (1998). Control of oocyte maturation in cows – biological factors. Theriogenology 49, 471–482.
Control of oocyte maturation in cows – biological factors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ps1GktQ%3D%3D&md5=e14e11de492846968c5a97893e25af60CAS | 10732028PubMed |

Yao, J., Ren, X., Ireland, J. J., Coussens, P. M., Smith, T. P., and Smith, G. W. (2004). Generation of a bovine oocyte cDNA library and microarray: resources for identification of genes important for follicular development and early embryogenesis. Physiol. Genomics 19, 84–92.
Generation of a bovine oocyte cDNA library and microarray: resources for identification of genes important for follicular development and early embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXoslShtro%3D&md5=9161883027e6e5b68f0784ee135059a0CAS | 15375196PubMed |

Zaraza, J., Oropeza, A., Velazquez, M. A., Korsawe, K., Herrmann, D., Camwath, J. W., and Niemann, H. (2010). Developmental competence and mRNA expression of preimplantation in vitro-produced embryos from prepubertal and postpubertal cattle and their relationship with apoptosis after intraovarian administration of IGF-1. Theriogenology 74, 75–89.
Developmental competence and mRNA expression of preimplantation in vitro-produced embryos from prepubertal and postpubertal cattle and their relationship with apoptosis after intraovarian administration of IGF-1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVWjtLk%3D&md5=f67bdebd8b511e2b3f9d1bd3777de745CAS | 20138354PubMed |

Zhao, H., Wang, Q., Zhang, H., Liu, Q., Du, X., Richter, M., and Greene, M. I. (2005). UXT is a novel centrosomal protein essential for cell viability. Mol. Biol. Cell 16, 5857–5865.
UXT is a novel centrosomal protein essential for cell viability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht12gsLfK&md5=3aa558ab0a75eee018e62cf785f5c4d3CAS | 16221885PubMed |