Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-18T09:40:48.789Z Has data issue: false hasContentIssue false

Effects of oocyte donor age and embryonic stage of development on transcription of genes coding for enzymes of the prostaglandins and progesterone synthesis pathways in bovine in vitro produced embryos

Published online by Cambridge University Press:  26 September 2014

A. Torres
Affiliation:
Reproduction and Obstetrics, CIISA, Faculty of Veterinary Medicine, University of Lisbon, Avenida da Universidade Técnica, Alto da Ajuda, 1300–477 Lisboa, Portugal.
M. Batista
Affiliation:
Reproduction and Obstetrics, CIISA, Faculty of Veterinary Medicine, University of Lisbon, Avenida da Universidade Técnica, Alto da Ajuda, 1300–477 Lisboa, Portugal.
P. Diniz
Affiliation:
Reproduction and Obstetrics, CIISA, Faculty of Veterinary Medicine, University of Lisbon, Avenida da Universidade Técnica, Alto da Ajuda, 1300–477 Lisboa, Portugal.
E. Silva
Affiliation:
Reproduction and Obstetrics, CIISA, Faculty of Veterinary Medicine, University of Lisbon, Avenida da Universidade Técnica, Alto da Ajuda, 1300–477 Lisboa, Portugal.
L. Mateus
Affiliation:
Reproduction and Obstetrics, CIISA, Faculty of Veterinary Medicine, University of Lisbon, Avenida da Universidade Técnica, Alto da Ajuda, 1300–477 Lisboa, Portugal.
L. Lopes-da-Costa*
Affiliation:
Reproduction and Obstetrics, CIISA, Faculty of Veterinary Medicine, Universidade de Lisboa, Avenida da Universidade Técnica, Alto da Ajuda, 1300–477 Lisboa, Portugal.
*
All correspondence to: Luís Lopes-da-Costa. Reproduction and Obstetrics, CIISA, Faculty of Veterinary Medicine, Universidade de Lisboa, Avenida da Universidade Técnica, Alto da Ajuda, 1300–477 Lisboa, Portugal. E-mail: lcosta@fmv.utl.pt

Summary

The ability of early bovine embryos to produce prostaglandins (PGs) and progesterone (P4), and the role of these mediators in embryonic development and survival are poorly understood. In this study we tested the hypothesis that day 7 bovine embryos are able to transcribe genes coding for enzymes of the PGs (PTGS2, PGES, PGFS) and P4 (StAR, P450scc, 3β-HSD) synthesis pathways, and that transcription levels of these genes are associated with developmental progression and heifer age-related [pre-pubertal (PP) versus post-pubertal cyclic (C)] oocyte competence. Compared with C heifer oocytes, PP heifer oocytes showed a lower (P < 0.0001) in vitro blastocyst rate, but in embryos developing until day 7, heifer age had no effect on quality grade. Day 7 quality grade 1–2 embryos were selected for RNA extraction and gene transcription analysis by qRT-PCR, in a 2 × 2 factorial design [age (PP or C) × embryonic stage (compact morulae and early blastocysts, CM + EBL, or blastocysts and expanded blastocysts, BL + BEX); 15 embryos/group]. Transcription levels of PTGS2, PGES, PGFS, P450scc and 3β-HSD were not affected by heifer age but were higher (P < 0.01) in BL + BEX than in CM + EBL. In conclusion, the main limiting factor for embryo production from PP heifers is oocyte competence. Day 7 bovine embryos evidence transcription of genes coding for enzymes of PGs and P4 synthesis pathways, and transcription levels are associated with blastocyst differentiation. This prompts for an autocrine/paracrine action of PGs and P4 in early bovine embryonic development.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andersen, C.L., Jensen, J. & Ørntoft, T. (2004). Normalization of real-time quantitative reverse transcription-PCR data: a model based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245–50.CrossRefGoogle Scholar
Armstrong, D.T. (2001). Effects of maternal age on oocyte developmental competence. Theriogenology 55, 1303–22.Google Scholar
Arosh, J.A., Banu, S.K., Chapdelaine, P., Emond, V., Kim, J.J., MacLaren, L.A. & Fortier, M.A. (2003). Molecular cloning and characterization of bovine prostaglandin E2 receptors EP2 and EP4: expression and regulation in endometrium and myometrium during the estrous cycle and early pregnancy. Endocrinology 144, 3076–91.CrossRefGoogle ScholarPubMed
Arosh, J.A., Banu, S.K., Chapdelaine, P. & Fortier, M.A. (2004). Temporal and tissue-specific expression of prostaglandin receptors EP2, EP3, EP4, FP, and cyclooxygenases 1 and 2 in uterus and fetal membranes during bovine pregnancy. Endocrinology 145, 407–17.CrossRefGoogle ScholarPubMed
Asselin, E., Goff, A.K., Bergeron, H. & Fortier, M.A. (1996). Influence of sex steroids on the production of prostaglandins F and E2 and response to oxytocin in cultured epithelial and stromal cells of the bovine endometrium. Biol. Reprod. 54, 371–9.Google Scholar
Aurich, C. & Budik, S. (2005). Expression of enzymes involved in the synthesis of prostaglandins in early equine embryos. Reprod. Dom. Anim. 40, 344.Google Scholar
Baskar, J.F., Torchiana, D.F., Biggers, J.D., Corey, E.J., Andersen, N.H. & Subramanian, N. (1981). Inhibition of hatching of mouse blastocysts in vitro by various prostaglandin antagonists. J. Reprod. Fertil. 63, 359–63.CrossRefGoogle ScholarPubMed
Bazer, F.W., Burghardt, R.C., Johnson, G.A., Spencer, T.E. & Wu, G. (2008). Interferons and progesterone for establishment and maintenance of pregnancy: interactions among novel cell signaling pathways. Reprod. Biol. 8, 179211.Google Scholar
Buuck, M.J., Breuel, K.F., Fukuda, A. & Schrick, F.N. (1997). Embryonic development of the rat associated with elevated prostaglandin F2α. Biol. Reprod. 56 (Suppl. 1), 188.Google Scholar
Camargo, L.S.A., Viana, J.H.M., , W.F., Ferreira, A.M. & Vale Filho, V.R. (2005). Developmental competence of oocytes from prepubertal Bos indicus crossbred cattle. Anim. Reprod. Sci. 85, 53–9.Google Scholar
Charpigny, G., Reinaud, P., Tamby, J.P., Creminon, C. & Guillomot, M (1997). Cyclooxygenase-2 unlike cyclooxygenase-1 is highly expressed in ovine embryos during the implantation period. Biol. Reprod. 57, 1032–40.Google Scholar
Clemente, M., de La Fuente, J., Fair, T., Al Naib, A., Gutierrez-Adan, A., Roche, J.F., Rizos, D. & Lonergan, P. (2009). Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium? Reproduction 138, 507–17.CrossRefGoogle ScholarPubMed
Davis, D.L., Pakrasi, P.L. & Dey, S.K. (1983). Prostaglandins in swine blastocysts. Biol. Reprod. 28, 1114–8.Google Scholar
Desjardins, C. & Hafs, H.D. (1969). Maturation of bovine female genitalia from birth through puberty. J. Anim. Sci., 28, 502–7.Google Scholar
Dey, S.K., Chien, S.M., Cox, C.L. & Crist, R.D. (1980). Prostaglandin synthesis in the rabbit blastocyst. Prostaglandins 19, 449–53.Google Scholar
Diskin, M.G. & Morris, D.G. (2008). Embryonic and early foetal losses in cattle and other ruminants. Reprod. Domest. Anim. 43 (2), 260–7.CrossRefGoogle ScholarPubMed
Fazio, R.A., Buuck, M.J. & Schrick, F.N. (1997). Embryonic development of frozen–thawed bovine embryos cultured in vitro in response to elevated concentrations of prostaglandin F2α. Biol. Reprod. 56 (Suppl. 1; Abstr.), 187.Google Scholar
Ferguson, C.E., Kesler, D.J. & Godke, R.A. (2012) Progesterone enhances in vitro development of bovine embryos. Theriogenology 77, 108–14.CrossRefGoogle ScholarPubMed
Forde, N., Carter, F., Fair, T., Crowe, M.A., Evans, A.C., Spencer, T.E., Bazer, F.W., McBride, R., Boland, M.P., O’Gaora, P., Lonergan, P. & Roche, J. (2009). Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol Reprod. 81 (4), 784–94.Google Scholar
Helliwell, R., Adams, L. & Mitchell, M. (2004). Prostaglandin synthases: recent developments and a novel hypothesis. Prostaglandins Leukot. Essent. Fatty Acids 70, 101–13.CrossRefGoogle Scholar
Holm, P., Booth, P.J., Schmidt, M.H., Greve, T. & Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683700.CrossRefGoogle ScholarPubMed
Holmes, P.V. & Gordashko, B.J. (1980). Evidence of prostaglandin involvement in blastocyst implantation. J. Embryol. Exp. Morphol. 55, 109–22.Google Scholar
Huang, J.C., Wan, W-S-A., Goldsby, J.S. & Wu, K.K. (2004). Cyclooxygenase 2 derived endogenous prostacyclin enhances mouse embryo hatching. Hum. Reprod. 19, 2900–6.Google Scholar
Hwang, D.H., Pool, S.H., Rorie, R.W., Boudreau, M. & Godke, R.A. (1988). Transitional changes in arachidonic acid metabolism by bovine embryos at different developmental stages. Prostaglandins 35 (3), 387402.CrossRefGoogle ScholarPubMed
Hyland, J.H., Manns, J.G. & Humphrey, W.D. (1982). Prostaglandin production by ovine embryos and endometrium in vitro . J. Reprod. Fertil. 65, 299304.CrossRefGoogle ScholarPubMed
Juengel, J.L. & Niswender, G.D. (1999). Molecular regulation of luteal progesterone synthesis in domestic animals. J. Reprod. Fert. 54, 193205.Google Scholar
Kanka, J., Nemcova, L., Toralova, T., Vodickova-Kepkova, K., Vodicka, P., Jeseta, M. & Machatkova, M. (2012). Association of the transcription profile of bovine oocytes and embryos with developmental potential. Anim. Reprod. Sci. 134 (1–2), 2935.CrossRefGoogle ScholarPubMed
Kelly, J.M., Kleeman, D.O. & Walker, S.K. (2005). Enhanced efficiency in the production of offspring from 4- to 8-week-old lambs. Theriogenology 63, 1876–90.Google Scholar
Kennedy, T.G., Gillio-Meina, C. & Phang, S.H. (2007). Prostaglandins and the initiation of blastocyst implantation and decidualization. Reproduction 134, 635–43.Google Scholar
Khatir, H., Lonergan, P., Carolan, C. & Mermillod, P. (1996). Prepubertal bovine oocyte: a negative model for studying oocyte developmental competence. Mol. Reprod. Dev. 45, 231–9.3.0.CO;2-3>CrossRefGoogle ScholarPubMed
Leoni, G., Succu, S., Berlinguer, F., Rosati, I., Bebbere, D., Bogliolo, L., Ledda, S. & Naitana, S. (2006a). Delay on the in vitro kinetic development of prepubertal ovine embryos. Anim. Reprod. Sci. 92, 373–83.CrossRefGoogle ScholarPubMed
Leoni, G.G., Bebbere, D., Succu, S., Berlinguer, F., Mossa, F., Galioto, M., Bogliolo, L., Ledda, S. & Naitana, S. (2006b). Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol. Reprod. Dev. 74, 249–57.CrossRefGoogle Scholar
Lewis, G.S., Thatcher, W.W., Bazer, F.W. & Curl, J.S. (1982). Metabolism of arachidonic acid in vitro by bovine blastocysts and endometrium. Biol. Reprod. 27, 431–9.CrossRefGoogle ScholarPubMed
Lim, H., Paria, B.C., Das, S.K., Dinchuk, J.E., Langenbach, R., Trzaskos, J.M. & Dey, S.K. (1997). Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91, 197208.Google Scholar
Lonergan, P. (2011). Influence of progesterone on oocyte quality and embryo development in cows. Theriogenology 76, 1594–601.Google Scholar
Majerus, V., De Roover, R., Etienne, D., Kaidi, S., Massip, A., Dessy, F. & Donnay, I. (1999). Embryo production by ovum pick up in unstimulated calves before and after puberty. Theriogenology 52, 1169–79.Google Scholar
Majerus, V., Lequarré, A.S., Ferguson, E.M., Kaidi, S., Massip, A., Dessy, F. & Donnay, I. (2000). Characterization of embryos derived from calf oocytes: kinetics of cleavage, cell allocation to inner cell mass, and trophectoderm and lipid metabolism. Mol. Reprod. Dev. 57, 346–52.Google Scholar
Mann, G.E. & Lamming, G.E. (2001). Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction 121, 175–80.CrossRefGoogle ScholarPubMed
Marshburn, P.B., Shabanowitz, R.B. & Clark, M.R. (1990). Immunohistochemical localization of prostaglandin H synthase in the embryo and uterus of the mouse from ovulation through implantation. Mol. Reprod. Dev. 25, 309–16.Google Scholar
Matsumoto, H., Ma, W.G., Smalley, W., Trzaskos, J., Breyer, R.M. & Dey, S.K. (2001). Diversification of cyclooxygenase-2-derived prostaglandins in ovulation and implantation. Biol. Reprod. 64, 1557–65.Google Scholar
Maurer, R.R. & Beier, H.M. (1976). Uterine proteins and development in vitro of rabbit preimplantation embryos. J. Reprod. Fertil. 48, 3341.CrossRefGoogle ScholarPubMed
McCracken, J.A., Custer, E.E. & Lamsa, J.C. (1999). Luteolysis: a neuroendocrine-mediated event. Physiol. Rev. 79, 263323.CrossRefGoogle ScholarPubMed
Merlo, B., Iacono, E. & Mari, G. (2006) Effect of progesterone and epidermal growth factor on in vitro-produced eight-cell bovine embryos in a serum free culture medium. Reprod. Fertil. Dev., 19, 211.Google Scholar
Mishra, S., Lei, Z.M. & Rao, Ch.V. (2003). A novel role of luteinizing hormone in the embryo development in cocultures. Biol. Reprod. 68, 1455–62.Google Scholar
O’Brien, J.K., Beck, N.F.G., Maxwell, W.M.C. & Evans, G. (1997). Effect of hormone pre-treatment of prepubertal sheep on the production and developmental capacity of oocytes in vitro and in vivo . Reprod. Fertil. Dev. 9, 625–31.CrossRefGoogle ScholarPubMed
Okumu, L.A., Forde, N., Fahey, A.G., Fitzpatrick, E., Roche, J.F., Crowe, M.A. & Lonergan, P. (2010). The effect of elevated progesterone and pregnancy status on mRNA expression and localisation of progesterone and oestrogen receptors in the bovine uterus. Reproduction 140, 143–53.CrossRefGoogle ScholarPubMed
Oropeza, A., Wrenzycki, C., Herrmann, D., Hadeler, K-G. & Niemann, H. (2004). Improvement of the developmental capacity of oocytes from prepubertal cattle by intraovarian IGF-I application. Biol. Reprod. 70, 1634–43.Google Scholar
Parrish, J.J., Krogenaes, A. & Susko-Parrish, J.L. (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44, 859–69.Google Scholar
Pereira, R.M., Pimenta, J., Becker, J.D., Baptista, M.C., Vasques, M.I., Horta, A.E.M. & Marques, C.C. (2005). Cyclooxygenase-2 (COX-2) expression by in vitro produced bovine embryos. Preliminary results. RPCV 104 (555–6), 181–4.Google Scholar
Presicce, G.A., Jiang, S., Simkin, M., Zhang, L., Looney, C.R., Godke, R.A. & Yang, X. (1997). Age and hormonal dependence of acquisition of oocyte competence for embryogenesis in prepubertal calves. Biol. Reprod. 56, 386–92.CrossRefGoogle ScholarPubMed
Ptak, G., Loi, P., Dattena, M., Tischner, M. & Cappai, P. (1999). Offspring from one-month-old lambs: studies on the developmental capability of prepubertal oocytes. Biol. Reprod. 61, 15681574.CrossRefGoogle ScholarPubMed
Ptak, G., Tischner, M., Bernabo, N. & Loi, P. (2003). Donor dependant developmental competence of oocytes from lambs subjected to repeated hormonal stimulation. Biol. Reprod. 69, 278–85.Google Scholar
Robinson, R.S., Mann, G.E., Lamming, G.E. & Wathes, D.C. (2001). Expression of oxytocin, oestrogen and progesterone receptors in uterine biopsy samples the oestrous cycle and early pregnancy in cows. Reproduction 122, 965–79.CrossRefGoogle ScholarPubMed
Saint-Dizier, M., Guyader-Joly, C., Charpigny, G., Grimard, B., Humblot, P. & Ponter, A.A. (2011). Expression of enzymes involved in the synthesis of prostaglandin E2 in bovine in vitro-produced embryos. Zygote 19, 277–83.CrossRefGoogle ScholarPubMed
Sayre, B.L. (2007). Effect of prostaglandins E2 and F2α on in vitro development and hatching of caprine blastocysts. Small Rumin. Res. 67, 257–63.Google Scholar
Sayre, B.L. & Lewis, G.S. (1993). Arachidonic acid metabolism during early development of ovine embryos: a possible relationship to shedding of the zona pellucida. Prostaglandins 45, 557–69.CrossRefGoogle ScholarPubMed
Scenna, F.N., Edwards, J.L., Rohrbach, N.R., Hockett, M.E., Saxton, A.M. & Schrick, F.N. (2004). Detrimental effects of prostaglandin F2α on preimplantation bovine embryos. Prostaglandins Other Lipid Mediat. 73, 215–26.Google Scholar
Shemesh, M., Milaguir, F., Ayalon, N. & Hansel, W. (1979). Steroidogenesis and prostaglandin synthesis by cultured bovine blastocysts. J. Reprod. Fert. 56, 181–5.Google Scholar
Soto, P., Natzke, R.P. & Hansen, P.J. (2003). Identification of possible mediators of embryonic mortality caused by mastitis: actions of lipopolysaccharide, prostaglandin F2α, and the nitric oxide generator, sodium nitroprusside dihydrate, on oocyte maturation and embryonic development in cattle. Am. J. Reprod. Immunol. 50, 263–72.Google Scholar
Stocco, C., Telleria, C. & Gibori, G. (2007). The molecular control of corpus luteum formation, function, and regression. Endocr. Rev. 28, 117–49.Google Scholar
Stringfellow, D.A. & Seidel, S.M. (eds) (1998). Manual of the International Embryo Transfer Society. Savoy, Illinois, USA: International Embryo Transfer Society, Inc. Google Scholar
Tan, H.N., Liu, Y., Diao, H.L. & Yang, Z.M. (2005). Cyclooxygenases and prostaglandin E synthases in preimplantation mouse embryos. Zygote 13, 103–8.CrossRefGoogle ScholarPubMed
Tervit, H.R., McMillan, W.H., McGowan, L.T., Smith, J.F., Hall, D.R. & Donnison, M.J. (1997). Effect of juvenile calf age on follicular dynamics and in vitro embryo production. Theriogenology 47, 300.Google Scholar
Torres, A., Batista, M., Diniz, P., Mateus, L. & Lopes-da-Costa, L. (2013). Embryo-luteal cells co-culture: an in vitro model to evaluate steroidogenic and prostanoid bovine early embryo-maternal interactions. In Vitro Cell. Dev. Biol. Anim. 49 (2), 134–46.Google Scholar
Wang, H.B., Wen, Y., Mooney, S., Behr, B. & Polan, M.L. (2002). Phospholipase A2 and cyclooxygenase gene expression in human preimplantation embryos. J. Clin. Endocrinol. Metab. 87, 2629–34.CrossRefGoogle ScholarPubMed
Watson, E.D. & Sertich, P.L. (1989). Prostaglandin production by horse embryos and the effect of co-culture of embryos with endometrium from pregnant mares. J. Reprod. Fert. 87, 331–6.Google Scholar
Weber, J.A., Woods, G.L., Freeman, D.A. & Vanderwall, D.K. (1992). Prostaglandin E2 secretion by day 6 to day 9 equine embryos. Prostaglandins 43, 55–9.Google Scholar
Weems, C.W., Weems, Y.S. & Randel, R.D. (2006). Prostaglandins and reproduction in female farm animals. Vet. J. 171 (2), 206–28.Google Scholar
Wilson, J.M., Zalesku, D.D., Looney, C.R., Bondioli, K.R. & Magness, R.R. (1992). Hormone secretion by preimplantation embryos in a dynamic in vitro culture system. Biol. Reprod. 46, 295300.Google Scholar
Yang, X., Presicce, G.A., Du, F. & Jiang, S. (1997). Pregnancies and calves derived from pre-pubertal calf oocytes. Theriogenology 47, 163.CrossRefGoogle Scholar
Zhao, S. & Fernald, R.D. (2005). Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 12, 1047–64.Google Scholar