High hydrostatic pressure treatment improves the quality of in vitro-produced ovine blastocysts
Luisa Bogliolo A C , Federica Ariu A , Giovanni Leoni B , Stefania Uccheddu A and Daniela Bebbere A
+ Author Affiliations
- Author Affiliations
A Department of Veterinary Clinics and Pathology, University of Sassari, Via Vienna, 07100 Sassari, Italy.
B Department of Animal Biology, University of Sassari, Via Vienna, 07100 Sassari, Italy.
C Corresponding author. Email: luis@uniss.it
Reproduction, Fertility and Development 23(6) 809-817 https://doi.org/10.1071/RD11023
Submitted: 19 January 2011 Accepted: 8 March 2011 Published: 7 July 2011
Abstract
Exposure to sub-lethal hydrostatic pressure (HP) treatment is emerging as an approach to improve the general resistance of gametes and embryos to in vitro conditions. The present study was aimed to evaluate the effect of HP treatment on in vitro-produced ovine blastocysts. Experiment 1 was aimed to define optimal treatment parameters: two different HP treatments were applied to blastocysts and embryo survival was evaluated. In Experiment 2, HP parameters (40 MPa, 70 min, 38°C) selected in Experiment 1 were used to treat blastocysts. Embryo quality was assessed and compared with untreated controls by counting total cell number, the inner cell mass (ICM) and trophectoderm (TE) cells and by evaluating nuclear picnosis. HP-treated blastocysts were processed for gene expression analysis (AQP3, ATP1A1, BAX, CDH1, HSP90β, NANOG, OCT4 and TP53) 1, 5 h after the end of HP exposure. Results showed that the hatching rate of embryos treated at 40 MPa was significantly higher than that of the 60 MPa-treated group (P < 0.01) and similar to untreated embryos. Blastocysts exposed at 40 MPa showed higher ICM (P < 0.05) and TE (P < 0.01) cell number and a lower percentage of picnotic nuclei (P < 0.05) compared with the control group. Significantly lower abundance for BAX (P < 0.01) and OCT4 (P < 0.05) transcripts were observed in HP embryos than in the control group. In conclusion, treatment with HP improved the quality of in vitro-produced ovine blastocysts by increasing their cell number and reducing the proportion of nuclear picnosis.
Additional keywords: blastocyst cell number, gene expression analysis, picnosis.
References
Arya, R., Mallik, M., and Lakhotia, S. C. (2007). Heat-shock genes – integrating survival and death. J. Biosci. 32, 595–610.| Heat-shock genes – integrating survival and death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFalsrs%3D&md5=5a022996fe300d01376d1f9ebd4bcc10CAS | 17536179PubMed |
Bebbere, D., Bogliolo, L., Ariu, F., Fois, S., Leoni, G. G., Succu, S., Berlinguer, F., and Ledda, S. (2010). Different temporal gene expression patterns for ovine pre-implantation embryos produced by parthenogenesis or in vitro fertilization. Theriogenology 74, 712–723.
| Different temporal gene expression patterns for ovine pre-implantation embryos produced by parthenogenesis or in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGrtbvF&md5=aa8f2ad635974339ec6fc3b1a9f77657CAS | 20451995PubMed |
Bergeron, L., Perez, G. I., Macdonald, G., Shi, L., Sun, Y., Jurisicova, A., Varmuza, S., Latham, K. E., Flaws, J. A., Salter, J. C., Hara, H., Moskowitz, M. A., Li, E., Greenberg, A., Tilly, J. L., and Yuan, J. (1998). Defects in regulation of apoptosis in caspase-2 deficient mice. Genes Dev. 12, 1304–1314.
| Defects in regulation of apoptosis in caspase-2 deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtVejsrc%3D&md5=712d47cfa91827f7507b0944e0a42d1cCAS | 9573047PubMed |
Biggers, J. D. (2001). Thoughts on embryo culture conditions. Reprod. Biomed. Online 4, 30–38.
Bock, I., Losonczi, E., Mamo, S., Polgar, Z., Dinnyes, A., Harnos, A., and Pribenszky, C. (2010). Stress tolerance and transcriptional response in mouse embryos treated with high hydrostatic pressure to enhance cryotolerance. Cryo Lett. 31, 401–412.
Boelhauve, M., Sinowatz, F., Wolf, E., and Paula-Lopes, F. F. (2005). Maturation of bovine oocytes in the presence of leptin improves development and reduces apoptosis of in vitro-produced blastocysts. Biol. Reprod. 73, 737–744.
| Maturation of bovine oocytes in the presence of leptin improves development and reduces apoptosis of in vitro-produced blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCgtrjO&md5=fbc80420861e1be18801dd0053d73f86CAS | 15958729PubMed |
Boiani, M., and Schöler, H. R. (2005). Regulatory networks in embryo-derived pluripotent stem cells. Nat. Rev. Mol. Cell Biol. 6, 872–881.
| Regulatory networks in embryo-derived pluripotent stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFKlsLzE&md5=fe194691fd557b2521a7731c80baafdaCAS | 16227977PubMed |
Christians, E. S., Zhou, Q., Renard, J. P., and Benjamin, I. J. (2003). Heat-shock proteins in mammalian development. Semin. Cell Dev. Biol. 14, 283–290.
| Heat-shock proteins in mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtF2ksQ%3D%3D&md5=785420abac783cd0a8d4fe0cb8c3cee6CAS | 14986858PubMed |
Csermely, P., Schnaider, T., Soti, C., Prohaszka, Z., and Nardai, G. (1998). The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review. Pharmacol. Ther. 79, 129–168.
| The 90-kDa molecular chaperone family: structure, function, and clinical applications. A comprehensive review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltVOktrc%3D&md5=16676aa8d0542a31c667d506a139395dCAS | 9749880PubMed |
Dinnyes, A., Polgar, Z., Pribenszky, Cs., and Pirity, M. K. (2010). Improved embryoid body cryopreservation and cardiomyocyte differentiation following high hydrostatic pressure treatment. In ‘Proceedings of the 1st International Congress on Controversies in Cryopreservation of Stem Cells, Reproductive Cells, Tissue and Organs, Valencia, Spain, 27–30 May 2010’. (CometMed: Israel.)
Du, Y., Pribenszky, Cs., Molnár, M., Zhang, X., Yang, H., Kuwayama, M., Pedersen, A. M., Villemoes, K., Bolund, L., and Vajta, G. (2008a). High hydrostatic pressure (HHP): a new way to improve in vitro developmental competence of porcine matured oocytes after vitrification. Reproduction 135, 13–17.
| High hydrostatic pressure (HHP): a new way to improve in vitro developmental competence of porcine matured oocytes after vitrification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhs1CksL8%3D&md5=40791d16b93fdb5869c2b24e049634e6CAS | 18159079PubMed |
Du, Y., Lin, L., Schmidt, M., Bogh, I. B., Kragh, P. M., Sorensen, C. B., Li, J., Purup, S., Pribenzsky, C., Molnár, M., Kuwayama, M., Zhang, X., Yang, H., Bolund, L., and Vajta, G. (2008b). High hydrostatic pressure treatment of porcine oocytes before handmade cloning improves developmental competence and cryosurvival. Cloning Stem Cells 10, 325–330.
| High hydrostatic pressure treatment of porcine oocytes before handmade cloning improves developmental competence and cryosurvival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVOmu7zK&md5=b506b8174c8acf205ea12b3eddf32e98CAS | 18479211PubMed |
Edwards, J. L., and Hansen, P. J. (1997). Differential responses of bovine oocytes and pre-implantation embryos to heat shock. Mol. Reprod. Dev. 46, 138–145.
| Differential responses of bovine oocytes and pre-implantation embryos to heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXoslWhtQ%3D%3D&md5=5dceffa5a96a2a75d219df7f1b477999CAS | 9021745PubMed |
Enright, B. P., Lonergan, P., Dinnyes, A., Fair, T., Ward, F. A., Yang, X., and Boland, M. P. (2000). Culture of in vitro-produced bovine zygotes in vitro vs. in vivo: implications for early embryo development and quality. Theriogenology 54, 659–673.
| Culture of in vitro-produced bovine zygotes in vitro vs. in vivo: implications for early embryo development and quality.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FovVGrsg%3D%3D&md5=48686f28cf98f8cab42c55445240f10fCAS | 11101029PubMed |
Gardner, D. K. (2008). Dissection of culture media for embryos: the most important and less important components and characteristics. Reprod. Fertil. Dev. 20, 9–18.
| Dissection of culture media for embryos: the most important and less important components and characteristics.Crossref | GoogleScholarGoogle Scholar | 18154693PubMed |
Garrido, C., Brunet, M., Didelot, C., Zermati, Y., Schmitt, E., and Kroemer, G. (2006). Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle 5, 2592–2601.
| Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhslyhsL4%3D&md5=2bc3736a832ee23cecc773abe14635e3CAS | 17106261PubMed |
Gjørret, J. O., Knijn, H. M., Dieleman, S. J., Avery, B., Larsson, L. I., and Maddox-Hyttel, P. (2003). Chronology of apoptosis in bovine embryos produced in vivo and in vitro. Biol. Reprod. 69, 1193–1200.
| Chronology of apoptosis in bovine embryos produced in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 12773422PubMed |
Hardy, K. (1999). Apoptosis in the human embryo. Rev. Reprod. 4, 125–134.
| Apoptosis in the human embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmsVCmu7c%3D&md5=5f9696a20800fd6c14988ed53d1eea07CAS | 10521149PubMed |
Hardy, K., Handyside, A. H., and Winstons, R. M. L. (1989). The human blastocyst: cell number, death and allocation during late pre-implantation development in vitro. Development 107, 597–604.
| 1:STN:280:DyaK3c7is1eruw%3D%3D&md5=8fbc90629c3af95ef61104c947667c69CAS | 2612378PubMed |
Huang, S. Y., Pribenszky, Cs., Kuo, Y. H., Teng, S. H., Chen, Y. H., Chung, M. T., and Chiu, Y. F. (2009). Hydrostatic pressure affects the protein profile of boar sperm before and after freezing–thawing. Anim. Reprod. Sci. 112, 136–149.
| Hydrostatic pressure affects the protein profile of boar sperm before and after freezing–thawing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXivVWktLY%3D&md5=2a49c99e47c4c0f934903021e7bfd878CAS | 18538515PubMed |
Kaarniranta, K., Elo, M., Sironen, R., Lammi, M. J., Goldring, M. B., Eriksson, J. E., Sistonen, L., and Helminen, H. J. (1998). Hsp70 accumulation in chondrocytic cells exposed to high continuous hydrostatic pressure coincides with mRNA stabilization rather than transcriptional activation. Proc. Natl. Acad. Sci. USA 95, 2319–2324.
| Hsp70 accumulation in chondrocytic cells exposed to high continuous hydrostatic pressure coincides with mRNA stabilization rather than transcriptional activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhsleit7g%3D&md5=4f40a662c3dac4c649a5f9a8847693e2CAS |
Kidson, A., Rubio-Pomar, F. J., Van Knegsel, A., Van Tol, H. T., Hazeleger, W., and Ducro-Steverink, D. W. (2004). Quality of porcine blastocysts produced in vitro in the presence or absence of GH. Reproduction 127, 165–177.
| Quality of porcine blastocysts produced in vitro in the presence or absence of GH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitVWrt70%3D&md5=0de71e17dcc663436a1b34bc5fe7e6d4CAS | 15056782PubMed |
Kirchhof, N., Carnwath, J. W., Lemme, E., Anastassiadis, K., Schöler, H., and Niemann, H. (2000). Expression pattern of Oct-4 in pre-implantation embryos of different species. Biol. Reprod. 63, 1698–1705.
| Expression pattern of Oct-4 in pre-implantation embryos of different species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVKhtrY%3D&md5=863842f823286619a97fcdd448ffb110CAS | 11090438PubMed |
Knijn, H. M., Wrenzycki, C., Hendriksen, P. J., Vos, P. L., Herrmann, D., van der Weijden, G. C., Niemann, H., and Dieleman, S. J. (2002). Effects of oocyte maturation regimen on the relative abundance of gene transcripts in bovine blastocysts derived in vitro or in vivo. Reproduction 124, 365–375.
| Effects of oocyte maturation regimen on the relative abundance of gene transcripts in bovine blastocysts derived in vitro or in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsV2ht7o%3D&md5=f1fc53410cba3315c5af151f40d11080CAS | 12201810PubMed |
Kültz, D. (2003). Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J. Exp. Biol. 206, 3119–3124.
| Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function.Crossref | GoogleScholarGoogle Scholar | 12909693PubMed |
Kuo, Y. H., Pribenszky, Cs., and Huang, S. Y. (2008). Higher litter size is achieved by the insemination of high hydrostatic pressure-treated frozen–thawed boar semen. Theriogenology 70, 1395–1396.
| Higher litter size is achieved by the insemination of high hydrostatic pressure-treated frozen–thawed boar semen.Crossref | GoogleScholarGoogle Scholar |
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 |
Leoni, G. G., Berlinguer, F., Succu, S., Bebbere, D., Mossa, F., Madeddu, M., Ledda, S., Bogliolo, L., and Naitana, S. (2008). A new selection criterion to assess good-quality ovine blastocysts after vitrification and to predict their transfer into recipients. Mol. Reprod. Dev. 75, 373–382.
| A new selection criterion to assess good-quality ovine blastocysts after vitrification and to predict their transfer into recipients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVCqug%3D%3D&md5=ec1e786012125d8ebceff3958bb9b750CAS | 17440971PubMed |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-Delta Delta CT. Method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2-Delta Delta CT. Method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=e0ea026c02920b4196beca401ea8984bCAS | 11846609PubMed |
Lonergan, P. (2007). State-of-the-art embryo technologies in cattle. Soc. Reprod. Fertil. Suppl. 64, 315–325.
| 1:STN:280:DC%2BD2s3otlKiuw%3D%3D&md5=fd996e76d0f70daa66a28bae89ab9bccCAS | 17491156PubMed |
Lonergan, P., Rizos, D., Gutiérrez-Adán, A., Fair, T., and Boland, M. P. (2003). Effect of culture environment on embryo quality and gene expression – experience from animal studies. Reprod. Biomed. Online 7, 657–663.
| Effect of culture environment on embryo quality and gene expression – experience from animal studies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2FkvFahsw%3D%3D&md5=27942f48e276dd6758eee451aace1715CAS | 14748964PubMed |
Luft, J. C, and Dix, D. J. (1999). Hsp70 expression and function during embryogenesis. Cell Stress Chaperones 4, 162–170.
| Hsp70 expression and function during embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXms1Whtb0%3D&md5=2d6d720eec5517ae1f691bf141dc27b4CAS | 10547065PubMed |
Melka, M. G., Rings, F., Hölker, M., Tholen, E., Havlicek, V., Besenfelder, U., Schellander, K., and Tesfaye, D. (2010). Expression of apoptosis regulatory genes and incidence of apoptosis in different morphological quality groups of in vitro-produced bovine pre-implantation embryos. Reprod. Domest. Anim. 45, 915–921.
| Expression of apoptosis regulatory genes and incidence of apoptosis in different morphological quality groups of in vitro-produced bovine pre-implantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSgtLbL&md5=d3921b72f699741e2bb2a8de57dbcf81CAS | 19392665PubMed |
Moussa, M., Tremoleda, J. L., Duchamp, G., Bruyas, J. F., Colenbrander, B., and Bevers, M. M. (2004). Evaluation of viability and apoptosis in horse embryos stored under different conditions at 5–8°C. Theriogenology 61, 921–932.
| Evaluation of viability and apoptosis in horse embryos stored under different conditions at 5–8°C.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2FlslWquw%3D%3D&md5=7926aaeed361c92786369611d605543eCAS | 14757477PubMed |
Pomar, F. J., Teerds, K. J., Kidson, A., Colenbrander, B., Tharasanit, T., Aguila, B., and Roelen, B. A. (2005). Differences in the incidence of apoptosis between in vivo- and in vitro-produced blastocysts of farm animal species: a comparative study. Theriogenology 63, 2254–2268.
| Differences in the incidence of apoptosis between in vivo- and in vitro-produced blastocysts of farm animal species: a comparative study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFyrtbg%3D&md5=094730150a1dbf3ac7905dd14f5d3ec8CAS | 15826688PubMed |
Pribenszky, C., and Vajta, G. (2010). Cells under pressure: how sublethal hydrostatic pressure stress treatment increases gametes’ and embryos’ performance? Reprod. Fertil. Dev. 23, 48–55.
| Cells under pressure: how sublethal hydrostatic pressure stress treatment increases gametes’ and embryos’ performance?Crossref | GoogleScholarGoogle Scholar |
Pribenszky, C., Molnár, M., Cseh, S., and Solti, L. (2005a). Improving post-thaw survival of cryopreserved mouse blastocysts by hydrostatic pressure challenge. Anim. Reprod. Sci. 87, 143–150.
| Improving post-thaw survival of cryopreserved mouse blastocysts by hydrostatic pressure challenge.Crossref | GoogleScholarGoogle Scholar | 15885447PubMed |
Pribenszky, C., Molnár, M., Ulrich, P., Barbosa, C., Hatamoto, L., and Santos, C. (2005b). Pressure assisted cryopreservation: a novel possibility for IVP bovine blastocyst cryopreservation. Reprod. Domest. Anim. 40, 338..
Pribenszky, C., Molnár, M., Horváth, A., Harnos, A., and Szenci, O. (2006). Hydrostatic pressure induced increase in post–thaw motility of frozen boar spermatozoa. Reprod. Fertil. Dev. 18, 162–163.
| Hydrostatic pressure induced increase in post–thaw motility of frozen boar spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Pribenszky, C., Molnár, M., Horváth, A., Kútvölgyi, G., Harnos, A., Szenci, O., Dengg, J., and Lederer, J. (2007). Improved post-thaw motility, viability and fertility are achieved by hydrostatic pressure-treated bull semen. Reprod. Fertil. Dev. 19, 181–182.
| Improved post-thaw motility, viability and fertility are achieved by hydrostatic pressure-treated bull semen.Crossref | GoogleScholarGoogle Scholar |
Pribenszky, C., Siquiera, E., Molnár, M., and Rumpf, R. (2008a). Improved post-warming developmental competence of open-pulled straw-vitrified in vitro-produced bovine blastocysts by sub-lethal hydrostatic pressure pre-treatment. Reprod. Fertil. Dev. 20, 125.
| Improved post-warming developmental competence of open-pulled straw-vitrified in vitro-produced bovine blastocysts by sub-lethal hydrostatic pressure pre-treatment.Crossref | GoogleScholarGoogle Scholar |
Pribenzsky, C., Du, Y., Molnár, M., and Vajta, G. (2008b). Sub-lethal stress on porcine oocytes enhances the efficacy of ART procedures. Hum. Reprod. 23, 161..
Pribenszky, C., Molnár, M., Kútvölgyi, G., Harnos, A., Horváth, A., and Héjja, I. (2009). Sub-lethal hydrostatic pressure treatment improves fresh and chilled boar semen quality in vitro and in vivo. Reprod. Fertil. Dev. 21, 107.
| Sub-lethal hydrostatic pressure treatment improves fresh and chilled boar semen quality in vitro and in vivo.Crossref | GoogleScholarGoogle Scholar |
Pribenszky, C., Vajta, G., Molnar, M., Du, Y., Lin, L., and Bolund, J. Y. (2010). Stress for stress tolerance? A fundamentally new approach in mammalian embryology. Biol. Reprod. 83, 690–697.
| Stress for stress tolerance? A fundamentally new approach in mammalian embryology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlGlsrfL&md5=39b1b328b40c31a18cdbe5133f697bc1CAS | 20554920PubMed |
Rizos, D., Fair, T., Papadopoulos, S., Boland, M. P., and Lonergan, P. (2002). Developmental, qualitative and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro. Mol. Reprod. Dev. 62, 320–327.
| Developmental, qualitative and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlWku7w%3D&md5=c059b816070193adca631f38aba19068CAS | 12112595PubMed |
Rizos, D., Gutiérrez-Adán, A., Pérez-Garnelo, S., de la Fuente, J., Boland, M. P., and Lonergan, P. (2003). Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance and messenger RNA expression. Biol. Reprod. 68, 236–243.
| Bovine embryo culture in the presence or absence of serum: implications for blastocyst development, cryotolerance and messenger RNA expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFWj&md5=015f202f8f190c52ac233569fc70d98eCAS | 12493719PubMed |
Rizos, D., Gutierrez-Adan, A., Moreira, P., O’Meara, C., Fair, T., Evans, A. C., Boland, M. P., and Lonergan, P. (2004). Species-related differences in blastocyst quality are associated with differences in relative mRNA transcription. Mol. Reprod. Dev. 69, 381–386.
| Species-related differences in blastocyst quality are associated with differences in relative mRNA transcription.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpvFOluro%3D&md5=1dc584f8665de0a0fdfb4eead96822a5CAS | 15457517PubMed |
Saijoh, Y., Fujii, H., Men, C., Sato, M., Hirota, Y., Nagamatsu, S., Ikeda, M., and Hamada, H. (1996). Identification of putative downstream genes of Oct-3, a pluripotent cell-specific transcription factor. Genes Cells 1, 239–252.
| 1:CAS:528:DyaK28XksFWgs7k%3D&md5=c4e17c09d2dea9c9eeb1184e659c7cf8CAS | 9140067PubMed |
Schöler, H. R. (1991). Octamania: the POU factors in murine development. Trends Genet. 7, 323–329.
| 1781030PubMed |
Siqueira, F. E., Caixeta, E. S., Molnár, M., Pribenszky, C., Franco, M. M., and Rumpf, R. (2009). Sub-lethal hydrostatic pressure pre-treatment: effect in bovine embryos gene expression. Biol. Reprod. 81, 629..
Söti, C., and Csermely, P. (2007). Protein stress and stress proteins: implications in ageing and disease. J. Biosci. 32, 511–515.
| Protein stress and stress proteins: implications in ageing and disease.Crossref | GoogleScholarGoogle Scholar | 17536170PubMed |
Succu, S., Bebbere, D., Bogliolo, L., Ariu, F., Fois, S., Leoni, G. G., Berlinguer, F., Naitana, S., and Ledda, S. (2008). Vitrification of in vitro-matured ovine oocytes affects in vitro pre-implantation development and mRNA abundance. Mol. Reprod. Dev. 75, 538–546.
| Vitrification of in vitro-matured ovine oocytes affects in vitro pre-implantation development and mRNA abundance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhs1Crsrk%3D&md5=c9dea223094b106fa6fa09aee65c9858CAS | 17886274PubMed |
Thompson, J. G. (1997). Comparison between in vivo-derived and in vitro-produced pre-elongation embryos from domestic ruminants. Reprod. Fertil. Dev. 9, 341–354.
| Comparison between in vivo-derived and in vitro-produced pre-elongation embryos from domestic ruminants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svgsFaisA%3D%3D&md5=2af72ca7c7ae3b5b3b4bab6c955f2ac2CAS | 9261882PubMed |
Walker, S. K., Hill, J. L., Kleemann, D. O., and Nancarrow, C. D. (1996). Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations. Biol. Reprod. 55, 703–708.
| Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltlKgurw%3D&md5=13ea7aa0154cd7c0c2acc5fcf9bf46caCAS | 8862790PubMed |
Wang, P., Shu, Z., He, L., Cui, X., Wang, Y., and Gao, D. (2005). The pertinence of expression of heat shock proteins (HSPs) to the efficacy of cryopreservation in HELAs. Cryo Lett. 26, 7–16.
Welch, T. J., Farewell, A., Neidhardt, F. C., and Bartlett, D. H. (1993). Stress response of Escherichia coli to elevated hydrostatic pressure. J. Bacteriol. 175, 7171–7177.
Wemekamp-Kamphuis, H. H., Karatzas, A. K., Wouters, J. A., and Abee, T. (2002). Enhanced levels of cold-shock proteins in Listeria monocytogenes LO28 upon exposure to low temperature and high hydrostatic pressure. Appl. Environ. Microbiol. 68, 456–463.
| Enhanced levels of cold-shock proteins in Listeria monocytogenes LO28 upon exposure to low temperature and high hydrostatic pressure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtV2gtbc%3D&md5=ed334437703f510578263c62fceea683CAS | 11823178PubMed |
Wrenzycki, C., Herrmann, D., Carnwath, J. W., and Niemann, H. (1999). Alterations in the relative abundance of gene transcripts in pre-implantation bovine embryos cultured in medium supplemented with either serum or PVA. Mol. Reprod. Dev. 53, 8–18.
| Alterations in the relative abundance of gene transcripts in pre-implantation bovine embryos cultured in medium supplemented with either serum or PVA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitleju7s%3D&md5=1a411bbbee8e665fb728141b77ab215cCAS | 10230812PubMed |
Wrenzycki, C., Herrmann, D., Keskintepe, L., Martins, A., Sirisathien, S., Brackett, B., and Niemann, H. (2001). Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos. Hum. Reprod. 16, 893–901.
| Effects of culture system and protein supplementation on mRNA expression in pre-implantation bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Cqs74%3D&md5=8f19df08ce927b044a8f697385152bc0CAS | 11331635PubMed |
Wrenzycki, C., Herrmann, D., and Niemann, H. (2003). Timing of blastocyst expansion affects spatial messenger RNA expression patterns of genes in bovine blastocysts produced in vitro. Biol. Reprod. 68, 2073–2080.
| Timing of blastocyst expansion affects spatial messenger RNA expression patterns of genes in bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1GgsLw%3D&md5=4e298d20e0c9d24ff59f89094ff5d880CAS | 12606328PubMed |
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 |
Zuccotti, M., Merico, V., Sacchi, L., Bellone, M., Brink, T. C., Bellazzi, R., Stefanelli, M., Redi, C. A., Garagna, S., and Adjaye, J. (2008). Maternal Oct-4 is a potential key regulator of the developmental competence of mouse oocytes. BMC Dev. Biol. 6, 88–97.
