Regulation of heat-inducible HSPA1A gene expression during maternal-to-embryo transition and in response to heat in in vitro-produced bovine embryos
Jean-Marc Lelièvre A E G , Nathalie Peynot A , Sylvie Ruffini A , Ludivine Laffont A , Daniel Le Bourhis A B F , Pierre-Marie Girard C D and Véronique Duranthon A
+ Author Affiliations
- Author Affiliations
A UMR BDR, INRA, ENVA, Université Paris Saclay, 78350 Jouy-en-Josas, France.
B UNCEIA R&D, 13 Rue Jouët, 94704 Maisons-Alfort, France.
C Institut Curie, PSL Research University, CNRS UMR3347, INSERM U1021, 91405 Orsay, France.
D Université Paris-Sud, Université Paris-Saclay, Rue Georges Clémenceau, 91405 Orsay, France.
E Present address: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, France.
F Present address: Biotechnologie de l’Embryon, Allice, Station de Phénotypage, 37380 Nouzilly, France.
G Corresponding author. Email: jean-marc.lelievre@inra.fr
Reproduction, Fertility and Development 29(9) 1868-1881 https://doi.org/10.1071/RD15504
Submitted: 1 December 2015 Accepted: 12 October 2016 Published: 17 November 2016
Abstract
In in vitro-produced (IVP) bovine embryos, a burst in transcriptional activation of the embryonic genome (EGA) occurs at the 8–16-cell stage. To examine transcriptional regulation prior to EGA, notably in response to heat stress, we asked (1) whether the spontaneous expression of a luciferase transgene that is driven by the minimal mouse heat-shock protein 1b (hspa1b) gene promoter paralleled that of HSPA1A during EGA in IVP bovine embryo and (2) whether expression of the endogenous heat-inducible iHSPA group member HSPA1A gene and the hspa1b/luciferase transgene were induced by heat stress (HS) prior to EGA. Using two culture systems, we showed that luciferase activity levels rose during the 40-h long EGA-associated cell cycle. In contrast, iHSPA proteins were abundant in matured oocytes and in blastomeres from the two-cell to the 16-cell stages. However, normalised results detected a rise in the level of HSPA1A and luciferase mRNA during EGA, when transcription was required for their protein expression. Prior to EGA, HS-induced premature luciferase activity and transgene expression were clearly inhibited. We could not, however, establish whether this was also true for HSPA1A expression because of the decay of the abundant maternal transcripts prior to EGA. In bovine embryos, heat-induced expression of hspa1b/luciferase, and most likely of HSPA1A, was therefore strictly dependent on EGA. The level of the heat-shock transcription factor 1 molecules that were found in cell nuclei during embryonic development correlated better with the embryo’s capacity for heat-shock response than with EGA-associated gene expression.
Additional keywords: gene regulation, preimplantation, stress.
References
Anckar, J., and Sistonen, L. (2011). Regulation of HSF1 function in the heat stress response: implications in aging and disease. Annu. Rev. Biochem. 80, 1089–1115.| Regulation of HSF1 function in the heat stress response: implications in aging and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptVCntrc%3D&md5=688b03597b0e14261947850b507fdb1dCAS |
Angulo, L., Guyader-Joly, C., Auclair, S., Hennequet-Antier, C., Papillie, P., Boussaha, M., Fritz, S., Hugot, K., Moreews, F., Ponsart, C., Humblot, P., and Dalbies-Tran, R. (2016). An integrated approach to bovine oocyte quality: from phenotype to genes. Reprod. Fertil. Dev. 80, 1089–1115.
| An integrated approach to bovine oocyte quality: from phenotype to genes.Crossref | GoogleScholarGoogle Scholar |
Barnes, F. L., and First, N. L. (1991). Embryonic transcription in in vitro cultured bovine embryos. Mol. Reprod. Dev. 29, 117–123.
| Embryonic transcription in in vitro cultured bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFWhurs%3D&md5=027e04fbc879d77e99ab5b40807cf509CAS |
Bellier, S., Chastant, S., Adenot, P., Vincent, M., Renard, J. P., and Bensaude, O. (1997). Nuclear translocation and carboxyl-terminal domain phosphorylation of RNA polymerase II delineate the two phases of zygotic gene activation in mammalian embryos. EMBO J. 16, 6250–6262.
| Nuclear translocation and carboxyl-terminal domain phosphorylation of RNA polymerase II delineate the two phases of zygotic gene activation in mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnt1artb8%3D&md5=980ecccc79ead9e06bfdb3381d157e53CAS |
Bensaude, O., Babinet, C., Morange, M., and Jacob, F. (1983). Heat shock proteins, first major products of zygotic gene activity in mouse embryo. Nature 305, 331–333.
| Heat shock proteins, first major products of zygotic gene activity in mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlsFGqtb0%3D&md5=d70f76b5ceae37d278672efc369922ffCAS |
Bettegowda, A., Lee, K. B., and Smith, G. W. (2008). Cytoplasmic and nuclear determinants of the maternal-to-embryonic transition. Reprod. Fertil. Dev. 20, 45–53.
| Cytoplasmic and nuclear determinants of the maternal-to-embryonic transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFCis7Y%3D&md5=ea1a949841a48e5dcad48886c23c5138CAS |
Bevilacqua, A., Fiorenza, M. T., and Mangia, F. (2000). A developmentally regulated GAGA box-binding factor and Sp1 are required for transcription of the hsp70.1 gene at the onset of mouse zygotic genome activation. Development 127, 1541–1551.
| 1:CAS:528:DC%2BD3cXjtFWmsbs%3D&md5=d75ab0fd8079a620e22346b8f493a36bCAS |
Bierkamp, C., Luxey, M., Metchat, A., Audouard, C., Dumollard, R., and Christians, E. (2010). Lack of maternal heat shock factor 1 results in multiple cellular and developmental defects, including mitochondrial damage and altered redox homeostasis, and leads to reduced survival of mammalian oocytes and embryos. Dev. Biol. 339, 338–353.
| Lack of maternal heat shock factor 1 results in multiple cellular and developmental defects, including mitochondrial damage and altered redox homeostasis, and leads to reduced survival of mammalian oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1ajurY%3D&md5=a670d95332d0abe251732bf1ae742a0eCAS |
Breton, A., Le Bourhis, D., Audouard, C., Vignon, X., and Lelièvre, J. M. (2010). Nuclear profiles of H3 histones trimethylated on Lys27 in bovine (Bos taurus) embryos obtained after in vitro fertilization or somatic cell nuclear transfer. J. Reprod. Dev. 56, 379–388.
| Nuclear profiles of H3 histones trimethylated on Lys27 in bovine (Bos taurus) embryos obtained after in vitro fertilization or somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar |
Camous, S., Heyman, Y., Meziou, W., and Menezo, Y. (1984). Cleavage beyond the block stage and survival after transfer of early bovine embryos cultured with trophoblastic vesicles. J. Reprod. Fertil. 72, 479–485.
| Cleavage beyond the block stage and survival after transfer of early bovine embryos cultured with trophoblastic vesicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2M%2Fot1ygtw%3D%3D&md5=91e98bcf5b9f59c48ee74ea8aedef4b7CAS |
Camous, S., Kopecny, V., and Flechon, J. E. (1986). Autoradiographic detection of the earliest stage of [3H]-uridine incorporation into the cow embryo. Biol. Cell 58, 195–200.
| Autoradiographic detection of the earliest stage of [3H]-uridine incorporation into the cow embryo.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s7osF2lsQ%3D%3D&md5=14dfb7f93e4eef71f96afba294090bc3CAS |
Chandolia, R. K., Peltier, M. R., Tian, W., and Hansen, P. J. (1999). Transcriptional control of development, protein synthesis, and heat-induced heat shock protein 70 synthesis in 2-cell bovine embryos. Biol. Reprod. 61, 1644–1648.
| Transcriptional control of development, protein synthesis, and heat-induced heat shock protein 70 synthesis in 2-cell bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns1ynt7k%3D&md5=484b06ad4e61c7b89765dd7638f465bdCAS |
Christians, E., Campion, E., Thompson, E. M., and Renard, J. P. (1995). Expression of the HSP 70.1 gene, a landmark of early zygotic activity in the mouse embryo, is restricted to the first burst of transcription. Development 121, 113–122.
| 1:CAS:528:DyaK2MXjtlentLc%3D&md5=97d123258f31a74acc7a7dba18dd7ec0CAS |
Christians, E., Michel, E., Adenot, P., Mezger, V., Rallu, M., Morange, M., and Renard, J. P. (1997). Evidence for the involvement of mouse heat shock factor 1 in the atypical expression of the HSP70.1 heat shock gene during mouse zygotic genome activation. Mol. Cell. Biol. 17, 778–788.
| Evidence for the involvement of mouse heat shock factor 1 in the atypical expression of the HSP70.1 heat shock gene during mouse zygotic genome activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmvVKjtQ%3D%3D&md5=07b1e8ec38e71dee4303b5e853246715CAS |
Edwards, J. L., Ealy, A. D., Monterroso, V. H., and Hansen, P. J. (1997). Ontogeny of temperature-regulated heat shock protein 70 synthesis in preimplantation bovine embryos. Mol. Reprod. Dev. 48, 25–33.
| Ontogeny of temperature-regulated heat shock protein 70 synthesis in preimplantation bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlt1SisrY%3D&md5=f833fc7d7548ee2bd98883701c838b49CAS |
Fear, J. M., and Hansen, P. J. (2011). Developmental changes in expression of genes involved in regulation of apoptosis in the bovine preimplantation embryo. Biol. Reprod. 84, 43–51.
| Developmental changes in expression of genes involved in regulation of apoptosis in the bovine preimplantation embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlvVegtbg%3D&md5=b804be9944fca306b03c015228aafbbbCAS |
Fiorenza, M. T., Bevilacqua, A., Canterini, S., Torcia, S., Pontecorvi, M., and Mangia, F. (2004). Early transcriptional activation of the hsp70.1 gene by osmotic stress in one-cell embryos of the mouse. Biol. Reprod. 70, 1606–1613.
| Early transcriptional activation of the hsp70.1 gene by osmotic stress in one-cell embryos of the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOmsbk%3D&md5=c927fc39c10841d77f98a0ab39941ed3CAS |
Frei, R. E., Schultz, G. A., and Church, R. B. (1989). Qualitative and quantitative changes in protein synthesis occur at the 8–16-cell stage of embryogenesis in the cow. J. Reprod. Fertil. 86, 637–641.
| Qualitative and quantitative changes in protein synthesis occur at the 8–16-cell stage of embryogenesis in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkslGgtrk%3D&md5=303e52c7b31c74c25618c58175f04f2fCAS |
Gilda, J. E., and Gomes, A. V. (2013). Stain-free total protein staining is a superior loading control to β-actin for western blots. Anal. Biochem. 440, 186–188.
| Stain-free total protein staining is a superior loading control to β-actin for western blots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1aqsLjK&md5=10bd5d96d5de4e4858670b52628723a5CAS |
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 |
Graf, A., Krebs, S., Zakhartchenko, V., Schwalb, B., Blum, H., and Wolf, E. (2014). Fine mapping of genome activation in bovine embryos by RNA sequencing. Proc. Natl. Acad. Sci. USA 111, 4139–4144.
| Fine mapping of genome activation in bovine embryos by RNA sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtlyhsrs%3D&md5=cf905f517802a0ee07f0e56c0b5298f0CAS |
Hansen, P. J. (2007). To be or not to be – determinants of embryonic survival following heat shock. Theriogenology 68, S40–S48.
| To be or not to be – determinants of embryonic survival following heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlaiurw%3D&md5=e4505a8045cc2089beaff348fcac36f5CAS |
Harvey, S. A., Sealy, I., Kettleborough, R., Fenyes, F., White, R., Stemple, D., and Smith, J. C. (2013). Identification of the zebrafish maternal and paternal transcriptomes. Development 140, 2703–2710.
| Identification of the zebrafish maternal and paternal transcriptomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1OmsbbP&md5=7ede49e350982ead0704357c64176d83CAS |
Hellemans, J., Mortier, G., De Paepe, A., Speleman, F., and Vandesompele, J. (2007). qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.
| qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data.Crossref | GoogleScholarGoogle Scholar |
Holm, P., Booth, P. J., Schmidt, M. H., Greve, T., and 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, 683–700.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7pvVGnsw%3D%3D&md5=5d4c5f6302122967eb232c091decd402CAS |
Holm, P., Booth, P. J., and Callesen, H. (2002). Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media. Reproduction 123, 553–565.
| Kinetics of early in vitro development of bovine in vivo- and in vitro-derived zygotes produced and/or cultured in chemically defined or serum-containing media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFGhtbs%3D&md5=020d6f2fafcd3d7d299ea364ed04468cCAS |
Kampinga, H. H., Hageman, J., Vos, M. J., Kubota, H., Tanguay, R. M., Bruford, E. A., Cheetham, M. E., Chen, B., and Hightower, L. E. (2009). Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaperones 14, 105–111.
| Guidelines for the nomenclature of the human heat shock proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVyktLk%3D&md5=9e63a1b127764ef6c5d9677be6ae382eCAS |
Kaňka, J., Kepkova, K., and Nemcova, L. (2009). Gene expression during minor genome activation in preimplantation bovine development. Theriogenology 72, 572–583.
| Gene expression during minor genome activation in preimplantation bovine development.Crossref | GoogleScholarGoogle Scholar |
Kawarsky, S. J., and King, W. A. (2001). Expression and localisation of heat shock protein 70 in cultured bovine oocytes and embryos. Zygote 9, 39–50.
| Expression and localisation of heat shock protein 70 in cultured bovine oocytes and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvVygsrs%3D&md5=237f0e4262bb49d7361f743d4baafcd9CAS |
Kettleborough, R. N., Busch-Nentwich, E. M., Harvey, S. A., Dooley, C. M., de Bruijn, E., van Eeden, F., Sealy, I., White, R. J., Herd, C., Nijman, I. J., Fenyes, F., Mehroke, S., Scahill, C., Gibbons, R., Wali, N., Carruthers, S., Hall, A., Yen, J., Cuppen, E., and Stemple, D. L. (2013). A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature 496, 494–497.
| A systematic genome-wide analysis of zebrafish protein-coding gene function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvF2jsLk%3D&md5=3f85feec06c74efbf920da3b8e8cd2dfCAS |
Khan, D. R., Dube, D., Gall, L., Peynot, N., Ruffini, S., Laffont, L., Le Bourhis, D., Degrelle, S., Jouneau, A., and Duranthon, V. (2012). Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo. PLoS One 7, e34110.
| Expression of pluripotency master regulators during two key developmental transitions: EGA and early lineage specification in the bovine embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlsFamsbk%3D&md5=6ad39d63e8dea8cad62e4b5b4767052cCAS |
King, W. A., Niar, A., Chartrain, I., Betteridge, K. J., and Guay, P. (1988). Nucleolus organizer regions and nucleoli in preattachment bovine embryos. J. Reprod. Fertil. 82, 87–95.
| Nucleolus organizer regions and nucleoli in preattachment bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c7hvVGqsQ%3D%3D&md5=2d224817c6d3ed5b2a1772b73242a443CAS |
Kopecny, V. (1989). High-resolution autoradiographic studies of comparative nucleologenesis and genome reactivation during early embryogenesis in pig, man and cattle. Reprod. Nutr. Dev. 29, 589–600.
| High-resolution autoradiographic studies of comparative nucleologenesis and genome reactivation during early embryogenesis in pig, man and cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c7gsVGmug%3D%3D&md5=3c996bf99c9933b17068508db225a204CAS |
Ladner, C. L., Yang, J., Turner, R. J., and Edwards, R. A. (2004). Visible fluorescent detection of proteins in polyacrylamide gels without staining. Anal. Biochem. 326, 13–20.
| Visible fluorescent detection of proteins in polyacrylamide gels without staining.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtV2hsbw%3D&md5=bd2ba56f8fdc20a064adf0ed9fbbeb8fCAS |
Leese, H. J. (2015). History of oocyte and embryo metabolism. Reprod. Fertil. Dev. 27, 567– .
| History of oocyte and embryo metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntVWnurg%3D&md5=8eaa8c159a12b234d6eb86845e861b8dCAS |
Lelièvre, J. M., Le Bourhis, D., Breton, A., Hayes, H., Servely, J. L., and Vignon, X. (2010). Heat-induced and spontaneous expression of Hsp70.1Luciferase transgene copies localized on Xp22 in female bovine cells. BMC Res. Notes 3, 17.
| Heat-induced and spontaneous expression of Hsp70.1Luciferase transgene copies localized on Xp22 in female bovine cells.Crossref | GoogleScholarGoogle Scholar |
Le Masson, F., and Christians, E. (2011). HSFs and regulation of Hsp70.1 (Hspa1b) in oocytes and preimplantation embryos: new insights brought by transgenic and knockout mouse models. Cell Stress Chaperones 16, 275–285.
| HSFs and regulation of Hsp70.1 (Hspa1b) in oocytes and preimplantation embryos: new insights brought by transgenic and knockout mouse models.Crossref | GoogleScholarGoogle Scholar |
Lequarre, A. S., Marchandise, J., Moreau, B., Massip, A., and Donnay, I. (2003). Cell cycle duration at the time of maternal zygotic transition for in vitro produced bovine embryos: effect of oxygen tension and transcription inhibition. Biol. Reprod. 69, 1707–1713.
| Cell cycle duration at the time of maternal zygotic transition for in vitro produced bovine embryos: effect of oxygen tension and transcription inhibition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosV2rs70%3D&md5=f3c25e0470dc9c5524c82e2c954b974aCAS |
Memili, E., and First, N. L. (2000). Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.
| Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjvVemtLo%3D&md5=a36eeb97082ea7d3757a2a74c0008e5bCAS |
Menck, M., Mercier, Y., Campion, E., Lobo, R. B., Heyman, Y., Renard, J. P., and Thompson, E. M. (1998). Prediction of transgene integration by noninvasive bioluminescent screening of microinjected bovine embryos. Transgenic Res. 7, 331–342.
| Prediction of transgene integration by noninvasive bioluminescent screening of microinjected bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVOktLg%3D&md5=82cb72001377a9c64cc8229aece3f00bCAS |
Metchat, A., Akerfelt, M., Bierkamp, C., Delsinne, V., Sistonen, L., Alexandre, H., and Christians, E. S. (2009). Mammalian heat shock factor 1 is essential for oocyte meiosis and directly regulates Hsp90alpha expression. J. Biol. Chem. 284, 9521–9528.
| Mammalian heat shock factor 1 is essential for oocyte meiosis and directly regulates Hsp90alpha expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjs1ymsbg%3D&md5=c38cade97223760b073b545e084d4046CAS |
Misirlioglu, M., Page, G. P., Sagirkaya, H., Kaya, A., Parrish, J. J., First, N. L., and Memili, E. (2006). Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos. Proc. Natl. Acad. Sci. USA 103, 18905–18910.
| Dynamics of global transcriptome in bovine matured oocytes and preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlChu77M&md5=7310cc0a7dc48dc0c94406d956c2a2f5CAS |
Neil, M. A., Juskaitis, R., and Wilson, T. (1997). Method of obtaining optical sectioning by using structured light in a conventional microscope. Opt. Lett. 22, 1905–1907.
| Method of obtaining optical sectioning by using structured light in a conventional microscope.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2FisVCitA%3D%3D&md5=52dd99016f40860fa2acf746ee824a74CAS |
O’Regan, L., Sampson, J., Richards, M. W., Knebel, A., Roth, D., Hood, F. E., Straube, A., Royle, S. J., Bayliss, R., and Fry, A. M. (2015). Hsp72 is targeted to the mitotic spindle by Nek6 to promote K-fiber assembly and mitotic progression. J. Cell Biol. 209, 349–358.
| Hsp72 is targeted to the mitotic spindle by Nek6 to promote K-fiber assembly and mitotic progression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXoslaiu7g%3D&md5=3b0256d7539c660925b658f7ed255fc8CAS |
Place, R. F., and Noonan, E. J. (2014). Non-coding RNAs turn up the heat: an emerging layer of novel regulators in the mammalian heat shock response. Cell Stress Chaperones 19, 159–172.
| Non-coding RNAs turn up the heat: an emerging layer of novel regulators in the mammalian heat shock response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtlKjtL0%3D&md5=7fd8eb4cd89bb804885e98efbabfd1a7CAS |
Ponter, A. A., Guyader-Joly, C., Nuttinck, F., Grimard, B., and Humblot, P. (2012). Oocyte and embryo production and quality after OPU-IVF in dairy heifers given diets varying in their n-6/n-3 fatty acid ratio. Theriogenology 78, 632–645.
| Oocyte and embryo production and quality after OPU-IVF in dairy heifers given diets varying in their n-6/n-3 fatty acid ratio.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtFertrk%3D&md5=ff6299ab942fc16270a5dbff2f1a21b5CAS |
Rivera, R. M., and Hansen, P. J. (2001). Development of cultured bovine embryos after exposure to high temperatures in the physiological range. Reproduction 121, 107–115.
| Development of cultured bovine embryos after exposure to high temperatures in the physiological range.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslarsQ%3D%3D&md5=fba46932c2853abb183769d85e7a935cCAS |
Robertson, I., and Nelson, R. E. (1998). Certification and identification of the embryo. In ‘Manual of the International Embryo Transfer Society’. 3rd edn. (Eds D. A. Stringfellow and S. M. Seidel.) pp. 103–116. (IETS: Savoy, IL, USA.)
Sakatani, M., Alvarez, N. V., Takahashi, M., and Hansen, P. J. (2012). Consequences of physiological heat shock beginning at the zygote stage on embryonic development and expression of stress response genes in cattle. J. Dairy Sci. 95, 3080–3091.
| Consequences of physiological heat shock beginning at the zygote stage on embryonic development and expression of stress response genes in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xntlyrtrc%3D&md5=28ee04b866e6d138568cb8d2dfea2447CAS |
Sendler, E., Johnson, G. D., Mao, S., Goodrich, R. J., Diamond, M. P., Hauser, R., and Krawetz, S. A. (2013). Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Res. 41, 4104–4117.
| Stability, delivery and functions of human sperm RNAs at fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVKitr8%3D&md5=bd9acad32b2d14c293f9bab146b8fa19CAS |
Sirard, M. A. (2010). Activation of the embryonic genome. Soc. Reprod. Fertil. Suppl. 67, 145–158.
| 1:STN:280:DC%2BC3MnosFeguw%3D%3D&md5=a3fbcf91ba025284092bb0f5bc3979ccCAS |
Tadros, W., and Lipshitz, H. D. (2009). The maternal-to-zygotic transition: a play in two acts. Development 136, 3033–3042.
| The maternal-to-zygotic transition: a play in two acts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSisbfM&md5=ef7f95cfea1d7ffebcae3f4b98b971b0CAS |
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=1f6d12b4e2402266f8af16a4a2f4f58dCAS |
Thompson, J. G., and Peterson, A. J. (2000). Bovine embryo culture in vitro: new developments and post-transfer consequences. Hum. Reprod. 15, 59–67.
| Bovine embryo culture in vitro: new developments and post-transfer consequences.Crossref | GoogleScholarGoogle Scholar |
Thompson, E. M., Christians, E., Stinnakre, M. G., and Renard, J. P. (1994). Scaffold attachment regions stimulate HSP70.1 expression in mouse preimplantation embryos but not in differentiated tissues. Mol. Cell. Biol. 14, 4694–4703.
| Scaffold attachment regions stimulate HSP70.1 expression in mouse preimplantation embryos but not in differentiated tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXkslGiu7s%3D&md5=ca28c95cbbf284fb0752144c377868ceCAS |
Vabulas, R. M., Raychaudhuri, S., Hayer-Hartl, M., and Hartl, F. U. (2010). Protein folding in the cytoplasm and the heat shock response. Cold Spring Harb. Perspect. Biol. 2, a004390.
| Protein folding in the cytoplasm and the heat shock response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKqt7c%3D&md5=cd70bc1067cfeb702a1b8990d5f76f2eCAS |
Vigneault, C., Gravel, C., Vallee, M., McGraw, S., and Sirard, M. A. (2009). Unveiling the bovine embryo transcriptome during the maternal-to-embryonic transition. Reproduction 137, 245–257.
| Unveiling the bovine embryo transcriptome during the maternal-to-embryonic transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovV2ksL8%3D&md5=a3093644ae8b6a7abc5dce51b47ba0fbCAS |
Voellmy, R., and Rungger, D. (1982). Transcription of a Drosophila heat shock gene is heat-induced in Xenopus oocytes. Proc. Natl. Acad. Sci. USA 79, 1776–1780.
| Transcription of a Drosophila heat shock gene is heat-induced in Xenopus oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhslGhtbs%3D&md5=d47a2d5f152bc3c9e7c33ff157efddc4CAS |
Vujanac, M., Fenaroli, A., and Zimarino, V. (2005). Constitutive nuclear import and stress-regulated nucleocytoplasmic shuttling of mammalian heat-shock factor 1. Traffic 6, 214–229.
| Constitutive nuclear import and stress-regulated nucleocytoplasmic shuttling of mammalian heat-shock factor 1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit1Srs7g%3D&md5=9df62a03069a888884c0a334f62ca8c0CAS |
Westerheide, S. D., Raynes, R., Powell, C., Xue, B., and Uversky, V. N. (2012). HSF transcription factor family, heat shock response, and protein intrinsic disorder. Curr. Protein Pept. Sci. 13, 86–103.
| HSF transcription factor family, heat shock response, and protein intrinsic disorder.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFamtLo%3D&md5=55c5d297fd226cb49f817be634c7882eCAS |
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=39b64c8d36589b766dfbb4ac4c16b14cCAS |
Xue, Z., Huang, K., Cai, C., Cai, L., Jiang, C. Y., Feng, Y., Liu, Z., Zeng, Q., Cheng, L., Sun, Y. E., Liu, J. Y., Horvath, S., and Fan, G. (2013). Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500, 593–597.
| Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFygsLrL&md5=96ec4ec239db965ca363bfaa78fcb2fdCAS |
Zeng, F., and Schultz, R. M. (2005). RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Dev. Biol. 283, 40–57.
| RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFGitL8%3D&md5=9dae545504bce2987d8074e22b7b022cCAS |
