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

Actions of activin A, connective tissue growth factor, hepatocyte growth factor and teratocarcinoma-derived growth factor 1 on the development of the bovine preimplantation embryo

Jasmine Kannampuzha-Francis A , Paula Tribulo A and Peter J. Hansen A B
+ Author Affiliations
- Author Affiliations

A Department of Animal Sciences, D.H. Barron Reproductive and Perinatal Biology Research Program, and Genetics Institute, University of Florida, Gainesville, FL32611-0910, USA.

B Corresponding author. Email: hansen@animal.ufl.edu

Reproduction, Fertility and Development 29(7) 1329-1339 https://doi.org/10.1071/RD16033
Submitted: 19 January 2016  Accepted: 20 April 2016   Published: 17 May 2016

Abstract

The reproductive tract secretes bioactive molecules collectively known as embryokines that can regulate embryonic growth and development. In the present study we tested four growth factors expressed in the endometrium for their ability to modify the development of the bovine embryo to the blastocyst stage and alter the expression of genes found to be upregulated (bone morphogenetic protein 15 (BMP15) and keratin 8, type II (KRT8)) or downregulated (NADH dehydrogenase 1 (ND1) and S100 calcium binding protein A10 (S100A10)) in embryos competent to develop to term. Zygotes were treated at Day 5 with 0.01, 0.1 or 1.0 nM growth factor. The highest concentration of activin A increased the percentage of putative zygotes that developed to the blastocyst stage. Connective tissue growth factor (CTGF) increased the number of cells in the inner cell mass (ICM), decreased the trophectoderm : ICM ratio and increased blastocyst expression of KRT8 and ND1. The lowest concentration of hepatocyte growth factor (HGF) reduced the percentage of putative zygotes becoming blastocysts. Teratocarcinoma-derived growth factor 1 increased total cell number at 0.01 nM and expression of S100A10 at 1.0 nM, but otherwise had no effects. Results confirm the prodevelopmental actions of activin A and indicate that CTGF may also function as an embryokine by regulating the number of ICM cells in the blastocyst and altering gene expression. Low concentrations of HGF were inhibitory to development.

Additional keywords: blastocyst, embryokine, gene expression, inner cell mass, trophectoderm.


References

Aasrum, M., Ødegård, J., Thoresen, G. H., Brusevold, I. J., Sandnes, D. L., and Christoffersen, T. (2015). Gab1 amplifies signaling in response to low-intensity stimulation by HGF. Cell Biol. Int. 39, 1177–1184.
Gab1 amplifies signaling in response to low-intensity stimulation by HGF.CrossRef | 1:CAS:528:DC%2BC2MXhsFejtb3M&md5=56d5e984a5532f76f70c86dee183f36cCAS | 26146811PubMed | open url image1

Ahlström, A., Westin, C., Reismer, E., Wikland, M., and Hardarson, T. (2011). Trophectoderm morphology: an important parameter for predicting live birth after single blastocyst transfer. Hum. Reprod. 26, 3289–3296.
Trophectoderm morphology: an important parameter for predicting live birth after single blastocyst transfer.CrossRef | 21972253PubMed | open url image1

Betteridge, K. J., and Fléchon, J. E. (1988). The anatomy and physiology of pre-attachment bovine embryos. Theriogenology 29, 155–187.
The anatomy and physiology of pre-attachment bovine embryos.CrossRef | open url image1

Block, J., and Hansen, P. J. (2007). Interaction between season and culture with insulin-like growth factor-1 on survival of in vitro produced embryos following transfer to lactating dairy cows. Theriogenology 67, 1518–1529.
Interaction between season and culture with insulin-like growth factor-1 on survival of in vitro produced embryos following transfer to lactating dairy cows.CrossRef | 1:CAS:528:DC%2BD2sXkvFGgtLw%3D&md5=d0f620b62d78da504fb7cf7520fd4fd9CAS | 17452048PubMed | open url image1

Block, J., Fischer-Brown, A. E., Rodina, T. M., Ealy, A. D., and Hansen, P. J. (2007). The effect of in vitro treatment of bovine embryos with IGF-1 on subsequent development in utero to Day 14 of gestation. Theriogenology 68, 153–161.
The effect of in vitro treatment of bovine embryos with IGF-1 on subsequent development in utero to Day 14 of gestation.CrossRef | 1:CAS:528:DC%2BD2sXmsFKgsL4%3D&md5=a8ddae963fc1e9b83b3fec1878f683ceCAS | 17532038PubMed | open url image1

Bonilla, A. Q., Ozawa, M., and Hansen, P. J. (2011). Timing and dependence upon mitogen-activated protein kinase signaling for pro-developmental actions of insulin-like growth factor 1 on the preimplantation bovine embryo. Growth Horm. IGF Res. 21, 107–111.
Timing and dependence upon mitogen-activated protein kinase signaling for pro-developmental actions of insulin-like growth factor 1 on the preimplantation bovine embryo.CrossRef | 1:CAS:528:DC%2BC3MXlsFamtbs%3D&md5=9a83ae31121df3e4ee1853401f7f98c9CAS | 21459028PubMed | open url image1

Brigstock, D. R., Steffen, C. L., Kim, G. Y., Vegunta, R. K., Diehl, J. R., and Harding, P. A. (1997). Purification and characterization of novel heparin-binding growth factors in uterine secretory fluids: identification as heparin-regulated Mr 10,000 forms of connective tissue growth factors. J. Biol. Chem. 272, 20 275–20 282.
Purification and characterization of novel heparin-binding growth factors in uterine secretory fluids: identification as heparin-regulated Mr 10,000 forms of connective tissue growth factors.CrossRef | 1:CAS:528:DyaK2sXltlGku7w%3D&md5=1dc0eddaf36ce3aa2e728013205b8acdCAS | open url image1

Brinkhof, B., van Tol, H. T., Groot Koerkamp, M. J., Riemers, F. M., IJzer, S. G., Mashayekhi, K., Haagsman, H. P., and Roelen, B. A. (2015). A mRNA landscape of bovine embryos after standard and MAPK-inhibited culture conditions: a comparative analysis. BMC Genomics 16, 277.
A mRNA landscape of bovine embryos after standard and MAPK-inhibited culture conditions: a comparative analysis.CrossRef | 25888366PubMed | open url image1

Buyalos, R. P., and Cai, X. (1994). Preimplantation embryo development enhanced by epidermal growth factor. J. Assist. Reprod. Genet. 11, 33–37.
Preimplantation embryo development enhanced by epidermal growth factor.CrossRef | 1:STN:280:DyaK2M%2FjslWmsQ%3D%3D&md5=fb696c6458b5a06783a3c1de6416b16fCAS | 7949833PubMed | open url image1

Chang, C. C., Hsu, W. H., Wang, C. C., Chou, C. H., Kuo, M. Y. P., Lin, B. R., Chen, S. T., Tai, S. K., Kuo, M. L., and Yang, M. H. (2013). Connective tissue growth factor activates pluripotency genes and mesenchymal–epithelial transition in head and neck cancer cells. Cancer Res. 73, 4147–4157.
Connective tissue growth factor activates pluripotency genes and mesenchymal–epithelial transition in head and neck cancer cells.CrossRef | 1:CAS:528:DC%2BC3sXhtValu7zJ&md5=8200a67b25c27502806eec688c4c73efCAS | 23687336PubMed | open url image1

Chen, X., Zhang, J., Wu, X., Cao, S., Zhou, L., Wang, Y., Chen, X., Lu, J., Zhao, C., Chen, M., and Ling, X. (2014). Trophectoderm morphology predicts outcomes of pregnancy in vitrified-warmed single-blastocyst transfer cycle in a Chinese population. J. Assist. Reprod. Genet. 31, 1475–1481.
Trophectoderm morphology predicts outcomes of pregnancy in vitrified-warmed single-blastocyst transfer cycle in a Chinese population.CrossRef | 25123128PubMed | open url image1

de Moraes, A. A., and Hansen, P. J. (1997). Granulocyte–macrophage colony-stimulating factor promotes development of in vitro produced bovine embryos. Biol. Reprod. 57, 1060–1065.
Granulocyte–macrophage colony-stimulating factor promotes development of in vitro produced bovine embryos.CrossRef | 1:CAS:528:DyaK2sXmvFSntL8%3D&md5=2de5889c12ff9ce6ff45327e96b8a83fCAS | 9369171PubMed | open url image1

Denicol, A. C., Dobbs, K. B., McLean, K. M., Carambula, S. F., Loureiro, B., and Hansen, P. J. (2013). Canonical WNT signaling regulates development of bovine embryos to the blastocyst stage. Sci. Rep. 3, 1266.
Canonical WNT signaling regulates development of bovine embryos to the blastocyst stage.CrossRef | 23405280PubMed | open url image1

Denicol, A. C., Block, J., Kelley, D. E., Pohler, K. G., Dobbs, K. B., Mortensen, C. J., Ortega, M. S., and Hansen, P. J. (2014). The WNT signaling antagonist Dickkopf-1 directs lineage commitment and promotes survival of the preimplantation embryo. FASEB J. 28, 3975–3986.
The WNT signaling antagonist Dickkopf-1 directs lineage commitment and promotes survival of the preimplantation embryo.CrossRef | 1:CAS:528:DC%2BC2cXhsFanur%2FM&md5=713729e205ed6cd2233c6608fd6eb905CAS | 24858280PubMed | open url image1

Dobbs, K. B., Gagné, D., Fournier, E., Dufort, I., Robert, C., Block, J., Sirard, M. A., Bonilla, L., Ealy, A. D., Loureiro, B., and Hansen, P. J. (2014). Sexual dimorphism in developmental programming of the bovine preimplantation embryo caused by colony-stimulating factor 2. Biol. Reprod. 91, 80.
Sexual dimorphism in developmental programming of the bovine preimplantation embryo caused by colony-stimulating factor 2.CrossRef | 25078682PubMed | open url image1

Ebner, T., Tritscher, K., Mayer, R. B., Oppelt, P., Duba, H. C., Maurer, M., Schappacher-Tilp, G., Petek, E., and Shebl, O. (2016). Quantitative and qualitative trophectoderm grading allows for prediction of live birth and gender. J. Assist. Reprod. Genet. 33, 49–57.
Quantitative and qualitative trophectoderm grading allows for prediction of live birth and gender.CrossRef | 26572782PubMed | open url image1

El-Sayed, A., Hoelker, M., Rings, F., Salilew, D., Jennen, D., Tholen, E., Sirard, M. A., Schellander, K., and Tesfaye, D. (2006). Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients. Physiol. Genomics 28, 84–96.
Large-scale transcriptional analysis of bovine embryo biopsies in relation to pregnancy success after transfer to recipients.CrossRef | 1:CAS:528:DC%2BD28XhtlCmtrzK&md5=562fd59235e5a1a07e593a026558b4caCAS | 17018689PubMed | open url image1

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 | 1:STN:280:DC%2BD3M%2FovVGrsg%3D%3D&md5=1a406e3afd26ea28ff8d52520f620cfaCAS | 11101029PubMed | open url image1

Farin, C. E., Farmer, W. T., and Farin, P. W. (2010). Pregnancy recognition and abnormal offspring syndrome in cattle. Reprod. Fertil. Dev. 22, 75–87.
Pregnancy recognition and abnormal offspring syndrome in cattle.CrossRef | 1:CAS:528:DC%2BC3cXitlagurc%3D&md5=3430dcc8102cd43862ec219b65b8bc7aCAS | 20003848PubMed | open url image1

Fischer-Brown, A. E., Lindsey, B. R., Ireland, F. A., Northey, D. L., Monson, R. L., Clark, S. G., Wheeler, M. B., Kesler, D. J., Lane, S. J., Weigel, K. A., and Rutledge, J. J. (2004). Embryonic disc development and subsequent viability of cattle embryos following culture in two media under two oxygen concentrations. Reprod. Fertil. Dev. 16, 787–793.
Embryonic disc development and subsequent viability of cattle embryos following culture in two media under two oxygen concentrations.CrossRef | 1:STN:280:DC%2BD2svotlGnsQ%3D%3D&md5=c067ea9e8e3a9b1f37a698e9e678f7afCAS | 15740702PubMed | open url image1

Forde, N., Spencer, T. E., Bazer, F. W., Song, G., Roche, J. F., and Lonergan, P. (2010). Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiol. Genomics 41, 53–62.
Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium.CrossRef | 1:CAS:528:DC%2BC3cXhtlakt7jN&md5=1233ced98d2ee46d3f931e2298bd0d8eCAS | 19996158PubMed | open url image1

Fry, R. C., Batt, P. A., Fairclough, R. J., and Parr, R. A. (1992). Human leukemia inhibitory factor improves the viability of cultured ovine embryos. Biol. Reprod. 46, 470–474.
Human leukemia inhibitory factor improves the viability of cultured ovine embryos.CrossRef | 1:CAS:528:DyaK38Xht1Klsbc%3D&md5=18511311145e1501b7d9e22ff8ec2fdcCAS | 1617019PubMed | open url image1

Gad, A., Hoelker, M., Besenfelder, U., Havlicek, V., Cinar, U., Rings, F., Held, E., Dufort, I., Sirard, M. A., Schellander, K., and Tesfaye, D. (2012). Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol. Reprod. 87, 100.
Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions.CrossRef | 22811576PubMed | open url image1

Ghanem, N., Salilew-Wondim, D., Gad, A., Tesfaye, D., Phatsara, C., Tholen, E., Looft, C., Schellander, K., and Hoelker, M. (2011). Bovine blastocysts with developmental competence to term share similar expression of developmentally important genes although derived from different culture environments. Reproduction 142, 551–564.
Bovine blastocysts with developmental competence to term share similar expression of developmentally important genes although derived from different culture environments.CrossRef | 1:CAS:528:DC%2BC3MXhtlyitb%2FL&md5=c2ed909a32a987b6d95b2ddc5f5a49a9CAS | 21799070PubMed | open url image1

Gómez, E., Correia-Álvarez, E., Caamaño, J. N., Díez, C., Carrocera, S., Peynot, N., Martín, D., Giraud-Delville, C., Duranthon, V., Sandra, O., and Muñoz, M. (2014). Hepatoma-derived growth factor: from the bovine uterus to the in vitro embryo culture. Reproduction 148, 353–365.
Hepatoma-derived growth factor: from the bovine uterus to the in vitro embryo culture.CrossRef | 25009202PubMed | open url image1

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 | 16324220PubMed | open url image1

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 | 1:CAS:528:DC%2BC2cXjtlyhsrs%3D&md5=cf905f517802a0ee07f0e56c0b5298f0CAS | 24591639PubMed | open url image1

Hansen, P. J. (2015). Developmental programming in the preimplantation period: can it be exploited to enhance postnatal function in cattle? Anim. Reprod. 12, 428–436. open url image1

Hansen, P. J., Denicol, A. C., and Dobbs, K. B. (2014). Maternal embryokines that regulate development of the bovine preimplantation embryo. Turk. J. Vet. Anim. Sci. 38, 589–598.
Maternal embryokines that regulate development of the bovine preimplantation embryo.CrossRef | open url image1

Hansen, P. J., Dobbs, K. B., Denicol, A. C., and Siqueira, L. G. (2016). Sex and the preimplantation embryo: implications of sexual dimorphism in the preimplantation period for maternal programming of embryonic development. Cell Tissue Res. 363, 237–247.
Sex and the preimplantation embryo: implications of sexual dimorphism in the preimplantation period for maternal programming of embryonic development.CrossRef | 26391275PubMed | open url image1

Harding, P. A., Surveyor, G. A., and Brigstock, D. R. (1998). Characterization of pig connective tissue growth factor (CTGF) cDNA, mRNA and protein from uterine tissue. DNA Seq. 8, 385–390.
Characterization of pig connective tissue growth factor (CTGF) cDNA, mRNA and protein from uterine tissue.CrossRef | 1:CAS:528:DC%2BD3cXislSrtLg%3D&md5=0e22cd3e30417f490364d88fa02dbd5cCAS | 10728823PubMed | open url image1

Herrler, A., Krusche, C. A., and Beier, H. M. (1998). Insulin and insulin-like growth factor-I promote rabbit blastocyst development and prevent apoptosis. Biol. Reprod. 59, 1302–1310.
Insulin and insulin-like growth factor-I promote rabbit blastocyst development and prevent apoptosis.CrossRef | 1:CAS:528:DyaK1cXnvVKku70%3D&md5=31504d499753c0a5f6d13bb3f17c08b1CAS | 9828171PubMed | open url image1

Hill, M. J., Richter, K. S., Heitmann, R. J., Graham, J. R., Tucker, M. J., DeCherney, A. H., Browne, P. E., and Levens, E. D. (2013). Trophectoderm grade predicts outcomes of single-blastocyst transfers. Fertil. Steril. 99, 1283–1289.e1.
Trophectoderm grade predicts outcomes of single-blastocyst transfers.CrossRef | 23312233PubMed | open url image1

Huang, F. I., Chen, Y. L., Chang, C. N., Yuan, R. H., and Jeng, Y. M. (2012). Hepatocyte growth factor activates Wnt pathway by transcriptional activation of LEF1 to facilitate tumor invasion. Carcinogenesis 33, 1142–1148.
Hepatocyte growth factor activates Wnt pathway by transcriptional activation of LEF1 to facilitate tumor invasion.CrossRef | 1:CAS:528:DC%2BC38XhtVShsb7O&md5=da61646bf71056da8506b1e89410a3e7CAS | 22436613PubMed | open url image1

Hyrapetian, M., Loucaides, E. M., and Sutcliffe, A. G. (2014). Health and disease in children born after assistive reproductive therapies (ART). J. Reprod. Immunol. 106, 21–26.
Health and disease in children born after assistive reproductive therapies (ART).CrossRef | 25438931PubMed | open url image1

Jousan, F. D., and Hansen, P. J. (2007). Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling. Mol. Reprod. Dev. 74, 189–196.
Insulin-like growth factor-I promotes resistance of bovine preimplantation embryos to heat shock through actions independent of its anti-apoptotic actions requiring PI3K signaling.CrossRef | 1:CAS:528:DC%2BD2sXmsV2rtQ%3D%3D&md5=db92a9ab2b86e1649e52a39597350d6dCAS | 16955404PubMed | open url image1

Kauma, S. W., and Matt, D. W. (1995). Coculture cells that express leukemia inhibitory factor (LIF) enhance mouse blastocyst developmnt in vitro. J. Assist. Reprod. Genet. 12, 153–156.
Coculture cells that express leukemia inhibitory factor (LIF) enhance mouse blastocyst developmnt in vitro.CrossRef | 1:STN:280:DyaK2MvgtVSqsw%3D%3D&md5=d066e8f565c4efad4cbdb8abab28a51cCAS | 7670275PubMed | open url image1

Koraishy, F. M., Silva, C., Mason, S., Wu, D., and Cantley, L. G. (2014). Hepatocyte growth factor (Hgf) stimulates low density lipoprotein receptor-related protein (Lrp) 5/6 phosphorylation and promotes canonical Wnt signaling. J. Biol. Chem. 289, 14 341–14 350.
Hepatocyte growth factor (Hgf) stimulates low density lipoprotein receptor-related protein (Lrp) 5/6 phosphorylation and promotes canonical Wnt signaling.CrossRef | 1:CAS:528:DC%2BC2cXotFGmsb0%3D&md5=6bd087021ba84179e7cbc06b7df52b44CAS | open url image1

Kubota, S., and Takigawa, M. (2015). Cellular and molecular actions of CCN2/CTGF and its role under physiological and pathological conditions. Clin. Sci. (Lond.) 128, 181–196.
Cellular and molecular actions of CCN2/CTGF and its role under physiological and pathological conditions.CrossRef | 1:CAS:528:DC%2BC2cXhslWiurrF&md5=eac3955eaebfeb24374cf2bec235f838CAS | 25294165PubMed | open url image1

Lazzari, G., Colleoni, S., Lagutina, I., Crotti, G., Turini, P., Tessaro, I., Brunetti, D., Duchi, R., and Galli, C. (2010). Short-term and long-term effects of embryo culture in the surrogate sheep oviduct versus in vitro culture for different domestic species. Theriogenology 73, 748–757.
Short-term and long-term effects of embryo culture in the surrogate sheep oviduct versus in vitro culture for different domestic species.CrossRef | 1:STN:280:DC%2BC3c7ot1aksw%3D%3D&md5=f56371678ea4028ff5dff82b3e0b7e9fCAS | 19726075PubMed | open url image1

Ledgard, A. M., Meier, S., and Peterson, A. J. (2011). Evaluation of the uterine environment early in pregnancy establishment to characterise cows with a potentially superior ability to support conceptus survival. Reprod. Fertil. Dev. 23, 737–747.
Evaluation of the uterine environment early in pregnancy establishment to characterise cows with a potentially superior ability to support conceptus survival.CrossRef | 1:STN:280:DC%2BC3MjhsVCktA%3D%3D&md5=cf1534bae7f31f1196311d6689196761CAS | 21791175PubMed | open url image1

Lee, K. B., Bettegowda, A., Wee, G., Ireland, J. J., and Smith, G. W. (2009). Molecular determinants of oocyte competence: potential functional role for maternal (oocyte-derived) follistatin in promoting bovine early embryogenesis. Endocrinology 150, 2463–2471.
Molecular determinants of oocyte competence: potential functional role for maternal (oocyte-derived) follistatin in promoting bovine early embryogenesis.CrossRef | 1:CAS:528:DC%2BD1MXlsFCisrg%3D&md5=b5c917e9d48b563683676dada64b78a2CAS | 19179440PubMed | open url image1

Lee, K. H., Choi, E. Y., Kim, M. K., Lee, S. H., Jang, B. I., Kim, T. N., Kim, S. W., Kim, S. W., Song, S. K., Kim, J. R., and Jung, B. C. (2010). Hepatoma-derived growth factor regulates the bad-mediated apoptotic pathway and induction of vascular endothelial growth factor in stomach cancer cells. Oncol. Res. 19, 67–76.
Hepatoma-derived growth factor regulates the bad-mediated apoptotic pathway and induction of vascular endothelial growth factor in stomach cancer cells.CrossRef | 1:CAS:528:DC%2BC3MXhsFymtr0%3D&md5=5e0264012fe649768ae13f1e6ae65b9bCAS | 21302807PubMed | open url image1

Lim, K. T., Gupta, M. K., Lee, S. H., Jung, Y. H., Han, D. W., and Lee, H. T. (2013). Possible involvement of Wnt/β-catenin signaling pathway in hatching and trophectoderm differentiation of pig blastocysts. Theriogenology 79, 284–290.e2.
Possible involvement of Wnt/β-catenin signaling pathway in hatching and trophectoderm differentiation of pig blastocysts.CrossRef | 1:CAS:528:DC%2BC38XhslSmu7nO&md5=de75cdf4b32d20594dd5e35d88bc3e01CAS | 23174779PubMed | open url image1

Lin, T. C., Yen, J. M., Gong, K. B., Hsu, T. T., and Chen, L. R. (2003). IGF-1/IGFBP-1 increases blastocyst formation and total blastocyst cell number in mouse embryo culture and facilitates the establishment of a stem-cell line. BMC Cell Biol. 4, 14.
IGF-1/IGFBP-1 increases blastocyst formation and total blastocyst cell number in mouse embryo culture and facilitates the establishment of a stem-cell line.CrossRef | 14499003PubMed | open url image1

Loureiro, B., Bonilla, L., Block, J., Fear, J. M., Bonilla, A. Q. S., and Hansen, P. J. (2009). Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro. Endocrinology 150, 5046–5054.
Colony-stimulating factor 2 (CSF-2) improves development and posttransfer survival of bovine embryos produced in vitro.CrossRef | 1:CAS:528:DC%2BD1MXhsVCht7bF&md5=b305084c703fa07cf75a98da47489422CAS | 19797121PubMed | open url image1

Loureiro, B., Block, J., Favoreto, M. G., Carambula, S., Pennington, K. A., Ealy, A. D., and Hansen, P. J. (2011). Consequences of conceptus exposure to colony-stimulating factor 2 on survival, elongation, interferon-τ secretion, and gene expression. Reproduction 141, 617–624.
Consequences of conceptus exposure to colony-stimulating factor 2 on survival, elongation, interferon-τ secretion, and gene expression.CrossRef | 1:CAS:528:DC%2BC3MXmvFCisr0%3D&md5=1a3eba98e976660e4838024d15c3e66fCAS | 21339286PubMed | open url image1

Mo, X., Wu, G., Yuan, D., Jia, B., Liu, C., Zhu, S., and Hou, Y. (2014). Leukemia inhibitory factor enhances bovine oocyte maturation and early embryo development. Mol. Reprod. Dev. 81, 608–618.
Leukemia inhibitory factor enhances bovine oocyte maturation and early embryo development.CrossRef | 1:CAS:528:DC%2BC2cXot1yksbo%3D&md5=90e70661bd7368a60887a0c3f653ad8cCAS | 24687528PubMed | open url image1

Murakami, S., Miyamoto, Y., Fujiwara, C., Takeuchi, S., Takahashi, S., and Okuda, K. (2001). Expression and action of hepatocyte growth factor in bovine endometrial stromal and epithelial cells in vitro. Mol. Reprod. Dev. 60, 472–480.
Expression and action of hepatocyte growth factor in bovine endometrial stromal and epithelial cells in vitro.CrossRef | 1:CAS:528:DC%2BD3MXosl2qtrc%3D&md5=47aeae13ade29c3eb17d1906ef7219f6CAS | 11746958PubMed | open url image1

Nagatomo, H., Kagawa, S., Kishi, Y., Takuma, T., Sada, A., Yamanaka, K. I., Abe, Y., Wada, Y., Takahashi, M., and Kono, T. (2013). Transcriptional wiring for establishing cell lineage specification at the blastocyst stage in cattle. Biol. Reprod. 88, 158.
Transcriptional wiring for establishing cell lineage specification at the blastocyst stage in cattle.CrossRef | 23677984PubMed | open url image1

O’Neill, C. (2005). The role of paf in embryo physiology. Hum. Reprod. Update 11, 215–228.
The role of paf in embryo physiology.CrossRef | 1:CAS:528:DC%2BD2MXjsFOmt7Y%3D&md5=bd593764e2293fd979771b97c8d745ebCAS | 15790601PubMed | open url image1

Orimo, T., Taga, M., Matsui, H., and Minaguchi, H. (1996). The effect of activin-A on the development of mouse preimplantation embryos in vitro. J. Assist. Reprod. Genet. 13, 669–674.
The effect of activin-A on the development of mouse preimplantation embryos in vitro.CrossRef | 1:STN:280:DyaK2s%2Flt1Cqtg%3D%3D&md5=a27d9abf911a2276732fdb3b2a8f1556CAS | 8897128PubMed | open url image1

Ozawa, M., and Hansen, P. J. (2011). A novel method for purification of inner cell mass and trophectoderm cells from blastocysts using magnetic activated cell sorting. Fertil. Steril. 95, 799–802.
A novel method for purification of inner cell mass and trophectoderm cells from blastocysts using magnetic activated cell sorting.CrossRef | 21055741PubMed | open url image1

Ozawa, M., Sakatani, M., Yao, J., Shanker, S., Yu, F., Yamashita, R., Wakabayashi, S., Nakai, K., Dobbs, K. B., Sudano, M. J., Farmerie, W. G., and Hansen, P. J. (2012). Global gene expression of the inner cell mass and trophectoderm of the bovine blastocyst. BMC Dev. Biol. 12, 33.
Global gene expression of the inner cell mass and trophectoderm of the bovine blastocyst.CrossRef | 1:CAS:528:DC%2BC3sXlvA%3D%3D&md5=b5e73ae9b27b7f930e23a1ac47440ec3CAS | 23126590PubMed | open url image1

Park, J. E., Oh, H. J., Hong, S. G., Jang, G., Kim, M. K., and Lee, B. C. (2010). Effects of activin A on the in vitro development and mRNA expression of bovine embryos cultured in chemically-defined two-step culture medium. Reprod. Domest. Anim. 45, 585–593.
| 1:CAS:528:DC%2BC3cXhtVOntbnK&md5=35a37a9654ee288370e3ce44bf7a43ebCAS | 19090825PubMed | open url image1

Parrish, J. J., Susko-Parrish, J. L., Leibfried-Rutledge, M. L., Critser, E. S., Eyestone, W. H., and First, N. L. (1986). Bovine in vitro fertilization with frozen–thawed semen. Theriogenology 25, 591–600.
Bovine in vitro fertilization with frozen–thawed semen.CrossRef | 1:STN:280:DC%2BD283pvV2itQ%3D%3D&md5=9fddc262c2bd76e8223bdbbd4bc7e9a6CAS | 16726150PubMed | open url image1

Rizos, D., Ramirez, M. A., Pintado, B., Lonergan, P., and Gutierrez-Adan, A. (2010). Culture of bovine embryos in intermediate host oviducts with emphasis on the isolated mouse oviduct. Theriogenology 73, 777–785.
Culture of bovine embryos in intermediate host oviducts with emphasis on the isolated mouse oviduct.CrossRef | 1:STN:280:DC%2BC3c7ot1Gmug%3D%3D&md5=e113563277758d1142751bd2c0192772CAS | 19939442PubMed | open url image1

Sakagami, N., Umeki, H., Nishino, O., Uchiyama, H., Ichikawa, K., Takeshita, K., Kaneko, E., Akiyama, K., Kobayashi, S., and Tamada, H. (2012). Normal calves produced after transfer of embryos cultured in a chemically defined medium supplemented with epidermal growth factor and insulin-like growth factor I following ovum pick up and in vitro fertilization in Japanese black cows. J. Reprod. Dev. 58, 140–146.
Normal calves produced after transfer of embryos cultured in a chemically defined medium supplemented with epidermal growth factor and insulin-like growth factor I following ovum pick up and in vitro fertilization in Japanese black cows.CrossRef | 1:CAS:528:DC%2BC38XlvVOntLY%3D&md5=7c409971b35aac4ee25bea66ad213cf7CAS | 22075559PubMed | open url image1

Sjöblom, C., Wikland, M., and Robertson, S. A. (1999). Granulocyte–macrophage colony-stimulating factor promotes human blastocyst development in vitro. Hum. Reprod. 14, 3069–3076.
Granulocyte–macrophage colony-stimulating factor promotes human blastocyst development in vitro.CrossRef | 10601098PubMed | open url image1

Sjöblom, C., Roberts, C. T., Wikland, M., and Robertson, S. A. (2005). Granulocyte–macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology 146, 2142–2153.
Granulocyte–macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis.CrossRef | 15705781PubMed | open url image1

Spencer, T. E. (2014). Biological roles of uterine glands in pregnancy. Semin. Reprod. Med. 32, 346–357.
Biological roles of uterine glands in pregnancy.CrossRef | 1:CAS:528:DC%2BC2cXhvVeku7jP&md5=5469cbe0c50685a8afb882107b40f3f8CAS | 24959816PubMed | open url image1

Surveyor, G. A., Wilson, A. K., and Brigstock, D. R. (1998). Localization of connective tissue growth factor during the period of embryo implantation in the mouse. Biol. Reprod. 59, 1207–1213.
Localization of connective tissue growth factor during the period of embryo implantation in the mouse.CrossRef | 1:CAS:528:DyaK1cXmvF2js7w%3D&md5=aea58c37aad3de27886c72729232ac9aCAS | 9780329PubMed | open url image1

Thongkittidilok, C., Tharasanit, T., Songsasen, N., Sananmuang, T., Buarpung, S., and Techakumphu, M. (2015). Epidermal growth factor improves developmental competence and embryonic quality of singly cultured domestic cat embryos. J. Reprod. Dev. 61, 269–276.
Epidermal growth factor improves developmental competence and embryonic quality of singly cultured domestic cat embryos.CrossRef | 1:CAS:528:DC%2BC28Xns1Gmu7s%3D&md5=3653208ff26c9bd5898ec168712aead5CAS | 25985792PubMed | open url image1

Tribulo, P., Siqueira, L. G., and Hansen, P. J. (2015). Endometrial expression of genes involved in growth factor, cytokine, hormone, and WNT signaling during the early estrous cycle of the cow. In ‘Proceedings of the 48th Annual Meeting of the Society for the Study of Reproduction’. Abstract no. 281. Available at http://www.ssr.org/sites/ssr.org/files/uploads/attachments/node/315/2015_ssr_abstracts.pdf [Verified 29 April 2016]

Trigal, B., Gómez, E., Díez, C., Caamaño, J. N., Martín, D., Carrocera, S., and Muñoz, M. (2011). In vitro development of bovine embryos cultured with activin A. Theriogenology 75, 584–588.
In vitro development of bovine embryos cultured with activin A.CrossRef | 1:CAS:528:DC%2BC3MXjs1KmtA%3D%3D&md5=879ad6b45865367b3da1ae70abcdf2e3CAS | 21040964PubMed | open url image1

Uzumcu, M., Homsi, M. F. A., Ball, D. K., Coskun, S., Jaroudi, K., Hollanders, J. M. G., and Brigstock, D. R. (2000). Localization of connective tissue growth factor in human uterine tissues. Mol. Hum. Reprod. 6, 1093–1098.
Localization of connective tissue growth factor in human uterine tissues.CrossRef | 1:CAS:528:DC%2BD3MXjsFKnsw%3D%3D&md5=3ee5bc4d4604a62bbf6c7a88a1674c2eCAS | 11101692PubMed | open url image1

Ying, S. Y. (1988). Inhibins, activins, and follistatins: gonadal proteins modulating the secretion of follicle-stimulating hormone. Endocr. Rev. 9, 267–293.
Inhibins, activins, and follistatins: gonadal proteins modulating the secretion of follicle-stimulating hormone.CrossRef | 1:CAS:528:DyaL1cXksVyntLk%3D&md5=86a3fbeead25efca0fe8e0f84255e151CAS | 3136011PubMed | open url image1

Yoshioka, K., Suzuki, C., and Iwamura, S. (1998a). Activin A and follistatin regulate developmental competence of in vitro-produced bovine embryos. Biol. Reprod. 59, 1017–1022.
Activin A and follistatin regulate developmental competence of in vitro-produced bovine embryos.CrossRef | 1:CAS:528:DyaK1cXmvFyqurk%3D&md5=2ed6e7d65face7e49a933f434ce349dbCAS | 9780304PubMed | open url image1

Yoshioka, K., Takata, M., Taniguchi, T., Yamanaka, H., and Sekikawa, K. (1998b). Differential expression of activin subunits, activin receptors and follistatin genes in bovine oocytes and preimplantation embryos. Reprod. Fertil. Dev. 10, 293–298.
Differential expression of activin subunits, activin receptors and follistatin genes in bovine oocytes and preimplantation embryos.CrossRef | 1:CAS:528:DyaK1MXjvFSjs7w%3D&md5=eb93bdf813d31bfe8c1045c412b1b997CAS | 11596877PubMed | open url image1

Ziebe, S., Loft, A., Povlsen, B. B., Erb, K., Agerholm, I., Aasted, M., Gabrielsen, A., Hnida, C., Zobel, D. P., Munding, B., Bendz, S. H., and Robertson, S. A. (2013). A randomized clinical trial to evaluate the effect of granulocyte–macrophage colony-stimulating factor (GM-CSF) in embryo culture medium for in vitro fertilization. Fertil. Steril. 99, 1600–1609.e2.
A randomized clinical trial to evaluate the effect of granulocyte–macrophage colony-stimulating factor (GM-CSF) in embryo culture medium for in vitro fertilization.CrossRef | 1:CAS:528:DC%2BC3sXit1Khtr0%3D&md5=6d0dbb0ca92a2b1a65b42251ec59556fCAS | 23380186PubMed | open url image1



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