Combinatorial effects of epidermal growth factor, fibroblast growth factor 2 and insulin-like growth factor 1 on trophoblast cell proliferation and embryogenesis in cattle
Ming Xie A , Sarah R. McCoski A , Sally E. Johnson A , Michelle L. Rhoads A and Alan D. Ealy A B
+ Author Affiliations
- Author Affiliations
A Department of Animal and Poultry Sciences, Virginia Tech, 175 West Campus Drive, Blacksburg, VA 24061, USA.
B Corresponding author. Email: ealy@vt.edu
Reproduction, Fertility and Development 29(2) 419-430 https://doi.org/10.1071/RD15226
Submitted: 6 June 2015 Accepted: 24 July 2015 Published: 25 August 2015
Abstract
Uterine secretions are crucial for conceptus development in mammals. This is especially important for species that undergo extended preimplantation development, like cattle and other ungulates. The present study examined cooperative interactions for epidermal growth factor (EGF), fibroblast growth factor-2 (FGF2) and insulin-like growth factor-1 (IGF1) on the proliferation of the bovine trophoblast cell line CT1 and bovine embryo development. Proliferation of CT1 cells increased after supplementation of the culture medium with 10 ng mL–1 EGF, 10 ng mL–1 FGF2 or 50 ng mL–1 IGF1, as well as with any combination of two factors. Greater increases in CT1 cell proliferation were detected when the growth medium was supplemented with all three factors. Supplementing the culture medium with individual or multiple factors during bovine embryo culture resulted in several positive outcomes, including increased blastocyst development, expansion, and hatching to varying degrees depending on the particular factor or combination of factors. Supplementation of the culture medium with all three factors increased embryonic trophoblast cell numbers on Day 8, as well as hatching rates and blastocyst diameter on Day 12 after fertilisation. Western blot analyses and the use of pharmacological inhibitors suggest that EGF and IGF1 affect CT1 proliferation by activating mitogen-activated protein kinase 3/1, whereas FGF2 activates AKT. In conclusion, the findings of the present study indicate that there are cooperative interactions among EGF, FGF2 and IGF1 that enhance trophoblast cell development during early embryogenesis.
Additional keywords: bovine, embryo development, placenta, uterine factor.
References
Ball, B. A., Altschul, M., Freeman, K. P., and Hillman, R. B. (1989). Culture of equine trophoblastic vesicles in vitro. Theriogenology 32, 401–412.| Culture of equine trophoblastic vesicles in vitro.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFCnuw%3D%3D&md5=c515f44340781208b051b2404e7dd129CAS | 16726686PubMed |
Bazer, F. W., Kim, J., Ka, H., Johnson, G. A., Wu, G., and Song, G. (2012). Select nutrients in the uterine lumen of sheep and pigs affect conceptus development. J. Reprod. Dev. 58, 180–188.
| Select nutrients in the uterine lumen of sheep and pigs affect conceptus development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptVKju7k%3D&md5=8d53c2b4a708592b47cd4c23085e66f9CAS | 22738901PubMed |
Beenken, A., and Mohammadi, M. (2009). The FGF family: biology, pathophysiology and therapy. Nat. Rev. Drug Discov. 8, 235–253.
| The FGF family: biology, pathophysiology and therapy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisVShur4%3D&md5=c3d47274a1760b1a78f0f19c73327e1cCAS | 19247306PubMed |
Block, J., Wrenzycki, C., Niemann, H., Herrmann, D., and Hansen, P. J. (2008). Effects of insulin-like growth factor-1 on cellular and molecular characteristics of bovine blastocysts produced in vitro. Mol. Reprod. Dev. 75, 895–903.
| Effects of insulin-like growth factor-1 on cellular and molecular characteristics of bovine blastocysts produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktFGhtrY%3D&md5=27aac5b94325af350e49fd71c83a9015CAS | 17926346PubMed |
Bo, G. A., and Mapletoft, R. J. (2013). Evaluation and classification of bovine embryos. Anim. Reprod. 10, 344–348.
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFamtbs%3D&md5=75869897a102756e8e04fea897a6fd88CAS | 21459028PubMed |
Böttcher, R. T., and Niehrs, C. (2005). Fibroblast growth factor signaling during early vertebrate development. Endocr. Rev. 26, 63–77.
| Fibroblast growth factor signaling during early vertebrate development.Crossref | GoogleScholarGoogle Scholar | 15689573PubMed |
Cebrian-Serrano, A., Salvador, I., and Silvestre, M. A. (2014). Beneficial effect of two culture systems with small groups of embryos on the development and quality of in vitro-produced bovine embryos. Anat. Histol. Embryol. 43, 22–30.
| Beneficial effect of two culture systems with small groups of embryos on the development and quality of in vitro-produced bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3svmtVCjsQ%3D%3D&md5=79bf095ef14d48b776f34d52ba31840eCAS | 23488942PubMed |
Clemente, M., Lopez-Vidriero, I., O’Gaora, P., Mehta, J. P., Forde, N., Gutierrez-Adan, A., Lonergan, P., and Rizos, D. (2011). Transcriptome changes at the initiation of elongation in the bovine conceptus. Biol. Reprod. 85, 285–295.
| Transcriptome changes at the initiation of elongation in the bovine conceptus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpslOnurg%3D&md5=331789df4189a3c1aadc671c79f881a0CAS | 21508349PubMed |
Cross, M. J., Stewart, A., Hodgkin, M. N., Kerr, D. J., and Wakelam, M. J. (1995). Wortmannin and its structural analogue demethoxyviridin inhibit stimulated phospholipase A2 activity in Swiss 3T3 cells. Wortmannin is not a specific inhibitor of phosphatidylinositol 3-kinase. J. Biol. Chem. 270, 25 352–25 355.
| Wortmannin and its structural analogue demethoxyviridin inhibit stimulated phospholipase A2 activity in Swiss 3T3 cells. Wortmannin is not a specific inhibitor of phosphatidylinositol 3-kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFylt7s%3D&md5=07360b9677b413f1447e92aa3cd94111CAS |
Dardik, A., and Schultz, R. M. (1991). Blastocoel expansion in the preimplantation mouse embryo: stimulatory effect of TGF-alpha and EGF. Development 113, 919–930.
| 1:CAS:528:DyaK38XhtVSjtrw%3D&md5=8eb56c535da5c392f224959756cedceaCAS | 1821860PubMed |
Demmers, K. J., Derecka, K., and Flint, A. (2001). Trophoblast interferon and pregnancy. Reproduction 121, 41–49.
| Trophoblast interferon and pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnslakug%3D%3D&md5=97f2e6088d3675eaf4363b8c8e96bc8cCAS | 11226028PubMed |
Desai, N., Lawson, J., and Goldfarb, J. (2000). Assessment of growth factor effects on post-thaw development of cryopreserved mouse morulae to the blastocyst stage. Hum. Reprod. 15, 410–418.
| Assessment of growth factor effects on post-thaw development of cryopreserved mouse morulae to the blastocyst stage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtlCru7k%3D&md5=5fd324aef383fe57fd59288d4f6bbd62CAS | 10655314PubMed |
Dilly, M., Hambruch, N., Haeger, J. D., and Pfarrer, C. (2010). Epidermal growth factor (EGF) induces motility and upregulates MMP-9 and TIMP-1 in bovine trophoblast cells. Mol. Reprod. Dev. 77, 622–629.
| Epidermal growth factor (EGF) induces motility and upregulates MMP-9 and TIMP-1 in bovine trophoblast cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVahsLg%3D&md5=b9bce6e77f0276939834aebcdecbdf9eCAS | 20578063PubMed |
Dobbs, K. B., Gagne, 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 | GoogleScholarGoogle Scholar | 25078682PubMed |
Dunlap, K. A., Palmarini, M., Varela, M., Burghardt, R. C., Hayashi, K., Farmer, J. L., and Spencer, T. E. (2006). Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc. Natl Acad. Sci. USA 103, 14 390–14 395.
| Endogenous retroviruses regulate periimplantation placental growth and differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOgsrzJ&md5=f661d93c0e273357cab35ec0f74cd152CAS |
Feldman, B., Poueymirou, W., Papaioannou, V. E., DeChiara, T. M., and Goldfarb, M. (1995). Requirement of FGF-4 for postimplantation mouse development. Science 267, 246–249.
| Requirement of FGF-4 for postimplantation mouse development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjt1ensbo%3D&md5=b06806ac248f00e29b0c1e2a39714dd6CAS | 7809630PubMed |
Fields, S. D., Hansen, P. J., and Ealy, A. D. (2011). Fibroblast growth factor requirements for in vitro development of bovine embryos. Theriogenology 75, 1466–1475.
| Fibroblast growth factor requirements for in vitro development of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkt1KjsLk%3D&md5=5c238d7a38cfa90c9ca2a3c8ee98edd4CAS | 21295834PubMed |
Flood, M. R., Gage, T. L., and Bunch, T. D. (1993). Effect of various growth-promoting factors on preimplantation bovine embryo development in vitro. Theriogenology 39, 823–833.
| Effect of various growth-promoting factors on preimplantation bovine embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1eru70%3D&md5=3c387886356e5762d6f625871a3040a9CAS | 16727256PubMed |
Forbes, K., Westwood, M., Baker, P. N., and Aplin, J. D. (2008). Insulin-like growth factor I and II regulate the life cycle of trophoblast in the developing human placenta. Am. J. Physiol. Cell Physiol. 294, C1313–C1322.
| Insulin-like growth factor I and II regulate the life cycle of trophoblast in the developing human placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVGhu74%3D&md5=a39e48ae4f32b0c9f070efbabc8aab94CAS | 18400990PubMed |
Gray, C. A., Taylor, K. M., Ramsey, W. S., Hill, J. R., Bazer, F. W., Bartol, F. F., and Spencer, T. E. (2001). Endometrial glands are required for preimplantation conceptus elongation and survival. Biol. Reprod. 64, 1608–1613.
| Endometrial glands are required for preimplantation conceptus elongation and survival.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvFGgsbs%3D&md5=7e6c8ae6295e07c722a9f97e2fe51d9cCAS | 11369585PubMed |
Gray, C. A., Burghardt, R. C., Johnson, G. A., Bazer, F. W., and Spencer, T. E. (2002). Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction 124, 289–300.
| Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVCitL8%3D&md5=99d2efe70c6bbdec1809d34d42889deaCAS | 12141942PubMed |
Guillomot, M. (1995). Cellular interactions during implantation in domestic ruminants. J. Reprod. Fertil. Suppl. 49, 39–51.
| 1:CAS:528:DyaK2MXmslWit7g%3D&md5=fe3843ef2cd1b3d2b3694f7dc00b7047CAS | 7623329PubMed |
Hambruch, N., Haeger, J. D., Dilly, M., and Pfarrer, C. (2010). EGF stimulates proliferation in the bovine placental trophoblast cell line F3 via Ras and MAPK. Placenta 31, 67–74.
| EGF stimulates proliferation in the bovine placental trophoblast cell line F3 via Ras and MAPK.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFyns7zK&md5=2d4e32b9fcf92233d943fe7844a25acbCAS | 19914712PubMed |
Han, J., Li, L., Hu, J., Yu, L., Zheng, Y., Guo, J., Zheng, X., Yi, P., and Zhou, Y. (2010). Epidermal growth factor stimulates human trophoblast cell migration through Rho A and Rho C activation. Endocrinology 151, 1732–1742.
| Epidermal growth factor stimulates human trophoblast cell migration through Rho A and Rho C activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXks1Cmtb4%3D&md5=d496263e4283d21362d6e0cb038477ceCAS | 20150581PubMed |
Jeong, W., Kim, J., Bazer, F. W., and Song, G. (2013). Epidermal growth factor stimulates proliferation and migration of porcine trophectoderm cells through protooncogenic protein kinase 1 and extracellular-signal-regulated kinases 1/2 mitogen-activated protein kinase signal transduction cascades during early pregnancy. Mol. Cell. Endocrinol. 381, 302–311.
| Epidermal growth factor stimulates proliferation and migration of porcine trophectoderm cells through protooncogenic protein kinase 1 and extracellular-signal-regulated kinases 1/2 mitogen-activated protein kinase signal transduction cascades during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFOgt7jN&md5=3663d3aff63d6496aa9e8cf5358b1834CAS | 24012778PubMed |
Jeong, W., Kim, J., Bazer, F. W., and Song, G. (2014a). Proliferation-stimulating effect of colony stimulating factor 2 on porcine trophectoderm cells is mediated by activation of phosphatidylinositol 3-kinase and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase. PLoS One 9, e88731.
| Proliferation-stimulating effect of colony stimulating factor 2 on porcine trophectoderm cells is mediated by activation of phosphatidylinositol 3-kinase and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 24520418PubMed |
Jeong, W., Kim, J., Bazer, F. W., and Song, G. (2014b). Stimulatory effect of vascular endothelial growth factor on proliferation and migration of porcine trophectoderm cells and their regulation by the phosphatidylinositol-3-kinase–AKT and mitogen-activated protein kinase cell signaling pathways. Biol. Reprod. 90, 50.
| Stimulatory effect of vascular endothelial growth factor on proliferation and migration of porcine trophectoderm cells and their regulation by the phosphatidylinositol-3-kinase–AKT and mitogen-activated protein kinase cell signaling pathways.Crossref | GoogleScholarGoogle Scholar | 24451985PubMed |
Jeong, W., Song, G., Bazer, F. W., and Kim, J. (2014c). Insulin-like growth factor I induces proliferation and migration of porcine trophectoderm cells through multiple cell signaling pathways, including protooncogenic protein kinase 1 and mitogen-activated protein kinase. Mol. Cell. Endocrinol. 384, 175–184.
| Insulin-like growth factor I induces proliferation and migration of porcine trophectoderm cells through multiple cell signaling pathways, including protooncogenic protein kinase 1 and mitogen-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjslKisbY%3D&md5=c8590f4301f09daabe211be0a4b78f3eCAS | 24508636PubMed |
Jousan, F. D., and Hansen, P. J. (2004). Insulin-like growth factor-I as a survival factor for the bovine preimplantation embryo exposed to heat shock. Biol. Reprod. 71, 1665–1670.
| Insulin-like growth factor-I as a survival factor for the bovine preimplantation embryo exposed to heat shock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1yitr0%3D&md5=303b39cb4912e059477476b147303db5CAS | 15253925PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsV2rtQ%3D%3D&md5=f6ca28aa5d4039cfb9586cb4631cf51bCAS | 16955404PubMed |
Jousan, F. D., Oliveira, L. J., and Hansen, P. J. (2008). Short-term culture of in vitro produced bovine preimplantation embryos with insulin-like growth factor-i prevents heat shock-induced apoptosis through activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol. Reprod. Dev. 75, 681–688.
| Short-term culture of in vitro produced bovine preimplantation embryos with insulin-like growth factor-i prevents heat shock-induced apoptosis through activation of the phosphatidylinositol 3-kinase/Akt pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtFClu7k%3D&md5=53ff8669119362c2344d94546710090fCAS | 18161856PubMed |
Katagiri, S., and Takahashi, Y. (2004). Changes in EGF concentrations during estrous cycle in bovine endometrium and their alterations in repeat breeder cows. Theriogenology 62, 103–112.
| Changes in EGF concentrations during estrous cycle in bovine endometrium and their alterations in repeat breeder cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt1Sks7w%3D&md5=ecbb857365a9e435a5d04beb0bdb0059CAS | 15159105PubMed |
Keefer, C. L., and Desai, J. P. (2011). Mechanical phenotyping of stem cells. Theriogenology 75, 1426–1430.
| Mechanical phenotyping of stem cells.Crossref | GoogleScholarGoogle Scholar | 21295841PubMed |
Kliem, A., Tetens, F., Klonisch, T., Grealy, M., and Fischer, B. (1998). Epidermal growth factor receptor and ligands in elongating bovine blastocysts. Mol. Reprod. Dev. 51, 402–412.
| Epidermal growth factor receptor and ligands in elongating bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnt1Ortrs%3D&md5=5109f6a6346ad055211993cd685add63CAS | 9820199PubMed |
Kuijk, E. W., van Tol, L. T., Van de Velde, H., Wubbolts, R., Welling, M., Geijsen, N., and Roelen, B. A. (2012). The roles of FGF and MAP kinase signaling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos. Development 139, 871–882.
| The roles of FGF and MAP kinase signaling in the segregation of the epiblast and hypoblast cell lineages in bovine and human embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmsl2hu7c%3D&md5=8f8577234fbc3bf76abfbf413b724921CAS | 22278923PubMed |
LaMarca, H. L., Dash, P. R., Vishnuthevan, K., Harvey, E., Sullivan, D. E., Morris, C. A., and Whitley, G. S. (2008). Epidermal growth factor-stimulated extravillous cytotrophoblast motility is mediated by the activation of PI3-K, Akt and both p38 and p42/44 mitogen-activated protein kinases. Hum. Reprod. 23, 1733–1741.
| Epidermal growth factor-stimulated extravillous cytotrophoblast motility is mediated by the activation of PI3-K, Akt and both p38 and p42/44 mitogen-activated protein kinases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXoslGqurw%3D&md5=06e2e8146c4f1431735a09879eb76dbaCAS | 18487214PubMed |
Larson, R. C., Ignotz, G. G., and Currie, W. B. (1992). Transforming growth factor beta and basic fibroblast growth factor synergistically promote early bovine embryo development during the fourth cell cycle. Mol. Reprod. Dev. 33, 432–435.
| Transforming growth factor beta and basic fibroblast growth factor synergistically promote early bovine embryo development during the fourth cell cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpsFSisw%3D%3D&md5=aab7059d817e1048a50d16ec7369b88aCAS | 1472373PubMed |
Li, R. H., and Zhuang, L. Z. (1997). The effects of growth factors on human normal placental cytotrophoblast cell proliferation. Hum. Reprod. 12, 830–834.
| The effects of growth factors on human normal placental cytotrophoblast cell proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsF2mu7s%3D&md5=a918cdbe8e57cc42ffd4c12fd1854e1eCAS | 9159451PubMed |
Lim, K. T., Jang, G., Ko, K. H., Lee, W. W., Park, H. J., Kim, J. J., Lee, S. H., Hwang, W. S., Lee, B. C., and Kang, S. K. (2007). Improved in vitro bovine embryo development and increased efficiency in producing viable calves using defined media. Theriogenology 67, 293–302.
| Improved in vitro bovine embryo development and increased efficiency in producing viable calves using defined media.Crossref | GoogleScholarGoogle Scholar | 16979228PubMed |
Lonergan, P., Carolan, C., Van Langendonckt, A., Donnay, I., Khatir, H., and Mermillod, P. (1996). Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro. Biol. Reprod. 54, 1420–1429.
| Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtV2nsLo%3D&md5=9c6ca64524daf91ad08381ba784b5edaCAS | 8724373PubMed |
Matsuura, K. (2014). Numerical calculations for diffusion effects in the well-of-the-well culture system for mammalian embryos. Reprod. Fertil. Dev. 26, 742–751.
| Numerical calculations for diffusion effects in the well-of-the-well culture system for mammalian embryos.Crossref | GoogleScholarGoogle Scholar | 23697480PubMed |
McCarthy, S. D., Roche, J. F., and Forde, N. (2012). Temporal changes in endometrial gene expression and protein localization of members of the IGF family in cattle: effects of progesterone and pregnancy. Physiol. Genomics 44, 130–140.
| Temporal changes in endometrial gene expression and protein localization of members of the IGF family in cattle: effects of progesterone and pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlslOgsrk%3D&md5=77187b6bd531def4a7b2dc4dd39a1474CAS | 22085906PubMed |
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=5b6b3bd0b256de10a3492414ee274f9cCAS | 10840878PubMed |
Michael, D. D., Alvarez, I. M., Ocon, O. M., Powell, A. M., Talbot, N. C., Johnson, S. E., and Ealy, A. D. (2006). Fibroblast growth factor-2 is expressed by the bovine uterus and stimulates interferon-tau production in bovine trophectoderm. Endocrinology 147, 3571–3579.
| Fibroblast growth factor-2 is expressed by the bovine uterus and stimulates interferon-tau production in bovine trophectoderm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlOrsbk%3D&md5=1b49a839e01c7e4866513f9d983dd782CAS | 16574787PubMed |
Moore, K., and Thatcher, W. W. (2006). Major advances associated with reproduction in dairy cattle. J. Dairy Sci. 89, 1254–1266.
| Major advances associated with reproduction in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1SjsLY%3D&md5=69a89cff9355cf05a788637256d6ff24CAS | 16537958PubMed |
Moreira, F., Paula-Lopes, F. F., Hansen, P. J., Badinga, L., and Thatcher, W. W. (2002). Effects of growth hormone and insulin-like growth factor-I on development of in vitro derived bovine embryos. Theriogenology 57, 895–907.
| Effects of growth hormone and insulin-like growth factor-I on development of in vitro derived bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjs1KhsLs%3D&md5=3356a9c5d341a31c9976ef846bc948d1CAS | 11991392PubMed |
Nakanishi, S., Kakita, S., Takahashi, I., Kawahara, K., Tsukuda, E., Sano, T., Yamada, K., Yoshida, M., Kase, H., Matsuda, Y., Hashimoto, Y., and Nonomura, Y. (1992). Wortmannin, a microbial product inhibitor of myosin light chain kinase. J. Biol. Chem. 267, 2157–2163.
| 1:CAS:528:DyaK38XhtVWlt7Y%3D&md5=f07963b263061e125b80268b7970f023CAS | 1733924PubMed |
Neira, J. A., Tainturier, D., Pena, M. A., and Martal, J. (2010). Effect of the association of IGF-I, IGF-II, bFGF, TGF-beta1, GM-CSF, and LIF on the development of bovine embryos produced in vitro. Theriogenology 73, 595–604.
| Effect of the association of IGF-I, IGF-II, bFGF, TGF-beta1, GM-CSF, and LIF on the development of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVOiurk%3D&md5=2063ff71faf1e2e67effec91286a013aCAS | 20035987PubMed |
Ocón-Grove, O. M., Cooke, F. N., Alvarez, I. M., Johnson, S. E., Ott, T. L., and Ealy, A. D. (2008). Ovine endometrial expression of fibroblast growth factor (FGF) 2 and conceptus expression of FGF receptors during early pregnancy. Domest. Anim. Endocrinol. 34, 135–145.
| Ovine endometrial expression of fibroblast growth factor (FGF) 2 and conceptus expression of FGF receptors during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 17223006PubMed |
Ozawa, M., Yang, Q. E., and Ealy, A. D. (2013). The expression of fibroblast growth factor receptors during early bovine conceptus development and pharmacological analysis of their actions on trophoblast growth in vitro. Reproduction 145, 191–201.
| The expression of fibroblast growth factor receptors during early bovine conceptus development and pharmacological analysis of their actions on trophoblast growth in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtlOnt74%3D&md5=63377719c63a02cbb5017b099a306f53CAS | 23241344PubMed |
Palma, G. A., Muller, M., and Brem, G. (1997). Effect of insulin-like growth factor I (IGF-I) at high concentrations on blastocyst development of bovine embryos produced in vitro. J. Reprod. Fertil. 110, 347–353.
| Effect of insulin-like growth factor I (IGF-I) at high concentrations on blastocyst development of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvFKrsLw%3D&md5=9a76661bd3b736dc36e0ff374942e226CAS | 9306989PubMed |
Pfeffer, P. L., and Pearton, D. J. (2012). Trophoblast development. Reproduction 143, 231–246.
| Trophoblast development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFOqs7c%3D&md5=b256e0ffcac1c8de31c11f82f2cab378CAS | 22223687PubMed |
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=8a4565fc147604a05291a09199e46929CAS | 11226033PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvVOntLY%3D&md5=b8bf10f24b8bb0cf7f8925a5a71278ccCAS | 22075559PubMed |
Schlafer, D. H., Fisher, P. J., and Davies, C. J. (2000). The bovine placenta before and after birth: placental development and function in health and disease. Anim. Reprod. Sci. 60–61, 145–160.
| The bovine placenta before and after birth: placental development and function in health and disease.Crossref | GoogleScholarGoogle Scholar | 10844191PubMed |
Shimada, A., Nakano, H., Takahashi, T., Imai, K., and Hashizume, K. (2001). Isolation and characterization of a bovine blastocyst-derived trophoblastic cell line, BT-1: development of a culture system in the absence of feeder cell. Placenta 22, 652–662.
| Isolation and characterization of a bovine blastocyst-derived trophoblastic cell line, BT-1: development of a culture system in the absence of feeder cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvV2ltb8%3D&md5=03d6bf1e62ef5e58156091de7866df3dCAS | 11504534PubMed |
Singh, M., Chaudhry, P., and Asselin, E. (2011). Bridging endometrial receptivity and implantation: network of hormones, cytokines, and growth factors. J. Endocrinol. 210, 5–14.
| Bridging endometrial receptivity and implantation: network of hormones, cytokines, and growth factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovVGjurY%3D&md5=2e5ee2e7462ce502f166a6c664be53acCAS | 21372150PubMed |
Sirisathien, S., and Brackett, B. G. (2003). TUNEL analyses of bovine blastocysts after culture with EGF and IGF-I. Mol. Reprod. Dev. 65, 51–56.
| TUNEL analyses of bovine blastocysts after culture with EGF and IGF-I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXis1als7o%3D&md5=d13ea11a2fa55b7f1746982dea6819aaCAS | 12658633PubMed |
Sirisathien, S., Hernandez-Fonseca, H. J., and Brackett, B. G. (2003). Influences of epidermal growth factor and insulin-like growth factor-I on bovine blastocyst development in vitro. Anim. Reprod. Sci. 77, 21–32.
| Influences of epidermal growth factor and insulin-like growth factor-I on bovine blastocyst development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlGiu7k%3D&md5=eeca0eb5b2ac98f91bbd4b644bbb0da1CAS | 12654525PubMed |
Spencer, T. E., and Bazer, F. W. (2004). Uterine and placental factors regulating conceptus growth in domestic animals. J. Anim. Sci. 82 E-Suppl, E4–E13.
| 1:STN:280:DC%2BD2crjt1Clsw%3D%3D&md5=cebc2e2b70c8ad167087f446062b01b1CAS | 15471813PubMed |
Spencer, T. E., Burghardt, R. C., Johnson, G. A., and Bazer, F. W. (2004). Conceptus signals for establishment and maintenance of pregnancy. Anim. Reprod. Sci. 82–83, 537–550.
| Conceptus signals for establishment and maintenance of pregnancy.Crossref | GoogleScholarGoogle Scholar | 15271478PubMed |
Talbot, N. C., Caperna, T. J., Edwards, J. L., Garrett, W., Wells, K. D., and Ealy, A. D. (2000). Bovine blastocyst-derived trophectoderm and endoderm cell cultures: interferon tau and transferrin expression as respective in vitro markers. Biol. Reprod. 62, 235–247.
| Bovine blastocyst-derived trophectoderm and endoderm cell cultures: interferon tau and transferrin expression as respective in vitro markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotVOktw%3D%3D&md5=34f8e3f37924cb6ad56a6c92f0934e0eCAS | 10642558PubMed |
Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A., and Rossant, J. (1998). Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072–2075.
| Promotion of trophoblast stem cell proliferation by FGF4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVOqsrk%3D&md5=c09caf969726ad3b38609f6ac10a2833CAS | 9851926PubMed |
Velazquez, M. A., Hermann, D., Kues, W. A., and Niemann, H. (2011). Increased apoptosis in bovine blastocysts exposed to high levels of IGF1 is not associated with downregulation of the IGF1 receptor. Reproduction 141, 91–103.
| Increased apoptosis in bovine blastocysts exposed to high levels of IGF1 is not associated with downregulation of the IGF1 receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVehs7g%3D&md5=d5bcf6e03aff601f73bda77f0a9ae74fCAS | 20926690PubMed |
Wagener, J., Yang, W., Kazuschke, K., Winterhager, E., and Gellhaus, A. (2013). CCN3 regulates proliferation and migration properties in Jeg3 trophoblast cells via ERK1/2, Akt and Notch signalling. Mol. Hum. Reprod. 19, 237–249.
| CCN3 regulates proliferation and migration properties in Jeg3 trophoblast cells via ERK1/2, Akt and Notch signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktFOiur8%3D&md5=023e5b70aebeab9cde0f36bbd0616338CAS | 23220688PubMed |
Watson, A. J. (1992). The cell biology of blastocyst development. Mol. Reprod. Dev. 33, 492–504.
| The cell biology of blastocyst development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXpvVGmtg%3D%3D&md5=5a75b50ddc1184b456a21f3830edf589CAS | 1335276PubMed |
Yang, Q. E., Fields, S. D., Zhang, K., Ozawa, M., Johnson, S. E., and Ealy, A. D. (2011a). Fibroblast growth factor 2 promotes primitive endoderm development in bovine blastocyst outgrowths. Biol. Reprod. 85, 946–953.
| Fibroblast growth factor 2 promotes primitive endoderm development in bovine blastocyst outgrowths.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtl2is7bJ&md5=a8433f02cf5fd0bde6ea56a2a96029d7CAS | 21778141PubMed |
Yang, Q. E., Giassetti, M. I., and Ealy, A. D. (2011b). Fibroblast growth factors activate mitogen-activated protein kinase pathways to promote migration in ovine trophoblast cells. Reproduction 141, 707–714.
| Fibroblast growth factors activate mitogen-activated protein kinase pathways to promote migration in ovine trophoblast cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFCis7w%3D&md5=8e7b5f9ca775886226582e5cbc27ca53CAS | 21310815PubMed |
Yang, Q. E., Johnson, S. E., and Ealy, A. D. (2011c). Protein kinase C delta mediates fibroblast growth factor-2-induced interferon-tau expression in bovine trophoblast. Biol. Reprod. 84, 933–943.
| Protein kinase C delta mediates fibroblast growth factor-2-induced interferon-tau expression in bovine trophoblast.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGisro%3D&md5=259e201316d35cd2f4464937d7abe43bCAS | 21191110PubMed |
Yang, Q. E., Ozawa, M., Zhang, K., Johnson, S. E., and Ealy, A. D. (2014). The requirement for protein kinase C delta (PRKCD) during preimplantation bovine embryo development. Reprod. Fertil. Dev. , .
| The requirement for protein kinase C delta (PRKCD) during preimplantation bovine embryo development.Crossref | GoogleScholarGoogle Scholar | 25116760PubMed |
Zhang, K., Hansen, P. J., and Ealy, A. D. (2010). Fibroblast growth factor 10 enhances bovine oocyte maturation and developmental competence in vitro. Reproduction 140, 815–826.
| Fibroblast growth factor 10 enhances bovine oocyte maturation and developmental competence in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFKqtLY%3D&md5=ac6a7972f9f74d5715400062644e5193CAS | 20876224PubMed |
