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

Localisation of stem cell factor, stanniocalcin-1, connective tissue growth factor and heparin-binding epidermal growth factor in the bovine uterus at the time of blastocyst formation

M. Muñoz A E , D. Martin A , S. Carrocera A , M. Alonso-Guervos B , M. I. Mora C , F. J. Corrales C , N. Peynot D , C. Giraud-Delville D , V. Duranthon D , O. Sandra D and E. Gómez A
+ Author Affiliations
- Author Affiliations

A Centro de Biotecnología Animal, Servicio Regional de Investigación y Desarrollo Agroalimentario (SERIDA), Camino de Rioseco 1225, 33394 Gijón, Spain.

B Unidad de Microscopía Fotónica y Proceso de Imágenes, Servicios Científico Técnicos, Universidad de Oviedo, Instituto Universitario de Oncología de Asturias (IUOPA), 33006, Oviedo, Spain.

C Unidad de Proteomica, Centro de Investigación Médica Aplicada (CIMA) – Universidad de Navarra, 31008, Pamplona, Navarra, Spain.

D UMR BDR, INRA, ENVA, Université Paris Saclay, 78350, Jouy en Josas, France.

E Corresponding author. Email: mmunoz@serida.org

Reproduction, Fertility and Development 29(11) 2127-2139 https://doi.org/10.1071/RD16383
Submitted: 28 September 2016  Accepted: 12 January 2017   Published: 24 February 2017

Abstract

Early embryonic losses before implantation account for the highest rates of reproductive failure in mammals, in particular when in vitro-produced embryos are transferred. In the present study, we used molecular biology techniques (real-time quantitative polymerase chain reaction), classical immunohistochemical staining coupled with confocal microscopy and proteomic analysis (multiple reaction monitoring and western blot analysis) to investigate the role of four growth factors in embryo–uterine interactions during blastocyst development. Supported by a validated embryo transfer model, the study investigated: (1) the expression of stem cell factor (SCF), stanniocalcin-1 (STC1), connective tissue growth factor (CTGF) and heparin-binding epidermal growth factor-like growth factor (HB-EGF) in bovine uterine fluid; (2) the presence of SCF, STC1, CTGF and HB-EGF mRNA and protein in the bovine endometrium and embryos; and (3) the existence of reciprocal regulation between endometrial and embryonic expression of SCF, STC1, CTGF and HB-EGF. The results suggest that these growth factors most likely play an important role during preimplantation embryo development in cattle. The information obtained from the present study can contribute to improving the performance of in vitro culture technology in cattle and other species.

Additional keywords: early embryo–maternal communication, embryo, endometrium.


References

Alavi-Shoushtari, S. M., Asri-Rezai, S., and Abshenas, J. (2006). A study of the uterine protein variations during the estrus cycle in the cow: a comparison with the serum proteins. Anim. Reprod. Sci. 96, 10–20.
A study of the uterine protein variations during the estrus cycle in the cow: a comparison with the serum proteins.CrossRef | 1:CAS:528:DC%2BD28Xps1CitLY%3D&md5=0eebfe012f38426faa4d59fbb59d09b6CAS |

Arceci, R. J., Pampfer, S., and Pollard, J. W. (1992). Expression of CSF-1/c-fms and SF/c-kit mRNA during preimplantation mouse development. Dev. Biol. 151, 1–8.
Expression of CSF-1/c-fms and SF/c-kit mRNA during preimplantation mouse development.CrossRef | 1:CAS:528:DyaK38Xit1yjsbw%3D&md5=ec7028f45bb9c8af4c0e4cc95ea1e430CAS |

Barnard, J. A., Graves-Dea, R., Pittelkow, M. R., DuBois, R., Cook, P., Ramsey, G. W., Bishop, P. R., Damstrup, L., and Coffey, R. J. (1994). Auto- and cross-induction within the mammalian epidermal growth factorrelatedpeptide family. J. Biol. Chem. 269, 22 817–22 822.
| 1:CAS:528:DyaK2cXlvFKrsrw%3D&md5=52237eebb7a986751ad4fd81eabb170aCAS |

Bauersachs, S., Ulbrich, S. E., Gross, K., Schmidt, S. E., Meyer, H. H., Einspanier, R., Wenigerkind, H., Vermehren, M., Blum, H., Sinowatz, F., and Wolf, E. (2005). Gene expression profiling of bovine endometrium during the oestrous cycle: detection of molecular pathways involved in functional changes. J. Mol. Endocrinol. 34, 889–908.
Gene expression profiling of bovine endometrium during the oestrous cycle: detection of molecular pathways involved in functional changes.CrossRef | 1:CAS:528:DC%2BD2MXlslCisL8%3D&md5=7b6aa0e391bd85791dc9f7f7110bb159CAS |

Berendt, F. J., Fröhlich, T., Schmidt, S. E., Reichenbach, H. D., Wolf, E., and Arnold, G. J. (2005). Holistic differential analysis of embryo-induced alterations in the proteome of bovine endometrium in the preattachment period. Proteomics 5, 2551–2560.
Holistic differential analysis of embryo-induced alterations in the proteome of bovine endometrium in the preattachment period.CrossRef | 1:CAS:528:DC%2BD2MXmtF2gt7k%3D&md5=6712312df2650d9451c4bbdb03efb471CAS |

Brown, N., Deb, K., Paria, B. C., Das, S. K., and Reese, J. (2004). Embryo–uterine interactions via the neuregulin family of growth factors during implantation in the mouse. Biol. Reprod. 71, 2003–2011.
Embryo–uterine interactions via the neuregulin family of growth factors during implantation in the mouse.CrossRef | 1:CAS:528:DC%2BD2cXhtVWgsrrN&md5=2f97a16e4b5d75e4f0a62e53f2760d95CAS |

Carr, S. A., Abbatiello, S. E., Ackermann, B. L., Borchers, C., Domon, B., Deutsch, E. W., Grant, R. P., Hoofnagle, A. N., Hüttenhain, R., Koomen, J. M., Liebler, D. C., Liu, T., MacLean, B., Mani, D. R., Mansfield, E., Neubert, H., Paulovich, A. G., Reiter, L., Vitek, O., Aebersold, R., Anderson, L., Bethem, R., Blonder, J., Boja, E., Botelho, J., Boyne, M., Bradshaw, R. A., Burlingame, A. L., Chan, D., Keshishian, H., Kuhn, E., Kinsinger, C., Lee, J. S., Lee, S. W., Moritz, R., Oses-Prieto, J., Rifai, N., Ritchie, J., Rodriguez, H., Srinivas, P. R., Townsend, R. R., V.an Eyk, J., Whiteley, G., Wiita, A., and Weintraub, S. (2014). Targeted peptide measurements in biology and medicine: best practices for mass spectrometry-based assay development using a fit-for-purpose approach. Mol. Cell. Proteomics 13, 907–917.
Targeted peptide measurements in biology and medicine: best practices for mass spectrometry-based assay development using a fit-for-purpose approach.CrossRef | 1:CAS:528:DC%2BC2cXktlWjt7s%3D&md5=efd2587a4b9dfbb45efd06121bb5872eCAS |

Chronopoulou, E., and Harper, J. C. (2015). IVF culture media: past, present and future. Hum. Reprod. Update 21, 39–55.
IVF culture media: past, present and future.CrossRef |

Correia-Álvarez, E., Gómez, E., Martín, D., Carrocera, S., Pérez, S., Otero, J., Peynot, N., Giraud-Delville, C., Caamaño, J. N., Sandra, O., Duranthon, V., and Muñoz, M. (2015). Expression and localization of interleukin 1 beta and interleukin 1 receptor (type I) in the bovine endometrium and embryo. J. Reprod. Immunol. 110, 1–13.
Expression and localization of interleukin 1 beta and interleukin 1 receptor (type I) in the bovine endometrium and embryo.CrossRef |

Faulkner, S., Elia, G., Mullen, M. P., O’Boyle, P., Dunn, M. J., and Morris, D. (2012). A comparison of the bovine uterine and plasma proteome using iTRAQ proteomics. Proteomics 12, 2014–2023.
A comparison of the bovine uterine and plasma proteome using iTRAQ proteomics.CrossRef | 1:CAS:528:DC%2BC38Xpt12rtbo%3D&md5=efd1b8275a4a9b95d81ee974002d702eCAS |

Faulkner, S., Elia, G., O’ Boyle, P., Dunn, M., and Morris, D. (2013). Composition of the bovine uterine proteome is associated with stage of cycle and concentration of systemic progesterone. Proteomics 13, 3333–3353.
Composition of the bovine uterine proteome is associated with stage of cycle and concentration of systemic progesterone.CrossRef | 1:CAS:528:DC%2BC3sXhs1Clt7bM&md5=349ae900f1121f9c70bde127cfa39f3fCAS |

Garlow, J. E., Ka, H., Johnson, G. A., Burghardt, R. C., Jaeger, L. A., and Bazer, F. W. (2002). Analysis of osteopontin at the maternal–placental interface in pigs. Biol. Reprod. 66, 718–725.
Analysis of osteopontin at the maternal–placental interface in pigs.CrossRef | 1:CAS:528:DC%2BD38XhvVeiur8%3D&md5=0a2b7efa4b4bbe8481ecbfc7321d7ca0CAS |

Gillette, M. A., and Carr, S. A. (2013). Quantitative analysis of peptides and proteins in biomedicine by targeted mass spectrometry. Nat. Methods 10, 28–34.
Quantitative analysis of peptides and proteins in biomedicine by targeted mass spectrometry.CrossRef | 1:CAS:528:DC%2BC38XhvFShtb%2FF&md5=49f48f82ad16888a47395b99cff61e5aCAS |

Gómez, E., and Muñoz, M. (2015). Multiple-embryo transfer for studying very early maternal–embryo interactions in cattle. Reproduction 150, R35–R43.
Multiple-embryo transfer for studying very early maternal–embryo interactions in cattle.CrossRef |

Gómez, E., Rodríguez, A., Muñoz, M., Caamaño, J. N., Carrocera, S., Martín, D., Facal, N., and Díez, C. (2008). Development and quality of bovine morulae cultured in serum-free medium with specific retinoid receptor agonists. Reprod. Fertil. Dev. 20, 884–891.
Development and quality of bovine morulae cultured in serum-free medium with specific retinoid receptor agonists.CrossRef |

Gómez, E., Caamaño, J. N., Corrales, F. J., Díez, C., Correia-Álvarez, E., Martín, D., Trigal, B., Carrocera, S., Mora, M. I., Pello-Palma, J., Moreno, J. F., and Muñoz, M. (2013). Embryonic sex induces differential expression of proteins in bovine uterine fluid. J. Proteome Res. 12, 1199–1210.
Embryonic sex induces differential expression of proteins in bovine uterine fluid.CrossRef |

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 |

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 |

Goossens, K., Van Soom, A., Van Zeveren, A., Favoreel, H., and Peelman, L. J. (2009). Quantification of fibronectin 1 (FN1) splice variants, including two novel ones, and analysis of integrins as candidate FN1 receptors in bovine preimplantation embryos. BMC Dev. Biol. 9, 1.
Quantification of fibronectin 1 (FN1) splice variants, including two novel ones, and analysis of integrins as candidate FN1 receptors in bovine preimplantation embryos.CrossRef |

Goossens, K., Tesfaye, D., Rings, F., Schellander, K., Hölker, M., Van Poucke, M., Van Zeveren, A., Lemahieu, I., Van Soom, A., and Peelman, L. J. (2010). Suppression of keratin 18 gene expression in bovine blastocysts by RNA interference. Reprod. Fertil. Dev. 22, 395–404.
Suppression of keratin 18 gene expression in bovine blastocysts by RNA interference.CrossRef | 1:CAS:528:DC%2BC3cXjtlar&md5=ac1e851d62e7dad66ba8090810098f29CAS |

Grebe, S. K., and Singh, R. J. (2011). LC-MS/MS in the clinical laboratory – where to from here? Clin. Biochem. Rev. 32, 5–31.

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=ae5b97667045b0d775d16f449283e5f4CAS |

Hardy, K., and Spanos, S. (2002). Growth factor expression and function in the human and mouse preimplantation embryo. J. Endocrinol. 172, 221–236.
Growth factor expression and function in the human and mouse preimplantation embryo.CrossRef | 1:CAS:528:DC%2BD38XhvVejt78%3D&md5=5bc8fa11f2497757355c76560b69b23dCAS |

Hidalgo, C. O., Gomez, E., Prieto, L., Duque, P., Goyache, F., Fernández, L., Fernández, I., Facal, N., and Díez, C. (2004). Pregnancy rates and metabolic profiles in cattle treated with propylene glycol prior to embryo transfer. Theriogenology 62, 664–676.
Pregnancy rates and metabolic profiles in cattle treated with propylene glycol prior to embryo transfer.CrossRef | 1:CAS:528:DC%2BD2cXltF2rsrc%3D&md5=64abf4caf48b098b22eba2639c519cbaCAS |

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 | 1:STN:280:DC%2BD3c7pvVGnsw%3D%3D&md5=4b5bf1ef366000f0c309b3ada47205f5CAS |

Hugentobler, S. A., Morris, D. G., Sreenan, J. M., and Diskin, M. G. (2007). Ion concentrations in oviduct and uterine fluid and blood serum during the estrous cycle in the bovine. Theriogenology 68, 538–548.
Ion concentrations in oviduct and uterine fluid and blood serum during the estrous cycle in the bovine.CrossRef | 1:CAS:528:DC%2BD2sXotlWqu78%3D&md5=defda0e87d325717e691852a00db552bCAS |

Ibrahim, S., Salilew-Wondim, D., Rings, F., Hoelker, M., Neuhoff, C., Tholen, E., Looft, C., Schellander, K., and Tesfaye, D. (2015). Expression pattern of inflammatory response genes and their regulatory microRNAs in bovine oviductal cells in response to lipopolysaccharide: implication for early embryonic development. PLoS One 10, e0119388.
Expression pattern of inflammatory response genes and their regulatory microRNAs in bovine oviductal cells in response to lipopolysaccharide: implication for early embryonic development.CrossRef |

Inagaki, N., Stern, C., McBain, J., Lopata, A., Kornman, L., and Wilkinson, D. (2003). Analysis of intra-uterine cytokine concentration and matrix-metalloproteinase activity in women with recurrent failed embryo transfer. Hum. Reprod. 18, 608–615.
Analysis of intra-uterine cytokine concentration and matrix-metalloproteinase activity in women with recurrent failed embryo transfer.CrossRef | 1:CAS:528:DC%2BD3sXit1yruro%3D&md5=ebd856179c8616239134b77654fa5b32CAS |

James, A., and Jorgensen, C. (2010). Basic design of MRM assays for peptide quantification. Methods Mol. Biol. 658, 167–185.
Basic design of MRM assays for peptide quantification.CrossRef | 1:CAS:528:DC%2BC3cXhtFKqsLrM&md5=447f0893ec667e89ebd54292d9f9d3ebCAS |

Johnson, G. A., Spencer, T. E., Burghardt, R. C., Burghardt, R. C., and Bazer, F. W. (1999). Ovine osteopontin: I. Cloning and expression of messenger ribonucleic acid in the uterus during the periimplantation period. Biol. Reprod. 61, 884–891.
Ovine osteopontin: I. Cloning and expression of messenger ribonucleic acid in the uterus during the periimplantation period.CrossRef | 1:CAS:528:DyaK1MXmtlajsb4%3D&md5=a43691550e58b96ecab204b725d3e858CAS |

Joyce, M. M., Burghardt, J. R., Burghardt, R. C., Hooper, R. N., Bazer, F. W., and Johnson, G. A. (2008). Uterine major histocompatibility class I molecules and 2 microglobulin are regulated by progesterone and conceptus interferons during pig pregnancy. J. Immunol. 181, 2494–2505.
Uterine major histocompatibility class I molecules and 2 microglobulin are regulated by progesterone and conceptus interferons during pig pregnancy.CrossRef | 1:CAS:528:DC%2BD1cXptlKqu74%3D&md5=58d341cb964f32ea6a363df0bc353543CAS |

Kannampuzha-Francis, J., Tribulo, P., and Hansen, P. J. (2016). 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. Reprod. Fertil. Dev. , .
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.CrossRef |

Kauma, S., Huff, T., Krystal, G., Ryan, J., Takacs, P., and Turner, T. (1996). The expression of stem cell factor and its receptor, c-kit in human endometrium and placental tissues during pregnancy. J. Clin. Endocrinol. Metab. 81, 1261–1266.
| 1:CAS:528:DyaK28Xhs1agtL8%3D&md5=41a4c20d05d58e1e12d151e58e82b1a3CAS |

Kikuchi, M., Nakano, Y., Nambo, Y., Haneda, S., Matsui, M., Miyake, Y., Macleod, J. N., Nagaoka, K., and Imakawa, K. (2011). Production of calcium maintenance factor Stanniocalcin-1 (STC1) by the equine endometrium during the early pregnant period. J. Reprod. Dev. 57, 203–211.
Production of calcium maintenance factor Stanniocalcin-1 (STC1) by the equine endometrium during the early pregnant period.CrossRef | 1:CAS:528:DC%2BC3MXnsFKmtbk%3D&md5=bffbde475d78f50a952915fbbfe08aabCAS |

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 | 1:CAS:528:DyaK1cXnt1Ortrs%3D&md5=dd2dc046da1eb26d33c5a555cbadcb68CAS |

Ledgard, A. M., Lee, R. S., and Peterson, A. J. (2009). Bovine endometrial legumain and TIMP-2 regulation in response to presence of a conceptus. Mol. Reprod. Dev. 76, 65–74.
Bovine endometrial legumain and TIMP-2 regulation in response to presence of a conceptus.CrossRef | 1:CAS:528:DC%2BD1cXhsFemtL3P&md5=ba3614842c8f2c5f918130c222587090CAS |

Lim, J. J., Lee, D. R., Song, H. S., Kim, K. S., Yoon, T. K., Gye, M. C., and Kim, M. K. (2006). Heparin-binding epidermal growth factor (HB-EGF) may improve embryonic development and implantation by increasing vitronectin receptor (integrin alphanubeta3) expression in peri-implantation mouse embryos. J. Assist. Reprod. Genet. 23, 111–119.
Heparin-binding epidermal growth factor (HB-EGF) may improve embryonic development and implantation by increasing vitronectin receptor (integrin alphanubeta3) expression in peri-implantation mouse embryos.CrossRef |

Lim, J. J., Eum, J. H., Lee, J. E., Leroy, J. L., and Bols, P. E. (2010). Stem cell factor/c-Kit signaling in in vitro cultures supports early mouse embryonic development by accelerating proliferation via a mechanism involving Akt-downstream genes. J. Assist. Reprod. Genet. 27, 619–627.
Stem cell factor/c-Kit signaling in in vitro cultures supports early mouse embryonic development by accelerating proliferation via a mechanism involving Akt-downstream genes.CrossRef |

Lonergan, P., Rizos, D., Gutiérrez-Adán, A., Fair, T., and Boland, M. P. (2003). Effect of culture environment on embryo quality and gene expression – experience from animal studies. Reprod. Biomed. Online 7, 657–663.
Effect of culture environment on embryo quality and gene expression – experience from animal studies.CrossRef | 1:STN:280:DC%2BD2c%2FkvFahsw%3D%3D&md5=dbbf8ebbf18f93558c21f6100efa7edcCAS |

Mansouri-Attia, N., Aubert, J., Reinaud, P., Giraud-Delville, C., Taghouti, G., Galio, L., Everts, R. E., Degrelle, S., Richard, C., Hue, I., Yang, X., Tian, X. C., Lewin, H. A., Renard, J. P., and Sandra, O. (2009). Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiol. Genomics 39, 14–27.
Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation.CrossRef | 1:CAS:528:DC%2BC3cXhtlakt7rM&md5=214c62741cf51d70dd8a3300d7b1966bCAS |

Martin, K. L., Barlow, D. H., and Sargent, I. L. (1998). Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium. Hum. Reprod. 13, 1645–1652.
Heparin-binding epidermal growth factor significantly improves human blastocyst development and hatching in serum-free medium.CrossRef | 1:CAS:528:DyaK1cXkslOlurc%3D&md5=27d01175bc02d30c3126bedc16f8c765CAS |

Marx, V. (2013). Targeted proteomics. Nat. Methods 10, 19–22.
Targeted proteomics.CrossRef | 1:CAS:528:DC%2BC38XhvFShurvJ&md5=4fc698ff2abb80f67d2a3801bf06c488CAS |

Maybin, J. A., Barcroft, J., Thiruchelvam, U., Hirani, N., Jabbour, H. N., and Critchley, H. O. (2012). The presence and regulation of connective tissue growth factor in the human endometrium. Hum. Reprod. 27, 1112–1121.
The presence and regulation of connective tissue growth factor in the human endometrium.CrossRef | 1:CAS:528:DC%2BC38XksVarsLg%3D&md5=b22a5ceba3dbb6ba9ce22d0497102259CAS |

Mishra, A., and Seshagiri, P. B. (2000). Heparin binding-epidermal growth factor improves blastocyst hatching and trophoblast outgrowth in the golden hamster. Reprod. Biomed. Online 1, 87–95.
Heparin binding-epidermal growth factor improves blastocyst hatching and trophoblast outgrowth in the golden hamster.CrossRef | 1:CAS:528:DC%2BD3MXos1Grsb4%3D&md5=20b7fc9a583ac5950a7ce748316c115cCAS |

Mitsunari, M., Harada, T., Tanikawa, M., Iwabe, T., Taniguchi, F., and Terakawa, N. (1999). The potential role of stem cellfactor and its receptor c-kit in the mouse blastocyst implantation. Mol. Hum. Reprod. 5, 874–879.
The potential role of stem cellfactor and its receptor c-kit in the mouse blastocyst implantation.CrossRef | 1:CAS:528:DyaK1MXmsVaqtL4%3D&md5=4042743791ca0fa98fd5a23e9f4b544aCAS |

Moussad, E. E., and Brigstock, D. R. (2000). Connective tissue growth factor: what’s in a name? Mol. Genet. Metab. 71, 276–292.
Connective tissue growth factor: what’s in a name?CrossRef | 1:CAS:528:DC%2BD3cXms1yjurw%3D&md5=c2a756c73976047667b3b8a14ecbeec5CAS |

Moussad, E. E., Rageh, M. A., Wilson, A. K., Geisert, R. D., and Brigstock, D. R. (2002). Temporal and spatial expression of connective tissue growth factor (CCN2; CTGF) and transforming growth factor beta type 1 (TGF-beta1) at the utero-placental interface during early pregnancy in the pig. Mol. Pathol. 55, 186–192.
Temporal and spatial expression of connective tissue growth factor (CCN2; CTGF) and transforming growth factor beta type 1 (TGF-beta1) at the utero-placental interface during early pregnancy in the pig.CrossRef | 1:CAS:528:DC%2BD38Xlt1yrt74%3D&md5=81356881f4c321fcbeeedba3814fb3e2CAS |

Mullen, M. P., Elia, G., Hilliard, M., Parr, M. H., Diskin, M. G., Evans, A. C., and Crowe, M. A. (2012). Proteomic characterization of histotroph during the preimplantation phase of the estrous cycle in cattle. J. Proteome Res. 11, 3004–3018.
Proteomic characterization of histotroph during the preimplantation phase of the estrous cycle in cattle.CrossRef | 1:CAS:528:DC%2BC38XkslWju7c%3D&md5=088e1ab7ed45fbf0ceac5cae5f5b248dCAS |

Muñoz, M., Peirson, S. N., Hankins, M. W., and Foster, R. G. (2005). Long-term constant light induces constitutive elevated expression of mPER2 protein in the murine SCN: a molecular basis for Aschoff’s rule? J. Biol. Rhythms 20, 3–14.
Long-term constant light induces constitutive elevated expression of mPER2 protein in the murine SCN: a molecular basis for Aschoff’s rule?CrossRef |

Pernemalm, M., and Lehtiö, J. (2014). Mass spectrometry-based plasma proteomics: state of the art and future outlook. Expert Rev. Proteomics 11, 431–448.
Mass spectrometry-based plasma proteomics: state of the art and future outlook.CrossRef | 1:CAS:528:DC%2BC2cXhtFCrtLzP&md5=df42866b26525685b09f9b1d83099d06CAS |

Picotti, P., and Aebersold, R. (2012). Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions. Nat. Methods 9, 555–566.
Selected reaction monitoring-based proteomics: workflows, potential, pitfalls and future directions.CrossRef | 1:CAS:528:DC%2BC38XotVSrurg%3D&md5=fb9a8f305e68b5770159334927a267faCAS |

Richter, K. S. (2008). The importance of growth factors for preimplantation embryo development and in-vitro culture. Curr. Opin. Obstet. Gynecol. 20, 292–304.
The importance of growth factors for preimplantation embryo development and in-vitro culture.CrossRef |

Robertson, S. A., Chin, P. Y., Schjenken, J. E., and Thompson, J. G. (2015). Female tract cytokines and developmental programming in embryos. Adv. Exp. Med. Biol. 843, 173–213.
Female tract cytokines and developmental programming in embryos.CrossRef |

Salamonsen, L. A., Edgell, T., Rombauts, L. J., Stephens, A. N., Robertson, D. M., Rainczuk, A., Nie, G., and Hannan, N. J. (2013). Proteomics of the human endometrium and uterine fluid: a pathway to biomarker discovery. Fertil. Steril. 99, 1086–1092.
Proteomics of the human endometrium and uterine fluid: a pathway to biomarker discovery.CrossRef | 1:CAS:528:DC%2BC38XhsVyhtLvF&md5=73659f12e4e92d64301866e3f7d8f0a4CAS |

Sharkey, A. M., Dellow, K., Blayney, M., Macnamee, M., Charnock-Jones, S., and Smith, S. K. (1995). Stage-specific expression of cytokine and receptor messenger ribonucleic acids in human preimplantation embryos. Biol. Reprod. 53, 974–981.
Stage-specific expression of cytokine and receptor messenger ribonucleic acids in human preimplantation embryos.CrossRef | 1:CAS:528:DyaK2MXotFyisrc%3D&md5=0e759a733ef69c4c9948ff88cb8a6966CAS |

Song, G., Bazer, F. W., Wagner, G. F., and Spencer, T. E. (2006). Stanniocalcin (STC) in the endometrial glands of the ovine uterus: regulation by progesterone and placental hormones. Biol. Reprod. 74, 913–922.
Stanniocalcin (STC) in the endometrial glands of the ovine uterus: regulation by progesterone and placental hormones.CrossRef | 1:CAS:528:DC%2BD28Xjsl2jurs%3D&md5=4c669bb56547718b82b9b6b4e465f365CAS |

Song, G., Dunlap, K. A., Kim, J., Bailey, D. W., Spencer, T. E., Burghardt, R. C., Wagner, G. F., Johnson, G. A., and Bazer, F. W. (2009). Stanniocalcin 1 is a luminal epithelial marker for implantation in pigs regulated by progesterone and estradiol. Endocrinology 150, 936–945.
Stanniocalcin 1 is a luminal epithelial marker for implantation in pigs regulated by progesterone and estradiol.CrossRef | 1:CAS:528:DC%2BD1MXhs1Sgtr0%3D&md5=47e333dd0cb6b69ac55470fd3d6ead9bCAS |

Stasko, S. E., DiMattia, G. E., and Wagner, G. F. (2001). Dynamic changes in stanniocalcin gene expression in the mouse uterus during early implantation. Mol. Cell. Endocrinol. 174, 145–149.
Dynamic changes in stanniocalcin gene expression in the mouse uterus during early implantation.CrossRef | 1:CAS:528:DC%2BD3MXisF2ktLo%3D&md5=832ccc9cf61c9f44211b17b7c73e922aCAS |

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=c394db1dd21da7f47bd722a79acf6e19CAS |

Swain, J. E., Carrell, D., Cobo, A., Meseguer, M., Rubio, C., and Smith, G. D. (2016). Optimizing the culture environment and embryo manipulation to help maintain embryo developmental potential. Fertil. Steril. 105, 571–587.
Optimizing the culture environment and embryo manipulation to help maintain embryo developmental potential.CrossRef |

Takatsu, K., and Acosta, T. J. (2015). Expression of heparin-binding EGF-like growth factor (HB-EGF) in bovine endometrium: effects of HB-EGF and interferon-τ on prostaglandin production. Reprod. Domest. Anim. 50, 458–464.
Expression of heparin-binding EGF-like growth factor (HB-EGF) in bovine endometrium: effects of HB-EGF and interferon-τ on prostaglandin production.CrossRef | 1:CAS:528:DC%2BC2MXntFSgs74%3D&md5=114c368a8415fbececbf6f77f5eeb8e6CAS |

Urrego, R., Rodriguez-Osorio, N., and Niemann, H. (2014). Epigenetic disorders and altered gene expression after use of assisted reproductive technologies in domestic cattle. Epigenetics 9, 803–815.
Epigenetic disorders and altered gene expression after use of assisted reproductive technologies in domestic cattle.CrossRef | 1:CAS:528:DC%2BC2cXhs1GntbvE&md5=2ab98caf4763fe9d53c1ce99f48428c5CAS |

Uzumcu, M., Homsi, M. F., Ball, D. K., Coskun, S., Jaroudi, K., Hollanders, J. M., 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=d529c9a393e8120eeead888f5fde619eCAS |

Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034.1.
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.CrossRef |

Vega-Díaz, B., Herron, G. S., and Michel, S. (2001). An autocrine loop mediates expression of vascular endothelial growth factor in human dermal microvascular endothelial cells. J. Invest. Dermatol. 116, 525–530.
An autocrine loop mediates expression of vascular endothelial growth factor in human dermal microvascular endothelial cells.CrossRef |

Walker, C. G., Meier, S., Littlejohn, M. D., Lehnert, K., Roche, J. R., and Mitchell, M. D. (2010). Modulation of the maternal immune system by the pre-implantation embryo. BMC Genomics 11, 474.
Modulation of the maternal immune system by the pre-implantation embryo.CrossRef |

Wang, J., Mayernik, L., Schultz, J. F., and Armant, D. R. (2000). Acceleration of trophoblast differentiation by heparin-binding EGF-like growth factor is dependent on the stage-specific activation of calcium influx by ErbB receptors in developing mouse blastocysts. Development 127, 33–44.
| 1:CAS:528:DC%2BD3cXpvFGrtQ%3D%3D&md5=6ced794a04eee23c2656087bc2fbd21dCAS |

Xiao, L. J., Yuan, J. X., Song, X. X., Li, Y. C., Hu, Z. Y., and Liu, Y. X. (2006). Expression and regulation of stanniocalcin 1 and 2 in rat uterus during embryo implantation and decidualization. Reproduction 131, 1137–1149.
Expression and regulation of stanniocalcin 1 and 2 in rat uterus during embryo implantation and decidualization.CrossRef | 1:CAS:528:DC%2BD28Xpt1ehu74%3D&md5=bb25cef9d86e414d98ba376a73e1566aCAS |

Yeung, B. H., Law, A. Y., and Wong, C. K. (2012). Evolution and roles of stanniocalcin. Mol. Cell. Endocrinol. 349, 272–280.
Evolution and roles of stanniocalcin.CrossRef | 1:CAS:528:DC%2BC3MXhs1Cqsb3E&md5=1103be6afe32f3804f13ebc2bb0033abCAS |



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