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RESEARCH ARTICLE

Soluble Delta-like ligand 1 alters human endometrial epithelial cell adhesive capacity

Michelle Van Sinderen A , Jennifer Oyanedel A B , Ellen Menkhorst A , Carly Cuman A C , Katarzyna Rainczuk A , Amy Winship A B , Lois Salamonsen A , Tracey Edgell A and Evdokia Dimitriadis A C D
+ Author Affiliations
- Author Affiliations

A Hudson Institute of Medical Research, 27–31 Wright St, Clayton, Vic. 3168, Australia.

B Department of Anatomy and Developmental Biology, Monash University, Clayton, Vic. 3168, Australia.

C Department of Molecular and Translational Sciences, Monash University, Clayton, Vic. 3168, Australia.

D Corresponding author. Email: evdokia.dimitriadis@hudson.org.au

Reproduction, Fertility and Development 29(4) 694-702 https://doi.org/10.1071/RD15313
Submitted: 1 August 2015  Accepted: 23 October 2015   Published: 30 November 2015

Abstract

The endometrium undergoes substantial morphological and functional changes to become receptive to embryo implantation and to enable establishment of a successful pregnancy. Reduced Delta-like ligand 1 (DLL1, Notch ligand) in the endometrium is associated with infertility. DLL1 can be cleaved by ‘a disintegrin and metalloprotease’ (ADAM) proteases to produce a soluble ligand that may act to inhibit Notch signalling. We used an enzyme-linked immunosorbent assay to quantify soluble DLL1 in uterine lavages from fertile and infertile women in the secretory phase of the menstrual cycle. We also determined the cellular location and immunostaining intensity of ADAM12 and 17 in human endometrium throughout the cycle. Functional effects of soluble DLL1 in receptivity were analysed using in vitro adhesion and proliferation assays and gene expression analysis of Notch signalling targets. Soluble DLL1 was significantly increased in uterine lavage samples of infertile women compared with fertile women in the secretory phase of the menstrual cycle. This coincided with significantly increased ADAM17 immunostaining detected in the endometrial luminal epithelium in the mid-secretory phase in infertile women. Soluble DLL1 significantly inhibited the adhesive capacity of endometrial epithelial cells via downregulation of helix–loop–helix and hairy/enhancer of split family member HES1 mRNA. Thus, soluble DLL1 may serve as a suitable target or potential biomarker for receptivity.

Additional keywords: implantation, infertility, Notch signalling, uterus.


References

Aghababaei, M., Perdu, S., Irvine, K., and Beristain, A. G. (2014). A disintegrin and metalloproteinase 12 (ADAM12) localizes to invasive trophoblast, promotes cell invasion and directs column outgrowth in early placental development. Mol. Hum. Reprod. 20, 235–249.
A disintegrin and metalloproteinase 12 (ADAM12) localizes to invasive trophoblast, promotes cell invasion and directs column outgrowth in early placental development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXis1WqsLw%3D&md5=736423edd4da94a7f33eb634d7033d08CAS | 24243624PubMed |

Aplin, J. D. (1997). Adhesion molecules in implantation. Rev. Reprod. 2, 84–93.
Adhesion molecules in implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktV2nurw%3D&md5=296a8fe3a25dd159af277b6cea73fd39CAS | 9414470PubMed |

Artavanis-Tsakonas, S., and Muskavitch, M. A. (2010). Notch: the past, the present and the future. Curr. Top. Dev. Biol. 92, 1–29.
Notch: the past, the present and the future.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12jtLvP&md5=6f82d0ff83638ca675b5b48ac2d05441CAS | 20816391PubMed |

Artavanis-Tsakonas, S., Rand, M. D., and Lake, R. J. (1999). Notch signalling: cell-fate control and signal integration in development. Science 284, 770–776.
Notch signalling: cell-fate control and signal integration in development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivVKrs7Y%3D&md5=02b38a2d20e08d1d22734ca9cc6f6ffcCAS | 10221902PubMed |

Bazer, F. W., Spencer, T. E., Johnson, G. A., Burghardt, R. C., and Wu, G. (2009). Comparative aspects of implantation. Reproduction 138, 195–209.
Comparative aspects of implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptlemt74%3D&md5=004657dc95deb8c9d20e9b7fee5476d7CAS | 19502456PubMed |

Bilandzic, M., Wang, Y., Ahmed, N., Luwor, R. B., Zhu, H. J., Findlay, J. K., and Stenvers, K. L. (2014). Betaglycan blocks metastatic behaviours in human granulosa cell tumours by suppressing NFkappaB-mediated induction of MMP2. Cancer Lett. 354, 107–114.
Betaglycan blocks metastatic behaviours in human granulosa cell tumours by suppressing NFkappaB-mediated induction of MMP2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVaktb3O&md5=10063d89c4b4ae0d21d90f79a36ae201CAS | 25128652PubMed |

Bray, S. J. (2006). Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7, 678–689.
Notch signalling: a simple pathway becomes complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xot12isr4%3D&md5=b26777887d8829db306260b459d492a4CAS | 16921404PubMed |

Brou, C., Logeat, F., Gupta, N., Bessia, C., LeBail, O., Doedens, J. R., Cumano, A., Roux, P., Black, R. A., and Israel, A. (2000). A novel proteolytic cleavage involved in Notch signalling: the role of the disintegrin–metalloprotease TACE. Mol. Cell 5, 207–216.
A novel proteolytic cleavage involved in Notch signalling: the role of the disintegrin–metalloprotease TACE.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhslyht7s%3D&md5=9a6dbdf88b990af492606e58ebbc673dCAS | 10882063PubMed |

Carson, D. D., Bagchi, I., Dey, S. K., Enders, A. C., Fazleabas, A. T., Lessey, B. A., and Yoshinaga, K. (2000). Embryo implantation. Dev. Biol. 223, 217–237.
Embryo implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksFeqs7o%3D&md5=d08f73f5549f68ca2b0d71311b486a07CAS | 10882512PubMed |

Casado-Vela, J., Rodriguez-Suarez, E., Iloro, I., Ametzazurra, A., Alkorta, N., Garcia-Velasco, J. A., Matorras, R., Prieto, B., Gonzalez, S., Nagore, D., Simon, L., and Elortza, F. (2009). Comprehensive proteomic analysis of human endometrial fluid aspirate. J. Proteome Res. 8, 4622–4632.
Comprehensive proteomic analysis of human endometrial fluid aspirate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFehurfE&md5=7049be710480c6cc75b55b35a60b6107CAS | 19670903PubMed |

Casslen, B. (1986). Uterine fluid volume. Cyclic variations and possible extrauterine contributions. J. Reprod. Med. 31, 506–510.
| 1:STN:280:DyaL283otFChtQ%3D%3D&md5=ff1d24ee5348cfebbf96047ef4929c61CAS | 3735263PubMed |

Cuman, C., Menkhorst, E. M., Rombauts, L. J., Holden, S., Webster, D., Bilandzic, M., Osianlis, T., and Dimitriadis, E. (2013). Preimplantation human blastocysts release factors that differentially alter human endometrial epithelial cell adhesion and gene expression relative to IVF success. Hum. Reprod. 28, 1161–1171.
Preimplantation human blastocysts release factors that differentially alter human endometrial epithelial cell adhesion and gene expression relative to IVF success.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlags7o%3D&md5=11ee89ec0e669f7dc394a9f8ae5d6e18CAS | 23477906PubMed |

Cuman, C., Menkhorst, E., Winship, A., Van Sinderen, M., Osianlis, T., Rombauts, L., and Dimitriadis, E. (2014). Fetal–maternal communication: the role of Notch signalling in embryo implantation. Reproduction 147, R75–R86.
Fetal–maternal communication: the role of Notch signalling in embryo implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktlOnsbc%3D&md5=c5a23aca8718b8757534ac7552c8c339CAS | 24357662PubMed |

Degaki, K. Y., Chen, Z., Yamada, A. T., and Croy, B. A. (2012). Delta-like ligand (DLL)1 expression in early mouse decidua and its localisation to uterine natural killer cells. PLoS One 7, e52037.
Delta-like ligand (DLL)1 expression in early mouse decidua and its localisation to uterine natural killer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsVyitg%3D%3D&md5=ad077bd90f8c226b79723df542ae93eeCAS | 23284862PubMed |

de La Coste, A., and Freitas, A. A. (2006). Notch signalling: distinct ligands induce specific signals during lymphocyte development and maturation. Immunol. Lett. 102, 1–9.
Notch signalling: distinct ligands induce specific signals during lymphocyte development and maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1SksrbI&md5=42251bbfba4633817fe98596000af369CAS | 16140393PubMed |

Dunwoodie, S., Clements, M., Sparrow, D., Sa, X., Conlon, R., and Beddington, R. (2002). Axial skeletal defects caused by mutation in the spondylocostal dysplasia/pudgy gene Dll3 are associated with disruption of the segmentation clock within the presomitic mesoderm. Development 129, 1795–1806.
| 1:CAS:528:DC%2BD38Xjt1eitL8%3D&md5=fd1713c912c229840d0df81cb2243153CAS | 11923214PubMed |

Dyczynska, E., Sun, D., Yi, H., Sehara-Fujisawa, A., Blobel, C. P., and Zolkiewska, A. (2007). Proteolytic processing of Delta-like 1 by ADAM proteases. J. Biol. Chem. 282, 436–444.
Proteolytic processing of Delta-like 1 by ADAM proteases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkslSl&md5=8a7c754abc722bcf5ed6a78debc03a88CAS | 17107962PubMed |

Edwards, D. R., Handsley, M. M., and Pennington, C. J. (2008). The ADAM metalloproteinases. Mol. Aspects Med. 29, 258–289.
The ADAM metalloproteinases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ShsLnM&md5=77a3b4a1aecab06e523403e3067c005dCAS | 18762209PubMed |

Estrach, S., Cordes, R., Hozumi, K., Gossler, A., and Watt, F. (2008). Role of the Notch ligand Delta1 in embryonic and adult mouse epidermis. J. Invest. Dermatol. 128, 825–832.
Role of the Notch ligand Delta1 in embryonic and adult mouse epidermis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtFOmsr0%3D&md5=812ae4255ca8b5a1459b8c70d59095f4CAS | 17960184PubMed |

Evans, J., D’Sylva, R., Volpert, M., Jamsai, D., Merriner, D. J., Nie, G., Salamonsen, L. A., and O’Bryan, M. K. (2015). Endometrial CRISP3 is regulated throughout the mouse oestrous and human menstrual cycle and facilitates adhesion and proliferation of endometrial epithelial cells. Biol. Reprod. 92, 99.
Endometrial CRISP3 is regulated throughout the mouse oestrous and human menstrual cycle and facilitates adhesion and proliferation of endometrial epithelial cells.Crossref | GoogleScholarGoogle Scholar | 25715794PubMed |

Gilpin, B. J., Loechel, F., Mattei, M. G., Engvall, E., Albrechtsen, R., and Wewer, U. M. (1998). A novel secreted form of human ADAM 12 (meltrin alpha) provokes myogenesis in vivo. J. Biol. Chem. 273, 157–166.
A novel secreted form of human ADAM 12 (meltrin alpha) provokes myogenesis in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvFShtw%3D%3D&md5=d98b2526fd20ea7c6365b6be96c42069CAS | 9417060PubMed |

Graham, C. H., Hawley, T. S., Hawley, R. G., MacDougall, J. R., Kerbel, R. S., Khoo, N., and Lala, P. K. (1993). Establishment and characterisation of first trimester human trophoblast cells with extended lifespan. Exp. Cell Res. 206, 204–211.
Establishment and characterisation of first trimester human trophoblast cells with extended lifespan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1OisL0%3D&md5=3f875f981d94bbcf9d51c92d8df13433CAS | 7684692PubMed |

Groot, A. J., and Vooijs, M. A. (2012). The role of ADAMs in Notch signalling. Adv. Exp. Med. Biol. 727, 15–36.
The role of ADAMs in Notch signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht12mt7jE&md5=fd19abce2646886cc918f9b84de9f467CAS | 22399336PubMed |

Hannan, N. J., Stoikos, C. J., Stephens, A. N., and Salamonsen, L. A. (2009a). Depletion of high-abundance serum proteins from human uterine lavages enhances detection of lower-abundance proteins. J. Proteome Res. 8, 1099–1103.
Depletion of high-abundance serum proteins from human uterine lavages enhances detection of lower-abundance proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksA%3D%3D&md5=72c1ec7b2ea094ffc5934c44e548d4e8CAS | 19113883PubMed |

Hannan, N. J., Stephens, A. N., Rainczuk, A., Hincks, C., Rombauts, L. J. F., and Salamonsen, L. A. (2009b). 2D-DiGE analysis of the human endometrial secretome reveals differences between receptive and nonreceptive states in fertile and infertile women. J. Proteome Res. 9, 6256–6264.
2D-DiGE analysis of the human endometrial secretome reveals differences between receptive and nonreceptive states in fertile and infertile women.Crossref | GoogleScholarGoogle Scholar |

Hannan, N. J., Paiva, P., Dimitriadis, E., and Salamonsen, L. A. (2010). Models for study of human embryo implantation: choice of cell lines? Biol. Reprod. 82, 235–245.
Models for study of human embryo implantation: choice of cell lines?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVSns7k%3D&md5=8e65308e439cb9b6950cf40b05cf6b62CAS | 19571263PubMed |

Hodkinson, P. S., Elliott, P. A., Lad, Y., McHugh, B. J., MacKinnon, A. C., Haslett, C., and Sethi, T. (2007). Mammalian NOTCH-1 activates beta1 integrins via the small GTPase R-Ras. J. Biol. Chem. 282, 28 991–29 001.
Mammalian NOTCH-1 activates beta1 integrins via the small GTPase R-Ras.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVOmtbjE&md5=c4f238cde35771b2be443b84cb4467ebCAS |

Hynes, R. O., and Lander, A. D. (1992). Contact and adhesive specificities in the associations, migrations and targeting of cells and axons. Cell 68, 303–322.
Contact and adhesive specificities in the associations, migrations and targeting of cells and axons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xht1GgsL8%3D&md5=e988f3e504580e3d2ac0b937ee830ba6CAS | 1733501PubMed |

Jin, G., Zhang, F., Chan, K., Xavier Wong, H., Liu, B., Cheah, K., Liu, X., Mauch, C., Liu, D., and Zhou, Z. (2011). MT1-MMP cleaves DLL1 to negatively regulate Notch signalling to maintain normal B-cell development. EMBO J. 30, 2281–2293.
MT1-MMP cleaves DLL1 to negatively regulate Notch signalling to maintain normal B-cell development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtV2hsb0%3D&md5=faf7c2037f69707d61157ae3b1911817CAS | 21572390PubMed |

Jokimaa, V., Oksjoki, S., Kujari, H., Vuorio, E., and Anttila, L. (2002). Altered expression of genes involved in the production and degredation of endometrial extracellular matrix in patients with unexplained infertility and recurrent miscarriages. Mol. Hum. Reprod. 8, 1111–1116.
Altered expression of genes involved in the production and degredation of endometrial extracellular matrix in patients with unexplained infertility and recurrent miscarriages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsFOntL0%3D&md5=c38b6382dfa4a32921323d07a9f26548CAS | 12468644PubMed |

Jowicz, A. P., Brown, J. K., McDonald, S. E., Shaw, J. L., Critchley, H. O., and Horne, A. W. (2013). Characterisation of the temporal and spatial expression of a disintegrin and metalloprotease 17 in the human endometrium and fallopian tube. Reprod. Sci. 20, 1321–1326.
Characterisation of the temporal and spatial expression of a disintegrin and metalloprotease 17 in the human endometrium and fallopian tube.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhslWjt7fL&md5=d50c5a4e0392a56dbc383c8f98851553CAS | 23585341PubMed |

Kim, J., Kim, H., Lee, S. J., Choi, Y. M., Lee, S. J., and Lee, J. Y. (2005). Abundance of ADAM-8, -9, -10, -12, -15 and -17 and ADAMTS-1 in mouse uterus during the oestrous cycle. Reprod. Fertil. Dev. 17, 543–555.
Abundance of ADAM-8, -9, -10, -12, -15 and -17 and ADAMTS-1 in mouse uterus during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlejt7s%3D&md5=ac7a3bf2e0b2fec3b284b5f6c8529fbeCAS | 15907280PubMed |

Kim, J., Kang, S. G., Kim, J. I., Park, J. H., Kim, S. K., Cho, D. J., and Kim, H. (2006). Implication of ADAM-8, -9, -10, -12, -15, -17 and ADAMTS-1 in implantational remodelling of a mouse uterus. Yonsei Med. J. 47, 558–567.
Implication of ADAM-8, -9, -10, -12, -15, -17 and ADAMTS-1 in implantational remodelling of a mouse uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCmtLnM&md5=e120a45ebf3d1b86e368c377559c1267CAS | 16941747PubMed |

Leong, K. G., and Karsan, A. (2006). Recent insights into the role of Notch signalling in tumourigenesis. Blood 107, 2223–2233.
Recent insights into the role of Notch signalling in tumourigenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFOjt7s%3D&md5=5d27704a4c1b38220e6313956bf4bc8cCAS | 16291593PubMed |

Liu, D., Ha, C., Zhang, X., Zhang, Z., and Liu, P. (2013). Molecular implication of ADAM-15 and -17 in intrauterine adhesions. Eur. J. Obstet. Gynecol. Reprod. Biol. 170, 264–269.
Molecular implication of ADAM-15 and -17 in intrauterine adhesions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1emtrrM&md5=552499ed453c9805759c34c12e9d7f86CAS | 23910172PubMed |

Marwood, M., Visser, K., Salamonsen, L. A., and Dimitriadis, E. (2009). Interleukin-11 and leukaemia inhibitory factor regulate the adhesion of endometrial epithelial cells: implications in fertility regulation. Endocrinology 150, 2915–2923.
Interleukin-11 and leukaemia inhibitory factor regulate the adhesion of endometrial epithelial cells: implications in fertility regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVGjsrs%3D&md5=dc1ceb38908a1489b910cc89aba897a1CAS | 19213836PubMed |

Miller, M. A., Meyer, A. S., Beste, M. T., Lasisi, Z., Reddy, S., Jeng, K. W., Chen, C. H., Han, J., Isaacson, K., Griffith, L. G., and Lauffenburger, D. A. (2013). ADAM-10 and -17 regulate endometriotic cell migration via concerted ligand and receptor shedding feedback on kinase signalling. Proc. Natl. Acad. Sci. USA 110, E2074–E2083.
ADAM-10 and -17 regulate endometriotic cell migration via concerted ligand and receptor shedding feedback on kinase signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFalsbfO&md5=d5c882207dbda104aa2b476d944a9dfbCAS | 23674691PubMed |

Mishra-Gorur, K., Rand, M., Perez-Villamil, B., and Artavanis-Tsakonas, S. (2002). Downregulation of Delta by proteolytic processing. J. Cell Biol. 159, 313–324.
Downregulation of Delta by proteolytic processing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosVaks74%3D&md5=84fec343cc3217b914222bed3ab63f55CAS | 12403816PubMed |

Muraguchi, T., Takegami, Y., Ohtuska, T., Kitajima, S., Chandana, E., Omura, A., Miki, T. R. T., Matsumoto, N., Ludwig, A., Noda, M., and Takahashi, C. (2007). RECK modulates Notch signalling during cortical neurogenesis by regulating ADAM10 activity. Nat. Neurosci. 10, 838–845.
RECK modulates Notch signalling during cortical neurogenesis by regulating ADAM10 activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvFKmsLk%3D&md5=1a1d9c657b7f3b8bd74f14911a367fd4CAS | 17558399PubMed |

Murata, A., Okuyama, K., Sakano, S., Kajiki, M., Hirata, T., Yagita, H., Zuniga-Pflucker, J., Miyake, K., Akashi-Takamura, S., Moriwaki, S., Niida, S., Yoshino, M., and Hayashi, S. (2010). A Notch ligand, Delta-like 1, functions as an adhesion molecule for mast cells. J. Immunol. 185, 3905–3912.
A Notch ligand, Delta-like 1, functions as an adhesion molecule for mast cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFyisrvO&md5=cb3e5f711f6bf630ac39d94dbbce18f1CAS | 20810995PubMed |

Murphy, C. (1995). The cytoskeleton of uterine epithelial cells: a new player in uterine receptivity and the plasma membrane transformation. Hum. Reprod. Update 1, 567–580.
The cytoskeleton of uterine epithelial cells: a new player in uterine receptivity and the plasma membrane transformation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3jtlajug%3D%3D&md5=f73b5bbdc3b95236354c20f4869d6c97CAS | 9079397PubMed |

Murphy, C. R. (2004). Uterine receptivity and the plasma membrane transformation. Cell Res. 14, 259–267.
Uterine receptivity and the plasma membrane transformation.Crossref | GoogleScholarGoogle Scholar | 15353123PubMed |

Murta, D., Batista, M., Trindade, A., Silva, E., Mateus, L., Duarte, A., and Lopes-da-Costa, L. (2015). Dynamics of Notch signalling in the mouse oviduct and uterus during the oestrous cycle. Reprod. Fertil. Dev. , .
Dynamics of Notch signalling in the mouse oviduct and uterus during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 25940784PubMed |

Navot, D., Bergh, P. A., Williams, M., Garrisi, G. J., Guzman, I., Sandler, B., Fox, J., Schreiner-Engel, P., Hofmann, G. E., and Grunfeld, L. (1991). An insight into early reproductive processes through the in vivo model of ovum donation. J. Clin. Endocrinol. Metab. 72, 408–414.
An insight into early reproductive processes through the in vivo model of ovum donation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7itlegtQ%3D%3D&md5=41b42091d4819ff766c9985d7855b14cCAS | 1991811PubMed |

Noyes, R., Hertig, A., and Rock, J. (1950). Dating the endometrial biopsy. Fertil. Steril. 1, 3–25.

Nyren-Erickson, E. K., Jones, J. M., Srivastava, D. K., and Mallik, S. (2013). A disintegrin and metalloproteinase-12 (ADAM12): function, roles in disease progression and clinical implications. Biochim. Biophys. Acta 1830, 4445–4455.
A disintegrin and metalloproteinase-12 (ADAM12): function, roles in disease progression and clinical implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1enu7vE&md5=4a5df71351d857eacbd2890880aeef9cCAS | 23680494PubMed |

Paiva, P., Salamonsen, L. A., Manuelpillai, U., and Dimitriadis, E. (2009). Interleukin 11 inhibits human trophoblast invasion indicating a likely role in the decidual restraint of trophoblast invasion during placentation. Biol. Reprod. 80, 302–310.
Interleukin 11 inhibits human trophoblast invasion indicating a likely role in the decidual restraint of trophoblast invasion during placentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOitb8%3D&md5=21b93e0b83a932751f9e8d9a4a505c20CAS | 18987331PubMed |

Pollheimer, J., Fock, V., and Knofler, M. (2014). Review: the ADAM metalloproteinases - novel regulators of trophoblast invasion? Placenta 35, S57–S63.
Review: the ADAM metalloproteinases - novel regulators of trophoblast invasion?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGlt7zI&md5=a7d7cd48df078ba3830ba508a36da2e4CAS | 24231445PubMed |

Psychoyos, A. (1973). Hormonal control of ovoimplantation. Vitam. Horm. 31, 201–256.
Hormonal control of ovoimplantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXksVOktr0%3D&md5=2dc9f1ea8051c5a89b206380ccf6e625CAS | 4620375PubMed |

Sahraravand, M., Jarvela, I. Y., Laitinen, P., Tekay, A. H., and Ryynanen, M. (2011). The secretion of PAPP-A, ADAM12 and PP13 correlates with the size of the placenta for the first month of pregnancy. Placenta 32, 999–1003.
The secretion of PAPP-A, ADAM12 and PP13 correlates with the size of the placenta for the first month of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFGjt7bN&md5=ad10cdb95aefda98f936902911052855CAS | 22015022PubMed |

Salamonsen, L. A., Nie, G., Hannan, N. J., and Dimitriadis, E. (2009). Society for Reproductive Biology Founders’ Lecture 2009. Preparing fertile soil: the importance of endometrial receptivity. Reprod. Fertil. Dev. 21, 923–934.
Society for Reproductive Biology Founders’ Lecture 2009. Preparing fertile soil: the importance of endometrial receptivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVartbfM&md5=2281e89108ab536df917ebd59364b1beCAS | 19698296PubMed |

Six, E., Ndiaye, D., Laabi, Y., Brou, C., Gupta-Rossi, N., Israel, A., and Logeat, F. (2003). The Notch ligand Delta1 is sequentially cleaved by an ADAM protease and gamma-secretase. Proc. Natl. Acad. Sci. USA 100, 7638–7643.
The Notch ligand Delta1 is sequentially cleaved by an ADAM protease and gamma-secretase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlt1Wru7Y%3D&md5=2e761979422ffaf3f47a08038d060b58CAS | 12794186PubMed |

Thathiah, A., Blobel, C. P., and Carson, D. D. (2003). Tumour necrosis factor-alpha-converting enzyme/ADAM 17 mediates MUC1 shedding. J. Biol. Chem. 278, 3386–3394.
Tumour necrosis factor-alpha-converting enzyme/ADAM 17 mediates MUC1 shedding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1Kisg%3D%3D&md5=78d51794445d2a2b5bb6f969b2cadd4dCAS | 12441351PubMed |

Thie, M., and Denker, H. W. (2002). In vitro studies on endometrial adhesiveness for trophoblast: cellular dynamics in uterine epithelial cells. Cells Tissues Organs 172, 237–252.
In vitro studies on endometrial adhesiveness for trophoblast: cellular dynamics in uterine epithelial cells.Crossref | GoogleScholarGoogle Scholar | 12476051PubMed |

Van Sinderen, M., Cuman, C., Winship, A., Menkhorst, E., and Dimitriadis, E. (2013). The chrondroitin sulfate proteoglycan (CSPG4) regulates human trophoblast function. Placenta 34, 907–912.
The chrondroitin sulfate proteoglycan (CSPG4) regulates human trophoblast function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1yksrjO&md5=c2e312b06a31af79635f5e758f04a6f2CAS | 23953863PubMed |

Van Sinderen, M., Cuman, C., Gamage, T., Rainczuk, K., Osianlis, T., Rombauts, L., and Dimitriadis, E. (2014). Localisation of the Notch family in the human endometrium of fertile and infertile women. J. Mol. Histol. 45, 697–706.
Localisation of the Notch family in the human endometrium of fertile and infertile women.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1ais7jK&md5=951401f1fc9c962aa8b0f2bea4ce22e0CAS | 25034535PubMed |

Xu, J., Krebs, L., and Gridley, T. (2010). Generation of mice with a conditional null allele of the Jagged2 gene. Genesis 48, 390–393.
Generation of mice with a conditional null allele of the Jagged2 gene.Crossref | GoogleScholarGoogle Scholar | 20533406PubMed |

Zhang, L., Guo, W., Chen, Q., Fan, X., Zhang, Y., and Duan, E. (2009). ADAM12 plays a role during uterine decidualisation in mice. Cell Tissue Res. 338, 413–421.
ADAM12 plays a role during uterine decidualisation in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVersrfE&md5=cd743b60ce3e838f18d8ae75bf00adf7CAS | 19841944PubMed |

Zhang, S., Lin, H., Kong, S., Wang, S., Wang, H., and Armant, D. R. (2013). Physiological and molecular determinants of embryo implantation. Mol. Aspects Med. 34, 939–980.
Physiological and molecular determinants of embryo implantation.Crossref | GoogleScholarGoogle Scholar | 23290997PubMed |

Zolkiewska, A. (2008). ADAM proteases: ligand processing and modulation of the Notch pathway. Cell. Mol. Life Sci. 65, 2056–2068.
ADAM proteases: ligand processing and modulation of the Notch pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotVyktLs%3D&md5=354ef4584dfb40269cde3af1f6264919CAS | 18344021PubMed |