Embryo Implantation II: Invasiveness of Trophoblast
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Overview
Main Findings:
- Embryo implantation in the uterus is a fascinating biological phenomenon: On one hand it is decisive for the establishment of pregnancy, on the other it can serve as a model for invasive behaviour of cells (trophoblast in this case), a central property of e.g. malignant tumor cells.
- Implantation can start only if trophoblast and its partner tissue, the endometrium of the uterus, have simultaneously entered a special cell biological state: invasiveness in case of the trophoblast, receptivity in case of the endometrium.
- Serine proteinases while playing a central role in the dissolution of blastocyst coats (see research topic 4) do not appear to be involved in penetration of the trophoblast through the uterine epithelium, as shown by our proteinase inhibition experiments in vivo. Matrix metalloproteinases may play a role during the subsequent phase of stromal invasion.
- Therefore, explanations for the initial phase of implantation, epithelial adhesion and penetration, must consider details of the cell biology of the two partner tissues which, however, had remained largely obscure. In order to make progress here it was helpful to first realize that we are dealing with a phenomenon which can be called a cell biological paradox: Trophoblast and uterine epithelium make their first adhesive contact with their apical cell poles although in other simple epithelia these parts of cells use to be non-adhesive (and even anti-adhesive). In a theoretical model we have postulated that there must be parallels to another biological phenomenon, i.e. the so-called embryonic fusion processes. In that case (and in tumor cell invasion as well) epithelial-mesenchymal transition (EMT) has been found to play a crucial role. We thus have proposed that it will be of heuristic value to make use of the advances of EMT research for studies on embryo implantation (and vice versa).
- A detailed experimental analysis based on this concept revealed that changes in apico-basal polarity of the two partner epithelia (trophoblast and uterine epithelium) must be a key issue here: partial loss or destabilisation of polarity, at acquisition of invasiveness and receptivity, respectively. These cells do not show complete EMT, however, but they strategically use elements of EMT processes.
- We have developed in vitro systems which allow studying these phenomena using human cell lines and which avoid involving human embryos: adhesion and invasion models using multicellular spheroids and various types of extracellular matrices. We consider it ethically unacceptable to use human embryos.
- This approach has allowed gaining insight into certain aspects of trophoblast invasiveness and its regulation in relation to the state of differentiation and cytoskeletal organisation (e.g. cellular responses to physical properties of various extracellular matrices). There is a delicate cross-talk between trophoblast and its host tissue: While the trophoblast remodels the latter it simultaneously responds to cells and matrices that it encounters on its route, and changes its properties. We have thus arrived at a view of the invasive process which is quite different from the simplifying traditional concept that viewed the trophoblast as the only active part and the endometrial host tissue as simply passive.
List of Publications
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DENKER, H.-W.:
Rise of the rabbit model for implantation research. A commemoration of the scientific work of Bent G. Boving (1920-2019).
Biology of Reproduction 102 (6): 1170-1176 (2020). DOI: 10.1093/biolre/ioaa038
PubMed
BOR
BOR (free access)
DENKER, H.-W.:
Implantation: Cell biology of embryo penetration route revisited.
(Comment on: UCHIDA, H. et al.: How to create an embryo penetration route. Am. J. Reprod. Immunol. 75(3): 326-332, 2016. DOI: 10.1111/aji.12476)
Am. J. Reprod. Immunol. 76(6): 429-431 (2016). DOI: 10.1111/aji.12591
PubMed
AJRI
pdf-download (219 KB)
summary (68 KB)
HOHN, H.-P., DONNER, A.J. and DENKER, H.-W.:
Endometrial receptivity: Selective adhesion competence of rabbit uterine epithelium for trophoblast but not for various tumor cells.
Cells Tissues Organs 173: 204-216 (2003). PubMed pdf-download (720 KB)
DENKER, H.-W. (ed.):
Molecular Approaches to Cell-Cell Adhesion: From Leukocyte Extravasation to Embryo Implantation.
Basel etc.: S. Karger AG, 2002 (=Cells Tissues Organs, Vol. 172, No. 3, pp. 147-254, 2002; ISBN 3-8055-7532-7, ISSN 1422-6405).
Contents pdf-download (30.6 KB)
Karger Verlag
Online Access
German National Library
HOHN, H.-P. and DENKER, H.-W.:
Experimental modulation of cell-cell adhesion, invasiveness and differentiation in trophoblast cells.
Cells Tissues Organs 172: 218-236 (2002). PubMed pdf-download (391 KB)
DENKER, H.-W. and THIE, M.:
The regulatory function of the uterine epithelium for trophoblast attachment: experimental approaches.
In: Molecular, Cellular and Developmental Biology of Reproduction: Basic and Clinical Aspects (P.M. Motta, S.A. Nottola, G. Macchiarelli and S. Correr, Eds.).
Italian Journal of Anatomy and Embryology 106 (2 Supplement 2): 291-306, 2001.
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PubMed
HOHN, H.-P., MÖLLER, W., HEYDER, J., DENKER, H.-W.:
Die Expression von Differenzierungsmarkern zeigt in BeWo-Chorionkarzinomzellen eine inverse Korrelation mit der Steifheit des Zytoskeletts.
(Abstr.) Verh. Anat. Ges. 96; Ann. Anat. 183 (Suppl.), 180, 2001.
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HOHN, H.-P., LINKE, M. and DENKER, H.-W.:
Adhesion of trophoblast to uterine epithelium as related to the state of trophoblast differentiation: in vitro studies using cell lines.
Mol. Reprod. Dev. 57: 135-145 (2000). PubMed pdf-download (33.0 MB)
| 2000s | 1990s | 1980s | 1970s |
HUELSEWEH, B., HUCH, G., HOHN, H.-P., DENKER, H.-W.:
Identification and Characterization of a cDNA with Differential Expression in Trophoblast Cells.
(Abstr.) Placenta 20, A.31 (1999).
pdf-download (628 KB)
HOHN, H.-P., MÖLLER, W., HEYDER, J., DENKER, H.-W.:
Differentiation of BeWo Choriocarcinoma Cells as Correlated with Biophysical Properties of the Cytoskeleton.
(Abstr.) Europ. J. Cell Biol. 78, (Suppl. 49), 54 (1999).
pdf-download (300 KB)
HOHN, H.-P., MÖLLER, W., HEYDER, J., DENKER, H.-W.:
Differentiation of BeWo Choriocarcinoma Cells May be Correlated Inversely with Stiffness of the Cytoskeleton.
(Abstr.) Placenta 20, A.30 (1999).
pdf-download (667 KB)
HOHN, H.-P., HUCH, G. HÜLSEWEH, B., DENKER, H.-W.:
Differentielle Expression eines bisher unbekannten Gens im Trophoblasten des ersten Trimenons.
(Abstr.) Verh. Anat. Ges. 94, Anat. Anz., Annals of Anatomy 181, Suppl., 216 (1999).
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HUCH, G.; HOHN, H.-P. and DENKER, H.-W.:
Identification of differentially expressed genes in human trophoblast cells by differential-display RT-PCR.
Placenta 19, 557-567 (1998). PubMed
HOHN, H.-P.; LINKE, M.; UGELE, B. and DENKER, H.-W.:
Differentiation markers and invasiveness: Discordent regulation in normal trophoblast and chorion carcinoma cells.
Exptl. Cell Res. 244, 249-258 (1998). PubMed
HOHN, H.-P., DENKER, H.-W.:
Die Bedeutung mechanisch/struktureller Faktoren für die Zelldifferenzierung: Das „Tensegrity“-Konzept.
(Abstr.) Verh. Anat. Ges. 93, Anat. Anz./Annals of Anatomy 180, Suppl., 242-243 (1998)
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HOHN, H.-P., GRÜMMER, R., BOSSERHOFF, S., GRAF-LIGNAU, S., DENKER, H.-W.:
Mechanical/structural signaling may direct differentiation of choriocarcinoma cells on extracellular matrix.
(Abstr.) Ann. Meet. Deutsche Gesellschaft für Zellbiologie, Halle (Saale) 1997. Europ. J. Cell Biol. 72, Suppl. 43, 19 (1997)
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HOHN, H.-P., GRÜMMER, R., BOSSERHOFF, S., GRAF-LIGNAU, S., REUSS, B., BÄCKER, C., DENKER, H.-W.:
The role of matrix contact and of cell-cell interactions in choriocarcinoma cell differentiation.
Europ. J.Cell Biol. 69, 76-85 (1996). PubMed pdf-download (6.86 MB)
HOHN, H.-P., LINKE, M., UGELE, B., DENKER, H.-W.:
Induction of differentiation may stimulate invasiveness in subpopulations of tumor cells.
(Abstr.) Sixth Internatl. Congress of the Metastasis Research Soc., Gent 1996, Clin. Exper. Metastasis 14, Suppl. I, 36 (1996)
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HOHN, H.-P., HUCH, G., LINKE, M., DENKER, H.-W.:
Correlation between invasiveness and RNA expression patterns of malignant vs. normal trophoblast cells.
(Abstr.) Verh. Anat. Ges. 91 (Ann. Anat. / Anat. Anz., Suppl. 178), 41-42 (1996)
HOHN, H.-P., HUCH, G., LINKE, M., DENKER, H.-W.:
Parameter in Korrelation mit Unterschieden in der Invasivität von Trophoblast- und Chorionkarzinomzellen.
(Abstr.) Verh. Anat. Ges. 91 (Ann. Anat. / Anat. Anz., Suppl. 178), 332 (1996)
pdf-download (420 KB)
RÖSPEL, R., HOHN, H.-P., DE BRAGANÇA, K., SEITZ, H.M., DENKER, H.-W.:
Cell surface molecules of trophoblast cells involved in adhesion of Toxoplasma gondii.
(Abstr.) Sixth Internatl. Congress of the Metastasis Research Soc., Gent 1996, Clin. Exper. Metastasis 14, Suppl. I, 29 (1996)
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DENKER, H.-W.:
Cell biological views of embryo implantation (A Review).
Turkish J. of Medical Sciences, Suppl., 1-12 (1995). pdf-download (29.1 MB)
HUCH, G., HOHN, H.-P., DENKER, H.-W.:
Gene activity and trophoblast invasiveness: DDRT-PCR studies.
(Abstr.) VIth Meeting of the European Placenta Group, Joint Meet. with the Rochester Trophoblast Conference, Spa 1995. Placenta 16, A. 28 (1995)
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HOHN, H.-P., HUCH, G., LINKE, M., DENKER, H.-W.:
Parameters correlated with differences in invasiveness of trophoblast and choriocarcinoma cells.
(Abstr.) VIth Meeting of the European Placenta Group, Joint Meet. with the Rochester Trophoblast Conference, Spa 1995. Placenta 16, A. 27 (1995)
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HOHN, H.-P., DENKER, H.-W.:
The role of cell shape for differentiation of choriocarcinoma cells on extracellular matrix.
Exp. Cell Res. 215, 40-50 (1994). PubMed
DENKER, H.-W.:
Cell biology of endometrial receptivity and of trophoblast-endometrial interactions.
In: Endocrinology of Embryo-Endometrium Interactions (S.R. Glasser, J. Mulholland and A. Psychoyos, eds.) New York: Plenum Press, 1994, pp. 17-32. DOI: 10.1007/978-1-4615-1881-5_3
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LINKE, M., HOHN, H.-P., DENKER, H.-W.:
Modulation of differentiation alters adhesiveness and invasiveness of choriocarcinoma cells.
(Abstr.) IVth European Cell Biol. Congress, Prague 1994, Cell Biol. Int. 18, 576 (Abstr. Th-153) (1994)
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HOHN, H.-P., LINKE, M., JOHN, N., DENKER, H.-W.:
Zur Korrelation von Differenzierung und Invasivität von Chorionkarzinomzellen.
(Abstr.) Verh. Anat. Ges. 89 (Ann. Anat. 176, Suppl.), 226-227 (1994)
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HOHN, H.-P., GRÜMMER, R., HOOK, M., DENKER, H.-W.:
Induction of cell differentiation by extracellular matrix: Mechanical vs. chemical signalling.
(Abstr.) Journal of Cellular Biochemistry, Suppl. 18C, 249 (1994)
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DENKER, H.-W.:
Implantation: A cell biological paradox.
J. Exp. Zool. 266, 541-558 (1993). PubMed pdf-download (75.9 MB)
HOHN, H.-P., BOOTS, L.R., DENKER, H.-W., HÖÖK, M.:
Differentiation of human trophoblast cells in vitro stimulated by extracellular matrix.
In: Fetal Growth and the Placenta - From Implantation to Delivery. (H. Schneider, R. Bischof and R. Leiser, eds.) (Trophoblast Research, Vol. 7). University of Rochester Press, Rochester, NY. 181-200 (1993). pdf-download (44.0 MB)
HOHN, H.-P., LINKE, M. DENKER, H.-W.:
Induction of differentiation in choriocarcinoma cells modulates elements of invasiveness in in-vitro-models.
(Abstr.) J. Cancer Res. Clin. Oncol. 119, (Suppl. 2), 86 (1993)
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DENKER, H.-W.:
Endometrial receptivity and trophoblast invasiveness: Cell biological aspects.
(Abstr.) 8th World Congress on In Vitro Fertilization and Alternate Assisted Reproduction, Kyoto, Japan, 1993. Journal of Assisted Reproduction and Genetics 10 No. 6 (Suppl.), 29 (1993)
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HOHN, H.-P., PARKER, Jr. C.R., BOOTS, L.R., DENKER, H.-W., HÖÖK, M.:
Modulation of differentiation markers in human choriocarcinoma cells by extracellular matrix: on the role of a three-dimensional matrix structure.
Differentiation 51, 61-70 (1992). PubMed
HOHN, H.-P., LINKE, M., JOHN, N., and DENKER, H.-W.:
Induction of differentiation reduces cell adhesion of choriocarcinoma cells in an in vitro model. (Abstr.)
(Abstr.) Clin. Exptl. Metastasis, Vol. 10, Suppl. 1, 39 (1992)
DENKER, H.-W.:
Cell biology of endometrial receptivity and of trophoblast-endometrial interactions: recent aspects.
(Abstr.) Sympos. on Endocrinology of Embryo-Endometrial Interactions (Satellite Sympos. of the Ninth International Congress of Endocrinol., N.I.C.E. 92), Bordeaux 1992, Abstr. No. S 1.
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HOHN, H.-P., HÖÖK, M. und Denker H.-W.:
Zur Bedeutung der physikalischen Eigenschaften der extrazellulären Matrix für die Induktion der Differenzierung von Chorionkarzinomzellen.
(Abstr.) Verh. Anat. Ges. 87 (Anat. Anz. Suppl. 174), 62 (1992)
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GRÜMMER, R. und DENKER, H.-W.:
Untersuchungen zum Invasionsverhalten dreidimensional wachsender Chorion-Karzinomzellen.
(Abstr.) Verh. Anat. Ges. 85 (Anat. Anz. Suppl. 170), 591-592 (1991)
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HOHN, H.-P., HÖÖK, M. and DENKER, H.-W.:
Differentiation of choriocarcinoma cells and normal trophoblast cells in response to extracellular matrix.
(Abstr.) IVth Meeting of the European Placenta Group (EPG) / Joint Meeting with the Rochester Tropholast Conference (RTC), Gwatt (Switzerland) 1991. Placenta 12, 400 (1991)
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DENKER, H.-W.:
Das Implantationsfenster: Zellbiologische Grundlagen der Invasivität des Trophoblasten und der Rezeptivität des Endometriums.
(Abstr.) Dreiländertagung "Fertilität und Sterilität" der deutschen Gesellschaft zum Studium der Sterilität und Fertilität, gemeinsam mit der Österreichischen Gesellschaft zum Studium der Sterilität und Fertilität und der Schweizerischen Gesellschaft für Fertilität und Sterilität, Goslar 1991, Zusammenfassender Bericht (Alete Wissenschaftlicher Dienst) pp. 36-38
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JOHN, N.J., GRÜMMER, R. and DENKER, H.-W.:
Attachment of human choriocarcinoma cell spheroids to uterine epithelial monolayers: quantitative measurements of adhesion.
(Abstr.) Sixth Sympos. of the Section of Experimental Cancer Research (SEK) of the German Cancer Society, Heidelberg 1991. J. Cancer Res. Clin. Oncol. 117 (Suppl.), S 56 (1991).
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HOHN, H.-P., HÖÖK, M. and DENKER, H.-W.:
Induction of differentiation in choriocarcinoma cells by extracellular matrix: on the role of physical properties of the matrix.
(Abstr.) Sixth Sympos. of the Section of Experimental Cancer Research (SEK) of the German Cancer Society, Heidelberg 1991. J. Cancer Res. Clin. Oncol. 117 (Suppl.), S 49 (1991).
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HOHN, H.-P., DENKER, H.-W. und HÖÖK, M.:
Differenzierung von Chorionkarzinomzellen auf extrazellulärer Matrix.
(Abstr.) Verh. Anat. Ges. 84 (Anat. Anz. Suppl. 168), 49-50 (1991)
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HOHN, H.-P., HÖÖK, M., and DENKER, H.-W.:
Induction of differentiation in choriocarcinoma cells by extracellular matrix: On the role of physical properties of the matrix.
(Abstr.) Europ. J. Cell Biol., Suppl. 32 (Vol. 54), 48 (1991)
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DENKER, H.-W. and APLIN, J.D. (eds.):
Trophoblast Invasion and Endometrial Receptivity. Novel Aspects of the Cell Biology of Embryo Implantation.
New York and London: Plenum Medical Book Com., 1990 (=Trophoblast Research, Vol. 4).
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SpringerLink
MARX, M., WINTERHAGER, E. and DENKER, H.-W.:
Penetration of the basal lamina by processes of uterine epithelial cells during implantation in the rabbit.
In: Trophoblast Invasion and Endometrial Receptivity. Novel Aspects of the Cell Biology of Embryo Implantation. (H.-W. Denker and J.D. Aplin, eds.) (Trophoblast Research, Vol. 4). New York and London: Plenum Medical Book Comp., 1990, pp. 417-430.
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GRÜMMER, R., HOHN, H.-P. and DENKER, H.-W.:
Choriocarcinoma cell spheroids: An in vitro model for the human trophoblast.
In: Trophoblast Invasion and Endometrial Receptivity. Novel Aspects of the Cell Biology of Embryo Implantation. (H.-W. Denker and J.D. Aplin, eds.) (Trophoblast Research, Vol. 4). New York and London: Plenum Medical Book Comp., 1990, pp. 97-111.
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SpringerLink
HOHN, H.-P. and DENKER, H.-W.:
A three-dimensional organ culture model for the study of implantation of rabbit blastocyst in vitro.
In: Trophoblast Invasion and Endometrial Receptivity. Novel Aspects of the Cell Biology of Embryo Implantation. (H.-W. Denker and J.D. Aplin, eds.) (Trophoblast Research, Vol. 4). New York and London: Plenum Medical Book Comp., 1990, pp. 71-95.
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DENKER, H.-W.:
Trophoblast-endometrial interactions at embryo implantation: A cell biological paradox.
In: Trophoblast Invasion and Endometrial Receptivity. Novel Aspects of the Cell Biology of Embryo Implantation. (H.-W. Denker and J.D. Aplin, eds.) (Trophoblast Research, Vol. 4). New York and London: Plenum Medical Book Comp., 1990, pp. 3-29.
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| 2000s | 1990s | 1980s | 1970s |
HOHN, H.-P., PARKER, R., BOOTS, L., DENKER, H.-W. and HÖÖK, M.:
Induction of differentiation in choriocarcinoma cells by placental extracellular matrix.
(Abstr.) Ann. Meet. Deutsche Ges. f. Zellbiologie, München 1988. Europ. J. Cell Biol. 46 , Suppl. 22, 32 (1988)
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BÜKERS, A., HOHN, H.-P., DENKER, H.-W.:
Lectin histochemical evaluation of an in-vitro model for trophoblast invasion.
(Abstr.) International Symposium "Lectins and Glycoconjugates in Oncology. Structure, Function, Clinical Application", Göttingen / FR Germany, 4-5 December 1987.
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DENKER, H.-W.:
Implantation: recent approaches to understand a cell biological paradox.
(Abstr.) VIth World Congress on Human Reproduction, Tokyo 1987, p. 26
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LEISER, R. and DENKER, H.-W.:
Remodelling of the endometrial vascular bed during trophoblast invasion in the rabbit.
(Abstr.) 24th Annual Meeting of the Cell, Tissue and Organ Culture Study Group (C.T.O.C.), Heidelberg 1986, p. 19
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HOHN, H.-P., DONNER, A. and DENKER, H.-W.:
Evaluation of an in vitro model for embryo implantation: selective receptivity of rabbit endometrium for trophoblast attachment.
(Abstr.) 24th Annual Meeting of the Cell, Tissue and Organ Culture Study Group (C.T.O.C.), Heidelberg 1986, p. 9
HOHN, H.-P., DONNER, A. and DENKER, H.-W.:
Evaluation of an in vitro model for embryo implantation: Selective receptivity of rabbit endometrium for trophoblast attachment.
(Abstr.) Ann. Meet. Deutsche Ges. Zellbiologie, Tübingen 1986. Europ. J. Cell Biol. 39, Suppl. 12, 18 (1985)
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HOHN, H.-P. and DENKER, H.-W.:
Confrontation of blastocysts and endometrium in organ culture: towards an in-vitro model for embryo implantation.
Abstract No. 147, 1st Meeting of the Europ. Soc. of Human Reproduction and Embryology, Bonn 1985. Human Reprod. 1 (Suppl. 1), 49-50 (1986)
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DENKER, H.-W., ENDERS, A.C. and SCHLAFKE, S.:
Bizarre hypertrophy of vascular endothelial cells in rhesus monkey endometrium: experimental induction and electron microscopical characteristics.
Verh. Anat. Ges. 79, Anat. Anz. Suppl. 157, 545-548 (1985). pdf-download (1.94 MB)
DENKER, H.-W., DONNER, A. and HOHN, H.-P.:
Interaction of trophoblast and of tumor cells with endometrial fragments in organ culture.
(Abstr.) 23. Annual Meeting of the Cell, Tissue and Organ Culture Study Group (C.T.O.C.), Kollekolle (Denmark) 1985
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WINTERHAGER, E., BRÜMMER, F. and DENKER, H.-W.:
Gap junction formation in the uterine epithelium in response to embryo recognition.
(Abstr.) Annual Meeting Belgian Soc. Cell Biol./ German Soc. Cell Biol., Bonn 1985. Europ. J. Cell Biol. 36, Suppl. 7, 74 (1985)
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HOHN, H.-P. and DENKER, H.-W.:
Attachment and invasion of rabbit blastocysts confronted with endometrium in organ culture.
(Abstr.) Annual Meeting Belgian Soc.Cell Biol./German Soc. Cell Biol., Bonn 1985. Europ. J. Cell Biol. 36, Suppl. 7, 28 (1985)
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DENKER, H.-W.:
Embryo implantation: controlled invasion of a non-tumor tissue.
(Abstr.) Annual Meeting Belgian Soc. Cell Biol. / German Soc. Cell Biol., Bonn 1985. Europ. J. Cell Biol. 36, Suppl. 7, 15 (1985)
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DENKER, H.-W.:
Embryo implantation and trophoblast invasion.
In: Cell Movement and Neoplasia (M. De Brabander et al., eds.) Oxford/New York: Pergamon Press, 1980, pp. 151-162.
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| 2000s | 1990s | 1980s | 1970s |
DENKER, H.-W.:
Implantation: The Role of Proteinases, and Blockage of Implantation by Proteinase Inhibitors.
Berlin-Heidelberg-New York: Springer-Verlag, 1977 (= Adv. Anat. Embryol. Cell Biol., Vol. 53, Fasc. 5). (English version of Habilitation Thesis). Print-ISBN: 978-3-540-08479-2. DOI: 10.1007/978-3-642-66781-7
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